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traits from a two-month field study (Sumatra), local ecological knowledge (Peninsular Malaysia), and published and unpublished accounts.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.Funding provided by: Yayadan Sime Darby*Crossref Funder Registry ID: Award Number: M0005.54.04Funding provided by: Rufford FoundationCrossref Funder Registry ID: http://dx.doi.org/10.13039/100007463Award Number: 10108‐1We review knowledge on seed dispersal by the Sumatran rhino, using two newly collected datasets along with published and unpublished research collected mainly from the 1960s to the 1980s.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 (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. 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