2. PHYSICAL, CHEMICAL, AND BIOLOGICAL FACTORS AFFECTING SUBMERSED PLANT GROWTH

Among the submersed vascular plants, there is great variation in life cycle, morphology, physiology, and reproduction which somewhat reflects the diversity of their terrestrial ancestors (Arber, 1920). This diversity is illustrated by the wide range of physical and chemical conditions to which various species are adapted. The species composition and abundance in a submersed plant community will depend upon the totality of these factors to which an area is subjected. The purpose of this section is to provide an overview of the importance of factors other than light which may limit the abundance, or even the occurrence, of aquatic vascular plants. While the discussion focuses on the submersed life forms, many of the factors mentioned also relate to emergent and floating leaved species.

2.1 FLUCTUATING WATER LEVELS

Fluctuating water levels are common features in many shallow aquatic ecosystems. The distribution of wetland plants in response to a drop and subsequent rise in water level in a prairie pothole marsh is illustrated in a study by van der Valk and Davis (1976). The submerged zone was completely exposed during a summer drought which almost eliminated Ceratophyllum demersum when reflooding occurred the following year. Another submersed species, Potamogeton sp. aff. pusillus, was little affected but moved 4 or 5 m closer to shore after reflooding. There was a tendency during the drought for emergent species to germinate and invade the submersed zone such that biomass and species richness of the zone increased after reflooding. This illustrates that although some submersed species are severely affected by extreme water level fluctuation (e.g., Ceratophyllum, which is not rooted), others adapt by a shift in zonation. However, considering the community as a whole, irrespective of life form, there was little overall change in community production and diversity due to water level fluctuation.

Where drawdown can be artificially controlled it is commonly used in control procedures for aquatic macrophytes. Peltier and Welch (1970) suggested that drawdown, along with low rainfall, resulted in greatly increased coverage by Najas spp. in an Alabama reservoir. Similarly, Jackson and Starret (1959) note that Potamogeton pectinatus grew best when water levels remained low in the shallow, floodplain of Lake Chataqua, Illinois. In the Chippewa Flowage, Wisconsin, which has received repeated winter drawdowns for 50 years, Nichols (1975) identified five submersed species that either recovered, or increased in coverage after repeated water fluctuation. On the other hand, if drawdowns are not properly conducted, problems resulting from excessive macrophyte growth may result especially in areas with long growing seasons, as predicted by Hestand et al. (1973) for Lake Ocklawaha, Florida.

Where drawdowns persist for several years or are frequent during a single growing season, as in some reservoirs, submersed vascular plants will not survive. Reservoirs typically have highly turbid waters and few shallow areas which further reduces chances for establishment of submersed vegetation. Controlled drawdowns have been used in the TVA reservoir system for management of Myriophyllum spicatum, a nuisance plant (Leon Bates, personal communication).

Submersed species may be limited in their length of growth by shallow water, but it is uncertain whether this would affect rates of production. For example, Lind and Cottam (1969) found that Myriophyllum exalbescens, in Lake Mendota, Wisconsin, was about half as dense at .0 to .5 m depth as at 1 m, but the average weight per plant was about twice as great in the deeper water. Whether Myriophyllum would respond to increasing water depths during a single growing season by elongation and reduction in density is uncertain. Alternatively, reduced depths may result in greater fragmentation and uprooting from turbulence as more of the plant floats near the surface.Martin and Uhler (1939) stated that at least a few inches of water must be retained for truly aquatic plants to remain established. Of the species that they suggested for propagation in periodically exposed wetlands, none are submersed aquatics. None of the seeds of aquatic plants mentioned by Sculthorpe (1967) that require drying before germination were from submersed species.

2.2 CURRENTS AND WAVES

In medium to large lakes the eroding forces of waves may prevent the establishment or result in the fragmentation of submersed aquatic plants in the shallowest zone. Their absence is probably more commonly due to the abrasive action of waves rather than instability of the substrates. In mature basins, the amount of erodable inorganic material in this high energy zone is usually small, having long since been removed (Kutchinson, 1975). There is a tendency for submersed vascular plants that grow in these situations to be small and their occurrence probably depends on resistance to fragmentation.

