The Other Squirrel of Singapore:

Slender Squirrels
Sundasciurus tenuis (Horsfield, 1824)





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Figure 1: A slender squirrel. (Photographed by budak on Flickr, Creative Commons CC BY-NC-SA 2.0)













Overview


This species page is meant to introduce readers to the charming Singaporean native, the slender squirrel (Sundasciurus tenuis). This webpage will serve to provide a broad overview about slender squirrels. Do navigate to your areas of interest using the Table of Contents. If you are interested to find out more about these furry little squirrels, do check out the references at the bottom of the page. Have fun!

Introduction


DO YOU KNOW?

1. Slender squirrels (Sundasciurus tenuis) are one of the two common squirrels in Singapore (Baker, 2013). Unlike its larger, more gregarious relative, the plantain squirrel (Callosciurus notatus) that are common in urban parks, slender squirrels are forest obligates (Baker, 2013) . They are common where they are found though, so you might have passed these squirrels while in the forests without noticing them! So do keep your eyes peeled for these charmers the next time you visit the forested reserves and parks!

2. An interesting fact: the front teeth of slender squirrels, like other rodents, never stop growing! Therefore, they have to continuously gnaw to wear down their teeth ("Squirrel", 2013).



Biology



Habitat



  • Slender squirrels inhabit mature secondary and primary tropical lowland rainforests (Baker, 2013).
  • However, they have been able to be tolerant of disturbance, and have been recorded in degraded habitats like logged forests (Sundasciurus tenuis, 2013a), or even scrub, gardens and parkland (Baker & Lim, 2008; Francis, 2008).
  • It is a primarily arboreal tree squirrel, from the lower canopy including bushes near the ground to middle canopy (e.g. 7m high) (Baker and Lim, 2008; Francis, 2008; Kemper & Bell, 1985). Though less often, they can be spotted on the ground, on tree roots, from moving to another bush or tree.
  • Occurs in both lowlands and mountains (Sundasciurus tenuis, 2013a). However, there is insufficient data to estimate density changes with elevation (Batin et al., 2002, Md. Nor et al., 2001), though both studies caught one at 800m elevation at Mount Nuang, Malaysia.



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Figure 4: A slender squirrel hiding among the vegetation in a tropical rainforest in Malaysia.
(Photographed via camera trapping by Smithsonian Wild on Flickr, Creative Commons CC BY-NC-SA 2.0)



Diet



Slender squirrels eat (Francis, 2008)

  • Fruits
  • Seeds
  • Insects from tree trunks
  • Gnaw tree bark


Their exact food items and diet composition is not known, though they have been observed feeding on six species of figs (Lambert, 1990) and on the insects from the orders Orthoptera and Coleoptera (Muda, 1991).


















Video 1: A slender squirrel gnawing bark. (Video by lenachow on Youtube. )



DO SLENDER SQUIRRELS HOARD?


Food hoarding is a well-known behaviour among squirrels in temperate regions (Somanathan et al., 2007), such as the common North American red squirrels (Tamiasciurus hudsonicus) and gray squirrels (Sciurus carolinensis) (Goheen & Swihart, 2003). However, hoarding is not well-documented in Southeast Asia, with Yasuda et al.’s (2000) study being a rare documentation of scatterhoarding rodents including the three-striped ground squirrel (Lariscus insignis) in a Malaysian rainforest. Slender squirrels have not been observed performing food hoarding behaviours.



Activity pattern



Just like us, slender squirrels are diurnal (Francis, 2008), but detailed information on its activity pattern throughout the day is lacking.



Communication



Slender squirrels are able to

  • communicate via vocalisation. They can make bird chirping alarm calls (Harrison, 1966).In other squirrel species, plantain squirrels (Callosciurus notatus), Sunda black-banded squirrel (Callosciurus nigrovittatus) and grey-bellied squirrels (Callosciurus caniceps), squirrels make different anti-predator calls and adopt different anti-predator behaviours and escape strategies in response to different kinds of predators (e.g. raptors, snakes or terrestrial carnivores) (Tamura & Yong, 1993). It is possible that Sundasciurus tenuis also exhibit various and specialised alarm calls and predator avoidance behaviours in different contexts, though their full vocal repertoire is less well-known.
  • exhibit tail flicking.
  • possibly communicate via eye contact. Partan et al.'s (2009) study on multisensory alarm responses show that tail flicking and staring are implicated in alarm responses in the eastern grey squirrel (Sciurus carolinensis).




