The smallest Zosterophyllum plant from the Lower Devonian of South China and the divergent life history strategies in zosterophyllopsids

Plants have evolved different life history strategies to overcome the limited amount of available resources; however, when and how divergent strategies of sexual reproduction evolved in early land plants is not well understood. As one of the notable and vital components of early terrestrial vegetation, the Zosterophyllopsida and its type genus Zosterophyllum, reached maximum species diversity during the Pragian (Early Devonian; ca. 410.8–407.6 million years ago). Here we describe a new species, Z. baoyangense sp. nov., based on well-preserved specimens from the Pragian-aged Mangshan Group of Duyun, Guizhou Province, China. The new plant is characterized by its small size, K-shaped branching, and tiny spikes with five to ten sporangia. This plant is most likely r-selected, completing its whole lifespan in a short time, and such a strategy contributes to reproduction in a suitable window time. By contrast, most other species of Zosterophyllum and the zosterophyllopsids on a broader scale are larger in body size and have greater investments in fertile tissues reflected in the size and total number of sporangia. We argue that the zosterophyllopsids probably benefited from the divergence of various life history strategies and thus constituted a major part of the Early Devonian floras.

Methods
(a) Morphological measurements of Zosterophyllum species

The morphological descriptors of Zosterophyllum species are shown in Figure S2, including the width and length of spikes, width, and length of axes, sporangial height and width, etc. These descriptors are commonly used in the documentation of fossil plants and can be easily obtained.

Compared to extant plants, the fertile investment involving the total number of spores and survival rate of spores cannot be obtained from plant fossils. Here, we define a new descriptor, total sporangial accommodation (TSA), to evaluate the mass or energy investment for spore production in each plant. The TSA is estimated by the following formula for each fertile axis:

TSA = n·(h·w·t)

where the total number of visible sporangia in a spike or fertile region is symbolized as n, and the sporangial height, width, and thickness are symbolized as h, ,w and t respectively.

The sporangial thickness is rarely observed, but it is seemingly stable as observed in a few records (such as Hao, 1992; Hao et al., 2010). Here we assume a constant value for the thickness of sporangia (0.6 mm, as measured in the well-preserved specimens of Zosterophyllum shengfengense (Hao et al., 2010); that is, it is assumed that t = 0.6 mm for all plants). For example, the spike of Z. qujingense consists of 3–8 sporangia, which are 2.5–4.5 mm high and 3.1–4.7 mm wide, and therefore the value of TSA is 14.0–101.5 mm3. When the number of visible sporangia or estimated sporangia is not documented in species descriptions, we obtained an estimation from the published illustrations in the original literature.

In addition to our plant, data on other Zosterophyllum species were collected from descriptions in the original literature or were directly measured by the authors based on the published illustrations. The data sources include those of Cascales-Miñana and Meyer-Berthaud (2014) and recent new works, such as Edwards et al. (2015), Edwards and Li (2018a), and Wang et al. (2018), spanning from Silurian to Early Devonian. However, only species of Zosterophyllum that have been well-studied or well-illustrated are included, while species with open nomenclature such as those with sp. and aff. are excluded, except for the earliest record Zosterophyllum sp. from the Silurian of Canada (Kotyk et al., 2002). The exact assignment of species with such open nomenclature requires further work. The same species from different localities are regarded as different data points.

Plant height cannot be measured directly for most species of Zosterophyllum, but we could assess their possible height, or compare with each other for specimens with a similar preservation condition. An exceptional specimen of Z. shengfengense provides a good illustration that the plants of this group can be divided into four parts: the subterraneous fibrous root-like axes, the semi-below or below-ground rhizome, the basal aerial axes with K- or H-shaped branching, and the main erect part containing fertile regions or spikes (Hao et al., 2010; Hao and Xue, 2013). Hence, the combination of lengths of the latter two parts is regarded as representing the majority of the plant height.

Here, the plant remains of Zosterophyllum were divided into three groups, based on their preservation status. Most specimens are only preserved in the middle to upper fertile parts (Group I); some specimens exhibit fertile axes with K- or H-shaped branching (Group II), such as Z. qujingense, Z. minorstachyum, and our plant; and a few other specimens show complete plants, such as Z. shengfengense, here considered as Group III. If rhizomes and aerial fertile parts of a species are found, although they may not be directly connected, such as in Z. xishanense, Z. sinense, and Z. myretonianum, such species are also included in Group III.