Fragmentation due to wave action was determined by Jupp and Spence (1977b) for Potamogeton filiformis in Loch Leven, Scotland. By comparing peak biomass of plots protected from wave action and waterfowl grazing (243 g/sq m ) with plots protected only from waterfowl grazing (125 g/sq m ), a loss of 118 g/sq m was attributable to wave action. Since plant densities did not differ significantly between treatments, all of this loss was due to wave pruning of shoots. It is uncertain, however, to what extent fragmentation calculated by this procedure actively occurred and to what degree wave action may have merely inhibited potential growth.

In running waters only rooted growth forms become established and thus they are restricted to areas of sediment deposition, with the notable exception of members of the mostly tropical Podostemaceae which are attached to rocks in fast flowing water (Arber, 1920). Hynes (1970a) stated that no rooted plants show any special adaptation to running water, and the species that occur in streams and rivers have tough, flexible stems or leaves, a creeping growth habit, frequent adventitious roots, and strictly vegetative reproduction.

According to Westlake (personal communication) the relationship between plant distribution, depth, light and compensation point are complex, particularly in the relatively shallow depths colonized in fairly turbid river waters. In these conditions many plants are capable of growing from the bottom and creating a leaf array containing most of their biomass near the illuminated surface. Such stands are ultimately limited in biomass partly by turbidity, but mainly by self-shading. Their depth limits, as defined by the deepest water in which they are rooted, are probably fixed by their capacity to grow from reserves, out of the dark bottom waters and into the light before other plants shade them. Size of storage organs is therefore important. These principles apply also to still water conditions.

In many flowing water situations, the occurrence of spates or freshets following heavy rains severely limits the abundance of submersed species due to strong currents. For example, Bilby (1977) quantified the effects of macrophyte distribution in a stream pool before and after a spate resulting from a large rainstorm in New York. The two dominant species, Elodea canadensis and Potamogeton crispus underwent a pattern of displacement toward lower current speeds following the spate. Most of the reduction in macrophyte cover was where current speeds were highest.

Where current movement is slow as in irrigation canals, submersed plants may become exceedingly abundant, as in south Florida (Blackburn et a1., 1968). Likewise, the steady flow and transparent waters of Florida spring runs often support high biomass of submersed species, whose year-round productivity is limited by light (Odum, 1956). In these latter two examples water current serves as an important auxiliary energy source by increasing nutrient availability and exporting waste products. Within a range of slow currents for which flow is laminar (0.02 - 0.5 cm/sec), Westlake (1967) demonstrated that photosynthesis of submersed plants in the laboratory increased with increasing current velocity. However, the high velocities that occur during flooding of most streams and rivers would represent stressful and often quite damaging conditions for macrophytes (Haslam, 1978).

2.3 SUSPENDED SEDIMENTS AND THEIR EFFECTS ON SUBMERSED PLANTS

Suspended sediments have effects on submersed macrophytes in addition to those directly related to a reduction in available light. For example, the composition of bottom materials in which plants are rooted depends on the balance between the rate of sediment supply and the rate at which sediments are carried away by currents. Current velocity, particle density, and particle size are mainly responsible for this balance. These variables will be treated briefly prior to discussing the relationship between macrophytes and sediment types.

The settling velocity of particles is classically described by Stokes law which is formalized as

where v is the velocity of the particle (cm/sec), r is its radius (cm), g is acceleration of gravity, n is the viscosity of the fluid (poises), and d1 and d2 are the densities of the particle and fluid (g/sq m ), respectively. If all other conditions are constant, then the settling velocity is directly proportional to the square of the particle radius, and the equation simplifies to where C1 represents the various constants. This law does not hold for large particles because above about 0.1 mm in diameter the settling velocities are proportional to the square root of the radius according to the impact law. The simplified form of the impact law is where various constants are included in C2 . Viscous forces operable in Stokes law become negligible. Thus the settling velocity will follow the experimental curve shown in Figure 1.

Figure 1. Comparison of settling velocities described by Stokes' Law and the impact law. The experimental curve is also shown. From Stratigraphy and Sedimentation, Second Edition, by W.C. Krumbein and L.L. Sloss. W.H. Freeman and Company, Copyright, 1963.

