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MARINE ECOLOGY PROGRESS SERIES Vol. 71: 85-96, 1991 Published March 28 Mar. Ecol. Prog. Ser.

REVIEW The balance of losses and gains in seaccrass M. A. ~emminga',P. G. ~arrison~,F. van ~ent'

' Delta Institute for Hydrobiological Research, Vierstraat 28,4401EA Yerseke. The Netherlands Dept of Botany, University of British Columbia, 3529-6270 University Blvd, Vancouver, British Columbia, Canada V6T 2B1

ABSTRACT: abound in the dynamic environment of shallow marine waters. From the often high annual biomass production it can be deduced that meadows have high requirements for inorganic , although the nutrient demands will be met to some extent by internal recycling. A series of processes lead to nutrient losses from the seagrass bed. Export of and fragments with currents, leaching losses from photosynthetically active leaves and from senescent and dead plant material, and nutrlent transfer by mobile foraging animals, are processes speclfic to seagrass meadows;in addition, the nutrient losses are aggravated by 2 processes con~monlyoccurring in marine sedirnents: denitrification and of nutrients from the sediments to the overlying water column. The persistence in time of most seagrass meadows points to an existing balance between nutrient losses and gains. Three processes may contributeto the replenishment of nutrients: -fixation, sedimentation and nutrient uptake by the leaves. Nitrogen-fixation undoubtedly is important, but continued biomass production requires other nutrientsas well. Crucial contributions,therefore, must come from sedimenta- tion and/or leaf uptake. The concept of the seagrass as an open system, with nutrient fluxes from and to the system varylng in time, allows for imbalances between nutrient losses and gains. It is suggested that these imbalances may contribute to fluctuations in annual seagrass biomass production.

INTRODUCTION with a discussion of the annual nutrient requirements for seagrass growth, offering a background against Seagrass meadows are the biological and physical which the importance of the various processes can be foundation for many coastal marine from assessed. The long-standing view that seagrass pro- the tropics to boreal regions. These meadows have a duction is often nitrogen limited has resulted in a rela- high nutrient demand, to support their high annual tively large number of papers dealing with nitrogen production, which ranks them among the most produc- dynamics in seagrass systems, and emphasis therefore tive of submerged aquatic ecosystems (Zieman& Wet- will be on nitrogen in this review. However, it is obvi- zel 1980, Hillman et al. 1989). The nutrients involved, ous that nutnent losses and gains in seagrass meadows however, are not all retained within the seagrass beds. will not be restricted to nitrogen, but will also include In the dynamic environment of the shallow marine waters, a continual loss of nutrients may occur; the Table 1. Processes contributing to the loss or gain of nutrients in seagrass meadows (discussed in this paper) export of sloughed and decomposing leavesis only one of the more conspicuous processes contributingto this loss. If only export of nutrients occurred, the impover- Losses ExudationAeaching from Living and dead plant material ishment of the biotope ultimately would lead to the Export of sloughed leaves and leaf fragments disappearance of the seagrass vegetations. Obviously, Nutrient transfer by foraging animals their persistence in time will depend on mechanisms Denitrification effecting a continuous replenishment of nutrients. In Diffusion from sediment this paper, we examine the processes which contnbute Inputs Nitrogen-fixatlon to either nutrient losses or gains (Table 1). The quan- Sedimentation titative importance of the individual processes is indi- Nutrient uptake by leaves cated as much as the available data allow. We begin

