Mass balance constraints on nutrient cycling in tropical seagrass beds

AquatiC botany ELSEVIER

Aquatic Botany 50 (1995) 21-36

Mass balance constraints on nutrient cycling in tropical seagrass beds Paul L.A. Erftemeijel~'b, Jack J. Middelburg a'* "Netherlands Institute of Ecology, Centre for Estuarine and Coastal Ecology, Vierstraat 28, 4401 EA Yerseke, The Netherlands ~Catholic University Nijmegen, Toernooiveld, Nijmegen, The Netherlands

Accepted 17 November 1994

Abstract A relatively simple mass balance model is presented to study the cycling of nutrients (nitrogen and phosphorus) in tropical seagrass beds. The model is based on quantitative data on nutrient availability, seagrass primary production, community oxygen metabolism, seagrass tissue nutrient contents, sediment-water nutrient exchange rates, and seasonal dynamics in seagrass and environmental variables for two contrasting seagrass meadows from a single study area in South Sulawesi (Indonesia). Possible pathways of nutrient acquisition and nutrient cycling are described and quantified, and implications for leaf/root uptake and autotrophy/heterotrophy are discussed. It is concluded that, on an annual basis, the tropical seagrass ecosystems in the study area are more or less equally balanced between net autotrophy and net heterotrophy. Root uptake may potentially account for 66-98% of total nutrient uptake from external sources. Model simulation based on 50% internal nutrient resorption (withdrawal of nutrients from old plant parts and translocation to new growing parts) shifted the ratio between leaf vs. root-uptake, increasing the importance of leaf uptake. The results of these mass balance calculations indicate that root and leaf uptake contribute about equally to total plant nutrient uptake in tropical seagrass beds.

1. Introduction The relatively high primary productivity of (tropical) seagrass beds implies a high demand for nitrogen and phosphorus, two of the main elements essential to plant growth. In tropical areas, where nutrient concentrations in the seawater are typically low, the high nutrient demand o f seagrasses appears to be met by highly efficient systems of nutrient trapping, uptake and recycling. Nutrient losses due to export of dissolved and particulate * Corresponding author at: Netherlands Institute of Ecology, Vierstraat 28, 4401 EA Yerseke, The Netherlands. 0304-3770/95/$09.50 © 1995 Elsevier Science B.V. All rights reserved SSDl0304-3770(94)00440-4

22

P.L.A. Erftemeijer, J.J. Middelburg /Aquatic Botany 50 (1995) 21-36

seagrass-derived organic material, animal grazing and denitrification are balanced by nitrogen inputs such as nitrogen fixation, particulate organic matter trapping and mineralization, and leaf uptake of dissolved nutrients (Hemminga et al., 1991 ). Nutrient recycling can be accomplished through rapid in situ decomposition of seagrass-derived organic matter within the seagrass bed, and through internal remobilization of nutrients from older plant parts during their senescence (Borum et al., 1989; Nienhuis et al., 1989; Hemminga et al., 1991 ). Several authors have examined nutrient limitation of seagrass growth in various parts of the world and have reached different conclusions (see Erftemeijer et al., 1994). Short (1987) tried to draw a basis for the different conclusions reached by postulating that seagrasses growing in northern temperate climates (and) in habitats with terrigenous sediments typically experience nitrogen-limitation whereas those in tropical environments (and) on carbonate sediments appear to experience phosphorus limitation. Short (1987) offered the sorption of phosphate to the carbonate sediments as the mechanism to account for this contrast. The general information available on nutrient dynamics in tropical seagrass beds, however, is scarce and scattered geographically or divided into smaller subjects. This makes it difficult to draw general conclusions on nutrient cycles and fluxes, and to establish balances between losses and gains of nutrients in tropical seagrass beds. Considerable losses of organic material (and thus nutrients) from seagrass beds have been documented for some areas (Hemminga et al., 1991), but in several other cases, seagrass beds are described as highly efficient sediment traps (Scoffin, 1970; Phillips, 1978; Short and Short, 1984; Fonseca and Fisher, 1986; Zhuang and Chappell, 1990), likely to accumulate significant amounts of allochthonous organic material (and thus nutrients). As such, it remains unclear whether tropical seagrass beds must be considered as a significantly autotrophic, heterotrophic, or equally-balanced ecosystem, or that, perhaps, such may vary from one locality to another. Field and laboratory experiments by various researchers have indicated that seagrasses are capable of taking up nutrients with both their leaves and roots. It remains unclear, however, what the relative contributions of these different uptake pathways are to the total plant uptake, and by what factors this is affected. Only few quantitative and comprehensive datasets have been recorded in literature on nutrient cycling and annual nutrient budgets in seagrass beds. Pedersen and Borum (1993) recently estimated that nitrogen uptake from external media (49% from water column and 51% from sediment) supplied 73% of annual N-incorporation in eelgrass Zostera marina L. in Denmark, while internally reclaimed nitrogen accounted for 27%. With regard to this topic, they stated that nothing is known for subtropical and tropical seagrass meadows in more permanently nutrient-poor waters, and they suggested that the strategies used by these species to obtain sufficient nutrients to support their high annual production rates might differ considerably from that used by temperate eelgrass. The present paper discusses the mass balance and fluxes of nutrients in tropical seagrass beds in South Sulawesi, Indonesia. Calculations are based on an exhaustive set of data on production, nutrient concentrations and resources, diffusion rates, seasonal dynamics, and plant C-, N- and P-contents in this area, which have been published elsewhere (Erftemeijer and Middelburg, 1993; Erftemeijer et al., 1993; Erftemeijer, 1994; Erftemeijer and Herman, 1994). Data are from a coastal seagrass bed on terrigenous sediment and a reef associated

