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Rapid environmental changes may cause plant functional traits to become mismatched with current environmental conditions. Current species distributions reflect both present ecological sorting and past selective pressures, and range expansion or survival in new geographic locations are dependent upon traits that are preadapted to the new environment. These preadaptations are likely to have competitive and evolutionary advantages, such as those observed in nonnative species with unconstrained growth and that become invasive (Mack et al., 2007) and replace native species. What is uncertain is whether the presence of nonnative species retains or changes the functionality of the previous ecosystem to the disadvantage of native species. In this paper we examine to what extent the functional traits of native and nonnative submersed aquatic plants (SAPs) are similar in an aquatic ecosystem.
One system where environmental conditions markedly constrain plant community functionality is the submersed aquatic ecosystem (Sculthorpe, 1965). Plant functional traits can be measured at metabolic, physiological and morphological levels. Functional metabolic traits include photosynthetic pathways, the substrates used for photosynthesis, and the ability to respond to varying light intensities. SAPs have constraints on photosynthesis that are imposed by carbon availability and light in the water column (Dennison et al., 1993). To cope with the low-CO2 environment in the water column, most SAPs have a carbon concentration mechanism (CCM; Maberly & Madsen, 2002) that allows them to store carbon for photosynthesis, either from CO2 or HCO3 substrates (Van et al., 1976; Sand-Jensen, 1983). The main photosynthetic pathways for SAPs are C3, often coupled with CCMs (Maberly & Madsen, 2002), and many use other photosynthetic pathways, including C4, CAM (Crassulean acid metabolism), and C3–C4 intermediates (Keeley, 1999; Ueno, 2001; Bowes et al., 2002; Keeley & Rundel, 2003). Most SAPs are restricted by light partitioning in the water column, with excess light at the surface and low light in deeper water (Dennison et al., 1993). Some SAPs are known to switch from C3 photosynthesis in the light-limited environment at depth to a C4-like photosynthesis and also in the high-light environment of the surface (Ueno, 2001). This facultative C4-like metabolism includes some of the properties of the C4 metabolic pathway, such as fixation of CO2 by phosphoenolpyruvate into malic acid (Ueno, 2001), and no activation of the xanthophyll cycle (Peñuelas et al., 1993, 1997). C4-like metabolism (Keeley, 1999; Keeley & Rundel, 2003) has been demonstrated for some SAP species, including Hydrilla verticillata (Salvucci & Bowes, 1981), Myriophyllum spicatum (Van et al., 1976), Egeria densa (Casati et al., 2000), and potentially Cabomba caroliniana (Salvucci & Bowes, 1981).
Functional physiological traits include the distribution, arrangement and composition of plant biochemical compounds (nutrients, pigments, Chl, etc.), and how these building blocks are combined to overcome environmental limitations such as submergence, high light, salinity, or temperature. Functional morphological traits include plant organs (leaves, stems, roots) and traits such as leaf : root ratios, morphology (entire and dissected leaves, fine and tap roots, etc.), and architecture (three-dimensional distributions of leaves and stems, leaf angle distribution, ratio of leaves to stem, leaf to root, etc.). At the leaf level, morphological and physiological traits of SAP leaves are often similar to shade adaptations (Mommer et al., 2005), and their typically spherical leaf angle distributions allow them to absorb diffuse light from all directions. There are three main types of leaves in submersed plants: blade-shaped leaves (strap-shaped, elongated or ribbon-like, which are associated with lentic and lotic environments); dissected leaves (deeply cut or subdivided leaves); and whorled leaves (three or more blades at each node), which are associated with lentic environments (Luther, 1947; Sculthorpe, 1965). The metabolic, biochemical, and morphological plasticity and diversity of SAPs make them particularly well adapted to varying environmental conditions, and therefore have high potential to spread into new habitats. The functionality of ecosystem processes can be affected by changes in plant community composition depending on whether nonnative species replace or change the functions that native species performed.
