Lost mutualisms: seed dispersal by Sumatran rhinos, the world’s most threatened megafauna

Diverse assemblages of seed-dispersing megafauna once existed in Asian rainforests, but are now almost solely represented by elephants. Asia’s rhinos persist in remnant, ecologically-extinct populations and the most threatened of these is the Sumatran rhino, Dicerorhinus sumatrensis. To understand the seed dispersal role of Sumatran rhinos, we consolidated information on fruit consumption, seed dispersal and fruit traits from a two-month field study (Sumatra), local ecological knowledge (Peninsular Malaysia), and published and unpublished accounts. We evaluated differences between the taxa and traits of fruits dispersed by rhinos and elephants, and identified other dispersers of megafaunal-syndrome fruits that were rhino-dispersed. At least 79 plant species were dispersed by rhinos: overstorey plants (trees and climbers; 78% of species) had large, usually “mammal-coloured”, fruits and seeds, and were mainly drupes and berries; 61% of these were megafaunal-syndrome fruits (>4 cm wide). Understorey plants (herbs, shrubs, small trees) had small, often capsular, fruits and seeds that are potentially dispersed following the “foliage-is-the-fruit” hypothesis. Rhinos were the only known disperser for 35% of the megafaunal-fruit genera. The highest dispersal overlap shown was with elephants: fruits dispersed by rhinos tended to be capsular and were smaller than fruits dispersed by both elephants and rhinos. Given these findings and the different foraging and ranging behaviour of Sumatran rhinos and elephants, we suggest these megafauna had important differences in their seed dispersal roles. Asian rainforests have, therefore, lost an important seed dispersal mutualist. Conservation efforts should aim to protect and restore the ecological function of these unique creatures.

Methods
We review knowledge on seed dispersal by the Sumatran rhino, using two newly collected datasets along with published and unpublished research collected mainly from the 1960s to the 1980s. The two novel datasets on seed dispersal by Sumatran rhinos were from: (a) a brief field study on seed dispersal by Sumatran rhinos in Way Kambas National Park, Sumatra, Indonesia and (b) interviews with Orang Asli indigenous people, about seed dispersal by (the now locally extinct) rhinos in the Belum‐Temengor Forest Complex, Peninsular Malaysia.

Way Kambas Field Study, Sumatra

The field study in Way Kambas National Park was conducted across two and a half months spread between July and November 2011. We searched for rhino dung along 18.5km of forest trails, walking each trail three times. For all dungs found, we recorded dung age (<12h, 2–3 d, 3–7 d, 1 wk–1 mo, >1 mo; guesstimated by the field team based on previous experience), bolus size, habitat, and whether it was a single defecation or occurred in a latrine; rhinos often deposit multiple dungs in the same place and these are termed latrines. We searched the dungs for seeds, conducting in‐situ searches for large seeds (>5 mm wide). For smaller seeds we quantified the number in a sample comprising 15% of the dung pile by mass which was later washed over a fine‐mesh sieve. Dung mass ranged from 150 g to 3250 g, and averaged 602 ± 542 g (mean ± SD). Seed length and width were measured. We also collected fruits from all sources we found to use as an aid to identify seeds in dung.

Interview data from Peninsular Malaysia

We documented local ecological knowledge as a second source of information to identify plant species dispersed by Sumatran rhinos. These interviews were conducted as part of a broader study on the seed dispersal network of the Belum‐Temengor forest complex (Ong et al., 2021), Peninsular Malaysia, where the rhino is presumed to have gone extinct in the early 2000s. We interviewed 15 Orang Asli (Peninsular Malaysia's indigenous people) from the Jahai and Temiar communities, who are very familiar with the local flora and fauna. Since only one respondent claimed to be able to identify the fruits consumed by rhinos, these results were not included in the final seed dispersal network (Ong et al., 2021) but are presented here. The respondents were asked if the animal swallowed, chewed, or discarded the seeds of each plant species identified as consumed. We also collected measurements and descriptions of the fruits and seeds in the region (n = 164 species), so that each rhino–fruit interaction we asked about in the interviews was accompanied by fruit and seed trait information. We recorded fruit and seed length and width, seed number per fruit, color, fruit‐type, and growth form (see Ong et al., 2021 for full details).