P.L.A. Erftemeijer, Z.L Middelburg / Aquatic Botany 50 (1995) 21-36

23

seagrass bed on carbonate sediment. The extensive set of data on all these various variables from the very same study area provided the unique opportunity to establish a mass balance of nutrients for a tropical seagrass bed. The aims were to estimate the relative contributions of leaf- and root uptake to the annual nutrient incorporation, to study the dependence of the seagrass beds on inputs of nutrients from external sources (either in dissolved forms or as particulate organic matter), and to determine the effects of internal nutrient resorption on nutrient uptake pathways.

2. Sites description All data in this paper were derived from studies conducted in the Spermonde Archipelago and adjacent coastal waters in South Sulawesi, Indonesia, during 1990-1993. Data from two contrasting field sites were selected for working out a detailed mass balance calculation. These included the shallow-water reef fiat of the reef island Barang Lompo (5 ° 03' S, 119 ° 20' E), located c. 14 km off the coast, and the coastal intertidal mudflat Gusung Tallang (5 ° 04' S, 119 ° 27' E), located approximately 0.5 km north of the mouth of the Tallo River I

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24

P.L.A. Erftemeijer, J.J. Middelburg / Aquatic Botany 50 (1995) 21-36

(Fig. 1). Both sites are characterized by extensive well-developed seagrass beds dominated by Thalassia hemprichii (Ehrenb.) Aschers. and Enhalus acoroides (L.f.) Royle at Barang Lompo (mixed-species) and by E. acoroides at Gusung Tallang (largely monospecific). The two sites are considered representative of reef-associated and coastal seagrass beds in the area (Erftemeijer, 1994).