It should be noted that signals might by communicated via multi-sensory channels (e.g. using visual and audio signals simultaneously), as in the arboreal eastern grey squirrel (Sciurus carolinensis), therefore the meanings of signals might be misinterpreted if examined by focusing on one communication mode at a time (e.g. either audio or visual) (Partan et al., 2009).



















Video 2: Take a look at the slender squirrel communication in action: vocalisation and tail-flicking. (Video by StopAskingForMyName on Youtube.)



Reproduction and Life cycle



Detailed information regarding life history and reproduction is few and scattered:
  • Their litter size is estimated at 3 individuals (Anage entry for Sundasciurus tenuis, 2012).
  • A captive individual has been recorded to live to 10 years of age (Anage entry for Sundasciurus tenuis, 2012).
  • Nest is made of short branches and stems, and has been observed as low as a metre above ground in the crooks of trees (Baker, 2013) .


Sociality



Tree squirrels are typically less social than ground squirrels and marmots, which live in highly cohesive familial social groups (Partan et al., 2009). However, slender squirrels have been spotted in groups of up to ten interacting with each other (Baker, 2013).



Pathogens



Like us, slender squirrels can suffer from infection by pathogens and parasites such as the sucking louse Neohaematopinus callosciuri (Shinozaki et al., 2004), the mite Chelonoius selenirhynchus (Fain & Nadchatram, 2009), intestinal helminths Fissicauda sp., Rictularia tani and Subulura pigmentata (Betterton, 1979), and dicrocoelid liver flukes Zonorchis sp. (Betterton & Lim, 1977). However, how these pathogens affect the ecology and biology of Sundasciurus tenuis is not well known.




Ecological role



The ecological roles of slender squirrels include being:
  • Seed dispersers and predators (Francis, 2008) . Small mammals, in particular, are involved in rainforest ecosystems as seed predators and dispersers, and may thus affect long-term forest compositions (Sanchez-Codero & Martinez-Gallardo, 1998; Stoner et al., 2007; Wells et al., 2009; Wong et al., 1998). In Indomalayan regions, squirrels are a primary seed dispersal and pre-dispersal predator (Stoner et al., 2007).
  • Prey for higher members in the food webs of the ecosystem, which may include known rodent predators such as snakes (Baker & Lim, 2008), the leopard cat (Prionilurus bengalensi) (Baker & Lim, 2008), and a dietary supplement for common palm civet (Paradoxurus hermaphrodites) (Su Su & Sale, 2007; Jothish, 2011). Slender squirrel abundance might hence impact predator abundance in their habitat.

  • Insect predators (Francis, 2008), thereby possibly impacting insect communities in their habitat.


Conservation



Slender squirrels are of Least Concern status in the IUCN red list, due to their being common and widespread in Southeast Asia (Sundasciurus tenuis, 2013a).

However, they were rarely observed in a survey conducted by Saifu and Nordin (2004) in the Weng-River subcatchment in Kedah, Malaysia, which might point to a decreasing population (Sundasciurus tenuis, 2013a) , though the data was deficient for population estimates.



Names


  • Common name: Slender squirrel
  • Scientific name: Sundasciurus tenuis (Horsfield, 1824)
  • Synonyms (Sundasciurus (sundasciurus) tenuis, 2011):
    • batus Lyon, 1916
    • mansalaris Miller, 1903
    • sianticus Chasen and Kloss, 1928
    • tiomanicus Robinson, 1917
  • Etymology: The generic name Sundasciurus is likely names as this genus of squirrels are found in Sundaland, which is a region of Southeast Asia that contains Peninsular Malaysia and islands on the Sunda shelf including Singaporean islands, Sumatra and Borneo (den Tex et al., 2010). The specific name tenuis simply means thin, thereby describing the slender squirrel.



