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Juglans Cinerea L R E S E A R C H A R T I C L E ABSTRACT: To mitigate the loss of native tree species threatened by non-native pathogens, managers need to better understand the conservation status of remaining populations and the conditions that favor successful regeneration. Populations of Juglans cinerea L. (butternut), a wide-ranging riparian species, • have been devastated by butternut canker, a disease caused by a non-native fungal pathogen. We as- sessed J. cinerea within Great Smoky Mountains National Park (GSMNP) to determine post-disease survivorship and health, recruitment history, environmental conditions associated with survival, and the Conservation Status extent of hybridization with a non-native congener. Monitoring records were used to locate and collect data for 207 J. cinerea trees in 19 watersheds. Tree cores were collected from a subset of individuals to of a Threatened Tree assess recruitment history. We sampled vegetation plots within areas that contained J. cinerea to assess site conditions and overstory species composition of characteristic habitat. We collected leaf samples for Species: Establishing genetic analysis to determine the frequency of hybridization. Our reassessment of monitoring records suggests that J. cinerea abundance in GSMNP has declined due to butternut canker and thirty years of a Baseline for poor regeneration. Populations displayed continuous recruitment following Park establishment (1934) until around 1980, after which regeneration declined drastically. Ordination analysis revealed that J. Restoration of Juglans cinerea in the contemporary forest was associated with greater distance from homesites and reduced basal area of competing species. Hybrids comprised a small portion of sampled trees. The presence of cinerea L. in the healthy trees and low rate of hybridization suggest that these trees may contribute to the development of disease-resistant genotypes for future restoration efforts. Southern Appalachian Index terms: butternut, cohort structure, disturbance regime, forest disease, fungal pathogen, hybridiza- Mountains, USA tion, mortality, recruitment history Amanda M. Parks1 INTRODUCTION in tree species (Lovett et al. 2006; Loo 1Department of Forestry and Natural Re- 2009; Holzmueller et al. 2010). While sources Exotic diseases are an increasing threat research has focused on the effects of Purdue University to native biodiversity as global movement diseases on common species, less is known 715 West State St. of materials introduces non-native patho- about the effects of introduced pathogens West Lafayette, IN, 47907, USA gens, and changing land use facilitates on less-common species, for which the their spread (Lovett et al. 2006). Fungal consequences of disease may be ampli- pathogens have devastated North Ameri- fied because of inherently low population Michael A. Jenkins1,4 can forests in the last century, resulting density and limited reproduction of the Keith E. Woeste2 in fundamental alterations to ecosystems host species. 3 (Ellison et al. 2005; Lovett et al. 2006; Loo Michael E. Ostry 2009; Holzmueller et al. 2010). Baseline The four-decade program to produce a 2Northern Research Station (pre-disease) data are necessary to exam- blight-resistant hybrid of C. dentata is USDA Forest Service ine the overall effects of species loss, but nearing the stage of active restoration Hardwood Tree Improvement and often extensive mortality occurred before (Jacobs 2007). As the program progressed, Regeneration Center detailed information was collected, making other researchers have focused on the Purdue University it difficult to determine the true effects of restoration of other tree species affected 715 West State St. disease on ecosystem processes (Ellison by exotic disease (Windham et al. 1998; West Lafayette, IN, 47907, USA et al. 2005). Griffin 2000; Ostry and Moore 2008). For example, Juglans cinerea L. (butternut), a 3Northern Research Station species whose range extends across much USDA Forest Service Several eastern tree species have been virtu- 1561 Lindig Ave. ally eliminated by introduced pathogens; of eastern North America, has experienced St. Paul, MN 55108, USA others have experienced such severe decline extensive mortality from butternut canker that they no longer retain their pre-disease caused by the non-native fungal pathogen ecological function (Loo 2009). Chestnut Ophiognomonia clavigignenti-juglan- • blight, caused by Cryphonectria parasitica dacearum (Nair, Kostichka, & Kuntz) Murrill (Barr) and perhaps the best example Broders & Boland (Woeste et al. 2009). 