Rhamnus Cathartica: Native and Naturalized Distribution and Habitat Preferences1

November 24, 2007

By Kurylo, J S Knight, K S; Stewart, J R; Endress, A G

KURYLO, J. S. (Division for Ecology and Conservation Science, Illinois Natural History Survey, Champaign, IL 61820), K. S. KNIGHT (USDA Forest Service Northern Research Station, Delaware, OH 43015 and Department of Ecology, Evolution, and Behavior, University of Minnesota, 100 Ecology Building, 1987 Upper Buford Circle, St. Paul, MN 55108), J. R. STEWART (Department of Natural Resources and Environmental Sciences, University of Illinois at Urbana-Champaign, Urbana, IL 61801), AND A. G. ENDRESS (Department of Natural Resources and Environmental Sciences, University of Illinois at Urbana-Champaign, Urbana, IL 61801 and Division of Biodiversity and Economic Entomology, Illinois Natural History Survey, Champaign, IL 61820). Rhamnus cathartica: native and naturalized distribution and habitat preferences. J. Torrey Bot. Soc. 134: 420-430. 2007.- Rhamnus cathartica L. is a large shrub or small tree native throughout much of Europe and eastern Asia, but invasive in North America. In this review, the current native and invasive distributions of R. cathartica are documented and possible factors limiting its naturalized distribution are considered. Within its broad distribution, R. cathartica occurs in diverse habitats ranging from urban forests to fens. Rhamnus cathartica is shade tolerant, prefers disturbed areas with moist, but not saturated, soils and may have an affinity for alkaline soils high in calcium carbonate. Key words: buckthorn, calciophile, distribution, disturbance, Rhamnus cathartica, soil moisture.

The genus Rhamnus L. is a member of the Rhamneae tribe, one of twelve recognized tribes in the cosmopolitan family Rhamnaceae (Richardson et al. 2000). It is one of 11 genera of Rhamnaceae possessing two to four seeds per fruit (Medan and Schirarend 2004). There are approximately 100 (Medan and Schirarend 2004) to 125 (Mabberley 1997) Rhamnus species worldwide; in North America there are eight native (Johnston and Johnston 1978, Hickman 1993) and 12 introduced species (Gil-Ad and Reznicek 1997). Rhamnus species are typically found in temperate and subtropical climates of the Northern Hemisphere (Richardson et al. 2000, Bolmgren and Oxelman 2004) with greater representation in the tropics of the Old World than in the Neotropics (Johnston and Johnston 1978).

Rhamnus cathartica L. is within the series Catharticae of the large section Cervispina (Grubov 1949), which is characterized by species with true thorns (Bolmgren and Oxelman 2004). Rhamnus cathartica is the type species of the genus Rhamnus (Britton and Brown 1970). It has many historical and regional common names: Rhineberry, waythorn, Kreuzdorn (cross thorn), European buckthorn, purging buckthorn, Hart’s thorn, Christ’s thorn, rainberry, Rhinethorn and common buckthorn (Godwin 1943, Gorham 1944, Gurney 1958, Britton and Brown 1970, Rehder 1927, Hegi 1965).

Charcoal deposits from early human fires facilitate reconstruction of historic vegetation. The earliest evidence of Rhamnus in Europe comes from such deposits. Wood, stems, fruits, and charcoal of R. cathartica have been identified in the British Isles from the Neolithic age (Clark et al. 1935, Phillips 1935) and charcoal samples from the French Pyrenees indicate the presence of several species of Rhamnus, including R. cathartica, which existed in open shrub communities during the late glacial interstadial period, between 13,000 and 11,320 +- 410 years before present (YBP) (Heinz and Barbaza 1998). Around 10,770 +- 100 YBP, as the climate of Europe warmed from that interstadial period, Rhamnus species became more abundant. With the establishment of deciduous oak forests in the postglacial period 9700 +- 80 YBP, Rhamnus populations began to decline (Heinz and Barbaza 199.8).

While the physiology and ecological relationships of Rhamnus cathartica have been reviewed elsewhere (Knight et al. in press), the large-scale distribution and smaller-scale habitat preferences have not been fully explored in published literature. In this review, hybridization and habitat preferences are discussed, a distribution is complied for native and naturalized ranges based on available literature, and future research needs are identified for R. cathartica.

Description of Plant and Hybridization. Rhamnus cathartica is a deciduous shrub or small tree with nearly opposite branches often ending in short thorns (Wolf 1938). The thin bark is gray and becomes fissured with age (Godwin 1943, Young 1994). The simple green leaves are ovate to elliptical (Rehder 1927) with a sub- opposite to alternate arrangement (Soper and Heimburger 1982). Flowers are green, small, inconspicuous, and pollinated by insects. Flowering occurs between April and May and drupes ripen to a purplish black between September and October. Reproduction is entirely sexual (Godwin 1943).

Rhamnus cathartica is a polymorphic species within its native range (Sokolov 1958), particularly within the southern range of its native distribution (Grubov 1949, Sokolov 1958). The large degree of intraspecific morphological variation may be due to the capability of the taxon to naturally hybridize with other species within the section Cervispina (Grubov 1949, Sokolov 1958, Gil-Ad and Reznicek 1997). The native distributions of nearly 42 Rhamnus species overlap or co-occur (Grubov 1949); many can purportedly hybridize with R. cathartica, including Rhamnus utilis Decne. (Grubov 1949, Gil-Ad and Reznicek 1997), Rhamnus tinctoria L. (Grubov 1949), Rhamnus saxatilis Jacq. (Grubov 1949), Rhamnus pallasii Fisch. & C. A. Mey (Grubov 1949), Rhamnus spathulifolia Fisch. & C. A. Mey (Grubov 1949, Sokolov 1958), and Rhamnus villarsii (Grubov 1949, Sokolov 1958).