O Inter-Research/Printed in Germany 86 Mar. Ecol. Prog Ser. 71: 85-96, 1991

other important nutrients such as , which and transported to sites of growth and storage (Chapin recently has been put forward as a limiting factor for 1980). Recent empirical support for this idea is found in seagrass vegetation on carbonate sediments (Short the work of Borum et al. (1989). They found that older 1987, Short et al. 1990). leaves did lose substantially more of their nitrogen (42 O/O and 57 O/O of the initial content from the fourth and fifth youngest leaves, respectively) than did ANNUAL NUTRIENT REQUIREMENTS FOR younger leaves (e.g. only 3 % from the second leaf) SEAGRASS GROWTH during 1 wk, but translocation accounted for 92 % of the loss. Even when eelgrass shoots had adequate Considering the high primary productivity of - external supplies of nitrogen (i.e. 50 pm01 ammonium grasses and the chemical composition of the plant 1-l), the youngest 2 leaves obtained about 2/3 of their parts, it is easy to determine that seagrasses have high new nitrogen via translocation from older leaves. requirements for inorganic nutrients. For one wide- Young segments were another sink for nitro- spread , marina (eelgrass), short-term gen mobilized from older leaves. Borum et al. (1989) measurements of above-ground used the difference between the maximum leaf nitro- during the time of peak growth give rates of 5 to 19 g gen content (in the almost fully grown, third-youngest dry wt m-2 d-' (Sand-Jensen 1975, Jacobs 1979, Mukai leaf) and the content of old leaves just before they were et al. 1979, Thorne-Miller & Harlin 1984, Hamburg & sloughed to estimate that 24 O/O of the nitrogen needed Homan 1986, Kentula & McIntyre 1986, Ibarra-Obando for new leaf growth in eelgrass is recycled internally. & Huerta-Tamayo 1987, Roman & Able 1988, Umebay- Umebayashi (1989) provided data on nitrogen content ashi 1989). These values correspond to 150 to 574 mg N of mature and senescing leaves, growth rates, and m-2 d-I (Borum et al. 1989, Umebayashi 1989). Allow- defoliation rates for eelgrass in Japan during a short ing for seasonal variation in rates of primary production period of rapid growth from which we calculated that and growth, on an annual basis the above-ground 17 % of the estimated 574 mg N m-2 d-' needed for primary production of eelgrass growing in both the new leaf growth in May could be provided by recycling Atlantic and Pacific has been estimated as 440 nitrogen from senescent leaves. Extending the calcula- to 1400 g dry wt m-2 (Sand-Jensen 1975, Jacobs 1979, tion to cover a year's cycle for a perennial population is Kentula & McIntyre 1986, Murray & Wetzel 1987, difficult. We estimate that conservation of nitrogen Roman & Able 1988). Assuming a range of nitrogen reduces the annual requirement for uptake of nitrogen content of 1.5 to 3 O/O (Harrison & Mann 1975, Thayer et by about 25 %, to somewhere in the range 5 to 35 g N al. 1977), the annual nitrogen requirement for leaf mP2. growth will be somewhere between 6.6 and 42 g N mP2. For tropical species similar requirements have been calculated; e.g. 9 g N m-2 yr-' for LOSSES OF NUTRIENTS FROM SEAGRASS BEDS australis and 18 g N m-2 for antarctica (Walker & McComb 1988). The below-ground parts Leaching also require nitrogen, but their needs are small com- pared with those of the leaves, e.g. 7 % (Umebayashi Live seagrasses release up to 2 % of the they 1989) to 11 O/O (Kenworthy & Thayer 1984) for eelgrass. fix in in the form of dissolved organic Nonetheless, the range of annual requirement for nitro- molecules (Brylinski 1977, Penhale & Smith 1977, Wet- gen will extend to a somewhat higher value than 42 g zel & Penhale 1979, Moriarty et al. 1986). The amounts N m-2, but probably not higher than 50 g N m-', when of nitrogen or phosphorus released from healthy leaves below-ground biomass production is included. are unclear but laboratory studies with 32P04suggested The annual nutrient requirements for primary pro- that eelgrass leaves excreted 1 to 3 % of the phos- duction may to some extent be met by internal re- phorus that the had absorbed (Penhale & Thayer cycling processes. Senescence of seagrass leaves is 1980). At least a part of the excreted nutrients will be accompanied by a decrease in certain chemical con- captured by epiphytes on the leaves and in the stituents, e.g. carbon (20 to 25 %: Harrison & Mann and thus retained in the seagrass bed (Har- 1975; 36 O/O: Thayer et al. 1977) and nitrogen (20 to lin 1973, Penhale & Smith 1977, Penhale & Thayer 25 O/O: Harrison & Mann 1975; 21 %: Thayer et al. 1980, Moriarty et al. 1986), but another (unknown) 1977). Phosphorus content, too, declines with age by as portion will escape into the water (Jerrgensen et al. much as 40 to 60 '10 (Walker & McComb 1988, Umebay- 1981). ashi 1989). These changes may be partly the result of Nutrient losses from the leaves may continue during conservation mechanisms operating in the plant, with the phases of senescence and decay: increased leaki- selected components being removed from aging leaves ness of the leaves may be responsible for part of the Hernminga et al.: Nutrients in seagrass meadows 87

decrease in tissue concentrations of nutrients during growth of leaves in Lake Grevelingen was subse- senescence. Release of large amounts of soluble quently lost from the seagrass bed when it was depo- material from senescent leaves indeed has been sited as very small particles in the sediment of the demonstrated in Posidonia australis (Irkman & Reid deepest part of the Lake (Pellikaan & Nienhuis 1988). 1979), but the chemical composition of the leacheate In conclusion, export of particulate material, either was not determined. Leaching is a process which prob- whole leaves or small particles, is likely to result in ably will continue throughout the period of senescence ongoing nutrient losses. In view of the data presented and subsequent decay. Harrison & Harrison (1980) above, these losses will strongly vary between sites showed that even after aging 5 mo intertidally, Zostera and, following our estimates of annual requirements for marina leaves still contained 10 % of the dry weight in nitrogen uptake, may fall anywhere in the range 0 to an easily extracted state. 30 g N m-' ~r-'.

Export of sloughed leaves and leaf fragments Nutrient transfer by foraging animals

Transport of seagrass material followed by deposi- There are a number of mobile, larger animals, par- tion outside the seagrass beds, in deeper waters or on ticularly , which may be involved in the the shore, is commonly observed (e.g. Gallagher et al. transfer of nutrients from seagrass meadows, by tap- 1984, Suchanek et al. 1985, Newel1 et al. 1986, Whit- ping the resources of the beds and producing fecal field 1988). This loss is not restricted to relatively nu- matter outside the meadow when the animals have trient-poor senescent or dead leaves. In an investiga- moved from their feedlng ground. Potentially important tion of massive depositions of Zostera noltii wrack in this respect are , turtles, and washed ashore on the Mauntanian , it was found , and birds (see reviews by Thayer et al. 1984, that this material had the characteristics Lanyon et al. 1989). Direct consumption of fresh, grow- and the appearance of rather fresh leaves, and there- ing seagrasses, however, is generally considered to be fore probably consisted mostly of nutrient-rich leaves limited, although the frequently cited paper of Green- which were detached from the shoots while alive way (1976) shows that, locally, pressure may (Hemminga 81Nieuwenhuize 1991). be very high. In the , which is noted for a Estimates of the losses due to leaf export from sea- relatively high number of seagrass herbivores, Zieman grass beds range from < l O/O of primary production for et al. (1979) found that only 5 to 10 % of the productiv- testudinum (Zieman et al. 1979), and 12 % ity of was consumed. Even lower for Posidonia australis (Kirkman & Reid 1979), to 1 and values have been estimated for direct seagrass con- 30 % for (Josselyn et al. 1983, Bach et sumption in temperate regions, where waterfowl al. 1986), 2 to 74 % for Halodule wrightii (Bach et al. species are the dominant larger herbivores (Thayer et

