Sediment interactions with submersed macrophyte growth and community dynamics

Aquatic Botany, 41 ( 1991 ) 41-65

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Elsevier Science Publishers B.V., Amsterdam

Sediment interactions with submersed macrophyte growth and community dynamics John W. Barko a, Douglas G u n n i s o n a and Stephen R. Carpenter b aEnvironmental Laboratory, Waterways Experiment Station, Vicksburg, MS 39180-6199, USA bCenterfor Limnology, University of Wisconsin, Madison, W153706, USA (Accepted for publication 25 October 1990)

ABSTRACT Barko, J.W., Gunnison, D. and Carpenter, S.R., 199 I. Sediment interactions with submersed macrophyte growth and community dynamics. Aquat. Bot., 41:41-65. We review and synthesize information available in the literature on sediment interactions with submersed macrophyte growth and community dynamics. Sources of particular nutrients for uptake by submersed macrophytes are critically evaluated. Sediment physical and chemical properties are considered as a product of macrophyte growth as well as potential delimiters of growth. Aspects of macrophyte nutrition that influence littoral nutrient dynamics and macrophyte community composition are highlighted, with attention to factors affecting sediment nutrient availability. Interactive effects of sediment nutrient depletion, sedimentation, bioturbation, and microbial activity on macrophyte growth are emphasized. Major linkages and feedbacks between aquatic macrophytes and sediment properties are considered in terms of elemental exchanges and responses at the ecosystem level. Changes in macrophyte community composition during lake aging, or over relatively shorter time periods, are suggested to occur partially in response to altered sediment properties.

INTRODUCTION

Submersed macrophytes are unique among rooted aquatic vegetation because they link the sediment with overlying water. This linkage is responsible for great complexities in nutrition, and has potentially important implications for nutrient cycling. During the past 15 years, it has become clear that, in addition to serving as a base for physical attachment, sediment also provides a source of nutrient supply to submersed macrophytes. It is now recognized that sediment composition exerts an important influence on macrophyte productivity and species composition. However, the mechanisms involved are complex. Most recent attention has focused on interactions between aquatic macrophyte growth and sediment nutrient status. This line of investigation has suggested that submersed macrophytes have more than a passive role in responding to their sediment environment. Relatively little attention has been given to specific processes in the littoral zone affecting 0304-3770/91/$03.50

© 1991 - - Elsevier Science Publishers B.V.

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sediment nutrient dynamics. It is becoming increasingly apparent that sediment nutrient availability is closely coupled with changes in macrophyte community composition; this in turn influences ecosystem processes on a broader scale. In this article we review and synthesize information available on sediment interactions with submersed macrophyte growth and community dynamics. MACROPHYTE NUTRITIONAL ECOLOGY

Nutrient acquisition." roots vs. shoots

For many years considerable controversy has persisted regarding the role of roots vs. shoots and sediment vs. open water in the nutrition of submersed aquatic macrophytes (reviewed by Sculthorpe, 1967; Denny, 1980; Smart and Barko, 1985; Agami and Waisel, 1986; Barko et al., 1986 ). Quantification of the relative contribution of sediment and water to nutrient uptake by submersed macrophytes remains critical to improved understanding of littoral nutrient cycling and littoral-pelagic nutrient exchanges. Based on a variety of information sources (above references and personal knowledge), a generalized synthesis of sources of nutrient uptake by rooted submersed macrophytes is provided in Table 1. Phosphorus and nitrogen have been studied most extensively, and for these nutrients, sediment is the primary source for uptake. Sediment appears to be the principal site for uptake of iron, manganese, and micronutrients as well. These elements tend to coprecipitate and are usually present in extremely low concentrations in oxygenated surface waters (Golterman, 1975 ). Dissolution products of relatively abundant salts are taken up principally from the open water. Among these TABLE 1 Primary sources of nutrient uptake by submersed aquatic macrophytes Nutrient (s)