Distribution. EURASIAN DISTRIBUTION. Rhamnus cathartica is native to Europe and the northern and western parts of Asia (Bean 1914, Rehder 1927, Steyermark 1963, Davis 1967) (Fig. 1). The northern range limit is southern Scandinavia below 61[degrees]40′ (Godwin 1943, Grubov 1949, Clapham et al. 1987) and 56[degrees]40′ in western Siberia (Shishkin and Bobrov 1949), where it reaches its most eastern extent at the Ob River (Sokolov 1958) and northwestern China (Yilin and Bangkai 1982). The southern limits appear to be northern Afghanistan, Iran, and Turkey and northeastern Spain (Godwin 1943, Grubov 1949, Davis 1967, Browicz 1984). Rhamnus cathartica is found sparingly at high altitudes in northern Algeria and Morocco (Druce 1932, Godwin 1943, Clapham et al. 1987, Browicz 1984). It is absent from the Balearics, Corsica, Sardinia, islands of the Aegean Sea, and possibly southern Greece (Godwin 1943, Grubov 1949, Browicz 1984). Species with large native ranges tend to be invasive (Petit et al. 2004) and many subsequently have large invaded ranges (Rejmanek 1996).

NORTH AMERICAN DISTRIBUTION. In North America, Rhamnus cathartica is naturalized throughout the north eastern and northcentral USA (Keller and Brown 1905, Tatnall 1946, Steyermark 1963, Wherry et al. 1979, Gourley 1985, Dorn 1984, Voss 1985, Great Plains Flora Association 1986, Mitchell 1986, Ownbey and Morley 1991, Eilers and Roosa 1994, Swink and Wilhelm 1994, Cooperrider 1995, Catling 1997, Cronquist et al. 1997, Magee and Ahles 1999, Dorn 2001, Jones 2005; R. Caul, and C. Morse, pers. comm.) and southern and eastern Canada (Scoggan 1978, Soper and Heimburger 1982, Moss 1983) (Fig. 2). The species is most abundant from southern Quebec and Ontario (Archibold et al. 1997) into New England (Magee and Ahles 1999), southern Michigan (Voss 1985) and Wisconsin (Gourley 1985), southeastern Minnesota (Ownbey and Morley 1991), and northern Illinois (Spyreas et al. 2004) and Iowa (Eilers and Roosa 1994). Rhamnus cathartica is uncommon on or north of the Canadian Shield, a geological formation of bare Precambian Era rock, in Canada (Soper and Heimburger 1982). Within its invaded range, it is difficult to map the finescale distribution or abundance of R. cathartica within states and provinces because complete and up-to-date information at the county level is mostly unavailable. The recent inclusion of shrubs and herbaceous plants, including R cathartica, into the U.S. Forest Service Forest Inventory and Analysis (FIA) National Program (USDA Forest Service 2007) will be very helpful in assessing abundance and understanding the fine-scale distribution of these plants in the USA. Data from the FIA phase 3 plots, which will be made available soon, will be useful for land management decisions.

FIG. 1. The native range of Rhamnus cathartica based on complied literature.

At the margins of its distribution, naturalized R cathartica may be infrequent (Steyermark 1963, Scoggan 1978, Maw 1981, Dorn 1984, Lackschewitz 1991, Moss 1983, Archibold et al. 1997, Cronquist et al. 1997, Jones 2005; E. Lane, C. Morse, and C. Seibert, pers. comm.). In Colorado, for example, it escaped from cultivation into nearby gulches north of the Denver metropolitan area (Weber and Wittmann 1996; E. Lane, pers. comm.). In Montana, naturalized specimens are present in two counties, but more than half of the counties have cultivated specimens (C. Seibert, pers. comm.).

Naturalized populations of R. cathartica are undetermined in Maryland and Tennessee. While Brown and Brown (1972) reported the taxon as “becoming naturalized” in Maryland, the University of Maryland Norton-Brown Herbarium (MARY) currently contains only pressed specimens of cultivated plants (C. Delwiche, pers. comm.). Herbaria from both the University of North Carolina (NCU) and University of Tennessee (TENN) list a single record for an uncultivated specimen of R. cathartica in Tennessee (University of Tennes see Herbarium and Austin Peay State University 2002, Liu et al. 2005), but recent books on Tennessee plants do not mention it (Wofford and Krai 1993) or consider it cultivated and/or persistent (Wofford and Chester 2002). FIG. 2. The North American naturalized range of Rhamnus cathartica based on complied literature.

In West Virginia, Rhamnus cathartica is not confirmed as naturalized and specimens are only documented in one county (Harmon et al. 2006; P. Harmon, pers. comm.). The previous record of R cathartica in Virginia was apparently based on a misidentified Rhamnus davurica Pallus specimen (Virginia Botanical Association 2005, Weakly 2005). The PLANTS database (USDA 2007) lists R. cathartica as occurring in North Carolina, Idaho, and California, but evidence of naturalized R cathartica could not be found in the literature or by searching herbarium databases to support the listing of these three states (Hickman 1993, Weakly 2005; S. Robins, pers. comm.).

By combining the naturalized distribution of Rhamnus cathartica with climate, soil, and geological information, a potential boundary of its spread can be determined (Gourley 1985). To the north, the naturalized range appears to be generally limited by spodic soils (i.e., acidic soils commonly associated with coniferous forests), duration of temperatures too cold for flowering and seed set, and possible winter-kill temperatures. The Rocky Mountains and arid Great Plains appear to be the western boundary of the naturalized range of R. cathartica, with the Atlantic Ocean as its eastern boundary. To the south, the distribution of R. cathartica is likely limited by a lack of basic soils (i.e., the soils are too acidic) (Gourley 1985).

