Latisemenia longshania, gen. et sp. nov., a new Late Devonian seed plant from China

1. Introduction

The first major evolutionary radiation of seed plants (spermatophytes) occurred in the Famennian of the Late Devonian, when ovules show great diversification in the morphology and structure of integuments and cupules [1–5]. Sometimes, the term seed (fertilized ovule producing an embryo) instead of ovule (unfertilized organ) is used in fossil plants, although usually it is unknown if fertilization has happened [2,6]. Famennian ovules are borne on the tip of an axis or branch (see below), and these earliest ovules are known mainly from Euramerica (Europe and North America). In this study, the coeval Latisemenia longshania gen. et sp. nov. from China presents an opportunity to extend phytogeographically our knowledge of the earliest seed plants. With its derived features, including ovules borne oppositely on the fertile axis, previously unknown for Devonian spermatophytes but common in younger seed plant lineages, Latisemenia contributes also to our understanding of early diversification of seed plants.

2. Material, methods and age

The fossils were collected from the Wutong (Wutung) Formation of Longshan section (GPS data: 30°51′52′′ N, 119°44′53′′ E), Lincheng Town, Changxing County, Zhejiang Province, China. All specimens are deposited in Geological Museum of Peking University, Beijing. Steel needles were used to expose ovules, cupules and fertile axes. Serial dégagement was employed to reveal the morphology and structures of cupule segments, integumentary lobes of ovules, and the nucellar apex. Sections are not informative and maceration of the specimens has failed to reveal the megaspore. Photographs were made with a Nikon digital camera and a Nikon microscope.

Wutong Formation, widespread in the lower reaches of the Yangtze River, including Zhejiang, consists of the Guanshan Member characterized by quartzose sandstone and conglomerate, and the overlying Leigutai Member characterized by inter-beds of quartzose sandstone and mudstone [7]. Assemblages of plants, spores, fish and conchostracans indicate that the Wutong Formation is Upper Devonian (Famennian) in age [7,8]. Concerning the spores of this formation, an AL assemblage (Aneurospora asthenolabrata and Radiizonates longtanensis) from the Guanshan Member is interpreted as Fa2b-c in age, and a LH assemblage (Retispora lepidophyta and Apiculiretusispora hunanensis) of the mid-lower part of the Leigutai Member as Fa2d [7–9]. At the Longshan section, the lower part of the Guanshan Member is not exposed; Latisemenia longshania was found in the mid-upper part (fifth bed) of the exposed strata of this member (electronic supplementary material, figure S1). These data indicate Fa2c age (Famennian) for L. longshania.

From a thin layer of mudstone, we obtained about 120 specimens, with hundreds of ovules preserved as impressions or compressions. Ovules of Latisemenia longshania (figures 1–4) occur with Sphenopteris-like foliage (figure 5), the lycopsid Leptophloeum rhombicum, the progymnosperm Archaeopteris sp. and remains of an unnamed conchostracan invertebrate. Leptophloeum rhombicum and Archaeopteris were distributed worldwide in the Late Devonian [10,11]. Fossils, depositional data and geochemical analyses indicate that the Wutong Formation in the lower reaches of the Yangtze River contains continental sediments but mainly represents littoral zones [12–14], and that the Late Devonian conchostracans lived in brackish and shallow water [15].

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3. Systematic palaeontology

Division Spermatophyta

Latisemenia longshania Wang et al. gen. et sp. nov.

(a) Etymology

Generic name from Latin latus (lateral) and semen (seed) refers to the ovules borne on the side of the fertile axis; the specific epithet from Longshan, the name of the section at the type fossil locality.

(b) Holotype designated here

PKUB13302a, b (Geological Museum of Peking University, Beijing) (figures 1a,b, 2a–f).

(c) Paratypes

PKUB13390 (figure 1e); PKUB13326a, b (figures 3a,b, 4e,i); PKUB13356a, b (figure 4a,d); PKUB13304a (figure 4m); PKUB13357a, b (figure 4o,q).

