Traits related to disturbance frequency and intensity
The opportunistic strategy should be selected in the more disturbed situations [i.e. proximal extremity of the (c) axis, Fig. 3]. In this part of the scheme, the occurrence of any plant species should be determined mostly by an ability to tolerate disturbances and to regenerate in gaps. Traits allowing survival during disturbances are usually grouped under the ‘ruderal’ or ‘r’ strategy. Several authors have defined the key-traits of this strategy:
- 1The ‘r’ strategists of Southwood (Southwood, 1988) have a large number of small seeds with wide dispersal ability, and early maturation (i.e. small size and lack of vegetative spread).
- 2Ruderals of the Grime model are of small size with a limited lateral spread, a short life cycle and a high frequency of flowering. These species have numerous small seeds or spores dispersed by wind, and should be able to persist in the seed bank in a dormant form for long periods (Grime, 2002).
- 3Ruderals of the Kautsky model are of small size, with a limited lateral spread, and have a short life-span with a large proportion of the annual biomass production spent on sexual reproduction, with no vegetative propagules, but numerous dormant seeds or zygotes (Kautsky, 1988).
- 4Traits related to the ‘explerent’ explorative strategy (Rabotnov, 1975; in Onipchenko, Semenova & Van Der Maarel, 1998) include a high production of small seeds, a large seed bank and a high relative growth rate, which leads to rapid growth if nutrients are available.
Connell & Slatyer (1977) suggested that large highly disturbed patches should be recolonized mainly by external colonizers, whereas the less disturbed patches should be partly re-colonized by seeds and propagules from the soil reservoir. Field observations partially confirm this prediction, although similarities between seed bank and established vegetation remain relatively high in areas frequently exposed to disturbances (Tabacchi et al., 2005).
When sexual reproduction is effective, seeds are expected to have a high dispersability. In the Salicaceae, for example, dispersability is efficient through small wind-dispersed seeds that must reach suitable habitats rapidly after release in order to compensate for low viability of the diaspores (Guilloy et al., 2002). Mahoney & Rood (1998) developed a model showing that the efficiency of dispersal of such species depends on a narrow timeframe. As a consequence, their recruitment is highly variable from year to year. Water dispersal should be highly favoured, as it increases the opportunity for propagules to reach gaps immediately after the disturbance, but such dispersal requires high buoyancy of propagules (Andersson, Nilsson & Johansson, 2000; Boedeltje et al., 2004; Riis & Sand-Jensen, 2006). Seeds of the helophytes Alisma plantago-aquatica L., Carex flava L. and Cladium mariscus (L.) Pohl., like seeds of the hydrophyte Hippuris vulgaris L., are able to float for >1.5 years (Praeger, 1913). Seeds of the disturbance-tolerant species Berula erecta (Hudson) Coville and Myriophyllum spicatum L. are able to float for about 7 days (Guppy, 1906; Praeger, 1913), while fragments of several species that colonize disturbed habitats are able to float for several weeks (Barrat-Segretain, Bornette & Hering-Vilas-Bôas, 1998; Boedeltje et al., 2003). Conversely, seeds and fragments of plants species that colonize undisturbed habitats tend to have low buoyancy: seeds of Baldellia ranunculoides (L.) Parl., Oenanthe fistulosa L., Oenanthe aquatica (L.) Poir. and Nuphar lutea (L.) Sm. (I. Combroux & G. Bornette, pers. obs.), or fragments of Potamogeton coloratus Hornem. sink immediately or very soon after release (Barrat-Segretain, Henry & Bornette, 1999).
Seeds of plants that colonize disturbed habitats tend to have no dormancy, or dormancy breakage depending on a signal from the disturbance itself (Thompson & Grime, 1979; Jutila, 2001; Karrenberg, Edwards & Kollman, 2002), which enables them to be immediately available when gaps are created. For example, Charophytes are pioneer species, which usually bloom after disturbance (Bornette & Arens, 2002), suggesting that the disturbance itself induces oospore germination. During floods, the abrasive effects of sediment movement can break cuticular dormancy. Seeds of several species that colonize disturbed habitats [Luronium natans (L.) Raf., Potamogeton pectinatus L., and Potamogeton pusillus L., Bornette et al., 1998) show increasing germination if they are scarified (S. Greulich & G. Bornette, pers. obs. for L. natans, and Teltscherova & Hejny, 1973).