How will climate change, which is predicted to alter temperature and moisture patterns, affect the spread of Rhamnus cathartica within its invaded range? One might theorize that R cathartica would advance northwards in areas where winter temperatures become less severe and growing seasons lengthen, as has been predicted for other tree species (Iverson et al. 2005). At least for eastern North America, however, the composition of the substrate comprising the Canadian Shield region may continue to impose a geological barrier to the species ability to dominate woodlands as it does now. Range data appear to imply R cathartica is unable to invade forests in semitropical to tropical climates, which may point to a northerly advance of its southern extents as the North American climate warms. Changes in moisture toward wetter climates may favor R. cathartica, while drought may limit it.

Table 1. Reported Eurasian habitats of Rhamnus cathartica.

Habitat Preferences. The local distribution of Rhamnus cathartica depends on many factors, including moisture, soil properties, proximity to urban areas, and disturbance. The ability of R. cathartica to tolerate a wide range of conditions is evidenced by its occupation of diverse habitats (Sokolov 1958), ranging from steep ravine slopes (Sokolov 1958) to fens (Godwin 1943) in both Eurasia (Table 1) and North America (Table 2). Several life history and ecophysiological traits enable R cathartica to be successful in various environments (Knight et al. in press).

SHADE TOLERANCE. In its native range, R. cathartica is usually found in open areas or forest edges (Gassmann 2005, L. C. Skinner and J. Oleksyn pers. comm.). In its invaded range, it is not only found in the interiors of woodlands (Gourley 1985, Leitner 1985, Heneghan et al. 2004), but it thrives in shady understory conditions (Archibold et al. 1997). Its shade tolerance was demonstrated by high survival (80-100%) of potted seedlings grown in low-light conditions (0.3 to 2% of full sunlight) in controlled experimental conditions (Grubb et al. 1996; K. S. Knight and P. B. Reich, unpubl.).

Although Rhamnus cathartica tolerates shade, optimum growth occurs at intermediate light levels (Gourley and Howell 1984). In an experiment where seedlings of R. cathartica were grown in a forest understory for three years across a gradient from 1 to 16% midsummer canopy openness, seedling biomass in highest-light environments was nearly two orders of magnitude greater than in the lowest-light environments (Knight 2006). Reduced growth of R. cathartica at very low light levels (Gourley 1985, Knight 2006) suggests the very deep shade of forests dominated by maple (Acer spp.), pine (Pinus spp.), or boreal species may limit R. cathartica invasion (Gourley 1985). In a survey of Wisconsin forests, R. cathartica shrubs were also found to be most abundant in vegetation types with greater light penetration (Leitner 1985).

Rhamnus cathartica exhibits its most rapid growth rates in open areas (Harrington et al. 1989, Wyckoff et al. 2005, Gourley and Howell 1984), although desiccation and competition from other plants in open areas may restrict it to lightly shaded areas in savannas (Wyckoff et al. 2005). Waterlogging, however, may restrict its occurrence in open wetlands (Gourley 1985). A more comprehensive discussion of the population ecology and ecophysiology of shade tolerance for R. cathartica can be found in Knight et al. (in press).

Table 2. Reported North American habitats of Rhamnus cathartica.

SOIL MOISTURE. Reported soil-moisture preferences of Rhamnus cathartica range from dry to moist in both European and North American habitats. Several reports state that R. cathartica prefers dry soils (Wolf 1938, U.S. Forest Service 1948, Billington 1949, Sokolov 1958, Britton and Brown 1970, Moor 1981), but others restrict this preference by stating that it avoids dry, exposed (Godwin 1943), or sandy (Archibold et al. 1997) places. Rhamnus cathartica is also reported to grow well in both moist and dry habitats (Tansley 1939, Godwin 1943, Soper and Heimburger 1982, Browicz 1984, EUenberg 1988).

However, there is evidence that optimal growth of Rhamnus cathartica occurs in moist soil conditions. A high germination rate, seedling survivorship, and abundant populations were associated with moist, non-saturated, or poorly drained soils in field surveys (Mulligan 1952, Gourley and Howell 1984, Gourley 1985, Gill and Marks 1991, Wyckoff et al. 2005). At the University of WisconsinMadison Arboretum, for example, R cathartica was abundant on poorly drained soils and grew most vigorously in open and wet areas (Gourley and Howell 1984). In the same arboretum, R. cathartica saplings in less-waterlogged parts of wetlands and wet woods grew faster than those in adjacent drier woods (Gourley 1985). In England, a high winter water table limited R. cathartica colonization of some fen areas (Godwin and Bharucha 1932), but the species became more dominant in less waterlogged parts of the fen (Godwin et al. 1974). Hegi (1965) made the same observation for Central Europe, where R. cathartica avoided the wettest parts of the fens. Growth of R. cathartica was less inhibited under stagnant water conditions than well-drained conditions in a controlled field experiment (Frye and Grosse 1992). Upon exposure to partial flooding, R. cathartica showed leaf epinasty and reduced photosynthetic rates, but was able to adjust as evidenced by recovery of photosynthesis and normal shoot development in a greenhouse study (Stewart and Graves 2004).

