IAWA Journal 42 (1), 2021: 3–30 Wood and bark of Buddleja: uniseriate phellem, and systematic and ecological patterns Kamil E. Frankiewicz1,⁎, John H. Chau2, and Alexei A. Oskolski3,4 1Institute of Evolutionary Biology, Faculty of Biology, University of Warsaw, Biological and Chemical Research Centre, Żwirki i Wigury 101, 02-089 Warsaw, Poland 2Centre for Ecological Genomics and Wildlife Conservation, Department of Zoology, University of Johannesburg, PO Box 524, Auckland Park 2006, Johannesburg, South Africa 3Department of Botany and Plant Biotechnology, University of Johannesburg, PO Box 524, Auckland Park 2006, Johannesburg, South Africa 4Botanical Museum, Komarov Botanical Institute, Prof. Popov 2, 197376 St. Petersburg, Russia *Corresponding author; email: [email protected] Accepted for publication: 20 June 2020 ABSTRACT Wood anatomy of Buddleja is well-explored but not in many southern African members, which form a grade of species and small clades that form successive sister groups to the rest of the genus, and its bark structure has not been studied at all. We provide new descriptions of wood anatomy for twelve species, including nearly all Buddleja from southern Africa and two species of Freylinia in the sister group of Buddleja. We also describe bark structure from fifteen species. To assess if wood anatomy provides phylogenetic and/or ecological signal, we compiled data on wood traits and climatic variables from the distributions of 53 species. Wood traits counteracting cavitation correlated with higher temperature and precipitation seasonality; simultaneously they were better expressed in species with smaller max- imal plant height. It is likely that hotter and drier areas harbour smaller plants which have traits conveying higher conductance safety. Bark structure varies considerably. In bark of Buddleja section Gomphostigma, periderm is ini- tiated in the outer cortex and develops thin-walled phellem, and sclerification of their phloem does not occur. This resembles bark in Freylinia, supporting the position of section Gomphostigma as sister to the rest of Buddleja.In the remaining Buddleja species, bark is characterised by formation of periderm with phelloid cells in the secondary phloem. The phellem is often uniseriate, a condition not reported elsewhere. Its formation occurs close in time to solid sclerification of the cut-off phloem, suggesting a possible novel ontogenetic mechanism. Keywords:cavitation; Freylinia; phelloid cells; phloem sclerification; phylogenetic signal; Scrophulariaceae; uniseriate phellem; wood ecology. In memory of Prof. Fritz Hans Schweingruber INTRODUCTION Although genus Buddleja (tribe Buddlejeae, Scrophulariaceae) has been recognised since 1753 (Linnaeus) its phylogenetic relationships were resolved only recently. The traditional narrow circumscription of the genus was shown to be paraphyletic, and four allied genera (Chilianthus, Emorya, Gomphostigma and Nicodemia) were subsequently merged into Buddleja (Chau etal. 2017).This new circumscription resulted in a genus of ca. 108 species from North and South America (66 species), Asia (24 species), and Africa including Madagascar (18 species). They are characterised by a diversity of life forms (shrubs, trees, lianas; Fig. 1) and wide ecological preferences (including montane tropical, subtropical and warm-temperate habitats; Table 1). Most of the southern African species (B. auriculata, B. dysophylla, B. glomerata, B. incompta, B. loricata, B. saligna, B. salviifolia and B. virgata) were determined to form a grade of small clades that are successive sister groups to the rest of Buddleja.The precise relationships among these lineages are still uncertain, including which taxon is sister to the rest of the genus. Two conflicting topologies were resolved by Chau et al. (2017): (a) section Gomphostigma, sister to the remaining Buddleja; and (b) section Salviifoliae, sister to the remaining Buddleja (Fig. 2). In either case, it is clear that these southern African species are crucial for understanding patterns of evolution within the genus. © The authors, 2021 DOI 10.1163/22941932-bja10020 This is an open access article distributed under the terms of the CC BY-NC-ND 4.0 license. Downloaded from Brill.com10/10/2021 10:37:14AM via free access 4 IAWA Journal 42 (1), 2021 Figure 1. Habit diversity of exemplar Buddleja species. (A) B. virgata (shrub); (B) B. loricata (shrub); (C) B. salviifolia (intermediate between shrub and tree); (D) B. coriacea (tree). The first detailed descriptions of Buddleja wood anatomy were provided by Mennega (in: Leeuwenberg 1980, p. 112–161) and were further elaborated by Quintanar et al. (1996), Carlquist (1997), and Aguilar-Rodríguez & Terrazas (2001). Additional species are also included in the InsideWood database (2004; Wheeler 2011). Altogether, to date the wood anatomy of 41 Bud- dleja species have been studied. Carlquist (1997) concluded that only the occurrence of crystals in ray cells might be of any taxonomic value in Buddleja, while other wood anatomical traits reflect species-specific ecological