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N:P balance in wetland forests: productivity across a biogeochemical continuum.

II. Introduction

Wetlands perform many important functions (Mitsch & Gosselink, 1993) among which is their ability to intercept water, sediment, and nutrients from adjacent uplands (Weller et al., 1994). As a result of the high degree of hydrologic interconnectivity inherent in riparian systems, wetland forests have the potential to influence the biogeochemistry of extensive landscapes. A key facet of that function is the transformation of nutrient forms during passage of water through a riverine system. Although many empirical studies have documented these transformations (Elder, 1985; Lowrance et al., 1984; Peterjohn & Correll, 1984) and an understanding has developed of some aspects of the controlling processes (Groffman et al., 1996; Lowrance, 1992; Mulholland, 1992; Nelson et al., 1995), many uncertainties remain. Thus, efforts at synthesizing general concepts or paradigms concerning biogeochemical functioning of riverine forests (Brinson, 1990, 1993; Lockaby & Walbridge, 1998; Lugo et al., 1990) are handicapped by an inadequate knowledge base.

As a result of the essential functions performed by these systems in combination with ever-increasing societal pressures from land-use conversion and pollutant loadings, it is very critical that we improve our general understanding of wetland function and the driving forces behind biogeochemical distinctions among systems. We suggest that progress toward these goals might be made by examining the N:P balance of wetland forests and investigating how vegetation productivity and nutrient circulation are altered as changes occur in N:P status.

We further suggest that N:P balances of wetland forests will be reflected in the N:P ratios of vegetation and that as ratios of different systems shift along a N:P continuum, factors controlling the processing and circulation of elements will differ. As suggested by Koerselman and Meuleman (1996), N:P ratios in forest vegetation may serve as a bioassay of biogeochemical constraints on vegetation net primary productivity (NPP) as well as tendencies for distinctions to occur in NPP partitioning and conversions between organic and mineral forms of N and P.

Although the initial N:P balance of a wetland forest may be determined by its landscape position and the natural features of the hydrologic catchment, there exists great potential for that balance to shift in either direction along the continuum as a result of NPS pollution inputs (Caraco, 1995; Caraco & Cole, 1996; Turner & Rabalais, 1991). In addition, since forest management pressures on many riparian corridors continue to increase, a better understanding of relationships between nutrient circulation and forest productivity would enhance management capabilities and simultaneously ensure maintenance of biogeochemical functions during management. Consequently, the need for unifying concepts and an improved understanding of factors driving variation in biogeochemistry among riparian ecosystems is urgent.

III. Elemental Ratios as Indicators of Biogeochemical Balance

The concept of using elemental ratios as indicators of nutritional constraints on productivity as well as general biogeochemical status has precedence more in aquatic than in terrestrial systems. Ratios of [greater than]15 or [less than] 15 (atom basis) have been suggested to represent P and N limitation, respectively, in phytoplankton (Redfield, 1958). More recently, studies in freshwater systems have indicated that the biological significance of N and importance of N and P balance for phytoplankton populations were greater than previously supposed (Elser et al., 1990). The nature of phytoplankton abundance shifts in relation to changes in N:P balance may be strongly related to changes in community composition (Smith, 1982; Suttle & Harrison, 1988).

Differences in N:P ratios between oligotrophic and eutrophic lakes may reflect sources of biogeochemical inputs, according to Downing and McCauley (1992). These authors indicated that waters emanating from undisturbed watersheds display larger N:P ratios than do those influenced by pollution. Caraco (1995) has extended the use of N:P ratios in rivers and suggested that the ratios may aid in estimating the relative magnitude of nonpoint vs. point sources of N and P inputs, indicating that aquatic N:P balances might serve as sensitive biogeochemical indicators of trends in N or P pollution (Caraco & Cole, 1996; Turner & Rabalais, 1991).

Ratios of N:P may also serve as indicators of the tendency for some microbial processes to occur. A forest floor ratio of 10:1 (concentration by weight basis) may be optimum for meeting the N and P demands of decomposer organisms (Vogt et al., 1986). Presumably, ratios [greater than] 10 or [less than] 10 would imply P or N imbalance respectively in the decomposition process. Vogt et al. (1986) have observed that N:P ratios in forest litterfall range from approximately 9 to 27 across all forest regions of the world and suggest that as ratios increase beyond 10, detrital inputs may be less palatable to decomposer populations. Similarly, during decomposition of floodplain litter with ratios slightly higher than 10, tendencies for P to be immobilized while N was mineralized suggest P limitation to microbial processes as well (Lockaby et al., 1996).

