KEW BULLETIN (2018) 73:39 ISSN: 0075-5974 (print) DOI 10.1007/S12225-018-9764-3 ISSN: 1874-933X (electronic) A linear sequence to facilitate curation of herbarium specimens of Annonaceae Lars W. Chatrou1, Ian M. Turner2,3, Bente B. Klitgaard4, Paul J. M. Maas5 & Timothy M. A. Utteridge4 Summary. This paper provides a linear sequence of four subfamilies, 15 tribes and 106 genera of the magnoliid family Annonaceae, based on state-of-the-art and stable phylogenetic relationships. The linear sequence facilitates the organisation of Annonaceae herbarium specimens. Key Words. Annonaceae, classification, herbaria, phylogenetic hypotheses, systematics, taxonomy. Introduction Botany in the eighteenth and nineteenth century Plant taxonomy is a scientific expression for one of the to a large extent involved the rejection of Linnaeus’ defining characteristics of the human species: observ- artificial system, replacing it with classifications that ing, assembling and classifying. The ordering of the reflected supposed evolutionary relationships based plant world has been attempted ever since the origin on careful observations of plant characters. This of modern man, and even before. Neanderthals were endeavour was greatly facilitated by collections that able to distinguish fruit, nuts, roots, bulbs and tubers arrived in Europe from all over the world and were that were exploited as food resources (Henry et al. kept in newly established flourishing herbaria. Up to 2011), and upper palaeolithic hunter-gatherers that point, private ownership of plant collections recognised and categorised plants for economic and had been common practice. In the mid-19th ritual uses (Nadel et al. 2013; Power et al. 2014). From century, however, these collections were often sold Theophrastus onwards, in the fourth century BC, to the burgeoning herbaria, with the specific goal of botanists have attempted to organise plants into making the collections available for study by staff classification systems. The sexual system published by and visitors. Until then, classifications such as those Linnaeus (1753) in his Systema Naturae is the classical by Linnaeus and de Jussieu (1789) had primarily example of a classification system that has been been based on European temperate plants. The designed for convenience, most notably to facilitate influx of samples representing the wide plant plant recognition and identification, and unequivocal diversity in colonial territories challenged these communication about plants. classification systems, with many non-temperate In Linnaeus’s time the practice of drying and plant groups such as Annonaceae that were largely conserving plants for future study was well established. unknown to European botanists. Proliferating col- In the first half of the 16th century, the Bolognese lections and botanical studies resulted in natural botanist Luca Ghini introduced a new way of studying classifications by, e.g., Bentham & Hooker (1862 – plants by making the earliest hortus siccus. By pressing 1883) and Engler & Gilg (1924), which have been plants and storing them in a book, he invented the the basis for taxonomic literature and for the herbarium. It is in this era that botanic gardens, arrangement of herbaria and botanic gardens for a illustrated botanical publications, and herbaria were long time. Given the Herculean task of changing established as a trinity of resources for botanical the classification system followed in any sizeable sciences, a foundation that is still fundamental to herbarium (e.g. Wearn et al. 2013;LeBraset al. botanical research today. 2017), many herbaria are still organised to date on Accepted for publication 19 June 2018. 1 Wageningen University and Research, Biosystematics group, Droevendaalsesteeg 1, 6708 PB, Wageningen, The Netherlands. e-mail: [email protected] 2 Singapore Botanical Liaison Officer, Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AB, UK. 3 Herbarium, Singapore Botanic Gardens, National Parks Board, 1 Cluny Road, Singapore, 259569, Singapore. e-mail: [email protected]. 4 Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AB, UK. 5 Naturalis Biodiversity Center, Section Botany, P.O. Box 9517, 2300, RA, Leiden, The Netherlands. Ian M. Turner is the corresponding author. © The Author(s), 2018 39 Page 2 of 10 KEW BULLETIN (2018) 73:39 the basis of outmoded classification systems going the most species-rich and abundant families in tropical back in time a century or more. rain forest communities (e.g. Cardoso et al. 2017; Sosef Over the past two decades or so, phylogenetic et al. 2017; Turner in press) and is amply represented systematics has resulted in a notable transformation in major herbaria. of the classification of plants, and of angiosperms in particular. Based on the results of phylogenetic analyses, initially the delineation of angiosperm Linear sequences orders and families was evaluated and changed if Haston et al.