1986), and 27 to 79 O/O for Syringodum filiforme (Fry & al. 1984, Nienhuis & Groenendijk 1986). Considering Virnstein 1988). Morphological characteristics such as the fact that fecal production may also occur during the dimensions of lacuna1 spaces, susceptibility to foraging in the meadows, and part of the nutrients grazing by larger herbivores such as and turtles, ingested therefore potentially returns to the seagrass which sever blades and allow large fragments to float system, ~t can be assumed that this type of nutrient loss away (Zieman et al. 1979, Bjorndal 1980), and represents only a relatively minor flux from the sea- environmental conditions, e.g. wind and currents grass meadows. Detailed discussion of this topic, there- (Bach et al. 1986), determine the extent of leaf loss fore, will be omitted here. from seagrass beds. In cases where the canopy is dense and water currents are slow, seagrass beds act as traps for particulate matter in the water (Fonseca et Denitrification al. 1982) and a larger proportion of the sloughed leaves will decay in the bed. The microbial reduction of to gaseous nitro- It is more difficult to assess the export of smaller gen (N20 and NZ) makes nitrogen essentially unavail- particles from seagrass beds. Bach et al. (1986) conjec- able for biological production, except for diazotrophs tured that the loss of small particles from eelgrass beds (see below). Nitrate in the sediment usually is sup- in the southeastern USA could exceed the export of plied either by diffusion from the overlying water or surface-floating leaf material which was up to 30 % of by bacterial nitrification occurring in the sediment the production. A comprehensive study of eelgrass (Koike & S~rensen1988), the latter process generally growth and decay in the Netherlands suggested that being the more important (e.g. Seitzinger 1987). In almost half of the nitrogen incorporated into a year's contrast to denitrification, which is a strictly 88 Mar. Ecol. Prog. Ser. 71: 85-96, 1991

anaerobic process, the transformation of ammonium Diffusion to nitrate in the process of nitrification requires aerobic conditions. Nonetheless these processes may Mineralization processes in the sediment of marine be tightly coupled (Jenkins & Kemp 1984). Vegetated systems result in the formation of ammonium, which aquatic sediments offer an environment where nitrifi- subsequently (or after oxidation to nitrate) may diffuse cation and denitrification may coincide deep in the into the overlying water. Ammonium in the sediment sediment. Via the roots of macrophytes, oxygen dif- of the seagrass bed will result primarily from the fuses into the sediment, creating a mosaic of oxic and decomposition of particulate organic material, which anoxic microenvironments throughout the zone. contains the major part of the nitrogen pool in the Furthermore, the relatively high organic content of sediment (Boon 1986b), but deamination of amino vegetated sediments, due to input of organic partic- acids exuded by seagrasses (Jsrgensen et al. 1981) date material and root exudation processes, provides may be another source (Boon et al. 1986b). Although abundant substrate both for NH: regeneration, which several studies report on ammonium regeneration in would in turn enhance nitrification, and for denitrifi- seagrass beds (Iizumi et al. 1982, Short 1983a, Short et cation (cf. Nixon 1981, Kemp et al. 1982). Christensen al. 1985, Boon et al. 1986a, b, Dennison et al. 1987), an & Ssrensen (1986) indeed found that the root zone estimation of diffusion losses of ammonium from the accounted for a major part of the annual denitrifica- sediment of a seagrass bed has been obtained only by tion in a stand of the freshwater macrophyte LittoreLla Short (1983a). This author found in field perturbation uniflora. The importance of rhizosphere processes is experiments that removing eelgrass leaves and seai- also well demonstrated in a recent study of Reddy et ing the sediment surface resulted in a rapid increase al. (1989), who performed growth chamber experi- of the sehment interstitial ammonium concentration. ments with various aquatic plant species. Mass In sealed plots net ammonium production, calculated balance calculations of 15NH: added to the soil indi- from the soil profiles of accumulated ammonium, was