While remote sensing is effective at monitoring invaded plant communities over large spatial extents (Lehmann & Lachavanne, 1997; Elmore et al., 2003; Kerr & Ostrovsky, 2003; Cohen & Goward, 2004; Coppin et al., 2004; Asner & Vitousek, 2005; Bradley & Mustard, 2006), imaging spectroscopy is well established for remote detection of plant biochemistry, photosynthetic efficiency, and leaf morphology and canopy structure (Ustin & Curtiss, 1990; Peñuelas et al., 1993; Jacquemoud et al., 1994; Gamon et al., 1997; Zhang et al., 1997; Asner, 1998; Kokaly, 2001; Ollinger & Smith, 2005). Imaging spectroscopy (also called hyperspectral remote sensing) measures hundreds of contiguous narrow bands spanning the solar reflective spectrum from 400 to 2500 nm. The result is a nearly continuous spectrum measured in each pixel that provide the information needed to detect SAPs in the water column (Zhang et al., 1997; Underwood et al., 2006; Hestir et al., 2008), despite interactions with the water column itself (Holden & LeDrew, 2001; Han, 2002; Bostater et al., 2003; Hall et al., 2004), which obscures the characteristic SAP spectral patterns. When plant species are spectrally distinct (Fyfe, 2003), imaging spectroscopy is a likely method for mapping SAPs down to species level (Ustin et al., 2009). Imaging spectrometers capture spectral differences resulting from species morphological (leaf and canopy), biochemical (pigment concentration) and metabolic (photosynthesis) traits. When the analysis framework includes additional biophysical information, such as stable isotope data (Farquhar et al., 1989; Raven et al., 2002; Carvalho et al., 2009), the combination provides multiple lines of evidence to compare and contrast functionality across species.
We applied this combined approach to the SAP species that co-occur in the Sacramento–San Joaquin River Delta (henceforth referred to as the Delta) in California, USA. The Delta is one of the major gateways for nonnative aquatic species in the United States (Cohen & Carlton, 1995, 1998). In the last 30 yr the aquatic plant community has dramatically changed: the number of species has increased (Atwater et al., 1979; Cohen & Carlton, 1998; Bossard et al., 2000; Light et al., 2005; Santos et al., 2009), with the plant community composition now c. 50% nonnative plant species (Fig. 1; Santos et al., 2009). The assemblage today includes five native and four nonnative SAPs (Table 1). All nonnative species in the Delta have both the C3 pathway and a facultative C4-like metabolism (Van et al., 1976; Salvucci & Bowes, 1981; Casati et al., 2000), as does the native Elodea canadensis (Nichols & Shaw, 1986). Varied types of leaf morphologies are found in the Delta SAP assemblage. All nonnative species have wider and longer leaves than native SAP and distinct growth forms, with blade-like and dissected leaves evenly distributed along the stem length through the water column (Sculthorpe, 1965).
Figure 1. Submersed aquatic plant species co-occurring in the Sacramento–San Joaquin River Delta. The top four species are natives and the bottom four species are nonnatives. Egeria densa and Myriophyllum spicatum are invasive. Note the difference in the leaf structure among the different species: wide leaves include Potamogeton nodosus, E. densa, and Potamogeton crispus; fine leaves include Elodea canadensis, Stuckenia pectinata, and Myriophyllum spicatum; and whorled leaves include Ceratophyllum demersum and Cabomba caroliniana.
