Evolution of plant architecture, functional diversification and divergent evolution in the genus Atractocarpus (Rubiaceae) for New Caledonia

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Linking functional traits and plant architecture

Growth habit results from the integration of a combination of several individual traits (e.g. branching pattern, body size and shape, position of inflorescences, anatomy…) that have often been studied separately (e.g. Carlquist, 1984; Givnish et al., 2009; Isnard et al., 2012; Wagner et al., 2014). As such, growth habit provides some evidence for the correlated evolution (sensu Pagel, 1994) of two or more traits across lineages. Some of these trait associations, known as global spectra (e.g. Reich et al., 2003; Wright et al., 2004; Chave et al., 2009; Díaz et al., 2016), are considered as primary drivers of plant evolution and functional diversity worldwide (Díaz et al., 2004; Poorter and Bongers, 2006; Díaz et al., 2016). Among the oldest and best documented are Corner’s rules (Corner, 1949, 1953-1954) describing a universal correlation between branching intensity, leaf size, stem size, fruit size, and inflorescence complexity (Corner, 1949; White, 1983b; Bond and Midgley, 1988; Lauri, 1988; Brouat et al., 1998; Cornelissen, 1999; Brouat and McKey, 2001; Westoby et al., 2002; Preston and Ackerly, 2003; Westoby and Wright, 2003; Pickup et al., 2005; Sun et al., 2006; Normand et al., 2008). As such, selection on a single trait is likely to affect whole plant form and function (Figure 1.2). In this context, evolution of growth habit needs to be Plant architecture characterizes the spatial arrangement and specialization of structures (morphological origin, branching pattern, axis categorization) and their evolution during ontogeny (Hallé et al., 1978; Barthélémy and Caraglio, 2007, see Chapter 2 for more details). It can consequently highlight how plant structure correlates with function and help identify the evolutionary processes behind plant evolution (see Bateman, 1994; Bateman, 1999; Sussex and Kerk, 2001; Meyer-Berthaud et al., 2010). Architectural studies have taught us that plants are modular organisms composed of structural elements that can differ in their organization and function (Hallé et al., 1978; Barthélémy and Caraglio, 2007). For instance in many tree and treelet species, the trunk mainly assumes exploration and support functions while branches are, in comparison, more specialized in assimilation and reproduction. As such, plant architecture provides integrative tools to understand plant spatial and temporal exploitation of resources (Barthélémy and Caraglio, 2007; Smith et al., 2014). Architectural traits have been shown to impact plant fitness either directly (Küppers, 1989; Millet et al., 1999; Charles-Dominique et al., 2010; Charles-Dominique et al., 2012; Millan, 2016; Charles-Dominique et al., 2017) or in interaction with other functional traits (Pérez-Harguindeguy et al., 2013; Trueba et al., 2016). Plant architecture thus has much to offer in comparative studies that aim to decipher the evolution of plant growth habits and their associated traits.

The monocaulous growth habit

From the above architectural background, we know that plant functions are generally partitioned into different axis categories. However, among the diversity of extant and past known architectures (see Galtier and Hueber, 2001; Hallé, 2004; Meyer-Berthaud and Decombeix, 2009; structure that they are constituted by a single stem (Hallé et al., 1978).
Monocauly classically characterizes woody plants constituted by a single unbranched trunk supporting a distal rosette of large leaves (Corner, 1949). The term was used in various domains, and formal definitions – when provided – often differ among studies (see Chapter 3 for a more detailed review). This growth habit, particularly atypical for non-monocots, has fascinated naturalists for a long time (e.g. Von Humboldt, 1808; Cotton, 1944; Corner, 1949; D’Arcy, 1973; Hedberg and Hedberg, 1979) and is at the center of highly discussed ecological and evolutionary theories. Monocaulous species were long considered as relicts of the ancestral form for Angiosperms (Corner, 1949). Recent molecular phylogenies have indicated multiple recent evolution of monocauly in Angiosperms (e.g. Chomicki et al., 2017) but the evolutionary history of extant monocauls remains unclear. Monocaulous plants were also at the inception of Corner’s rules (Corner, 1949, 1953-1954) (Figure 1.2), whose statements are today among the most widely documented global spectra (leaf – stem scaling or foliage – stem scaling, e.g. Westoby and Wright, 2003; Olson et al., 2009; Yang et al., 2009). Probably because of their global rarity and restriction to tropical areas, monocaulous species have rarely been included in ecological and evolutionary studies. The most famous case of the evolution of monocauly is represented by “unbranched shrubs.

