Unveiling the many meanings of the term ‘naked bud’

In recent work, we shed light on the vastly understudied phenomenon of naked resting buds in temperate, woody species: buds that, while dormant between subsequent growing seasons, overwinter without cataphyll protection. We did this by creating a classification system for resting bud morphologies (Schoonderwoerd & Friedman, 2021). A comment by Burrows (2022) describes in detail the bud architecture and phenological features of Eucalyptus, a taxon that we listed as possessing naked buds to acknowledge its long-standing association with the term naked bud in the literature (e.g. Carey, 1930; Schulze, 1934; Jacobs, 1935, 1955; Bean & Russo, 1989; Waters et al., 2010; Burrows, 2013). Burrows' comment perfectly illustrates the challenges and complexities of the morphological classification process in the absence of year-round direct observations. Interpreting a morphological structure from written sources that use imprecise morphological language (Jones, 2021); that appear to directly contradict each other (Schoonderwoerd & Friedman, 2021); and that describe only a single phenological stage is not a straight-forward task. Therefore, reactions from experts on local flora and taxonomic groups are most valuable contributions. We appreciate that Burrows (2022) agrees with our decision to exclude axillary eucalypt buds from our climate and trait analyses because of their incompatibility with naked resting buds of the northern hemisphere (and that he shares our scepticism of the geographical patterns in Australia generated with our database). We also welcome the opportunity to think more deeply about a huge and fascinating taxon that, although it did not play a part in the findings of our original study, may contribute to important insights on the morphology and architecture of buds with and without dormancy—as we will show here. Burrows' comment (2022) concerns the classification of the axillary bud present in the axil of recently expanded eucalypt leaves, which, in the words of Graham et al. (1998) ‘is often called the naked bud to distinguish it from the protected accessory buds’. This terminology appears to have been popularised by the work of M.R. Jacobs (1935), but has not been universally adopted. Cremer (1972), for example, used the term ‘primary bud’ to refer to the same structure and Hallé et al. (1978) noted that “it is interesting that Eucalyptus would be described as having ‘naked’ buds in a morphological sense”. Clearly, as we showed in our recent work, morphological descriptions of buds as ‘naked’ are all too often a point of contention. To understand why, careful evaluation is required of several features of the bud structure in question. Unlike Cremer and Hallé et al., Burrows (2022) supports the usage of the term naked buds for the axillary structures of Eucalyptus, but he calls into question that these should be classified as ‘archetypal’, one of our six morphological categories of naked buds. While we agree, upon review, with Burrows' assessment that the primary axillary buds of eucalypts are not archetypal naked buds, it is not the bud morphological structure itself that precludes Eucalyptus from being classified as ‘archetypal’. Like the naked resting buds that we classified as ‘archetypal’, most eucalypt axillary structures match these three morphological criteria: (1) they do not contain specialised scale leaves (cataphylls); (2) the lamina of each leaf contained in the bud will be fully expanded; and (3) the outermost leaves occupy a position in the bud that directly exposes them to the aerial environment (Schoonderwoerd & Friedman, 2021). Rather, the problem is that these buds are not resting buds. In most Eucalyptus species, according to Burrows, the axillary structures either produce sylleptic branches (reviewed in Barthélémy & Caraglio, 2007), or they are aborted. ‘They do not undergo prolonged dormancy’ (Graham et al., 1998). This conclusion has two important implications. First, it adds one further morphological structure that has been described using the nebulous term naked bud to the various distinct resting bud forms described in Schoonderwoerd & Friedman (2021). But, most interestingly (at least from our perspective), according to Burrows (2022) and Cremer (1972), these abortive axillary structures appear to have transitioned into archetypal naked overwintering buds in at least one species, Eucalyptus regnans, which might offer further insight into the ancestral state of lineages with naked resting buds (Jones, 2021; Schoonderwoerd & Friedman, 2022). From a functional perspective, the structures that most closely resemble resting buds (buds that lead to delayed or proleptic branching) in the majority of eucalypts are the accessory buds, which are endogenously formed and recessed in the cortex (young stems) or bark (older stems). These buds may or may not bear cataphylls (Burrows, 2022), but they certainly are not exposed naked buds (sensu Schoonderwoerd & Friedman, 2021). They do not have embryonic foliage leaves that are exposed to the aerial environment during the resting period. Rather than an adaptation to frost avoidance – as might be hypothesised in species that grow in climates with a winter with