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Tansley review Drowned, buried and carried away: effects of plant traits on the distribution of native and alien species in riparian ecosystems Author for correspondence: Roland Jansson Tel: +46 90 786 9573 Email: [email protected] Received: 10 March 2014 Accepted: 19 June 2014

Jane A. Catford1,2,3* and Roland Jansson4* 1

School of Botany, The University of Melbourne, Melbourne, Vic. 3010, Australia; 2Fenner School of Environment and Society, The

Australian National University, Canberra, ACT 0200, Australia; 3Department of Ecology, Evolution and Behavior, University of a University, SE-901 87 Ume
a, Minnesota, Saint Paul, MN 55108, USA; 4Department of Ecology and Environmental Science, Ume
Sweden

Contents Summary

19

V.

Modification and management of riparian plant communities

30

I.

Introduction

19

VI.

Conclusions and future research

32

II.

Functional traits and life history adaptations of riparian plants

20

Acknowledgements

33

III.

Local and regional patterns in the distribution of riparian plants

24

References

33

IV.

Alien plant invasion in riparian zones

26

Summary New Phytologist (2014) 204: 19–36 doi: 10.1111/nph.12951

Key words: community assembly, disturbance, exotic species, flooding regime, functional traits, hydrochory, inundation, non-native species.

Riparian vegetation is exposed to stress from inundation and hydraulic disturbance, and is often rich in native and alien plant species. We describe 35 traits that enable plants to cope with riparian conditions. These include traits for tolerating or avoiding anoxia and enabling underwater photosynthesis, traits that confer resistance and resilience to hydraulic disturbance, and attributes that facilitate dispersal, such as floating propagules. This diversity of life-history strategies illustrates that there are many ways of sustaining life in riparian zones, which helps to explain high riparian biodiversity. Using community assembly theory, we examine how adaptations to inundation, disturbance and dispersal shape plant community composition along key environmental gradients, and how human actions have modified communities. Dispersalrelated processes seem to explain many patterns, highlighting the influence of regional processes on local species assemblages. Using alien plant invasions like an (uncontrolled) experiment in community assembly, we use an Australian and a global dataset to examine possible causes of high degrees of riparian invasion. We found that high proportions of alien species in the regional species pools have invaded riparian zones, despite not being riparian specialists, and that riparian invaders disperse in more ways, including by water and humans, than species invading other ecosystems.

I. Introduction Riparian zones, defined as areas bordering running waters and lakes that are temporarily flooded and influenced by elevated water *These authors contributed equally to this work. Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust

tables, are challenging environments for vascular plants. Riparian species must be able to cope with waterlogging, fluctuating water levels and physical disturbance from floods and, in cold areas, ice (Lytle & Poff, 2004; Bornette et al., 2008; Merritt et al., 2010b; Lind et al., 2014). The hydrology of many rivers, for example in desert environments, is highly unpredictable, requiring that New Phytologist (2014) 204: 19–36 19 www.newphytologist.com

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riparian species are able to withstand long periods between suitable environmental conditions, which may themselves be of short duration (Capon, 2003). Riparian zones often have distinct species assemblages (Sabo et al., 2005) and are often more species-rich than surrounding ecosystems (Brown & Peet, 2003). Riparian zones also experience high degrees of invasion by alien species (i.e. species introduced beyond their native range) (Stohlgren et al., 1999; Richardson et al., 2007). This raises something of a puzzle: why are riparian zones often so rich in species, given that riparian species need one or several specialized traits to cope with the environment? High native species richness could result from large proportions of regional species pools being able to colonize riparian zones (Mouw & Alaback, 2003) or high rates of diversification (high speciation and/or low extinction rates) among clades of riparian specialists. High invasion of alien species suggests the former is true (Stohlgren et al., 1999; Richardson et al., 2007). Both high species richness and high degrees of invasion are facilitated by spatial and temporal environmental heterogeneity (Chesson & Huntly, 1997; Melbourne et al., 2007). Fluctuations in environmental conditions, often from disturbance, can result in successional mosaics, facilitating local species coexistence (Chesson & Huntly, 1997). In riparian zones, floods remove plant biomass and provide new substrate for colonization. With time, these resource-rich, early successional patches transition into communities dominated by superior competitors; this usually occurs on infrequently flooded surfaces (Dahlskog, 1966; Kalliola & Puhakka, 1988). Coexistence is also facilitated by differences in seed production, dispersal, germination and establishment among species (Grubb, 1977). Overlaid on this gradient of flood disturbance is the ecophysiological stress caused by inundation. The high diversity of environmental conditions in riparian zones necessitates a diversity of physiological, morphological or life-history strategies, but the role of these in determining patterns in riparian plant composition at various spatial and temporal scales is poorly understood. Here, we review traits that enable plant species to inhabit riparian zones and examine the ways in which these adaptations determine where species occur in space and time. Specifically, we ask: (1) Which functional and life-history traits allow plant species to inhabit riparian environments, and how have these traits evolved, as demonstrated by their phylogenetic distribution? (2) How do plant adaptations affect the composition of riparian plant communities at different spatial scales? (3) What plant traits and environmental conditions facilitate high degrees of alien plant invasion in riparian zones? (4) How do human activities modify the process of community assembly and the functional composition of riparian plant communities? We address these questions by reviewing the literature on plant adaptations to inundation stress, physical disturbance from floods, and dispersal along watercourses. We use the concept of community assembly to examine ways in which species’ traits affect local riparian assemblages by enabling certain species to pass the dispersal, environmental and biotic filters of a site. Treating alien plant invasions like an (uncontrolled) experiment in community assembly, we use riparian invasions to illuminate the riparian community assembly process. We test whether invading species are New Phytologist (2014) 204: 19–36 www.newphytologist.com

New Phytologist better able to disperse into, tolerate local environmental conditions of, and compete in riparian zones as compared with other ecosystems. We discuss the processes by which human actions can change the composition of riparian flora and how such changes can be ameliorated, and conclude by outlining research needs. Our discussion is limited to plants that inhabit the wet–dry ecotone, excluding plants with a fully aquatic habit unless they are found in riparian zones. We focus on riparian zones along running waters and lakes (including floodplains and floodplain wetlands), but do not consider coastal wetlands.

II. Functional traits and life-history adaptations of riparian plants 1. Key structuring forces of the riparian environment Despite occupying relatively small areas, riparian ecosystems play a crucial role in the landscape. Occurring at the land–water interface, they filter nutrients and other compounds that flow from upland ecosystems (Lowrance et al., 1984). Riparian vegetation stabilizes riverbanks (Hubble et al., 2010), buffers temperature variation in streams through shading (Barton et al., 1985), increases habitat heterogeneity (e.g. roots, logs) and provides energy and nutrients to aquatic ecosystems (Wallace et al., 1997). The key characteristic that distinguishes riparian zones from adjacent aquatic and terrestrial environments is the occurrence of periodic flooding and waterlogging. The water regime is considered the most important disturbance factor in freshwater ecosystems (Puckridge et al., 1998), and numerous studies have evaluated how plants respond to variation in the flooding regime (Poff et al., 1997; Lytle & Poff, 2004; Merritt et al., 2010b). Here, we focus on traits that allow plants to cope with, and benefit from, physical and chemical effects of flooding and flows. They can be organized into three main categories: (1) stress from inundation and waterlogging, which can limit plant growth and development; (2) physical disturbance from floods, where high-velocity flows and sediment erosion and deposition (exacerbated by ice action in cold climates) can result in plant mortality and biomass loss, and increases in resource availability; (3) waterborne dispersal through stream networks, where water typically flows in a single direction down a river (Grant et al., 2007) and laterally in riparian zones in response to water-level fluctuations. Building on previous reviews of riparian plant adaptations (Lytle & Poff, 2004), strategies (Bornette et al., 2008) and response guilds (Merritt et al., 2010b), we concentrate on traits that enable some plants in the regional species pool to colonize and thrive in riparian zones. We also consider the evolution of traits: if a trait occurs in many clades, it implies that new, unrelated species potentially able to colonize riparian zones have evolved relatively frequently. Conversely, if traits are found in few clades, this suggests the presence of barriers that inhibit adaptation to riparian environments, so that specialists, whose clade evolution is restricted to riparian zones, dominate the riparian flora. The review is not exhaustive, but is intended to highlight the diversity of traits Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust

New Phytologist possessed by riparian plant species. All traits identified are listed in Table 1. Note that references to traits are only found in the table. 2. Inundation Vascular plant species have evolved several traits to deal with life on land (e.g. gamete transfer through air, tissue for structural support, and vessels for internal fluid transport), which means that tolerating periods of inundation can be challenging, especially for seedlings. Gas diffusion is considerably slower underwater than in air (CO2 diffusion being 104 times slower underwater; Armstrong et al., 1994) and low underwater light availability limits photosynthesis (Vervuren et al., 2003). Underwater photosynthesis is enhanced by having thin or finely dissected leaves with thin cuticle facilitating underwater gas exchange, and chloroplasts in or close to the epidermis (Table 1). Some amphibious genera, such as Iso€e tes, Crassula and Littorella, possess CO2-concentrating mechanisms to facilitate photosynthesis. However, internal transport of mineral nutrients and photosynthetates becomes difficult in the absence of leaf evapotranspiration, which is only possible in air (Kozlowski, 1984). Inundation may also disrupt sexual reproduction (Crawford, 1987) and can lead to anoxic and toxic root environments (Jackson & Drew, 1984). By inhibiting respiration, oxygen shortage can lead to a lack of energy (Voesenek et al., 2006). Even among flood-tolerant species, roots cannot tolerate anaerobic conditions for more than a few days (Vartapetian & Jackson, 1997). Plant adaptations to oxygen shortage either reduce the need for oxygen and/or increase the tolerance of low oxygen conditions, or avoid low oxygen conditions (Table 1; Bailey-Serres & Voesenek, 2008). The physiological tolerance of anoxia can be increased, and oxygen requirements reduced, for short time periods by minimizing energy use, producing ATP by glycolysis and fermentation, and synthesizing compounds that protect cells from toxins produced during anoxia (Table 1). Species adapted to prolonged inundation avoid anoxia by extending out of the water (shoot elongation and hyponastic growth) or by transporting oxygen to oxygen-deficient parts. Interconnected gas-filled spaces known as aerenchyma allow oxygen diffusion from shoots to roots, where oxygen helps to detoxify the rhizosphere. Adventitious roots form at shoot bases to replace roots killed by anoxia. Anoxia can also be avoided through dormancy, during which metabolic activity is low, or if the timing of life cycle events (e.g. flowering and seed release) corresponds with periods of receding or low water levels. Many plants can tolerate longer periods of inundation when dormant. Accordingly, the lower elevational limits of species seem to be primarily determined by the duration of summer floods (Vervuren et al., 2003; van Eck et al., 2006). Several adaptations can facilitate photosynthesis in submerged conditions. When analysing the number of times adaptations to inundation have evolved, it is difficult to make a distinction between aquatic and riparian species, as the fully aquatic habit represents one end in the range of flooding tolerance amongst angiosperms (Jackson et al., 2009). The water lilies, Nymphaeales, are entirely aquatic and diverged at the base of the angiosperm tree (APG III, 2009), showing that adaptations to submergence evolved early. Similarly, Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust

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the aquatic and wetland clades Acorales and Alismatales, also diverged at the base of the monocot clade (APG II, 2003). Evolution of inundation tolerance from terrestrial ancestors has occurred 205–245 separate times among seed plants (Cook, 1999), and traits such as aerenchyma, thin cuticles and finely dissected leaves are found in many clades. Thus, overcoming the stress of inundation – and passing that particular environmental filter to enable occupancy of riparian conditions – does not seem to have been a major evolutionary hurdle. 3. Physical disturbance from water-level variation Riparian plants may cope with physical disturbance from floods and ice through traits that enable survival of an individual (‘resistance’, sensu Townsend & Hildrew, 1994), or traits that facilitate rapid population growth and (re)colonization of disturbed patches or recently deposited substrate (‘resilience’, sensu Townsend & Hildrew, 1994). Resistance strategies include stem, leaf and root flexibility, reduction of plant size, increased plant density, brittle twigs enabling self-thinning, and deep and widespread root systems (Table 1). Although some biomass may be lost, these strategies help individuals to survive disturbance events. Flexible stems, widespread root systems and perennating organs below or close to the ground protect against ice scour. ‘Resilient’ plants able to recover following the accumulation of litter and sediment tend to have large seeds, persistent seed banks and capacity for lateral spread (Table 1). Cleared areas and new surfaces can be rapidly (re)colonized by plant species producing many seeds or vegetative propagules, or by recruitment from soil seedbanks. In some species, seed release is timed to the most suitable periods, such as the recession of spring floods, which facilitates colonization of exposed surfaces. Many resilient species are annual or have high growth rates once established. Vegetative reproduction can confer both resistance and resilience to flood disturbance. Many riparian species produce suckers, tillers or shoots from deeply buried, and thus protected, plant organs. Rhizomes, for example, facilitate recolonization of disturbed patches and reduce the risk that floods destroy entire clones. Vegetative fragments can become detached and dispersed during disturbance events, further enhancing recolonization ability. Vegetative fragments are often buoyant and so aid in dispersal, and can remain viable for weeks after detachment. They can also start to produce roots shortly after detachment, facilitating rapid establishment once stranded. Being subject to water-level variation, riparian zones may experience long periods of drought. Plants can avoid (or ‘resist’) effects of drought by having traits such as phreatophytic roots that extend to the water table, or can be resilient to drought through traits that enable rapid recolonization, such as those described earlier (Capon, 2003; Stromberg et al., 2007). Traits conferring resilience to floods and droughts are not unique to riparian taxa, but can be found in many clades adapted to episodic disturbance, suggesting that numerous disturbanceadapted species in regional species pools may colonize riparian zones. Many resistance traits, such as deep, wide root systems and New Phytologist (2014) 204: 19–36 www.newphytologist.com

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Table 1 Plant traits and means by which they enable occupancy and facilitate growth in riparian environments Trait

Function

Adaptations to inundation and submergence in water Facilitation of photosynthesis Thin cuticle Enhances gas exchange to counteract slow diffusion in water Chloroplasts in, or close to, epidermis Thin or finely dissected leaves CAM or C4 physiology to concentrate CO2 Anoxia tolerance Economic use of energy (ATP) Biochemical pathways for ATP production in anoxic conditions (glycolysis and fermentation) Synthesis of compounds (e.g. phytoglobins and antioxidants) that reduce harmful and toxic effects of anoxia in cells Anoxia avoidance Shoot elongation Hyponastic growth

Aerenchyma Oxygenation of rhizosphere Suberin barriers in the epidermis of basal roots Adventitious roots Lenticels on stems and roots Low metabolic activity Timing of life cycle events

Increase access to light and promote carbon uptake from water Increase leaf area to maximize carbon and nutrient uptake from water Enables carbon uptake from sediment

Mommer et al. (2005), Mommer & Visser (2005), Voesenek et al. (2006) Mommer et al. (2005), Mommer & Visser (2005), Voesenek et al. (2006) Mommer et al. (2005), Mommer & Visser (2005), Voesenek et al. (2006) Madsen & Sand-Jensen (1991), Keeley (1998)

Reduction in the use of ATP when in short supply; fast recovery of protein synthesis at reoxygenation Energy production in the absence of oxygen

Bailey-Serres & Voesenek (2008), Colmer & Voesenek (2009) Bailey-Serres & Voesenek (2008), Colmer & Voesenek (2009)

Protects against toxic compounds such as nitric oxide and reactive oxygen species (ROS) produced during anoxia

Visser et al. (2003)

