New ecological and physiological dimensions of beech bark disease development in aftermath forests Jonathan A. Cale a,⇑ , Stephen A. Teale a , Mariann T. Johnston b , Gregory L. Boyer c , Katherine A. Perri c , John D. Castello a a Department of Environmental and Forest Biology, State University of New York, College of Environmental Science and Forestry, Syracuse, NY, USA b Department of Forest and Natural Resources Management, State University of New York, College of Environmental Science and Forestry, Syracuse, NY, USA c Department of Chemistry, State University of New York, College of Environmental Science and Forestry, Syracuse, NY, USA article info Article history: Received 22 July 2014 Received in revised form 17 October 2014 Accepted 18 October 2014 Available online 7 November 2014 Keywords: Neonectria Cryptococcus fagisuga Xylococculus betulae Bark phenolics Bark phosphorus Tree chemistry abstract The ecology of northeastern North American forests is significantly altered by the effects of beech bark disease (BBD) on American beech (Fagus grandifolia). The conventional understanding is that BBD involves two native pathogenic fungi, Neonectria ditissima and N. faginata, which are preceded by Crypto- coccus fagisuga, a non-native, invasive scale insect. Described in the early 20th century, this model of dis- ease development describes the sequence of insect colonization at the expanding front of this invasive disease complex but lacks supporting data in long-affected (aftermath) forests. A clearer understanding of factors governing BBD development in aftermath forests is needed to develop sound, targeted manage- ment strategies. We established a case-control study to determine how Neonectria infections and C. fagisuga infestations are driven by nutritional, physiological, and entomological factors of the previous year. Findings suggest that N. ditissima infection is predisposed by the native scale insect Xylococculus betulae and low bark levels of phosphorus and the phenolic isorhamnetin while C. fagisuga and low bark levels of phosphorus and the phenolic catechin predispose trees to N. faginata infection. C. fagisuga population growth was best predicted by insect density the previous year, but was variously correlated with bark chemistry factors. We conclude that the classic BBD development model does not adequately predict disease development in aftermath forests of New York, and propose separate modified models for N. ditissima and N. faginata that include distinct abiotic and biotic factors. An improved understanding of the ecological interactions among the organisms involved and the physiological basis of infection have implications for future disease development and resistance biomarkers. We suggest that BBD management in aftermath forests should avoid single-factor strategies in favor of multi-factor approaches targeting specific pathosystems. Ó 2014 Elsevier B.V. All rights reserved. 1. Introduction Forests provide a myriad of ecosystem functions and services (Luyssaert et al., 2008), which may be severely altered by disease- and insect-induced tree mortality (Boyd et al., 2013). Our ability to mitigate and manage this mortality requires understanding funda- mental tree-level interactions between pathogens or insect pests and host trees (Barakat et al., 2009). Chief among these interactions are those predisposing factors governing attack success (e.g., infec- tion or infestation) by mortality agents. Progressive spread of beech bark disease (BBD) across north- eastern North America has caused extensive crown mortality of American beech (Fagus grandifolia Ehrh.) trees for over a century (Hewitt, 1914; Houston, 1994a; Morin et al., 2005). This mortality has had several important ecological consequences including altered forest composition, structure, biodiversity, nutrient cycling and hard mast availability for wildlife, and reduced regeneration of desirable timber species (Twery and Patterson, 1984; Lovett et al., 2010; Rosemier and Storer, 2010; Garnas et al., 2011a; Cale et al., 2013). BBD involves infection by the pathogenic fungi Neonectria ditissima Samuels & Rossman and N. faginata Castlebury et al. which produce annual necrotic lesions (cankers) on infected beech bark (Ehrlich, 1934; Spaulding et al., 1936). Coalescing cankers cause reduced radial growth, leaf chlorosis, and crown dieback and death when the tree bole is girdled (Gavin and Peart, 1993; Houston, 1994a). Neonectria infection is often preceded by infestations of beech scale (Cryptococcus fagisuga Lind.; Hemiptera, Eriococcidae) – an invasive, non-native phloem-feeding insect http://dx.doi.org/10.1016/j.foreco.2014.10.019 0378-1127/Ó 2014 Elsevier B.V. All rights reserved. ⇑ Corresponding author. Tel.: +1 (315)470 6965. E-mail address: jacale@syr.edu (J.A. Cale). Forest Ecology and Management 336 (2015) 99–108 Contents lists available at ScienceDirect Forest Ecology and Management journal homepage: www.elsevier.com/locate/foreco