3. Data base Data used in this paper are derived from studies in South Sulawesi by the first author. They include data on primary production and oxygen metabolism of the seagrasses (Erftemeijer et al., 1993), nutrient concentrations and resources in the seagrass beds (Erftemeijer and Middelburg, 1993; Erftemeijer, 1994), nutrient diffusive fluxes across the sedimentwater interface (Erftemeijer and Middelburg, 1993), and seasonal dynamics of environmental variables and seagrass characteristics (Erftemeijer and Herman, 1994). Instead of recapitulating in the present paper how these data were collected, we have confined ourselves to referring to these publications, in which details on sampling and analysis are extensively elaborated. Data on nutrient concentrations and resources in the seagrass beds at the two localities are summarized in Fig. 2. They are summarized as the absolute quantities of nitrogen and phosphorus present in the various components in a cubic metre of seagrass ecosystem containing 8501 of seawater (water column) and 1501 of sediment (including 751 (B arang Lompo) to 1001 (Gusung Tallang) of pore water). These data are annual averages, derived from Erftemeijer and Herman (1994). In both sedimentary environments, the majority of the entire pool of nutrients ( > 85%) is present in the sediment, largely unavailable to the plants. This remained virtually unchanged when the relative proportions of water: sediment in the box of the model was changed from 850: 150 to a 950:50 or a 500:500 basis. Only a tiny fraction ( < 0.001%) of the total pool of nutrients is present in the water column and pore water in dissolved forms directly available for uptake by the plants (both environments). Approximately 13.8% of the nitrogen and 2.7% of the phosphorus is contained in the seagrass biomass in the meadow at the reef site. The amount of N and P contained in other biota (epiphytes, macroalgae, phytoplankton, microphytobenthos) is negligible ( < 0.1%) at this site. In the seagrass bed at the coastal site only 4.3% of the total pool of N and 0.4% of the total pool of P is captured in the plant biomass. At this environment, an additional 2-3 % of the total pool of N and 0.1-0.2 % of the total pool of P is contained in macroalgae. Table 1 summarizes data on water column nutrient concentrations, diffusive fluxes of nutrients across the sediment-water interface, seagrass leaf production, and N- and Pcontents of seagrass leaves. From these data, we calculated the nutrient requirements of the seagrasses (for both sites), which are also included in Table 1. Data on the oxygen evolution in the two seagrass beds under investigation, as measured using bell jars and electrodes (see Erftemeijer et al., 1993), are summarized in Table 2. In this article we use the term 'nutrient requirement' to represent the multiplication of production and nutrient contents. To simplify this matter, we only used data on leaf production (which represents c. 85% of the total annual plant production) and leaf nutrient

P.L.A. Erftemeijer, J.J. Middelburg / Aquatic Botany 50 (1995) 21-36 BARANG

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P.L.A. Erftemeijer, J.J. Middelburg / Aquatic Botany 50 (1995) 21-36

26

Table 1 Annual meana values for measured water column nutrient concentrations, calculated diffusive fluxes of nitrogen and phosphorus across the sediment-water interface, seagrass leaf production, and N- and P-contents of seagrass leaves, and annual nutrient requirements of seagrases (calculated from these values) for the two study sites

Water column NH4 (p,M) Water column NO3 + NO2 (/zM) Water column PO4 (p~M) Diffusive N-flux (g N m -2 year- ~) Diffusive P-flux (g P m- 2 year- l ) Seagrass production (g DW year- ~) N-contents ( % of DW) P-content (% of DW) Annual N-requirement (g N m- 2 year - 1) Annual P-requirement (g P m -2 year -~ )

Barang Lompo

Gusung Tallang

0.8 2.2 0.9 0.53 0.42 1100 2.07 0.15 22.55 1.65

1,4 3.2 1.4 1.56 0.14 200 2.28 0.22 4.56 0.44

a Mean values are derived from data published elsewhere (see text). Table 2 Gross primary production, community respiration and net production of seagrass ecosystems at the two study sites (BL, Barang Lompo; GT, Gusung Tallang), measured with bell jars equipped with oxygen electrodes in areas of varying seagrass density (see Erftemeijer et al., 1993 for details) Site

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within the plant, i.e. nutrients that are r e m o b i l i z e d internally f r o m older plant parts during their d e c a y for use in y o u n g plant parts during growth. Possible p a t h w a y s o f nutrient c y c l i n g in the seagrass system are s u m m a r i z e d in a d i a g r a m which is presented in Fig. 3. Here, we refer to ' o l d ' nutrients as to those nutrients which are regenerated f r o m old d e c a y i n g plant organic matter, either by internal resorption or by in situ d e c o m p o s i t i o n within the e c o s y s t e m (external r e c y c l i n g ) . W e refer to ' n e w ' nutrients as to those w h i c h are transported into the seagrass e c o s y s t e m f r o m outside via precipitation, water m o v e m e n t , particulate import and by nitrogen fixation (Barnes and Mann, 1991).