Enables shoots and leaves to extend out of the water to facilitate gas exchange, flowering and pollination Differential cell elongation in for example petioles of leaves to make organs more upright, which enables plants to reach water surface and/or acquire more light and helps limit sedimentation on leaves Hollow areas allowing internal oxygen diffusion from shoots to roots Detoxifies the rhizosphere from reduced forms of iron, manganese and hydrogen sulphide Limits loss of oxygen from roots and ensures that roots act as a ‘pipeline’ for oxygen transport to root tips New roots in aerated soils replacing roots killed by anoxia, or soils supplied with oxygen from roots Allow gas diffusion and entrance of oxygen through the bark of woody species Limits negative effects of energy deficit Ensures that events such as flowering, seed release and germination occur at appropriate times, such as during periods of low water levels

Ridge (1987), Voesenek et al. (2004)

Adaptations to disturbance by floods and ice Resistance High stem, root or leaf flexibility Decreases the risk of biomass loss as a result of high-velocity flows Reduction in plant size Smaller and more compact plants are more resistant to mechanical damage from flow Reduced internode or spacer Smaller and more compact plants are more resistant to length mechanical damage from flow Twig bases with preformed Allows self-thinning and hence reduces the drag force of flowing breaking points water Deep and wide root systems Resistance to scour from flow and ice, and ability to acquire resources over a large area Budding parts at or below the Protects the perennating organs of herbs from ice scour ground and being frozen into ice Resilience Large seeds Seedlings more likely to penetrate upwards through layers of sediment or litter Lateral spread with runners, tillers Faster recolonization of disturbed patches; less likely that an entire or rhizomes clone is affected by a physical disturbance

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References

Ridge (1987)

Seago et al. (2005), Voesenek et al. (2006) Laan et al. (1989) Jackson & Drew (1984) Blom et al. (1994) Kozlowski (1997) Geigenberger (2003) Blom & Voesenek (1996)

Karrenberg et al. (2002) Boeger & Poulson (2003), Puijalon & Bornette (2004) Pollux et al. (2007) Beismann et al. (2000) Karrenberg et al. (2002) €m et al. (2011) Engstro

Xiong et al. (2001) Xiong et al. (2001)

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Table 1 (Continued) Trait Persistent seed bank

Vegetative reproduction

Function

References

More likely that viable seeds are present and germinate following disturbance or when suitable environmental conditions occur (e.g. desert systems); external sources of propagules are less important Rapid recolonization following disturbance

Xiong et al. (2001), Bossuyt & Honnay (2008)

Timing of reproduction and seed release High growth rates

Arrival of seeds when conditions are suitable for germination and establishment, such as exposed surfaces saturated with water Increase ability to capitalize on suitable environmental conditions, which may be transient Early reproduction and large Increase likelihood of reproducing and increasing population size investment in seeds while environmental conditions are suitable; high investment in reproduction increases probability of species persisting in space and time Traits enhancing dispersal along streams and rivers Propagule floating ability Enables long-distance dispersal and effective colonization of riparian zones Corky or spongy tissue of low density Increases propagule buoyancy Waxy, cuticularized epidermis Prevents imbibition and sinking of propagules Surface with furrows, pits or hairs Traps air bubbles, which increases the buoyancy of propagules Floating vegetative propagules Enables long-distance dispersal and effective colonization of riparian zones Timing of propagule release More likely that propagules are released when conditions are suitable for dispersal and germination Tolerance to passing the digestive system of fish Seeds with hard coat and tolerance of anoxic conditions

Enables dispersal by riverine fish Abrasion resistance and tolerance of burial, which enables seed transport with sediment and litter and enhances longevity in the soil seedbank

resting buds at, or close to, the ground are found in a large number of clades. By contrast, several of the resistance traits are primarily found in the family Salicaceae (Table 1), with the genera Salix and Populus dominating active floodplains in the Northern Hemisphere (Karrenberg et al., 2002), in which the riparian habit is primitive. 4. Dispersal by water Compared with terrestrial plants, plants that border streams and rivers may disperse their propagules (diaspores) via two additional pathways: by water (hydrochory) or via fish (ichtyochory). Although the prevalence of hydrochory in riparian floras is not well quantified and is likely to vary among biogeographic regions, evidence suggests that a large proportion of riparian plant species disperse by hydrochory (Andersson et al., 2000a; Pettit & Froend, 2001; Boedeltje et al., 2004; Jansson et al., 2005; Merritt & Wohl, 2006). Hydrochores can be dispersed floating on the water surface or underwater (including along the stream bed; Parolin, 2006). Although the former arguably receives more attention, large numbers of propagules of many species are transported underwater (Goodson et al., 2003; Gurnell et al., 2008). In a study of seed transport along two Rocky Mountain rivers, Merritt & Wohl (2006) found that 31 and 56% of the seeds were transported on the surface of the two streams, whereas the remaining seeds were Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust

Barrat-Segretain et al. (1999), Riis & Sand-Jensen (2006) Mahoney & Rood (1998) Karrenberg et al. (2002) Pettit & Froend (2001), Bagstad et al. (2005)

Nilsson et al. (2010) van der Pijl (1972) Sculthorpe (1967) Rivadavia et al. (2009) Boedeltje et al. (2004), Riis & Sand-Jensen (2006) Kubitzki & Ziburski (1994), Pettit & Froend (2001), Karrenberg et al. (2002) Horn et al. (2011) Goodson et al. (2003), Gurnell et al. (2008)

transported in suspension or along the channel bed. Hydrochory is usually a secondary dispersal mechanism; propagules typically drop onto the ground before being carried away during floods (Schneider & Sharitz, 1988; Parolin, 2006). Some riparian plants, however, such as orchids of the ‘Disa uniflora type’ in southern Africa (Kurzweil, 1993), lean over and drop their seeds directly into streams. Buoyancy of viable seeds can be achieved through corky tissue and seed coats that prevent imbibition, and adaptations like aerenchyma may enable vegetative propagules to float (Table 1). Propagules lacking buoyancy can still be transported by water by sticking to floating objects, such as logs, branches and leaf-litter packs (Nilsson et al., 2010). Hydrochory offers five main advantages to riparian plants. First, a large proportion of hydrochores, especially buoyant hydrochores, can disperse long distances compared with other dispersal vectors (Andersson et al., 2000b; Pollux et al., 2009). Secondly, unlike wind-dispersed seeds, the dispersal distance of buoyant hydrochores is largely independent of their mass (Ikeda & Itoh, 2001). Accordingly, hydrochores tend to be heavier than wind-dispersed seeds (Moles et al., 2005), and heavier seeds have higher seedling survival (Moles & Westoby, 2004). Thirdly, by preventing desiccation, immersion in water increases the longevity of vegetative propagules. Fourthly, being bound to stream networks, hydrochory increases the probability that propagules are deposited in sites suitable for germination and growth, such as bare, waterlogged soil (van der Valk, 1981; Schneider & Sharitz, New Phytologist (2014) 204: 19–36 www.newphytologist.com