(d) Locality and horizon

Longshan, Lincheng, Changxing, Zhejiang, China; Guanshan Member of Wutong Formation; Upper Devonian (Famennian).

(e) Generic and specific diagnoses

Fertile axis bearing one terminal ovule and two opposite ovules. Cupules uniovulate and consisting of several free segments; cupule segments five per terminal ovule, elongate cuneate and extending about three-fifths of length of ovule; cupule segments per non-terminal ovule at least three. Ovules oval in shape, radially symmetrical with four integumentary lobes that are flattened and fused for one-half to two-thirds of total length of ovule. With exception of apex, nucellus adnate to fused part of integument. Nucellar apex well below tip of integumentary lobes.

4. Results

The axes to which the ovules are attached are undivided and 0.6–1.0 mm wide (figures 1, 3a–c). The longest axis of 26.8 mm length bears an ovule in what appears to be the lower part of a fertile region (figure 1e). The holotype demonstrates a fertile axis with one terminal cupulate ovule (figures 1a,b, 2a–d) and two additional cupulate ovules borne in an opposite pair on the sides of the fertile axis (figures 1a,b, 2e,f). The distance between the attachment of the terminal ovule and that of two paired ovules is approximately 8.8 mm. The total number of ovules per fertile axis is at least three (figure 1a,b), although more evidence could reveal additional ovules on the axis. Ovules appear to have been readily shed from axes, so that some specimens show only one ovule borne on the side of the axis (figures 1c–j, 3a,b) or just short pedicels where one would have expected to see ovules (figure 3a,b). Terminal ovules are rarely found (figures 1a and 3c) and detached ovules are common (figures 1f lower part, 3d,e, 4a–r).

Cupule segments are often incompletely preserved (figures 1a arrows 1–3, 1e arrow, 1g–j arrows 1–3, 2a arrows, 2b arrow, 2e arrow, 4e arrow, 4f arrow) but the cupules are known to have been uniovulate. Cupule segments appear terete in lateral view (figures 1e arrow, 1g–j arrows 1–3, 2a arrow 1). Dégagement of a terminal ovule presents two free and complete cupule segments (figure 2d arrows 4 and 5) separately in face and oblique-face view, with the former segment clearly showing an elongate cuneate shape. Part (figure 2b arrow 3) and counterpart (figure 2c arrows 1 and 2, 2d arrows 4 and 5) of this dégaged ovule indicate that the total number of segments or tips per terminal cupule may be five. As for another complete cupule segment shown in figure 3c (upper arrow), the distal part in oblique lateral view is expanded and the remaining part in lateral view is terete. These three complete cupule segments, 4.3–6.7 mm long and 1.8–2.0 mm at the maximum width, extend obliquely upwards to as much as 60% the length of the ovule. Serial dégagement of a specimen illustrates an ovule borne on the side of the axis (figure 1i arrow), and in this specimen the cupule appears to consist of only three free segments (figure 1g–j arrows 1–3).

Ovules are oval in shape, 6.3–10.7 mm long and 2.4–5.3 mm at the maximum width. Pedicels of ovules are short and 0.4–1.0 mm long and 0.5–0.9 mm wide at the base (figure 3a,d,e). Three ovules in part and counterpart (figure 4a–i,n–q) and one completely preserved ovule (figure 4j,k) show that the integument possesses four distal broad lobes. Lobes are 2.0–4.2 mm long and 1.2–1.9 mm wide, distally rounded and free in the distal 30–45% of integument length. Integumentary lobes of some ovules appear to curve inward to enclose the nucellus (figures 1c,e,f arrow, 3b–d). One ovule shows the outline of a nucellus (figure 4a arrows) which is closely linked with the integument, but the nucellar apex and megaspore are unclear. Two dégaged ovules display the nucellar apex (figure 4l–o,r arrows), which is well below the tips of the integumentary lobes. These ovules indicate that the nucellar apex extends slightly into the region where the integumentary lobes are free, but the nucellus is mostly adnate to the fused part of the integument. In other cases, the nucellus has not been recognized even through serial dégagement of ovules (figure 4e–k).