cated that 34 O/O of the added ammonium was deni- 47 mg N m-2 d-'. Ammonium diffusion was calculated trified in soil columns with rice plants, whereas the as the difference between the production in the sealed corresponding figure in columns without plants was plots and the estimated ammonium uptake by the root only 11 %. system of the local seagrass vegetation, resulting in a Few studies have addressed nitrification and deni- diffusion rate of 30 mg N m-2 d-l. This rate is within trification in seagrass beds, but the processes men- the range reported in non-vegetated sediments (Hale tioned above undoubtedly operate in these marine 1976, Nixon et al. 1976, Blackburn & Henriksen 1983). meadows. Nitrate and nitrite are present in tropical Such a diffusion rate would represent a substantial (Boon 1986a) and in temperate sediments of seagrass loss (64 O/O) of the net ammonium production in the beds, even below 30 cm depth (Iizumi et al. 1980), sediment, but the moderate interstitial ammonium indicating nitrification in the root zone. The latter concentrations and the rather low production rate of authors measured in situ rates of denitrification in the this nutrient in the seagrass beds studied by Short, as upper 7 cm of the sediments equivalent to a daily loss compared to other data on interstitial concentrations of 0.3 to 3 mg N m-'. As denitrification was also found and production (e.g. Dennison et al. 1987), may imply below 20 cm depth, this most probably is a conserva- that it is not a particularly high rate for seagrass sedi- tive estimate. In situ denitrification rates in the top ment~. It should be added here that diffusion of 10.5 cm of the sediment of a Zostera novazelandica nutrients from the sediment does not necessarily equal bed varied between 1.2 and 6.0 mg N mP2 d-' (Kaspar a loss of nutrients from the : 1983). The denitrification rates reported for seagrass although diffused nutrients evade root uptake, the beds thus are on the low end of the range of activities seagrass leaves (and also benthic and leaf measured in coastal bays and estuarine sediments (0 epiphytes present in the system) may capture a part of to 130 mg N m-2 d-l; see review by Koike & Ssrensen the released nutrients (cf. Prieto & Corredor 1984); 1988). However, the potential denitrification rates in however, the effectiveness of this mechanism in the the sediment of seagrass meadows (measured in seagrass biotope is unknown. nitrate-saturated soil slurries), are much hgher (Kas- par 1983, Caffrey & Kemp 1990). It is possible, there- fore, that under favourable conditions of high nitrate INPUTS OF NUTRIENTS TO SEAGRASS BEDS availabihty higher in situ denitrification rates do occur, but this remains to be investigated. On the basis of the As counterparts for the processes which result in scarce data presently available, the losses due to nutrient losses from the seagrass beds, there are sev- denitrification would be somewhere in the range 0.1 to eral processes potentially able to enrich the pools of 2 g N m-' yr-l. nutrients. First, nitrogen-fixation specifically results in Hemminga et al.: Nutrients in seagrass meadows 89

enrichment with nitrogen nutrients. Second, sedimen- numbers of nitrogen-fixing bacteria associated with tation of particles from the watercolumn may resupply roots are several orders of magnitude higher than in the the soil both with micro- and macronutrients. Finally, sediment between the roots (Shieh et al. 1989). The nutrient uptake by the leaves of the plants offers a third diurnal and seasonal variation in nitrogen fixation rates mechanism by which nutrient pools of the seagrass bed in the root zone of seagrass beds (Capone & Taylor may be resupplied. These 3 processes will be discussed 1977, 1980, Smith & Hayasaka 1982) also points to the successively in the next section. importance of metabolic activities of the seagrass plants to the nitrogen-fixing community. However, active populations of nitrogen-fixing bacteria are also Nitrogen fixation associated with rhizome detntus in the sediment, which suggests that degradation of this detrital The observation of Patriquin & Knowles (1972) that material can also support the process of nitrogen-fixa- nitrogen fixation occurred in the rhizosphere of several tion (Kenworthy et al. 1987). It is somewhat remarkable tropical and temperate seagrass species was followed that seagrass detritus does not show an accumulation of by a number of studies, which were no doubt elicited nitrogen during decay (see review by Harrison 1989). by the suggestion of the authors that the nitrogen This may either be due to a rapid release of fixed requirements of the seagrasses could be completely nitrogen from the seagrass detritus or to the relatively covered by this process. Some of the nitrogen-fixing minor contribution of diazotrophs to the nitrogen pool bacteria in the sediment of seagrass beds are present in of the detritus. As Kenworthy et al. (1987) calculated close association with roots and . Davidson et that 0.565 g N m-' yr-', which is equivalent to only 1 to al. (1984) showed with the aid of a fluorescent antibody 2 mg N m-2 d-l, was supplied by nitrogen-fixation technique that nitrogen-fixing bacteria were located in associated with the detritus, the latter alternative is the intercellular spaces between root cortical cells in more probable. Halodule wrightii. This type of association may be of Nutrient enrichment of the seagrass biotope by direct benefit to the growing plants; however, to what nitrogen-fixing organisms may also be found in the extent the relation between seagrasses and nitrogen- phyllosphere, but the consistency of the process is less fixers resembles the symbiotic association between than in the rhizosphere (Goering & Parker 1972, diazotrophs and higher plants (Schubert 1986) is Capone & Taylor 1977). The direct association of unknown. Capone & Taylor (1980) reported that ni- diazotrophs with the living plant leaves again offers the trogen-fixation rates were related to weight of below- possibhty of a close coupling between nitrogen fixa- ground biomass in beds of Thalassia testudinum. Sea- tion and uptake of nitrogen by the leaves. Nutrient grasses transport gases and organic compounds, transfer from seagrass leaves to epiphytes has been synthesized during photosynthesis, to their root zones found (Harlin 1973, McRoy & Goering 1974, Penhale & (Oremland & Taylor 1977, Wetzel & Penhale 1979, Thayer 1980), and the reverse process also has been Iizumi et al. 1980, Moriarty et al. 1986), and nitrogen- demonstrated (Harlin 1973). fixers are probably stimulated by these processes. It The nitrogen input by nitrogen-fixation in meadows may be for this reason that, on a wet weight basis, the of a subtropical (Thalassia testudinum) and a temper-