In streams and lakes which have turbulent flow, particles are kept in suspension by kinetic energy that overcomes the gravitational and cohesive forces. The relationship between velocity, particle size and the fate of the particles is shown by the Hjulstrom scheme in Figure 2. This graph incorporates the critical erosion velocity in addition to the settling velocity which brackets the regions in which particles will be eroded, transported, or deposited. This conceptual model is based on a number of assumptions, few of which have much applicability to field situations where the flow velocity is stochastic and particles are seldom spherical, of homogeneous size, or of similar density.

Figure 2. The relationship between current velocity and particle size which determines whether particles will be eroded, transported, or deposited (after Hjulstrom, 1935).

Nevertheless, Figure 2 correctly conveys the concept of segregation of particle size with respect to flow velocity. In considering dredging actvities, fine particles with their slow settling velocities will remain in suspension longer and will tend to be transported greater distances than larger particles. Particles from sediments largely composed of organic matter have lower densities and will have an even greater tendency to remain in suspension. It becomes obvious that the duration of shading and the extinction coefficient of the water will depend greatly on the composition of the material brought into suspension, whether by natural (floods) or by human activity (dredging or other disturbances).

Submersed macrophytes and other structural features may act as sediment traps because of their effectiveness in reducing flow velocity. Growth of rhizomes and roots in the sediment further stabilizes the substratum. The restriction of vascular plant beds to the relatively low energy sectors of streams contributes to the extremely patchy distribution that is often observed.

In highly organic bottoms, such as in open water areas of peat bogs, the soft ooze severely restricts the establishment of aquatic macrophytes. Plant beds are often restricted to species that produce dense and persistent networks of rhizomes, as in the case of members of the Nymphaeceae. Although this family is characterized by floating leaves, some members have submersed 'water leaves' which may persist year round in the southeastern United States (Brinson and Davis, 1976). The importance of these leaves to the carbon balance of the plant has never been established.

Not only must sediments be stable for successful colonization of macrophytes, but the particle size distribution also influences the species that occur. Spence (1964) showed that in Scottish lochs submersed broad leaf forms predominated in water greater than 150 cm deep only when the sediments were composed of fine muds. However, other factors such as light and turbulence all change with depth, so it is not possible to single out substrate type as the most important variable except perhaps by controlled experiments (Pond, 1903; Brown, 1913; Bourn, 1932; Misra, 1938).

Pearsall's (1920) work on the English lakes during the early part of this century singled out the physicochemical nature of the sediment as the main factor in determining composition of the vegetation, although the original interpretation of these results is somewhat questionable (Spence, 1967). Isoetes was restricted to stony areas with thin silt. This genus apparently cannot colonize areas of sediment deposition because it cannot alter its root level. Potamogeton perfoliatus grows in areas with a high clay fraction, which may also be related to nutrient availability, rather than texture alone. However, life forms with a stoloniferous habit are probably able to adjust to changes in sediment depth except in the most extreme cases of accumulation.

Another aspect of siltation is the accumulation of material on leaf surfaces which reduces light transmission to photosynthetic surfaces and possibly alters gas and nutrient exchange. Sculthorpe (1967) suggested that the linear leaves of Potamogeton pectinatus remain free of settling particles and thus the species may colonize areas unsuited for submersed plants with leaf forms more amenable to silt accumulation. Schiemer and Prosser (1976) confirmed that the sediment coating on Myriophyllum spicatum, which has finely divided, feathery leaves, is markedly greater than for P. pectinatus in sheltered bays of Neusiedlersee, Austria. In addition, they suggested that silt deposition is enhanced by the presence of epiphytic algae on heavily infested macrophytes. Increased plant weight due to silt deposition was also noted as having an inhibitory effect on macrophyte growth. These factors in addition to wave action appear to be largely responsible for the distribution of M. spicatum in Neusiedlersee.

2.4 GROWING SEASON AND DORMANCY

Submersed macrophytes may resist the effects of freezing by colonizing depths below the zone of surface ice formation as compared with emergent or floating leaved species that are exposed to freezing temperatures. In spite of this, many temperate submersed species undergo a period of dormancy during the winter and a few species are anatomically and physiologically adapted to overwintering. However, a number of submersed perennials merely subsist with reduced or negligible growth rates and reduced biomass until more favorable light and temperature conditions at the onset of the growing season. Except in cases of a limited number of annuals where viable seed development and favorable conditions for germination must occur, most submersed species are perennial and overwinter by means of vegetative structures.

