Allelopathic Invasive Tree (Rhamnus Cathartica) Alters Native Plant Communities
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Allelopathic invasive tree (Rhamnus cathartica) alters native plant communities R. J. Warren, Adam Labatore & Matt Candeias Plant Ecology An International Journal ISSN 1385-0237 Volume 218 Number 10 Plant Ecol (2017) 218:1233-1241 DOI 10.1007/s11258-017-0766-2 1 23 Your article is protected by copyright and all rights are held exclusively by Springer Science+Business Media B.V.. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy Plant Ecol (2017) 218:1233–1241 DOI 10.1007/s11258-017-0766-2 Allelopathic invasive tree (Rhamnus cathartica) alters native plant communities R. J. Warren II . Adam Labatore . Matt Candeias Received: 23 February 2017 / Accepted: 1 September 2017 / Published online: 4 September 2017 Ó Springer Science+Business Media B.V. 2017 Abstract Many plants release allelopathic chemi- test if patterns observed in the field could be explained cals that can inhibit germination, growth, and/or by adding increased dosages of R. cathartica to soils survival in neighboring plants. These impacts appear containing five plant species, including native and magnified with the invasion of some non-native plants non-native woody and herbaceous species. In the which may produce allelochemicals against which highly invaded urban forest, we found that herbaceous native fauna have not co-evolved resistance. Our cover, shrubs and woody seedlings negatively covar- objective was to examine the potential allelopathic ied with R. cathartica basal area and seedlings density. impact of an invasive non-native shrub/tree on mul- In the mesocosm experiments, R. cathartica resulted tiple plant species using field observation and exper- in significant decreases in plant community species imental allelopathy studies. We surveyed and richness, abundance, and shifted biomass allocation collected an invasive, non-native tree/shrub (Rhamnus from roots. Our results provide evidence that R. cathartica) at Tifft Nature Preserve (a 107-ha urban cathartica is highly allelopathic in its invaded range, natural area near Lake Erie in Buffalo, NY). We also that R. cathartica roots have an allelopathic effect and surveyed understory plant communities in the urban that some plant species appear immune. We suggest forest to examine correlations between R. cathartica that these effects may explain the plant’s ability to abundance and local plant community abundance and form dense monocultures and resist competitors, as richness. We then used experimental mesocosms to well as shift community composition with species- specific impacts. Communicated by Luke Flory. Keywords Allelopathy Á Phytotoxicity Á Recruitment Á Urban ecology R. J. Warren II (&) Department of Biology, SUNY Buffalo State, 1300 Elmwood Ave., Buffalo, NY, USA e-mail: [email protected] Introduction A. Labatore U.S. Army Corps of Engineers, Washington, DC, USA e-mail: [email protected] Plants release secondary chemical compounds (not essential for growth, reproduction, and survival) that M. Candeias deter and inhibit herbivores and other plants; the Department of Natural Resources and Environmental Sciences, 1102 Goodwin Ave., Urbana, IL, USA deleterious effect on other plants is called allelopathy e-mail: [email protected] (Rice 1984). Allelopathic plants release phytotoxic 123 Author's personal copy 1234 Plant Ecol (2017) 218:1233–1241 chemicals into the soil environment through root and (Archibold et al. 1997; Klionsky et al. 2011; Seltzner leaf leachate that can inhibit the germination, growth, and Eddy 2003), though these effects require substan- and/or survival of neighboring plants (Fernandez et al. tiation (Knight et al. 2007). Rhamnus cathartica 2016; Lankau 2011; Orr et al. 2005). Some invasive leaves and fruit demonstrably reduced germination plants appear to gain considerable advantage in novel in some native and ornamental species, but R. ecosystems because they produce phytotoxic allelo- cathartica bark and roots did not, and the effects chemicals against which invaded-range native species appeared species specific (Klionsky et al. 2011; may not have co-evolved resistance (Callaway and Knight et al. 2007). Hence, R. cathartica allelopathic Ridenour 2004; Fernandez et al. 2016; Pisula and effects may depend on its tissue type, and the Meiners 2010; Thorpe et al. 2009). As a result, some effectiveness may depend on the identity and life invasive plants may form dense monocultures where stage of the target species. native plants cannot compete well. Our objective was to examine the allelopathic European or common buckthorn (Rhamnus cathar- impact of an invasive non-native shrub/tree on plant tica L.) is a shrub/small tree native to most of Europe species using field