4. Mass b a l a n c e a p p r o a c h In the f o l l o w i n g discussion o f the mass balance o f nutrients in the two tropical seagrass beds, we c o n s i d e r three types o f nutrient sources: (1) dissolved ' n e w ' nutrients; (2)

P.L.A, Er)'?emeijer, J.J. Middelburg / Aquatic Botany 50 (1995) 21-36

27

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particulate 'new' nutrients; (3) 'old' regenerated nutrients. Other nutrient sources are excluded, because we do not have data. We realize that internal resorption may be important as additional mechanism, although we have no data on this for the seagrasses in the study area or any other tropical seagrass bed. Initially we present the model without internal resorption, and then we determine the effects of internal resorption on the outcome of the model. Our mass balance model has the following assumptions: (1) On an annual basis, the seagrass ecosystem is in steady state (i.e. the meadow is not expanding, or decreasing). (2) The mass balance approach concerns the entire seagrass ecosystem (not individual seagrass plants); thus including the various fauna components, epiphytes, etc. (3) The uptake of N and P is coupled to the ratio in which they are available (availability ratio). (4) All regeneration takes place in the sediment (decomposition). (5) Seagrass leaves do not release nutrients into the surrounding water (foliar release of phosphorus was found to be negligible in experiments with Zostera noltii Hornem., see Perez-Llorens et al., 1993). The first situation, described in the following model, is that of no internal resorption, i.e. nutrient requirements are fully met (100%) by nutrient uptake (either 'new' or 'old' nutrients). For nitrogen and for phosphorus, respectively, we then obtain the following mass balances:

P.L.A. Erftemeijer, J.J. Middelburg /Aquatic Botany 50 (1995) 21-36

28

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Fig. 4. The modelling effects of varying the N / P-ratio of mineralization on (a,b) the net autotrophy or heterotrophy of the seagrass system and (c,d) the relative contributions of leaf and root uptake, at the two study sites. (Ndisadv, advective export of dissolved N species; Npartimp, particulate import of N; Pdisadv, advective export of dissolved P species; Ppartimp, particulate import of P.)

N-uptake = N-mineralization + (N-conc.water × flushing)

(1A)

P-uptake = P/N-ratio × N-mineralization + (P-conc.water × flushing)

( 1B)

The mineralized N and P include both 'old' regenerated nutrients from dead seagrass material as well as 'new' nutrients derived from mineralization of organic matter trapped in the seagrass bed. The model parameter 'flushing' reflects the number of times that water has to be replaced to supply the required nutrients (to meet the required nutrient demand). The P/N ratio represents the molar ratio of phosphorus to nitrogen that is available for uptake after mineralization and subsequent modifications in the sediment. The result of this model are two equations with three unknown values, being: flushing, N-mineralization and P/N-ratio. Although there is no single solution to this problem, the equations can be solved for each chosen N/P-ratio (inverted as P/N ratio in the calculations of the model), by standard substitution/elimination (mathematical) procedures. The results of this type of modelling (i.e. by choosing varying N/P-ratios) are presented in Fig. 4 ad. 4.1. Autotrophy vs. heterotrophy Figs. 4a and 4b show the net import or export of dissolved and particulate nutrients as a function of the N / P ratio available following mineralization. Import and export are