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1988). Finally, contact with water often acts as a phenological cue (Kubitzki & Ziburski, 1994). In temperate climates, immersion of seeds in water tends to break dormancy in spring and induce dormancy in autumn, ensuring that germination only occurs in spring (Boedeltje et al., 2004). Indeed, some riparian species time seed release to periods suitable for hydrochory or germination (Table 1). For many species, traits enabling hydrochory have probably evolved for other reasons (Johansson et al., 1996; Andersson et al., 2000b); their role in facilitating water dispersal has been a secondary effect. For example, traits enhancing wind dispersal, such as wings, hairs or plumes, can facilitate hydrochory where propagules ‘float’ on water surface tension. For a number of tree species, floating distances can be several times longer than typical wind-related transport (S€aumel & Kowarik, 2013). Likewise, barbs, hooks and other structures that facilitate animal dispersal can reduce water surface tension and enhance buoyancy. Hence, it is not only species that have evolved in riparian habitats that can disperse well by water. Ichtyochory represents a special case of hydrochory (Horn et al., 2011). There are at least 275 fruit-eating fish species, most of which are tropical. Frugivorous fish can be effective seed dispersers by dispersing large and nonbuoyant seeds, and contributing to longdistance, as well as upstream, dispersal (Horn et al., 2011). As with hydrochory, it is doubtful whether plants have adapted to ichtyochory by selection. Although fish disperse many seeds, fruits may have evolved to be consumed by a range of animals, not just fish. 5. Phylogenetic patterns Plants found in riparian zones are scattered across the angiosperm phylogeny (APG II, 2003; APG III, 2009). For example, in the riparian floras of northern Sweden and Alberta, Canada, all the major families present in the regional flora are also represented in riparian zones (Dynesius et al., 2004). This indicates that little evolutionary adaptation is required for (formerly) terrestrial-only species to start occupying riparian zones as well, or that many species from the regional species pool can inhabit riparian ecosystems without the need for specific adaptations. To better understand how adaptations to riparian environments have evolved, studies where multiple traits are mapped onto phylogenies are required. There are examples of single riparian representatives in otherwise terrestrial clades, as well as clades that are entirely aquatic/riparian. One might hypothesize that the greater the differences between terrestrial and riparian environmental conditions, the greater the adaptations required by terrestrial clades to occupy riparian or aquatic environments. Amphibious and truly aquatic species should therefore occur in fewer lineages than species occupying higher riparian elevations. This pattern is observed in the genus Ranunculus, which consists of c. 600 herbaceous species (H€orandl & Emadzade, 2012). The aquatic and wetland Ranunculus species are found in two clades: sections Hecatonia/Batrachium and Flammula, which possess numerous adaptations to flood tolerance and hydrochory, such as finely dissected leaves, aerenchyma, physiological tolerance of New Phytologist (2014) 204: 19–36 www.newphytologist.com

anoxia and hydrochoric seeds (H€orandl & Emadzade, 2012). In addition to these two clades, there are many riparian Ranunculus species in predominantly terrestrial clades. These species have fewer adaptations to cope with inundation, and are accordingly found at higher riparian elevations (He et al., 1999).

III. Local and regional patterns in the distribution of riparian plants 1. Community assembly The framework of assembly rules can be used to understand the ways in which plant adaptations to inundation, flood disturbance and dispersal shape riparian plant community composition. Community assembly can be conceived as a series of sieves, or nested species pools, that are determined by dispersal, environmental and biotic constraints (Fig. 1, Belyea & Lancaster, 1999; G€otzenberger et al., 2012). These filters vary in space and time, and each can be modified (Fig. 1). Although this conceptual model represents community assembly as a sequential, one-way process (Fig. 1), this is primarily for clarity of presentation and comprehension. The filters, and processes governing them, necessarily interact (see examples in Section V.5). The first filter relates to dispersal. Acting on the regional species pool, species’ fecundity and dispersal ability (such as capacity for hydrochory) determine the pool of potential colonists for a given site at a particular point in time (Fig. 1). Once present in the geographic species pool (sensu Belyea & Lancaster, 1999), a species must pass the environmental filters of that site. Depending on the local conditions, a species may need to be able to tolerate prolonged inundation, desiccation or scour to become a member of the ecological species pool (Fig. 1). Interspecific differences in tolerance to physical disturbance, flooding and drawdown may lead to the classic zonation of vegetation observed in riparian systems (Fig. 2). By grouping species with similar environmental niches, environmental filtering typically results in coexisting species having ecophysiological traits that are more similar than expected by chance (i.e. trait underdispersion or convergence; Weiher & Keddy, 1995b; de Bello, 2012). The third and final filter relates to biotic interactions, representing the outcome of interactions (including competition, mutualism and predation) among individuals in that community. In the following section, we illustrate ways in which community assembly filtering can influence the spatial distribution of riparian plants at various spatial scales, from local to regional, retaining our focus on inundation, flood disturbance and hydrochory (Table 2). 2. Spatial patterns in riparian plant community composition As mentioned earlier, riparian vegetation often forms zones along an elevation gradient (Fig. 2), transitioning from terrestrial species tolerant of only short periods of inundation, to amphibious species, to obligate aquatic species at the lowest elevations (Blom et al., 1994). This zonation may be driven by species’ increasing tolerance of submergence (Vervuren et al., 2003; van Eck et al., 2006) or by species’ niche differences that relate to species’ competitive abilities Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust

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INVADER CHARACTERISTICS

ECOSYSTEM CHARACTERISTICS Regional species pool

(a) Not applicable

(b) High rates of introduction because

of: large edge effects; close proximity to human activities, e.g. agriculture; hydrochory as an additional dispersal opportunity.

Dispersal filter

(c) Wide range of environmental

Environmental filter

(a) Bias towards riparian specialists in the exotic species pool. (b) Riparian invaders have higher

Geographic species pool

filters because of high temporal and spatial environmental heterogeneity.

(d) Frequent disturbance reduces

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Ecological species pool Biotic filter

propagule availability and greater dispersal capacity, e.g. because of a close association with humans.

(c) Riparian invaders can pass through a broader range of filters than other types of invaders.

(d) Riparian invaders more invasive

strength of competition for resources.

Actual species pool

than species that invade other ecosystems.

Local community assemblage Fig. 1 Possible explanations for high degrees of invasion in riparian ecosystems. Explanations are based on characteristics of riparian ecosystems and characteristics of the invading species (see Section V). Explanation types: a, regional species pool; b, dispersal filter; c, environmental filter; d, biotic filter. The filters interact and determine the composition of the geographic, ecological and actual species pools (sensu Belyea & Lancaster, 1999). Explanations are not mutually exclusive. Native species are white symbols and alien species grey symbols; circles, triangles and stars represent three hypothetical species’ functional groups.

(a)

(b)

Fig. 2 Zonation of riparian vegetation along an elevation gradient. Each zone is characterized by a different type of vegetation, as illustrated by variation in vegetation texture and colour with increasing wetland depth. (Source: J. A. Catford, River Murray wetlands, Victoria, Australia.)

(Grace, 1988) and tradeoffs between tolerance of soil drying vs tolerance of inundation (Silvertown et al., 1999; Table 2). As well as differences in species’ characteristics, there are also differences in Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust

the number of species along the elevation gradient, with species richness generally declining towards lower elevations (Fig. 3), presumably reflecting that fewer species in the geographic species pool are tolerant of inundation. Changes in species’ occupancy with increasing distance from the channel may be caused by other factors, such as probability of propagules arriving at a site or successional processes (Table 2). Merritt & Wohl (2006) found that the probability of encountering hydrochoric species decreased from 90% at the edge of the stream channel to 1% in areas that were 10 m from the stream channel. This could be because hydrochores are more likely to be deposited along stream margins (dispersal filter) or because hydric species tolerating conditions close to the channel tend to be waterdispersed (environmental filter). Differences in community composition among patches or along a reach can reflect variation in time since disturbance, where each patch undergoes succession with species being replaced via facilitation or competition (biotic interactions). Likewise, disturbance frequency may affect species richness, with maximum species richness at intermediate disturbance frequency and site productivity (Pollock et al., 1998). However, flood duration and intensity are usually highly correlated with frequency of disturbance (Hupp & Osterkamp, 1985), making it difficult to distinguish their effects. In a rare experimental test of community assembly, Weiher & Keddy (1995a) were able to replicate the segregation of plant communities found in riverine wetlands by manipulating flood duration and productivity. Dispersal can result in differences in community composition among riparian zones at the reach scale. Surveys (Andersson et al., 2000b) and experiments (Jansson et al., 2005; Merritt et al., 2010a) show that species richness is higher on riverbanks that receive many hydrochores. There are also more species with long-floating propagules in riparian than in terrestrial communities (Johansson New Phytologist (2014) 204: 19–36 www.newphytologist.com

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Table 2 Potential ways that inundation, disturbance and dispersal affect the distribution of riparian plants at different spatial scales Community assembly filter

Scale

Pattern

Factor

Hypothesized mechanism

Local

Species separated along elevation gradients

Inundation

Differences among species in their tolerance of inundation depth and duration Segregation of species as a result of tradeoffs between tolerance of soil drying and waterlogging Fewer species can tolerate long periods of inundation