Description and diagnosis



To the untrained eye, slender squirrels might be mistaken for other squirrels and small mammals. Turn yourself into a slender squirrel spotting expert with the tips shown in Table 1.


Table 1: Diagnostic differences between the slender squirrels and other small mammals in Singapore that might appear similar to the slender squirrels (Francis, 2008; Baker, 2013; Sundasciurus tenuis, 2013b)
Features
Slender squirrel (Sundasciurus tenuis)
Plaintain squirrel (Callosciurus notatus)
Variable squirrel (Callosciurus finlaysonii)
Shrew-faced ground squirrel (Rhinosciurus laticaudatus)
Common treeshrew (Tupaia glis)

external image 1394155_10151873712983521_28566469_n.jpg
(Photograph by Ng Xin Yi Iris)
external image 1454701_10151873714218521_1132481101_n.jpg
(Photograph by Ng Xin Yi Iris)
external image 1459918_10151873725863521_711054629_n.jpg
(Photograph by Jerry Oldenettel on Flickr, Creative Commons CC BY-NC-SA 2.0)
external image 1395930_10151873761308521_1628416523_n.jpg
(Photograph by Ng Xin Yi Iris using camera trapping)
external image 1459280_10151873761168521_1930024133_n.jpg
(Photography by Ng Xin Yi Iris using camera trapping)
Size
  • Head-body: 13-16cm

  • Tail: 12-13cm (85-95% of head-body length)
  • Head-body: 17-22cm

  • Tail: 16-21cm

Note that younger individuals might be smaller.
  • Head-body: 21-22cm

  • Tail: 22-24cm
  • Head-body: 19.5-23.3cm
  • Tail:13.1-17cm (less than 70% of head-body length)
  • Head-body: 13.5-24cm
  • Tail: 12.5-24cm (800-105% of head-body length)
Colouration
Upperparts of body and tail olive brown, underside buff or greyish. Whitish or buff tips to the fur. Pale around eyes.
Upperside and tail olive brown. Belly and inside of limbs reddish-brown. A black and white stripe on each side of body. Pale around eyes.
Extreme geographic variation in colouration.
Subspecies introduced to Singapore C. f. floweri has brown upperparts, and often reddish around head and tail. Underside white.
Upperparts dark brown, underside buff.
Upperparts brown, sometimes olive bran or reddish-brown. Often has a pale stripe on shoulder. Underside buffy brown.
Shape
  • Round head with short, blunt snout.

  • Slender and small

  • Tail is long and thin, furry but bristle-like.
  • Round head with short, blunt snout.

  • Larger, stouter body compared to the slender squirrel.

  • Tail is long, furry, but thick and bushy.
  • Round head with short, blunt snout.

  • Larger body compared to the slender squirrel.
  • Long, bushy tail.
  • Elongated, pointed snout.

  • Short, bushy tail
  • Elongated, pointed snout, even longer than the shrew-faced ground squirrel's.
  • Long, furry tail
Remarks
  • Restricted to primary and secondary forests.
  • Arboreal from low to mid canopy.
  • Diverse, from primary and secondary forests, to urban parks.
  • Arboreal, can range from low to high canopy.
  • Diverse, from primary and secondary forests, to urban parks.
  • Restricted to undisturbed primary and mature secondary forests.
  • Forest floor-dwelling.

  • Secretive and rarely spotted.
  • Primary and mature secondary forests.
  • Forest floor-dwelling.


Distribution



Global distribution

Slender squirrels's distribution spans from the southern edges of Thailand, Peninsular Malaysia, Singapore, Sumatra to Borneo, and some smaller Indonesian islands (Sundasciurus tenuis, 2013b). They are native to Southeast Asia, including Singapore.




















Figure 2: Global distribution of slender squirrels. (Sourced using GoogleMaps)




Local distribution


Bukit Timah Nature Reserve, Central Catchment Nature Reserve, Singapore Botanic Gardens Rainforest, Bukit Batok Nature Park (Chan, 2012; Baker, 2013; Sundasciurus tenuis, 2013b).





