In addition, ratios in seagrass foliage have been used to indicate the occurrence and magnitude of P deficiency in a Florida marsh (Fourqurean & Zieman, 1992). In the marsh described, N:P ratios ranged from 30 to 60 as distance from bird colonies (i.e., point sources of P) increased.

During the last 30 years, much attention has been devoted to the use of elemental ratios as indicators of deficiencies or imbalance in nutrition of commercial crops and forests. Ingestad (1979) reported that optimum growth of several genera of trees occurred at N:P ratios in live foliage ranging from 14 to 30, although these are predicated on the presence of optimal levels of other macroelements as well. Koerselman and Meuleman (1996) argue convincingly for the use of N:P ratios in live vegetation as a diagnostic tool for identification of general N or P limitation and to test some well-known hypotheses at the ecosystem level regarding relationships between N and P availability vs. plant density or succession.

IV. Oligotrophic vs. Eutrophic Wetland Forests

We propose to extend N:P balance concepts stemming from aquatic systems and commercial forest nutrition to natural wetland forests. We will use this extension to develop the concept of a biogeochemical continuum based on N:P balance that could serve as a general framework for hypotheses concerning differences among wetland forests in terms of biogeochemical constraints on NPP and the capability to influence nutrient loads in ground- and surface waters.

In many portions of the world, riverine systems may be classed in a general sense as eutrophic or oligotrophic, based, in part, on landscape position and soil characteristics of associated catchments. A classic pair of such river systems is the Rios Negro and Maranon in Brazil which merge to form the Amazon. The Rio Negro is a blackwater river stemming from a hydrologic catchment dominated by sandy, infertile soils, and consequently it is generally nutrient and sediment poor. In contrast, the Rio Maranon carries a substantial load of clayey sediment which results in a more fertile floodplain due to greater alluviation compared to that of the Negro.

The vegetation of the two floodplains reflects the differential in floodborne nutrients. The Rio Negro is occupied by low productivity, igapo forests while the Rio Maranon floodplains are vegetated by higher-productivity, more diverse varzea forests (Prance, 1989). Although forest productivities of the Negro and Maranon floodplains differ, aquatic productivities within both systems are low. Vegetation productivities of both systems are controlled by biogeochemistry, while aquatic productivities are constrained by divergent limiting factors. In the case of the Rio Maranon, lack of light from turbidity limits river production, whereas production in the Rio Negro is constrained by low nutrient availability (Brinkmann, 1989).

V. Aboveground Productivity vs. Hydrology

Litterfall values have been used as an indicator of minimum levels of NPP in forests (Bray & Gorham, 1964), and the amount of annual litterfall is of major importance to energy and nutrient cycles, especially in floodplain systems (Mattraw & Elder, 1984). Several studies (Conner & Day, 1976; Conner et al., 1981; Shure & Gottschalk, 1985) have indicated that within a given geographical zone, litterfall values for wetland forests are often greater than in nonwetland areas. In wetlands, litter production is often, but not always, higher in flowing-water situations than in still-water areas (Brinson et al., 1980; Brown & Peterson, 1983; Conner & Day, 1976; Schlesinger, 1978).

Litterfall studies encompassing more than one or two years are uncommon, making it difficult to consider annual variations in litter production and the factors causing these variations. The extent and timing of flooding has been shown to affect tree growth rates (Broadfoot & Williston, 1973; Conner et al., 1981), which should also be reflected in leaf litter production. Studies have shown that forest productivity appears to peak at a once-per-year flood frequency if flooding occurs during the dormant season (Gosselink et al., 1981).

Higher litterfall values appear also to be related to regular inputs of water, oxygen, and nutrients by floodwaters. Nutrient input and redox conditions determine, to a large extent, the mineralization patterns that influence various nutrient transformations in wetland soils. Nutrient limitations in wetlands have been reported by Brown (1981) for cypress domes responding to phosphorus inputs and by Mitsch et al. (1979) who found higher net productivity in riparian wetlands during years of increased nutrient loading.

Continuous, stagnant flooding may render some nutrients unavailable (e.g., increased denitrification, decreased mineralization, and lower nutrient inflow) and thus lower productivity (Brinson et al., 1981; Conner & Day, 1982). Flooding with stagnant water decreases the rate of height growth, needle expansion, and dry weight increment of Taxodium. The dry weight increment of foliage of Nyssa grown in stagnant water was up to five times less than that of seedlings grown in moving water (Hook et al., 1970).

In general, average litter production in a nutrient-enriched Louisiana crawfish pond was at the high end of that reported for seasonally flooded forests in several states (Bates, 1989; Conner & Day, 1976; Muzika et al., 1987; Shure & Gottschalk, 1985; and many others). Litter production in the crawfish pond was even greater than that reported in a sewage-enriched cypress stand (Nessel, 1978) or a sewage-enriched cypress dome (Brown, 1981).