Source

Nitrogen Phosphorus Iron Manganese Micronutrients

Sediment Sediment Sediment Sediment Sediment

Calcium Magnesium Sodium Potassium Sulfate Chloride

Open Open Open Open Open Open

water water water water water water

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ions, potassium and calcium are potentially most important in affecting submersed macrophyte growth. Potassium can be obtained from the sediment, but is taken up by submersed macrophytes most abundantly from the open water (Barko, 1982; Huebert and Gorham, 1983; Barko et al., 1988). Under some conditions this element may be exchanged by submersed macrophyte roots for ammonium ions in sediment (Barko et al., 1988 ). Calcium is a component of the carbonate system and plays an important role in photosynthetic bicarbonate utilization (LSwenhaupt, 1956; Smart and Barko, 1986). We concentrate here on phosphorus (P) and nitrogen (N) because these elements have the greatest potential for limiting macrophyte production in aquatic systems. A simple empirical model for predicting the relative contribution of sediments and open water to the P economy of submersed macrophytes has been developed by Carignan ( 1982 ). In application, the model predicts that more than 50% of the supply of P to submersed aquatic macrophytes is from sediments where the ratio of dissolved reactive phosphorus ( D R P ) in the sediment interstitial water to DRP in the open water exceeds about 4. Concentrations of soluble P in the surface waters of lacustrine systems supporting submersed aquatic macrophytes rarely exceed 10/2g l- 1 ( e.g. Patterson and Brown, 1979 ). Indeed, concentrations approaching about 20 #g l- 1 can cause the exclusion of submersed macrophytes as a result of light attenuation associated with stimulated algal growth (e.g. Jupp and Spence, 1977; Phillips et al., 1978; Sand-Jensen and Sondergaard, 198 l; Twilley et al., 1985 ). From Carignan's model, it is apparent that at 10/~g l- ~ DRP in the open water, as little as 40 jig l- 1 DRP in sediment would provide approximately half the P supplied to submersed aquatic macrophytes. In evaluating submersed macrophyte growth in relation to specific properties of compositionally diverse sediments, Barko and Smart ( 1986 ) reported DRP concentrations in the sediment interstitial water ranging from 40 to more than 9000 jig l- l, with an overall average of 1150 j~g 1- i. These results, in combination with predictions of Carignan's model, suggest that P acquired from most sediments probably accounts for much more than 50% of total P uptake by rooted submersed macrophytes. Results of in situ investigations conducted in a mesotrophic region of Lake Memphremagog indicated that the contribution of P from sediments to rooted submersed macrophytes can approach 100% (Carignan and Kalff, 1980). Chambers et al. ( 1989 ) recently reported that submersed macrophytes growing in rivers, even on infertile, coarse-textured sediments, obtained more than 70% of required P from the sediment. In laboratory studies, production of submersed macrophyte biomass in excess of 1 kg dry mass m -2 has been achieved routinely on sediments with no P in solution (Smart and Barko, 1985). Owing to the large exchangeable pool of P in most lake sediments (Carignan and Flett, 1981 ), it is unlikely that submersed macrophytes are often

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limited in their growth by P availability. Indeed, attempts to stimulate submersed macrophyte growth in situ by P addition to sediment (e.g. Anderson and Kalff, 1986; Moeller et al., 1988 ), or to retard growth by reducing sediment P availability (Messner and Narf, 1987), have been unsuccessful. This generalization, however, may not apply to extremely infertile sediments. For example, the growth ofLittorella uniflora (L.) Aschers. on sand in the oligotrophic Lake Hampen, Denmark, was limited by the availability of sediment P (Christiansen et al., 1985). The degree of attention paid to the P economy of submersed aquatic macrophytes reflects the unparalleled importance of this nutrient in the eutrophication of lacustrine systems (Schindler, 1974, 1977). Given the demonstrated capacity of these plants to take up P directly from sediments, vegetation of the littoral zone needs to be viewed as a potential source of this nutrient to other components of the aquatic environment (Barko and Smart, 1980; Carignan and Kalff, 1980; Smith and Adams, 1986; Moeller and Wetzel, 1988). Information on the relative contributions of sediment and open water to the N economy of submersed macrophytes is quite limited in comparison with that available for P. However, a few experiments incorporating use of the ~SN isotope have demonstrated that this element can be supplied to submersed macrophytes readily from both the sediment and the open water (Nichols and Keeney, 1976a; Short and McRoy, 1984). These experiments indicated collectively that uptake rates were proportional to N concentration in respective sediment or open water media, and that the studied macrophyte species preferred ammonium over nitrate as the form of N. As the concentration of ammonium-N in sediment is usually much greater than in the open water of lacustrine systems (e.g. Nichols and Keeney, 1976b), sediment appears to provide the major source for N uptake by rooted submersed macrophytes. However, this generalization may not apply to enriched riverine systems, such as the Potomac River, where ammonium-N concentrations routinely exceed 100/~g 1-~ in macrophyte beds (Carter et al., 1987). In any event, it is clear, based on laboratory studies, that submersed macrophytes can satisfy their N requirements over at least the short term by uptake exclusively from sediments (Barko and Smart, 1981; Huebert and Gorham, 1983). In contrast to results of in situ P fertilization experiments, yielding little or no effects (see above), fertilization of sediment by addition of N alone or in combination with other elements has significantly increased the growth of submersed macrophytes both in freshwater (Anderson and Kalff, 1986; Duarte and Kalff, 1988; Moeller et al., 1988 ) and marine systems (Orth, 1977; Bulthuis and Woelkerling, 1981 ). These results suggest that the availability of N in sediments may under some circumstances limit the growth of submersed macrophytes. Based on studies of ammonium availability and eelgrass growth, Dennison et al. (1987) suggest that concentrations of ammonium-N at levels less than about 140 pg 1- ~ in the sediment interstitial water

SED1MENT-MACROPHYTE INTERACTIONS AND COMMUNITY DYNAMICS

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may result in N-limited growth. This value seems reasonable, but does not account for differences in site-specific N turnover rates (see Carignan, 1985 ) that may affect N availability. Pools of ammonium-N in sediment interstitial water appear to be buffered by smaller exchangeable pools than for P (Carignan, 1985; Chen and Barko, 1988; Barko et al., 1988). Thus, N is depleted from sediments much more rapidly than P (see below), and is more likely than P to limit production of submersed macrophytes. EFFECTS OF SEDIMENT FERTILITY ON MACROPHYTE GROWTH