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Table 1. Submersed aquatic plant (SAP) species occurring in the Sacramento–San Joaquin River Delta, CA, USA
|Family||Scientific names||Common names||Code||Roots||Leaf||Statusa|
|Hydrocharitaceae||Egeria densa||Brazilian waterweed||EGDE||Yes||Entire, wide blade||Nonnative|
|Hydrocharitaceae||Elodea canadensis||Waterweed||ELCA||Yes||Entire, narrow blade||Native|
|Ceratophyllaceae||Ceratophyllum demersum||Coontail||CEDE||No||Dissected, whorl||Native|
|Potamogetonaceae||Stuckenia pectinata||Sago pondweed||STPE||Yes||Entire, no blade||Native|
|Potamogetonaceae||Stuckenia filiformis||Broadleaf sago pondweed||STFI||Yes||Entire, no blade||Native|
|Potamogetonaceae||Potamogeton nodosus||American pondweed||PONO||Yes||Entire, floating blade||Native|
|Potamogetonaceae||Potamogeton crispus||Curlyleaf pondweed||POCR||Yes||Entire, wide blade||Nonnative|
|Haloragaceae||Myriophyllum spicatum||Eurasian watermilfoil||MYSP||Yes||Dissected, whorl||Nonnative|
|Cabombaceae||Cabomba caroliniana||Carolina fanwort||CACA||Yes||Dissected, whorl||Nonnative|
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- Materials and Methods
- Supporting Information
Our results show that morphological differences in plant structure and biochemistry allow spectral differentiation between natives and nonnatives. While many previous studies succeeded in discriminating terrestrial species (Cochrane, 2000; Lewis, 2000; Fyfe, 2003; Andrew & Ustin, 2006; Hutto et al., 2006; Atkinson et al., 2007), the aquatic environment presents a much greater challenge to spectral differentiation (Marshall & Lee, 1994; Hestir et al., 2008). So far, only a few submerged aquatic species have been successfully differentiated (Williams et al., 2003; Dogan et al., 2009). This differentiation challenge results from linear and nonlinear mixing with water, as well as the properties of the water column itself (Williams et al., 2003; Hestir et al., 2008; Dogan et al., 2009). Our data collection was designed to reduce the known challenges of optical remote sensing over aquatic systems, which include meteorological and illumination variability, in-water radiance, and water-leaving radiance (Giardino & Zilioli, 2001; Holden & LeDrew, 2001; Bostater et al., 2003; Vis et al., 2003; Williams et al., 2003; Dogan et al., 2009). To account for meteorological and illumination variability, we specified flight times that minimized clouds and specular reflectance and we controlled for wind velocities and time of the day during data acquisition (Hestir et al., 2008). In-water radiance varies with the ratio of SAP to water in the water column, as different mixtures have different results in the amount of radiance. In the Delta there are freshwater outflows with high turbidity gradients, which mix with tidal water inflows. These dynamics make the in-water radiance highly variable during the daily tidal cycles. To reduce the effects of in-water radiance variability we restricted our analysis to pure pixels, where individual SAP species were the dominant cover in the pixel rather than water (Hestir et al., 2008). Finally, SAP contribution to water-leaving radiance is likely affected by the depth of the water column above the SAP cover (Han & Rundquist, 1997; Han, 2002). To reduce this effect we restricted our imagery collection to low-tide conditions (Hestir et al., 2008). In a parallel study testing the impact of the water column, we observed no significant deterioration of the submerged plant spectra with depth, and the water column overlying the canopy did not limit the plant detectability (Hestir, 2010).
We have shown that native and nonnative species have systematic differences in their spectral properties related to biochemistry, light use, and morphological, and structural traits, in both ‘controlled’ and natural canopies. At the leaf level, reflectance is affected by the structure of the leaf tissue and biochemistry, and the size, shape, and orientation of the leaf. Submerged leaves have a poorly differentiated mesophyll and a high frequency of epidermal chloroplasts that are likely to be under selective pressure by the reduced diffusion coefficient of carbon dioxide in water (MacFarlane & Raven, 1990), which is not offset by the use of bicarbonate in photosynthesis (Raven et al., 2005). The presence of epidermal chloroplasts that maximize light absorption by the submersed leaf (Sculthorpe, 1965) results in minimal spectral differences between species. Hence, we believe that the structure of leaf tissue may be more important to differentiate between nonsubmersed and submersed plants rather than between co-occurring submersed plants. Nonsubmersed aquatic plants have a greatly differentiated mesophyll with palisade and spongy layers, and internal anatomy similar to land plants. In fact, our results show that the only SAP species with nonsubmersed leaves, P. nodosus, is spectrally distinct from all other submersed species (Fig. 2). The leaf structure of S. pectinata is also substantially different from the other species – stems without leaf blades, allowing S. pectinata to be spectrally separated from other SAPs in the glasshouse spectrometer data (Table 2). In the landscape, however, S. pectinata occurs in very sparse canopies, which often form patches smaller than the ground pixel size of 9 m2, producing low biomass per pixel area. As a result, S. pectinata is indistinguishable from other species in the airborne data (Table 2), despite its very characteristic laboratory spectrum (Fig. 2).