Publications and final data compilation for review

Finally, we reviewed previous publications on the ecology of Sumatran rhinos, mostly accounts by explorers, hunters, and scientists who visited Sumatra and the Malay Peninsula in the 1900s, and collated their accounts of the fruit diet and seeds found in dungs. We also included more recent unpublished reports written in Bahasa Indonesia. The names of all plant species identified were checked on Kew's Plants of the World Online database and the list of species we present has the most recent names. We also collected information on the vegetative components of the rhino's diet to determine which dispersed species might also be consumed for other plant parts. We searched for information on the fruit and seed traits (see previous section for list), and plant growth form for all species identified as having the fruit consumed by Sumatran rhinos, using local floras and online sources. We categorized mammal colored fruits as colors usually associated with terrestrial mammals (green, brown, yellow, and orange) (Bunney et al., 2019; Yokoyama et al., 2005). We checked each plant species on the IUCN Red List to determine its status.

Literature Cited

Bunney, K. Robertson, M., & Bond, W. (2019). The historical distribution of megaherbivores does not determine the distribution of megafaunal fruit in southern Africa. Biological Journal of the Linnean Society, 128, 1039–1051. https://doi.org/10.1093/biolinnean/blz109

Ong, L., Campos‐Arcei, A., Loke, V. P. W., Pura, P. B., Tunil, C. M. T. B., Din, H. S., Angah, R. B., Amirrudin, A. B., Tan, W. H., Lily, O., Solana‐Mena, A., & McConkey, K. R. (2021). Building networks with local ecological knowledge in hyper‐diverse and logistically challenging ecosystems. Methods in Ecology and Evolution, , 2042–2053.

Yokoyama, S., Takenaka, N., Agnew, D. W., & Shoshani, J. (2005). Elephants and human color‐blind deuteranopes have identical sets of visual pigments. Genetics, 170, 335–344.

亚洲热带雨林中曾存在多样的种子传播巨型动物类群，但如今几乎仅存大象。亚洲犀牛的种群仅残存于破碎化栖息地，已在生态上濒临灭绝，其中处境最危急的是苏门答腊犀牛（Dicerorhinus sumatrensis）。为阐明苏门答腊犀牛的种子传播功能，我们整合了来自两项为期两个月的野外研究（苏门答腊）、本土生态知识（马来西亚半岛）以及已发表和未发表记录的果实取食、种子传播与果实性状相关信息。我们对比了犀牛与大象传播的果实类群及性状差异，并识别出其他曾由犀牛传播的巨型动物综合征果实的传播者。经统计，至少有79种植物可由犀牛传播：其中上层层植物（乔木与藤本，占物种数的78%）多具有大型、通常呈"哺乳动物可视色"的果实与种子，主要为核果与浆果；61%的此类果实属于巨型动物综合征果实（宽度大于4厘米）。下层层植物（草本、灌木、小乔木）的果实与种子体型较小，多为蒴果，其传播可能符合"叶即果实"假说。对于35%的巨型动物综合征果实属而言，犀牛是目前已知的唯一传播者。二者传播重叠度最高的类群为大象：犀牛传播的果实多为蒴果，且体型小于大象与犀牛共同传播的果实。结合上述发现，以及苏门答腊犀牛与大象不同的觅食与活动范围行为，我们认为这两类巨型动物在种子传播功能上存在显著差异。因此，亚洲热带雨林已丧失了一类重要的种子传播互利共生伙伴。相关保护工作应致力于保护并恢复这类独特生物的生态功能。

研究方法
我们通过两份新采集的数据集，结合1960年代至1980年代主要收集的已发表与未发表研究成果，梳理了苏门答腊犀牛的种子传播相关知识。两份关于苏门答腊犀牛种子传播的全新数据集分别来自：(a) 印度尼西亚苏门答腊岛韦坎巴斯国家公园内的苏门答腊犀牛种子传播短期野外研究；(b) 对奥朗阿斯利（Orang Asli）原住民的访谈，内容关于马来西亚半岛贝伦-特门戈尔森林综合体中现已局部灭绝的犀牛的种子传播行为。