Table 2. Estimates of daily nitrogen inpu t by nitrogen fixation in seagrass meadows

Vegetation Compartment N2-fixation Source (mg m-2 d-l) Thalassia testudinum Various TO McRoy et al. (1973) Thalassia testudinum Rhizosphere 5.1-5.3 Capone et al. (1979) Thalassja testudinum Rhizosphere 5-24 Capone & Taylor (1980) Thalassia testudinum Phyllosphere 0-5 Capone & Taylor (1977) Thalassia testudinum Phyllosphere 150 Goering & Parker (1972) Thalassia testudnum Phyllosphere 1.1-3.2 Capone et al. (1979) Thalassla testudinum Detritus 0.6-0.8 Capone et al. (1979) Zostera marina Various 0 McRoy et al. (1933) Zostera marina Rhizosphere 3.9-6.5 Capone (1982) Zostera manna Rhizosphere 0.2 Smith & Hayasaka (1982) Zostera marina Phyllosphere 0.2 Smith & Hayasaka (1982) Zostera marina Detritus 1.3 Kenworthy et al. (1987) 90 Mar. Ecol. Prog. Sei

ate species (Zostera marina) as measured in various ments of stable carbon isotope ratios in sediments and studies is summarized in Table 2. Additional data on , Kemp et al. (1984) concluded that ca 40 nitrogen-fixation in seagrass beds can be found in O/O of the vegetated sediment carbon probably was of reviews of Capone (1983, 1988). Except for the early planktonic origin. Sediment organic delta-13c values in studies of Goering & Parker (1972) and McRoy et al. a Zostera marina meadow were intermediate between (1973), the values indicate that nitrogen-fixation leads eelgrass and phytoplankton (Cooper 1989), which may to a daily input of several to several tens of milligrams also indicate the contribution of phytoplankton to N m-'. The seasonal fluctuations of nitrogen-fixation sediment organic carbon in seagrass beds, but the rates makes it difficult to estimate inputs on an annual unknown effect of benthic algae on the values hampers basis, but this figure may amount to 1 to 6 g m-2 if we a simple interpretation. combine the estimated annual inputs in both rhizo- The quantitative importance of sedimentation for the sphere and phyllosphere of T. testudinum given by input of nutrients to seagrass beds can only be assessed Capone & Taylor (1977, 1980). in a very preliminary way with the limited data avail- able. Harlin et al. (1982) found a sediment accretion of 2.5 cm in field plots of Zostera manna in a low energy Sedimentation area in Rhode Island (current velocity 3 cm S-' at 20 cm above the sediment) between August and October, i.e. Quantitative observations of sediment texture in from the period of highest shoot density through the beds of seagrass vegetations frequently have shown period of population decline in autumn. Assuming a that mean particle size of sediment grains is low com- specific gravity of 2.4 g cm-3, and a nitrogen content of pared to unvegetated sediments. This phenomenon 0.1 O/O on a wet weight basis, this would represent an generally has been ascribed to a decrease in current input of 60 g N m-2. In comparison, the organic input velocity by the resistance of the seagrass canopy, from phytoplankton to an eelgrass sediment has been which causes a reduction in the sediment-carrying estimated as 50 to 300 g C m-' yr-' (Kenworthy & capacity of the water. Reduction of current velocities Thayer 1984) which is equivalent to ca 7 to 45 g N m-' inside seagrass vegetations repeatedly has been yr-l. Thus sedimentation may provide the vegetation reported (Scoffin 1970, Fonseca et al. 1982, Harlin et with more nitrogen than we estimated is demanded al. 1982, Almasi et al. 1987). Sedimentation in sea- annually for biomass production (5 to 35 g m-2). grass beds is influenced by several factors: Short & Sedimentation rates, however, may differ strongly Short (1984) added various types of sediment partic- between sites: in a dynamic area (current velocity 17.5 les to culture systems with and without seagrasses. cm S-'), Harlin et al. (1982) found little sediment fluctu- Turbidity consistently decreased more rapidly in the ation; at higher current velocities in sparse vegetations, systems with seagrasses. A clear species difference, between shoots can be observed (Scoffin 1970). however, was noticed, the flat-bladed species A limited sedimentation rate, 4.96 g dry wt m-2 wk-' in Halodule wrightii being more efficient at trapping summer and 1.60 g dry wt m-2 wk-' in winter (equiva- particles than , which has cylin- lent to ca 0.3 g N m-2 yr-l), was also found by Almasi et drical leaves. Both differences in the morphology of al. (1987) in plots of Thalassia. Apart from the large the leaves and in shoot density were held responsible variations in sedimentation rates between various for this phenomenon. Other factors such as flow vel- growth locations, an assessment of the importance of ocity and relative water depth are also expected to sedimentation processes for nutrient budgets in sea- affect sedimentation (Scoffin 1970, Fonseca & Fisher grass beds is complicated by the fact that accretion may 1986). only be a seasonal phenomenon, coinciding with the It is obvious that the trapping effect of seagrass production of above-ground biomass. After senescence canopies is not restricted to sediment particles sus- and die-back of the canopy, the bed surface is no pended in the water, but also will include organic longer protected and scouring will result in the gradual particles such as phytoplankton and detritus. The disappearance of the sediment depositions. Such a observations carried out in a tributary of Chesapeake chain of events can be derived from the experiments of Bay are illustrative in this respect. In submersed vascu- Harlin et al. (1982), who denuded plots of eelgrass and lar plant beds dominated by the macrophytes Ruppia found that rapid sediment erosion followed. Presum- maritima and Potamogeton perfoliatus, a decreased ably, ths process will nullify the nutrient input coinci- level of planktonic chlorophyll a was demonstrated in dent with the preceding sediment deposition. Theoreti- the water column (Kemp et al. 1984, Ward et al. 1984). cally, seasonal erosion may even outreach seasonal Moreover, sediments in the plant beds were signifi- deposition, resulting in a net loss of nutrients from the cantly enriched in organic carbon and chlorophyll a system, but there appear to be no quantitative data to compared to unvegetated beds. Applying measure- substantiate this possibility. Hemminga et al.: Nut1.ients In seagrass meadows 91