Geological and Paleoclimatic history

New Caledonia’s main island (along with Belep and the Ile des Pins) is a part of the New Caledonian ridge that split and spread from the eastern margin of the Gondwanan supercontinent during the Cretaceous (ca. -120 to -80 Myr) (Picard, 1999; Cluzel et al., 2001; Pelletier, 2006; Cluzel et al., 2012). The presence of numerous endemic relictual lineages on the island led some authors to think that this piece of Gondwana remained emerged from the rifting event until today (e.g. Raven and Axelrod, 1972). However geological insights have shown that New Caledonia was submerged from the Paleocene to the Eocene (ca. -62 to -50 Myr) at which time it was obducted under the Pacific plate and covered by oceanic crust (Picard, 1999; Cluzel et al., 2001; Pelletier, 2006; Cluzel et al., 2012), leading to the formation of metamorphic rocks and to the atypical ultramafic substrate. New Caledonia reemerged during the Eocene (-50 to -35 Myr, and probably ca. -37 Myr) after which the ultramafic layer progressively weathered to the present day resulting in the partial exposure of subjacent volcano-sedimentary substrates. This scenario is coherent with the evolutionary history of several New Caledonian lineages which suggests that local radiations are younger than 37 Myr (Murienne et al., 2005; Grandcolas et al., 2008; Pillon, 2012). The Loyalty Islands emerged more recently (Pliocene, ca. -2 Myr) through an uplifting of the Loyalty ridge (Picard, 1999; Pelletier, 2006).
Paleoclimatic data indicate that the Southwest Pacific has experienced a general cooling since early Neogene (ca. -23 Myr), leading to an increase in aridity (Gallagher et al., 2001; Zachos et al., 2001; Dodson and Macphail, 2004). This trend was punctuated by several more or less pronounced oscillations such as the drastic increase in both temperature and precipitation in the Miocene (ca. -15 to -17 Myr, Zachos et al., 2001; Böhme, 2003) coupled with intense cooling (Gallagher et al., 2003; Dodson and Macphail, 2004). This overall climate aridification had important consequences on vegetation, especially a decline of rainforest areas, which probably disappeared in some regions such as Australia (Gallagher et al., 2003; Crisp et al., 2004; Dodson and Macphail, 2004; Byrne et al., 2008; Byrne et al., 2011). For New Caledonia, paleoclimatic data are scarce but its small size and isolated position in the Pacific are thought to have buffered the effects of general aridification (Barrabé, 2013). Nevertheless, the archipelago is likely to have experienced several glacial episodes during the Neogene (ca. -6.5 Myr) and Quaternary (ca. -2.5 Myr) (Chevillotte et al., 2006; Karas et al., 2011) and also more recently (-22000 and -12000 yr, Tournebize et al., 2017). Despite these glacial episodes, rainforests seem to have continuously persisted in New Caledonia for quite a long period (Hope and Pask, 1998; Stevenson and Hope, 2005; Tournebize et al., 2017), contrary to adjacent regions (Kemp, 1978; Gallagher et al., 2003.