(2007, 2009) published a simple method- necessary to make plant families comply with the ology for translating tree-like relationships into a prime guiding criterion of monophyly (APG I 1998; linear sequence, and applied this to a phylogenetic APG II 2003;APGIII2009;APGIV2016). Subse- tree of angiosperm families. Similarly, linear se- quently, working groups of systematists have applied quences have been produced for gymnosperms the results of phylogenetic analyses to revise (Christenhusz et al. 2011a) and lycophytes and ferns infrafamilial classifications (e.g. Schneider et al. (Christenhusz et al. 2011b). In order to extend the 2014;Boneet al. 2015; Chacón et al. 2016;Claudel phylogenetic arrangement of collections to the level of et al. 2017;DeFariaet al. 2017; Simões & Staples genera, linear sequences that translate family phylog- 2017), an endeavour that is still ongoing. Systematists enies are indispensable. So far, linear sequences are have spent great effort in revising the classification of available for Fabaceae (Lewis et al. 2013), and mono- angiosperms because of the awareness that phyloge- cots excluding Poaceae and Orchidaceae (Trias-Blasi netics has brought methodological rigour to system- et al. 2015). atics and predictivity to classifications, which enabled The assembly of the phylogenetic tree underpin- the treatment of phylogenetic relationships — and ning the linear sequence, and the translation of the therefore of classifications — as testable hypotheses, tree into the sequence consisted of the following steps. rather than opinions of scientists, however scholarly they might be. Y a summary tree showing relationships of all genera of Recently, the herbarium of the Royal Botanic Annonaceae was assembled. Details are given below, Gardens, Kew, was reorganised following the APG in the section ‘Annonaceae classification’.Nodesthat III system at the family level and taking phylogenetic did not receive significant support (parsimony or classifications into account at the infrafamiliar level. maximum likelihood bootstrap percentages, Bayesian Linear sequences of plant taxa enable curators to posterior probabilities) in any of the published studies curate herbarium collections in accordance with were resolved according to the topology most fre- phylogenetic relationships among genera. Linear quently inferred in all used publications. sequences reflect the order of names attached to Y we defined clade size in terms of number of species, the tips of a phylogenetic tree, after the branches in and not number of higher taxa (e.g. number of thetreehavebeenorderedaccordingtosome genera to define the size of tribes) as the former projection method. Alternatively, herbarium collec- estimate of clade size can be expected to be more tions may be organised alphabetically, and the stable than the latter, i.e. more robust to changing choice between an arrangement based on alphabet taxonomic concepts (Hawthorne & Hughes 2008). or on classification has been cause for debate (Funk Y species numbers for all genera were taken from 2003;Burger2004). Storing collections according to Annonbase (Rainer & Chatrou 2006). any organising system remains indispensable as Y following Haston et al.(2007), nodes of the phylo- herbaria have retained their historic functions, being genetic tree were rotated in such a way that clades the basis for plant systematics and taxonomy, floris- with fewer species were placed before clades with tics and identification, assessment of botanical diver- more species. This clade size criterion was applied sity, and teaching. In addition, scientific subsequently to all nodes in the tree, starting from developments have unlocked new applications of the root node (Fig. 1). The names along the tips, herbarium collections, such as the characterisation reading down from the top, represent the linear of phenological responses to climate change (Willis sequence. et al. 2017), the assessment of global rarity of plant species to guide conservation (bioquality; Marshall et al. 2016), the sequencing of near-complete Annonaceae classification plastomes (Bakker et al. 2016; Hoekstra et al. 2017) Historically, botanists have been reluctant to provide a and the targeted enrichment of nuclear genes (Hart classification for genera in the magnoliid family et al. 2016), both for phylogenetic and evolutionary Annonaceae. Even though subfamilies and tribes were studies. described by eminent botanists such as Rafinesque In this paper, we present a linear sequence of (1815), Endlicher (1839), Hooker & Thomson (1855) genera of Annonaceae. Generally, the family is among and Baillon (1868), these were hardly used