Figure 3: Distribution of slender squirrels in Singapore. (Sourced using GoogleMaps)








Taxonomy



Squirrels belong to the taxon Sciuridae, which consists of 273 species, classified under Sciurinae (tree and ground squirrels) or Pteromyinae (flying squirrels) (Steppan et al., 2004). The genus Sundasciurus contains 15 species, all found in the Sunda shelf, Palawan islands and Greater Mindanao (den Tex et al., 2010). Further, 5 subspecies have been described under Sundasciurus tenuis, which are
  • S. tenuis tenuis
  • S. tenuis bancarus
  • S. tenuis modestus
  • S. tenuis parvus
  • S. tenuis procerus
The Singaporean subspecies is S. tenuis tenuis.

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Figure 5: Taxonavigation for the slender squirrel (Encyclopedia of Life, Tree of Life web http://tolweb.org/Callosciurini/16809 ). (Picture by Ng Xin Yi Iris)





Phylogeny



Phylogenetic analysis on Sciuridae has been performed by Steppan et al. (2004), using C-myc and RAG1 nuclear genes, manual and Sequencher alignment software, and maximum parsimony, maximum likelihood and Bayesian analyses. The study revealed that the Sciuridae clade consists of five major lineages, of which Callosciurini, which contains slender squirrels, is one. The study provided strong support that the 57 species-strong Callosciurini (oriental tree squirrels) is a monophyletic clade (Steppan et al., 2004). It is also suggested that the sciurid lineages diverged in the following order: the ancestors of the flying squirrels and Sciurini (New World tree squirrels) diverged first, followed by the Callosciurini and another clade dominated by ground-dwelling squirrels (Steppan et al., 2004). Figure 6 summarises the results in a phylogenetic tree of sciurids.


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Figure 6: Phylogenetic tree of sciurids using maximum likelihood analysis. Numbers above branches denote likelihood and parsimony bootstrap values respectively. The capital letters circled in red represent the 5 major lineages in the Sciuridae clade, with D representing the Callosciurini clade. Branches of the callosciurini clade are in yellow. (Image sourced from Steppan et al., 2004, with red and yellow modifications by Ng Xin Yi Iris)


A separate study focused on the phylogeny of the genus Sundasciurus, using cyt b gene, and maximum parsimony, maximum likelihood and Bayesian analyses (den Tex et al., 2010).

In fact, the study reveals phylogenetic issues with the species Sundasciurus tenuis:
  • S. tenuis is not monophyletic, and only forms a monophyletic group if S. jentinki and S. brookei are included.
  • Deep divergence exist between the lowland S. tenuis populations on peninsular Malaysia, Sumatra and Borneo, and they are not monophyletic.
  • The two montane S. tenuis populations S. tenuis altitudinis from Sumatra, and S. tenuis tahan from peninsular Malaysia exhibit genetic divergence between each other and other populations. However the two montane populations are monophyletic. In fact, S.tenuis tahan might be more closely related to S. jentinki, a montane squirrel in Borneo, than to lowland S. tenuis populations.
  • The lowland and montane forms diverged in the pre-Pleistocene epoch.
  • The two montane forms (S. tenuis tahan and S. tenuis altitudinis) also split in the pre-Pleistoene epoch.
  • A taxonomic revision of the S. tenuis subspecies may be needed.





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Figure 7: Phylogenetic tree of Sundasciurus using Bayesian analysis. Yellow branches trace the common ancestor of subgenus Sundasciurus to point B, showing that this subgenus is not monophyletic. Blue branches trace members of the Sundasciurus tenuis species to a common ancestor, showing that this species is also not monophyletic. (Image sourced from den Tex et al, 2010, with blue and yellow modifications by Ng Xin Yi Iris)





Type information



Type specimens of a species are required as an anchor for the species description. The slender squirrel's type information is as follows:

Table 2: Slender squirrel's type information
Specimen location
Smithsonian Institution
Author
Horsfield, 1824
Type locality
Singapore




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References



Anage entry for sundasciurus tenuis. In (2012). AnAge. Retrieved from http://genomics.senescence.info/species/entry.php?species=Sundasciurus_tenuis

Baker, N. (2013). Slender squirrel. Retrieved from http://www.ecologyasia.com/verts/mammals/slender_squirrel.htm

Baker, N., & Lim, K. (2008). Wild animals of singapore: A photographic guide to mammals, reptiles, amphibians and freshwater fishes. (p. 137). Singapore: Draco Publishing and Distribution Pte. Ltd. and Nature Society (Singapore).