observation and experimental and Western Asia that appears restricted to open and allelopathy studies. Given the known allelochemical edge habitats in its native range but is able to invade content, and predicted allelopathic effects, of R. forest understories and dominate native ecosystems cathartica, we predicted that increased soil amend- which were introduced in northern North America ments with R. cathartica leaf and root tissues would (Knight et al. 2007; Kurylo and Endress 2012). The inhibit plant germination and growth in five woody shrub forms dense thickets that correspond with and herbaceous plant species. noticeable declines in native plant abundance and diversity (Archibold et al. 1997; Boudreau and Wilson 1992; Mascaro and Schnitzer 2007). The cause and Methods effect between R. cathartica and native plant commu- nities remains unclear, however, as the shrub appears Study site as an opportunist, which employs multiple potential competitive mechanisms. Rhamnus cathartica toler- The Tifft Nature Preserve is a 107-ha urban natural ates a poor habitat (e.g., dry, shady), and it germinates, area located on the shore of Lake Erie in Buffalo, NY grows and reproduces vigorously in disturbed habitats (U.S.). The landscape was used for industrial and where sunlight is plentiful (Gavier-Pizarro et al. 2010; residential refuse, and turned into a natural area in the Knight et al. 2007; Moffatt and McLachlan 2004). 1970s. The preserve contains deciduous forest (dom- Still, R. cathartica invasion success may not be just inated by Populus deltoides W. Bartram ex Marshall), opportunistic. The shrub leafs out earlier and thus is wetlands, and open fields. able to photosynthesize longer than co-occurring native species, allowing invasion into canopy under- Forest survey data collection story, and it produces copious seed-bearing fruits that are dispersed by birds and mammals (Godwin 1936; Herbaceous and woody plants were surveyed in the Harrington et al. 1989). Tifft woodlands and grasslands in August 2013. Three Rhamnus cathartica also produces secondary com- random transects were established in each of these two pounds that alter soil chemistry, deter native herbi- habitats (n = 6 transects); all were 500 m long except vores, and appear to suppress native flora and fauna one woodland transect which was 250 m long due to (Grunzweig et al. 2015; Heneghan et al. 2006; forest shape. Plots were established at 50-m intervals Klionsky et al. 2011; Schuh and Larsen 2015; Seltzner (n = 55 plots). Areas with active management and and Eddy 2003; Trial Jr. and Diamond 1979). In edges were avoided by moving plots 50 m. Total particular, phytotoxic compounds leached from the herbaceous percent cover and species richness, as well bark, leaves, stems and fruit—including emodin and as woody seedlings (\1 cm dbh), were measured in other anthraquinones, tannins, and flavonoids (see 1m2 subplots (n = 55). For woody species, each plot Izhaki 2002 and references therein)—may suppress was sampled using the point-center quarter technique the germination, survival and growth of other plants (n = 51, Cottam and Curtis 1956) at the same 50-m 123 Author's personal copy Plant Ecol (2017) 218:1233–1241 1235 intervals along the transects. Point-center quarter is a NC (USA) in 2013 and stored in a dry cabinet. The P. long-used forest sampling protocol in which a random strobus, S. oolentangiense, and L. cylindracea seeds point is selected, a compass used to divide the area into were cold stratified at 4.5 °C for 60 days; the other quadrants and the nearest tree ([11.7 cm dbh) and seeds were not cold stratified. shrub (\11.7 cm dbh) located, and identified, and dbh Ten mesocosms were designated for each of the (stem diameter at 1.4 m height) measured in each four treatments (and a control) [n = 50 total]. The quadrant. mesocosms were placed under full spectrum growth lights and warmed to 21.5 °C using seed heating pads Forest survey data analysis to encourage germination. The location of each mesocosm was randomized and shifted under different We examined 1-m2-subplot-level variation among grow lights once per week. After 12 weeks, all plants herbaceous cover (%) and herbaceous species rich- were harvested, above- and belowground matter ness, and point-quarter-plot-level tree richness, shrub separated, and dried for 3 days at 15 °C before richness, woody seedling density (stems Á m-2), R. weighing. The species that germinated survived until cathartica basal area (stem basal area * stem density), the end of the experiment. tree basal area, shrub basal area, and R. cathartica basal area using principal component analysis (PCA) Mesocosm data analysis using the ‘‘prcomp’’ method and ‘‘scale’’ option (standardizes all variables to unit length) in the ‘‘R’’ We evaluated the R.