P.L.A. Erftemeijer. J.J. Middelburg /Aquatic Botany 50 (1995) 21-36

29

expressed in grammes of N or P per square metre ecosystem per year; negative values represent export, positive values imply import. The most simple case is when the point of intersection of these two graphs is the same as the N/P-ratio in the seagrass leaves. In other words, N/P-ratio mineralization = N/P-ratio leaves. This implies that losses of organic matter (might they occur) are replenished by mineralization of trapped particulate organic matter with the same N/P-ratio as that of the leaves. An increase of the N/P-ratio (mineralization) above that of the seagrass leaf material implies that the system requires an input (import) of dissolved nutrients, and that the system is exporting (particulate) organic (seagrass) material. This, in turn, implies net autotrophy of the seagrass ecosystem. A decrease of the N/P-ratio (mineralization) below that of the seagrass leaf material implies that the system requires an input (import) of particulate material (nutrients), and that the system is exporting dissolved nutrients. This, in turn, implies net heterotrophy of the seagrass ecosystem. Bell jar measurements of oxygen metabolism in these seagrass meadows (Table 2; see Erftemeijer et al., 1993) indicate that net oxygen production during daytime is balanced by total community respiration. In other words, there is a net balance between autotrophy and heterotrophy. In Figs. 4a and 4b this balance is approached around the point of intersection (i.e. at a N/P-ratio of mineralization of about 28.5 for Barang Lompo and about 18 for Gusung Tallang). For Gusung Tallang, this seems to be further supported by the fact that the N/P-ratio of pore water nutrients (19.6) is approximately the same as that in the seagrass leaf material (19.7) (see Erftemeijer and Middelburg, 1993). At Barang Lompo the N/P-ratio of pore water nutrients is much lower than that in the seagrass leaf material. This would imply for considerable net heterotrophy of the system at this site. Bell jar measurements of oxygen metabolism at this site, do however indicate a net balance. Apparently, there are additional biogeochemical processes that regulate the availability of N and P (Capone et al., 1992; Erftemeijer and Middelburg, 1993). Another constraint to the model is supplied by the rate of diffusion exchange. The measured/calculated diffusive flux of N and P from the sediment into the water column determines the maximum possible export of dissolved nutrients from the ecosystem. The system can never export more dissolved nutrients than the amount of nutrients that diffuses across the sediment-water interface. This constraint provides an upper limit to the heterotrophy of the system, through a minimum limit to the N/P-ratio of mineralization (i.e. 24 for Barang Lompo; 15 for Gusung Tallang). This is a consequence of two assumptions: ( 1) all regeneration takes place in the sediment; (2) seagrass leaves do not release nutrients into the surrounding water. 4.2. L e a f uptake vs. root uptake

The estimated relative uptake of nitrogen and phosphorus by roots and leaves are plotted as a function of the N / P ratio in Figs. 4c and 4d. By using the results of the solutions to eqs. 1a and lb, the relative contributions of leaf- and root-uptake to the total nutrient uptake can be calculated as follows: Root uptake = [ ( minerali zation-diff.flux) /incorporation ] X 100%

(2A)

Leaf uptake = [ (diff.flux + (flushing X conc. ) ) / incorporation ] X 100%

( 2B )

30

P.L.A. Erftemeijer,J.J. Middelburg/Aquatic Botany50 (1995) 21-36

Fig. 4c shows that N-uptake at Barang Lompo is almost fully accounted for by root uptake (93-100%), little dependent on the N/P-ratio. At Gusung Tallang, root-uptake accounts for 60-70% of N-uptake, again little dependent on the N/P-ratio chosen (Fig. 4d). As N-uptake at both sites appears relatively insensitive to the N/P-ratio of mineralization that is chosen, we think that this provides a rather robust estimate of the relative contributions of leaf- and root N-uptake in the absence of internal resorption (at the points of intersection in Figs. 4a and 4b this gives: Barang Lompo, 98% root uptake/2% leaf uptake; Gusung Tallang, 66% root uptake/34% leaf uptake). For phosphorus, root-uptake accounts for 44-99% of total plant requirement at Barang Lompo (intersection point at N/P ratio of 29: 74%). At Gusung Tallang root-uptake constitutes 40-100% of total plant P-uptake (at intersection N/P = 18: 75%). The P-uptake appears to be sensitive to the choice of N/P-ratio in the model.

4.3. Stripping and trapping efficiency From the mass balance model we can calculate flushing rates for both sites for each given N/P-ratio (of mineralization). This is the minimum flushing rate (A) required to either export the excess of nutrients or to import the lack of required ('new') nutrients, based on measured actual average nutrient concentrations in the water column. From diurnal field measurements (unpublished) of current velocity and data on the geometry of the meadows, we can calculate the actual water flushing rates (B) for the two sites (i.e. 6.1 day -a at Barang Lompo; 11.5 day- ~ at Gusung Tallang). The ratio between A and B ( × 100%) is considered to represent the relative stripping efficiency (i.e. the efficiency with which the seagrass leaves are stripping nutrients from the water column) or the trapping efficiency (i.e. the extent to which the seagrass beds trap and subsequently mineralize allochthonous organic material relative to the load of organic matter in the water). Stripping efficiency varied from - 2.2 to + 1.9 % at Barang Lompo, and - 0.16 to 0.13 % at Gusung Tallang (for both N and P, since we assume coupled N and P uptake). Negative values indicate a release of nutrients from the system into the surrounding waters, positive values indicate actual uptake of 'new' dissolved nutrients. For Barang Lompo, the trapping efficiency of allochthonous POM varied from - 0 . 1 2 to + 0.14 % for N, and from - 0.60 to + 0.70 % for P. For Gusung Tallang, the dependency on allochthonous POM varied from -0.01 to 0.01% for N, and from - 0 . 0 4 to + 0.05 % for P.