In recent laboratory investigations, Barko and Smart ( 1986 ) demonstrated relatively poor growth of Hydrilla verticillata (L.f.) Royle and Myriophyllum spicatum L. on highly organic sediments and on sands compared with growth on fine-textured inorganic sediments. The growth of these species decreased almost linearly with increasing sediment organic matter up to a concentration of about 20% (Fig. 1 ). From fertilization experiments, they concluded that macrophyte growth limitation on sands and organic sediments resulted from nutrient deficiencies. As organic matter and sand (i.e. coarse-textured sediment) have opposing influences on sediment density, their effects on macrophyte growth can be generalized as a function of sediment density (Fig. 2). Sands possess high bulk density and low nutrient availability. However, the actual fertility of sands may vary considerably in nature with groundwater nutrient inputs to the root zone (Fortner and White, 1988; Lodge et al., 1988 ). Organic sediments possess low bulk density, and their nutrient content (commonly considered to be high) is actually quite low on the basis of sediment volume (DeLaune et al., 1979; Barko and Smart, 1986). Nutrient uptake by rooted submersed macrophytes growing on low-density organic sediments is potentially hindered by the long distances over which nutrients must diffuse (Barko and Smart, 1986 ). In addition, nutrient availability in these sediments can be limited by com-

O nO

=

SEDIMENT

ORGANIC

MATTER

Fig. 1. Idealized relationship between submersed macrophyte growth and the organic matter content of fine-textured sediment (after Barko and Smart, 1986). Growth decreases with increasing organic matter content up to about 20%.

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SEDIMENT DENSITY

Fig. 2. Idealizedrelationshipbetweensubmersedmacrophytegrowthand sedimentdensity (after Barko and Smart, 1986). Density increaseup to about 0.9 g ml-t reflectsdecreasingsediment organic matter content. Densityincreasebeyondthis value reflectsincreasingsedimenttexture. Macrophyte growth is maximal on fine-textured sediments with density rangingbetween approximately 0.8 and approximately 1.0 g ml-~. plexation with organic matter (Wali et al., 1972; Sikora and Keeney, 1983 ). Macrophyte nutrition on highly organic sediments may also be disrupted by the presence of phytotoxic compounds produced during anaerobic decomposition (e.g. Drew and Lynch, 1980). Additions of labile organic matter at low levels to sediments, for example from the precipitation of algal detritus (Moeller et al., 1988 ), may provide nutritional benefits to submersed macrophytes, particularly on coarse-textured sediments in oligotrophic systems (Sand-Jensen and Sondergaard, 1979; Ki~rboe, 1980). However, the accumulation in sediments of large amounts of refractory organic matter, with potential inhibitory properties (Barko and Smart, 1983 ), can generally be expected to diminish sediment nutrient availability and associated growth of rooted submersed macrophytes. During the aging of lakes, an increasing proportion of sediment organic matter derives from emergent vegetation (Godshalk and Wetzel, 1978; Godshalk and Barko, 1985 ) and is refractory to decomposition. Consequences of this aging process can result in dramatic changes in the species composition of littoral macrophyte communities (see Section "Littoral Community Dynamics" ). ADJUSTMENTS IN MACROPHYTEROOT:SHOOT RATIO Aquatic macrophytes can adapt to gradients in sediment fertility through adjustments in the ratio of root:shoot (R:S) biomass (Fig. 3 ). By 'root biomass' we refer to all below-sediment plant structures. Numerous instances of increased R: S biomass in submersed macrophytes have been reported in response to sediment infertility (e.g. Denny, 1972; Sand-Jensen and Sondergaard, 1979; Barko and Smart, 1986; Barko et al., 1988 ). A high ratio of R: S biomass is characteristically associated with plants growing in infertile environments (Aung, 1974). Conversely, plants tend to maximize shoot production under fertile conditions. Root growth in Myriophyllum spicatum has been reported to increase linearly with decreasing concentrations of N and P

SEDIMENT-MACROPHYTE

INTERACTIONS

AND COMMUNITY

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o IIx I--

oo "r O IO O Ix P

SEDIMENT FERTILITY

Fig. 3. Idealizedrelationshipbetweenmacrophyteroot: shoot ratio and sedimentfertility. This relationship appliesto all life forms of rooted aquatic macrophytes,and is basedon information obtained from a variety of sources (see text). in the root zone (Mantai and Newton, 1982 ). On sediments of low fertility, relatively great root biomass undoubtedly aids in macrophyte nutrition by increasing the absorptive surface area exposed to sediment. In addition, the greater anatomical complexity of most species exhibiting a high R: S ratio (Sculthorpe, 1967) facilitates nutrient translocation and retention. These conservative characteristics and, in addition, low rates of biomass turnover function in concert with a high R: S ratio in adapting submersed macrophytes to infertile environments (Rich et al., 1971; Moeller, 1975, 1978; Sand-Jensen and Sondergaard, 1979 ). The R:S ratio can perhaps be a useful indicator of relative nutritional stress, but it is important to recognize that broad variations in this ratio occur among different macrophyte taxa (Sculthorpe, 1967; Westlake, 1982). In general, emergent and floating-leaved aquatic macrophytes exhibit R: S ratios that are much greater than those for submersed macrophytes. However, among submersed macrophytes, certain species can exhibit exceptionally high R:S ratios (in excess of 1.0) in infertile environments (e.g. Sand-Jensen and Sondergaard, 1979). Aquatic macrophytes, including emergent and floatingleaved species, with characteristically high R:S ratios appear to be less affected by unfavorable sediment properties than species with low R:S ratios (Sculthorpe, 1967; Sand-Jensen and Sondergaard, 1979; Barko and Smart, 1983). From rather few studies (Denny, 1972; Barko and Smart, 1981, 1986), it is apparent that there are great variations in the ability of submersed macrophytes to modify their R: S ratio in response to sediment fertility. It has been suggested that variations in R: S flexibility may influence macrophyte response to spatial and temporal gradients in sediment composition (Barko and Smart, 1986). This aspect of the ecology of submersed aquatic macrophytes needs greater investigative attention because of its potential bearing on com-