4 Corresponding author: of a fungal disease that led to the loss of a While estimates of mortality caused by but- [email protected] keystone species, functionally eliminated ternut canker are as high as 92% (Carlson Castanea dentata [American chestnut, and Guthmiller 1993), evidence suggests (Marsh.) Borkh] from eastern forests in that genetic resistance exists and may the early twentieth century. Other fungal potentially be exploited for conservation diseases, including beech bark disease, and restoration efforts (Thompson et al. Natural Areas Journal 33:413–426 Dutch elm disease, and dogwood anthrac- 2006; Ross-Davis et al. 2008). Efforts are nose, have caused widespread declines underway to identify resistant individuals Volume 33 (4), 2013 Natural Areas Journal 413 (Ostry and Moore 2008) and establish a dominance by other early-successional Wisconsin (Carlson and Guthmiller 1993), framework for the development of resistant species; and (4) What was the temporal within GSMNP, numerous scattered indi- genotypes (Michler et al. 2006). recruitment pattern of surviving J. cinerea viduals and groups of trees remain (Figure populations and when did contemporary 1) within a continuous (non-fragmented) The persistence of J. cinerea in contempo- competitors establish? forest that may limit exposure to non-na- rary forests is precarious not only because tive genes and where high ridges further of the effects of butternut canker, but also isolate watersheds. METHODS due to habitat loss, poor regeneration, and genetic dilution from hybridization with Juglans cinerea has a range of historic and non-native Juglans ailantifolia Carr. (Japa- Study Area modern uses: Native Americans and early nese walnut; Hoban et al. 2009). Juglans American settlers had several uses for the ailantifolia was historically planted within Great Smoky Mountains National Park nuts, bark, and sap, including dyes, foods, agricultural landscapes (Hoban et al. 2009) is an internationally renowned center of and medicines (Ostry and Pijut 2000; and has been present within the range of biological diversity in North America, lead- Schultz 2003). Historically in areas where J. cinerea for multiple generations. As ing to its designation as an International J.cinerea was common, its wood was nearly with other uncommon species that co-oc- Biosphere Reserve in 1976 and World equal in value to that of Juglans nigra L. cur with a non-native congener, such as Heritage Site in 1983 (Jenkins 2007). Be- (black walnut) (Nicholls 1979). Although Celastrus scandens (American bittersweet) cause of its large size (over 210,000 ha), J. cinerea is largely a riparian species and C. orbiculatus (oriental bittersweet), biological diversity, and protected status, that rarely dominates stands, the loss of genetic dilution as a result of hybridization GSMNP serves a vital role in conservation J. cinerea could have ecological impacts presents a serious threat to the persistence within the southeastern United States and because it is a highly cold-tolerant hard of the species (Pooler et al. 2002). When observed changes within the biota of GS- mast species whose nuts are preferred by hybridization occurs in conjunction with MNP serve as baselines for comparison to many species of wildlife (Ostry and Pijut an invasive pathogen, the threat to a native other state and federal lands (Jenkins 2007). 2000). In addition, J. cinerea litter has high species is amplified. GSMNP was once extensively settled and concentrations of nitrogen and calcium 75% of the Park was logged prior to its compared to most other riparian species Successful restoration of J. cinerea not establishment in 1934 (Pyle 1985), but for- (Ricklefs and Matthew 1982). only depends upon mitigating the effects est communities in GSMNP have received of disease and developing resistant geno- minimal direct human disturbance over the Survivorship, Health, and types, but also requires understanding the last 75 years. Distribution regeneration dynamics of J. cinerea and the community context in which it his- Focal Species To assess survivorship and health, we torically occurred and currently persists used a National Park Service (NPS) (Thompson et al. 2006). In this study, we Juglans cinerea typically grows in high- monitoring database to locate J. cinerea examined the contemporary health, genetic light environments along streams in the trees throughout GSMNP, systematically integrity, canopy associates, and recruit- moist, fertile soils of riparian forests (Rink sampling watersheds to represent the full ment history of J. cinerea populations 1990), although the species has been ob- distribution of J. cinerea. We used site (defined in this study as all individuals directions and geographical coordinates to occurring within a watershed; Figure 1) served on drier, rocky sites (Cogliastro et al. 1997). The loss of riparian habitats caused search for individual trees, and those not within Great Smoky Mountains National found at specified
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