Plant architecture

Plant architecture is a domain of plant science that concerns the nature and organization of plant parts and their evolution during ontogeny. It emerged with the fundamental works of Hallé et al. (Hallé and Oldeman, 1970; Hallé et al., 1978) in which fundamental principles of plant morphology (growth patterns, branching modalities, axis differentiation, and the position of reproductive functions) were combined into a comprehensive and dynamic approach to define 23 architectural models. These models illustrate both the general architecture of a plant and the way it was constructed (Hallé and Oldeman, 1970; Hallé et al., 1978; Barthélémy et al., 1989; Nicolini, 1997) (Figure 2.3-A). While compelling for the recognition of common overall species forms, architectural models appeared too general to understand fines aspects of complex plant construction (Edelin, 1977; Barthélémy and Caraglio, 2007).
A deeper characterization of plant architecture came with the development of notions of axis category and architectural units (Edelin, 1977, 1984; Barthélémy et al., 1989; Barthélémy et al., 1991). Individuals of each species are made of a limited number of axis categories (1-6), each characterized by a non-limitative combination of morphological, anatomical and functional traits (Figure 2.3-B). The number of axis categories, their characteristics and their spatial arrangement determine the so-called architectural unit, i.e. the species-specific expression of an architectural model (Barthélémy and Caraglio, 2007). The higher an axis category (i.e. situated at the periphery of the plant), the more functionally specialized it is (Barthélémy and Caraglio, 2007). For example, in most of tree and treelet species, trunks (axis category 1 = C1) have the general functions of support and storage. The more the axis number increases (C2, C3…), the more specialized the axis is in exploration, photosynthesis and reproductive functions. Extreme examples of axis specialization are provided by some inflorescences for reproduction function (Van Steenis, 1963; Hallé et al., 1978) or by phyllomorphic branches for photosynthesis (Corner, 1949; Hallé, 1967; Hallé et al., 1978).

Toward a new definition of monocauly: between structure and function

Plant architecture has taught us that plant form is due to the genetically controlled association of several structuro-functionnal entities (phytomers, growth units, axis categories, reiterates…) whose arrangement and differentiation change with age and are shaped by the environment. This integrative approach revealed objective criteria that could be powerful for defining growth habit (Millan, 2016). For instance, among the few attempts to define the monocaulous habit (see Chapter 3), that of Hallé et al. (1978) is probably the most successful.
These authors made the distinction between the structural definition (“trees with a single axis” = monoaxial) and the physiognomic definition (“trees with a single trunk or visible stem of the plant” = monocaulous). The latter, referring to the general appearance of the plant rather than its structural construction, seems more appropriate for an ecological study since it is directly linked with the space exploration strategy of species. To pursue this functional aspect of growth habit further, monocauls could be defined as “self-supporting woody plants whose cardinal functions rely on a single visible stem”. This functional definition, better suited to studying the adaptive aspects of growth habit, is the one we will use here. Beyond giving a clear physiognomic definition of monocauly, the architectural approach of Hallé et al. (Hallé and Oldeman, 1970; Hallé et al., 1978) was the first to provide clear discriminating morphological criteria. The classification of a species in the monocaulous class relies on the selection of structural types fitting the given definition of monocauly. In the work of Hallé et al. (Hallé and Oldeman, 1970; Hallé et al., 1978), structural types corresponded to architectural models. This classification, while providing a fundamental basis for plant architecture, nevertheless appeared to be too general to understand the precise architecture of plants and more integrative concepts such as architectural units and reiteration were later developed (see section 2.2). The work of Hallé et al. (Hallé and Oldeman, 1970; Hallé et al., 1978) aimed to present the known diversity of developmental plans observed in tropical trees. Our aim is different, since our interest is to segregate plants for which vegetative functions are assumed by one visible stem, from other plants (i.e. branched). For all these reasons, we will not strictly refer to architectural models to define our structural types of monocauly but our classification will, in essence, largely overlap that of Hallé et al. (1978). Our definition of monocauly, focusing on function rather than structure, includes true woody plants with a single orthotropic entity functioning as a trunk and determined plagiotropic structures functioning as leaves. The only other aboveground structures are those specialized in reproduction (i.e. inflorescences) or are due to exogenous stimuli (i.e. opportunistic reiterates).

