Diversity in habit expands the environmental niche of Ziziphus (Rhamnaceae)

Aim: Ziziphus (Rhamnaceae) is a widely distributed genus across the Australasian and African tropics with unusual diversity in habit, and many species of significance to people. Here, we quantify the environmental limits of Ziziphus species and examine inter-specific relationships among functional traits, environment, biome and range size.

Methods: We developed a curated geolocation database for Ziziphus and used it to examine the environmental limits of the genus relative to temperature, rainfall and seasonality. To assess the relationship between biome and habit, Permanova were used, while hierarchical clustering was used to determine whether habit, leaves and fruit traits were related to biome. For 40 species with adequate geolocation data, range size was calculated to assess its relationship with habit, biomes, and cultivation. Finally, niche identity tests were used to determine niche equivalency among cultivated and non-cultivated species.

Results: Liana species are restricted to closed forest and the geoxylic habit is found only in open grasslands. Further, habit is significantly associated with range size, with trees having on average larger range sizes than shrubs, lianas and geoxyles, but biome was not correlated with range size. Cultivated species have ranges ~10 times that of non-cultivated tree species and with significantly different and broader environmental niches.

Conclusion:  The unusually wide distribution of Ziziphus can be explained by its diversity of habits associated with different biomes spanning continents. This, along with the usage of many Ziziphus species by people for their fruits, expands the range and environmental occupation of the genus.

Methods
We curated species occurrence records that resulted in a taxonomically verified database of 1847 unique records for 50 species of Ziziphus. We primarily used the BIEN package v1.2.4 (downloaded 9 December 2020) which integrates global botanical observation data from sources such as plot data, herbaria, and specimen records and where data have undergone additional taxonomic and spatial verification to that supplied by GBIF (The Global Biodiversity Information Facility 2021) (Maitner et al 2017). Following Meyer, Diniz-Filho and Lohmann (2017), where species had <10 geolocations, records were added from a combination of georeferenced herbarium specimens and from additional GBIF data (Table S1). For three species (Z. apetala, Z. hoaensis, and Z. linnaei) no geographic information was available, possibly due to a combination of factors; the tropics are undercollected (Prance et al 2000), the availability of digitized herbarium specimens varies greatly, and digitized resources often suffer from a lack of maintenance and updating (Lughadha et al 2018). Records without latitude and longitude were excluded as were specimens for the same occurrences, and the remaining spatially georeferenced records were cleaned by removing occurrences outside of the known distribution of the genus. Taxonomy was checked using the Taxonomic Name Resolution Service, Plants of the World Online, GBIF, and floras.

Species of Ziziphus were assigned to biomes based on data from floras, peer-reviewed articles, grey literature such as doctoral dissertations, United Nation Development Programme (UNDP) reports, herbarium labels, and expert knowledge from Dr. Gopal Rawat (personal correspondence) (Table S4). Biomes were categorised as ‘open’, ‘closed’, and ‘desertic’. Following the typology of Earth’s ecosystems by Keith et al (2020) that groups ecosystems into biomes for the purpose of enabling comparative work, in the analyses here, closed biomes are analogous to T1 ‘tropical and subtropical forests’ that include lowland rainforests, tropical montane forests, tropical dry forests, and tropical heath forests. Desertic biomes are analogous to T5 ‘deserts and semi-deserts’, that includes semi-desert steppes, thorny deserts and semi-deserts, sclerophyll hot deserts and semi-deserts, cool deserts and semi-deserts, and hyper-arid deserts. Open biomes are analogous to T3 ‘shrublands and shrubby woodlands’ and T4 ‘savannas and grasslands’ following Bond (2019) as both ecosystems are mediated by similar processes (Keith et al 2020). These include seasonally dry tropical shrublands, seasonally dry temperate heaths and shrublands, cool temperate heathlands, rocky pavements, screes and lava flows, trophic savannas, pyric tussock savannas, hummock savannas, temperate woodlands, and temperate subhumid grasslands.

Cultivated species and primary human uses were identified from peer-reviewed articles, floras, and grey literature such as a United States Department of Agriculture Handbook (Table S4). Following Flower et al (2021), we distinguished between species with no use or unknown uses, species which are widely used but not cultivated (harvested in situ), and species which are deliberately cultivated. Uses for non-cultivated species included spiritual, medicinal, edible, and wood for building or forage. Where multiple uses were listed for a species, the most common usage was selected.