Vegetative regeneration is a key function for the maintenance of species subjected to recurrent disturbance, particularly in infertile situations that can prevail in the most disturbed floodplain habitats (Bellingham & Sparrow, 2000; Klimešová & Klimeš, 2007). Several authors have demonstrated the prevalent role of clonal growth in species maintenance after disturbances through survival of deeply anchored roots or rhizomes, spreading from refuges or sprouting from vegetative propagules (Prach & Pyšek, 1994; Henry et al., 1996; Barsoum, 2002). As an example, along U.S.A. rivers, two shrubs common on the channel shelf (a bank feature), Alnus serrulata (Ait.) Willd. and Cornus amomum Mill., are relatively resistant to destruction by flooding because of small, highly resilient stems and the ability to sprout rapidly from damaged stumps (Hupp & Osterkamp, 1985). This high capability of regrowth is also facilitated by the production of adventitious roots that utilize nutrients in alluvial material deposited by floods, allowing for rapid rooting of flood-detached branches (Hupp & Osterkamp, 1996). Plants that produce rhizomatous systems resist flood disturbance by vegetative production of new shoots from resistant rhizomes (Bartley & Spence, 1987; Willby, Abernethy & Demars, 2000; Kotschy & Rogers, 2008). Plants having a high growth rate should also be selected when disturbance frequency increases. High growth rate would be important not only for seedlings, but also for plants that regenerate from plant fragments, or that colonize empty patches by growing in from the edge (Barrat-Segretain & Amoros, 1996; Henry & Amoros, 1996).
Disturbance affects the size of eroded versus deposited patches, as patches tend to be larger when disturbances increase in intensity. Traits linked to vegetative and to sexual reproduction are involved differently in the recolonization process, depending on patch size (Miller, 1982; Belsky, 1986). The growth rate of plants at the patch edge, as well as patch size, determine the contribution of vegetative propagation to recolonization (Connell & Keough, 1985). In large patches, seed colonization tends to dominate, whereas the edge effect tends to be low (Vandvik, 2004). Further, Miller (1982) also suggested that large patches should be colonized mostly by species having high rates of reproduction and high dispersal ability, whereas small patches should be colonized mostly by more competitive species with a high growth rate located around the patch perimeter (edge effect). Consequently, even if the regenerative strategies involved in the colonization process vary according to patch size, large patches (i.e. patches that are usually generated by a high frequency and/or intensity of disturbances) should be colonized mainly by seeds with high dispersal ability.
Traits related to the deposition versus erosion nature of disturbance
Traits increasing resistance. The type of disturbance greatly influences which species attributes are most important (Armesto & Pickett, 1985; Pickett et al., 1989). Resistance to flood disturbances should involve different adaptations depending on the deposition versus erosion nature of floods. A resistance strategy should be particularly efficient for depositional floods. Indeed, such events usually do not lead to mechanical destruction of vegetation, but to burial, elevated turbidity and long inundation periods (lasting months in some cases, e.g. southeastern U.S.A. coastal plain). Consequently, the duration of inundation is a highly influential factor that controls lowland floodplain vegetation patterns. Recurrent flood inundations reduce substrate porosity through deposition of fine sediment, which leads to disconnection between surface water and ground water, increase of eutrophication and substrate anoxia. Such processes result frequently in low species richness of both hydrophytes and helophytes (Brock, Van Der Velde & Van De Steeg, 1987; Van Geest et al., 2005). The tallest plants, able to remain emerged during floods or that have sufficiently high biomass, are more probably to tolerate long-term submersion (Mommer et al., 2006). The coincident high turbidity and deposition of fine particles should favour floating species (Kalliola et al., 1991; Bini et al., 1999), species able to anchor themselves in sediment of low cohesive strength (Hanley & Lamont, 2002), or species able to produce adventitious roots or to spread laterally close to the surface of the newly deposited sediment or at the surface of the water (Sorrell et al., 2000; Xiong et al., 2001). Rapid adventitious root formation allows the rooting of the elongated stems lacking support tissues when water level decreases. Ultimately, deposition processes can impede regrowth of Nymphaeaceae species from rhizomes. As seeds of these species require early supply of light to hypocotyls (Smits et al., 1990), their growth could be impeded in frequently turbid habitats. Species able to survive should have storage systems (e.g. large rhizomes or tubers), making them able to generate vegetative parts of the individuals destroyed by long-term submersion (Brock et al., 1987). For example, Nymphoides peltata (S.G. Gmelin) Kuntze rapidly produced new leaves able to reach the water surface during a long-duration inundation (>3 weeks), but disappeared as the water level decreased, because its storage system was insufficient to produce subsequent new leaves over such a short time frame. Conversely, N. lutea and Nymphaea alba L., with their low growth rates and large storage systems, may survive long inundation. More generally, herbaceous plants tend to be intolerant of prolonged inundation (Grimoldi et al., 1999). Species that survive can be described as plastic, with morphological and/or metabolic adaptations to deal with inundation and anoxia, such as aerenchyma formation, adventitious root formation, increasing specific leaf area and leaf and stem elongation (Vartapetian & Jackson, 1997; Jackson & Colmer, 2005; Voesenek et al., 2006). Aerenchyme formation, and leaf and stem elongation should increase the plant capacity to reach the water surface, and thus to survive anoxia (Grimoldi et al., 1999; Lenssen et al., 2000).
