Platacanthomyidae, Rodentia): Climbing and Leaping in the Blind
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Mammalian Biology https://doi.org/10.1007/s42991-020-00043-9 ORIGINAL ARTICLE Locomotion and postures of the Vietnamese pygmy dormouse Typhlomys chapensis (Platacanthomyidae, Rodentia): climbing and leaping in the blind Dionisios Youlatos1 · Aleksandra A. Panyutina2 · Makrina Tsinoglou1 · Ilya A. Volodin3 Received: 2 January 2020 / Accepted: 29 May 2020 © Deutsche Gesellschaft für Säugetierkunde 2020 Abstract The Vietnamese pygmy dormouse is a small, arboreal, nocturnal, blind rodent that uses incipient echolocation to navigate in tree canopies. In order to assess its arboreal faculties in relation to echolocative capacity, the present study investigated the locomotor and postural behavior of the species in a simulated arboreal environment within an enclosure. The study subjects were intensively video and audio recorded and the two sets of data were synchronized for subsequent analyses. This is the frst study on the positional behavior and substrate use of the Vietnamese pygmy dormice. Our results showed that the species spent most of its time on arboreal substrates, mostly traveling and scanning. Locomotion was dominated by vertical climb and leap, occurring mostly on small vertical and on medium and large strongly inclined substrates, respectively. Locomotion and substrate type were strongly related to emission of echolocative pulses. These fndings most likely suggest that echolocation compensates for poor vision to efectively negotiate highly challenging arboreal constraints, and are in favor of the arboreal origins of pygmy dormice. Moreover, such a scenario could also support the echolocation-frst hypothesis for the emergence of echolocation in bats prior to active fight. Keywords Locomotion · Postures · Echolocation · Arboreal · Non-visual orientation Introduction shown that the genus Typhlomys includes four species: Typhlomys cinereus, T. daloushanensis, and T. nanus are The enigmatic rodent family Platacanthomyidae is the earli- endemic to China, while T. chapensis is found in southern est phylogenetic ofshoot of the Muroidea and includes two China and northern Vietnam (Wu and Wang, 1984; Wang morphologically unique genera distributed in the highlands et al. 1996; Cong et al. 2013; Abramov et al. 2014; Cheng of South and Southeast Asia (Musser and Carleton 2005; Lv et al. 2017). The Chapa or Vietnamese pygmy dormouse et al. 2006; Jansa et al. 2009): the monotypic Malabar spiny Typhlomys chapensis Osgood, 1932 is a nocturnal small dormouse Platacanthomys, restricted to the mountains of rodent (body mass about 10–20 g, head-body length about south-western India, and the pygmy dormouse Typhlomys, 70–100 mm), with yellowish gray soft dorsal pelage and confned to the highlands of southern China and northern slate gray ventral pelage, with a particularly long hairy tail Vietnam (Wilson and Reeder 2005). Recent research has (length about 100–135 mm), and prominent ears (length about 14–19 mm) (Abramov et al. 2014; Cheng et al. 2017). Handling editor: Daisuke Koyabu. It bears very small, reduced eyes, with an inner morphology that shows a signifcant structural degradation and suggests * Dionisios Youlatos the loss of visual acuity and focus (Panuytina et al. 2017; [email protected] Volodin et al. 2019). Such an organ is only suited for dis- 1 Department of Zoology, School of Biology, Aristotle tinguishing dark from light or help photoperiodicity, justi- University of Thessaloniki, Thessaloniki, Greece fying its generic name meaning ‘blind mouse’ (Panuytina 2 T. chapensis Severtsov Institute of Ecology and Evolution, Russian et al. 2017; Volodin et al. 2019). Moreover, Academy of Sciences, Moscow, Russia is characterized by regression of the gene for the interpho- 3 Department of Vertebrate Zoology, Faculty of Biology, toreceptor retinoid-binding protein (IRBP), which plays an Lomonosov Moscow State University, Moscow, Russia important role in the visual cycle (Cheng et al. 2017), as in Vol.:(0123456789)1 3 Mammalian Biology subterranean mammals, such as mole-rats, golden moles, Materials and methods and true moles (Emerling and Springer 2014). On the other hand, the species has developed a unique Studied subjects system of ultrasonic echolocation for beyond-tactile orien- tation during locomotion (Panyutina et al. 2017; Volodin For the purposes of the current study, we observed and et al. 2019). The ultrasonic vocalization of Typhlomys is flmed two male Chapa pygmy dormice Typhlomys chap- reminiscent of bat echolocation calls, yet the sweeps in this ensis (Rodentia, Muroidea, Platacanthomyidae). The two rodent are faint, compared to those of bats (Panyutina et al. studied animals were collected in mountain tropical for- 2017; Volodin et al. 2019). This