Weber and Nooden (1976a, b) described the role of turions in the over-wintering of Myriophyllum verticillatum. In this species turions are specialized compact buds that develop from nodes late in the growing season as a response to photoperiod and possibly temperature. These reproductive structures sink to the bottom after detachment from the parent plant. Dormancy is broken by cold temperatures (0 - 4É C) which compares well with observed turion germination before ice breakup.

Apart from highly modified organs such as turions, many other less specialized organs appear equally capable of overwintering. These include dormant apices and offsets, root tubers, stolons, and rhizomes. Dormant apices and offsets as well as turions can be important in plant dispersal. These structures in submersed aquatic plants appear to substitute for seed dispersal more commonly found in emergent or floating leaved species.

In addition to lower water temperatures and reduced day length during the nongrowing season, the presence of an ice and snow cover in northern latitudes poses severe restrictions on light penetration. Species that may have only reduced biomass and growth during the winter season if open water persists will be much reduced in more northern waters that become completely iced in. This may result in regional differences in standing crops of submersed plants at the beginning of the growing season.

The presence of ice may also result in physical disruption of macrophyte communities. Martin and Uhler (1939) described the scouring action of ice masses during spring breakup in flowing waters and shallow lentic habitats that may cause severe damage to beds of submersed plants.

2.5 NUTRIENT AVAILABILITY AND UPTAKE

There has been considerable controversy concerning the importance of roots in nutrient uptake from sediments. It is clear from a number of studies that roots do accumulate nutrients from the sediments and these may be translocated to the shoots. However, in many aquatic plants, significant ion absorption occurs by leaves and there appears to be a great diversity in the relative importance of roots and shoots in mineral nutrition.

Figure 3 illustrates the spectrum of all possible cases for aquatic macrophytes in which the x-axis represents a gradient in life form, root-shoot ratio, or anatomical complexity (Denny, 1972). Emergent species will obtain most of their mineral nutrition from the sediments, while those that have floating leaves are intermediate between emergent and submersed plants.

Figure 3. Schematic diagram of factors that contribute towards a tendency for nutrient adsorption by roots or shoots. Axes are arbitrary. Modified from Denny (1972).

The actual amount of nutrient absorption in field situations may be related also to the relative supply in the water and the sediments. For example, Bole and Allan (1978) demonstrated that Myriophyllum spicatum and Hydrilla verticillata utilized phosphorus from the sediment until concentrations in the water reach a threshold value which differs for the two species. Above these water concentrations uptake from the water column increases. Nutrient availability is not based solely on concentration since flowing waters of low concentration may actually be a better source of nutrients than higher concentrations in quiescent waters. Dense growths of submersed communities often require nitrogen and phosphorus in excess of the amount present in the water at any one time. Sediment texture and cation exchange capacity may also be important in the nutrient supply to roots. Since it has been demonstrated that some aquatic macrophytes translocate phosphorus (Twilley et al., 1977) and nitrogen (Nichols and Keeney, 1976) both from roots to shoots and from shoots to roots, it is unlikely that the sediments or the water alone are the singular source of nutrients.

Although nitrogen and phosphorus are generally believed to be the most important limiting nutrients in fresh waters, there are no clear cut cases where submersed macrophytes are excluded by the paucity of either. Rather it would seem that the rate of productivity may be limited by the supply of these nutrients. However, in the case of soft and hard waters (low and high CaCO3 concentration, respectively) there appears to be an important dichotomy in species distribution. This has been reviewed extensively by Hutchinson (1975) who also noted that pH may play an important role in species distribution in soft waters.

2.6 BIOLOGICAL FACTORS

The absence of submersed aquatic plants in fertile lakes and ponds has often been attributed to shading by dense populations of phytoplankton. Jupp and Spence (1977a) reported an inverse correlation between biomass of Potamogeton filiformis and open water chlorophyll a concentrations at certain times during a three-year study of Loch Leven, Scotland. Scums of blue-green algae accumulating near the shore during Anabaena flos-aquae blooms intensified shading in macrophyte beds. Jupp and Spence suggested that these algal blooms, apparently enhanced by high levels of phosphorus from cultural eutrophication, retard macrophyte growth by shading and possibly by producing elevated pH conditions.

