Correspondence: Margaret A.Brock Centre for Natural, Resources, New South Wales Department of Land and Water Conservation, Armidale, NSW 2351, Australia (Email: firstname.lastname@example.org)
Aquatic plants include a variety of life forms and functional groups that are adapted to diverse wetland habitats. Both similarities and differences in seed and seed-bank characteristics were discovered in comparisons of Australian (New South Wales) temporary upland wetlands with a North American (New Jersey) tidal freshwater marsh having both natural and constructed wetlands. In the former, flooding and drying are unpredictable and in the latter water levels vary diurnally and substrate is constantly moist. The hydrologic regimen provides the overriding selective force, with climate an important second factor. Other factors related to water level, such as oxygen availability, temperature and light, vary spatially and temporally, influencing germination processes, germination rates and seedling establishment. Seed and seed-bank characteristics (size, desiccation and inundation tolerance, germination cues and seed-bank longevity and depletion) differ, with the Australian temporary wetland being more similar to the small-seeded persistent seed bank of the constructed wetland site than to the natural tidal freshwater site with its larger seeds, transient seed bank and seasonal spring germination. Some non-spring germination can occur in the tidal constructed wetland if the soil is disturbed. In contrast, seeds in the temporary Australian wetlands germinated in response to wet/dry cycles rather than to season. Functional groups (e.g. submerged, amphibious) are more diverse in the Australian temporary wetlands, where all species tolerate drying. We suggest that the amphibious zone, with its hydrologic gradient, is the site of selection pressure determining establishment of wetland plants from seed. In this zone, multiple selective factors vary spatially and temporally.
Wetland plants (hydrophytes) grow in soil saturated by water or in the water itself (Penfound 1952). Because of variable hydrology, growth forms that vary within and between wetlands may be emergent, as well as floating, rooted with floating leaves or submerged (Sculthorpe 1967; Cook 1990). These plants occupy diverse habitats and have diverse phylogeny, germination responses and seed-bank types – topics that will be addressed briefly before turning to case studies to explore ecological and evolutionary trends.
Wetland plant habitats are extremely varied. They may be permanent or temporary, either predictable (e.g. vernal pools or in monsoonal climates) or unpredictable (areas with unpredictable rainfall patterns), freshwater or saline and have running or still water (Mitsch & Gosselink 1993; Whigham et al. 1993; Boulton & Brock 1999). The features of each wetland type result in selection for particular life history strategies. For example, North American east coast tidal salt marshes are dominated by a few perennial graminoids, but tidal freshwater marshes have many annual and perennial forbs.
The variable hydrology and resultant amphibious gradient produce zones favoring particular plant groups (Fig. 1). These functional groups have been determined on the basis of germination, establishment and reproduction in relation to presence or absence of water (Brock & Casanova 1997). Submerged and terrestrial species that cannot tolerate drying or submersion occupy the lower and upper extremes of a wetland-edge gradient, respectively. Many amphibious species that tolerate or respond to fluctuations of water presence and absence occupy the wet/dry ecotone. Some amphibious plants ‘respond’ to the fluctuating water levels by changing growth form (e.g. leaf shape, petiole or internode length), while others tolerate variations in flooding pattern without major change in form.
Hydrophytes occur widely and sporadically in phylogenetic treatments of plant families (Bremer et al. 1998; Cook 1999). Morphology of seeds and fruits resembles that of terrestrial ancestors (Cook 1990) but adaptiveness of polymorphic diaspores for dispersal is often obscure (Cook 1987). It is also noteworthy that highly successful dispersal of many aquatic plants may occur via vegetative propagules as happens, for example, in the absence of sexual reproduction when only one sex of a dioecious species is present or seed production is limited (Sculthorpe 1967; Cook 1987; Philbrick & Les 1996).
Because of the diverse origins of hydrophytes, seed attributes contributing to life history strategies are probably modifications of pre-existing ancestral dormancy and germination characteristics (Stebbins 1971; Cook 1999). Adaptation of seed traits ‘involves changes in character syndromes’ through modification of developmental patterns rather than complete reorganization (Stebbins 1971). Impermeable seed coats or mucilage may limit oxygen availability of seeds from terrestrial habitats (Crawford 1992); thus the ability of hydrophytes to survive prolonged inundation, and the anaerobic germination of some of them are related to terrestrial morphological and/or biochemical mechanisms to tolerate anaerobiosis.