Plant leaf biochemistry greatly influences reflectance (Ustin et al., 1991, 2009; Ustin et al., 2004). This factor is not totally independent of the internal leaf arrangement, as leaf optical properties often correspond to pigment concentrations (Blackburn, 2007; Ustin et al., 2009). Chlorophylls, carotenoids, and other pigments have absorption peaks at overlapping but different wavelengths (Ustin et al., 2009), between 400 and 700 nm, which were used to separate species (Table 3). Several plant pigments are instrumental in plant photosynthetic activity (Ustin et al., 2009), and differences in leaf biochemistry affect photosynthetic efficiency in moles of carbon assimilated per mole of photons absorbed.
Different leaf widths, shapes, and colors of these species may also contribute to the measured reflectance. With the exception of P. nodosus, most native species have no leaf blades, dissected leaf blades (e.g. C. demersum) or narrow blades (e.g. E. canadensis), which are distinctly different leaf morphologies from the wide blades and large dissected leaf whorls of nonnative species. These growth forms may influence the amount of light intercepted, and thus the light reflected. Our analysis showed that native species are spectrally distinct from nonnatives, which is likely a result of three convergent characteristics of nonnative species: wider ribbon-like leaves, greater leaf area per plant with higher Chl concentration, resulting in lower visible reflectance. Native and nonnative species have different reflectance in the visible region and most of the nonnative species have darker green leaves while native species are a brownish color, indicating different pigment compositions (Ustin et al., 2009). Our results corroborate this prediction as we found significantly higher pigment concentrations (Chl, carotenes and anthocyanins) in nonnative than in native species. Larger differences were found for pigments that harvest photons for photosynthesis (Chl and carotenes) than for anthocyanins. Our spectral profiles show significant differences in reflectance that match these differences in pigment concentrations. The PRI results show that potentially different pigment concentrations are present in native and nonnative species (see paragraph on 13C and PRI results). We conclude that the observed reflectance patterns are related to the interaction of shape, width and color of the leaves, which explains the separability of these species.
When scaling up from the leaf to the canopy, factors such as leaf density and canopy closure come into play. Many species are quite distinct, including most native species, such as C. demersum and P. nodosus; however, the ones most frequently confounded were the nonnative species, especially M. spicatum, P. crispus and E. densa. The canopy of the nonnative species found in the Delta tend to have higher leaf density (Fig. 1), resulting in high reflectance in the NIR (Fig. 2), and the spectral signatures are less impacted by the surrounding water. Thus, the effect of water absorption in this part of the spectrum should be less evident than measurements of canopies of native species. Furthermore, the effect of the water column as a potential confounding factor to the discriminant analysis was minimal because the imagery was acquired to avoid specular reflectance and at low tide, when most of the submersed plant canopies are at or near the surface.
Myriophyllum spicatum is overclassified (Fig. 4) and is often confused with E. densa and P. crispus, contrasting with their current Delta-wide distribution. E. densa is ubiquitous (Hestir et al., 2008), and tends to exist in most channels, in areas of moderate- and low-velocity water, shallow and deep waters, turbid and clear waters, and water with variable salinity (Santos et al., 2011). M. spicatum tends to be more restricted to somewhat deeper and more turbid waters with higher salinity (Grace et al., 2007), in the western part of the Delta. The great range of environmental conditions and species assemblages required to develop a classified map for the Delta may have washed out site-specific spectral differences between the species in the area represented in Fig. 4. While training the classifier was done to encompass the variability at the larger scale, it may have led to misclassification of the species at this finer scale. Additionally, in this region E. densa was frequently associated with epiphytic algae that could have contributed to its misclassification. In fact, the patches classified as pure E. densa did not have algal growth, while those with algal growth were misclassified.