Despite its reported presence in wet habitat types (Tables 1, 2), Rhamnus cathartica is not considered a hydrophyte in the USA based on its wetland indicator statuses, as assigned by the U.S. Fish and Wildlife Service (USFWS) (Reed 1988). To delineate jurisdictional wetlands in the USA, plant and animal species are assigned to a wetland indicator category representing their frequency of occurrence relative to local landscape hydrology in each of 12 regions where the species occurs (Environmental Laboratory 1987). The current wetland indicator status of R. cathartica ranges from facultative upland (FACU) (i.e., usually found in non-wetlands) in the Midwestern U.S. to upland (UPL) (i.e., occur in wetlands of other regions, but under natural conditions almost always occur in non-wetlands) in the northeastern USA (Reed 1988). Overall, this implies that R. cathartica across the landscape should be found in wetlands 33% of the time or less. A facultative negative (FAC-) indicator status (i.e., found in wetlands, but not as frequently as a facultative species) may be more appropriate for R. cathartica in the Midwestern USA (Eggers and Reed 1997). Indeed, most reports of R. cathartica occurring in wetlands are from that region (White 1965, Curtis 1971, Gourley 1985, Eggers and Reed 1997, Lindig- Cisneros and Zedler 2000; Kurylo, unpub. data). The 1996 draft revisions for wetland indicator statuses list FAC- for R. cathartica within part of the Northeast Region (the Great Lakes Plain subregion of Ohio, Pennsylvania, and New York) and the whole of the North Central Region (covering Illinois, Iowa, Indiana, Michigan, Minnesota, Missouri, and Wisconsin) (U.S. Fish and Wildlife Service 1996). This change would not classify R. cathartica as a hydrophyte (Reed 1988). For wetland delineators and regulators, this change would not change the status of jurisdictional wetlands containing R. cathartica, but would increase the number of potential wetland sites considered in surveys. This change may also be useful for organizations that work to restore or rehabilitate degraded environments by indicating a more gradual transition from upland to wetland habitats versus a more sudden change, as is reflected in the current USFWS indicator status for R cathartica.

Rethinking the hydrological landscape associations of Rhamnus cathartica may enable us to identify a potential wetland invader, but also raises several questions. Are R. cathartica populations in the Midwestern USA somehow ecologically distinct (e.g., an ecotype) from other populations elsewhere within its invaded range? Has the species been unreported from wetter habitats outside of the Midwestern USA? If there are true population differences, are the differences attributable to a difference, if any, between native seed sources? For instance, R. cathartica behaves differently on the European continent than it does in England, where it forms nearly monospecific stands in some fens (Godwin 1936; Knight et al., in press). If the seed source or a large portion of the initial North America seed source of R. cathartica came from England versus continental Europe, perhaps there was already a genetic modification predisposing the species to wetter habitat tolerances. What factors (e.g., climate, geology, availability of space to colonize, or disturbance) may allow the establishment R. cathartica in wetter habitats? SOIL NUTRIENTS. Other than a preference for “nutrient rich” (Kurdiani 1934) soils and a stated specific affinity for soils derived from (i.e., calcareous or alkaline soils) (Druce 1932, Kurdiani 1934, Godwin 1943, Tutin et al. 1968, Browicz 1984, Ellenberg 1988, Clapham et al. 1987) or treated (Hegi 1965) with calcium carbonate (lime), the soil nutrient requirements of R. cathartica are largely unreported. Interestingly, alkalinity may be more important than moisture to R. cathartica in habitat selection (Gurney 1958). A preference for alkaline soils is common among Central European plant species (Ewald 2003). In Germany, R. cathartica is mainly found on Gleyrendzina, a surface horizon with organic matter accumulation over lime-containing bedrock, and on Mergeln, lime-containing clays (Scamoni 1985, Arbeitsgruppe Boden 1994). It is also common near old castles in Germany where the lime- containing mortar has washed into the surrounding soils (Hegi 1965). In England, it is found throughout the countryside, but thrives in lime areas (Hulme 1914). Rhamnus cathartica is considered a component of habitat types ranging from wet to more dry conditions that are associated with alkaline soils (Tansley 1939, Godwin 1943, Gurney 1958, Rodwell et al. 1991).

There is little reported information on specific soil nutrient preferences of Rhamnus cathartica in North America. Rhamnus cathartica is associated with alkaline soils in Wisconsin (Gourley 1985) and recorded from alvars (i.e., open areas of thin soil over flat limestone) in the Great Lakes Region (Catling and Brownell 1995). The southern limit of spodic soils is one of a combination of several possible factors limiting the northern expansion of R. cathartica (Gourley 1985), but an aversion to acidic soils appears not to apply in New England where spodic and other acidic soils are common. Further analysis of sitespecific data is needed to determine the relation, if any, occurring between R. cathartica and soils in North America. Does the amount of lime applied to New England fields increase their suitability to R. cathartica! Does the taxon have a preference for alkaline soils, but tolerates neutral-to-slightly acidic soils? The change in soil texture and chemistry stretching from north and west of Chicago, IL, down around southern Lake Michigan, and into northwestern Indiana may yield useful information to examine this question as there appears to be a marked decrease in R cathartica abundance as you cross the state line into Indiana (Kurylo, pers. obs). How does pH affect the growth and reproductive abilities of R cathartica! Is R. cathartica limited by nutrients other than calcium? Questions are several, but answers currently are few.

Conclusion. Rhamnus cathartica is widely distributed within both its invaded range, North America, and in its native range, Eurasia. Within these ranges of distribution, it occurs in a wide variety of habitats, especially moist, but not saturated, calciumrich soils in disturbed areas. Climate and soil alkalinity levels are possible limiting factors for continued expansion of R. cathartica within its invaded range. How will climate change, including increased temperatures and changes in moisture regimes, affect the potential naturalized distribution of R. cathartica? Is the taxon a calciophile and would it be limited by a lack of basic soils in areas it has not yet invaded? Or does the taxon have merely a casual association with calcium and basic soils, as suggested by its existence in areas not known for those soil types (e.g., northeastern USA)? There are gaps in the available information about the habitat preferences and complete distribution of R. cathartica. With increased knowledge of this species, we can better manage our ecosystems to deter invasion, slow it, or find the best route for restoration of native flora.

