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A Blind Climber: the First Evidence of Ultrasonic Echolocation in Arboreal

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A Blind Climber: the First Evidence of Ultrasonic Echolocation in Arboreal Integrative Zoology 2017; 12: 172–184 doi: 10.1111/1749-4877.12249 1 ORIGINAL ARTICLE 1 2 2 3 3 4 4 5 5 6 6 7 A blind climber: The first evidence of ultrasonic echolocation in 7 8 8 9 arboreal mammals 9 10 10 11 11 12 12 13 Aleksandra A. PANYUTINA,1,2 Alexander N. KUZNETSOV,2 Ilya A. VOLODIN,2,3 Alexei V. 13 14 14 4,5 2 15 ABRAMOV and Irina B. SOLDATOVA 15 16 1Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, Russia, 2Department of Vertebrate Zoology, 16 17 17 Faculty of Biology, Lomonosov Moscow State University, Moscow, Russia, 3Scientific Research Department, Moscow Zoo, 18 18 Moscow, Russia, 4Zoological Institute, Russian Academy of Sciences, Saint Petersburg, Russia and 5Joint Vietnam–Russian Tropical 19 19 20 Research and Technological Centre, Hanoi, Vietnam 20 21 21 22 22 23 23 24 24 25 Abstract 25 26 The means of orientation is studied in the Vietnamese pygmy dormouse Typhlomys chapensis, a poorly known 26 27 enigmatic semi-fossorial semi-arboreal rodent. Data on eye structure are presented, which prove that Typhlo- 27 28 mys (translated as “the blind mouse”) is incapable of object vision: the retina is folded and retains no more than 28 29 2500 ganglion cells in the focal plane, and the optic nerve is subject to gliosis. Hence, Typhlomys has no oth- 29 30 er means for rapid long-range orientation among tree branches other than echolocation. Ultrasonic vocalization 30 31 recordings at the frequency range of 50–100 kHz support this hypothesis. The vocalizations are represented by 31 32 bouts of up to 7 more or less evenly-spaced and uniform frequency-modulated sweep-like pulses in rapid suc- 32 33 cession. Structurally, these sweeps are similar to frequency-modulated ultrasonic echolocation calls of some bat 33 34 species, but they are too faint to be revealed with a common bat detector. When recording video simultaneous- 34 35 ly with the ultrasonic audio, a significantly greater pulse rate during locomotion compared to that of resting an- 35 36 imals has been demonstrated. Our findings of locomotion-associated ultrasonic vocalization in a fast-climbing 36 37 but weakly-sighted small mammal ecotype add support to the “echolocation-first theory” of pre-flight origin of 37 38 echolocation in bats. 38 39 39 40 Key words: arboreal locomotion, reduced eyes, Rodentia, Typhlomys, ultrasonic echolocation 40 41 41 42 42 43 43 44 INTRODUCTION 44 45 45 46 Solid surfaces reflect both light and sound, which 46 47 gives animals an opportunity to perceive out-of-touch 47 48 Correspondence: Aleksandra A. Panyutina, Severtsov Institute surroundings using vision or echolocation. Use of vi- 48 49 of Ecology and Evolution, Russian Academy of Sciences, sion is much more common because life on Earth is full 49 50 Moscow, 119071, Russia. of sunlight. Only under poor light conditions are ani- 50 51 Email: [email protected] mals forced to expend their own metabolic energy to 51 172 © 2016 International Society of Zoological Sciences, Institute of Zoology/ Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd Bat-like echolocation in arboreal rodent 1 emit sounds and listen to echoes instead of using vision. “flight-first theory,” echolocation arose in bats after -ac 1 2 To approach acuity of vision echolocation calls must be quisition of flight ability (Speakman 2001, 2008; Sim- 2 3 composed of as short as possible wavelengths to come mons et al. 2010). The “echolocation-first theory” in- 3 4 into ultrasonic range. Among mammals, ultrasonic echo- sists that echolocation was acquired earlier than flight 4 5 location is used in water by odontocetes, from dolphins by quickly moving small mammals adapted to complex 5 6 up to pygmy sperm whale (Madsen et al. 2005), and is but poorly-lit environments (Fenton et al. 1995; Jones 6 7 used on land by chiropterans (excluding most fruit bats & Teeling 2006; Teeling 2009; Teeling et al. 2012). Ac- 7 8 [Pteropodidae]) (Jones & Teeling 2006). Beyond these cording to the “tandem theory,” the flight and echoloca- 8 9 species no other mammal has yet been shown to rely on tion developed simultaneously (Schnitzler et al. 2003). 9 10 ultrasonic echolocation as the main means of orienta- The “flight-first theory” is best supported by current -ev 10 11 tion, either in water or on land. idence due to the fact that there is an absence of extant 11 12 Early reports on ultrasonic echolocation in shrews examples of non-volant mammals using ultrasonic echo- 12 13 (Gould et al. 1964; Tomasi 1979; Forsman & Malmquist location. Followers of the “echolocation-first theory” 13 14 1988) were subject to doubt (Konstantinov & Movchan must find a peculiar prototype: a mammal that has ac- 14 15 1985). Indeed, ultrasonic echolocation is likely disad- quired ultrasonic echolocation and lives in an environ- 15 16 vantageous as compared to touch in the typical environ- ment more appropriate as a runway for flight than the 16 17 ment of shrews. Inside leaf-bedding the high-frequency depth of leaf-bedding. 