The benefits of improved fertility due to flooding may be diminished by physiological stresses associated with anaerobic soils (Mitsch & Rust, 1984). Dormant-season flooding increases production via deposition of nutrient-laden sediments (Brown, 1981; Mitsch et al., 1979) and improved soil moisture conditions during the growing season (Broadfoot, 1967). Production may be reduced, however, if flooding causes an anaerobic rooting zone during the growing season (Faulkner & Patrick, 1992; Hook & Brown, 1973; Megonigal et al., 1993). A comparison of Louisiana and South Carolina floodplain sites across flooding gradients showed that forests with persistent flooding had lower NPP than forests with periodic flooding (Megonigal et al., 1997). Overall, leaf litterfall was 38% lower on plots with mean growing-season water depths above the soil surface, and reductions in NPP were much greater (fivefold) in hydrologically altered sites.

VI. N:P Balance and Deficiency in Wetland Forests

Similar distinctions between oligotrophic blackwater (sediment-poor) and eutrophic alluvial or redwater (sediment-rich) systems occur in many other regions of the world and, in particular, in the southeastern United States (Sharitz & Mitsch, 1993; Walbridge & Lockaby, 1994; Wharton et al., 1982). We will use litterfall mass and element content data from published and unpublished sources for riverine and depressional forest wetland communities to develop the concept of the N:P balance continuum. We believe that the continuum concept represents a realistic framework for gaining a general understanding of some biogeochemical distinctions among disparate forest wetland systems on a global scale (Lockaby & Walbridge, 1998).

An evaluation of existing litterfall mass and nutrient data for wetland forests on a global scale allows some insight into relationships between aboveground NPP and nutrient circulation. Calculation of a nutrient use efficiency (NUE) index (Vitousek, 1982) for N and P [ILLUSTRATION FOR FIGURE 1 OMITTED], for both depressional and riverine wetland forests, reveals a range of NUE with stereotypic red- and blackwater systems representing the extremes. There is a general tendency for some blackwater riverine forests (i.e., systems 10 & 21) to exhibit high NUE for both elements. Conversely, redwater forests such as 9, 17, and 19 are much less efficient for N while systems 7 and 14 exhibit lower NUE for P. It is also apparent that other systems are distinctly intermediate in NUE and that there is no obvious separation between depressional and riverine systems in terms of NUE.

The systems identified as extremes in N or P NUE are not restricted to a single geographic region. The high NUE blackwater systems (10 & 21) occur in the southeastern United States and Brazilian Amazon, respectively. Similarly, low N NUE systems (9, 17 & 19) occur from Illinois to Brazil. Systems 7 and 14 (i.e., low P NUE) are both temperate forests which are known to be P rich.

Based on a differential in geochemical "openness" between depressional and riverine systems, there has been speculation that greater tendencies exist for P deficiency to occur in depressional systems (Lugo et al., 1990). This possibility stems from lower opportunities for geochemical inputs of P in basin wetlands, although, in theory, N inputs from atmospheric sources may negate a similar differential for that element. If this were the case, a better-defined relationship might be expected among P in circulation, NPP in depressional systems, and NPP in riverine systems. However, the P relationship is very weak among both riverine and depressional wetland forests and statistically not significant for depressional systems [ILLUSTRATION FOR FIGURE 2A, B OMITTED], which suggests that, for this subset of wetland systems, vegetation productivity is not closely linked to amounts of P circulating in litterfall in either category of wetland forest.

However, relationships between NPP and N in circulation are much stronger than those of P within both wetland forest types [ILLUSTRATION FOR FIGURE 2C, D OMITTED]. Consequently, as Figure 2c and d indicates, aboveground NPP is directly related to amounts of N in litterfall in wetland forests in general, and these relationships show similar strengths for both riverine and depressional systems.

This leads to questions about why aboveground NPP may be more related to N circulation than to that of P in wetland forests and why the strength of the relationships for P differs between the two wetland forest types. Vitousek (1982) suggested that the relationship between N or P in litterfall and NPP relates to element availability and, correspondingly, to the degree to which NPP is constrained by supply of a particular element. If this is the case, Figure 2 implies that P is secondary to N in terms of a constraint on forest NPP in both types of wetlands and, possibly, that P is not a constraint at all in depressional systems.