The hydrologic regimen of the amphibious zone (Fig. 1) determines the environments experienced by seeds, producing an array of interacting germination factors that probably, in turn, produce an array of germination responses (Roberts 1999). Along the amphibious gradient, water that contains <5% of the amount of oxygen present in air (Sculthorpe 1967) results in a range of aerobic, hypoxic or anoxic conditions and by its heat absorption capacity moderates daily temperature fluctuations. Depth and materials in the water column also affect light quality and intensity. In many wetlands the presence or absence of water, resulting in wet/dry cycles, cues for germination. Water may also affect sedimentation and litter deposition patterns, salinity, pH, nutrients and other physical and chemical characteristics that influence seeds (Mitsch & Gosselink 1993; Boulton & Brock 1999).
Wetland species show a considerable range of germination responses (Baskin & Baskin 1998), with a given regimen resulting in germination of one species and maintaining dormancy in another (Coops & van der Velde 1995; Leck 1996; Schütz 1997; Budelsky & Galatowitsch 1999). Extreme levels, which vary with species, may reduce viability. Seeds of most species can tolerate considerable periods of inundation and/or drying. An exception occurs with Impatiens capensis seeds which lose viability if dry or hypoxic/anaerobic for 1–2 months (Leck 1979, 1996).
Longevity of seeds in soil varies and seed banks are distinguished as transient or persistent (Thompson et al. 1997). Transient species (Type 1) are those that have viable seeds present for less than 1 year, while persistent species are those that have viable seeds persisting for fewer than 5 years (Type 2) or more than 5 years (Type 3). Tidal freshwater marsh Type 3 species were distinguished from Type 2 species by their presence in subsurface samples and absence in the vegetation (Leck & Simpson 1987). Seed-bank data for the Australian upland temporary wetlands come from long-term germination studies of dried sediment; species with persistent Type 3 seed banks germinated from sediments after 5 years of dry storage.
We explore evolutionary and ecological trends by examining seed and seed-bank germination in contrasting freshwater wetlands, temporary upland wetlands in Australia and permanent tidal wetlands in the USA. We address (i) physical and biotic factors that have selected for development of seed and seed-bank strategies of hydrophytes; (ii) seed dispersal and dormancy and germination strategies; (iii) independent strategies in unrelated phylogenetic lineages; and (iv) future research.
Case Study 1: Tidal freshwater marsh, New Jersey, USA
The Hamilton-Trenton Marsh is a tidal freshwater wetland on the Delaware River, where tidal amplitude is ~2.2 m and at high tide the high marsh is inundated to a depth of ~15 cm. Such tidal freshwater marshes are characterized by a variety of annual and perennial species (Simpson et al. 1983). Like vegetation in salt marshes, species and functional groups vary spatially and in their tolerances to hydrologic regimen.
Seed characteristics of natural marsh dominants are compared with species that colonized a nearby constructed wetland, which is part of the same wetland complex. The 38.9 ha constructed site, completed in 1994, has 32.3 ha of wetlands that replace, by New Jersey State law, 23.2 ha of wetland lost during highway construction.
Vegetation of the natural marsh has undergone historical changes affecting the species present and/or their distributions (Leck & Simpson 1995). Over more than 25 years of seed-bank study, however, this wetland has been quite stable hydrologically, although sediment accretion appears to be ~0.97 cm annually (Orson et al. 1990).
Our natural marsh studies examined size and diversity of seed banks (Leck & Graveline 1979), zonation patterns (Parker & Leck 1985), germination phenology (Leck et al. 1989), seasonal turnover and longevity (Leck & Simpson 1987) and importance of the seed rain (Leck & Simpson 1994), as well as seed bank, seedling and vegetation dynamics over 10 years (Leck & Simpson 1995). These data are complemented by germination data (Leck & Simpson 1993; Leck et al. 1994; Leck 1996). Since 1995, tidal habitats of the constructed wetland site have been rapidly colonized (Leck M. A. & Leck C. F. (1999) unpublished: Seed bank development and vegetation of a created tidal freshwater wetland on the Delaware River, near Trenton, NJ, USA (abstract). VIth International Seed Workshop, Merida, Yucatan, Mexico; unpublished observation, 1994–2000).