1 This research was supported, in part, by the Wetlands Group at the Illinois Natural History Survey and by USDA/CREES Hatch Award Nos. 875-324 and 875-348. Discussion and valuable feedback from collaborators and many co-workers are gratefully acknowledged. Many thanks also to Diane Greer of the GIS group at the Illinois Natural History Survey for producing the maps.

Literature Cited

APFELBAUM, S. I. AND A. HANEY. 1991. Management of degraded oak savanna remnants in the Upper Midwest: preliminary results from three years of study, p. 81-89. In G. V. Burger, J. Ebinger, and G. S. Wilhelm [eds.], Proceedings of the Oak Woods Management Workshop. Eastern Illinois University, Charleston, IL, USA.

ARCHIBOLD, O. W., D. BROOKS, AND L. DELANOY. 1997. An investigation of the invasive shrub European buckthorn, Rhamnus cathartica L., near Saskatoon, Saskatchewan. Can. Field Nat. Ill: 617-621.

ARBEITSGRUPPE BODEN. 1994. Bodenkundliche Kartieranleitung, 4th edn. Bundesanstalt fur Geowissenschaften und Rohstoffe und Geologische Landesamter in der Bundesrepublik Deutschland, Hannover, Germany. 392 p.

BEAN, W. J. 1914. Trees and Shrubs Hardy in the British Isles, Vol. II. John Murry, London, England. 736 p.

BILLINGTON, C. 1949. Shrubs of Michigan, 2nd ed. Bulletin #20. Cranbrook Institute of Science, Bloomfield Hills, MI, USA.

BOLMGREN, K. and B. Oxelman. 2004. Generic limits in Rhamnus L. s.l. (Rhamnaceae) inferred from nuclear and chloroplast DNA sequence phylogenies. Taxon 53: 383-390.

BRITTON, N. L. AND A. BROWN. 1970. An Illustrated Flora of the Northern U.S. and Canada, Vol. 2. Dover Publications, Inc., NY, USA. 735 p.

BROWICZ, K. 1984. Chorology of trees and shrubs in south-west Asia and adjacent regions, Vol. 3. Polish Scientific Publishers, Warsawa and Poznan, Poland. 88 p.

BROWN, R. G. AND M. L. BROWN. 1972. Woody Plants of Maryland. Port City Press, Baltimore, MD, USA. 347 p.

CATLING, P. M. 1997. The problem of invading alien trees and shrubs: some observations in Ontario and a Canadian checklist. Can. Field Nat. Ill: 338-342.

CATLING, P. M. AND V. R. BROWNELL. 1995. A review of the Alvars of the Great Lakes Region: distribution, floristic composition, biogeography and protection. Can. Field Nat. 109: 143-171.

CLAPHAM, A. R., T. G. TUTIN, AND E. F. WARBURG. 1987. Flora of the British Isles, 3rd ed. Cambridge University Press, Cambridge, England. 688 p.

CLARK, J. G. D., H. GODWIN, M. E. GODWIN, AND M. H. CLIFFORD. 1935. Report on recent excavations at Peacock’s farm, Shippea Hill, Cambridgeshire. Antiq. J. 15: 284-319.

COOPERRIDER, T. S. 1995. The Dicotyledoneae of Ohio. The Ohio State University Press, Columbus, OH, USA. 656 p.

CRONQUIST, A., N. HOLMGREN, AND P. HOLMGREN. 1997. Intermountain Flora: Vascular Plants of the Intermountain West Subclass Rosidae (except Fables), Vol. 3, Part A. The New York Botanical Garden, Bronx, NY, USA. 446 p.

CURTIS, J. T. 1971. The Vegetation of Wisconsin. The University of Wisconsin Press, Madison, WI, USA. 657 p.

DAVIS, P. H. 1967. Flora of Turkey and the East Aegean Islands, Vol. 2. University Press, Edinburgh, Scotland. 581 p.

DORN, R. 1984. Vascular Plants of Montana. Mountain West Publishing, Cheyenne, WY, USA. 276 p.

DORN, R. 2001. Vascular Plants of Wyoming. Mountain West Publishing, Cheyenne, WY, USA. 412 p.

DRUCE, G. C. 1932. The Comital Flora of the British Isles. T. Buncle and Co, Arbroath, Scotland. 407 p.

EGGERS, S. D. AND D. M. REED. 1997. Wetland plants and communities of Minnesota and Wisconsin (version 03SEP1998). Retrieved December 17, 2004 from U.S. Army Corps of Engineers, St. Paul District. Jamestown, ND: Northern Prairie Wildlife Research Center.

EILERS, L. J. AND D. M. ROOSA. 1994. The Vascular Plants of Iowa. University of Iowa Press, Iowa City, LA, USA. 304 p.

ELLENBERG, H. 1988. Vegetation Ecology of Central Europe, 4th ed. Cambridge University Press, United Kingdom. 731 p. [Translated by Gordon K. Strutt]

ENVIRONMENTAL LABORATORY. 1987. Corps of Engineers wetland delineation manual. U.S. Army Engineer Waterways Experiment Station, Vicksburg, Mississippi. Technical Report Y-87-1.

EWALD, J. 2003. The calcareous riddle: why are there so many calciphilous species in the Central European flora? Folia Geobot. 38: 357-366.

FRYE, J. and W. Grosse. 1992. Growth responses to flooding and recovery of deciduous trees. Z. Naturforsch. 47: 683-689.

GASSMANN, A. 2005. Developing biological control of buckthorns, p. 55-57. In L. C. Skinner [ed.], Proceedings: symposium on the biology, ecology and management of garlic mustard (Alliaria petiolata) and European buckthorn (Rhamnus cathartica). University of Minnesota, St. Paul, MN, USA.

