Karantanis, N.-E. (2017). Adaptive patterns and processes in mammalian arboreality (Doctoral dissertation). Aristotle University of Thessaloniki.
Editorial note. This dissertation is presented here in full for its unique framing material — the Abstract, Acknowledgments, Introduction, Conclusions, and Literature Cited — rather than repeating the six research chapters verbatim. Each of those chapters was subsequently developed into its own peer-reviewed paper, already published individually on this site; each chapter below links directly to its corresponding article rather than duplicating its full text and figures a second time.
The arboreal habitat is a complex mesh of intertwining elements, which make locomotion challenging. Nevertheless, mammals have managed to cope with its complexity. During above-branch arboreal locomotion, the necessity for safety and stability is greatly stressed. Towards this end, many mammals adjust their gait and related metrics in respect to substrate characteristics, such as substrate diameter and inclination. Moreover, as early eutherian mammals exhibit postcranial correlates for arboreality, it is important to assess the behavioural mechanisms that are related to competent arboreal locomotion. However, even though there is wealth of information on primate gaits, there is a general lack of research in other mammals, and especially at a small body size. This study utilizes an experimental approach of simulated arboreal settings, attempting to isolate substrate parameters and compare how different small mammals modify their gait for arboreal locomotion.
For the purposes of the current dissertation we examined eight small-bodied mammals: the acrobatid diprodont Acrobates pygmaeus (~12 g), the murid rodents Micromys minutus (~10 g), Apodemus agrarius (~20 g), Apodemus flavicollis (~30 g), and Thallomys paedulcus (~70 g) the cricetid rodent Myodes glareolus (~20 g), and the glirid rodents Muscardinus avellanarius (~20 g) and Glis glis (~130 g). All the specimens were filmed walking on four different arboreal substrate diameters (2mm, 5mm, 10mm, 25mm) and three different inclinations (45° descending, horizontal, 45° ascending) at 240 fps in a specially designed terrarium. Our analyses concerned basic gait parameters such as diagonality, duty factor, duty factor index, velocity, stride length and stride frequency. Most of the examined small clawed scansorial mammals primarily opted for lateral-sequence gaits during arboreal locomotion. Acrobates pygmaeus was a notable exception, by displaying diagonal-sequence gaits, convergently to primates. Most small mammals reduced diagonality, the relative swing phases of the limbs, and velocity on narrower substrates. These locomotor adaptations, although not always similar, represent behavioural mechanisms that increase stability, and promote continuous navigation along arboreal substrates. On wider substrates, most small mammals significantly increased velocity, and relative swing phases, which in some cases were enhanced by the use of asymmetrical gaits. These behaviours assist in swift movements, obstacle avoidance, and energetic optimization, and may also minimize exposure to predators. The effect of inclination on gait parameters and metrics was very dissimilar between the examined species, implying that there is probably much underlying complexity, and various mechanisms that affect it. In terms of velocity regulation, almost all small mammals increased velocity primarily by stride frequency, rather than stride length, which also promotes arboreal safety, by reducing body oscillations.
Moreover, some of the examined parameters, such as duty factor and stride frequency, were able to predict the degree of arboreality consistently. Increased duty factor and decreased stride frequency in more terrestrial species accommodated stability by reducing touchdown torques, increasing simultaneous contact points and contact periods with substrates for which they are not well adapted. On the other hand, decreased duty factor and increased stride frequency on more arboreal species facilitates obstacle avoidance and manoeuvrability. Diagonality, which has often been linked to arboreality, was not a good predictor of the level of arboreality, and does not seem to be necessary for successful arboreal locomotion, at least in small mammals.
In conclusion, despite some limited dissimilarities, small arboreal and scansorial mammals display behaviours that ultimately contribute to the successful exploitation of the arboreal milieu. More terrestrial species, which lack similar arboreal morphological adaptations, respond to arboreal substrates by adjusting their gaits to increase stability and safety, thus reducing the risk of falling. On the other hand, species that are more arboreally adapted in terms of morphology, also display gait adaptations to facilitate proficient use of arboreal substrates. Body size and morphological similarities between extant arboreal/scansorial small mammals and early eutherian ancestors (e.g. Eomaia and Juramaia ) suggest that these early forms would have behaved in similar ways, displaying lateral-sequence gaits, relatively high duty factors, and increasing velocity mainly by increasing stride frequency. These adaptations, which would have assisted in the efficient use of both terrestrial and arboreal substrates, very likely contributed to their successful dominance and subsequent radiations.