Environmental and biotic filters Biotic filter

Vervuren et al. (2003), van Eck et al. (2006)

Environmental filter

Fig. 3

Dispersal

Hydrochorous propagules more likely to be deposited close to the channel

Dispersal filter

Merritt & Wohl (2006)

Disturbance

Tradeoffs between species’ colonization and competitive abilities mean that early colonizers are replaced by superior competitors with increasing time since disturbance Hydrochory results in greater numbers of colonizing species

Biotic filter

Dahlskog (1966), Kalliola & Puhakka (1988)

Dispersal filter

Andersson et al. (2000b), Jansson et al. (2005)

Maximum species richness at intermediate disturbance frequency and vegetation growth rates Species with short-floating propagules are more likely to sink before being deposited along tranquil reaches

Biotic filter

Pollock et al. (1998)

Dispersal filter

Nilsson et al. (2002)

Hydrochorous species more likely to colonize riparian communities More species with capacity for hydrochory in riparian zones Intermediate disturbance in mid-reaches

Dispersal filter

Johansson et al. (1996)

Diversity of hydrochorous propagules increases downstream, but higher disturbance intensity limits species establishment in lower reaches Increasing disturbance intensity from floods

Dispersal and environmental filters

Local

Local

Reach

Reach to Landscape Reach to Landscape Reach to Landscape

Landscape

Regional

Decreased species richness with increasing duration of inundation More hydrochorous species close to stream channels Successional changes in vegetation following disturbance

Higher species richness in sites that receive hydrochorous propagules Maximum species richness at intermediate flood frequency and productivity More species with longfloating propagules along tranquil than turbulent reaches More species have propagules with floating capacity in riparian communities than upland communities Peaks in species richness in the mid-reaches of rivers

Inundation

Dispersal

Disturbance

Dispersal

Dispersal

Disturbance

Dispersal; disturbance

Monotonic decrease in species richness towards lower reaches

Disturbance

Environmental filter Environmental filter

Environmental filter

References

Silvertown et al. (1999)

Nilsson et al. (1989), Decamps & Tabacchi (1994) Nilsson et al. (1994)

€ f€alt et al. (2005) Reno

We list likely mechanisms and associated community assembly filters (Fig. 1) for the spatial patterns observed. References relate to the observed patterns, not to the hypothesized mechanisms, factors or community filters.

et al., 1996) and more on riverbanks along tranquil than along turbulent reaches (Nilsson et al., 2002), potentially because shortfloating propagules are more likely to sink before reaching riparian zones. Longitudinal patterns in riparian species richness have been extensively studied, with variation in both patterns found and explanations invoked. Several studies have documented peaks in species richness in mid-reaches (Nilsson et al., 1989; Decamps & Tabacchi, 1994), which has been interpreted both as an outcome of intermediate disturbance and as dispersal along the river (Nilsson et al., 1994). The complexity of the gradient is demonstrated by the fact that diversity patterns have been observed to vary depending on the type of riparian habitat studied and the time since major flood disturbance (Ren€of€alt et al., 2005). New Phytologist (2014) 204: 19–36 www.newphytologist.com

IV. Alien plant invasion in riparian zones 1. Expectations It is well established that riparian zones experience high degrees of alien plant invasion (Stohlgren et al., 1999; Richardson et al., 2007), whether that be in relation to the frequency of occurrence of alien species (Vila et al., 2007), or absolute (Stohlgren et al., 1998) or relative (Catford et al., 2012b) alien species richness and cover. The reasons for high degrees of riparian invasion are usually investigated from an ecosystem perspective, where their geography and environmental characteristics are primarily considered (Fig. 1, left-hand side). Common explanations include effective dispersal provided by hydrochory, the high edge-to-area ratio of riparian Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust

New Phytologist Amphibian species (22 sp.)

Tansley review Graminoids (36 sp.)

Willows (64 sp.)

Riparian forest (60 sp.)

Upland (46 sp.)

Number of species per plot

20

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Hypothesis 3. More alien species may be able to pass through the environmental filters and invade riparian ecosystems compared with other ecosystem types, as a result of, for example, the high environmental heterogeneity of riparian ecosystems. Hypothesis 4. Species that invade riparian ecosystems may reach higher abundance than species that invade other ecosystems. If the degree of invasion is based on total or per capita alien abundance (Catford et al., 2012b), higher occurrence of these species will result in riparian zones having higher degrees of invasion.

15

10

5

0 –350 –300 –250 –200 –150 –100

–50

0

50

100

Using plant community composition data collected across almost 30 000 quadrats in Victoria, Australia (Supporting Information, Table S1), and information on 458 higher plant species in the Global Invasive Species Database (GISD; ISSG, 2013), we assess the likelihood of these four explanations (Table S2). A description of the datasets and analysis is provided in Notes S1.

Elevation (cm) Fig. 3 Species richness in riparian zones declines at lower elevations as flood frequency and duration of inundation increase. The number of riparian plant species was recorded in 334 quadrats (0.25 m2, open circles and trendline), and the cumulative number of species per vegetation belt (hatched lines and names at the top of the figure) are plotted against the elevation in the riparian zone. 0 indicates the elevation of the annual high-water mark. Data were collected along a 200-m-long slow-flowing reach (Lappselet) of the freeflowing Vindel River in northern Sweden. Details of the sampling design can € m et al. (2012). The trendline is drawn with LOWESS be found in Stro regression in SPSS v. 21 (IBM Corp., Armonk, NY, USA), using a moving window that includes 50% of the points.

zones, high habitat heterogeneity, frequent flood disturbance, high human use and close proximity to human activities (Richardson et al., 2007; Catford et al., 2011; Eschtruth & Battles, 2011). Each of these factors can facilitate invasion by modifying community assembly (Section III.1, Fig. 1). Structured around community assembly processes and considering riparian invasion from the perspective of the invaders, we proffer four explanations for high degrees of riparian invasion (Fig. 1, right-hand side): Hypothesis 1. A high proportion of alien species in the regional species pool preferentially invade riparian zones. Species specifically adapted to riparian ecosystems may be overrepresented in the alien species pool because of an introduction bias, leading to higher alien species richness in riparian ecosystems. Hypothesis 2. Alien species are more likely to invade riparian ecosystems because: dispersal is more effective in river networks than in other parts of landscapes; species tend to have dispersal characteristics conducive to dispersal in river networks, namely hydrochory; or riparian invaders have a stronger association with humans than with other species. By planting and transporting certain plant species in high numbers, humans can increase the dispersal opportunities of species in a way that is independent of their traits (Catford et al., 2012a). Regardless of the cause, increased dispersal may allow more alien species to invade riparian zones (i.e. higher colonization pressure, sensu Lockwood et al., 2009) or it may increase the frequency and abundance of particular species that have many propagules (i.e. propagule pressure, sensu Lockwood et al., 2009). Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust

2. Findings Hypothesis 1 Few alien species exclusively invade riparian ecosystems in either of the datasets examined. Species specifically adapted to riparian environments do not appear to be overrepresented in the pool of potential invaders (the regional species pool, Fig. 1). Across the 458 higher plants listed in the GISD, two species invade riparian zones and wetlands exclusively. In Victoria, 10 of 1036 alien species exclusively invade the Riparian Scrubs ecosystem (24 species exclusively invade the Broad Riparian category, which combines three ecosystem types, Notes S1). Hypothesis 2 Information about the modes of dispersal used by invaders in the GISD suggests that riparian invaders disperse more widelyandinhighernumbersthanothertypesofinvaders(TableS2). They may therefore have higher colonization and propagule pressure than species that invade other ecosystems. Of 11 possible modes of dispersal, riparian invaders use more dispersal modes than species that do not invade riparian ecosystems (Fig. 4, Table S3). Compared with species that do not invade riparian zones, a greater proportion of riparian invaders are dispersed by hydrochory (riparian invaders (mean  SE), 0.41  0.04; non-riparian invaders, 0.24  0.03; P < 0.001, Table S4) and humans (riparian invaders, 0.59  0.038; non-riparian invaders, 0.42  0.029; P < 0.001, Table S5). Similar trends were found when comparisons were made using species that invade riparian zones and wetlands (i.e. Broad Riparian category). Hypothesis 3 Across both datasets, a high proportion of the alien or invasive species pool invades riparian zones. Based on the proportion of the invasive species pool invading any given ecosystem type (excluding Broad Riparian), riparian zones were ranked fourth in the GISD (Fig. 5a) and third in the Victorian data (Fig. 5b; second and first, respectively, if Broad Riparian was used). For the GISD, 37% of invaders are known to invade riparian zones and 47% to invade riparian zones or wetlands. In the Victorian dataset, 50% of the alien species recorded were observed in Riparian New Phytologist (2014) 204: 19–36 www.newphytologist.com