The possibility of limitations on NPP due to N deficiency in both wetland types contradicts the theories offered by Lugo et al. (1990) that NPP of riverine systems should only rarely be nutrient limited while that of depressional forests would be primarily constrained by P. If there exists a real tendency for depressional systems to be deficient in N, this may be due to the hydrological differences between these and their riverine counterparts. As noted by Brown (1990), basin wetlands tend to have stagnant flooding with little lateral flow of water. This results in incomplete "flushing" and consequent accumulation of organic matter, which may reflect low N and/or P mineralization. In turn, this may generate a negative feedback whereby lignin:N and lignin:P ratios widen with corresponding further reductions in mineralization rates. Conversely, the better-aerated, less frequent sheetflow events of riverine forests may be more conducive to higher rates of N mineralization and circulation. However, dominance of N deficiency as a constraint on depressional forest NPP does not imply that P is not also limiting; rather, indications of N deficiency may overwhelm and mask those of P.

The occurrence of N deficiency in riverine forests is also somewhat unexpected (Lugo et al., 1990). The geochemical "opportunity" for floodwater inputs in those forests has caused deficiencies of any element to seem unlikely (Lugo et al., 1990). However, at a global scale, N deficiencies in forests are quite common (Kimmins, 1987), and thus, in terms of a nutritional environment, it appears that floodplain forests generally share this trait with their upland counterparts. In addition, the presence of the relationship shown in Figure 2c implies that this subset of floodplain forests shows no indication of N saturation, a condition that bodes well for nitrate assimilation from polluted groundwater (Hill, 1996). As in the case of depressional systems, N-deficient riverine forests may also be secondarily deficient in P. This is particularly true where wide N:P ratios occur.

VII. The N:P Balance Continuum in Wetland Forests

The graphical relationship between N:P balance and aboveground NPP indicates that, for a range of litterfall mass of 2-10 tons per hectare per year, N:P ratios in litterfall range from 4 to 30 [ILLUSTRATION FOR FIGURE 3 OMITTED]. This range of N:P ratios is wide compared to that reported for worldwide, temperate forests in general by Vogt et al. (1986). A normal distribution (p [less than] 0.05) emerges in Figure 3 which is reminiscent of graphs of crop yield vs. element ratios in live foliage. Such graphs are used to define Diagnostic and Recommendation Integrated System (DRIS) norms (i.e., ideal ratios reflecting balanced element supply) for specific crops (Tisdale et al., 1985).

An N:P balance continuum is visually suggested in Figure 3 as highly P-deficient riverine systems (e.g., tropical igapo systems 18 & 21) display very large ratios ([greater than]15). It is apparent that systems occur along the entire range of N:P ratios as the latter approach a minimum of 4. If the DRIS norm analogy is extended, productivity (as indexed by litterfall) peaks at a ratio of approximately 12, a value that might be interpreted to represent the optimum balance between these two elements in forested wetlands. This value is numerically similar to mean N:P ratios in senesced foliage of many deciduous, woody species calculated from Aerts (1996) and Killingbeck (1996). It is slightly lower than the critical ratio in live vegetation (i.e., approximately 15) identified by Koerselman and Meuleman (1996) for nonforested wetland communities.

Furthermore, we suggest that availability of both N and P would increase as ratios become smaller but that P availability would rise more sharply relative to N [ILLUSTRATION FOR FIGURE 3 OMITTED]. There is some evidence from experiences with fertilization in bottomland hardwood stands that continuum soils span the range (i.e., from highly deficient to abundant) of soil P availability relative to hardwood response to P fertilizer. In Figure 3, levels of extractable soil P range across the continuum from 3 mg/kg (system 5) to 25 mg/kg (system 7), with values around 7 mg/kg representing a "critical" level for P fertilizer response in bottomland hardwoods (H. Kennedy [U.S. Forest Service Soil Scientist, retired], pers. comm.). Thus, it appears that soils in systems with smaller ratios may reflect abundant P availability while those with larger ratios may be highly deficient.

Relative to the geographic origin of the data, it may be worth noting that a "halo" of tropical sites (17, 18, 19 & 21) occurs above and to the right of the majority of data points [ILLUSTRATION FOR FIGURE 3 OMITTED]. This halo pattern suggests that some tropical wetland forests exhibit the same N:P vs. litterfall mass pattern as their boreal and temperate counterparts but at an extended level in terms of both variables. The lack of a tropical halo on the left of Fig. 3 is to be expected, since many tropical forests are not associated with high P availability.