Το ενδιαίτημα των δέντρων είναι ένα περίπλοκο πλέγμα κορμών, κλαδιών και φυλλώματος, τα οποία καθιστούν την κίνηση και μετακίνηση απαιτητικές. Όμως, τα θηλαστικά έχουν καταφέρει να ανταπεξέλθουν στην πολυπλοκότητά του. Κατά την κίνηση επί των κλαδιών, η αναγκαιότητα για ασφάλεια και σταθερότητα εντείνεται. Για αυτό το λόγο, πολλά θηλαστικά τροποποιούν την βάδισή τους και τις σχετικές μετρικές παραμέτρους με βάση τα χαρακτηριστικά των υποστρωμάτων, όπως η διάμετρος και η κλίση. Επιπρόσθετα, καθώς τα πρώιμα ευθήρια θηλαστικά επιδεικνύουν μετακρανιακό σκελετό που σχετίζεται με τη διαβίωση στα δέντρα, είναι σημαντικό να μελετήσουμε τους συμπεριφορικούς μηχανισμούς που σχετίζονται με την αποδοτική δενδρόβια κίνηση. Ωστόσο, αν και υπάρχει πλούτος πληροφοριών σχετικά με την βάδιση των πρωτευόντων, υπάρχει μία γενική έλλειψη ερευνών σε άλλα θηλαστικά και ιδιαίτερα τα πιο μικρόσωμα. Η παρούσα έρευνα χρησιμοποιεί μία πειραματική προσέγγιση προσομοιωμένων δενδρικών συνθηκών, επιχειρώντας να απομονώσει παραμέτρους των υποστρωμάτων και να συγκρίνει το πώς διαφορετικά μικρά θηλαστικά τροποποιούν τον βηματισμό τους για την δενδρόβια κίνηση.
Για τους σκοπούς της παρούσας διατριβής εξετάσαμε οκτώ μικρόσωμα θηλαστικά: το διπρωτοδόντιο μαρσιποφόρο Acrobates pygmaeus (~12 g), τα μυοειδή τρωκτικά Micromys minutus (~10 g), Apodemus agrarius (~20 g), Apodemus flavicollis (~30 g), και Thallomys paedulcus (~70 g), το κρηκιτοειδές τρωκτικό Myodes glareolus (~20 g), και τα μυωξοειδή τρωκτικά Muscardinus avellanarius (~20 g) και Glis glis (~130 g). Όλα τα δείγματα κινηματογραφήθηκαν να βαδίζουν επί τεσσάρων διαφορετικών διαμετρών δενδρικών υποστρωμάτων (2mm, 5mm, 10mm, 25mm) και τριών διαφορετικών κλίσεων (κάθοδος 45°, οριζόντιο, άνοδος 45°) στα 240 καρέ ανά δευτερόλεπτο σε ένα ειδικά σχεδιασμένο τερράριο. Οι αναλύσεις μας αφορούσαν βασικές παραμέτρους βάδισης, όπως η διαγωνιότητα, ο παράγοντας φόρτου, ο δείκτης παράγοντα φόρτου, η ταχύτητα, το μήκος διασκελισμού και η συχνότητα διασκελισμού. Τα περισσότερα από τα εξεταζόμενα μικρά γαμψονυχοφόρα αναρριχητικά θηλαστικά κατά κύριο λόγο επέλεξαν βάδιση πλευρικής-αλληλουχίας κατά την δενδρόβια κίνηση. Το Acrobates pygmaeus ήταν μια αξιοσημείωτη εξαίρεση, επιδεικνύοντας βάδιση διαγώνιας-αλληλουχίας, σε σύγκλιση με τα πρωτεύοντα.Τα περισσότερα μικρά θηλαστικά μείωσαν την διαγωνιότητα, τις σχετικές φάσεις αιώρησης των άκρων, και την ταχύτητα στα λεπτότερα υποστρώματα. Αυτές οι κινητικές προσαρμογές, αν και δεν ήταν πάντα όμοιες, αποτελούν συμπεριφορικούς μηχανισμούς που αυξάνουν την σταθερότητα και προωθούν την απρόσκοπτη πλοήγηση κατά μήκος δενδρικών υποστρωμάτων. Σε πλατύτερα υποστρώματα, τα περισσότερα μικρά θηλαστικά αύξησαν σημαντικά την ταχύτητα και τις σχετικές φάσεις αιώρησης, τα οποία σε κάποιες περιπτώσεις ενισχύθηκαν από την χρήση ασύμμετρης βάδισης. Αυτές οι συμπεριφορές βοηθούν σε ταχείες κινήσεις, στην αποφυγή εμποδίων και στην ενεργιακή βελτιστοποίηση, και μπορεί επίσης να ελαχιστοποιήσουν την έκθεση στους θηρευτές. Η επίδραση της κλίσης στις παραμέτρους βάδισης ήταν πολύ ανόμοια ανάμεσα στα εξεταζόμενα είδη, υπονοώντας ότι πιθανώς να υπάρχει κάποια ενδογενής περιπλοκότητα, και διάφοροι μηχανισμοί οι οποίοι να επιδρούν σε αυτή. Σε σχέση με την ρύθμιση της ταχύτητας, σχεδόν όλα τα μικρά θηλαστικά αύξησαν την ταχύτητα κυρίως μέσω της συχνότητας διασκελισμού, παρά μέσω του μήκους διασκελισμού, το οποίο επίσης προωθεί την δενδρόβια ασφάλεια, μειώνοντας τις σωματικές ταλαντώσεις.