Seed bank – natural marsh
Seed banks were fairly large and diverse (8870–21 210/m2 in surface (0–2 cm) samples; 5.1–10.8 spp./sample with 14–27 spp./site and 57 total spp.) (Leck & Simpson 1987). Over 15 years, 115 species occured in soil samples (Leck & Simpson 1993). Both transient and persistent seed-bank strategies (Fig. 2a) occured: 37% of the species were Type 1, 42% Type 2, and 21% Type 3. Most seeds (and many species) turned over each year during spring germination (Leck & Simpson 1987; Leck et al. 1989). There were 2.5–28.6-fold more seeds, and 1.5–2.4-fold more species germinating, from March than from June surface (0–2 cm) samples. Accordingly, the seed bank is substantially renewed each year (Leck & Simpson 1987), with number of seeds of a given species varying considerably over time (Leck & Simpson 1995). Longevity at a 32 cm depth was estimated to be 75 years (Leck et al. 1989); a few viable seeds also occured to depths of 65–70 cm (Cimpko, 1992, unpublished observations).
Seeds of transient species are larger than those of persistent species (Fig. 2a), as in terrestrial systems (Thompson & Grime 1979; Thompson et al. 1993; Bekker et al. 1998; Hodkinson et al. 1998). A given functional group (e.g. amphibious-tolerators) has a wide range of seed weights and therefore exploits various seed bank strategies. Also, it is notable that the high marsh lacks submerged and amphibious–responder groups. This may be related to poor seed set or poor dispersal or possibly to lack of suitable germination conditions in the greenhouse. These groups occur in shallow tidal channels and shallow tidepools elsewhere in the wetland, but generally the 2 m tides that occur twice daily do not provide a conducive environment for such species.
Except for coarse spines, barbed awns or hairy pappi of Asteraceae, seeds are fairly smooth. The non-Asteraceae exhibit variable surface textures and shapes (Montgomery 1977).
Table 1. Summary of germination characteristics of natural marsh species (based on Leck 1996)
Number of species
Bank Types 2 and 3
only +/− or −
Regardless of seed-bank type, after a stratification period, most species germinate at 5°C (Table 1; Leck 1996), ensuring that seeds germinate in spring, when space for growth is available. Thus there is a strong seasonal constraint. If disturbances open the canopy in autumn and alternating temperatures mimic those conducive for spring germination, some seedlings of species with persistent seed banks may appear but they do not survive winter (Leck, 1976–2000, unpublished observations). For nearly all species spring germination is due to physiological dormancy (Baskin & Baskin 1998); for Peltandra virginica, however, germination of the non-dormant seed is restricted by the fruit coat and low fall/winter temperatures (West & Whigham 1975–76). Another exception is Phalaris arundinacea, whose seeds are dispersed in early summer (late June), and if light and temperature are suitable, germination can occur during the season they are produced, although this has not been observed.
Oxygen availability also provides a strong germination cue (Table 1). Most species can germinate under aerobic and even hypoxic conditions, with 20% requiring hypoxia or anoxia (Leck 1996). For those that germinate under anaerobic conditions, root growth is impaired (Sculthorpe 1967; Crawford 1992; Leck & Simpson 1993). The hydrologic regimen exerts an overriding effect on germination. Flooding by 1 cm of water can significantly reduce seed-bank density and species richness, even after natural after-ripening in the field (Leck & Graveline 1979; Leck & Simpson 1987, 1994; Leck M. A. & Leck C. F. (1999) unpublished: Seed bank development and vegetation of a created tidal freshwater wetland on the Delaware River, near Trenton, NJ, USA (abstract). VIth International Seed Workshop, Merida, Yucatan, Mexico). In addition, burial may reduce viability of some species (Leck 1996).
Desiccation and inundation tolerance
Ability to tolerate drying (Table 1) also varies (Leck 1996); drying did not reduce germination in 25% of the 12 species studied. In addition, responses of seeds to hydrologic regimens showed varying degrees of tolerance to prolonged inundation, but only one species, Impatiens capensis, lost viability.
Many species appear to have high dispersal potential (Parker & Leck 1985). Dispersal may relate to the buoyancy of seeds or to the presence of mucilage (West & Whigham 1975–1976) or flower parts (Parker & Leck 1985). Small seeds probably do not break surface tension and float on or in the water column and those that have wings or hairs for air transport may be secondarily dispersed by water. Despite such potential for dispersal, dominant species of the high marsh were not common colonizers at the constructed wetland.