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Number of dispersal modes

9 8 7 6 5 4 3 2 1 (a)

0 Nonriparian invaders

Riparian invaders

Human-mediated Animals Water currents Garden escape* Ornamental* Hikers* Vegetative Vehicles* Unspecified Wind Agriculture* Forestry*

(b)

Contaminated 0.0

0.1

0.2

0.3 0.4 0.5 Proportion of invasive species

Scrubs, and 69% of the alien species occur across the three ecosystems that make up the Broad Riparian category (Fig. 5b). Hypothesis 4 As an indication of invasion success, we used the Victorian data to determine whether alien species in riparian zones contribute more cover relative to their richness than invaders in other types of ecosystems. Across the 20 ecosystem types, alien species that invade Riparian Scrubs contribute slightly more than average to total vegetation cover (i.e. they fall above the trendline in Fig. 6), although Wetlands and Riverine Grassy Woodlands (the other vegetation classes that can be considered riparian) do not. This evidence suggests that high degrees of invasion in these riparian ecosystems are not caused by riparian invaders being more invasive and attaining higher cover than species that invade other ecosystems. 3. Synopsis Based on our examination of the GISD and the Victoria data, species that invade riparian ecosystems may have higher colonization and propagule pressure (Hypothesis 2, H2) and are able to pass through a broader range of environmental filters (H3) than species New Phytologist (2014) 204: 19–36 www.newphytologist.com

0.6

0.7

Fig. 4 (a) Number of dispersal modes used by invasive higher plant species in the Global Invasive Species Database (GISD) that invade riparian ecosystems and species that do not (P < 0.001; Table S3; box shows interquartile range with the median as a horizontal line; whiskers show the highest and lowest values in the dataset). (b) Proportion of riparian invaders (grey) and non-riparian invaders (white) that use different dispersal modes. *, dispersal modes that are included as a form of human-mediated dispersal.

that invade other ecosystems. Although additional data on species traits and environmental conditions are required to ascertain support for H3, H2 and H3 seem more likely to explain high riparian invasion than those based on a bias towards riparian specialists in the alien regional species pool (H1) and riparian invaders being more invasive than invaders of other ecosystems (H4). We recognize that this analysis is limited to two datasets, but these findings appear to be in agreement with observed trends. Although there are exceptions, observations suggest that relatively few alien invaders occur in mid-elevation areas of riparian zones. In River Murray wetlands, Australia, only six of 57 alien species observed were classified as amphibious, inhabiting midelevations, compared with 38 out of 87 native species (Catford et al., 2011). Characterized by frequent flood disturbance and potentially long periods of both inundation and drying, this part of the riparian zone may represent both high stress and high disturbance, arguably an unusual combination of conditions requiring specialized adaptations (Grime, 1977; Westoby, 1998). Rather than having specialized adaptations to cope with fluctuating water levels and flood disturbance, most riparian invaders may be temporally or spatially opportunistic, completing Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust

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Tansley review Ruderal/disturbed Broad Riparian Natural Forests Agricultural Riparian* Urban Range/grassland Wetlands* Planted forests Scrub/scrublands Coastland Watercourses Lakes Unknown Estuarine Desert Marine

(a)

Broad riparian Plains woodlands or forests Dry forests Riparian scrubs or swampy scrubs and woodlands* Riverine grassy woodlands or forests* Lower slopes or hills woodlands Plains grasslands and chenopod shrublands Wetlands* Coastal scrubs grasslands and woodlands Herb-rich woodlands Lowland forests Heathy woodlands Mallee Salt-tolerant and/or succulent shrublands Box ironbark forests or dry/lower fertility woodlands Wet or damp forests Heathlands Rocky outcrop or escarpment scrubs Montane grasslands Sub-alpine grasslands Rainforests

Fig. 5 (a) Proportion of 458 invasive higher plant species in the Global Invasive Species Database (GISD) that invade each of 16 habitat types; (b) proportion of 1036 alien species in Victoria, Australia, that invade each of 20 ecosystem types. *, Broad Riparian category includes these ecosystems.

(b) 0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

Proportion of invading species

30 Plains grasslands and Chenopod shrublands

Relative alien species cover (%)

Coastal scrubs grasslands and Woodlands

25 Plains woodlands or Forests

Lower slopes or Hills woodlands

Riverine grassy woodlands or Forests

20 Riparian scrubs or Swampy scrubs and Woodlands

15

Rainforests

Salt−tolerant and/or Succulent shrublands

Herb−rich woodlands

Wetlands

Box ironbark forests or dry/lower fertility woodlands Heathy woodlands

Rocky outcrop or Escarpment scrubs

Mallee

10 Lowland forests

5

Wet or Damp forests

Dry forests

Heathlands Montane grasslands

Subalpine grassland

0 10

20

30

40

Relative alien species richness (%) Fig. 6 Relationships between relative alien species richness and relative alien species cover in 20 ecosystem types in Victoria, Australia. Means (points) and standard errors (whiskers) are shown; the grey dashed line indicates the line of best fit (y = 4.021 + 0.548x). Data collected from 29 991 30 m 9 30 m quadrats between 1970 and 2011 by the Victorian Department of Environment and Primary Industries.

their life cycles without being flooded. The vast majority of alien plant species that invade riparian environments in southeastern Australia tend to occur between flood events or in higher elevation areas that are less frequently flooded (Stokes et al., 2010; Catford et al., 2011). More alien species have an annual life history compared with the native riparian flora (Kyle & Leishman, 2009; Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust

Catford et al., 2011), which helps plants complete their life cycles between flood events (a ‘resilient trait’, Table 1). Similar trends have been observed in Europe and North America; many riparian invaders are annuals (Decamps et al., 1995) and many riparian invaders also occur in terrestrial, non-riparian habitats (PlantyTabacchi et al., 1996; Dynesius et al., 2004). New Phytologist (2014) 204: 19–36 www.newphytologist.com

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Riparian zones may be highly invaded at the ecosystem level, but it does not seem that all areas (i.e. elevations) within riparian zones are highly invaded. The high spatial and temporal heterogeneity of riparian zones may thus help to explain the apparent conundrum between high degrees of invasion and adaptations required to live in riparian zones. Even if invading species are unable to tolerate some of the environmental conditions, the high diversity of niche space of riparian ecosystems means that many different life strategies are viable, providing many opportunities for invasion.