Επιπροσθέτως, κάποιες από τις εξεταζόμενες παραμέτρους, όπως ο παράγοντας φόρτου και η συχνότητα διασκελισμού, προέβλεψαν με συνέπεια τον βαθμό δενδροδιαβίωσης. Ο αυξημένος παράγοντας φόρτου και η μειωμένη συχνότητα διασκελισμού στα περισσότερο εδαφόβια είδη διευκόλυναν την σταθερότητα της κίνησης, μειώνοντας τις ροπές κατά την επαφή των άκρων, αυξάνοντας τα ταυτόχρονα σημεία επαφής και τις περιόδους επαφής με υποστρώματα για τα οποία δεν είναι καλά προσαρμοσμένα. Αντίθετα, ο μειωμένος παράγοντας φόρτου και η αυξημένη συχνότητα διασκελισμού στα περισσότερο δενδρόβια είδη διευκολύνει την αποφυγή εμποδίων και την ικανότητα ελιγμών. Η διαγωνιότητα, η οποία έχει συχνά συνδεθεί με την δενδροδιαβίωση, δεν ήταν καλός παράγοντας πρόβλεψης του επιπέδου δενδροδιαβίωσης και δεν φαίνεται να είναι απαραίτητη για την επιτυχή δενδρόβια κίνηση, τουλάχιστον στα μικρά θηλαστικά.
Εν κατακλείδι, παρά κάποιες περιορισμένες ανομοιότητες, τα μικρά δενδρόβια και αναρριχητικά θηλαστικά επιδεικνύουν συμπεριφορές που εν τέλει συνεισφέρουν στην επιτυχημένη εκμετάλλευση του ενδιαιτήματος των δέντρων. Τα περισσότερο εδαφόβια είδη, τα οποία δεν κατέχουν όμοιες μορφολογικές προσαρμογές, αποκρίνονται στα δενδρικά υποστρώματα μεταβάλλοντας την βάδισή τους ώστε να αυξήσουν την σταθερότητα και ασφάλεια, ώστε να μειώσουν τον κίνδυνο πτώσης. Σε αντίθεση, τα είδη που είναι περισσότερο μορφολογικά προσαρμοσμένα στην δενδροδιαβίωση επιδεικνύουν προσαρμογές βάδισης που διευκολύνουν την ικανή χρήση δενδρικών υποστρωμάτων. Το σωματικό μέγεθος και οι μορφολογικές ομοιότητες μεταξύ σύγχρονων δενδρόβιων/αναρριχώμενων μικρών θηλαστικών και των πρώιμων προγόνων των ευθηρίων (π.χ. Eomaia kai Juramaia ) υπονοούν ότι αυτές οι πρώιμες μορφές θα συμπεριφέρονταν με παρόμοιους τρόπους, επιδεικνύοντας βάδιση πλευρικής-αλληλουχίας, σχετικά υψηλούς παράγοντες φόρτου, και αύξηση της ταχύτητας με αύξηση της συχνότητας διασκελισμού. Αυτές οι προσαρμογές, οι οποίες θα βοηθούσαν στην αποδοτική χρήση τόσο εδαφικών όσο και δενδρικών υποστρωμάτων, πολύ πιθανόν να συνεισέφεραν στην επιτυχή επικράτησή τους και στην ακόλουθη ακτινωτή διαπορά τους.
The research that I will be presenting in this doctoral dissertation is the result of a lifetime’s formal education. During this time, a great many people have influenced my way of thinking, my choices, and my life in general. First and foremost is my supervisor, Dr. Dionisios Youlatos, who has inspired, supported, and led me by example. Since we first met during my undergraduate studies, he has never ceased challenging me to improve myself, motivated me when I waivered, and taught me by example how to become a good scientist. He has actively inspired, and assisted me, in steadily acquiring the skills to become a confident, independent researcher with his careful guidance, attention to detail, and passion for experimental research. Beyond his academic qualities, Dr. Youlatos has been an example and role model to me, in his dedication to, and impeccable treatment of his students, peers, and family. I know that wherever I will be, or whatever I will be doing, I can always turn to him for advice and guidance.
Moreover, I wish to thank my other two advisors, who continuously supported me through my graduate studies. Dr. Leszek Rychlik, for being a most excellent host in the Adam Mickiewicz University of Poznań, Poland, making this entire project possible, and tutoring me on the ecology and behaviour of small mammals. Dr. Anthony Herrel for always being able to provide me with knowledge on the analysis of locomotion, and inspiring me to keep learning. Both, for their careful advice, corrections, and attention to detail, throughout the writing of this doctoral dissertation. I also wish to thank Dr. Eishi Hirasaki, who was my host and instructor during my visit at the Primate Research Institute of Kyoto University. He was a great inspiration in the early stages of my project, and has greatly influenced the way I approach the analysis of mammalian locomotion.
The projects contained in this work would not have been possible without the help of the many people who assisted me with data collection. First, Katarzyna Byczyk and other staff members of the Nowe Zoo of Poznań for providing the animals and assistance throughout many of my experiments. Also, Dr. Peter Klimant, who was also a graduate student at the time, for his assistance in trapping wild small mammals, and experiments, as well as the graduate students of the Adam Mickiewicz University. I am also indebted to Douglas Brown for essential modifications to the excellent open source Tracker software, which made data analysis possible. Furthermore, I cannot thank enough my good friend, Thodoris Tsompanidis, who helped me develop a program that has been indispensable for going through the vast amount of raw data I recorded.
Moreover, I would like to sincerely thank all the anonymous reviewers, as well as the editors of the Journal of Human Evolution, Journal of Mammalian Evolution, Mammalian Biology, Journal of Zoology, and Journal of Experimental Zoology Part A: Ecological Genetics and Physiology. Their constructive criticism, comments, and corrections ensured that my work has been well presented, as well as scientifically sound.