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petitive interactions and associated changes in macrophyte community composition. LITTORAL NUTRIENT DYNAMICS

Effects of macrophytes Given the significance of sediment in supplying N, P, and possibly other nutrients to submersed macrophytes, it is important to evaluate the effects of macrophyte growth on sediment nutrient availability. The capacity of some submersed macrophyte species (isoetids) to form chemical precipitates through direct oxidation of sediment has been demonstrated by Tessenow and Baynes ( 1975, 1978 ). By elevating sediment redox potential, submersed macrophytes under some conditions are capable of reducing concentrations of soluble P in the sediment interstitial water (Jaynes and Carpenter, 1986). The clearest evidence and most dramatic examples of sediment oxidation (redox increase) by submersed macrophytes derive from studies conducted in oligotrophic lakes (e.g. Wium-Andersen and Andersen, 1972; Jaynes and Carpenter, 1986). In contrast, the redox status of fertile sediments from eutrophic lakes may not respond to oxygen released by submersed macrophytes (Carpenter et al., 1983; Chen and Barko, 1988). Oxygen release rates appear to be remarkably similar across a broad range of submersed macrophyte taxa, and there is currently no evidence that species of oligotrophic lakes have greater rates of oxygen release (per unit root mass) than those of eutrophic lakes (Sand-Jensen et al., 1982; Carpenter et al., 1983; Sorrell and Dromgoole, 1987). Thus, the failure of submersed macrophytes to effectively elevate the redox potential of fertile sediments may be due to high rates of reductant generation. In addition, the ratio of root mass to shoot mass, with possible effects on relationships between root surface and sediment volume, may also influence the ability of aquatic macrophytes to modify sediment redox profiles (Chen and Barko, 1988 ). As noted above, the R: S ratio of isoetid species, common to oligotrophic lakes, is quite high among submersed macrophyte taxa. This may contribute to their sediment-oxidizing potential. Evidence from field studies is accumulating to suggest that rooted submersed macrophytes, even with relatively diminutive root systems, are capable of markedly depleting pools of N and P in sediments (Prentki, 1979; Short, 1983; Trisal and Kaul, 1983; Carignan, 1985). By way of confirmation, recent laboratory studies have demonstrated > 90% and > 30% reductions in concentrations of exchangeable N and extractable P, respectively, from sediment over two 6-week periods of growth ofHydrilla verticillata (Barko et al., 1988). As this species is essentially unable to elevate sediment redox poten-

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tial (Chen and Barko, 1988 ), nutrient uptake alone appears to account for its effect on sediment nutrient status. As emphasized earlier in this text, under most circumstances, rooted submersed macrophytes rely on sediment for major portions of their N and P economies. Thus, even in fertile systems where effects of submersed macrophytes on sediment redox status are probably minimal, depletion of sediment nutrient pools resulting from aquatic macrophyte uptake may significantly reduce sediment nutrient availability. High productivity and biomass turnover of aquatic macrophytes in fertile systems contribute to high rates of nutrient loss from sediments (Smith and Adams, 1986). Given the potential significance of sediment nutrient depletion to littoral community dynamics (see below), processes possibly balancing these deficits need to be examined in detail.

Effects of sedimentation Sedimentation provides an important means of nutrient renewal to the littoral zone, and to a large extent may balance nutrient losses due to macrophyte uptake. Factors affecting sedimentation have been studied extensively in the open water (e.g. Hakanson, 1977; Kamp-Nielson and Hargrave, 1978 ), but to a much lesser extent in the littoral zone of lakes. Aquatic macrophyte beds serve as effective traps for inflowing dissolved and particulate materials (Wetzel, 1979; Patterson and Brown, 1979; Carpenter, 1981 ). Moeller and Wetzel (1988) recently suggested that sedimentation of algae from macrophyte leaf surfaces may provide an important link for transfer of nutrients absorbed from the water (by algae) to the sediment surface. Similarly, it has been reported that under conditions of nutrient enrichment, decomposing filamentous algae can provide major inputs of N and P to sediment (HowardWilliams, 1981 ). By reducing turbulence, aquatic macrophytes also serve an important role in sediment stabilization (Madsen and Warncke, 1983 ). Sedimentation rates in the littoral zone have been shown to be about two times greater than rates of sedimentation in the adjacent erosional zone of a reservoir (James and Barko, 1988; 1990). In contrast with the opinion that physical disturbance in erosional zones directly limits submersed macrophyte development (e.g. Spence, 1982 ), Duarte and Kalff ( 1988 ) have recently suggested that erosion of fine-textured particles and associated nutrients may limit macrophyte growth by promoting nutritional deficiencies. Greater sedimentation with less erosion in gently sloped, rather than sharply sloped, littoral regions may account for the relationship established between littoral slope and the biomass of submersed macrophyte communities (Duarte and Kalff, 1986 ). Some submersed macrophyte species, e.g. the marine Phyllospadixspp., are able to adapt

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to the nutritional stress associated with existence in an erosional environment by specific anatomical modifications of roots (Cooper and McRoy, 1988 ). The composition of sediment delivered to the littoral zone has an important influence on aquatic macrophyte growth. Sedimentation of refractory organic matter, from either internal or external sources, can have significant negative effects on the nutrition of rooted submersed macrophytes (see above ). For example, declining populations of submersed macrophytes have been reported following major loadings of refractory organic matter (Kight, 1980; cf. Barko, 1982). Conversely, it has been suggested that the growth of submersed macrophytes may be stimulated by increased sediment fertility due to sedimentation of fine-textured inorganic materials (Barko and Smart, 1986 ). In general, it appears that rooted submersed macrophytes are replaced in lakes by nutritionally more conservative floating-leaved and emergent species as sediment organic matter accumulates (Walker, 1972; Wetzel, 1979; Carpenter, 1981, 1983). Pearsall (1920) observed that effects of organic matter accumulation on macrophyte species composition could be reversed by wave action or sedimentation of inorganic materials. We suggest that such reversions may be mediated, at least in part, by changes in sediment fertility.

