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Biotic Resistance to Exotic Invasions: Its Role in Forest Ecosystems, Confounding Artifacts, and Future Directions

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Biotic Resistance to Exotic Invasions: Its Role in Forest Ecosystems, Confounding Artifacts, and Future Directions Biol Invasions DOI 10.1007/s10530-017-1413-5 FOREST INVASIONS Biotic resistance to exotic invasions: its role in forest ecosystems, confounding artifacts, and future directions Gabriela C. Nunez-Mir . Andrew M. Liebhold . Qinfeng Guo . Eckehard G. Brockerhoff . Insu Jo . Kimberly Ordonez . Songlin Fei Received: 21 October 2016 / Accepted: 14 March 2017 Ó Springer International Publishing Switzerland 2017 Abstract Biotic resistance, the ability of communi- knowledge gaps related to biotic resistance with a ties to resist exotic invasions, has long attracted special emphasis on forest ecosystems. Overall, interest in the research and management communities. although the amount of research efforts on biotic However, inconsistencies exist in various biotic resis- resistance in forest ecosystems has increased since the tance studies and less is known about the current status mid-2000s, aspects such as resistance to exotic pests and knowledge gaps of biotic resistance in forest and pathogens remain understudied. In addition, we ecosystems. In this paper, we provide a brief review of synthesize ecological and statistical explanations of the history and mechanisms of the biotic resistance observed inconsistencies and provide suggestions for hypothesis, and summarize the central topics and future research directions. Some of the observed inconsistencies on biotic resistance can be attributed to (1) the interactive or additive effects of other Guest Editors: Andrew Liebhold, Eckehard Brockerhoff and ecological processes and (2) the statistical artifacts of Martin Nun˜ez / Special issue on Biological Invasions in Forests prepared by a task force of the International Union of Forest modifiable areal unit problem. With the advancement Research Organizations (IUFRO). of new statistical knowledge and tools, along with availability of big data, biotic resistance research can Electronic supplementary material The online version of be greatly improved with the simultaneous consider- this article (doi:10.1007/s10530-017-1413-5) contains supple- mentary material, which is available to authorized users. ation of key ecological processes, the attention to various scales involved, and the addition of under- G. C. Nunez-Mir Á I. Jo Á K. Ordonez Á S. Fei (&) studied systems. Department of Forestry and Natural Resources, Purdue University, West Lafayette, IN 47907, USA Keywords Competition Facilitation Modifiable e-mail: [email protected] Á Á area unit problem Á Pests Á Pathogens A. M. Liebhold USDA Forest Service Northern Research Station, Morgantown, WV, USA Introduction Q. Guo USDA Forest Service Southern Research Station, The numerous ecological, economic and social Research Triangle Park, NC, USA impacts of invasive exotic (alien, nonnative, or introduced) species have compelled major interest in E. G. Brockerhoff effective approaches to mitigate their establishment Scion (New Zealand Forest Research Institute), Christchurch, New Zealand and spread. In particular, research has focused on the 123 G. C. Nunez-Mir et al. intrinsic ability of communities to resist or control processes. We further describe the ecological pro- invasions—a phenomenon termed biotic resistance. cesses and statistical artifacts that may be causing the Interest in biotic resistance can be traced back to early observed inconsistencies by masking the effects of ecology (Elton 1958; MacArthur 1955, 1972), which biotic resistance. We end our review by proposing proposed that as the number of species in a community multiple fronts for future research to advance our increases, more niche spaces are occupied and understanding of biotic resistance. resources are more fully utilized, therefore enhancing the community’s competitive resistance to invasion. Understanding the degree and mechanisms of biotic Mechanisms of biotic resistance resistance has important ecological and conservation implications for it provides useful information for the Competition has been the most widely studied mech- identification of communities that may be at risk of anism of biotic resistance, particularly in the plant being invaded. Moreover, an understanding of biotic invasion literature. In-depth theoretical and empirical resistance can guide management efforts to enhance a studies of the mechanisms of competition show that community’s ability to control established invaders or native plants are able to decrease the performance of resist future ones (Funk et al. 2008). However, as biotic exotic plant species through direct reduction in resistance research advances, it has become clear that available space, light and nutrients (i.e., niche com- this phenomenon