I must also acknowledge all my friends, who supported and accompanied me in exploring life outside academia. My life could never have been as enjoyable as it now is without them. I also wish to thank Dimitra Madenidi, who has given me her unrelenting love and support, from the first day of my Ph.D. studies. She has always been there for me, believed in me, and supported me with patience through every step of this dissertation, including my many instances of frustration and stress, and despite long hours of work, and months of absence at times. She has been, and always be, essential to my life.
Last, but not least, I cannot express enough my gratitude to my parents, Angelos and Eftichia Karantanis. Throughout my life, they have supported all my choices and decisions, both emotionally and materially. I will always be grateful for the beautiful life they have provided me with, their love and affection, and hope that they are proud of the man I have become.
This project was supported financially by the Aristotle University of Thessaloniki, the Adam Mickiewicz University of Poznań, Erasmus Scholarships, and the State Scholarships Foundation of Greece.
There is a vast multiplicity of animal forms on earth, occupying extremely diverse environments, from the ice caps of the poles to deserts and tropical rainforests. In contrast to plants, animals need to move in order to evade predators, secure food and mate and have managed to do so in very diverse ways. Swimming through water, quadrupedal locomotion on the ground or on trees and flight through the air are just some of them. Aristotle was the first to systematically record some of the diversity of these specialisations, characteristically commenting in the opening paragraphs of his book “The History of Animals”: “Animals differ from one another in their modes of subsistence, in their actions, in their habits, and in their parts” (Thompson, 1910). After a long and complex history of scientific research on animal locomotion, we not only know a great amount of detailed information about it, but we are also able to effectively simulate it in computer programs and animate it but have also recently started to replicate it in robotics. Even though terrestrial locomotion has been thoroughly investigated, there is still a lot to be learned. In the study presented here, I will focus on quadrupedal gait adaptations involved in mammalian arboreality, with a special focus on the gaits and efficiency of quadrupedal locomotion of small mammals on arboreal supports and their links to different degrees of arboreality. Towards this end, the main corpus will be comprised of case studies on mammalian arboreal quadrupedal gaits, which will both offer answers to individual questions and complement each other towards connecting gaits to arboreality. In this way, both single-species studies as well as comparative studies will be presented and thoroughly discussed as individual units. Lastly, I will attempt an analysis and a comparison of the common and divergent patterns of arboreal gaits, and provide insights in the evolution of relevant adaptations to arboreality.
The arboreal habitat is a complex mesh of intertwining structural elements with specific particularities. Nevertheless, many animals, mammals included, have managed to cope with its complexity, and negotiate any available arboreal structure starting from low vegetation, such as the dense network of slender branches of shrubs near the ground, reaching up to tree trunks and the branches of all sizes and foliage in the topmost stories. The branches on a tree are limited in number and are highly variable in diameter and orientation. Pathways are interrupted where a branch ends and a new one begins, and can be oriented at any possible angle; even a single branch can change orientations numerous times along its length. Moreover, branches are unstable, subject to oscillations, bending, and even breaking. They can be set in motion in unpredictable trajectories by the wind, an animal’s own movement, as well as the movement of other animals. Falling, therefore, is a very prominent risk. For an arboreal mammal, tumbling to the ground can be deadly, due to injury or exposure to predators. Even if it remains unscathed, it must spend significant amounts of energy to re-ascend. Thus, the successful exploitation of the arboreal habitat is likely related to behavioural and morphological adaptations that reduce the possibility of falling. Arboreal mammals spend all or most of their lives in different vegetation layers, while scansorial mammals exploit both arboreal and terrestrial substrates (Hildebrand, 1995). In extant mammals, arboreality is widespread, and has evolved independently in numerous taxa (Alexander, 1992; Hildebrand, 1995; Nowak, 1999; Kemp, 2005; Rose, 2006). Among metatherians, the majority of opossums (Order Didelphimorphia) are adapted for arboreality, as well as many genera of diprotodonts (Order Diprotodontia), including a secondarily arboreal kangaroo (Hildebrand, 1995). Among extant eutherians, arboreality is present in most extant clades. Among the Xenarthra, the order Pilosa contains arboreal anteaters and sloths (Taylor, 1978, 1985). Both colugo species (Order Dermoptera) are arboreal climbing gliders (Panyutina, Korzun & Kuznetsov, 2015). Most Primates (Order Primates) are adept climbers or primarily arboreal, and quite possibly of arboreal ancestry (Cartmill, 1972, 1974a, 1992; Jenkins, 1974; Sussman, 1991; Soligo & Müller, 1999; Soligo & Martin, 2006; Cartmill, Lemelin & Schmitt, 2007). Even though few treeshrews (Order Scandentia) are arboreal and most are terrestrial (Emmons, 2000; Panyutina et al., 2015), all possess morphological features associated with arboreality and most probably descend from arboreal ancestors (Emmons, 2000; Olson, Sargis & Martin, 2004). Among the order Chiroptera, many species roost in trees, while some climb them as well (Hildebrand, 1995; Panyutina et al., 2015), and are most certainly of arboreal origin (Simmons, 1995). Many carnivorans (Order Carnivora) engage in arboreal or scansorial locomotion, and especially the procyonids (McClearn, 1992) and viverrids (Taylor, 1989). Rodents (Order Rodentia) display a wide locomotor diversity, with some families such as the Sciuridae (Thorington, Miller & Anderson, 1998) and Gliridae (Juškaitis, 2008; Kryštufek, 2010) being extensively arboreal (and of arboreal origin), and numerous arboreal representatives are present among the other families, such as the Anomaluridae, Critecidae, Erethizodontidae, Muridae, Nesomyidae, Platacanthomyidae, etc. (Samuels & Van Valkenburgh, 2008).