GIL-AD, N. L. AND A. A. REZNICEK. 1997. Evidence for hybridization of two old world Rhamnus species – R. cathartica and R. utilis (Rhamnaceae) – in the New World. Rhodora 99: 1-22.

GILL, D. S. AND P. L. MARKS. 1991. Tree and shrub seedling colonization of old fields in central New York. Ecol. Monogr. 61: 183-205. GODWIN, H. 1936. Studies in the ecology of Wicken Fen: III. The establishment and development of fen scrub (carr). J. Ecol. 28: 82-116.

GODWIN, H. 1943. Rhamnaceae – Rhamnus cathartica L., Frangula alnus Miller (Rhamnus frangula L.), part of The Biological Flora of the British Isles. J. Ecol. 31: 66-76.

GODWIN, H. AND F. R. BHARUCHA. 1932. Studies in the ecology of Wicken Fen: II. The fen water table and its control of plant communities. J. Ecol. 20: 157-191.

GODWIN, H., D. R. CLOWES, AND B. HUNTLY. 1974. Studies in the ecology of Wicken Fen: V. Development of fen carr. J. Ecol. 62: 197214.

GORHAM, R. P. 1944. The known distribution of the buckthorns in the Maritime Provinces. Acadian Naturalist 1: 118-124.

GOURLEY, L. C. 1985. A study of the ecology and spread of Buckthorn (Rhamnus cathartica L.) with particular reference to the University of Wisconsin Arboretum. Dissertation, University of Wisconsin, Madison, WI. 166 p.

GOURLEY, L. C. AND E. HOWELL. 1984. Factors in buckthorn invasion documented; control measure checked (Wisconsin). Rest. Manage. Notes 2: 87.

GREAT PLAINS FLORA ASSOCIATION. 1986. Flora of the Great Plains. University Press of Kansas, Lawrence, KS, USA. 1392 p.

GRUBB, P. J., J. KOLLMANN, AND J. WlLSON. 1996. Interaction of irradiance and soil nutrient supply on growth of seedlings of ten European tallshrub species and Fagus sylvatica. J. Ecol. 84: 827- 840.

GRUBOV, V. I. 1949. Monographic survey of the genus Rhamnus s.l. Flora et systematica plantae vasculares, Academiae scientiarum, Leningrad, Russia. 423 p. [In Russian]

GURNEY, R. 1958. Trees of Britain. Faber & Faber, London, England. 228 p.

HARRINGTON, R. A., B. J. BROWN, AND P. B. REICH. 1989. Ecophysiology of exotic and native shrubs in southern Wisconsin II. Annual growth and carbon gain. Oecologia 80: 368-373.

HARMON, P. J., D. FORD-WERNTZ, AND W. GRAFTON. 2006. Checklist and atlas of the vascular flora of West Virginia. West Virginia Division of Natural Resources, Wildlife Resources section, Elkins, WV, USA. 381 p.

HEGI, G. 1965. Illustrierte Flora von Mittel-Europa, 5 Band 3 Teil, (Linaceae-Violaceae). Carl Hanser Verlag, Munchen, Germany. 334 p.

HEINZ, C. AND M. BARBAZA. 1998. Environmental changes during the Late Glacial and Post-Glacial in the central Pyrenees (France): new charcoal analysis and archaeological data. Rev. Palaeobot. Palynol. 104: 1-17.

HENEGHAN, L., C. RAUCHENBERG, F. FATEMI, AND M. WORKMAN. 2004. European buckthorn (Rhamnus cathartica) and its effects on some ecosystem properties in an urban woodland. Ecol. Res. 22: 275-280.

HICKMAN, J. C. 1993. The Jepson Manual of Higher Plants of California. University of California Press, Berkeley, CA, USA. 1400 p.

HULME, F. E. 1914. Wild Fruits of the Country-side. FA Stokes Co., New York, NY, USA. 221 p.

IVERSON, L. R., A. M. Prasad, and M. W. Schwartz. 2005. Predicting potential changes in suitable habitat and distribution by 2100 for tree species of the eastern United States. J. Agric. Meteorol. 61: 29-37.

JOHNSTON, M. C. AND L. A. JOHNSTON. 1978. Rhamnus. Flora Neotropica. Monograph No. 20. The New York Botanical Garden, Bronx, NY, USA. 96 p.

JONES, R. L. 2005. Plant Life of Kentucky. The University Press of Kentucky, Lexington, KY, USA. 834 p.

KELLER, I. A. AND S. BROWN. 1905. Handbook of the Flora of Philadelphia and Vicinity. Philadelphia Botanical Club, Philadelphia, PA, USA. 360 p.

KNIGHT, K. S. 2006. Factors that influence invasion success of two woody invaders of forest understories. Dissertation, University of Minnesota, St. Paul, MN.

KNIGHT, K. S., J. S. KURYLO, A. G. ENDRESS, J. R. STEWART, AND P. B. REICH. In press. Ecology and ecosystem impacts of common buckthorn (Rhamnus cathartica): a review. Biol. Inv.

KURDIANI, S. Z. 1934. Dendrologia. ZakGIZ, Triflis, Russia. 488 p. [In Russian]

LACKSCHEWITZ, K. 1991. Vascular plants of WestCentral Montana: identification guidebook. General Technical Report, INT-277. U.S.D.A. Forest Service, Intermountain Research Station, Ogden, UT, USA. 648 p.

LAMBERT, J. M. 1951. Alluvial stratigraphy and vegetational succession in the region of the Bure Valley Broads: III. Classification, status, and distribution of communities. J. Ecol. 39: 149-170.

