FULL COMMUNICATIONS ANIMAL ECOLOGY Subsidiary adaptations: climbing techniques in vespertilionid bats Olga Emelianova1, Aleksandra Panyutina2, Ksenia Morozova1, Yakov Davidov1, Maria Kovalenko1, Daria Kalacheva1, and Anastasia Shvyrkova1 1Faculty of Biology, M. V. Lomonosov Moscow State University, Vorobjevy Gory, 1/12, Moscow, 119991, Russian Federation 2A. N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Leninskij Prospekt, 33, 119071, Moscow, Russian Federation Address correspondence and requests for materials to Aleksandra Panyutina, [email protected] Abstract The quadrupedal locomotion of bats still remains almost unexplored. Mean- while, in the life of many species, this type of movement plays an important role. This paper presents the study of characteristics of quadrupedal locomotion on vertical surfaces in bats. We provide the results of the analysis of climbing of five vespertilionid species. The study is based on high-speed video recording of locomotion in two planes in an experimental enclosure on various substrates (the bark of five tree species and the inner surface of the manufactured nest box for bats). For comparison, we used data on horizontal locomotion obtained using the same experimental facilities, as well as all available literature data to date. The time, metric and velocity characteristics of the movement of different species representatives are determined. We show how these characteristics Citation: Emelianova, O., Panyutina, A., are interrelated and how they differ in walking or climbing. The study compar- Morozova, K., Davidov, Y., Kovalenko, M., ing walking vs. climbing was performed for the second time ever. It is shown Kalacheva, D., and Shvyrkova, A. 2019. Subsidiary adaptations: climbing techniques that while climbing, bats retain the same limb sequence, but the gait is not a in vespertilionid bats. Bio. Comm. slow trot-like walk but a very slow walk. There are considerably fewer devia- 64(1): 20–30. https://doi.org/10.21638/ spbu03.2019.103 tions from the usual symmetrical sequence gait (wherein a forelimb movement Author’s information: Olga is followed by that of the contralateral hind limb) when climbing than when Emelianova, Graduate student, orcid. walking, and they are all associated with the search for support. Our results org/0000-0002-7656-2961; Aleksandra show that not all tree-dwelling species of vesper bats can move up the trees Panyutina, PhD, Senior Researcher, orcid.org/0000-0002-8379-8526; Ksenia which they use to roost. The surface of the inner walls of artificial shelters for Morozova, Undergraduate student, bats may be a significant factor in their occupancy. While designing such shel- orcid.org/0000-0002-9074-6038; Yakov Davidov, Undergraduate student, orcid. ters, it is advisable to consider the results of our experiments or conduct tests org/0000-0002-0851-1548; Maria on the behavior of particular species on specific artificial surfaces. Kovalenko, Undergraduate student, orcid. org/0000-0002-9431-112X; Daria Kalacheva, Keywords: climbing, terrestrial locomotion of bats, quadrupedal locomotion, Undergraduate student, orcid.org/0000- 0002-4600-8134; Anastasia Shvyrkova, gait analysis, metric walking characteristics. Undergraduate student, orcid.org/0000- 0002-8742-6295 Manuscript Editor: Pavel Skutschas, Department of Vertebrate Zoology, Faculty Introduction of Biology, Saint Petersburg State University, Saint Petersburg, Russia Received: February 21, 2019; Bats are the only mammals that mainly use flapping flight to move around. Other Revised: April 3, 2019; types of locomotion are either secondary to them or entirely absent. In some groups Accepted: April 6, 2019; of bats, the ability to walk or climb on solid surfaces was lost as a result of the acqui- Copyright: © 2019 Emelianova et al. sition of mechanical rigidity in the ribcage, up to complete fusion of the ribs in the This is an open-access article distributed under the terms of the License Agreement case of extreme specialization (Kovtun, 1984; Panyutina et al., 2018), which allows with Saint Petersburg State University, the bats to save muscle energy during flight. These groups include the horseshoe which permits to the authors unrestricted distribution, and self-archiving free of bats, the Old World leaf-nosed bats, a significant part of the New World leaf-nosed charge. bats and, to a lesser extent, the funnel-eared bats (Vaughan, 1970). However, the Funding: The data processing was fulfilled rigidity of the ribcage leads to the inability of such bats to climb, since the capacity with the support of RFBR (17-04-00954 А). Competing interests: The authors have to bend the spine is lost. As a result, the variety of places they can use as shelters declared that no competing interests exist. is strictly limited. As a rule, chiropterans with rigid ribcages mainly inhabit karst BIOLOGICAL COMMUNICATIONS, vol. 64, issue 1, January–March, 2019 | https://doi.org/10.21638/spbu03.2019.103 21 caves with wide entrances, where they can fly in and land range of available footholds, it can be assumed that their