Initial seed banks were of low density and diversity but quickly exceeded natural marsh values (1995–98 ranges: 1041752–>380 000/m2; 3.3–31.8 spp./sample (0–3 cm); and 65–112 spp./year. Dominant seed-bank species at the constructed wetland had very small seeds (Fig. 2a); Asteraceae, Cyperaceae, and Juncaceae, including a number of perennial species, were considerably more diverse (Appendix 1) and numerous than at the natural marsh. The small seed sizes suggest that seeds are persistent, in agreement with observations on seed banks in disturbed terrestrial and successional habitats (Fenner 1987; Leck & Leck 1998). Depletion of the seed bank during spring germination does not appear to occur, with large numbers of small-seeded species germinating in June samples (5th year).
Case study 2: temporary upland wetlands, New South Wales, Australia
Upland temporary wetlands occur on the New England Tablelands, an elevated plateau (800–1500 m above sea level) on the Great Dividing Range in north-eastern New South Wales, Australia. The region is variably influenced both by the winter-rainfall-dominated temperate climate of southern Australia and by the summer-rainfall-dominated subtropical climate of north-eastern Australia. Despite a slight summer dominance, rainfall varies both within and between years. Hence, the wetlands fill and dry unpredictably.
Most remaining natural wetlands are shallow depressions, <2 m maximum depth, with small catchments that rarely overflow (Brock et al. 1999). Because the catchments are small, water levels are greatly influenced by the timing of periods of above- or below-average rainfall. The natural wetlands include nearly permanent wetlands that only dry in extreme 1-in-20-year droughts, wetlands that flood for several years and then dry for as long, seasonally filling wetlands, wetlands that fill and dry several times a year and patches of boggy ground that might waterlog and fill only in the wettest years (Brock 1991; Brock & Casanova 1997; Brock 1998; Brock et al. 1999).
Temporary wetlands are characterized by a species-rich community representing a range of functional groups (Table 2; Fig. 2b; Appendix 1). Species and functional groups vary spatially and in tolerances to hydrologic regimen. In the wet/dry ecotone, a species-rich amphibious group has both fluctuation tolerators and fluctuation responders. Plants that respond to change in water level by altering growth form are a conspicuous and dominant element, in contrast to the tidal freshwater marsh, where tidal fluctuations do not allow time for morphological responses to water fluctuations.
Table 2. Comparisons of wetlands, and plant and seed characteristics. Comments for the constructed wetland are based on data and observations for the first 4 years following construction
USA: New Jersey tidal freshwater marsh
Australia: NSW temporary upland wetlands
Transient and persistent
Water within wetlands
Animals and wind between wetlands
Long lived seeds
Many short lived seeds
Long lived seeds
Rapid germination, after wetting not all seeds germinate
Rapid, early spring germination
Spring germination, with later germination possible
Hedge their bets
Little bet hedging
Some bet hedging
All tolerate drying
Many tolerate drying
Most (?) tolerate drying
All tolerate inundation
Most tolerate inundation
Most (?) tolerate inundation
Life history pattern
Mostly r species
Many K species
Mostly r species
Many small seeds
Large and small seeds
Small proportion of seeds germinate in each wetting event
Most seeds germinate in spring
Some seeds germinate in spring
Annuals and perennials
Annuals and perennials
Mainly tolerators and terrestrial
Mainly tolerators and terrestrial
Vary with lake and water regime
Species vary with duration/depth of inundation
Species vary with duration/ depth of inundation
Extensive, mostly high marsh
Extensive, mostly high marsh
Moves in space and time
Constant, variable inundation
Constant, variable inundation
Vegetation generally predictable
Seed bank characteristics
Seed banks are large and diverse, with over 100 species germinating from the five wetlands studied. Each wetland is dominated by only a few species but has a total of 21–47 species. Persistent seed bank strategies dominate (Fig. 3a), with 87% long-term persistent species (Type 3) and 11% short-term persistent (Type 2). The remaining 3% are rare and cannot be assigned to a particular seed-bank type.
Most species are long lived and not all seeds germinate during a particular wetting event (Fig. 3b; Brock 1998). After 7 years' dry storage, over 60% of the original seed-bank species germinated from the seed bank; after 9 years over 40% of them still germinated (Fig. 3b). Many species have viable seed remaining after several wetting events, as demonstrated by nearly 80% germinating from the same samples after four germination events and 20% after nine (Fig. 3b). The high degree of longevity and lack of seed-bank depletion in these unpredictable temporary wetlands contrasts with the high proportion of transient species and the high percentage of seeds germinating from natural tidal freshwater marsh samples.