LEITNER, L. A. 1985. An alien shrub in a changing landscape: The European buckthorn (Rhamnus cathartica) in southeastern Wisconsin. Dissertation, University of Wisconsin, Milwaukee, WI, USA. 184 p.

LINDIG-CISNEROS, R. AND J. B. ZEDLER. 2000. Restoring urban habitats: A comparative study. Ecol. Res. 18: 184-192.

LIU, X., R. K. PEET, AND A. S. WEAKLEY. 2005. Flora of the Southeast. Retrieved December 12, 2006 from The University of North Carolina Herbarium, USA. < firstviewer>

MABBERLEY, D. J. 1997. The Plant Book. Cambridge Univ. Press, Cambridge, England. 858 p.

MAGEE, D. W. AND H. AHLES. 1999. Flora of the Northeast. University of Massachusetts, Amherst, MA, USA. 1213 p.

MAW, M. G. 1981. Rhamnus cathartica L., common or European buckthorn (Rhamnaceae), p. 185189. In J. S. Kelleher and M. A. Hulme [eds.], Biological control programs against insects and weeds in Canada 1969-1980. Commonwealth Agricultural Bureau, United Kingdom.

MEDAN, D. AND C. SCHIRAREND. 2004. Rhamnaceae, p. 320-338. In K. Kubitzki [ed.], Flowering plants, dicotyledons: Celastrales, Oxalidales, Rosales, Cornales, Ericales. Springer-Verlag, NY, USA.

MITCHELL, R. S. 1986. A checklist of New York State plants. Bulletin No. 458. University of the State of New York, the State Education Department, Albany, NY, USA. 272 p.

MOOR, M. 1981. Die Trockengebusche (Berberidiori) der Reinacherheide. Bauhinia 7: 67-72.

Moss, E. H. 1983. Flora of Alberta, 2nd ed., (rev. by J. G. Packer). University of Toronto Press, Toronto, Canada. 687 p.

MULLIGAN, G. A. 1952. Survey of common barberry (Berberis vulgaris L.) and European buckthorn (Rhamnus cathartica L.) in eastern Ontario. Science Service, Division of Botany and Plant Pathology, Canadian Department of Agriculture, Ottawa, Canada. 16 p.

OWNBEY, G. B. AND T. MORLEY. 1991. Vascular Plants of Minnesota. University of Minnesota Press, Minneapolis, MN, USA. 307 p.

PETIT, R. J., R. BIALOZYT, P. GARNIER-GERE, AND A. HAMPE. 2004. Ecology and genetics of tree invasions: from recent introductions to Quaternary migrations. For. Ecol. Manag. 197: 117-137.

PHILLIPS, C. W. 1935. Notes on excavations Ty Newydd, Llanfaelog, Anglesey. Proc. Prehist. Soc. 1: 145.

REED, JR., P. B. 1988. National list of plant species that occur in wetlands. NERC-88/18.13. U.S. Fish and Wildlife Service, National Wetlands Inventory, USA. 416 p.

REHDER, A. 1927. Manual of Cultivated Trees and Shrubs Hardy in North America. MacMillian Co., NY, USA. 930 p.

REJMANEK, M. 1996. A theory of seed plant invasiveness: the first sketch. Biol. Conserv. 78: 171-181.

RICHARDSON, J. E., M. F. FAY, Q. C. B. CRONK, AND M. W. CHASE. 2000. A revision of the tribal classification of Rhamnaceae. Kew Bull. 55: 311-340.

RODWELL, J. S., C. D. PIGOTT, D. A. RATCLIFFE, A. J. C. MALLOCH, H. J. B. BIRKS, M. C. F. PROCTOR, D. W. SHIMWELL, J. P. HUNTLEY, E. RADFORD, M. J. WIGGINTON, AND P. WILKINS FOR THE NATURE CONSERVANCY COUNCIL. 1991. British Plant Communities, Vol. 1 (woodlands and scrub). Cambridge University Press, Cambridge, England. 395 p.

SCAMONI, A. 1985. Uber das okologjsche und soziologische Verhalten von Rhamnus cathartica L. und Frangula alnus Mill, in der planaren Stufe der DDR. Feddes Repert. 96: 139-144.

SCOGGAN, H. J. 1978. Flora of Canada, Part 3. Publications in Botany No. 7. National Museum of Natural Sciences, Ottawa, Canada. 568 p.

SHISHKIN, B. K. AND E. G. BOBROV. 1949. Flora of the U.S.S.R., Vol. XIV (Geraniales, Sapindales, Rhamnales). Botanical Institute of the Academy of Sciences of the USSR, Moskva-Leningrad. 616 p. [Translated from Russian, Israel Program for Scientific Translations, Jerusalem, 1974]

SOKOLOV, S. J. 1958. Trees and shrubs of the USSR, Vol. 4. Akedemia Nauk SSSR, Botanicheskia Institut, Mockba (Moscow). 973 p. [In Russian]

SOPER, J. H. AND M. L. HEIMBURGER. 1982. Shrubs of Ontario. Royal Ontario Museum, Toronto, Canada. 495 p.

SPYREAS, G., J. ELLIS, C. CARROLL, AND B. MOLANOFLORES. 2004. Non- native plant commonness and dominance in the forests, wetlands, and grasslands of Illinois, USA. Nat. Areas J. 24: 290-299.

STEWART, J. R. AND W. R. GRAVES. 2004. Photosynthesis and growth of Rhamnus caroliniana during drought and flooding: comparisons to the invasive Rhamnus cathartica. HortScience 39: 1280-1284.

STEYERMARK, J. A. 1963. Flora of Missouri. Iowa State University Press, Ames, IA, USA. 1752 p.

STOKES, D. W. 1981. The Natural History of Wild Shrubs and Vines, Eastern and Central North America. Harper and Row, NY, USA. 246 p.