4.4. Effects of internal resorption The effects of internal nutrient resorption on the relative contributions of leaf and root uptake were simulated in the model by lowering the uptake (incorporation) of N-only or of both N and P, while maintaining the same levels of N and P requirements. The results of this type of modelling are summarized in Figs. 5a-d. Modelling for the effects of 50% internal resorption of P-only, yielded unacceptable results (i.e. negative values for leaf uptake, which is equivalent to nutrient release by leaves, a process we have assumed not to occur). At Barang Lompo, the effects of internal resorption on N-uptake pathways are

P.L.A. Erftemeijer, J.J. Middelburg / Aquatic Botany 50 (1995) 21-36

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Fig. 5. The modelling effects of internal nutrient resorption on the relative contributions of leaf and root uptake to total nutrient demand of the seagrass beds at the balance of autotrophy and heterotrophy (i.e. at points of intersection of Fig. 4). Results are shown for no internal resorption (0 % N, 0 % P), 50 % resorption of nitrogen (50 % N, 0 % P) and 50 % resorption of N and P (50 % N, 50 % P). (a,b) Nitrogen and phosphorus uptake at Barang Lompo (BL); (c,d) Nitrogen and phosphorus uptake at Gusung Tallang (GT). relatively small (Fig. 5a). N-uptake by leaves remains insignificant relative to N-uptake by roots for each modelling situation. For P-uptake, however, the situation is different (Fig. 5b). Whereas leaf-uptake accounts for only about 20% of total P-uptake in the control (no internal resorption), a 50% internal resorption of N-only increases the relative importance of leaf uptake of P to over 80%. In the modelling situation of a 50% coupled N and P internal resorption, leaf uptake equals root uptake. At Gusung Tallang, the coastal locality, the effects of internal resorption are marked for both N and P uptake pathways. Internal resorption, whether N-only or N and P coupled, significantly reduces the relative importance of root uptake compared to leaf uptake (Fig. 5c). For P-uptake, the effects of internal resorption on leaf vs. root uptake closely resemble those observed for Barang Lompo (Fig. 5d). Accordingly, internal resorption of nutrients will increase the relative importance of leave uptake at the expense of root uptake.

32

P.L.A. Erftemeijer, J.J. Middelburg/ Aquatic Botany 50 (1995) 21-36

5. Discussion

The availability of a large comprehensive set of detailed quantitative data from two contrasting tropical seagrass beds from an area in South Sulawesi, Indonesia, provided the ideal opportunity to perform mass-balance calculations. These calculations have yielded some very interesting viewpoints and constraints to nutrient cycling in tropical seagrass ecosystems. They have provided insight in the relative importance of leaf versus root uptake of nutrients under different circumstances. Combined results from measurements of seagrass nutrient requirements, ambient nutrient availability, and oxygen metabolism of the entire community, provided insight in the fate of organic material produced in the seagrass beds. These mass balance calculations are essentially the first of its kind ever performed on data from a tropical seagrass ecosystem. 5.1. Autotrophy vs. heterotrophy

Combined results from nutrient requirement measurements, ambient nutrient availability, and oxygen evolution, suggest that tropical seagrass ecosystems are largely self-sustaining. The majority of the produced organic matter is kept within the system and decomposed in the sediment. This was also found by Lindeboom and Sandee (1989) who similarly studied oxygen evolution using bell jars in various seagrass beds in eastern Indonesia. Losses through export of seagrass material are probably small and appear to be balanced by significant imports of allochthonous organic matter, leaving the system balanced between autotrophy and heterotrophy, or even slightly heterotrophic (see also Table 2). This is in agreement with theories put forward by Smith ( 1981 ), Smith and MacKenzie (1987), and Smith and Hollibaugh (1993), who have suggested that coastal oceans, and in particular coastal marine macrophyte vegetations act as a global sink of organic matter rather than a source. In other words, coastal/marine ecosystems dominated by submerged aquatic vegetation may potentially be sites where more organic material is mineralized than produced. 5.2. Leaf vs. root uptake