Remains of pinnules are closely associated with the ovules but have not been found attached, although in some cases they occur on the same bedding planes (figure 5a arrows). At least four ultimate pinnae are alternately arranged on a penultimate pinna rachis (figure 5b,c). Five to six pinnules occur alternately or suboppositely on the ultimate pinna rachis, which is then terminated by a single pinnule. Pinnules are Sphenopteris-like, laminate, and 7.0–9.0 mm long and 2.3–6.3 mm at the maximum width, with margins entire or three-lobed. Veins are proximally parallel and dichotomize several times, ending at the pinnule margin (figure 5d).

5. Discussion

Latisemenia more closely resembles Pseudosporogonites [4] than any other Devonian ovules in its uniovulate and broad cupules, and in the largely exposed and similarly sized ovules with four broad integumentary lobes (table 1). However, the ovule of Pseudosporogonites is only basally surrounded by a collaret cupule without differentiation into segments, the cupule tip is not higher than the chalaza (fig. 2 in [4]), the integumentary lobes are only fused for one-third of the length of the ovule and their number per ovule is three or four, the lobed integument has been reported to be as long as the nucellus, and the nucellus is free from the integument except at the chalaza [4]. In contrast, the Latisemenia ovule is surrounded by several free cupule segments of elongate cuneate shape, the cupule segments may extend up to three-fifths of the length of the ovule, the integumentary lobes are fused for one-half to two-thirds of the length of the ovule and their number per ovule is consistently four, the integument is much longer than the nucellus, and the nucellus with the exception of apex is fused to the integument.

Ovules first appeared and became abundant in the Late Devonian (Famennian) [2,6]. In almost all cases, these ovules are surrounded by a cupule [4]. While cupules of putative ovules of Cosmosperma have recently been reported from the Famennian of China [5], Latisemenia represents the first unequivocal Devonian ovules found outside Euramerica. Among the earliest seed plants from the Famennian, Latisemenia is the only one known to bear non-terminal ovulate cupules, whereas other Famennian cupules, if found attached, occur singly, in pairs, or in threes on the top of a fertile branch, which is sometimes dichotomous [1,3,4,16–23] (table 1). Where known, these fertile branches are borne cruciately (Moresnetia and Elkinsia) or pinnately (Dorinnotheca) [19–21]. Middle Devonian Runcaria, interpreted as a seed plant precursor, has proto-ovules borne terminally on the branches [24,25]. The branches of Late Devonian seed plants terminated by cupules are long or short; therefore, the short pedicels of Latisemenia ovules may be derived from the reduction of branches with terminal cupules.

The presence of terminal ovules of Devonian spermatophytes and the discovery of non-terminal ovules on Latisemenia document the initial diversification of ovule arrangements in the earliest seed plants. This diversification is manifested by younger seed plants. For example, in the Carboniferous ovules may terminate branches (lyginopterids) or scales (cordaites), or be attached to pinnules (callistophytes) or megasporophylls (peltasperms) [2,26], or occur laterally/terminally on axes or pinna rachises (medullosans) [27,28]. As in Latisemenia, the cupules are sometimes in opposite pairs on the axes of Permian to Mesozoic corystosperms (e.g. Umkomasia) and caytonialians (e.g. Caytonia) [29,30].