Nutrient uptake by leaves instance, found that after a 24 h incubation of the leaves of Zostera marina with '5~-ammonium, tracer As is the case for other submerged aquatic mac- enrichment in the root-rhizome tissue was similar to rophytes, seagrasses are capable of removing N- that in the leaf tissue, indicating rapid translocation nutrients from both the water column and the sedi- from leaves to below-ground tissues. However, when ment. In the current literature on seagrass ecology, the roots had been exposed to the tracer, the I5N however, it is usually assumed that nutrient absorption enrichment of the leaves remained behind that of the by the roots is of major importance. This assumption is root system by at least an order of magnitude. In based on several pieces of evidence. Several studies another investigation with 32P-tracer hardly any trans- have shown that intensive ammonium regeneration location was found: transport between above- and occurs in the sediment of seagrass meadows; compari- below-ground tissues was only about 3 to 4 % of the sons of ammonium regeneration rates with estimates of tracer taken up during a 120 h incubation period (Brix plant nitrogen requirements indicate that in most cases & Lyngby 1985). These findings are remarkable in view the ammonium produced equals or even exceeds plant of the fact that the larger part of biomass production nitrogen demands (Iizumi et al. 1982, Short 1983a, generally occurs above-ground, and transport of Dennison et al. 1987, Caffrey & Kemp 1990); only in nutrients would be expected to be mainly in the one case, regeneration (in an organic-poor sediment) acropetal direction if nutrient uptake was dominated seemed inadequate to match plant demands (Short by the root system. 1983a). Ammonium regeneration in the water column The capacity of the leaves for nutrient uptake is is limited compared to regeneration in the sediment suggested by observations showing that seagrass com- (Iizumi et al. 1982). Obviously, the relatively high munities are able to reduce ammonium concentrations ammonium regeneration rate in the sediment a priori in the water column drastically (e.g. Short & Short 1984, advocates the role of the roots in plant nitrogen uptake. Short & McRoy 1984). As far as N-nutrients are con- Furthermore, the relationship between sediment type cerned, both ammonium and nitrate are taken up by and plant morphology was noted decades ago (e.g. the leaves, to an extent dependent on the ambient Ostenfeld 1908), and in recent times this relationship concentration (Iizumi & Hattori 1982, Short & McRoy has been shown to involve sediment nutrient condi- 1984). In contrast to the results obtained by the former tions (Short 1983b, 1987). Experimental enrichment of authors, the data given by Short & McRoy indicated a the sediment resulted in increased leaf growth rate preference for ammonium over nitrate uptake. In line (Bulthuis & Woelkering 1981), leaf length, biomass and with these results are the observations of Doddema & number of shoots (Orth 1977). Finally, the potential of Howari (1983) on nitrate reductase activity in the root-rhizome system as measured by in vitro incu- stipulacea. This enzyme catalyzes the first step in the bation experiments is such that, in relation to concen- reduction of nitrate, which is necessary for incorpora- trations of interstitial ammonium and nitrate, the major tion of the nitrogen moiety of the nitrate molecule into part of the plant nitrogen uptake may occur via these cellular compounds. Only very low activities were organs (Iizumi & Hattori 1982, Short & McRoy 1984). A found, both in above-ground and below-ground plant recent study of glutamine synthetase activity in Zostera parts, suggesting that nitrate was only a marginal manna roots points to a similar conclusion. After source of nitrogen to the plant. More substantial ammonia uptake, this enzyme performs the initial activities of the enzyme were established in Zostera assimilatory step by combining ammonia with gluta- manna (Roth & Pregnall 1988); leaf activity was found mate to form glutamine. The potential capacity of this to be conspicuously higher than root activity; more- enzyme in the roots appeared to be more than sufficient over, 6 d exposure of the seagrass plants to high nitrate to meet the plant nitrogen requirements (Pregnall et al. concentrations induced increased nitrate reductase 1987). activity in certain plants. The physiological capacity of Caution, however, should be observed in allotting seagrasses for nitrate uptake and assimilation therefore the root system the dominant role in nutrient uptake in appears to be variable, possibly depending on ambient the existing variety of field situations. It should be nitrate concentrations and the presence of an alterna- realized that much of the evidence mentioned above, tive nitrogen source. such as the high ammonium regeneration rate in the The observation that leaves of Zostera marina, on a sediment, is no direct proof for the presumed impor- dry weight basis, have a greater affinity for ammonium tance of root uptake. Furthermore, the data given in than roots (Thursby & Harlin 1982) can be interpreted several studies indicate that translocation of both N- as an adaptation to the relatively low nutrient condi- and P-tracers from roots to leaves is less intensive than tions of the water column. Indeed, the nutrient uptake the reverse process (Penhale & Thayer 1980, Borum et capacities measured for Zostera marina leaves indicate al. 1989, Iizumi & Hattori 1982). The latter authors, for that these plant parts can be very important in captur- 92 Mar. Ecol Prog. SErr. 71 85-96, 1991