Evolution of the monocaulous habit

The oldest known plant macrofossils, dated from ca. 430 Ma (Silurian), were probably isodichotomously branched, producing two daughter branches of similar size (e.g. Cooksonia) with terminal sporangia (Meyer-Berthaud and Decombeix, 2009). They presented a mixture of prostrate and erect axes. This simple morphology is suggested to have been dominant up to the Early Devonian (ca. -400 Myr). Devonian is also the period during which pseudomonopodial branching became widespread. In this mode of branching, daughter branches are different in size and orientation, leading to the appearance of a vertical growth and side branches. This mode of branching is suggested to have played an important role in the evolution toward arborescence (Meyer-Berthaud and Decombeix, 2009; Chomicki et al., 2017). These fossil plants were, however, of small size. The tree growth habit evolved in several lineages via convergent evolution (Niklas, 1997), with the earliest known modern tree dating from the Middle Devonian (-390 Myr) (Stein et al., 2007). In the Earth’s “oldest forest”, these tree-fern-like plants (Cladoxylopsida) had a trunk bearing large branches that probably abscised (cladoptosis or branch shedding), as a “frond-like module” (Stein et al., 2007). The architecture of these fossil plants corresponds to Berry’s model (Chomicki et al., 2017). Archaeopteris, another modern tree from the late Devonian, was shown to form excurrent deciduous branches (Type A, in Meyer-Berthaud’s model, Meyer-Berthaud et al., 1999; Chomicki et al., 2017). Thus, large fossil trees seem to be dominated by non-perennial photosynthetic or lateral structures. Among tree-ferns, an advance level of organization of branching has also been described (Galtier and Hueber, 2001), but most fossil tree-ferns known since the Carboniferous had a monocaulous trunk supporting large compound leaves, comparable to extant tree-ferns of Cyatheaceae and Dicksoniaceae. Plants expressing Corner’s architectural model are known from the early Devonian (ca. -400 Myr) and the Holttum’s model dates back to at least the Late Devonian (ca. -355 Myr), i.e. before the appearance of most extant and extinct architectural models (Chomicki et al., 2017). While these first unbranched plants probably do not fit with our definition of true woody monocauly (vascular cambium of extant species appearing in the late Triassic (-220 Myr, Savidge, 2008), they show that unbranched architectures were clearly more represented in the past. It was particularly abundant from the Carboniferous (ca. -350 Myr) to the early Cretaceous (ca. -110 Myr), representing between ca. 20% and 40% of the total fossil record for which information is available (Chomicki et al., 2017). From the early Cretaceous, the proportion of taxa with an unbranched architecture gradually decreased in favor of architectures expressing axillary branching. This is in agreement with the rise of small-leafed and highly branched angiosperms, which have progressively replaced the often large-leafed monocaulous habit of ferns and progymnosperms (Coiffard et al., 2012). Today, the monocaulous habit is estimated to represent only ca. 2% of the total known architectures (Chomicki et al., 2017).
The abundance and diversity of monocaulous forms in the floras of the Paleozoic and Mesozoic has often led scientists to consider it as primitive for seed plants (Galtier, 1999) or Angiosperms (Hallier, 1912 in Meeuse, 1967). In his Durian theory on the origin of the modern tree, Corner (1949) suggested that “the more remote ancestors [=of Angiosperms] appear to have been monocarpic and monocaulous, with the Cycad-habit”. This idea was supported by early classifications in which Cycas was placed as sister to Gymnosperms and Angiosperms. Such a primitive form was thought to have gradually evolved toward branched forms (with smaller and simpler leaves, flowers, seeds and fruits) to colonize drier and colder habitats, leading in the extant Angiosperm architectural diversity. Corner (1949) argued that extant monocaulous species, occurring in several tropical families, are “relicts” of this ancestral form. Other authors have suggested that the occurrence of monocauly in numerous unrelated families is instead evidence of recent convergent evolution (Richards, 1966; D’Arcy, 1973), the simplicity of monocaulous forms no being synonymous with “antiquity” (Mabberley, 1974b; Hallé et al., 1978). Recently, the rise of molecular phylogenies has largely supported this second view and – while the ancestral growth.

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Life history and environmental traits associated with monocauly