韦坎巴斯野外研究（苏门答腊）
本次野外研究于2011年7月至11月间开展，历时两个半月。我们沿着18.5公里的林道进行搜索，每条步道往返三次，寻找犀牛粪便。对于所有发现的粪便，我们记录了粪便年龄（<12小时、2~3天、3~7天、1周~1个月、>1个月，由野外团队根据过往经验估算）、粪团大小、生境，以及粪便为单次排便还是粪便聚集点（犀牛常于同一地点多次排便，此类区域被称为粪便聚集点）。我们对粪便进行种子搜索：对于大型种子（宽度>5毫米），采用原位搜索；对于小型种子，取粪便总质量15%的样本进行定量统计，随后通过细网筛冲洗分离。粪便质量范围为150克至3250克，平均质量为602±542克（平均值±标准差）。我们测量了种子的长度与宽度。同时，我们采集了所有发现的果实作为参考，以辅助鉴定粪便中的种子。

马来西亚半岛访谈数据
我们通过本土生态知识作为第二信息来源，以识别苏门答腊犀牛传播的植物物种。本次访谈作为贝伦-特门戈尔森林综合体一项更广泛的种子传播网络研究的一部分（Ong等，2021），该区域位于马来西亚半岛，犀牛被认为已于21世纪初局部灭绝。我们访谈了15名来自贾海族与特米尔族的奥朗阿斯利原住民（马来西亚半岛原住民），他们对当地动植物十分熟悉。由于仅有一名受访者表示能够识别犀牛取食的果实，因此该结果未被纳入最终的种子传播网络（Ong等，2021），但本文在此呈现。我们向受访者询问了每种被识别为犀牛取食的植物的种子是否被吞食、咀嚼或丢弃。我们还收集了该区域164种植物的果实与种子测量数据及形态描述，因此访谈中涉及的每一组犀牛-果实互动均配有果实与种子的性状信息。我们记录了果实与种子的长度、宽度、单果种子数、颜色、果实类型以及生长型（详细信息见Ong等，2021）。

文献查阅与最终数据整合
最后，我们梳理了此前关于苏门答腊犀牛生态学的研究，主要为20世纪到访苏门答腊与马来半岛的探险家、猎人与科学家的记录，并整合了他们关于犀牛果实取食与粪便中发现的种子的记载。我们还纳入了近年以印尼语撰写的未发表报告。所有鉴定出的植物物种名称均通过邱园世界植物在线数据库进行了校验，本文呈现的物种列表采用了最新的学名。我们还收集了犀牛饮食中的营养器官相关信息，以判断哪些被传播的物种可能同时因其他植物部位被取食。我们通过地方植物志与在线资源，收集了所有被记录为苏门答腊犀牛取食果实的物种的果实与种子性状（详见前文性状列表）以及植物生长型信息。我们将哺乳动物可视色果实定义为通常与陆生哺乳动物相关的颜色（绿色、棕色、黄色与橙色）（Bunney等，2019；Yokoyama等，2005）。我们还通过IUCN红色名录核查了每种植物的保护现状。

参考文献
1. Bunney, K., Robertson, M., & Bond, W. (2019). 巨型动物的历史分布并未决定南非巨型动物综合征果实的分布. 《林奈学会生物学期刊》, 128, 1039–1051. https://doi.org/10.1093/biolinnean/blz109
2. Ong, L., Campos-Arcei, A., Loke, V. P. W., Pura, P. B., Tunil, C. M. T. B., Din, H. S., Angah, R. B., Amirrudin, A. B., Tan, W. H., Lily, O., Solana-Mena, A., & McConkey, K. R. (2021). 在高多样性且后勤受限的生态系统中借助本土生态知识构建网络. 《生态学与进化方法》, 2042–2053.
3. Yokoyama, S., Takenaka, N., Agnew, D. W., & Shoshani, J. (2005). 大象与人类红色盲绿色弱个体拥有完全相同的视觉色素. 《遗传学》, 170, 335–344.