Figure 1.1. Reconstruction of Suminia getmanovi in both (a) flesh and (b) skeleton. From Fröbisch & Reisz (2009).
Apart from being widespread in extant mammals, arboreality has had a strong presence in mammalian evolutionary history. Plant-based life on the ground was not always as currently observed. The first plants started colonizing land at 470 to 425 mya (Bennici, 2008), fundamentally altering earth’s land-based ecosystems (Algeo, Scheckler & Maynard, 2002; Driese & Mora, 2002). The earliest organisms resembling our idea of trees were tree ferns, horsetails and lycophytes, which formed the first forests. Wattieza is the oldest known tree from the Middle Devonian (~385 mya) (Stein et al., 2007), followed by Archaeopteris (383-323 mya) (Beck, 1960). By the end of the Devonian period (417-354 mya), both invertebrate and vertebrate animals had also moved into terrestrial ecosystems. However, there is a significant gap (about 120 mya) in the fossil record separating the appearance of the first trees and the first recorded arboreal vertebrate. Suminia getmanovi (Fig. 1.1; Class Synapsida, Order Therapsida, Family Otsheridae), an herbivorous synapsid reptile (early mammalian ancestors), was the first truly arboreal vertebrate encountered in the fossil record, and lived approximately 260 mya, within the Late Permian (Ivakhnenko, 1994; Rybczynski, 2000). The postcranial anatomy of Suminia contains skeletal evidence for prehension and arboreality as indicated by its elongate limbs, intrinsic phalangeal proportions, a divergent first digit and a possibly prehensile tail (Fröbisch & Reisz, 2009). The first mammals and their sister taxa are encountered some 100 M years after Suminia, with a relatively rich record of fossil species showing scansorial and arboreal adaptations. Among them, the docodontan Agilodocodon scansorius was a small mammaliaform (27 g) from the Middle Jurassic (160 mya) possessing slender and gracile hands, feet, and digits, ending in curved claws (Fig. 1.2.a) indicating arboreal clinging and climbing activities (Meng et al., 2015). From the same period, representatives of another early mammalian clade, the Allotherian Euharamiyidans, also display skeletal features related to arboreality: Senshou lui (300 g; Fig. 1.2.b), Xianshou linklong (83 g), Xianshou songae (40 g) and Arboroharamiya jenkinsi (354 g), all possess forelimb, hind limb and axial postcranial adaptations for arboreal locomotion, including tail prehensility (Zheng et al., 2013; Bi et al., 2014). Another Late Jurassic mammal, the cladotherium Henkelotherium guimarotae also possesses adaptations associated with climbing and was possibly scansorial (Vázquez-Molinero et al., 2001). Moreover, around 125 mya, the multituberculate Sinobataar sp. bears morphological adaptations for arboreality (Hu et al., 1997). Concurrently, the eutriconodontan Volaticotherium antiquum was the first gliding arboreal mammal, belonging to a sister taxon of the ancestors of all extant mammals (Gaetano & Rougier, 2011). With a body mass at ~70 g and a body length at 120-140 mm, it possessed a sizable furry patagium (flying membrane) for gliding flight, as well as elongated tail and limbs, clearly adapted for arboreal life (Meng et al., 2006). To present, it represents the earliest gliding mammal, probably unrelated to extant gliders, and it stands as the first of the seven independent evolutionary lineages of mammalian gliding within the Diprotodontia (Petauridae, Acrobatidae, Pseudocheiridae), Dermoptera (Cynocephalidae) and Rodentia (Sciuridae, Anomaluridae) (Jackson & Thorington, 2012). More recent mammals of the early Cretaceous, the eutriconodontan Jeholodens (Chen & Wilson, 2015), multituberculate Sinobaatar (Hu & Wang, 2002), and symmetrodontan Zhangeotherium (Chen & Wilson, 2015), all possess postcranial morphologies suggesting scansoriality or arboreality.
Figure 1.2. Skeletal reconstructions of: (a) Agilodocodon scansorius (adapted from Meng et al., 2015); (b) Senshou lui (adapted from Bi et al., 2014); (c) Eomaia scansoria (adapted from Ji et al., 2002); (d) Juramaia sinensis (Luo et al., 2011). Please note that each reconstruction is at a different scale.
