Nonnative plant invasions are common in environments of anthropogenic disturbance (Hobbs & Huenneke, 1992), which has led to the generalization that nonnative invaders (hereafter ‘invaders’) are most likely to outperform native species in disturbed habitats with high resource availability (e.g. Daehler, 2003). Mechanisms attributed to these disturbance-mediated invasions include broad physiological advantages of invaders over natives following episodic increases in resource availability (Davis et al., 2000). If these resource-based mechanisms are true, then invaders should exhibit advantages in functional traits that contribute to high productivity given ample resources, such as high specific leaf area, photosynthetic ability, and relative growth rate compared with native competitors (van Kleunen et al., 2010; Drenovsky et al., 2012). However, it remains unclear if invasion success in resource-limited ecosystems can be explained by mechanisms described for high-resource environments.
Over the past 15 yr, there has been substantial development of plant strategy theory and resource-use economics (Reich et al., 1997; Westoby et al., 2002; Wright et al., 2004, 2005). Wright et al. (2004) reported a global pattern of coordinated variation in leaf traits (‘worldwide leaf economic spectrum’ (LES)) that invokes general ecophysiological tradeoffs in resource economics as a global axis of variation in plant strategies. This spectrum of strategic variation describes species from those with slow returns on investments (possessing traits such as low specific leaf area, high construction costs, low photosynthetic rates, and high leaf lifespan) to those at the opposite extreme of quick returns on resource investments. Strategies that lie outside of this general LES are presumed to either be selected against (ecologically constrained by biotic interactions) or biophysically or genetically impossible (Reich et al., 1999; Donovan et al., 2011).
In an effort to understand invasion processes in light of these developments, studies have explicitly placed invasive plants along a spectrum of leaf trait variation that emphasizes coordinated variation among leaf traits (e.g. Leishman et al., 2007, 2010; Ordonez et al., 2010; Peñuelas et al., 2010; Ordonez & Olff, 2013). In particular, Leishman et al. (2010) argued that native and invasive plants share similar carbon (C) capture strategies, with invaders subject to the same tradeoffs between physiological investments and returns (i.e. constrained within the same LES). They concluded that, although invasive plants found in disturbed sites had traits that conferred greater productivity, they also experienced higher resource costs relative to natives. Therefore, invasive plants have strategies that correspond to the early successional, fast investment return portion of the LES, a conclusion used to mechanistically explain their dominance in disturbed, high-resource ecosystems (Leishman et al., 2007, 2010).
However, ecosystems subject to strong resource limitation are not immune to invasion (Martin et al., 2009), including Eastern North American (ENA) deciduous forests that experience very low light and nutrient levels during the growing season (Fridley, 2008). It is an open question as to whether invasion mechanisms described for high-resource environments, such as old fields, anthropogenic sites, and roadsides, are applicable to less disturbed ecosystems of low resource availability (Funk & Vitousek, 2007). It is generally understood that species adapted to resource-poor habitats follow strategies that place a higher premium on efficient use of resources (conservative strategies) at the expense of rapid growth (Aerts & Chapin, 1999).
Demographic studies of temperate forest tree invasions suggest that invaders do not necessarily follow demographic or life history tradeoffs evident in the native flora, such as that between low-light survivorship and high-light growth (Martin et al., 2010) and between classic r/K strategies of fast growth and reproduction versus persistence (Closset-Kopp et al., 2007). Select comparative studies, often in habitats of limited light or nutrients, report invasive plants with seemingly superior performance compared with natives at a given metabolic or resource cost, including increased growth rates (Osunkoya et al., 2010), greater mean performance or trait plasticity (Funk, 2008; Godoy et al., 2012; Paquette et al., 2012), greater photosynthetic rates at lower respiratory costs (Pattison et al., 1998; McDowell, 2002) and greater resource- or energy-use efficiencies (Baruch & Goldstein, 1999; Nagel & Griffin, 2004; Funk & Vitousek, 2007; Boyd et al., 2009). All else being equal, these findings imply that invasive species are not constrained by the same tradeoffs as natives, leading to greater production given similar resource investments. It remains unclear why these seemingly more efficient adaptations are not evident in neighboring native species. Phylogenetic constraints may exist, with certain floras never evolving certain trait combinations, which can explain how certain nonnative plants with novel resource-use strategies are superior competitors in a new range (Mack, 2003). A recent global analysis of leaf traits supports the possibility that evolutionarily distinct floras within similar biomes may have evolved different tradeoffs in resource capture strategies (Heberling & Fridley, 2012).
In ENA, the naturalized flora includes European forbs that inhabit open, managed, and disturbed sites. By contrast, invasive plants in ENA (i.e. those of highest management concern) are primarily woody species from Central and East Asia that are often invasive in forested habitats (Fridley, 2008). These shade-tolerant plants are particularly troublesome for management because their populations may increase as succession proceeds (Martin et al., 2009). In a recent common garden study of ENA forest species, Fridley (2012) found that invaders exhibit systematic differences in growth phenology, with significantly later leaf senescence for invasive species. It is unclear if any fitness advantage of an extended growing season for invasive species is equalized by tradeoffs at the leaf level such as shorter lifespan (i.e. more rapid leaf turnover) or lower daily productivity.
To test whether invasive plants in ENA forests exhibit different patterns of resource use from natives, we measured leaf-level C gains, energy and nitrogen (N) investments, and resource-use efficiencies (RUEs) of invasive and native shrubs and lianas found in ENA deciduous forests. All plants were grown in a common garden to concentrate on intrinsic trait differences, rather than those that might arise from environmental differences. We expanded upon other invasion studies (e.g. Leishman et al., 2010) to focus on phylogenetically related groups of species found in resource-limited habitats and considered both instantaneous and time-integrated traits (e.g. Funk & Vitousek, 2007). As ENA understory species are constrained by both light and N availability (Aber et al., 1993; Finzi & Canham, 2000), we hypothesized that ENA invaders should have greater C gains at lower resource costs. Therefore, we predicted that invasions in ENA forests are not attributable to greater resource use than natives per se, but rather, greater efficiency in the use of those limiting resources (i.e. greater C gains per unit resource cost).