Unlike later ovules with an apical micropyle, the earliest ovules in the Late Devonian (Famennian) are characterized by more-or-less fused integument lobes and the absence of a defined micropyle (table 1). Some Famennian (e.g. Moresnetia, Elkinsia, Xenotheca and Kerryia) and Carboniferous (Mississippian) ovules (e.g. Genomosperma kidstonii) display primitive traits in their numerous, narrow and nearly free integumentary lobes [6,31,32]. Cupules of Famennian ovules are typically borne terminally in up to threes, and are commonly multiovulate and strongly overtopped with several terete cupule segments and many tips. In contrast, individual ovules of Latisemenia have four broad and largely fused integumentary lobes, and cupules are borne singly and are uniovulate and short with broad segments bearing few tips. Among existing hypotheses, the telome theory is most commonly accepted to explain the origin of the ovule [2,33–35]. This theory proposes that the integument evolved from the reduction of dichotomous ultimate axes (telomes) and that the cupule evolved from the coalescence of surrounding vegetative dichotomous branches [2,33,36–38]. In this context, the integument and cupule of Latisemenia were separately derived from extensive reduction of telomes and branches. Furthermore, uniovulate cupules may be derived from multiovulate cupules [39]. In this interpretation, Latisemenia demonstrates derived characters in both ovules and cupules. As in Latisemenia, Pseudosporogonites has broad integumentary lobes (although less fused), and cupules of both genera are broad but poorly developed (not overtopping the ovule); and cupules are lost in several groups of younger seed plants such as medullosans and callistophytes.

A more entire integument of early ovules, such as large (long and wide) and/or extensively fused integumentary lobes as found in Dorinnotheca, Glamorgania and Pseudosporogonites, may have aided pollen capture and provided additional protection to the nucellus and water loss reduction [1,4,6,20,21,23]. Such functions of the integument appear evident in Latisemenia, with its flattened integumentary lobes that enclose the nucellus except for the apex.

In the Late Devonian (Famennian), Europe and North America belonged to the Laurussian palaeocontinent [40], and South China was an isolated block near the equator [41]. Most of the Famennian cupulate ovules (table 1) and (possibly) acupulate ovules such as Warsteinia [42] have come from Europe and North America (electronic supplementary material, figure S2), while seed plants have been unknown or rare in the South China block. The palaeofloras of the two components of Laurussia have much in common, even sharing the same genus and species of ovules (e.g. Pseudosporogonites bertrandii [4]), and are known for pollen organs [43–45] or anatomy of seed plant branches [43,46–49]. Recently, the Famennian Cosmosperma (cupules and pollen organs) [5], Kongshania (pollen organs) [50], Placotheca (pollen organs) [51] and Yiduxylon (vegetative branches with anatomy) [52] have been reported from South China. These fertile and vegetative organs, now including ovules of Latisemenia, indicate that the earliest seed plants were more widely distributed than was previously understood.

Laminate pinnules have been rare among Late Devonian seed plants, and previously found associated with ovules [43] or pollen organs [45,50], and now also found in association with Latisemenia ovules. In our large collections, although not found attached, one type of pinnae and pinnules is closely and consistently associated with the ovules of Latisemenia. The foliage and ovules occur at the same horizon (figure 5b,c) and sometimes are adjacent on the same bedding plane (figure 5a). The Sphenopteris-like pinnules are abundant in this low-diversity flora, and their co-occurrence with ovules strongly suggests a former organic connection. Laminate pinnules of Elkinsia are roughly club-shaped with narrow to broad lobes [43], those of Kongshania are in wedge-tongue outline [50], and the leaves associated with Telangiopsis pollen organs are fan-shaped [45]. These seed plant pinnules [45,50], and pinnules associated with Latisemenia ovules in this paper, show divergent venation, supporting a hypothesis that in the evolutionary history of each lineage of Palaeozoic euphyllophytes including seed plants, laminate leaves began with divergent venation terminating at the leaf margins [53].

Authors' contributions

All authors collected the fossils, D.-M.W. conducted the observations and photography of specimens, D.-M.W., J.F.B. and J.-Z.X. were responsible for palaeobotanical interpretation, D.-M.W., P.H. and L.L. prepared the figures. All authors discussed the results and gave comments, and D.-M.W. wrote the manuscript with input from the other authors.

Competing interests

The authors declare no competing interests.

Funding

This work was supported by the National Basic Research Program of China (2012CB821900) of the Ministry of Science and Technology of China, and the National Natural Science Foundation of China (41172007).

Footnotes