Importantly, the two oldest known eutherian species have also been described as scansorial. Juramaia sinensis (Fig. 1.2.d; Class Mammalia, Infraclass Eutheria), the oldest known eutherian mammal is, dated at 160 mya, in the late Jurassic. Juramaia was a very small insectivore, weighing around 15-17 g. Their phalangeal indices suggest grasping capabilities similar to extant scansorial and arboreal mammals, and proposed paleohabitats involve small shrubs and medium to low height vegetation (Luo et al., 2011). Arboreal adaptations have been also reported from another early eutherian mammal, Eomaia scansoria (Fig. 1.2.c) dating from the early Cretaceous (~125 mya), and weighing around 20-25 g. Eomaia bears fore- and hind feet adaptations that have been functionally related to scansorial activities and are reminiscent of the dormouse Glis (Ji et al., 2002). More recent eutherians, from the Late Cretaceous, primarily include species adapted to terrestrial life (Hurum & Kielan-Jaworowska, 2008). However, the small basal euarchontan Deccanolestes appears to have postcranial adaptations related to scansoriality (Boyer et al., 2010; Fabre et al., 2014). In the other major clade of extant therian mammals, the Metatheria, the oldest representative (early Cretaceous), Sinodelphys szalayi, was also a small (~30 g) arboreally adapted mammal, hinting towards a possible arboreal ancestry. Sinodelphys is characterized by carpal, fore- and hind feet features that are linked to strong flexion and grasping, indicating climbing and scansoriality, as well as arboreal quadrupedalism (Luo et al., 2003). Discoveries of metatherians from the Late Cretaceous reveal a radiation of locomotor forms, including terrestrial, and semiaquatic species (Williamson, Brusatte & Wilson, 2014). Moreover, descriptions of fragmented postcranial elements from Deltatheroid metatherians hint at scansorial and/or arboreal habits for some of the discovered representatives (Szalay & Sargis, 2006; Chester et al., 2010, 2012). Arboreal locomotion appears to be widespread among extant eutherians and metatherians, and has apparently played an important role in their evolution. Apart from a significant record of Mesozoic mammals (sensu lato) bearing characters suggestive of scansorial and arboreal activities (Luo et al., 2003, 2011; Larson & Stern, 2006; Zheng et al., 2013; Bi et al., 2014; Meng et al., 2015), the oldest fossil specimens from the two most successful extant mammalian clades, the Eutheria and Metatheria, were arboreal/scansorial (Ji et al., 2002; Luo et al., 2003, 2011; Larson & Stern, 2006; Zheng et al., 2013; Bi et al., 2014; Meng et al., 2015). Taking this into account, the most parsimonious hypothesis is that the last common ancestor of these two clades (Eutheria and Metatheria) very likely involved a significant arboreal component in its locomotor repertoire. As most of these arboreal/scansorial Mesozoic mammals are generally small to very small (Jenkins, 1974; Ji et al., 2002; Luo et al., 2003, 2011; Larson & Stern, 2006; Kielan-Jaworowska, 2013; Zheng et al., 2013; Bi et al., 2014; Meng et al., 2015), it is also important to understand locomotion at a small size. Towards this end, the comparative study of locomotor behaviour in extant arboreal and scansorial small mammals can reveal common and divergent adaptive patterns in arboreal locomotion, and their driving factors. These observations can then be used in conjunction with morphological characteristics to understand the arboreal adaptations of ancestral species, and infer patterns related to the evolution of mammalian arboreal locomotion.
Tree branches and trunks are the primary substrates for arboreal locomotion. They essentially differ from terrestrial substrates by being discontinuous, limited in length and variable in width and inclination, and subject to bending and oscillations (Grand, 1972; Cartmill, 1974b). Potentially, this variety holds a distinct possibility of falling, with potential injury or death and/or exposure to predators. Under this selective pressure, arboreal adaptations (behavioural and morphological) evolved to facilitate safe and secure body displacement within the canopy, and to establish firm hold of arboreal substrates in order to avoid loss of balance or toppling over. Contact with a substrate is usually achieved with the fore- and hind feet (autopodia), and in some cases the tail (Cartmill, 1974b; Alexander, 1977; Hildebrand, 1995). Animals walking on a horizontal or sub-horizontal branch are always at risk of toppling over; a risk which can be counteracted by: (i) possessing relatively short limbs, in order to lower the centre of mass closer to the substrate, as exemplified by dormice (Juškaitis, 2008; Kryštufek, 2010), (ii) having prehensile extremities to keep a secure grip on the branch, a common attribute in most arboreal tetrapods (mammals included) (Sustaita et al., 2013), (iii) hanging below branch, as in sloths (Nyakatura et al., 2007), colugos (Dzulhelmi & Abdullah, 2009), and many monkeys and apes (Hunt, 1991), and (iv) reducing body size or adopting a crouched posture, as observed in some small arboreal mammals in order to have the support points more widely spread on the branch surface, and to rapidly shift direction of movement in face of irregularities of the supports (Schmidt, 2008). Most morphological adaptations of arboreal mammals stress the necessity for stability. Stability can be either static or dynamic (Lammers & Zurcher, 2011a). Static stability is the process when an animal remains motionless, with no forward or backward movements, nor any axial rotations; however, static stability may also apply to very slow body progression, as the underlying biomechanics remain similar. On the other hand, in faster locomotion, mass distribution on the limbs constantly changes, and so do the produced forces and torques (Lammers & Zurcher, 2011b). Combined with anatomical adaptations, gaits can be considered as a behavioural mechanism to further enhance dynamic stability during quadrupedal arboreal locomotion (Shapiro & Raichlen, 2005; Schilling & Hackert, 2006; Stevens, 2006; Young, 2009, 2012, Schmidt & Fischer, 2010, 2011, Lammers & Zurcher, 2011a, 2011b; Shapiro & Young, 2012).