Seeds from the upland temporary wetlands are smaller than those of many of the tidal freshwater marsh species (Fig. 2). These small sizes and weights of seeds parallel seed weights of the constructed wetland site. A given functional group (e.g. amphibious-tolerators or amphibious-responders) has a wide range of seed weights (Fig. 2b) and therefore exploits various seed bank strategies, as also shown by species of the tidal freshwater marsh.
Although emergence can occur for many species in any season, germination and establishment are favored in autumn and spring (Britton & Brock 1994). For many, germination occurs after wetting and establishment depends on continuing presence of water in the habitat. Diurnal temperature ranges are high, so that seeds in shallow water may experience a 15°C mean range in winter and a 28°C mean range in spring and summer. Because of wind mixing and shallow water, where secchi depths reach the bottom, it is assumed that neither oxygen nor light are limiting for the large numbers of species whose seeds germinate there. The minimal impact of inundation on species richness is in contrast with the tidal marsh, where inundation reduces germination. Germination data are lacking for individual species and we therefore cannot expand our interpretations of germination characteristics further for the Australian upland temporary wetland.
Long-lived seeds and rapid germination after wetting are general strategies of plants in these temporary wetlands (Table 2). Species further improve their chances with a small proportion of seeds germinating in any single wetting event (Fig. 3b) and germinating after wetting in any season.
Desiccation and inundation tolerance
Seeds of all the Australian species can tolerate drying and most germinate rapidly on reflooding, a prerequisite for survival in temporary wetlands. Also, all can tolerate inundation for at least short periods but germination under submerged conditions is common only in species of the submerged groups (Appendix 1).
Wind, water and birds disperse seeds locally within a wetland. Birds are probably the main dispersal vector between wetlands because the landscape lacks floodplains and thus wetlands are not connected by water.
Evolution and ecology
Although the tidal freshwater wetlands of the USA and the upland temporary wetlands of Australia are remarkably different ecosystem types in different climatic and geographic positions, they show strong parallels in plant and seed characteristics (Table 2). Research results provide clues on how environmental factors influence seed characteristics that allow us to consider evolution of seed traits for wetland plants. The caveat that ‘forces favoring the initial emergence of a trait are not necessarily the same as those maintaining it’ (Westoby et al. 1997; p.153) has been kept in mind as we consider the selective factors and responses across the amphibious zone (Fig. 1), desiccation and inundation tolerances, relationships to other wetland plant strategies and relationships of ecologic scale to wetland seed characteristics.
The hydrologic regimen is a dominating environmental factor in all wetlands (Fig. 4). (see van der Valk 1981; Weiher & Keddy 1998). Presence or absence of water over a range of spatial and temporal scales not only determines the type of wetland but also the biotic community that can develop. Timing, frequency, duration and depth of water are major parameters and the variability or consistency of each plays a major role in determining which plants survive and reproduce in a particular wetland type. Many biotic and abiotic factors (including aspects of anthropogenic change) will interact with water regime to determine the conditions for germination at various spatial and temporal scales. From our studies and from those of other wetlands, we suggest that every wetland type has an amphibious zone in which water presence or absence fluctuates on some scale. We suggest that the way in which the hydrological regimen acts in this amphibious zone is the primary environmental sieve that selects for wetland species with the seed, seed-bank and life-cycle characteristics conducive to these conditions.
Second to hydrology, climate appears to be the major selective factor. This is especially obvious for the natural marsh, where germination occurs in spring (Leck et al. 1989), and germination phenology may be coupled with the timing of seed ripening and dispersal in autumn. Studies of dormancy cycles, carried out only for a limited number of wetland species (Baskin et al. 1993, 1996; Milberg 1994; Schütz 1997), have shown a mechanism for spring germination (Hilhorst et al. 1996). Lack of germination in disturbed sites during summer but germination in these areas in autumn (Leck, 1996–2000, unpublished observations), tends to support the idea of cycling in a persistent seed bank species. However, this may be due to enforced dormancy caused by unsuitable temperatures and light under dense vegetation. Diurnal temperature fluctuations and number of temperature cycles provide germination cues for some wetland species (Ekstam & Forseby 1999; Ekstam et al. 1999).
In contrast, in the Australian temporary wetlands germination can occur in any season when water is present, with autumn and spring being the most likely seasons (Britton & Brock 1994). The unpredictability of rainfall will select for species that can improve their chances by germinating whenever wet conditions allow, without depleting the entire seed bank.