Our results show distinct δ13C and PRI values between native and nonnative species which were less negative for nonnative than for native species, and the two metrics were strongly correlated. Our results are within the ranges of other published δ13C (Cloern et al., 2002) and PRI data (Peñuelas et al., 1993). Several confounding factors could affect the interpretation of δ13C values, especially if native and nonnative species experienced different aquatic environments. In the Delta, natives and nonnatives co-occur throughout their distribution range (Cohen & Carlton, 1995; Jassby & Cloern, 2000; Lucas et al., 2002; Santos et al., 2011), all of which occupy slower water channels, where submerged plants are associated with a Delta-wide decrease in turbidity (Hestir, 2010), through their effects on sedimentation processes. All but one native species have roots, as do all the nonnatives (Table 1), and all experience δ13C from the same water sources. Thus we believe that there is a low probability that natives and nonnatives are experiencing the δ13C environment differentially, suggesting that the observed differences are the result of physiological differences. One possible explanation for these patterns is that different CCMs result in different δ13C signals. Since most native and nonnative SAPs have CCMs (Maberly & Madsen, 2002) and the resulting δ13C signal from either HCO3 or CO2 uptake is likely indistinguishable (Riebesell & Wolf-Gladrow, 1995), we can discard this possibility as explaining the observed differences. Alternatively, nonnative species have both C3 and C4-like photosynthetic pathways (Van et al., 1976; Salvucci & Bowes, 1981; Casati et al., 2000; Maberly & Madsen, 2002), which can overcome the high-light and -temperature limitations of C3-only plants. This may give nonnatives (mostly E. densa, and M. spicatum) the ability to maintain photosynthesis under high light and high temperature, which is supported by previous studies that have demonstrated that E. densa maintains continuous growth throughout the year (Pennington & Sytsma, 2005; Pennington, 2007; Santos et al., 2011). Our results also showed less negative PRI and δ13C values for P. crispus, which may indicate the presence of a C4-like mechanism, as suggested in previous research (Sand-Jensen, 1983; Nichols & Shaw, 1986). Exceptions, however, occur for E. canadensis and C. caroliniana, which have the highest PRI values and among the lowest δ13C values, suggesting both C3 and C4-like mechanisms as shown in previous research (Salvucci & Bowes, 1981; Sand-Jensen, 1983), or in the case of C. caroliniana that high-light photosynthesis can be activated with CO2 as a substrate (Smith, 1937). Finally, Stuckenia spp. showed the lowest PRI and the highest δ13C values, potentially because these species are heterophyllous, and their canopies are formed by submerged, emergent and terrestrial leaves that have high heterogeneity in photosynthetic traits (Iida et al., 2009).
The adaptive value of having a facultative C4-like photosynthesis allows plants to colonize environments that C3-only plants cannot utilize or utilize less efficiently, such as the high-light and -temperature conditions of shallower waters, and tidal sites of increased salinity (Nichols & Shaw, 1986). These conditions are common throughout the Delta, with the exception of water with carbon (and nutrient) limitations (Jassby & Cloern, 2000; Lucas et al., 2002). This plasticity in traits may allow the nonnatives to persist and succeed in the new environment (Simberloff & Holle, 1999; Simberloff, 2001). The nonnative species can occupy the same environments in which the native species occur, but also environments where natives are not competitive, giving nonnatives an advantage by occupying a wider range of environments of the Delta. Even if remote sensing identification is limited to identifying native and nonnative submersed species, this work advances systematic measurements of specific traits that may contribute to understanding invasibility and invasion success. This is a new approach to study invasiveness and elucidate why some species are more competitive, and we hope this information will be incorporated into systems for early detection and monitoring of new and recently introduced species.