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Ecosystem Legacy of the Introduced N2-Fixing Tree Robinia

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Ecosystem Legacy of the Introduced N2-Fixing Tree Robinia Oecologia (2013) 172:915–924 DOI 10.1007/s00442-012-2543-1 ECOSYSTEM ECOLOGY - ORIGINAL RESEARCH Ecosystem legacy of the introduced N2-fixing tree Robinia pseudoacacia in a coastal forest Betsy Von Holle • Christopher Neill • Erin F. Largay • Katherine A. Budreski • Barbara Ozimec • Sara A. Clark • Krista Lee Received: 22 September 2011 / Accepted: 22 November 2012 / Published online: 16 December 2012 Ó Springer-Verlag Berlin Heidelberg 2012 Abstract Habitat invasibility has been found to increase eliminated or reduced to less than 5 % cover by the dramatically following the alteration of ecosystem prop- hurricane. Net nitrification and extractable soil nitrate erties by a nonnative species. Robinia pseudoacacia, black concentration differed significantly between stand types, in locust, is a nitrogen-fixing, clonal tree species that the order Robinia [ former Robinia [ pine-oak. Nonna- aggressively invades open habitats and expands outside of tive species cover differed significantly between each stand plantations worldwide. Robinia pseudoacacia stands in type, in the order Robinia [ former Robinia [ pine-oak. Cape Cod National Seashore were particularly susceptible Invasion of Robinia pseudoacacia increased soil net nitri- to a hurricane in 1991 that caused widespread blowdown fication and nitrogen availability and precipitated a change and a dramatic reduction in Robinia in some stands. We in forest species composition that favored nonnative spe- used this change to investigate the lasting ecological effects cies. The presence of elevated soil nitrogen and nonnative of this nonnative species on this upland coastal ecosystem. species persisted at least 14 years after the removal of the We established replicate clusters of 20 9 20 m field plots original invading tree species, suggesting that the invasion within 50 m of each other that contained native pitch pine of a tree species left a legacy of altered soil biogeochem- (Pinus rigida) and oak (Quercus velutina, Q. alba) forest, istry, a higher number of nonnative species, and greater living Robinia stands, and stands in which Robinia was nonnative species cover. Keywords Black locust Á Facilitation Á Invasion ecology Á Communicated by Jason Kaye. Legacy effects Á Nitrogen cycling Electronic supplementary material The online version of this article (doi:10.1007/s00442-012-2543-1) contains supplementary material, which is available to authorized users. B. Von Holle (&) Present Address: Department of Biology, University of Central Florida, K. A. Budreski 4000 Central Florida Blvd., Orlando, FL 32816-2368, USA Stone Environmental, Inc., 535 Stone Cutters Way, e-mail: [email protected] Montpelier, VT 05602, USA C. Neill Present Address: Marine Biological Laboratory, The Ecosystems Center, B. Ozimec Woods Hole, MA 02543, USA Research House, 1867 Yonge St., Toronto, ON, Canada E. F. Largay Á K. A. Budreski Á B. Ozimec Á S. A. Clark Present Address: Harvard Forest, Harvard University, 324 North Main Street, S. A. Clark Petersham, MA 01366, USA 48130 Highway One, Big Sur, CA 93920, USA Present Address: K. Lee E. F. Largay Cape Cod National Seashore, 99 Marconi Site Road, Natureserve, 11 Avenue de Lafayette 5th Floor, Wellfleet, MA 02667, USA Boston, MA 02111, USA 123 916 Oecologia (2013) 172:915–924 Introduction Its ability to fix N2 and to reproduce clonally are two of the five characteristic traits of natural area invaders (Daehler Nonnative species that alter ecosystem functions are con- 1998). Robinia is thought to pose a threat to native species sidered to have the greatest impacts on native biodiversity because of its ability to form dense, monospecific stands (Mack and D’Antonio 1998; Parker et al. 1999; Vitousek that may crowd out native vegetation (Mehrhoff et al. 1990). Habitat invasibility has been found to increase 2003). For example, nonnative species richness under dramatically following the alteration of ecosystem prop- Robinia stands in the northeastern coastal US is ten times erties by a nonnative species (Mack and D’Antonio 1998). higher than under paired native stands 20 m away (Von The ecosystems that nonnative plant species have invaded Holle et al. 2006). have experienced altered fire regimes (D’Antonio and Robinia’s large effect on species composition may be Vitousek 1992), nutrient cycling (Ehrenfeld 2003), linked to its substantial effect on soil characteristics. In hydrology (Di Tomaso 1998), soil salinity (Kloot 1983; eastern forests, soils under Robinia have elevated levels of Vivrette and Muller 1977), and soil microbial communities N, P, and Ca as well as increased net N mineralization and (Liao et al. 2008; Rout and Callaway 2009; van der Putten net nitrification rates compared with adjacent native pine- et al. 2007), permanently altering ecosystems in ways that oak stands (Rice et al. 2004). In the southern Appalachians, prevent or decrease native species’ ability to persist under soils under Robinia have greater total N, organic matter, the new conditions (Maron and Jeffries 2001; Corbin and and nitrate than uneven-aged mixed oak (primarily D’Antonio 2004). Plant species capable of fixing atmo- Quercus prinus) forests (Boring and Swank 1984). In a spheric nitrogen have lasting impacts when they invade study of the effects of Robinia restoration on soil nitrogen ecosystems that are relatively poor in nutrients (Corbin and in the pine-scrub oak barrens of New York, Malcolm et al. D’Antonio 2004; Ehrenfeld 2003). Additionally, species (2008) found that soil nitrogen concentrations and net N with ecological functions that are novel to the recipient mineralization rates were reduced to levels similar to native ecosystem [e.g., fixing nitrogen (N2) where N2 fixation was stands two years after Robinia trees were physically previously low] can have the largest effects (Vitousek et al. removed from the sites and native plantings were estab- 1987; Vitousek and Walker 1989). For example, the non- lished. Additionally, net nitrification rates were signifi- native nitrogen-fixing tree Myrica faya increased soil cantly reduced in the restored Robinia stands four years nitrogen input to 23.5 kg/ha/yr from 5.5 kg/ha/yr in unin- after restoration (Malcolm et al. 2008). In the study vaded areas of young Hawaiian volcanic soils (Vitousek presented here, we aimed to examine the link between et al. 1987). The successional legacy left by this species is Robinia’s effect on soil characteristics and species com- an additional impact, with fast-growing nonnative under- position and the potential for legacy effects by Robinia, story grasses filling the gaps following the death of this following the loss of this species as the canopy dominant nitrogen-fixing overstory species (Adler 1998). due to a hurricane disturbance. The presence of individual tree species can influence the Previous land use can also alter soil chemical charac- important ecosystem process of N cycling in forest teristics and species composition across ecosystems, but ecosystems. For example, stands of sugar maple (Acer the lengths of the legacies of these effects can vary. For saccharum Marsh) have lower C:N, higher extractable soil example, widespread land tillage during the nineteenth - NO3 , and higher rates of net nitrification compared with century in the northeastern United States led to a forest tree stands of other tree species in northeastern US forests (Finzi and herb species composition that differs from that of old et al. 1998; Lovett et al. 2004; Venterea et al. 2003). These growth forests as well as secondary forests that developed differences, which indicate more rapid N cycling in sugar on land previously used only as woodlots (Bellemare et al. maple stands, can lead to changes to ecosystem functions at 2002; Eberhardt et al. 2003; Motzkin et al. 1996). In some - larger scales, such as higher NO3 watershed export in cases, the effects of previous tillage on soil characteristics stream water (Lovett et al. 2002). Changes in N availability and N cycling in reducing soil C:N, increasing soil N can also cause differences in growth rates among forest tree stocks and net N mineralization rates, and increasing species, potentially leading to long-term changes in forest nitrifying bacteria and net nitrification rates are ephemeral species composition (Zaccherio and Finzi 2007). This and do not persist beyond several decades (Compton et al. potential role for individual tree species suggests that 1998; Neill et al. 2007). In other cases, however, changes invasion by a nonnative tree species that triggers changes to to species composition, soil organic matter, and N cycling N cycling could have wide-ranging implications for both caused by alterations initiated by previous crop agriculture ecosystem biogeochemistry and species composition. may be evident for a century or more (Compton and Boone Black locust (Robinia pseudoacacia L.), hereafter 2000; Dupouey et al. 2002; Flinn and Vellend 2005; ‘‘Robinia,’’ is considered to be one of the top 100 woody Koerner et al. 1997). While it is clear that previous land use plant invaders worldwide (Cronk and Fuller 1995). can have long-lasting soil and species legacies, it is unclear 123 Oecologia (2013) 172:915–924 917 whether the invasion of a species that alters ecosystem pitch pine and oak forests across Cape Cod (Von Holle and properties can have long-lasting legacy effects. Important Motzkin 2007). questions about these legacies include (1) do changes to In July 2005 we identified twenty stands containing live soil N cycling alter forest species composition or facilitate Robinia and fifteen native forest stands comprising pre- invasion by nonnative species, and (2) how long will dominantly pitch pine (Pinus rigida), black oak (Quercus changes to soil biogeochemistry and species composition velutina), and white oak (Quercus alba)—hereafter last in the absence of the original invader? ‘‘pine-oak’’ stands—in the towns of Eastham, Wellfleet, We investigated how the invasion and then subsequent and Truro in the CCNS. We defined living Robinia stands decline in abundance of Robinia in the Cape Cod National as having[25 % living canopy cover of Robinia.
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