Our phylogenetic family diversity (Table 3; Appendix 1) is not surprising; it is well known that freshwater aquatic plants are derived from multiple angiosperm lines (Cook 1999). Interestingly, comparison of taxa shows that of the 38 families present, 13 are common to both case studies, with 11 common genera and three common species.
Table 3. Comparison of North American (NJ) and Australian (NSW) wetland seed taxa
Comparisons of our wetlands also show that seed germination factors, as influenced by hydrology (Fig. 4), have resulted in some similar but many different responses (Table 2). For example, while dormancy is primarily physiological the relatively stable natural marsh has selected for transient seed bank species with large seeds, compared with the constructed wetland or temporary Australian wetlands. Another interesting difference is the lack of some functional groups in the tidal marsh. A given functional group (e.g. tolerators), however, may exploit all seed bank strategies (Fig. 2) and contain species with a variety of dormancy/germination strategies with differing responses to oxygen, temperature, light and other cues.
Wetland hydrology may promote different behaviors designed to improve chances simply because seeds experience a complex set of germination factors that vary spatially and temporally (Figs 1, 4) and determine whether it is better to germinate early or late in the germination period. Even if the response is somewhat imprecise or rainfall presents a suboptimal establishment period, many wetland species, such as Cyperus spp., Elatine gratioides, Lindernia dubia and Limosella australis, have the capacity to flower and set seed when very small (1–2 cm).
Germination studies of individual Australian species are generally lacking; comparative data could provide clues to the impact of selective factors (Fig. 4). In addition, detailed studies of the relationships of seed size to other seed and plant characteristics, such as those carried out for seeds of terrestrial habitats (Thompson et al. 1993; Leishman et al. 1995; Bekker et al. 1998; Hodkinson et al. 1998) may yield fruitful insights.
Although recalcitrance (inability of embryos to survive dessication) is considered to be a feature of aquatic species (von Teichman & van Wyk 1994; Roberts 1999), aquatic species vary in their ability to tolerate drying (Aldridge & Probert 1992; Leck 1996). However, tolerance of desiccation is a prerequisite for temporary wetlands and our Australian studies show that many species survive drying for years (Fig. 3). Tolerance would permit survival of seeds during aerial transport and/or during drawdowns or droughts. Recalcitrant species may be able to alter responses depending on their environment. For example, seeds of Zizania palustris are recalcitrant at low temperatures (<25–30°C) but survive drying at high temperatures (Kovach & Bradford 1992; Berjak et al. 1994). However, it is also possible that transient species do not encounter desiccation. This may be due to dispersal in autumn, when droughts are unlikely; pericarp and mucilage prevent drying even when stranded (West & Whigham 1975–76; Leck 1996). Further, for species like Impatiens capensis, rapid imbibition (Holzbaur & Leck, 1994, unpublished observations) following short periods of rain may provide sufficient water for adequate hydration or ‘priming’, which is known to increase longevity (Probert et al. 1991).
In contrast, for orthodox species drying may promote germination by altering seed coat permeability (Sculthorpe 1967). Furthermore, the wet/dry drawdown cycles of temporary wetlands in Australia have selected for wetting/drying cycles as germination cues. Germination occurs most often during the wetting part of the cycle.
Although inundation reduces germination (Leck & Simpson 1987), the effect of hypoxia or anoxia on germination and seed survival varies with species (Table 1). Some germinate as drawdown occurs but not while flooded. Others require reduced oxygen levels that involve anaerobic metabolism (Crawford 1992). Obviously, species forming persistent seed banks must be able to survive in or on saturated soils. It is not known what features of seeds contribute to this success. For a few species, such as Nelumbo (Nelumbium) nucifera, impermeable seed coats combined with an oxygenated space within the seed (Baskin & Baskin 1998) may contribute to a species success. Attack of seeds by microbes may be reduced under anoxic conditions (Greenfield 1999).