Batin, Z., Md. Nor, S., & Mohd Yusoff, A. (2002). Influence of elevational habitat changes on non-volant small mammal species distribution and diversity on mount nuang, hulu langat, selangor, malaysia. Pakistan Journal of Biological Sciences, 5(8), 819-824.

Betterton, C. (1979). The intestinal helminths of small mammals in the malayan tropical rain forest: Patterns of parasitism with respect to host ecology. International Jounal for Parasitology, 9, 313-320.




Betterton, C., & Lim, B. (1977). Patterns in the morphological variation of zonorchis and skrjabinus (trematoda: Dicrocoelidae) from small mammals in malaysia. International Jounal for Parasitology, 7, 73-82.

Chan, K. W. (2012). Slender squirrel. Retrieved from http://www.wildsingapore.per.sg/fauna/facts/squirrel_slender.htm


den Tex, R., Thorington, R., Maldonado, J. E., & Leonard, J. A. (2010). Speciation dynamics in the se asian tropics: Putting a time perspective on the phylogeny and biogeography of sundaland tree squirrels,sundasciurus. Molecular Phylogenetics and Evolution, 55, 711-720.




Fain, A. & Nadchatram, M. (2009). Cheyletid parasites or commensals in Malaysia (Acara: Cheyletidae). International Journal of Acarology, 6(3), 191-200.

Francis, C. M. (2008). A field guide to the mammals of south-east Asia. New Holland Publishers (UK) Ltd.





Goheen, J. R., & Swihart, R. K. (2003). Food-hoarding behavior of gray squirrels and north american red squirrels in the central hardwoods region: implications for forest regeneration. Can. J. Zool., 81, 1636-1639.


Harrison, J. (1966). An introduction to mammals of singapore and malaya. (p. 162). Singapore: Tien Wah Press.



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Muda, H. (1991). Diet of small mammals in the secondary tropical forest in Malaysia. The Journal of Wildlife and Parks, 11, 44-52.

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Steppan, S. J., Storz, B. L., & Hoffmann, R. S. (2004). Nuclear dna phylogeny of the squirrels (mammalia: Rodentia) and the evolution of arboreality from c-myc and rag1. Molecular Phylogenetics and Evolution, 30, 703-719.


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Sundasciurus (sundasciurus) tenuis. In (2011). Smithsonian Natural Museum of Natural History. Retrieved from http://vertebrates.si.edu/msw/mswCFApp/msw/taxon_browser.cfm?msw_id=2647&CFID=10069953&CFTOKEN=87661161



Sundasciurus tenuis. In (2013a). IUCN Red List of Threatened Species. Retrieved from http://www.iucnredlist.org/details/21164/0


Sundasciurus tenuis. In (2013b). Raffles Museum of Biodiversity Research. Retrieved from http://rmbr.nus.edu.sg/dna/organisms/details/673


Su Su & Sale, J. (2007). Niche differentiation between common palm civet Paradoxurus hermaphrodites and small Indian civet Viverricula indica in regenerating degraded forest, Myanmar. Small Carnivore Conservation, 36, 30-34.


Tamura, N., & Yong, H. (1993). Vocalizations in response to predators in three species of malaysian callosciurus (sciuridae). Journal of Mammalogy, 74(3), 703-714.



Wells, K., Corlett, R. T., Lakim, M. B., Kalko, E. K. V., & Pfeiffer, M. (2009). Seed consumption by small mammals from borneo. Journal of Tropical Ecology, 25(5), 555-558.

Wong, T. C. M., Sodhi, N. S., & Turner, I. M. (1998). Artificial nest and seed predation experiments in tropical lowland rainforest remnants of singapore . Biological Conservation, 85, 97-104.

Yasuda, M., Miura, S., & Hussein, N. A. (2000). Evidence for food hoarding behaviour in terrestrial rodents in Pasoh Forest Reserve, a Malaysian lowland rainforest. Journal of Tropical Forest Science, 12, 154-173.