The mass-balance model of nutrient cycling described in this paper can be used to put constraints on the relative contribution of root vs. leaf uptake of nutrients by the seagrasses to meet their total annual requirement. The model results presented in Fig. 4 provide an upper limit for the relative contribution of root uptake because they are based on the assumptions that there is no internal resorption and that all mineralization occurs in the sediments. For these conditions, the model reveals that root uptake accounts for approximately 44-99% at Barang Lompo and 40-100% at Gusung Tallang. Intersection points of the modelled curves, representing a situation where the ecosystem is in net balance, yield 98% root uptake for N and 74% root uptake for P at Barang Lompo, and 66% root uptake for N and 75% root uptake for P at Gusung Tallang. It has been shown, that the estimates for N-uptake are constrained better than the estimates for P-uptake, owing to differences in sensitivity to the modelled parameter (N/P-ratio of mineralization). The withdrawal of nutrients from senescing leaves and other older plant parts prior to abscission allows a plant to use the same unit of nutrient to build up several leaves or other

P.L.A. Erftemeijer, J.J. Middelburg / Aquatic Botany 50 (1995) 21-36

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Table 3 Nutrient resorption (as percentage of total nutrient requirement) in some selected ecosystems Ecosystem

% Nutrient resorption

Source

Terrestrial grassland Temperature deciduous and pinewood forest Evergreen mediterranean trees ('forest') Freshwater wetlands Mangrove forest Eelgrass (Zostera marina) beds Eelgrass (Zostera marina) beds Eelgrass (Zostera marina) beds Eelgrass (Zostera marina) beds

33%

Clark, 1977

37-77%

Stachurski and Zimka, 1975

46-65% 25-60% 52-70% 17% 24% 12% 27%

Pugnaire and Chapin. 1993 Hopkinson, 1992 Rao et al., 1994; Slim, 1995 Umebayashi, 1989 Borum et al., 1989 Pedersen and Borum, 1992 Pedersen and Borum, 1993

plant parts successively. Such retranslocation within the plant during decay (here termed internal resorption) is an important mechanism to minimize nutrient loss in all plants (Chapin, 1980). Table 3 provides an overview of the relative contribution of nutrient resorption to total plant nutrient requirements for some typical ecosystems. For most plant systems, nutrient resorption roughly contributes 30-60% to total nutrient demand. For seagrasses, only limited data are available. Experiments with eelgrass Z. marina from mesotrophic and eutrophic temperate environments revealed values for nitrogen resorption in the range of about 12-27% (Borum et al., 1989; Umebayashi, 1989; Pedersen and Borum, 1992, 1993). It is, however, generally found that plants growing in nutrient-poor environments are more efficient in nutrient resorption than plants from fertile sites. Taking this and the values in Table 3 into account, we suppose that modelling for the effects of 50% nutrient resorption in tropical seagrass beds (as described above) may provide a reasonable upper limit. The mass balance model as described in this paper does not provide quantitative constraints to internal nutrient resorption as we lack the quantitative data for this. The model does, however, provide an indication of the direction in which the ratio between root and leaf uptake will change as a result of internal resorption. Internal resorption will increase the importance of leaf uptake relative to root uptake (Fig. 5). Model results based on 50% internal recycling of nutrients may thus be considered as a likely lower estimate for the relative contribution of root uptake in tropical seagrasses. On the basis of 50% internal resorption of nutrients, root uptake may account for about 32 (Gusung Tallang) to 95% (Barang Lompo) of the external nitrogen requirement and about 50% of the phosphorus uptake. Carignan (1982) developed a simple empirical model for predicting the relative contribution of roots in phosphorus uptake by submerged macrophytes. The model only uses data on pore water and surface water nutrient concentrations. The model of Carignan has the form: P = 99.8/( 1 + 2 . 6 6 ( s / w )

-0.83)