directly on the spot of their choosing (Kuzyakin, 1950). movements are not constrained by the substrate making Their locomotion at the roosting places is confined to it easy to climb. small movements on the cave ceiling on their hind limbs However, in the course of their research, our col- while hanging upside down. leagues (Adams and Karter, 2017) did not study the Unlike chiropterans with rigid ribcages, vesper bats speed of climbing and walking. Therefore, we can make are perfectly able to walk and climb on solid surfaces us- a comparison only with respect to the duration of lo- ing all the four limbs. This type of locomotion is their comotory cycles, as well as calculate a small number of key adaptation as it allows them to inhabit shelters with parameters based on the figures provided in the supple- small entrances like those in tree trunks, man-made ment. Thus, in the literature there is practically no suit- buildings, nest boxes, cracks in quarry walls, and others. able material for comparing vertical and horizontal lo- It is commonly known that vesper bats mainly use comotion of bats. the symmetrical gait moving their limbs in the follow- The goal of this study was to investigate the climb- ing order: left forelimb — right hind limb — right fore- ing of vesper bats on different types of wooden sub- limb — left hind limb, and so on. This order was termed strates that they come across in their daily lives, as well “the diagonal sequence” by Gray (1944) but “the lateral as to determine whether features that are characteristic sequence” by Hildebrand (1965), and we will keep Gray’s for horizontal locomotion (Emelianova et al., 2018) are terminology. However, there is some evidence of devia- also retained in climbing. As our research was largely re- tions from this sequence in bats (Lawrence, 1963; Ad- connaissance, we outlined a wide range of questions that ams and Carter, 2017; Emelianova et al., 2018). At the we wanted to get at least preliminary answers: moment, there are only two studies dedicated to climb- — What are the features (speed, limb sequence and ANIMAL ing locomotion of chiropterans. The first one (Riskin, gait, width and length of steps) of vertical climbing ECOLOGY 2000) concerns the Spix’s disk-winged bat (Thyroptera in vesper bats? tricolor), which was shown to climb smooth plant leaves — What are the trees in Central Russia that the vesper with the help of its attachment disks employing the slow bat can climb? pace (the left hind limb was extended anteriorly at the — Are different tree species equally suitable for bats? same time as the left forelimb, and the right hind limb — Do different species of bats climb trees equally well? with the right forelimb). The second study, which is — Are there any links between the ability to climb dif- more relevant for us, is based on the comparison of the ferent trees with the overall ecological characteris- quadrupedal locomotion in Microchiroptera and Mega- tics of a bat species? chiroptera (Adams and Carter, 2017). Experiments were carried out with five species of fruit bats (Eidolon helvum, To reach the goal outlined above, the following key Rousettus aegyptiacus, Pteropus hypomelanus, Pteropus tasks of experiments were identified: to figure out the pumilus, Cynopterus brachyotis), as well as with micro- gait vesper bats use for climbing; to measure the speed of bats presented by three species of Vespertillionidae (My- climbing and the characteristics of steps of five bat spe- otis thysanodes, Eptesicus fuscus, Nyticeius humeralis) cies on six tree samples and compare the results to the and one species of Phyllostomidae (Artibeus jamaicen- data obtained for horizontal locomotion; and to check sis). The authors investigated both horizontal walking for possible interconnections between the measured and vertical climbing of these species. They measured characteristics and known ecological features of the spe- the duration of the locomotory cycle (stride) and some cies in question. skeletal angles. All investigated bats climbed with the diagonal-sequence symmetrical gait (LF-RH-RF-LH) Materials and Methods (Adams and Carter, 2017: Fig. 7). The authors noted that megachiropterans initiated movement by a hind limb, Our research focused on five species of vesper bats found while microchiropterans initiated the movement by a in the Moscow Region, namely the common noctule forelimb. Also we noticed the pace in the climbing Eido- (Nyctalus noctula), the parti-coloured bat (Vespertilio lon helvum (Adams and Carter, 2017: S1 Video.). murinus), the pond bat (Myotis dasycneme), the Dauben- Adams and Carter (2017) emphasized that mega- ton’s bat (M. daubentonii), and the Nathusius’ pipistrelle chiropterans cycled their limbs significantly faster when (Pipistrellus nathusii). The choice of these species was climbing than when attempting to walk, whereas mi- determined by the fact that all these species tend to oc- crochiropterans cycled their limbs at significantly fast- cupy shelters with small entrances in tree trunks and/or er rates when walking than when climbing.