Effects of sediment bioturbation Activities of benthic invertebrates can significantly influence physical and chemical properties of sediment, thereby potentially affecting the availability of nutrients to aquatic macrophytes. Bioturbation by chironomid larvae transports P to overlying waters at significant rates in shallow ecosystems (Gallepp, 1979 ). Fukuhara and Sakamoto ( 1987 ) quantitatively assessed effects of chironomid larvae as well as tubificid worms on release of nutrients from sediment. Increasing densities of either of these organisms appear to have pronounced influences on release rates of both N and P from sediments. Case construction and tube irrigation activities of chironomids accelerate nutrient transport within sediment by increasing the area of the sediment-water interface, horizontal and vertical diffusional fluxes of nutrients within sediment, and sediment porosity. Vertical mixing of sediment by tubificid worms (McCall and Fisher, 1980) continuously increases levels of nutrients in the sediment interstitial water (Fukuhara and Sakamoto, 1987). As depicted in Fig. 4, the activity oftubificid worms, in concert with microbial and chemical processes, causes the release of soluble nutrients from particulate phases in the sediment. Dissolved nutrients may then diffuse to the sediment surface, or in the presence of rooted macrophytes, be taken up by roots. In addition, these worms effect a directional reworking of sediment particles that produces deposition of material at the sediment surface and an orderly vertical mixing of the upper 5-10 cm of sediment. These physical effects by both groups of invertebrates can result in vertical transport of recently deposited

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•~ ?o ".' "" • ~ "o Zt) O~0 • 0" "P " ~ ' : ' " •99

¢ ;;,,,ou.ION

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Fig. 4. Conceptual model of the effect of tubificid sediment mixing on inorganic substances released to solutionby chemicaland microbialprocesses (after McCall and Fisher, 1980). Other benthic invertebrates influenceprofiles of inorganicconstituents in sediment interstitial waters through different mechanisms (see text). materials to depth in the sediment (Krantzberg, 1985 ). Sediment reworking by benthic invertebrates in the littoral zone may be important in intermixing newly accreted sediment in the root zone of aquatic macrophytes. Benthic invertebrates can also increase the redox potential of surface sediment by circulating oxygen-rich water into the sediment (Hargrave, 1972; Davis, 1974; Fukuhara and Sakamoto, 1987 ). Redox potential is a major factor controlling availability of many nutrients in sediments; thus the extension of oxidizing conditions to deeper levels in sediment may serve to decrease nutrient availability (Jaynes and Carpenter, 1986). As ammonium-oxidizing bacteria require the simultaneous presence of both a m m o n i u m and dissolved oxygen, the potential exists for populations of these bacteria to develop along burrow walls and in upper pelletized layers, resulting in increased rates of a m m o n i u m oxidation to nitrite and nitrate. The latter forms of N are less favored than a m m o n i u m for uptake by aquatic macrophytes (Nichols and Keeney, 1976a). In addition, nitrate can diffuse back into nearby anaerobic zones where denitrifying bacteria may reduce nitrate to nitrogen gas, resulting in loss of nitrogen from the sediment (Reddy and Patrick, 1984). The net

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J.W. BARKO ETAL.

effect of these processes on nutrient availability to aquatic macrophytes has not been evaluated.

Effects of decomposition In situations where nutrient replenishment through sedimentation is minimal, other mechanisms of nutrient renewal may be required to sustain high levels of macrophyte productivity. An alternative source of nutrient supply in the littoral zone is the decomposition of materials sloughed by actively growing aquatic macrophytes. The potential significance of this process is perhaps best illustrated by tropical rain forests, where rapid decompositional processes continually release nutrients from dead plant tissues (Whittaker, 1970). These nutrients are then readsorbed almost immediately by adjacent living plants. The same processes are probably important, particularly in oligotrophic environments, where nutrient conservation is critical to sustain macrophyte productivity. It has been suggested that under conditions of nutrient (N) limitation, the rate of nutrient (N) renewal from macrophyte-derived sedimentary organic matter during decomposition may be a good predictor of macrophyte growth (Carignan, 1985 ). Aerobic decomposition predominates in the water column and at the surface of many sediments, converting available organic matter to its primary constituents. Several studies have shown that anaerobic decay proceeds at slower rates than aerobic decay (Mills and Alexander, 1974; Reddy and Patrick, 1975; Godshalk and Wetzel, 1978). In addition, anaerobic decomposition generally does not proceed to completion owing to the lack of oxidizing power and adequate levels of alternate electron acceptors (nitrate, oxidized forms of iron and manganese, sulfate) to fuel the process. Fermentation pathways, which prevail beneath the sediment surface, result in accumulation of reduced organic compounds (primarily fatty organic acids and alcohols) and other compounds that are decomposed poorly, if at all (lignins, tannins, and, to a lesser extent, phenolics). While some of these compounds may be utilized by sediment biota, others may be inhibitory or toxic to aquatic macrophytes. During decomposition a variety of biogeochemical pathways act on decomposing organic matter to form complex substances of a lignin-like nature (Crawford, 1981; Godshalk and Barko, 1985 ). As this occurs, the ability of decomposition to contribute to sediment nutrient pools becomes insignificant. Particularly under anaerobic conditions, the accumulation of large quantities of refractory organic matter can be expected to diminish overall sediment nutrient availability (Barko and Smart, 1986; and see above). The nature of the plant substrate is important in determining decomposition rate. Plant composition varies widely among species. Tissues of algae and aquatic macrophytes are generally flaccid and pithy. As succession proceeds and the littoral zone becomes more terrestrial in nature, the colonizing