Like all growth habits (see section 1.3), monocauly is not only characterised by an unbranched stem but also by a large set of morpho-physiological traits. The most striking feature, inherent in most terms used to describe monocauls (see section 3.1), is the presence of large leaves.
This relationship between branching intensity and leaf size is an element of Corner’s rules (Corner, 1949, 1953-1954). These rules concern two fundamental statements: (i) Axial conformity, stipulating that “the stouter, or more massive, the axis in a given species, the larger and more complicated its appendages” and (ii) Diminution on ramification, stipulating that “the greater the ramification, the smaller become the branches and their appendages” (Corner, 1949). By “appendages”, Corner meant leaves, fruits, inflorescences and flowers. Consequently, monocauls are not only expected to have larger leaves but also a thicker stem, larger fruits and more complex inflorescences (Figure 1.2). The relation between leaf area and twig thickness, namely the worldwide leaf size – twig size spectrum (Westoby and Wright, 2003), and to a lesser extent the relation between leaf area and fruit size, has been extensively investigated (White, 1983b; Bond and Midgley, 1988; Brouat et al., 1998; Cornelissen, 1999; Brouat and McKey, 2001; Westoby et al., 2002; Preston and Ackerly, 2003; Westoby and Wright, 2003; Pickup et al., 2005; Sun et al., 2006; Normand et al., 2008). On the other hand, the relation with branching intensity (i.e. Diminution on ramification) received much less consideration. Few studies have shown a negative correlation between branching intensity and twig cross-sectional area or leaf size (White, 1983b; Ackerly and Donoghue, 1998; Westoby and Wright, 2003) or inflorescence length (Ackerly and Donoghue, 1998) but, as far as we are aware, never with fruit size. Moreover, none of these studies included monocaulous species and the measurement methods used to quantify branching intensity are highly variable in the literature. For example, some authors measured the number of active growing tips on whole plants (White, 1983b; Ackerly and Donoghue, 1998) while others measured the mean length between apices and the first branch (Westoby and Wright, 2003), the proportion of trunk nodes producing branches (Ackerly, 1996), or the number of non-branched nodes between two branched nodes (Thomasson, 1972). Such discrepancies call for the need for the definition of a standardized index measuring branching intensity in relation to plants architecture and function. Consequently, our understanding of the relationships between monocauly and life history trait attributes largely comes from empirical observation and virtually never from attempts to quantify them. Such associations concern cauliflory (Hallé and Mabberley, 1976; Hallé et al., 1978; Barthélémy, 1988; Schmid, 1990), compound leaves (Corner, 1949; Hallé, 1967; Hallé and Mabberley, 1976; White, 1983a), short internodes (Corner, 1949; Chuah, 1977; Hallé et al., 1978; Sussex et al., 2010), dioecy (Hallé et al., 1978), rhythmic growth (Hallé et al., 1978), and high slenderness (D’Arcy, 1973). Their relationship with standard functional traits such as SLA (Specific Leaf Area) or related traits (see Wright et al., 2004) are difficult to estimate given that studies have never clearly included monocauls and that the relation with leaf area is unclear (Westoby and Wright, 2003). In terms of anatomy, studies suggest that pith area along with stem size and leaf area generally increase during ontogeny until the branching point and then progressively decrease (Eggert, 1961; Lauri, 1988). This in turn suggests a higher pith size in the distal part of the stem for monocaulous species than for branched taxa, as confirmed by several studies (Cotton, 1944; Carlquist, 1974; Mabberley, 1974a; Hallé et al., 1978; Meinzer and Goldstein, 1986). Research also suggests that monocauls have a large cortex (Cotton, 1944; Mabberley, 1974a; Hallé et al., 1978; Mosbrugger, 1990) and a thin wood layer composed of a high proportion of parenchyma (Cotton, 1944; Mabberley, 1974a; Aldridge, 1978). The relation between monocauly or pachycauly and vessel or fiber size has been investigated indirectly (Aldridge, 1978; Aldridge, 1981) but results are blurred by the variety of sampled environmental conditions. The life history and functional characteristics of monocaulous plants, as suggested by the published literature, are summarized in Figure 3.2.

Genus diversity and endemism

The presence of monocaulous species in a genus was significantly and positively associated with species richness (phylogenetic regression, pvalue < 0.001) implying that species-rich genera were more likely to have evolved monocauly or that the evolution of monocauly favored genera diversification. The proportion of endemic species in the monocaulous flora (98.9%) was significantly higher than expected by chance (permutation test, pvalue < 0.001). Only two monocaulous species (ca. 1%) were not New Caledonian endemics (Delarbrea paradoxa and Oxera baladica) compared to 9 % for the branched woody flora. By contrast, endemism at the generic level was low (21.9% vs. 22.9% for the branched flora) and unrelated to the occurrence of monocauly (phylogenetic regression, pvalue = 0.75 ± 0.01). Only 9 of the 72 endemic genera in our list (sensu Munzinger et al., 2016) contained monocauls (Acropogon, Beauprea, Bocquillonia, Dutaillyea, Mangenotiella, Phelline, Pycnandra, Salaciopsis, and Virotia, Figure 5.3).