preferences. Aguilar- Rodríguez et al. (2006) studied patterns in wood traits with respect to plant size, latitude, altitude, soil type, and climate (e.g., annual temperature amplitude, precipitation). They examined multiple specimens of a single species (B. cordata) and showed that within the species range, plant size and several wood traits (vessel frequency, fibre length, ray size) are affected by local climatic conditions, namely rainfall and temperature. Terrazas et al. (2008) explored correlations between selected wood traits, habit, and latitude. Unlike Aguilar-Rodríguez et al. (2006), they investigated multiple species and showed that most of the studied wood traits correspond with plant size rather than distribution. Thus, it seems that Buddleja wood can be affected by species-specific habit and/or ecology, but it is unknown if there are phylogenetic patterns. Regardless of whether wood anatomy has any taxonomic value in Buddleja, previous studies have focused mainly on Asian and American species in sections Alternifoliae and Buddleja, respectively. Of the eight species in the southern African grade comprising clades sister to the rest of the genus, only two (B. saligna and B. salviifolia) have been studied, leading to a gross underrepresentation of this highly diverse group (found in grassland, desert, riparian, and, most commonly, montane forest habitats; Fig. 1A–C; Table 1). Simultaneously, to the best of our knowledge, bark anatomy of Buddleja remains mostly unexplored — it was passingly mentioned by Moeller (1882, p. 182), and a single photo depicting bark structure of B. davidii is shown by Schweingruber et al. (2013, p. 263). Our study had three main goals focusing on wood and bark anatomy in Buddleja and representatives of the sister group to Buddleja in the genus Freylinia for comparison. First, we described wood anatomy of several BuddlejaDownloadedand fromFreylinia Brill.com10/10/2021species, 10:37:14AM via free access Table 1. Habitat descriptions of Buddleja species included in this study as presented in original sources. Reference list is provided below. Species Distribution Habitat Buddleja aromatica South America (Bolivia, Argentina) Rocky areas and semi-arid thorn scrub; 2900–4000 m a.s.l.1 Buddleja auriculata Africa (South Africa) In rocky ravines, on mountain sides or at forest margins in mountainous country2 Montane forests or thickets, often in gullies; 600–2000 m a.s.l.3 Buddleja cordata North America (Mexico, Guatemala) Very diversified habitat including Abies, Pinus, oak forests, montane mesophilic forests, tropical deciduous forests, xerophilic matorral, mostly in secondary vegetation; 1400–3200 m a.s.l.4 Cloud forests; 1700–2000 m a.s.l.5 Buddleja coriacea South America (Bolivia) 3000–4350 m1 Buddleja dysophylla Africa (South Africa) On forest margins, in patches of bush in kloofs or in streambank or riverbank bush2 Forest edges or scrub; 0–2600 m a.s.l.3 Frankiewicz et al. – Wood and bark anatomy of Buddleja Buddleja forrestii Asia (China, Bhutan, India, Myanmar) Forest, forest edges, scrub, mostly near riverbanks in the mountains; 2000–4000 m a.s.l.3 Buddleja glomerata Africa (South Africa) Among rocks on hills and mountains6 Among the rocks on the hills and mountains of the sandy karroid areas3 Buddleja lindleyana Asia (China, Japan) Mountains beside trails, scrub by streams, forest edges; 200–2700 m a.s.l.7 Bush on road sides, mostly in the mountains; 300–1800 m a.s.l. 3 Buddleja longiflora South America (Brazil) Rocky grasslands and shrublands at elevations above 2000 m a.s.l.8 Buddleja loricata Africa (South Africa) Slopes of high mountains, among boulders along water courses, or in damp sheltered gullies; 1600–2700 m a.s.l.3 Buddleja madagascariensis Africa (Madagascar) Bush in the mountains; 600–2000 m a.s.l.3 Buddleja pulchella Africa (South Africa, east Africa) In forest, mostly on margins or in open parts2 Woodland or light forest in the mountains; 1200–2000 m a.s.l., in forest, mostly at edges or in open places; 300–1100 m a.s.l.3 Buddleja saligna Africa (South Africa) Dry hillsides, mixed bushveld, mountainsides, wooded valleys, forest margins and along rivers2 In coastal bush at river mouth; 0–2000 m a.s.l.3 Buddleja salviifolia Africa (South Africa) Forest margins, rocky slopes, along watercourses, in dongas and isolated bushes on hillsides2 Forest edges, rocky slopes, along water courses, and in montane grassland; 1200–2500 m a.s.l. (near Cape from 150 m a.s.l.)3 Buddleja virgata Africa (South Africa) Along or near watercourses and rivers, growing in running water among boulders or on banks in sand or mud2 Downloaded fromBrill.com10/10/2021 10:37:14AM Along and in watercourses and rivers, only in running water among boulders, or on the banks in sand and mud; 600–2000 m a.s.l.9 1 Norman EM. 2000. Buddlejaceae. Flora Neotropica, volume 81. The New York Botanical Garden, New York, NY. 2 Retief E. & Herman PP. 1997. Loganiaceae, Scrophulariaceae. In Plants of the northern provinces of South Africa, keys and diagnostic characters. National Botanical Institute, Cape Town, p. 511–655. 3. Leeuwenberg AJM.