SEDIMENT-MACROPHYTE INTERACTIONS AND COMMUNITY DYNAMICS

•

~

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~

53

WEIGHT OF

PLANTMATERIAL ~

~NUMBERS

OF

LENGTH OF DECOMPOSITION

Fig. 5. Generalizeddescription of changes in weightof vegetation and abundance of microorganisms during decompositionof submersedaquatic plants (after Godshalk and Barko, 1985). This description applies to the decompositionof all vegetation having significantcontents of celluloseand lignin,and is based on informationobtained from a varietyof sources (see text). emergent and terrestrial plant species have significant levels of cellulose and lignin, tough vascular tissues, and protective outer layers (Godshalk and Wetzel, 1978; Danell and Sj6berg, 1979). Plant tissues having a high N content decompose quickly, releasing N to the environment (Carpenter and Adams, 1979; Carpenter, 1980). In contrast, tissues with low N levels (high carbon:nitrogen ratios) lose readily soluble (non cell wall) N at the beginning of decomposition, then may accumulate N for a prolonged period, and finally lose N again when only the most resistant materials remain (Kaushik and Hynes, 1971; Sardana and Mehrotra, 1981; Tiwari and Mishra, 1983 ). The stages of macrophyte decomposition are fairly predictable. Decay is first initiated by the liberation of soluble materials. Released substances apparently consist of intracellular cytoplasmic compounds, containing labile organic substances (sugars, fatty acids, amino acids), N, P, and cations (sodium (Na), potassium (K), calcium (Ca), and magnesium (Mg)). Leaching and autolysis are responsible for rapid, quantitatively significant losses of N, P, and K from plant tissues (Howard-Williams and Howard-Williams, 1978; Howard-Williams and Davies, 1979). Others have suggested that autolysis preceding actual tissue death may promote leaching of cellular constituents from aquatic macrophytes (Golterman, 1973; Otsuki and Wetzel, 1974). Leaching of materials from fresh detritus may explain the rapid decrease in weight (more than one-third ) often observed during initial decomposition of detritus (Petersen and Cummins, 1974; Carpenter, 1980; Polunin, 1982; Esteves and Barbieri, 1983), while later weight loss is associated with decomposition of more resistant organic materials, such as cellulose and lignin (Fig. 5).

Effects of rhizosphere microflora Microorganisms play a major role in nutrient cycling and energy transfer in the open water of aquatic ecosystems. However, sediment microorganisms

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have received much less attention (Duarte et al., 1988). Interactions in the rhizosphere between microorganisms and the roots of submersed aquatic macrophytes, while not examined extensively beyond the context of decomposition, appear to be important in the nutrition of these plants (Gunnison and Barko, 1989). Many nutrient transformations, fueled by decompositional processes, are carried out by microorganisms that reach high population levels only in the rhizosphere. Durako and Moffler ( 1987 ) have suggested that microflora-plant root relationships may be obligatory to the nutrition (particularly N) of aquatic macrophytes. Others have suggested that increased bacterial abundance in areas of increased macrophyte biomass may increase the volume of nutrient recycling (Duarte et al., 1988 ). Nitrogen fixation occurs within the rhizosphere of a variety of submersed marine macrophytes (Smith and Hayasaka, 1982a,b; Schmidt and Hayasaka, 1985 ). Other studies have indicated that deamination of amino acids carried out by rhizoplane microflora may provide a major source of ammonium for these plants (Smith et al., 1984; Boon et al., 1986). In the rhizosphere of the submersed freshwater macrophyte, Myriophyllum heterophyllum Michx., Blotnick et al. ( 1980 ) identified the occurrence of a variety of microbial processes of significance to macrophyte nutrition; these included ammonification, denitrification, nitrogen fixation, and acid production, important in the liberation of metals and phosphate from minerals. While bacteria in the rhizosphere of submersed macrophytes have been examined most extensively (see references cited above), fungi in the rhizosphere also contribute to macrophyte nutrition (Gunnison and Barko, 1989 ). These organisms attach themselves to the root surface, extending and increasing root surface area and nutrient uptake capabilities. Fungi as well as bacteria increase the availability of sediment-bound nutrients through their metabolic activities (e.g. Craven and Hayasaka, 1982 ). Mycorrhizal fungi are able to improve substratum physical stability through the development of an extensive mycelium growing outwards from the roots. Some aquatic macrophytes lack mycorrhizae (Khan, 1974), while others demonstrate slight to extensive mycorrhizal associations (Sondergaard and Laegaard, 1977; Bagyaraj et al., 1979; Chaubal et al., 1982; Clayton and Bagyaraj, 1984). The species of plant and the sediment environment are important in determining the community composition and population levels of microorganisms present in the rhizosphere (Alexander, 1977; Gunnison and Barko, 1989). Through their role in decomposition and nutrient cycling, microorganisms make available in sediments a variety of elements important to the nutrition of submersed aquatic macrophytes. Among these, N and P are highly significant as major growth-limiting factors in the aquatic environment. Chemical reduction of sediment through microbial metabolism is an important condition for plant growth, permitting accumulation of certain nutrients to levels beneficial for growth of submersed macrophytes. Ammonium-N can be pro-