However, Phillips et al. (1978) set forth a convincing argument for the role of epiphytes and filamentous algae in suppressing submersed macrophyte growth due to shading. They suggest that dense phytoplankton develops subsequently to the macrophyte decline rather than being its cause. Although the effects of shading will be treated more fully in later sections, the scheme of Wetzel and Ilough (1973) in the succession of littoral communities with increasing fertility (Figure 4) is of interest here. According to this, nutrients are initially limiting to macrophyte productivity and growth is proportional to nutrient availability. At high concentrations of nutrients, submersed macrophytes will be excluded due to shading by phytoplankton, epiphytes, and filamentous algae. The model probably applies somewhat to flowing water situations although phytoplankton is expected to be less important and physical factors more important than in lakes.

Figure 4. Hypothetical changes in relative primary productivity of submersed, emergent, epiphytic, and planktonic communities with increasing nutrient enrichment (after Hough and Wetzel, 1973, with modifications according to Phillips et al., 1978).

The importance of grazing on submersed plants has never received a comprehensive review. Repeated mowings during a single growing season may in some ways simulate high grazing intensities (Davis, in preparation). However, when one considers the total effect of consumer activity, the disruptive activity of feeding, whether on macrophytes or other food sources, may be quite substantial. For example, the feeding activities of carp in Lake Mattamuskeet, North Carolina, increased turbidity so greatly that submersed waterfowl food plants did not become established until the fish were removed (Cahoon, 1953).

Many migratory waterfowl species are primary consumers and may have temporarily devastating effects on wetlands, particularly marshes that receive overgrazing by geese (Lynch, et al., 1947). Muskrat 'eat outs' have also been observed, but again it is the conspicuous emergent species studied that are reported to have heavy damage. Anderson and Lav (1976) studied grazing rates on Potamogeton pectinatus by ducks in the open water region of a Manitoba prairie marsh. By comparing biomass in enclosures and in areas not excluding birds, they estimated that 40 percent of the peak standing crop of foliage and 18 percent of the peak standing crop of tubers were removed. Some of this reduced biomass was not consumed but was lost by activities associated with feeding. By comparison, Jupp and Spence (1977b) calculated that 30 percent of the peak standing crop of P. filiformis was removed by waterfowl grazing in Loch Leven. In this case, only shoot biomass showed significant grazing losses, perhaps due to difficulty of uprooting tubers in the fine clay substrate.

2.7 HYDROSTATIC PRESSURE

In exceptionally clear lakes of great depth, it would appear that there is adequate light for macrophyte growth at depths beyond the observed plant distribution. At lower altitudes one atmosphere of excess pressure is equal to the pressure in about 10 m of water. Hence, depth maxima of species tolerant to low light levels suggest that hydrostatic pressure is a factor in depth limitation of plant presence. As reviewed by Hutchinson (1975), charophytes, mosses, and the lower vascular plants tend to grow at greater depths than submersed angiosperms. R. G. Wetzel (quoted in Hutchinson, 1975) found that 0.5 atmosphere of excess pressure reduced photosynthesis in Najas flexilis by 50 percent. Spence (1976) compared depth maxima of vascular plants (including lower vascular plants) with various nonvascular plants in 23 freshwater lakes. Depth maxima summarized by Spence for submersed vascular plants and the non-vascular charophyte, Nitella spp., in some British lakes are plotted against the depth of 1 percent light transmission for each lake (Figure 5). Only the data collected by divers (as compared with from a boat) are used. The depth maxima for the vascular plants plateau at around 5.5 to 6 m regardless of water transparency. This suggests that factors other than available light limited the depth maxima for vascular plants and a case for hydrostatic pressure effects is strongly suggested. Depth maxima for Nitella spp., on the other hand, increased throughout the range with increasing light penetration, suggesting light limitation as being of primary importance.

Figure 5. Depth maxima for aquatic vascular plants and Nitella spp. as related to the 1 percent light transmission depth for some British lakes (data from Spence, 1976).

Adaptations which result in resistance to hydrostatic pressure are unclear. In laboratory experiments physiological and/or anatomical and growth changes in submersed angiosperms become apparent when hydrostatic pressures of 0.5 to 1 atmosphere excess are applied (Gessner, 1952; Ferling, 1957). One response is a decrease in the size of intercellular air spaces. Of course, environmental factors such as sediment characteristics, nutrient distribution, dissolved oxygen, temperature, and the quality of light reaching the bottom may play a part in restricting depth penetration by plants.