Perhaps the most intriguing question raised by studies of hypoxic and anoxic responses of wetland species, such as Pontederia cordata and Alisma subcordata that require a low level of oxygen to germinate (Table 1; Leck 1996), is how seeds monitor the oxygen environment. Zizania texana, for example, germinates differentially in 0.1, 1.0, 4.0 and 5.0 p.p.m. oxygen (85, 79, 8 and 3%, respectively)(Power & Fonteyn 1995). Furthermore, how does a species, such as Bidens laevis, respond to its water environment so that it germinates to a high percentage when the substrate is very moist but not on a surface sufficiently moist for germination of non-wetland species (Baskin, 1992, personal communication)? The advantages of such discrimination are apparent, especially in temporary wetlands, where responses to water level fluctuations are the key to successful establishment. Little is known about the physiological and biochemical bases for these responses. Species exploiting the same habitat, such as rice (Oryza sativa) and the rice weed (Echinochloa crusgalli), may have different germination responses: O. sativa is not inhibited by cyanide, but E. crusgalli is (Kennedy et al. 1987). Moreover, cultivars of E. crusgalli differ in their responses to flooding.
Compared to the stable, permanent tidal, freshwater wetland, the complexity of potential responses is probably greater in temporary (Australian) and newly colonized (constructed wetland) sites. Small seeds could experience a greater variety of cues, caused by variable spatial and temporal microenvironments, resulting in persistent seed banks.
Relationships to other life-history stages/strategies
The occurence of particular seed characteristics (size, dispersal mode, dormancy cues) does not appear to be related to whether species are annual or perennial, clonal or non-clonal or in different functional groups. The large seededness of natural marsh species (Fig. 2a) appears to be related to the advantage of having large seedlings where seedling densities are high and competition is a more important stress than physical factors caused by inundation (Parker & Leck 1985; Leck & Simpson 1993).
In aquatic habitats the constraints on sexual reproduction (Sculthorpe 1967; Philbrick & Les 1996) are countered by the beneficence of the aquatic milieu that allows for easy vegetative propagation, where even detached cotyledons can develop roots on the moist soil surface (e.g. Bidens laevis, Leck, 1985, unpublished observation). Production of turions and other vegetatively produced perennating structures is a feature of aquatic species (Sculthorpe 1967; Philbrick & Les 1996). However, these occur in saline and freshwater temporary wetlands (Brock 1982, 1983; Brock, Year?, unpublished observation), but not tidal freshwater habitats, where, instead, vivipary occurs in several species (e.g. Cyperus bipartitus, Juncus acuminatus, Poa trivialis and Scirpus polyphyllus;Leck, 1984–2000, unpublihsed observation).
Questions of scale
Wetland seed banks provide insights into the ecology and evolution of seeds at the population, community and ecosystem levels (Figs 1,4; Table 2). The levels are ultimately interrelated.
At the population level, individual species vary spatially and temporally in germination and establishment responses. Some species that occur both in the Australian temporary wetlands (Brock 1998) and in the New Jersey tidal freshwater marshes (Leck & Simpson 1987) are found only in the seed bank and not always in the vegetation. In the natural marsh, several small-seeded species (e.g. Dulichium arundinaceum, Juncus effusus and Ranunculus sceleratus) that appeared as fugitive seed bank species were colonizers at the nearby constructed wetland (Leck, 1995, unpublished observations).
Germination ecology of sets of congeneric species may provide clues to successional patterns and evolution of specific germination requirements. Observations suggest that there are differences in dormancy and germination requirements, including responses to substrate and microhydrology between, for example, Bidens laevis and Bidens cernua, Juncus effusus and Juncus acuminatus, and Polygonum punctatum, Polygonum hydropiper and Polygonum hydropiperoides. For example at the constructed wetland, Juncus effusus rapidly exploited new surfaces and then was rapidly replaced by other species in 1–2 years, while Juncus acuminatus seemed to be part of the vegetation for more than years. Germination ecology of sets of such species may provide clues to successional patterns and evolution of specific germination requirements.
Other studies show geographic differences in seed characteristics within species (Simpson et al. 1985). The wetland variety of Chamaecrista fasciculata (Fabaceae) found in tidal freshwater marshes on the Virginia (USA) coastal plain has greater flood tolerance and biomass accumulation under flooded conditions than the upland form (Fenster 1997). Another example is Sagittaria latifolia, in which northern populations have dormant seeds while southern ones do not. It is not surprising therefore that published reports of dormancy and germination requirements in this species are often conflicting (Marburger 1993). Application of molecular biological techniques to congeners and populations of a given species may allow us to understand genetic/biochemical differences and also provide clues to the evolution of seed characteristics.