STOVER, M. E. AND P. L. MARKS. 1998. Successional vegetation on abandoned cultivated and pastured land in Tompkins County, New York. J. Torrey Bot. Soc. 25: 150-164.

SWINK, F. AND G. WILHELM. 1994. Plants of the Chicago Region, 4th ed. Indiana Academy of Science, Indianapolis, IN, USA. 921 p.

TANSLEY, A. G. 1939. The British Islands and Their Vegetation. University Press, Cambridge, England. 930 p.

TATNALL, R. R. 1946. Flora of Delaware and the Eastern Shore. The Society of Natural History of Delaware, Wilmington, DE, USA. 313 p.

TUTIN, T. G., V. H. HEYWOOD, N. A. BURGES, D. H. Valentine, S. M. Walters, and D. A. Webb. 1968. Flora Europaea, Vol. 2. Cambridge University Press, Cambridge, England. 455 p.

UNIVERSITY OF TENNESSEE HERBARIUM AND AUSTIN PEAY STATE UNIVERSITY. 2002. Vascular plants herbarium. Retrieved December 13, 2006 from University of Tennessee, Department of Ecology & Evolutionary Biology, < vascular>

USDA, NRCS. 2007. The PLANTS Database. Retrieved February 22, 2007 from the National Plant Data Center, Baton Rouge, LA 70874- 4490 USA. <>

USDA Forest Service. 2007. Forest Inventory and Analysis National Program. Retrieved May 18, 2007 from Forest Inventory and Analysis National Office, USDA Forest Service. <> U.S. FISH AND WILDLIFE SERVICE. 1996. 1996 national list of vascular plant species that occur in wetlands. National Wetlands Inventory, U.S. Fish and Wildlife Service, Washington, DC, USA. 209 p.

U.S. FOREST SERVICE. 1948. Woody plant seed manual. USDA Misc. Publication #654. Washington, DC, USA. 416 p.

VIRGINIA BOTANICAL ASSOCIATION. 2005. Digital atlas of the Virginia flora. Retrieved August 29, 2005 from Virginia Tech, Department of Biology. <>

VOSS, E. G. 1985. Michigan Flora, Part II dicots (Saururaceae – Cornaceae). Bulletin #59. Cranbrook Institute of Science, University of Michigan Herbarium, Ann Arbor, MI, USA. 724 p.

WEAKLY, A. S. 2005. Flora of the Carolinas, Virginia, and Georgia: working draft. Retrieved August 24, 2005 from the University of North Caroloina Herbarium. < www>

WEBER, W. A. AND WITTMANN, R. C. 1996. Colorado Flora: Eastern Slope, revised ed. University Press of Colorado, Niwot, CO, USA. 524 p.

WHERRY, E. T., J. M. Fogg, Jr, and H. A. Wahl. 1979. Atlas of the Flora of Pennsylvania. The Morris Arboretum of the University of Pennsylvania, Philadelphia, PA, USA. 390 p.

WHITE, K. L. 1965. Shrub-carrs of southeastern Wisconsin. Ecology 46: 286-304.

WOLF, C. B. 1938. The North American species of Rhamnus. Monographs/Botanical Series 1. Rancho Santa Ana Botanic Garden, CA, USA. 136 p.

WOFFORD, B. E. AND E. W. CHESTER. 2002. Guide to the Trees, Shrubs, and Vines of Tennessee. The University of Tennessee Press, Knoxville, TN, USA. 286 p.

WOFFORD, B. E. AND R. KRAL. 1993. Checklist of the vascular plants of Tennessee, SIDA, botanical miscellany, No. 10. Botanical Research Institute of Texas, Inc., Fort Worth, TX, USA. 66 p. WYCKOFF, P., R. JANSEN, AND R. PATTEN. 2005. The European buckthorn (Rhamnus cathartica) invasion in West Central Minnesota, p. 49-52. In L. C. Skinner [ed.], Proceedings: symposium on the biology, ecology and management of garlic mustard (Alliaria petiolata) and European buckthorn (Rhamnus cathartica). University of Minnesota, St. Paul, MN, USA.

YILIN, C. AND Z. BANGKAI. 1982. Rhamnus L., p. 19-88. In C. Yilin [ed.], Flora Reipublicae Popularis Sinicae, Vol. 48. Science Press, Beijing, China. [In Chinese]

YOUNG, D. 1994. Kane County wild plants and natural areas, 2nd ed. Kane County Forest Preserve District, Geneva, IL, USA. 218 p.

J. S. Kurylo2

Division for Ecology and Conservation Science, Illinois Natural History Survey, 1816 S. Oak St,

Champaign, IL 61820

K. S. Knight

USDA Forest Service Northern Research Station, 359 Main Rd, Delaware, OH 43015 and

Department of Ecology, Evolution, and Behavior, University of Minnesota, 100 Ecology Building,

1987 Upper Buford Circle, St. Paul, MN 55108

J. R. Stewart

Department of Natural Resources and Environmental Sciences, 1102 S. Godwin Ave, University of Illinois

at Urbana-Champaign, Urbana, IL 61801

A. G. Endress

Department of Natural Resources and Environmental Sciences, 1102 S. Godwin Ave, University of Illinois

at Urbana-Champaign, Urbana, IL 61801 and

Division of Biodiversity and Economic Entomology, Illinois Natural History Survey, 1816 S. Oak St,

Champaign, IL 61820

2 Author for correspondence: E-mail: jkurylo@ inhs.uiuc.edu

Received for publication February 22, 2007, and in revised form May 25, 2007.

Copyright Torrey Botanical Society Jul-Sep 2007

(c) 2007 Journal of the Torrey Botanical Society. Provided by ProQuest Information and Learning. All rights Reserved.

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