Morphological adaptations. Even though the present research focuses mainly on behavioural adaptations to arboreal life, morphological and anatomical correlates are tightly linked to effective arboreal locomotion. No matter the specifics of locomotor patterns, both the forefeet and hind feet of arboreal mammals bear adaptations which enhance friction, interlocking, and bonding at the molecular level with the surfaces they are moving on. These mechanisms assist in propelling the body upwards, or braking when moving downwards in the discontinuous three-dimensional arboreal milieu and avoid falling while moving or standing, especially under challenging conditions (Alexander, 1992; Hildebrand, 1995). To achieve interlocking, the digits of both fore- and hind feet of arboreal mammals often end in deep curved claws. These interlock with the crevices of branches and trunks and are particularly useful in climbing (Cartmill, 1974b, 1985; Hildebrand, 1995; Soligo & Müller, 1999). On the other hand, enhanced gripping by the pads of the feet (Cartmill, 1974a, 1974b; Sussman, 1991; Soligo & Müller, 1999) has led to the reduction of claws to flat nails in some mammals, such as primates and some marsupials (Cartmill, 1974b). Finally, apical pads bond with substrates at the molecular lever, further assisted by the excretion of organic adhesives by glands on hands and feet (Hildebrand, 1995). The hind feet of arboreal mammals are commonly characterised by powerful grasping, especially combined with the reduction or modification of claws. Pedal grasping is identified as the orientation and positioning of toes so as to apply functionally effective forces onto a substrate, wholly or partly surrounding it, in order to establish a static and/or dynamic posture (Sustaita et al., 2013). Effective pedal grasping in arboreal mammals is achieved by robust musculature of the hind feet with powerful flexors with long tendons, independent movement of digits I, II and V, extended mobility of the upper and lower ankle, and inter-tarsal joints, as well as soft, sensitive and expanded foot pads with excretory glands at high densities, all contributing to an operative foot position that increases friction, interlocking and bonding with the substrate (Jones, 1953; Cartmill, 1974b, 1985; Jenkins & McClearn, 1984; Haffner, 1996, 1998; Meldrum, Dagosto & White, 1997; Smith & Smith, 2013; Sustaita et al., 2013). Among different grasping modes, pedal grasping using a strong, divergent hallux is especially efficient for securing firm foot holds on most types of arboreal supports, as displayed in primates and a few other arboreal mammals (e.g. Szalay & Dagosto, 1988; Sargis et al., 2007; Youlatos, 2008; Kingston et al., 2010; Sustaita et al., 2013; Urbani & Youlatos, 2013; Goodenberger et al., 2015; Youlatos et al., 2015; Youlatos, Karantanis & Panyutina, 2016). Kinematically, pedal grasping enables an animal to manipulate substrate reaction forces, i.e. the forces needed for propulsion (Preuschoft, 2002; Witte, Preuschoft & Fischer, 2002). By producing a counter-transfer of reaction moments with the substrate, pedal grasping assists in the dynamic shift of the weight from the forelimbs to the hind limbs (Reynolds, 1985). Overall, the grasping ability of hind feet appears to be of major importance in achieving stability during arboreal locomotion, as is demonstrated in many mammalian lineages (i.e. primates, didelphimorphs, diprotodonts, scandentians) possessing efficient prehensile feet which probably evolved prior to grasping forefeet (Cartmill, 1974a; Szalay, 1984; Szalay & Dagosto, 1988; Sargis, 2001; Bloch et al., 2007). The musculature and bone morphology of the forelimbs of arboreal mammals varies depending on the locomotor modes employed (suspension, vertical climbing, leaping, or above-branch quadrupedalism; e.g. Taylor, 1985; Stalheim-Smith, 1989; Youlatos, 2000; Argot, 2001). Despite differences, arboreal mammals tend to have extremities which assist their ability to climb, stay on top of, or hang below substrates. This commonly leads to possessing longer proximal phalanges and shorter metacarpals than their terrestrial relatives (Kirk et al., 2008). These are combined with the presence of overall long digits (Napier, 1967; Lemelin, 1999; Hamrick, 2001; Krattli, 2001; Zefferer, 2002; Kirk et al., 2008), which enhance gripping by allowing the fingers to wrap around substrates (Lemelin, 1999; Lemelin & Schmitt, 2007). Especially in a fine-branch milieu, this enables countering of the pitching and rolling of the torso during locomotion (Napier, 1967; Cartmill, 1974b; Preuschoft, Witte & Fischer, 1995; Lemelin & Schmitt, 2007) and increases general prehensility (Lemelin, 1999; Hamrick, 2001). Moreover, elongation of the digits to the extreme is also related to gliding, i.e. in colugos, another form of arboreal locomotion (Beard, 1993; Hamrick, 2001; Panyutina et al., 2015). In order to increase friction and interlocking with the substrate, forelimb digits form various grips, utilizing power exerted by strong flexors and extensors in the forearms. These muscles are differentially developed, depending on how digits apply power in each grip. Most primates habitually oppose the pollex to the lateral digits, thus gripping between digits I and II or I and III, when digit II is greatly reduced (Napier, 1961). However, arboreal metatherians and some primates form a zygodactylous or schizodactylous grasp (sensu Haines, 1958), establishing a powerful grip between digits II and III (Youlatos, 1999a, 2010). The grasping ability of the forelimbs can greatly contribute to stability during above-branch locomotion (Youlatos, 1999a, 2010), especially in a narrow-branch niche (Cartmill, 1992; but also see Orkin & Pontzer, 2011), as well as significantly assist the hind limbs in generating propulsion for vertical climbing (Youlatos, 2010; Reghem et al., 2012). Lastly, in some arboreal species, the tail is also used as a fifth limb, actively assisting in positional behaviour. When the tail alone can support the entire body, it is referred to as prehensile. Prehensile tails are curled at the end, and their caudal surface is often naked to increase friction (Lemelin, 1995; Youlatos, 2003; Organ, 2008). They are characterised by expanded sacroiliac joints and long proximal caudal regions or a high number of proximal caudal vertebrae, a powerful caudal flexor musculature and long flexor and extensor tendons, as well as developed mm. intertransversarii, and short, robust distal vertebrae with expanded transverse processes when present in both primates (Dor, 1937; Lemelin, 1995; Organ, 2008) and carnivores (Dor, 1937; Youlatos, 2003; Organ, 2008). Prehensile tails are more common in medium-sized (2-12 kg) species which mainly inhabit Neotropical forests, and may be evolutionarily linked to locomotion using weak branches, which are prone to downward deformation (Emmons & Gentry, 1983; Meldrum, 1998).