frequent freezing temperatures (the focus of our study) – these recessed accessory buds are likely to reflect a history of evolution in fire-prone habitats (Burrows et al., 2010; Waters et al., 2010; Burrows, 2013). Other than for environments with severe frosts, there are data supporting recessed buds as a likely adaptation to fire exposure. Most recently, a study on bud types in species along transects from fire-prone open savanna to wooded areas in the Cerrado of southeastern Brazil revealed that in fire-prone environments a larger proportion of species have buds that are mostly or completely recessed in the bark compared with environments in which fire is absent (Chiminazzo et al., 2021). It is interesting to consider that, although fire is probably the major cause of ecological disturbance for most eucalypts, their resprouting strategy can be equally effective after damage caused by frost, herbivory or other ecological drivers. As Burrows (2022) notes in response to our geographic summary, the distribution ranges of many woody species that experience frost in certain localities often expand into regions where frost rarely or never occurs. In other words, it is not uncommon for woody species to function in a wide range of climates using the same architectural blueprint. (Please refer to Edwards et al. (2015) for a discussion of the distribution ranges of the freezing-exposed species in the database compiled by Zanne et al. (2014).) If the (resting) accessory buds of eucalypts are the source of much of the growth and regeneration in trees – and if we hypothesise that their recessed position is adaptive – this begs the question why the Eucalyptus sylleptic axillary structures are present alongside another type of bud. After all, the axillary ‘naked buds’ are aborted in most instances. According to Jacobs (1935, 1954, 1955), the axillary structures allow for a rapid expansion of the shoot system under favourable circumstances, precisely because no dormancy is required between bud initiation and leaf expansion. Eucalypts can expand several orders of branches, all from axillary buds, in a single season (Jacobs, 1954). By contrast, resprouting from accessory buds may take longer, because the accessory buds are less developed than the axillary structures or because seasonality influences the interval between the time of disturbance and resprouting (Ceulemans et al., 1996). These observations take on new meaning in light of our thesis that resting bud structure is inextricably linked with shoot growth (Jones, 2021; Schoonderwoerd & Friedman, 2021, 2022). We hypothesised that, in certain lineages of woody plants, a trade-off might exist between, on the one hand, the ability of leaf growth to respond to current conditions within the growing season and, on the other hand, the development of a highly protected resting bud with cataphylls. This trade-off could potentially be an evolutionary selective force behind resting bud structure (Schoonderwoerd & Friedman, 2021, 2022). By the physical separation of buds that respond to current growing conditions (axillary buds) and buds that lie dormant (accessory buds), such a trade-off might have been decoupled in most of the eucalypts. Another potential functional consequence of the coexistence of the two different bud types to be considered lies in the kind of leaves that each bud type produces. In certain species of Eucalyptus, sprouts from epicormic and accessory buds (promoted, for example, through pruning in horticulture) produce juvenile leaves, whereas unimpeded growth ultimately leads to branches that bear leaves with an adult morphology (Ceulemans et al., 1996; Wirthensohn & Sedgley, 1998). Consequently, expanding a shoot from an axillary structure (vs an accessory bud) could hypothetically have consequences for photosynthetic productivity, both because of the phenology of leaf expansion and maturation, as well as because of the leaf shape and function of the produced leaves. Because our paper (Schoonderwoerd & Friedman, 2021) did not identify a clear association between resting bud structure and frost and cold winter temperatures, it is most interesting to consider how resting bud structure (and, in the case of Eucalyptus, branching patterns) might be shaped in the context of other ecological and evolutionary drivers such as fire, drought and herbivory. Work that describes the resting bud structures of local floras is a valuable resource for these types of questions, particularly work concerning regions for which traditional winter identification guides are not available. The paper by Gladys Carey (1930) on the flora of New South Wales that is highlighted by Burrows is a case in point. It is worth reflecting on the fact that over 90 yr after Carey (1930) responded to Foster's (1928) classic paper on northern-hemisphere buds (and the supposed rarity of naked resting buds), there is still much to be learned about the basic developmental morphology, architecture and functional biology of resting buds of the world's ecosystems, and other buds without prolonged dormancy! We thank Liesbeth Uijtewaal–de Vries for a guided tour of her private collection of Australian plants and for sharing her expertise in growing eucalypts in the Netherlands.