is much more complex than plementarity). For instance, Maron and Marler (2007) expected. Native species are able to interact with found that assemblages with higher plant species exotics in multiple ways that either decrease or richness not only displayed decreased soil moisture, increase the probability of exotic establishment and light and nitrogen availability, but also lower invasi- spread. Inconsistencies among research findings on bility than assemblages with lower species richness. how biological diversity impedes invasion success, Byers and Noonburg (2003) found that the sum of both within and across scales, further muddle our interspecific competitive effects in their competition understanding (Fridley et al. 2007). Moreover, intrin- model were a major driver of invasibility when sic ecosystem characteristics and underlying mecha- resources were held constant. Indeed, the strength of nisms that shape community composition and structure competitive resistance in plant communities has been have been found to influence the ability of native found to be closely related to abiotic factors, namely communities to resist invasion (Alofs and Jackson resource availability (Going et al. 2009; Shea and 2014; Kimbro et al. 2013; Smith-Ramesh et al. 2016). Chesson 2002). However, due to spatio-temporal Because different ecosystems vary with regard to variability in resource availability an exotic plant climate conditions, trophic levels, and interactions invader can still overcome competitive resistance by among resident species that can affect the biotic possessing an advantage over resident species at a resistance of the ecosystem (Fraterrigo et al. 2014; given time or location (Shea and Chesson 2002). Smith-Ramesh et al. 2016), current knowledge on Although there is a heavy focus on competition as a biotic resistance may be biased toward specific mechanism of biotic resistance, native communities ecosystems and thus may be inadequate for general- are able to resist invasion through other ecological izations across ecosystems. For example, species with processes, such as consumption (i.e., herbivory and early successional traits and adaptation to disturbance predation) and pathogeny. One of the earliest com- are strong invaders in grassland communities, but prehensive reviews of various mechanisms of biotic under vastly different environmental conditions and resistance compared the effects of competition, the disturbance regimes in forests, invaders require a diversity of resident competitors, herbivory and soil different set of traits and adaptations (e.g., shade- fungal communities on exotic plant establishment and tolerance) (Martin et al. 2009). performance through a meta-analysis of 52 biotic Here, we review and describe various interactions resistance studies (Levine et al. 2004). The meta- between native and exotic species that diminish analysis showed that competition, herbivory and invasion success (i.e., mechanisms of biotic resis- competitor diversity had strong effects on invader tance). We then review forest-specific biotic resistance establishment and performance. Evidence on the literature, in order to elucidate system-specific effects of mycorrhizal fungi and fungal pathogens, 123 Biotic resistance to exotic invasions on the other hand, showed inconsistent trends, high- 60 lighting the species-specific nature of pathogeny as a mechanism of biotic resistance. 50 Other Forests While the individual effect of these mechanisms is Grasslands 40 relatively well studied, the interactive and additive Aquatic effects of these mechanisms in conferring biotic 30 resistance is considerably less understood. Biotic resistance may be conferred indirectly, through inter- 20 actions that alter the abundances of species that do Number of articles interact directly with the exotic invader. Mitchell et al. 10 (2006) propose a theoretical framework to assess and quantify the interactive effects of two species of 0 enemies, mutualists, or competitors on an introduced 1994 1996 2004 2008 2012 1988 1990 1992 1998 2000 2002 2010 2014 2016 plant. 2006 Furthermore, we are beginning to understand how Fig. 1 Increase over time of the number of research articles intrinsic differences among ecosystems influence focused on biotic resistance per year. Stacked bars indicate the biotic resistance mechanisms, and consequently the number of articles each year specific to an ecosystem type relative importance of each mechanism in any given (aquatic, grasslands, forests, other). The number of articles in 2016 are an estimate given the trends observed per month from ecosystem. Studies have shown important differences January to June, when the literature retrieval took place between marine, freshwater, and terrestrial ecosys- tems. Consumptive resistance appears to be a much strongly in the literature. Forest ecosystems were not stronger mechanism of biotic resistance than compe- particularly
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