V. Modification and management of riparian plant communities As well as the addition of alien species to regional species pools, community composition can change through modification of any of the three community assembly filters. Significant changes to the dispersal, environmental or biotic filters are likely to prompt a change in the composition of the associated species pools and, consequently, the resultant community (Fig. 7). In the following, we briefly discuss some ways in which these filters can be modified by human activities in ways that affect riparian ecosystems (Fig. 7). 1. Changes to the regional species pool Species from other regions are often added to the regional species pool through the actions of humans: alien species may be imported as a commodity, they may arrive with transport, or they may spread from another invaded region (Hulme et al., 2008). Global patterns suggest that most alien plants escape into natural environments after being intentionally introduced, usually for ornamental purposes (Hulme et al., 2008; Dehnen-Schmutz, 2011). The construction of inland waterways and removal of dispersal barriers

can effectively provide new corridors for dispersal (Wilson et al., 2009), enabling species from different biogeographic regions to mix. Loss of native species from the regional species pool implies that they are lost locally first (which would result from changes to the three filters, discussed later). Species adapted to frequent disturbance tend to have propagules with greater longevity (Bossuyt & Honnay, 2008), so riparian specialists may persist for longer, although that is not always the case, as the short seed viability of the endangered Japanese floodplain species, Aster kantoensis, attests (Washitani et al., 1997). 2. Changes to dispersal filters Changes in habitat connectivity, the location and size of propagule sources and vector availability can alter species’ dispersal patterns and the composition of the geographic species pool (Belyea & Lancaster, 1999). The ability of species’ propagules to reach a given site is crucial, as is the number of propagules that arrive because this can effectively increase a species’ chance of colonization and dominance (Pacala & Tilman, 1994; Simberloff, 2009). It is therefore of little surprise that dispersal and propagule pressure facilitate invasions, as noted earlier. Reflecting the importance of hydrochory for riparian plants, loss of hydrological connectivity can limit the dispersal of many species. Lateral connectivity (river floodplain) can be impeded through the construction of walls and levees. Dams, weirs and associated impoundments inhibit downstream transport of hydrochores (Andersson et al., 2000a; Merritt & Wohl, 2006), potentially altering species composition and prompting the loss of some species below dams (Jansson et al., 2000). As well as reductions in connectivity, some habitats may become more connected. Roads

TYPES OF MODIFICATION

REMEDIATION STRATEGIES Regional species pool

(a) Exotic species introduction and

(a) Limit exotic introduction; assisted

loss of native species.

colonization to restock natives.

(b) New dispersal barriers, e.g.

Dispersal filter

dams, levees; changes in propagule sources and vectors, e.g. humans. (c) Environmental modification,

Geographic species pool

Environmental filter

e.g. flow regulation, climate change, urbanization.

(d) Changes in competition,

mutualisms and predation from changes in species occupancy and abundance.

(b) Restore connectivity; limit humanmediated dispersal; maintain buffer between agriculture/gardens and riparian ecosystem. (c) Amelioration of environmental

Ecological species pool Biotic filter Actual species pool

change, e.g. environmental flows, salt interception, water-sensitive urban design. (d) Limit native species harvest, e.g. logging, hunting; control of invasive species.

Local community assemblage Fig. 7 Ways in which human activities can alter community composition in riparian ecosystems through changes to the (a) regional species pool and the (b) dispersal, (c) environmental and (d) biotic filters. The filters interact and determine the composition of the geographic, ecological and actual species pools (sensu Belyea & Lancaster, 1999). Native species are white symbols and alien species are grey symbols; circles, triangles and stars represent three hypothetical species’ functional groups. New Phytologist (2014) 204: 19–36 www.newphytologist.com

Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust

New Phytologist and walking tracks can act as efficient corridors for dispersal (von der Lippe & Kowarik, 2012) and may connect anthropogenic habitats with riparian zones. Humans disperse plant propagules by using and travelling through riparian environments (Hodgkinson & Thompson, 1997). Species that frequently occur around areas of human activity (e.g. weeds, crops, ornamentals) will be dispersed more frequently and in greater numbers (von der Lippe & Kowarik, 2012). Habitat transformation can reduce the input of native riparian species’ propagules whilst increasing the propagule availability of species normally absent or scarce in riparian zones, such as alien species (Niggemann et al., 2009). Floodplains are often used for livestock grazing or crop production, and organic waste from gardens and agriculture is frequently dumped in riparian zones. Centres of human activity thus provide a large and ready source of propagules, the impact of which is heightened by the large edge effects typical of riparian zones, making them particularly susceptible to species invasion from surrounding environments. Propagule dispersal that coincides with peak flows can be interrupted by changes in flow regimes, inhibiting dispersal and reducing seedling survival (Rood & Mahoney, 1990). 3. Changes to environmental filters Abiotic conditions in riparian zones can be altered through activities like eutrophication, pollution, urbanization, salinization, climate change and flow regulation. Reflecting the focus of this paper on inundation and flood disturbance, we concentrate on flow regime modification. Damming of rivers has modified the amount, timing and type of water flow altering river hydrology, hydraulics, geomorphology and ecology (Rood et al., 1999). Given the strong influence of river flow regimes on riparian plants, hydrological modification is a key explanation for changes in the composition of riparian vegetation (Dynesius et al., 2004; Merritt et al., 2010b). In its simplest form, community composition can change with environmental modification in two ways (Catford et al., 2011). First, native species specifically adapted to the historical regime may be unable to tolerate modified conditions (Evangelista et al., 2008), prompting a decline in the vigour and size of their populations. Abundance of alien generalists may increase with any abiotic change provided it is to the detriment of its competitors. Such a scenario may have occurred along the upper Rhine River, France, where a reduction in flooding facilitated invasion of generalist species (Deiller et al., 2001). Secondly, if alien species are preadapted (or adapt rapidly; Whitney & Gabler, 2008) to the modified conditions, they may be able to outcompete native species that are poorly adapted to the new conditions. Invasion success will be greatest when a decline in native species is coupled with environmental conditions that favour alien specialists. For example, the success of alien Tamarix species along regulated rivers in southwestern USA is at least partially attributable to their superior adaptation to modified conditions (Stromberg et al., 2007). Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust

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4. Changes to biotic filters Biotic interactions within a community will change as the occupancy and abundance of species change. Such changes can be a result of human actions that directly affect biota and their interactions (e.g. logging, hunting, livestock grazing), but most changes probably result indirectly through the modification of the other filters. Working in the Eastern Sierra Nevada Mountains of California, Elderd (2003) found that reduced flooding below dams prompted an increase in non-riparian herbaceous cover, grass thatch and shading, which led to lower germination success and higher herbivory of Mimulus guttatus (common monkeyflower), a common riparian species. 5. Feedbacks and interactions among filters As well as changes that occur outside of a community (e.g. human activities), feedback effects from the resident community may amplify changes to the three community assembly filters and, consequently, to community composition. Some plants can modify abiotic characteristics, effectively changing environmental filters in their favour (Richardson et al., 2000). For example, in northern Australia, invasive Urochloa mutica (para grass) has been observed to decrease stream channel capacity by up to 85% (Bunn et al., 1998), increasing the frequency of overbank flows, which probably help the species to spread. 6. Remediation and amelioration of impacts Many of the changes to the structure and composition of riparian plant communities can be ameliorated through strategic management, as illustrated in the following sections. Regional species pool Limiting the transport and introduction of species through quarantine and screening would help to limit the number of alien species in the regional species pool. Assisted colonization may be used to reintroduce native species that have become locally extinct, although it would be essential to first address the cause of their initial decline. Dispersal filters Ensuring sufficient habitat connectivity is crucial formaintainingviablepopulationsofnativespecies.Physicalstructures that fragment riverine ecosystems, including structures between the riverchannelandtheriparianzone,canberemovedortheirdesignand constructionimproved(e.g.retrofittingdams(Bernhardtet al.,2005), leveebreachingandsetback(Palmeret al.,2005)).Thenumberofalien propagules, and the frequency by which they are dispersed, can be reduced through preferential use of native pasture or ornamental plants, appropriate disposal of organic waste, separation of urban or agricultural land from riparian zones with buffer strips (Catford et al., 2011), and cleaning vehicles, clothing and equipment before moving locations (Pickering & Mount, 2010). Environmental filters Recognizing the need to rectify some of the damage caused by changes in river flow regimes, the use of environmental flows (Arthington et al., 2006) and habitat New Phytologist (2014) 204: 19–36 www.newphytologist.com

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restoration (Jungwirth et al., 2002) have received growing support. Flows that restore crucial elements of the historical flooding regime should help redress the decline in native species and the increase in aliens observed in many river systems (Rood et al., 2003; Catford et al., 2011). Determining the characteristics of optimal environmental flows remains a challenge (Arthington et al., 2006) and environmental flows are not without risk (e.g. risk of invasive species spread; Howell & Benson, 2000). Biotic filters Biotic interactions can be directly addressed through the management of species populations. Limiting the decline of native species populations could involve: ensuring healthy populations of mutualists (e.g. pollinators, endophytes); limiting competition from, and predation by, alien species; and reducing species harvest, which would help to maintain ‘natural’ food web structures and trophic interactions. Invasive plant species populations can be directly managed through physical removal and biological and chemical control. Integrated approaches are often more effective than using a single technique (Rea & Storrs, 1999). Suitable control measures will vary depending on the target species, the stage of invasion, the resources available and the characteristics of the site. For example, mechanical control can be difficult in dense vegetation with poor access, and herbicide use is often restricted around waterways. As with other forms of population management, indirect impacts of alien species control should be considered in decision-making (Flory & Clay, 2009).