研究目的：枣属（Ziziphus，鼠李科Rhamnaceae）是广泛分布于澳大拉西亚和非洲热带地区的属，其生长型具有罕见的多样性，且诸多物种对人类具有重要价值。本研究旨在量化枣属物种的环境耐受极限，并探究功能性状、环境、生物群区（biome）与分布区面积之间的种间关系。
研究方法：我们构建了经过整理的枣属物种地理定位数据库，并借此分析该属物种在温度、降雨量与季节波动维度下的环境耐受极限。为评估生物群区与生长型之间的关联，本研究采用置换多元方差分析（Permanova）；同时通过层级聚类分析，判断生长型、叶部与果实性状是否与生物群区存在相关性。针对40条拥有充足地理定位数据的物种记录，我们计算了其分布区面积，以探究其与生长型、生物群区及栽培状态的关系。最后，通过生态位同一性测试（niche identity test），明确栽培与非栽培物种间的生态位等效性。
研究结果：藤本（liana）物种仅分布于闭合型森林中，而具木质地下茎的生长型（geoxylic habit）仅见于开阔草原。进一步分析显示，生长型与分布区面积存在显著关联：乔木的平均分布区面积显著大于灌木、藤本与具木质地下茎的植物（geoxyles）；但生物群区与分布区面积并无相关性。栽培物种的分布区面积约为非栽培乔木物种的10倍，且其生态位环境显著更宽泛且与非栽培物种存在差异。
研究结论：枣属之所以拥有异常广泛的分布范围，可归因于其与跨大陆不同生物群区相适配的多样生长型。加之诸多枣属物种的果实被人类开发利用，进一步拓展了该属的分布范围与环境占用维度。

研究方法
我们整理了物种出现记录，最终构建了包含50种枣属、共1847条唯一记录且经过分类学验证的数据库。本研究主要使用BIEN包v1.2.4（于2020年12月9日下载），该工具整合了全球植物学观测数据，数据来源包括样地数据、标本馆馆藏与标本记录，且相较于全球生物多样性信息设施（Global Biodiversity Information Facility，GBIF）提供的数据，其额外经过了分类学与空间验证（Maitner et al 2017）。参考Meyer、Diniz-Filho与Lohmann（2017）的研究方法，对于地理定位记录少于10条的物种，我们通过结合地理参考标本馆标本与额外的GBIF数据补充记录（附表S1）。有3个物种（Ziziphus apetala、Ziziphus hoaensis及Ziziphus linnaei）未获取到地理信息，这可能由多重因素导致：热带地区标本采集不足（Prance et al 2000）、数字化标本馆标本的可获取性差异巨大，以及数字化资源常缺乏维护与更新（Lughadha et al 2018）。我们剔除了无经纬度信息的记录以及同一出现点的重复标本，并对剩余的空间地理参考记录进行清洗：移除该属已知分布范围之外的出现记录。分类学校验通过分类学名称解析服务、世界在线植物志（Plants of the World Online）、GBIF及各类植物志完成。

枣属物种的生物群区归类基于植物志、同行评议论文、灰色文献（如博士学位论文）、联合国开发计划署（United Nations Development Programme，UNDP）报告、标本馆标签以及Gopal Rawat博士的专业知识（个人通信）（附表S4）。本研究将生物群区划分为“开阔型”“闭合型”与“荒漠型”三类。参考Keith等人（2020）的地球生态系统分类体系（该体系将生态系统归为生物群区以支持比较研究），本研究中的闭合型生物群区对应T1类“热带与亚热带森林”，包括低地热带雨林、热带山地森林、热带旱林与热带石楠林。荒漠型生物群区对应T5类“荒漠与半荒漠”，涵盖半荒漠草原、多刺荒漠与半荒漠、硬叶热荒漠与半荒漠、冷荒漠与半荒漠以及超干旱荒漠。开阔型生物群区对应Bond（2019）定义的T3类“灌丛与灌丛林地”与T4类“稀树草原与草原”，因这两类生态系统受相似的生态过程调控（Keith et al 2020），其包括季节性干旱热带灌丛、季节性干旱温带灌丛与灌丛地、冷温带石楠荒原、岩石裸露地、碎石坡与熔岩流区、营养型稀树草原、火控丛状稀树草原、丘状稀树草原、温带林地与温带亚湿润草原。

栽培物种及其主要人类用途通过同行评议论文、植物志以及灰色文献（如美国农业部（United States Department of Agriculture）手册）确定（附表S4）。参考Flower等人（2021）的分类标准，我们将枣属物种划分为三类：无用途或用途不明的物种、被广泛利用但未人工栽培（野外就地采收）的物种，以及经人工刻意栽培的物种。非栽培物种的人类用途包括精神祭祀、药用、食用以及建筑用材或饲用草料。若某一物种被记载有多种用途，则选取最普遍的用途作为其主要用途。