Extreme ecological specialization in a rainforest mammal, the Bornean tufted ground squirrel, Rheithrosciurus macrotis

The endemic Bornean tufted ground squirrel, Rheithrosciurus macrotis, has attracted great interest among biologists and the public recently. Nevertheless, we lack information on the most basic aspects of its biology. Here we present the first empirical data on the feeding ecology of tufted ground squirrels, and use data from 81 sympatric mammalian and avian vertebrates to place it within a broad comparative context. R. macrotis is a dedicated seed predator and shows much more extreme ecological specialization than any other vertebrate, feeding on a far smaller subset of available plant foods and demonstrating a greater reliance on a single plant species– Canarium decumanum–than any other vertebrate taxon. Our results suggest that R. macrotis plays an important, previously unknown role in the ecology of Bornean lowland forests, and highlight how much we have yet to learn about the fauna inhabiting some of the most diverse, and most severely threatened, ecosystems on the planet.


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The Bornean tufted ground squirrel, Rheithrosciurus macrotis, has been one of the most 34 talked-about squirrels in recent years. This began with its characterization in the journal Science 35 as the 'vampire squirrel' [1], which followed an account of local folklore that alleged these 36 squirrels kill deer [2]. The moniker 'vampire squirrel' spread widely on social media across the 37 globe. Interest in the squirrel spiked again in 2015 with the release of the first video recordings of 38 these squirrels in the wild at Gunung Palung National Park in West Kalimantan [3]. Despite this 39 global attention, R. macrotis remains a very poorly known and largely unstudied species. What we 3 40 do know is that the species is unusual in many respects. Firstly, phylogenetically it is the only 41 species in SE Asia related to the Sciurini tribe, a large group of Holarctic and South American 42 squirrel species. How R. macrotis colonized Borneo remains unclear because there are no known 43 fossils that link it with the other Sciurini from which it separated some 8.6 million years ago [4-44 6]. R. macrotis also stands out because of its unusual incisors in both the upper and lower jaw, 45 which bear a number of deeply carved ridges (~ 10) so that the incisors' cutting edge is saw- 46 shaped, an arrangement apparently not recorded among other mammals [7]. Its species name likely 47 links to this feature, with the Greek ρείθρο meaning gutter or groove. In addition, comparative 48 morphometric analyses of squirrel mandibles show that R. macrotis is a dramatic outlier compared 49 to other squirrels, particularly in its short, robust mandibles with short, wide articular processes 50 [8]. Finally, R. macrotis appears to have the largest tail relative to body size of all mammal species, 51 a possible anti-predator adaptation [2].

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Although R. macrotis is a biogeographic enigma and morphologically unique, little of its 53 basic ecology is known. To our knowledge there has not been any systematic field study of the 54 species' ecology, although it has been recorded on camera traps at several sites in Borneo (e.g.,

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[9,10]). The large size and unusual shape of R. macrotis skulls [8, 11] coupled with their extremely 56 stout incisors and powerful masseter muscles [12,13] suggest the species is adapted to feeding on 57 extremely hard seeds, but information on the species' feeding ecology is lacking. Here we present 58 results of a long-term, comparative study of the feeding ecology of an intact community of Bornean 59 rainforest vertebrates to describe the diet of R. macrotis and place the degree of its ecological 60 specialization in comparative context. Based on anecdotal published characterizations [14,15], we 61 hypothesized that R. macrotis diets would be dominated by fruit of plants containing hard seeds.

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In addition, we hypothesized that the extreme morphological specialization of tufted ground 4 63 squirrels would be reflected in comparatively extreme ecological specialization on a limited subset 64 of available plants. We found that R. macrotis is a dedicated seed predator and shows much more 65 extreme ecological specialization than any other vertebrate taxon in our comparative sample.     The field team recorded a total of 79 independent feeding observations for R. macrotis, 107 somewhat more observations than for the typical taxon in our dataset (mean= 52, SD = 112, range 108 1-549 observations/species). These 79 records included feeding on 5 plant taxa; the average 109 number of genera recorded for each vertebrate taxon was 10 (SD = 19, range = 1-88, S2 Data).

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The most commonly observed taxon in the R. macrotis diet was Canarium decumanum (n=61  We also found support for our second hypothesis. R. macrotis was extremely ecologically 126 specialized, restricting its feeding to a smaller subset of plant genera than any other vertebrate 127 taxon in our dataset (S2 Data). We observed vertebrate feeding on 159 plant genera. As expected,  comparable in its importance in vertebrate diets, comprising more than 80% of the diets of 148 rhinoceros hornbills (Buceros vigil) and gold-whiskered barbets (Megalaima chrysopogon) and 149 more than 20% of the diets of four other frugivores (Fig 2). No other plant genus comprised more 150 than 22% of the feeding observations of our twelve most well-sampled vertebrate taxa.   Our systematic study of the feeding ecology of Bornean tufted ground squirrels confirms 171 previous anecdotal descriptions of the species [14,15]. We provide clear evidence that the species 9 172 is a seed predator and focuses its feeding on plants bearing extremely hard seeds, especially C. 173 decumanum and M. leptopoda. Two measures indicate that R. macrotis is the most specialized 174 vertebrate taxon in this forest. First, when we controlled for sampling effort, the taxonomic 175 richness of R. macrotis diets is far less than that of any other vertebrate frugivore at Cabang Panti. context, it is truly remarkable how little we know about the species-although our evidence 210 suggests that "assassin squirrel" would be a better moniker than "vampire squirrel". This highlights 211 our more general ignorance of the biodiversity of Borneo and other parts of the tropics. The vast 212 majority of published research concerns a very limited subset of taxa (e.g., [35,36]) and with 213 forests in Indonesia and across the tropics being lost at alarming rates [37,38] we run the risk of 214 losing species before we can collect even the most basic information about their ecology. This is 215 of particular concern for species, such as R. macrotis, that are restricted to undisturbed lowland 216 forests and predicted to be highly intolerant of logging and other forms of disturbance [39].