Table of contents :

Chapter 1 — General Introduction
1.1 Islands as models in ecology and evolution
1.2 Convergence and adaptive value of traits
1.3 Convergence in growth habit
1.4 Linking functional traits and plant architecture
1.5 The monocaulous growth habit
1.6 Problematic and objectives
1.7 Thesis outline
Chapter 2 — General methodology
2.1 Study location: the New Caledonian archipelago
2.1.1 Geography and abiotic environment
2.1.2 Geological and Paleoclimatic history
2.1.3 Flora and vegetation
2.2 Plant architecture
2.3 Toward a new definition of monocauly: between structure and function
2.4 List of monocaulous species
Chapter 3 — The monocaulous growth habit: a review
3.1 History and definitions
3.2 Evolution of the monocaulous habit
3.3 Life history and environmental traits associated with monocauly
Chapter 4 — Novitates neocaledonicae VII: A new monocaulous species of Bocquillonia (Euphorbiaceae) from New Caledonia
4.1 Introduction
4.2 Material and Methods
4.3 Taxonomy
4.4 Identification key of McPherson & Tirel (1987), modified to include B. corneri.
Chapter 5 — A remarkable case of evolutionary convergence: correlated evolution and environmental contingencies of monocauly in the flora of New Caledonia
5.1 Introduction
5.2 Materials & methods
5.2.1 Definition of monocauly
5.2.2 Species list and phylogenetic trees
5.2.3 Character coding
5.2.4 Data analysis
5.3 Results…
5.3.1 Taxonomic and phylogenetic distribution of monocaulous plants
5.3.2 Genus diversity and endemism
5.3.3 Evolution of monocauly and phylogenetic signals
5.3.4 Contingent and correlated evolution
5.3.5 IUCN risk of extinction status and threats
5.4 Discussion
5.4.1 A remarkable evolutionary convergence
5.4.2 Diversity and endemism of monocaulous lineages
5.4.3 Life history correlates of monocauly
5.4.4 Evolution of plant architecture
5.4.5 A threatened and poorly known growth habit
5.4.6 Environmental contingency and ecological opportunities in New Caledonia.
5.4.7 Conclusions and future directions
Chapter 6 — Evolution of plant architecture, functional diversification and divergent evolution in the genus Atractocarpus (Rubiaceae) for New Caledonia
6.1 Introduction
6.2 Material and methods
6.2.1 Sampling
6.2.2 Branching index and plant architectural traits
6.2.3 Plant functional traits
6.2.4 Data analysis
6.3 Results…
6.3.1 Branching index
6.3.2 Architectural characterization
6.3.3 Functional characterization
6.3.4 Ancestral Character Estimation
6.3.5 Trait based diversification
6.4 Discussion
6.4.1 Evolution of plant architecture
6.4.2 Branching index, Corner’s rules, and ecological strategies
6.4.3 Divergence and ecological opportunities in New Caledonian rainforests
6.4.4 Conclusions
Chapter 7 — Back to Corner: functional characterization and leaf – stem scaling in monocaulous plant
7.1 Introduction
7.2 Material & methods
7.2.1 Study site and sampling
7.2.2 Traits analyzed
7.2.3 Data analysis
7.3 Results…
7.3.1 Functional differences between monocaulous and branched species
7.3.2 Anatomical implication of foliage – stem scaling
7.4 Discussion
7.4.1 Toward a functional characterization of rainforest monocaulous habit
7.4.2 Toward a functional explanation of the foliage – stem scaling
7.4.3 New Caledonian monocauls, a special case of monocauly?
Chapter 8 — General Discussion and Conclusions
8.1 Monocauly in New Caledonia: evolutionary convergence and an element of the archipelago’s functional disharmony?
8.2 Ecological and evolutionary implications of monocauly
8.2.1 A well-defined functional strategy
8.2.2 Environmental constraints on monocauly
8.2.3 Environmental correlates of monocauly in New Caledonia
8.2.4 Monocauly and species diversification
8.3.1 Architectural and functional traits to define growth habits
8.3.2 Heterochronic evolution
8.3.3 The reiteration process: a gap that needs to be filled
8.3.4 Constrained evolution of plant architecture
8.4 Conservation of the flora
8.5 Out of New Caledonia: monocaulies rather than monocauly?
8.6 Conclusion and perspectives


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