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duced under aerobic as well as anaerobic conditions. However, accumulation under aerobic conditions is restricted because of the ammonium-consuming activity of ammonium-oxidizing bacteria. Orthophosphate-P production can occur also under both aerobic and anaerobic conditions. However, accumulation under aerobic conditions is restricted because ferric oxyhydroxides, produced by rapid chemical oxidation of reduced iron in the presence of oxygen, rapidly sorb phosphates. Thus, submersed aquatic macrophytes, actively taking up ammonium-N and orthophosphate-P, must either grow in reduced sediments or in an oxidized zone intimately surrounded by reduced sediments. LITTORAL COMMUNITY DYNAMICS

Ecosystem interactions Major linkages between aquatic macrophytes and sediments include both positive and negative feedbacks (Fig. 6). One well-described positive feedback involves acceleration of P cycling by submersed macrophytes (Carpenter, 1981 ). Nutrients taken up by roots and translocated to shoots are released rapidly upon seasonal senescence (Carpenter, 1980; and elsewhere in this text), but are not released in appreciable quantities from healthy tissues (e.g.

_•_.,•.•

NUTRIENT POOL

K

~

PHYTOPLANKTON AND ATTACHED ALGAE

Mg CI SO 4

,

I MICRONUTRIENTSI

1

DETRITAL INPUTS

I NUTRIENT POOL

I

I

Fig. 6. Major linkages between aquatic macrophytes and bottom sediments in littoral systems. These linkages apply to all life forms of rooted aquatic macrophytes, and are based on information obtained from a variety of sources (see text).

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Denny, 1980; Barko and Smart, 1980). Among these nutrients, P is perhaps most important because it stimulates production of phytoplankton and attached algae. Recycling increases the amount of organic matter produced per P atom present in the lake and accelerates the rate of sediment accumulation (Carpenter, 1981 ). Both senescent macrophyte shoots and algal remains are eventually added to the sediments. As these materials are relatively labile, they constitute important vehicles in littoral nutrient cycling. Considering the relatively greater availability of P compared with N in most sediments, the littoral zone may serve to decrease the N : P ratio of macrophyte-derived detritus. As a consequence, elemental exchanges are potentially altered in favor of greater P than N export to the open water, possibly influencing phytoplankton community composition (Lodge et al., 1988). Recently recognized feedbacks involving sediment density, oxygen release, and sediment nutrient depletion directly by macrophyte uptake, add to the array of interactions between submersed aquatic macrophytes and sediments (Fig. 6 ). These feedbacks are significant and can have either positive or negative effects on submersed macrophyte growth. In high density (coarse-textured) sediments, addition of macrophyte-derived detritus will decrease sediment density and potentially increase macrophyte growth (Fig. 2 ). However, in low-to-moderate density sediments, addition of macrophyte detritus will decrease sediment density and potentially decrease macrophyte growth (Figs. 1 and 2 ). Sediment oxidation can have positive effects on macrophyte growth by oxidizing reduced toxicants such as sulfide, or by increasing sediment density through enhanced mineralization of organic matter. On the other hand, sediment oxidation and direct uptake of nutrients by roots can reduce sediment nutrient availability, potentially decreasing macrophyte growth (Barko et al., 1988). Effects of submersed aquatic macrophytes on nutrient cycling are most pronounced in shallow lakes that support extensive stands of robust submersed macrophytes, such as the large species of Myriophyllum, Potamogeton, and Elodea. These species have high biomass turnover during the growing season and therefore recycle nutrients when water temperatures are high and potential effects on pelagic plankton production are maximal (Carpenter, 1980, 1983 ). Submersed macrophytes (e.g. isoetids) of oligotrophic systems tend to have low biomass turnover (Moeller, 1978; Sand-Jensen and Sondergaard, 1978; McCreary 1985) and therefore can be expected to have low nutrient recycling rates. Moreover, sediment oxidation by macrophytes in oligotrophic systems may immobilize nutrients (particularly phosphorus) in sediments, further retarding recycling (Jaynes and Carpenter, 1986).