34

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where P is the relative contribution of the root in phosphorus uptake, s and w are the pore water and overlying water phosphate concentrations, respectively. We applied the Carignan model to data on annual mean nutrient concentrations in the study area in South Sulawesi (PO 4 concentrations: 10.9/zM in pore water and 0.9/zM in surface water at Barang Lompo; 0.8 /zM in pore water and 1.4/zM in surface water at Gusung Tallang). This yielded a relative root uptake accounting for 74.4% of plant phosphate uptake at Barang Lompo, and for 53.8% of plant phosphate uptake at Gusung Tallang. The phosphorus uptake results obtained with the empirical Carignan model (54-74 % root uptake) compare well with those obtained in our mass balance model (about 50% and 75% with and without internal resorption, respectively). From both modelling approaches it becomes clear that root and leave uptake contribute considerably to the total phosphorus uptake by seagrasses. Comparable results were obtained by Pedersen and Borum (1993), who studied nitrogen cycling in temperate eelgrass (Z. marina) beds. They used an exhaustive set of data from measurements of seasonal changes in eelgrass biomass, production losses and nitrogen contents of different plant tissues, to estimate nitrogen uptake and internal nitrogen recycling. They estimated that nitrogen uptake from external media (49% from water column and 51% from sediment) supplied 73% of the annual nitrogen requirements of the eelgrass population in their study area. Internal recycling of nitrogen accounted for the remaining 27% of the total N-demand. As yet, the site of the maj ority-uptake of nutrients by seagrasses (roots or leaves) remains an ongoing dispute. Studies using labelled isotopes of phosphorus and nitrogen (McRoy and Barsdate, 1970; Iizumi and Hattori, 1982; Borum et al., 1989; Perez-Llorens et al., 1993) have demonstrated that seagrasses are capable of acquiring nutrients through each of the two pathways (i.e. leaf uptake as well as root uptake). Several laboratory studies on nutrient uptake by seagrasses (mostly on temperate Zostera species), using partitioned chambers, yielded high contributions of leaf uptake (Thursby and Harlin, 1982; Short and McRoy, 1984; Hemminga et al., 1994). Penhale and Thayer ( 1980 ), however, using similar partitioned chambers in their experiments, concluded root uptake in Z. marina to dominate over leaf uptake. Two-compartment chamber experiments, which monitor nutrient uptake by individual seagrass plants during several hours, provide an interesting insight into the potential uptake capacity of different plant parts (i.e. within hours). Such an 'individual plant' approach and 'short-term' assessment, however, does not provide information on the actual (overall) ecosystem 'behaviour' on an annual basis. In other words, individual seagrass plants may have the capacity to assimilate large amounts of nutrients from external media with their leaves or roots within a few hours, such as might be necessary to replace significant losses (i.e. by grazing, low tide exposure) or to enable certain growth stages (e.g. generative production, lateral shoot elongation), but on an annual basis, root and leaf uptake contribute about equally to total plant nutrient uptake (Pedersen and Borum, 1993; and this paper). The ability of seagrasses to take up nutrients at high rates with both their leaves and roots provides a strategy to balance nutrient losses and to maintain high productivities in dynamic marine environments. Finally, it should be mentioned that a similar apparent discrepancy between results of short-term vs. long-term and small-scale vs. large-scale approaches has been observed in

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the discussion o f e c o s y s t e m nutrient limitation (Smith, 1984; Howarth, 1988; Stevenson, 1988). Short-term and small-scale approaches h a v e p r o v i d e d e v i d e n c e o f N-limitation o f (seagrass) growth, w h e r e a s m o r e large-scale and longer-term approaches have r e v e a l e d e v i d e n c e o f P-limitation o f the (seagrass) standing crop. The results o f this study indicate the need for a series o f l o n g - t e r m e c o s y s t e m studies that include plant and nutrient dynamics, before we can assess nutrient limitation o f seagrass m e a d o w s .

Acknowledgements The authors wish to a c k n o w l e d g e the critical c o m m e n t s and helpful suggestions m a d e by Prof. Dr. P.H. Nienhuis, Prof. Dr. C. den Hartog and Dr. M . A . H e m m i n g a . The authors felt greatly stimulated by Prof. Dr. C. den Hartog, w h o e n c o u r a g e d t h e m to write this paper. This w o r k was m a d e possible by a grant f r o m the Netherlands Foundation for the A d v a n c e m e n t o f T r o p i c a l R e s e a r c h ( W O T R O , W 8 4 - 2 9 3 ) . C o m m u n i c a t i o n No. 754 o f the Netherlands Institute o f E c o l o g y , Centre for Estuarine and Coastal E c o l o g y , Yerseke, Netherlands.

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