could be obtained by leaf uptake at average production rates of 0.003 g C g-l h-'; at ammonium concentrations of 2 pM and low production rates, potential leaf uptake would even exceed nitrogen demand. Evidently, the total amount of nutrients obtained by the canopy will be strongly dependent on the fluctuat- ing concentrations of ammonium and nitrate in the watercolumn and the seasonally changing shoot bio- mass. So far no attempt has been made to calculate nutrient uptake on an annual basis, talung into account the varylng conditions throughout the year. To obtain such an esbmate, we used the regressions of uptake by leaves and roots of Zostera marina vs ambient nutrient concentrations (ammonium, nitrate) determined by Short & McRoy (1984), and combined these results with our data for nutrient concentrations and biomass of a perennial population of Z, marina in Lake Grevelingen (The Netherlands), measured during a monitoring pro- gram in 1987 and 1988. Fig. 1 shows the calculated time course of the uptake of ammonium and nitrate by the above-ground biomass, and the uptake of ammonium by the roots. The characteristics of nitrate uptake by the roots were not measured by Short & McRoy, so the uptake of this compound by the roots could not be calculated; however, the interstitial con- centrations of nitrate are low compared to ammonium (Boon 1986a, b, van Lent unpubl.), and therefore its relative importance for below-ground nitrogen uptake presumably is small. The uptake curves fluctuate with time, reflecting the variable concentrations of ammonium and nitrate measured, and the changing biomass. L~vingroots and shoots of Z. marina in Lake Fig. 1. Tune course of calculated ammonium (0) and nitrate lo) Grevelingen are present throughout the year; however, uptake by a Zostera manna population in Lake Grevehgen in view of the low water temperatures during winter (The Netherlands). (a) Leaf uptake; (b) root uptake. The popu- and the fact that growth is restricted to spring and lahon is located on a permanently submersed, low current site Data on sediment lnterst~tialammonium (depth 0 to 10 cm), summer, uptake processes presumably are of quantita- ammon~umand n~trateIn the watercolumn, and determma- hve importance only from April to October. Therefore tions of above- and below-ground b~omass,carned out penod- the potential uptake of the various N-nutrients during ~callyin the seagrass bed, were comblned wth the following the winter months, shown by the curves in Fig. 1, was regressions denved from data of Short & McRoy (1984) y = ignored in the calculations of cumulative annual 0.8~+ 0.89 and y = 0.47~+ 0 84, descnbing leaf uptake (y) by Z. manna as a funcbon of ammon~umand nitrate concen- uptake, which was determined by calculating the area trahon (X) in the water column, respectively; and y = 0 008x + under the curves in the period from April to October/ 0.93, descnbing root uptake as a function of ambient November (non-shaded in Fig. 1). Results are given in ammonium concentrabon in the root compartment The part of Table 3. Calculated ammonium and nitrate uptake by the curves In the non-shaded penods was used for calculation of cumulative annual nutnent uptake Table 3 Zostera manna. Uptake of N-nutnents by leaves and by roots in Lake Grevelingen (The Netherlands). Cumulative uptake was calculated from the part of the curves (Fig. 1) in ing nutrients from the water column. Iizumi & Hattori the non-shaded periods (1982) estimated that at ambient ammonium and nitrate concentrations of 4 and 378 nM, respectively, 45 % of the nitrogen required for eelgrass growth can Leaves Roots Leaves Roots be supplied by leaf uptake. Short & McRoy (1984) calculated that at a water ammonium concentrabon of Nitrate (g N m-*) 4.3 6.0 3.7 pM one-third of the eelgrass nitrogen requirement Hemminga et al.: Nutnemnts in seagrass meadows 93