At the community level, seed, seed-bank and seedling adaptations influence vegetation dynamics (Leck & Simpson 1995; Brock 1998). Comparison of the predictable natural marsh with the unpredictable Australian upland wetlands and the constructed site shows the importance of persistent seed banks with disturbance, as occurs in terrestrial habitats (Grime 1989): transient seed banks of stable habitats have larger seeds. High seed densities coupled with high dispersibility provide the opportunity to find unoccupied sites but the high densities of a uniformly early germinating species with large seedlings may reduce growth of other species having smaller seedlings and/or germinating later. Therefore, greater sibling competition, which occurs at high densities, is more than compensated for by the ability to out-compete seedlings of other species.
At the ecosystem level, differences as well as similarities (Table 2) occur between these two geographically distant wetlands. The hydrologic regimen, influenced by climate, has selected for differences in desiccation and inundation tolerances as well as seed bank strategies, with accompanying differences in seed and seedling sizes and dormancy/germination strategies. Study of other wetlands may greatly improve understanding of wetland seed evolution.
The recent report implicating wet areas as sites for angiosperm evolution (Doyle 1998) emphasizes the importance of the amphibious zone to development of seed and seed-bank strategies for wetland species. Insights regarding the nature of adaptations to the amphibious zone could be provided by species whose populations vary in tolerances to flooding or have recalcitrant seeds that do not tolerate inundation. Correlation of life history or seed strategies with functional groups of the same or different species could also provide information that would help us to generalize about wetland seed evolution.
We hope that the questions raised by this paper will stimulate studies from germination to ecosystem levels (Table 4). Furthermore, we hope that they will lead to enhanced understanding of the ecology and evolution of wetland seeds, seed banks and vegetation processes at multiple temporal and spatial scales. Does the amphibious edge, in fact, drive selection of wetland seed characteristics?
Table 4. Questions and possible research directions presented at different scales. Some may bridge more than one level
What are the phylogenetic relationships of desiccation and inundation tolerances within and between families?
Are there common seed strategies within and among amphibious zone families?
How quickly can selection work to modify strategies?
How do seeds survive wetting/drying in the amphibious zone?
Is maternal environment integrated for the benefit of wetland seeds? If so, how?
How are dormancy, seed size, seedling size and dispersibility interrelated, and how are they related to habitat fitness?
Do tidal wetland species respond to tidal cycles?
Do seed components of transient and persistent seed bank types differ?
Is there a correlation between desiccation tolerance and germination cues? Do carbohydrates play a part? (See Foley 1997).
How does the amphibious zone vary among wetland types, and how do differences influence selection of seed characteristics?
How does a species seed characteristics change over time and space? How do these change as habitats are modified?
Regarding life cycles: What is the critical stage for selection? Seed? Seed bank? Seedling establishment?
Are amphibious ecotones the major zones of selection for all plants “at the edge” of their distribution ranges?
What is the importance of seed predation across the amphibious zone?
What is the biochemical/physiological/morphological basis for all seeds in the wetland seed bank not germinating synchronously?
How do ecological scale and process drive wetland seed characteristics? Insights from populations, communities, and ecosystems and successional vs. stable habitats.
M.A.L. is indebted to Rider University for a research leave and other support and to all who helped with field and greenhouse studies. M.A.B. thanks the Botany Department at the University of New England, and the Land and Water Resources Research and Development Corporation Armidale, New South Wales, Australia, for time and research support. Special thanks to K. Theodore and C. Cooper for help with longevity studies, to Drs D. Britton, M. Casanova and G. Smith for support during seed bank germination and establishment studies, to D. Bell for seed weight and germination data on Eleocharis spp. and to others who provided field help and comments. We both thank Carol Baskin and Nancy Garwood for the symposium invitation that challenged us to draw these comparisons. J. M. Baskin, P. Jarman and C. F. Leck provided many helpful suggestions for manuscript improvement. We gratefully acknowledge the many seed bank and germination studies, too numerous to consider here, that have informed our work.
Species list for seed-bank families in Australian upland temporary wetlands (NSW) and in a North American permanent tidal freshwater marsh (NJ, USA). Families common to both wetlands are followed by those occurring only in NSW and then by those only in NJ samples. Presence in each wetland type is noted; the tidal wetland is designated as natural and constructed (cw). Functional groups are: S, submerged; R, amphibious-responder; T, amphibious-tolerator; Ter., terrestrial. For the tidal marsh, only species exceeding 100/m2 are listed. All species are native except where indicated: *exotic species and */n exotic and native species. (Nomenclature is based on Gleason & Cronquist 1991 for USA, and Harden 1990, 1991, 1992, 1993 for Australia).