Comparisons of N and P resorption proficiency (RP) (Killingbeck, 1996) among the same wetland forests [ILLUSTRATION FOR FIGURE 4 OMITTED] indicate that RP for both elements tends to increase as N:P ratios from Figure 3 become larger. Increasing RP as N:P ratios increase may be an indication of increasing oligotrophy in those systems. As examples, some systems with large ratios, such as systems 18 and 21, exhibit almost complete resorption for P. Similarly, systems 1,4, and 5 are intermediate in RP, according to the P criteria of Killingbeck. These contrast with the occurrence of smaller N:P ratios where varying degrees of incomplete P resorption are usually displayed (i.e., systems 7, 8, 14 & 15).

The position of system 14 (Cache River in Arkansas) on Figure 4 is particularly interesting since we had previously speculated that, based on the very narrow N:P ratio, vegetation there is at or near P saturation. The Cache's position in Figures 3 and 4 would suggest that luxury consumption of P may have occurred in those forests to a much greater degree than in any other wetland forest included in our data subset. Although soil P data are unavailable, the presence of a P-rich substrate is possible on the Cache since high sediment accretion rates (from upstream agriculture) have been characteristically associated with that floodplain (Kleiss, 1996). Although not included as a data point in these figures due to lack of litterfall data, floodplain forests of the Atchafalaya River basin in Louisiana may reflect a similar biogeochemical status. The latter system has been subjected to high sediment loads from agriculture for many years, a condition that may be reflected in the very narrow N:P ratios in woody detritus reported there (Rice et al., 1997).

In contrast to the RP scenario for P, a relationship between RP for N and N:P ratios is less obvious. There is more variation among N:P ratios of systems exhibiting complete or intermediate RP for N than was the case for P. Apparently, low N resorption may occur across the entire N:P ratio range. This may imply that, while P deficiencies increase as N:P ratios increase, those ratios are not good predictors of N deficiency.

VIII. Concluding Remarks

We suggest that N:P ratios at the ecosystem or community level have considerable utility as an aid for understanding differences among wetland forests in terms of biogeochemical functions. The example described here focused on the productivity function, but we suggest that the utility of these simple ratios as an explanatory tool is not limited to this function alone. As an example, distinctions among wetland forests in terms of the efficiency of the biogeochemical transformation function (Lockaby & Walbridge, 1998) might be elucidated through its use. Thus, we are in agreement with Koerselman and Meuleman (1996), who previously suggested greater focus on this ratio for improved understanding of processes in a variety of ecosystem types.

We further suggest that the use of N: P ratios derived from abscised foliage are potentially as useful as those from live foliage for purposes of understanding system and community distinctions, although the former have not been historically utilized to the same extent. However, use of abscised foliage data probably requires some consideration of retranslocation proficiency among the same systems if the goal is to understand constraints on plant productivity. Furthermore, as observed by Koerselman and Meuleman (1996), when similar data on K (and, we suggest, Ca) become available to an increasing extent, calculation of ratios associated with these elements may help refine biogeochemical understanding considerably.

We speculate that hydrology and associated shifts in P supply are the primary drivers of the continuum. Thus, larger ratios are exhibited where hydroperiod is prolonged (with concomitant slow mineralization) and low P inflow as in floodplains 1, 5, and 10. Conversely, floodplains with hydroperiods of lower duration and much higher P inflows (i.e., systems such as 7 and 9, which are associated with high sediment loads stemming from agricultural sources) aggrade more rapidly in relative P availability than in that of N.

At the community level, relationships between litterfall mass and quantities of N in circulation are well defined for both wetland types. However, only a weak trend is apparent between litterfall mass vs. P in circulation for riverine forests, and no statistically significant trend is suggested within depressional forests. We interpret this to suggest that production in both types is primarily N limited, although the possibility of secondary P limitations is also likely in some cases.

Comparisons of resorption proficiency among systems indicate that P proficiency tends to increase in systems with larger N:P ratios. This seems to corroborate the possibility of secondary P deficiencies. Although an obvious trend was not apparent between resorption proficiency for N vs. N:P ratios, this does not weaken assertions that the primary limiting element in both system types is N. Rather, the lack of a trend may imply that N:P ratios are not good indicators of N availability and that ratio shifts may be primarily driven by changes in P supply. It should be noted that those systems with complete or intermediate resorption proficiency for N are generally those with low litterfall which occur at the lower left on Figure 2c and d. This suggests that those riverine and depressional systems are indeed N deficient.

While the initial balance between N and P in a floodplain forest is defined by natural features of the hydrologic catchment, human activities (e.g., non-point-source pollution) have the potential to cause bidirectional changes (dependent on whether N or P inputs are predominant) in positions of various systems on the continuum (Caraco & Cole, 1996). We suggest that human-induced, extreme shifts on the continuum could theoretically move wetland forests toward ratios reflecting luxury consumption of N or P and, in extreme cases such as that of the Cache River, saturation.

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Publication:The Botanical Review
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