the leaves in 1987 and 1988 is equivalent to 15.5 and therefore is undoubtedly important for the nitrogen 15.8 g N m-2, respectively. These data indicate that the enrichment of these systems; however, for a continued leaves are responsible for 60 to 70 % of the total plant biomass production other elements such as phosphorus uptake. The dominance of the leaves not only holds and micronutrients are required as well. This means when leaf uptake of ammonium and nitrate is con- that crucial contributions must come from either leaf trasted with root uptake of ammonium, but also when uptake or sedimentation, or - more likely - from a ammonium uptake only is considered. combination of both. Neither of these processes has This calculation exercise of course has its limitations; received much attention in the seagrass literature, par- for instance, fluctuating environmental factors such as ticularly not in the context of nutrient inputs to the light and temperature influence biomass production seagrass systems. Sedimentation is a phenomenon and undoubtedly also will affect nutrient uptake. The which is not equally conspicuous in all habitats where effects of these and other modifying factors are not seagrasses abound, for instance in water with low ses- included in the calculation, and the figures therefore ton content or in high current areas, where sedimenta- give only an indication of potential uptake values. The tion rates are low. Consequently, in these situations relevant aspect of this calculation, however, is that it nutrient replenishment is expected to become more shows the relative importance of leaf uptake vs root dependent on leaf uptake. It is interesting in this uptake, on an annual basis. respect that decreased sedimentation rates resulting By capturing ammonium and nitrate from the water from higher current velocities may coincide with an column, seagrass meadows are potentially enriched enhanced potential for leaf nutrient uptake, due to the with a substantial amount of nitrogen originating from reduction of the leaf surface boundary layer (Fonseca & outside the seagrass beds, a point which must be Kenworthy 1987). An intriguing situation presents itself stressed in the context of this paper. Moreover, leaf where seagrasses show luxuriant growth in clear, i.e. uptake presumably will reduce the losses of nutrients seston-poor water, of oligotrophic character, such as from the seagrass bed as nutrients diffusing from the may be found in tropical waters. In areas with nutrient- sediment to some extent wdl be intercepted by the poor sediments (e.g. carbonate sediments derived from canopy. In view of the capacity of the leaves for uptake coral reefs) it is doubtful if the root system alone can of N-nutrients, as discussed above, we may even go ensure an adequate nutrient supply. It would be of one step further and hypothesize that the ammonium great interest to measure uptake of nutrients by sea- resources supplied by regeneration processes in the grass leaves in these systems, to determine how the sediment of seagrass beds are not primarily tapped by plants have adapted to low ambient nutrient concen- the roots, but by the leaves. trations. The potential importance of leaves for the input of N- nutrients into the seagrass meadow, which emerges CONCLUDING COMMENTS from our discussion of leaf vs root uptake, is not surpris- ing if the structure of the leaves and the implications of With regard to nutrient fluxes, the seagrass meadow a submerged existence are considered. In terms of leaf must be considered as an open system. Fluxes of structure 3 points are relevant. First, most seagrasses nutrients from and to these systems are associated with have leaves with a high ratio of absorptive surface area a series of commonly occurring processes. The persist- to volume of nutrient-requiring tissue, because of both ence in time of most seagrass meadows obviously their strap-like shape and the presence of gas-filled points to a balance between nutrient losses and nu- lacunae that occupy much of the interior. Second, the trient gains. Such a balance in time need not imply a sites of high demand for nutrients, the photosynthetic continuous, complete equihbrium. Many processes cells, are concentrated in the epidermal layer, i.e. near- contribute to the final nutrient status of the seagrass est the surrounding water. Third, an efficient apoplastic system. Fluctuating biotic or abiotic factors in the route (i.e. through cell walls) for the transfer of dynamic marine environment may temporarily accen- nutrients from seawater to the epidermal cells appears tuate any of these processes, possibly resulting in year- to exist (Barnabas 1988). Thus seagrass leaves are to-year variations in net losses or net gains of nutrients. theoretically capable of acquiring nutrients without It is tempting to speculate that the consequences of relylng on root uptake. Considering that most sea- such imbalances may find their reflection in fluctua- grasses grow best when continually submerged, it is tions of the productivity of seagrass meadows. unlikely that acropetal transport of dissolved nutrients We have discussed 3 processes which may dominate from roots to leaves wdl be efficient because the normal the replenishment of nutrients: nitrogen-fixation, driving force, evapotranspiration from the leaves which sedimentation and leaf uptake. Nitrogen-fixation is a pulls water up the xylem vessels, is missing. Other feature of nearly all seagrass beds investigated and mechanisms such as root pressure could account for an 94 Mar. Ecol. Prog. Ser. 71: 85-96, 1991

upward flow (Salisbury & Ross 1985) but for seagrasses gen acquisition and conservation in eelgrass plants. Aquat. the situation is unknown. Bot. 35: 289-300 Direct absorption by seagrass leaves of large Brix, H., Lyngby, J. E. (1985). Uptake and translocation of phosphoms in eelgrass (Zostera marina). Mar Biol. 90: amounts of inorganic nutrients from the water column 111-116 implies that seagrasses may compete with other organ- Brylinsky, M. (1977). Release of dissolved organlc matter by isms in their environment. Potential competitors some marine macrophytes. Mar. Biol. 39: 213-220 include such as phytoplankton and attached Bulthuis, D. A., Woelkering, W. J. (1981). Effects of in situ nitrogen and phosphorus enrichment of the sedunents on algae, but also heterotrophs associated with detritus. the seagrass Heterozostera tasmanica (Martens ex Comparative studies of the nutrient uptake characteris- Aschers.) den Hartog in Western Port, Victoria, Australia. tics of seagrass leaves and other components of shallow J. exp. mar. Biol. Ecol. 53: 193-207 marine ecosystems are needed. Caffrey, J. M., Kemp, W. M. (1990). Nitrogen cycling in sedi- More study is required for all the processes covered ments with estuarine populations of Potamogeton per- fofiatus and Zostera marina. Mar. Ecol. Prog. Ser. 66: in this review because data are scarce and not all the 147-160 gains and losses have been measured in any one sea- Capone, D. C. (1982). Nitrogen fixation (acetylene reduction) grass system. It is clear, however, that a better under- by rhlzosphere sediments of the eelgrass Zostera manna. standing of the nutrient balance of seagrass meadows Mar. Ecol. Prog. 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This article was submitted to the editor Manuscript first received: June 11, 1990 Revised version accepted: January 21, 1991