Introduction

Tephroseris (Rchb.) Rchb., considered to contain 15 species by its last monographer (Cufodontis 1933) but more recently estimated to contain c. 50 species (Nordenstam 1978, 2007), is most closely related to Nemosenecio (Kitam.) B. Nord. and Sinosenecio B. Nord., a group of genera classified as subtribe Tephroseridinae C. Jeffrey & Y. L. Chen by Jeffrey & Chen (1984) and recovered as a well-supported monophyletic group in a molecular phylogenetic analysis of Senecioneae (Pelser & al. 2007). This clade is part of a larger clade known as the Ligularia–Cremanthodium–Parasenecio complex (L–C–P complex; Liu & al. 2006) which, besides Tephroseris, Nemosenecio and Sinosenecio, contains Cremanthodium Benth., Farfugium Lindl., Ligularia Cass., Ligulariopsis Y. L. Chen, Miricacalia Kitam., Parasenecio W.W. Smith & Small, Sinacalia H. Rob. & Brettell and Syneilesis Maxim. as understood by Nordenstam & al. (2009). This complex in turn is part of Tussilagininae s.str. (Nordenstam & al. 2009).

Tephroseris, Nemosenecio and Sinosenecio have been differentiated, among other characters, using leaf morphology (Jeffrey & Chen 1984; Nordenstam 2007). Thus, Tephroseris has been described as having pinnately veined, subentire or dentate leaves, Nemosenecio as having pinnately lobed or dissected leaves, and Sinosenecio as having palmately veined leaves (after exclusion of S. hainanensis (Chang & Tseng) C. Jeffrey & Y. L. Chen, with pinnately veined leaves, as Hainanecio Y. Liu & Q. E. Yang by Liu & Yang [2011]). Pinnate vs. palmate first-order vein topology represents the two major states of leaf venation in eudicotyledonous angiosperms, is not variable within species and has been used to describe higher-rank taxa (Hickey & Wolfe 1975). In the most recent molecular systematic study of Tephroseris, aimed at further investigating its circumscription (Wang & al. 2009), it was found that S. koreanus (Kom.) B. Nord. and S. newcombei (Greene) J. P. Janovec & T. M. Barkley fall into Tephroseris. Accordingly, the two species have been combined into Tephroseris as T. koreana (Kom.) B. Nord. & Pelser and T. newcombei (Greene) B. Nord. & Pelser by Nordenstam & Pelser (2011). On the other hand, T. changii B. Nord. was found to group outside Tephroseris. Close relationships of S. koreanus and S. newcombei to Tephroseris had been shown before by Golden & al. (2001), and a close relationship of T. changii to parts of Sinosenecio had been suspected by Jeffrey & Chen (1984). Beyond the relationships of the above two species of Sinosenecio to Tephroseris, Sinosenecio has been shown to be non-monophyletic (Wang & al. 2009; Ren & al. 2017). Because T. koreana and T. newcombei were considered to have palmately veined leaves (Wang & al. 2009), although Golden & al. (2001) described the venation pattern in T. newcombei (Fig. 1) as “clearly not strictly palmate”, Wang & al. (2009) concluded that characters used for the delimitation of Nemosenecio, Sinosenecio and Tephroseris, such as leaf venation, show widespread homoplasy.

Fig. 1.

Leaf shape and venation (abaxial leaf surface) and cross-sections (A, D, F, G; level of section indicated by dashed lines) of leaf bases. – A: Tephroseris integrifolia; B: T. newcombei; C: Senecio vulgaris; D: Jacobaea vulgaris; E–G: Ligularia stenocephala; E: basal leaf; F: middle cauline leaf; G: upper cauline leaf. – Circles in cross-sections represent vascular bundles. – Scale bars: all 5 mm.

While revising Tephroseris for a work in preparation by the first author, it became evident that leaf venation cannot really be described as pinnate when compared to leaf venation patterns in, e.g., Jacobaea Mill. and Senecio L. Also, pinnate leaf venation appears to be rather rare in the Ligularia–Cremanthodium–Parasenecio complex. Within the L–C–P complex, Cremanthodium has been described as having palmately, pinnately or parallel-veined leaves (Liu & Illarionova 2011), Farfugium as having palmately veined leaves (Nordenstam 2007), Ligularia as having palmately or pinnately veined leaves (Liu & Illarionova 2011), Ligulariopsis as having pinnately veined leaves (Nordenstam 2007), Miricacalia, Sinacalia and Syneilesis as having palmately veined leaves (Nordenstam 2007; Sinacalia: palmately veined or nearly so) and a clearly non-monophyletic Parasenecio (Ren & al. 2017) as usually having palmately veined leaves (Nordenstam 2007). The Parasenecio segregates, Japonicalia C. Ren & Q. E. Yang and Taimingasa (Kitam.) C. Ren & Q. E. Yang, appear to have palmately veined leaves.

The aim of this paper is to examine leaf venation in Tephroseris in order to find out whether the genus indeed contains species with either pinnately or palmately veined leaves, as claimed in the literature (Wang & al. 2009). For this purpose, we will compare leaf venation in Tephroseris with leaf venation in species of Senecio L. and Jacobaea Mill. with clearly pinnately veined leaves, and with a species of Ligularia, representing the L–C–P complex, with clearly palmately veined leaves.