Resistance to scouring floods should be limited, because such disturbances may remove substrate and plants (Riis & Biggs, 2003). Traits that reduce the hydrodynamic forces encountered by plants or increase mechanical resistance to breaking and uprooting enable them to reduce the risk of being damaged (Schutten & Davy, 2000; Puijalon et al., 2008). Willows, as well as many aquatic plants, are small to intermediate-sized species with highly flexible stems and strong anchorage, which decrease the risk of uprooting or breakage during floods (Karrenberg et al., 2003; Lytle & Poff, 2004). Some species also have breaking points (Salix fragilis L., Hottonia palustris L.) that enable a self-thinning of the crown and may thereby reduce resistance to floods (Brock, Mielo & Oostermeijer, 1989; Beismann et al., 2000) but also favour the dispersion of vegetative propagules produced by the flood itself (Cellot, Mouillot & Henry, 1998). Plastic responses, leading to small-sized, very flexible growth forms, or to an increasing allocation of resources to anchorage, also decrease the uprooting or breaking risk during floods. This ability to bend under moderate and high flows has direct feed-back consequences on siltation (Tsujimoto, 1999) and geomorphic processes (Kouwen & Li, 1980), and probably facilitates the anchorage of riverside plants.
Traits increasing resilience. Many plants have few or no specific morphological adaptations allowing them to resist disturbances, and their maintenance relies mainly on an ability to colonize the disturbed patch immediately after the disturbance.
Depositional floods strongly control recruitment of plants, as seeds and seedlings exhibit various tolerances to anoxia and low light conditions, and thus require particular water levels to germinate (Voesenek, Degraff & Blom, 1992; Smits et al., 1995; Middleton, 2000). Consequently, most aquatic species in such habitats are able either to germinate in turbid and oxygen-poor conditions and to rapidly reach the water surface, or to spread laterally. It is presumed that the interval between successive floods is sufficient for newly recruited individuals to reach the water surface, allowing sexual or at least vegetative reproduction. Clonal growth should also increase survival of individuals after disturbance, and increase recruitment success by maintaining a physiological relation between the parent plant and the newly produced ramets (Shumway, 1995; Pennings & Callaway, 2000; Yu, Chen & Dong, 2002). Because of these major restraints, resilience processes should be less involved in community maintenance in hydrosystems characterized by inundation.
In habitats with moderate frequency and intensity of erosional floods, perennial species may be broken (but rarely completely uprooted) by flood events. Such fragments should contribute to recolonization of disturbed patches (Henry et al., 1996), as long as they are able to disperse and regrow efficiently (Cellot et al., 1998; Karrenberg et al., 2002; Boedeltje et al., 2003). When scouring intensity and frequency are distinctly high, only annuals that are able to grow and reach reproductive maturity over a short period should occur (Schippers et al., 2001; Tabacchi et al., 2005). When normal flows alternate with highly scouring events, plants regrowing from diaspores may establish. Charophytes, as well as plants germinating from light diaspores (Zannichellia palustris L., P. pusillus, Nasturtium officinale R. Br.) can reach high cover in the newly scoured substrate of cut-off river channels (Bornette & Arens, 2002; Combroux & Bornette, 2004).