VI. Conclusions and future research 1. Plant traits and vegetation strategies At least 35 traits enable plants to live in riparian ecosystems (Table 1), many of which have not evolved specifically for riparian conditions. The fact that there are numerous ways of sustaining life in riparian zones (e.g. tolerating or avoiding stress) helps to explain why riparian environments can be rich in plant species despite being challenging environments to inhabit. The high heterogeneity of riparian zones makes them suitable for native and alien species with many different life strategies, representing a range of niches (Grubb, 1977). In the terminology of Grime’s (1977) CSR model, which classifies plant species into competitors, stress tolerators and ruderals, riparian zones are inhabited by stress tolerators coping with inundation, ruderal species adapted to frequent disturbance, and competitors that are able to outcompete other species where (and when) disturbance and inundation stress are low. However, many riparian species seem to possess traits that enable survival of both high stress and high disturbance, a combination of conditions that Grime (1977) saw as difficult to combine. Plant taxa such as Typha, Carex and Phragmites avoid anoxic stress by having aerenchyma and oxygenation of the rhizosphere, but they also have traits associated with disturbance adaptation, like deep and wide root systems, and vegetative reproduction. Moreover, species with high growth rates that form tall, monospecific stands (such as Typha and Phragmites) possess characteristics typical of competitors (Grace, 1988). New Phytologist (2014) 204: 19–36 www.newphytologist.com

Clearly, further research into traits of riparian species is required: to identify physiological tradeoffs pertinent to riparian environments; to determine whether there are combinations, or suites, of traits associated with different riparian plant strategies; and to test whether there are differences in the prevalence of certain plant traits and strategies among stream types and regions. Given that native and alien species are likely to come from different clades, comparing traits possessed by natives and aliens may help to distinguish between traits that facilitate survival from traits that are primitive and shared by all species in a clade. Westoby’s (1998) leaf-height-seed scheme provides an easy and tractable way to ascertain the prevalence of different CSR strategies in terrestrial environments, but a suitable scheme is not yet available for riparian zones. Because amphibious and aquatic plants require less structural support than terrestrial plants, the way in which plant height or specific leaf area should be interpreted is unclear. How should plant height be understood for species that are prostrate in terrestrial conditions, but floating when flooded? Heterophylly provides similar challenges for leaf ecophysiological measurements, as does the lack of tradeoff between seed mass and dispersal distance in hydrochores (Ikeda & Itoh, 2001). Identifying plant traits that are comparable across the different conditions and elevations within riparian ecosystems, as well between riparian and terrestrial ecosystems, is an area that is ripe for research. 2. Evolution of riparian flora The distribution of riparian traits have been mapped onto phylogenies in only few clades, so differences and similarities in trait evolution among clades remain unknown. For example, have some traits evolved more often than others? In clades with multiple adaptations, have traits evolved in a specific sequence, where possession of one trait enables acquisition of another? Are there differences in the proportion of species in regional species pools that can occupy riparian zones? In regions with humid climates, where bogs, swamps and other wet habitats are common, large proportions of the regional species pools are represented in riparian zones (Dynesius et al., 2004). Although quantitative comparisons are lacking, in more arid regions, where conditions in riparian zones differ markedly from matrix habitats, it seems that a smaller proportion of the regional species pool is able to cope with riparian conditions and these taxa tend to be confined to specific clades. Comparing the traits and phylogenetic relatedness of native and alien species will provide deeper insights into the factors that shape riparian communities. 3. Community assembly processes The distribution of plants within riparian zones, and the traits those plants possess, reflects processes that occur across all levels of the community assembly hierarchy, from the composition of the regional species pool down to local community dynamics. Most studies of community assembly processes focus on the effects of environmental filtering and biotic interactions (Weiher et al., 1998) and ways in which to disentangle them (de Bello, 2012). Despite the widely acknowledged importance of dispersal filters Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust

New Phytologist (G€otzenberger et al., 2012), relatively few studies specifically examine their effects on community assembly and the trait-based patterns that might emerge (Middleton, 2000). In this review, we found many patterns that could be explained by dispersal-related processes, highlighting the importance of regional- and landscapelevel processes in determining local species composition in riparian ecosystems. Similar to environmental filtering, dispersal filters presumably lead to underdispersion of traits related to dispersal and reproductive output. Given the prominent use of hydrochory and the strong structuring forces of flooding and inundation in riparian ecosystems, riparian zones seem to be suitable systems for studies that aim to disentangle the effects of dispersal and environmental filters. 4. Alien plant invasion and ecosystem management Relatively few alien species appear to be specifically adapted to riparian conditions, but many alien species are still able to invade riparian ecosystems. In general, a high proportion of introduced and invasive species can be classified as ruderals (Catford et al., 2012a), a suitable life strategy in ecosystems with frequent disturbance. Because early succession is not limited by competition for resources, an infinite number of species can theoretically coexist provided they are able to cope with disturbance (Catford et al., 2012a). However, as our analyses have shown, high alien species richness does not necessarily equate with high alien abundance or dominance. This is presumably because aliens are largely restricted – in space and time – to early successional patches that are usually dry (i.e. flooding and inundation in these areas would usually reset succession). Whether it is accurate to describe riparian ecosystems as highly invaded, as is often the case, depends upon the metric used and the community characteristics of interest. Hence, it is essential that suitable metrics are selected and clearly reported in studies. Understanding species invasions through the prism of community assembly can highlight the various factors that may facilitate, drive and inhibit invasion. Determining the relative importance of different filters in facilitating or limiting species invasions will help to guide suitable management responses to invasive plants, as well as other ecological problems. However, identifying the chief drivers of riparian invasion can be difficult because inferences are often based on surveys where important environmental variables are confounded (Catford et al., 2014). Hierarchical approaches that combine information about species traits with data about species distributions along environmental gradients can help to increase the diagnostic power of surveys (Catford et al., 2014).

Acknowledgements We thank Alistair Hetherington for encouraging us to write this review, Samantha Dawson for comments on an earlier draft, Shyama Pagad and the IUCN SSC Invasive Species Specialist Group who gave us access to some of the data in the GISD, Matt White and the Victorian Department of Environment and Primary Industries for permission to use their data, Mary Gardner for helping process the GISD data and Estıbaliz Palma for helping to analyse the Victorian data. We are grateful for feedback provided by the editor and three Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust

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anonymous reviewers. This work was supported by grants from the Swedish Research Council Formas (to R.J.) and the Australian Research Council (DE120102221 to J.A.C.).

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Supporting Information Additional supporting information may be found in the online version of this article. Table S1 Number of quadrats surveyed for each ecosystem type (or ecological vegetation class) in Victoria between 1970 and 2011 Table S2 Our approach for testing four hypotheses proposed to explain high degrees of riparian invasion based on characteristics of invading species Table S3 Results of a one-way ANOVA comparing the number of dispersal modes used by species that invade and do not invade riparian zones Table S4 Results of a one-way ANOVA comparing the prevalence of dispersal using water currents among species that invade and do not invade riparian zones Table S5 Results of a one-way ANOVA comparing the prevalence of human-mediated dispersal among species that invade and do not invade riparian zones Notes S1 Description of datasets and analyses regarding the degree of invasion of riparian zones Please note: Wiley Blackwell are not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing material) should be directed to the New Phytologist Central Office.

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