Material and methods

Results

Leaf shape and leaf venation (lower leaf surface) and leaf base cross-sections are shown in Fig. 1. Senecio vulgaris (Fig. 1C) and Jacobaea vulgaris (Fig. 1D) have pinnately veined leaves with one primary vein with lateral veins departing at more or less regular intervals toward the leaf tip. The petiole of S. vulgaris contains three vascular bundles and the petiole of J. vulgaris contains five vascular bundles. In contrast, clearly three primary veins enter the leaf in Tephroseris integrifolia (Fig. 1A) and more than five vascular bundles can be seen in cross-section. In T. newcombei (Fig. 1B), described as palmately veined in the literature, more than one primary vein can be seen entering the leaf. Ligularia stenocephala has clearly palmately veined basal leaves (Fig. 1E). The upper cauline leaves of this species have three primary veins, and five vascular bundles are visible in cross-section (Fig. 1G). In middle cauline leaves (Fig. 1F), several primary veins and several vascular bundles can be seen.

Discussion

Leaf venation in Tephroseris (T. integrifolia), described as pinnately veined in the literature (Jeffrey & Chen 1984; Nordenstam 2007), clearly is different from pinnate leaf venation as seen in Senecio (S. vulgaris) and Jacobaea (J. vulgaris). Whereas in the latter two species the leaves have one primary vein with lateral veins departing at more or less regular intervals toward the leaf tip (Fig. 1C, D), and thus are pinnately veined, T. integrifolia clearly has three veins entering the leaves (Fig. 1A). This difference is evident both from the venation pattern recognizable on the leaf surface and from leaf anatomy as seen in cross-sections. The cross-section of the petiole of J. vulgaris (Fig. 1D) shows, as is typical for Asteraceae (Stevens 2001+), that the primary vein of its leaves contains an arc of five vascular bundles, and three vascular bundles can be seen in S. vulgaris (Fig. 1C). In T. integrifolia, however, cross-sectioned at a similar position, clearly additional lateral vascular bundles can be seen (Fig. 1A), and these correspond to the additional veins entering the leaf from its very base.

It therefore seems clear that description of leaf venation in Tephroseris integrifolia as pinnately veined is inaccurate. Leaf venation in all other species traditionally included in Tephroseris is very similar to that seen in T. integrifolia, and only in species with a distinct petiole is it more difficult to see that more than one vein enters the leaf blade (Kadereit, pers. obs.). Leaf venation seen in T. newcombei (Fig. 1B), described as palmately veined by Wang & al. (2009) but as “clearly not strictly palmate” by Golden & al. (2001), can easily be derived from the T. integrifolia pattern by stronger outward curvature of the veins entering the leaf base, which probably is related to the somewhat reniform shape of the leaf blade of this species. Thus leaf venation pattern in Tephroseris, i.e. including T. koreana and T. newcombei, is essentially uniform and does not fall into two categories that could be described as pinnate or palmate.

The leaf venation pattern seen in Tephroseris does not easily fit into what is considered and illustrated as pinnately and palmately veined in the literature (Hickey & Wolfe 1975; Walls 2011; Sack & Scoffoni 2013). Interestingly, instead of resembling pinnately veined leaves of Jacobaea and Senecio, the leaves of T. integrifolia are similar to the upper cauline leaves (Fig. 1G) of Ligularia stenocephala (Maxim.) Matsum. & Koidz. Ligularia is a member of the L–C–P complex with either palmately or pinnately veined leaves (Liu & Illarionova 2011), and L. stenocephala has clearly palmately veined basal and lower cauline leaves (Fig. 1E). The upper cauline leaves of this species, however, clearly show three primary leaf veins entering the leaf at its very base (Fig. 1G). While the similarity between basal leaves of T. integrifolia and upper cauline leaves of L. stenocephala is evident in the venation pattern recognizable on the leaf surface, there exists a difference in leaf anatomy because only five vascular bundles are visible in the cross-section at the base of an upper cauline leaf of the latter species (Fig. 1G). However, in more transitional leaves a little further down the axis, a pattern similar to T. integrifolia can be seen with additional vascular bundles lateral to the five bundles of the central vein (Fig. 1F). In L. stenocephala, the two very different leaf morphologies seen in one individual are the endpoints of heteroblastic change of leaf morphology along the axis, i.e. ontogenetic change, as very commonly seen in angiosperms, where such heteroblastic change often consists of reduction of morphological complexity (Troll 1939). Although phylogenetic relationships are not well resolved in the L–C–P complex (Liu & al. 2006; Pelser & al. 2007; Wang & al. 2009; Ren & al. 2017), the predominance of palmate leaf venation in the complex (and indeed in Tussilagininae s.str.) make it likely that the condition seen in Tephroseris is derived. If correct, the presence in T. integrifolia of only leaves with several veins entering from the very base can then be interpreted as resulting from a phylogenetic loss of lower cauline leaves. In the context of discussing the evolution of flowering phenologies, reduction in number or loss of leaves observed in early-flowering genotypes has been referred to as “deletion” by Diggle (1999).

When the leaves of Tephroseris, examined in detail in T. integrifolia and T. newcombei, are considered homologous with the upper cauline leaves of L. stenocephala, they could be named palmate-derived. If this interpretation is correct, leaf venation pattern within the L–C–P complex may be less variable than described because the pattern seen in Tephroseris, and described as pinnately veined, fits into the presumable ancestral, palmately veined condition of the L–C–P complex.