Macrophyte community composition Over geologic time scales, lake basins fill inexorably with particulate material from the watersheds and autochthonous production (Lindeman, 1942;

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Wetzel, 1983 ). Sediment accretion establishes the long-term vector of macrophyte community change. For example, Walker (1972) used paleolimnological data to reconstruct 52 community transitions in hydroseres. Most (83%) of the transitions followed the classic sequence of dominance: phytoplankton -, submersed macrophytes~ floating-leaved macrophytes-,bogs or emergent macrophytes. Increases in water level accounted for all of the transitions that involved reversals of the classic sequence. At finer levels of resolution, patterns of macrophyte community change are much less clear, and at the species level, replacement sequences appear to be particularly variable. Over relatively short time scales of years to decades, numerous processes, many of which are affected by watershed activities, can interrupt or deflect long-term successional trends. Macrophyte-induced modifications in sediment composition may be pivotal in these changes. Early accounts, most notably those of Pond ( 1905 ), Pearsall (1920) and Misra (1938), provided evidence suggesting a connection between macrophyte species associations and physical and chemical properties of sediments. Numerous investigations conducted during recent years in a broad variety of aquatic systems have demonstrated that sediment composition plays a major role in affecting the growth and distribution of submersed aquatic macrophytes (e.g. Moeller, 1975; Schiemer and Prosser, 1976; Sand-Jensen and Sondergaard, 1979; Kiorboe, 1980; Wheeler and Giller, 1982; Chambers and Kalff, 1985; Chambers, 1987; Anderson and Kalff, 1988). Properties of bottom sediment potentially affecting macrophyte growth response are numerous and complex. However, given the importance of sediments in macrophyte nutrition, we suggest that sediment fertility is a key property affecting macrophyte community composition. Effects of sediment fertility on the growth of aquatic macrophytes vary considerably among species. In a classic investigation conducted in ponds, Denny (1972) demonstrated broad variations in the growth rates of several submersed macrophyte species in response to differences in sediment fertility. Much greater growth of all species occurred on mud than on sand, but the ratio of growth rate on mud to growth rate on sand differed among species over about a three-fold range. Denny suggested that variations in responsiveness to sediment type were related to differences in anatomy and morphology of studied species, thereby affecting nutrient accession from sediments. Similar indications of variations in responsiveness of specific aquatic macrophyte taxa to sediment fertility, based on laboratory studies, have been reported by Barko and Smart ( 1980, 1981, 1986). Variations in response among different aquatic macrophyte species to sediment fertility have been most recently demonstrated in investigations of Lake Memphremagog. Decreasing sediment fertility along a natural gradient in this lake was associated with an increase in the proportion of total submersed macrophyte biomass attributable to rosette and bottom-dwelling species, and a

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decrease in the proportion of canopy-forming and erect species (Chambers, 1987). In the same lake, submersed macrophyte species also varied over a broad range in their response to in situ sediment fertilization (Duarte and Kalff, 1988). In efforts to link the growth of aquatic macrophytes (at the community level) with sediment properties, relationships are potentially obfuscated by variations in the response of different species to sediment fertility (Anderson and Kalff, 1988). SYNTHESIS During the past 15 years, studies of submersed macrophyte nutrition have focused almost entirely on sources of nutrient acquisition. The nutrients of greatest importance in the nutritional ecology of these plants are N and P, which are largely sediment-derived. These nutrients are also of greatest interest in lake management as they have important effects on productivity, and ultimately on lacustrine succession. The effects of aquatic macrophytes on N and P cycles, both in the sediment and in the open water, need to be examined more closely, particularly in view of possible interactions with other components of the aquatic ecosystem. It is now apparent that sediment physical and chemical properties are as much a product of aquatic macrophyte growth as they are delimiters of macrophyte growth. A complex variety of processes regulate littoral nutrient dynamics, and these bear directly on submersed macrophyte productivity. Sedimentation, sediment bioturbation, and microbial activity in sediments have been studied extensively, but only to a limited extent within the context of aquatic macrophyte nutrition. These processes appear to act in concert in renewing nutrient supplies to rooted macrophytes in littoral sediments. The sustained vigor of submersed macrophyte communities depends on, among other factors, the balance between nutrient losses, gains, and overall availability to macrophytes in littoral sediments. Changes in this balance affected by watershed disturbance or other h u m a n interventions need to be evaluated in terms of effects on macrophyte productivity and species composition. Over geological time, the vector of vegetative change in lacustrine ecosystems is clear. However, many important scientific and management questions are more relevant to shorter time scales. Invasions of nuisance macrophytes, for example, often have cycles of a decade or so. Compositional changes in aquatic macrophyte communities over short time intervals remain largely unexplained. Macrophyte-sediment interactions at the community level appear to be both powerful and complex. Thus, a better understanding of these interactions should be useful in explaining short-term compositional changes, including species invasions and declines. Particular attention should be given to macrophyte-sediment interactions in weighing the relative influences of resource-based interspecific competition and habitat variability on

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macrophyte c o m m u n i t y composition. Analysis o f the effects o f interactions between rooted submersed macrophytes and sediment properties on littoral c o m m u n i t y dynamics offers a major frontier and opportunity for future research. Resource-based competition theory has been developed for terrestrial vegetation (Tilman, 1982 ) and appears to be directly applicable to aquatic macrophyte communities. Nutrient-based competition is an experimentally testable mechanism o f compositional change in macrophyte communities. Aquatic macrophyte communities m a y be superior to terrestrial communities as test systems because the fluctuations in soil moisture that have powerful interactions with nutrients in terrestrial systems are absent in submersed macrophyte communities. While a wide array of potentially limiting nutrients needs to be examined in terrestrial systems, we suggest that greatest attention be focused on N in aquatic systems. ACKNOWLEDGMENTS We thank T h o m a s L. Hart, Dwilette G. McFarland, and William D. Taylor of the Environmental Laboratory, Waterways Experiment Station and Nancy J. McCreary of Lafayette College for their reviews and other suggestions leading to improvements in this article. Financial support was provided by the U.S. Army Corps of Engineers Aquatic Plant Control Research Program. Permission to publish this article was granted by the Chief of Engineers.

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