17 18 calls would be reflected as noise from all the nearby ob- Zoologists have identified many mammals with re- 18 19 stacles, which are readily accessible to vibrissae. These duced eyes and many fast-climbing mammals, but no 19 20 calls would not pass beyond these obstacles to pro- mammal except the poorly studied Typhlomys (Fig. 1) 20 21 vide far-away echoes for long-range orientation. New- combines these extreme features together. Typhlomys, 21 22 er studies have failed to show ultrasonic echolocation in which means “the blind mouse,” belongs to an enigmat- 22 23 shrews (Catania et al. 2008; Siemers et al. 2009; Volo- ic rodent family, Platacanthomyidae (Jansa et al. 2009). 23 24 din et al. 2012, 2015; Zaytseva et al. 2015). It has been The genus Typhlomys consists of two species, of which 24 25 argued that lower-frequency calls (audible clicks and Typhlomys chapensis Osgood, 1932 (the Vietnamese 25 26 twitters) must be more appropriate for echolocation in pygmy dormouse) lives in northern Vietnam and Typh- 26 27 cluttered substrates, and can be used by shrews to gain lomys cinereus Milne-Edwards, 1877 lives in southern 27 28 echoes for orientation (Siemers et al. 2009; Volodin et China (Abramov et al. 2014). The pygmy dormice in- 28 29 al. 2015; Zaytseva et al. 2015). habit subtropical forests at the altitudes of 360–2000-m 29 30 30 All available speculations on echolocation regarding 31 31 small rodents come from behavioral experiments: dor- 32 32 mice, hamsters, voles and rats were vision-deprived and 33 33 forced to look for food (see review by Thomas & Jali- 34 34 li 2004). The only instance of potential ultrasonic echo- 35 35 location was seen in Norway rats [Rattus norvegicus 36 36 (Berkenhout, 1769)]. However, there was very limited 37 37 acoustic analysis provided in the study (Thomas & Jalili 38 38 2004). The study concluded that the calls were echo-lo- 39 39 cating based on weak evidence including the pulse-like 40 40 waveform of the calls, and on the fact that they were 41 41 produced by rats left alone in the dark. 42 42 43 Therefore, neither shrews nor typical rodents aid to 43 44 portray how a quadrupedal mammal can rely on ul- 44 45 trasonic echolocation. The issue is interesting not only 45 46 by itself, but also because such an animal, if discov- 46 47 ered, could serve as a model for the hypothesized ances- 47 48 tral state of bat echolocation. There are three current- 48 ly debated theories on how echolocation in bats may 49 Figure 1 Vietnamese pygmy dormouse Typhlomys chapen- 49 have evolved (Speakman 2001; Jones & Teeling 2006; 50 sis. Its reduced eyes are reflected in the generic name, which 50 51 Simmons 2008; Maltby et al. 2010). According to the means “the blind mouse.” 51 © 2016 International Society of Zoological Sciences, Institute of Zoology/ 173 Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd A. A. Panyutina et al. 1 a.s.l. (Smith 2008; Abramov et al. 2012). The biology with R2 = 0.650. 1 2 of these rodents is poorly studied; they are reported to We calculated the regression equation for bats, using 2 3 be both terrestrial and burrowing (Smith 2008), and we data on 11 bat species from Howland et al. (2004) as: 3 4 4 trapped T. chapensis by live cage-traps not only on the Log (eye axial length in mm) = 0.9566+ 0.3255*Log 5 5 ground but on tree branches too (Abramov et al. 2014), (body mass in kg), (3) 6 which indicates they have climbing ability. Keepers at 6 with R2 = 0.745. 7 the Moscow Zoo, which obtained 2 of these animals, 7 8 confirm their outstanding agility, especially in an arbo- After measurements were taken, all 4 eyeballs with 8 9 real environment, and also report their strictly nocturnal a bit of surrounding tissues were embedded in paraffin, 9 10 activity and the absence of any vocalizations. One can cut into 4 or 5-μm thick serial sections and stained ac- 10 11 hypothesize that with reduced eyes, the arboreal mobil- cording to Mallory or with hematoxylin and eosin using 11 12 ity in the dark and silence could be guided by ultrasonic standard procedures. Sections were studied under a Lei- 12 13 echolocation. ca DM 2500 M microscope. 13 14 In this study we have conducted the following exper- Experimental design 14 15 iments to provide evidence for use of ultrasonic echo- 15 16 location in Typhlomys: (1) checked vision quality using Two adult males of T.
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