By following the above methods, we compiled a new dataset of morphological measurements of Zosterophyllum species (see electronic supplementary material, table S3). The genus Zosterophyllum is probably not monophyletic based on phylogenetic analyses (Kenrick and Crane, 1997; Hao and Xue, 2013; Nibbelink and Tomescu, 2022). However, it is noted here that cladistic analyses of early land plants usually suffer from limited character sampling; for example, most Zosterophyllum species lack features of anatomy and spores. At present, we consider whether or not Zosterophyllum is monophyletic remains an unresolved issue. Nevertheless, we extended the scope of our analysis to consider other zosterophyllopsids, in order to provide (1) an extrapolation of our results to a higher-level category and (2) a discussion of character evolution within a (proposed) monophyletic group.

(b) Measurements of zosterophyllopsids (and early lycopsids)

Two different phylogenetic frameworks were employed herein (see electronic supplementary material, figure S5); the first recognized an inclusive clade, the Lycophytina sensu Kenrick et Crane (L-KC for short), which includes the Zosterophyllopsida sensu Kenrick et Crane, lycopsids, and some other taxa (Kenrick and Crane, 1997) and the second recognized the Zosterophyllopsida sensu Hao et Xue (Z-HX for short) as a monophyletic clade (Hao and Xue, 2013). By using the morphological descriptors shown in Figure S2, we obtained measurements of the members of L-KC and Z-HX. In fact, numerous zosterophyllopsids were not sampled in phylogenetic analyses (Gensel, 1992; Kenrick and Crane, 1997; Hao and Xue, 2013; Nibbelink and Tomescu, 2022), including some taxa that were recently described such as Baoyinia (Edwards and Li, 2018b). For those that have not been included in phylogenetic analyses, their assignment to the L-KC and the Z-HX was based on the authors’ own judgment. The dataset is shown in Table S4.

The species with open nomenclature were excluded, except for those from the Ludlow. The sporangiotaxis and sporangium orientation of other zosterophyllopsids are more divergent than in Zosterophyllum. For TSA, three types of taxa were not considered: (1) some taxa show sparsely attached sporangia, such as Danziella artesiana, Forania, Sawdonia, etc.; (2) sporangia in some taxa are scattered distributed on axes, and thus it is hard to discern a spike or fertile region, such as Deheubarthia, Gosslingia, etc.; (3) the fertile regions of some taxa are not complete, such as Crenaticaulis, Ventarura etc. However, other morphological parameters of all these taxa, such as the width of axes and sporangial size, were included in the analyses.

(c) Data analyses

We assigned the sampled taxa to five-time bins, based on the international chronostratigraphic chart v 2023/09 (https://stratigraphy.org/chart#latest-version), that is, the Ludlow, Pridoli, Lochkovian, Pragian, and Emsian in ascending order. The majority of Zosterophyllum species are usually confined within a single-time bin (singletons). The species that extend across two or more time bins are rare, and our treatments are as follows. We treated the Zosterophyllum species from the Xujiachong Formation as Pragian age; the reason is that most plants occur in the middle to upper part of the Xujiachong Formation, although the upper part of this formation is regarded as early Pragian to ?earliest Emsian in age based on spore assemblages (Wellman et al., 2012). Z. rhenanum and Z. confertum were suggested to be derived from Lochkovian to Emsian or Pragian to Emsian deposits, but the occurrences of both species are mainly distributed in the Pragian (Schweitzer, 1979; Gossmann et al., 2022), and thus a Pragian age was assigned to them in our dataset. For the species in the L-KC and the Z-HX, we followed the age assignments in the original literature and used the range-through method for their statistics, that is, if one species was recorded from the Lochkovian to Emsian, then it was counted once separately in the Lochkovian, Pragian, and Emsian.

Our dataset was analyzed and visualized by using R v.4.3.2 (RStudio/2023.09.1+494) with packages ggplot2 v.3.4.2 and ggsci v. 3.0.0.

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