unique adaptive mecha- est in northern Vietnam between 2010–2012 by live cage- nism appears to facilitate arboreal faculties, including con- traps set up on branches and on the ground (Panyutina fdent progression through an unfamiliar environment, over et al. 2017). The two animals were kept at the Moscow inclined and vertical branches, as well as aimed leaps from Zoo in relatively large and enriched cages, where they branch to branch, over gaps several times greater than the could move on diferent kinds of substrates and on the cage tactile reach of the vibrissae (Panyutina et al. 2017). This foor. Both males were fully habituated to human presence, lifestyle of Typhlomys is also implied by the long vibrissae, and did not display any stereotypical or stressful behav- large ears, long hind feet and elongated hairy tail, although iors at the time of the observations. Although the number there is little direct evidence on its biology (Abramov et al. of the sampled individuals is limited, it is important to 2014; Panyutina et al. 2017). Similar morphological adapta- note that the animal is classifed as endangered, it has a tions are also found in some other nocturnal rodents, but, in restricted range, is rare and difcult to catch in the feld. contrast to Typhlomys, they are coupled with relatively large Furthermore, the studied individuals are the only ones specialized eyes (Cartmill 1985; Niederschuh et al. 2015, kept alive in a zoo in the world underlining the paramount 2017; Arkley et al. 2017). In fact, the incipient echolocation importance of behavioral observations. of Typhlomys is very likely a compensatory mechanism for the poor vision and focus for canopy exploration (Panyutina et al. 2017). This interplay between echolocation and arbo- Video and audio recordings real exploration may have important implications for under- standing the evolution of non-visual orientation and, more The present data derived from the analysis of video record- particularly, echolocation in bats (Fenton et al. 1995; Jones ings of the two captive males. Video recording for behavio- and Teeling 2006; Teeling et al. 2012; Carter and Adams ral observation occurred in a specifc experimental enclosure 2015, 2016; Adams and Carter 2017; Panuytina et al. 2017). (height: 50 cm × length: 120 cm × depth: 30 cm) backed by In order to assess the arboreal faculties of the Vietnamese white plastic walls, fronted by a glass window, with wire- pygmy dormice, the present study investigated the locomotor mesh sides. The foor was covered with mulch. Within the and postural behavior of the species in a simulated arboreal enclosure, a variety of arboreal substrates of various sizes environment within an enclosure. The arboreal environment and inclinations were arranged enabling the animals to move is a three-dimensional discontinuous network of unstable, freely. The recording sessions occurred between February structurally variable and diversely oriented substrates. and July 2013. Two camcorders were applied simultaneously To move rapidly along arboreal substrates, to climb up or for video recording: a JVC GC-PX10 camcorder (Victor down vertical substrates, and to cross wide gaps represent Company of Japan, Yokohama, Japan) was used for the high- the most demanding locomotor challenges within the arbo- defnition video (1920 × 1080 pixels, 50 fps, 1/1000 s) and real environment (Cartmill 1985). In the case of a scansorial a Casio EX-F1 camcorder (Casio Computer, Tokyo, Japan) mammal, such as Typhlomys, the poor eyesight and ill focus was used for the high-speed video (512 × 384 pixels, 299.7 would signifcantly reduce the efciency of balance on small fps, 1/2000s). The total duration of the analyzed videos was unstable substrates, the secure use of steeply inclined sub- 106.6 min. The experiments are described in detail in Panyu- strates, and the successful negotiation of wide gaps between tina et al. (2017). substrates. Extensive use of relatively wide and horizontal During the video recording procedures, a Pettersson substrates and the crossing of small gaps, where the tac- D 1000X recorder with a built-in microphone (Petters- tile vibrissae would serve as guide, would be more suitable. son Elektronik AB, Uppsala, Sweden) was used for the However, if the echolocative capacity of Typhlomys chap- audio recording (sampling rate 768 kHz, 16 bit; frequency ensis allows for successful canopy orientation, we expect response from 5 to 235 kHz). The total duration of the this species (a) to exhibit an agile arboreal repertoire, (b) to audio recordings accompanying the videos was 60.6 min. frequently use vertical climbing and leaping, and (c) to pre- The respective audio- and video-tracks were synchronized fer and commonly use small unstable and strongly inclined based on clicker signals. arboreal substrates. 1 3 Mammalian