Gaits and their metrics in arboreal locomotion. Competent locomotion requires the effective combination of morphological and behavioural adaptations, to which they may be functionally related. During arboreal locomotion, gaits can serve as a mechanism to assure stability and consequent safe navigation in the arboreal milieu. A gait is the pattern, or sequence, of limb movements during locomotion over a solid substrate. Animals select a few different gaits on the basis of the velocity, the features of the substrate used, the need to manoeuvre, and the energetic efficiency (Hildebrand, 1967, 1968, 1976, 1995; Cartmill, Lemelin & Schmitt, 2002). A stride is the series of events between two consequent touchdowns of a foot. Stride period is the time interval during which a stride takes place. When velocity is kept constant, this interval remains the same for all feet. A gait cycle encompasses the sequence of fore- and hind limb displacements that take place within a stride period. Gaits can be either symmetrical, in which the movements of the left and right limbs of a girdle are evenly spaced in time, or asymmetrical, in which they move more or less concurrently. Asymmetrical gaits can be described by duty factor and duty factor index, whereas symmetrical gaits additionally include another important parameter, diagonality. Diagonality, or forelimb-hind limb phase (Hildebrand, 1967; Cartmill et al., 2007), is the percentage of the stride cycle the footfall of a forelimb follows behind the ipsilateral hind limb. It is measured as a scale variable ranging from 0 to 100, but is also often divided into ordinal classes: (a) Lateral Sequence Lateral Couplets (0≤LSLC<25), (b) Lateral Sequence Diagonal Couplets (25≤LSDC<50), (c) Trot (=50), (d) Diagonal Sequence Diagonal Couplets (50<DSDC≤75), (e) Diagonal Sequence Lateral Couplets (75<DSLC≤100). Even more simplified, it can be divided into three categories: (a) Lateral Sequence (0≤LS<50), (b) Trot (=50), (c) Diagonal Sequence (50<DS≤100).
Figure 1.3. Support patterns in a lateral-sequence (A; Diagonality = 26) and a diagonal-sequence (B; Diagonality = 56) walk with a duty factor of 64. Reproduced from Cartmill et al. (2002).
Moreover, during a gait cycle, a foot can be either on the substrate (stance phase) or in the air (swing phase). A foot’s duty factor (Hildebrand, 1967) is the percentage of the stride cycle during which it is anchored on the substrate (Fig. 1.3). If the duty factor of a gait is higher than 50, each foot will be on the substrate for most of the gait cycle. If the gait is symmetrical, it would be called a walk. On the other hand, a symmetrical gait with a duty factor below 50 is a running gait. Symmetrical gaits and their parameters are considered important in arboreal locomotion, as they have been linked to arboreal adaptations (Prost, 1965; Tomita, 1967; Kimura, Okada & Ishida, 1979; Cartmill et al., 2007). Nevertheless, recent results highlight that asymmetrical gaits are also common among arboreal mammals and should thus be further explored (Young, 2009; Schmidt & Fischer, 2010; Shapiro, Kemp & Young, 2016). Lastly, the duty factor index (DFI) is calculated as the hundredfold ratio of the duty factor of the hind limbs divided by that of the forelimbs, and expresses the relative contact of the hind limbs compared to that of the forelimbs (Cartmill et al., 2007). When the DFI is over 100, the hind limbs have a longer relative stance phase compared to the forelimbs, while this is inversed if the DFI is below 100. Consequently, the DFI can be insightful for detecting differences in the relative contribution of the forelimbs and hind limbs during locomotion (Cartmill et al., 2002, 2007; Nyakatura, Fischer & Schmidt, 2008; Nyakatura & Heymann, 2010).
Figure 1.4. Support polygons during locomotion in a lateral-sequence gait. Note that 3 feet are in contact with the substrate at all times, hence a duty factor of 75. Reproduced from Lammers & Zurcher (2011a).
In symmetrical gaits, DS gaits (Diagonality > 50) involve a footfall pattern in which a forelimb touches down after more than half of the stride cycle following the touchdown of the ipsilateral hind limb. On the other hand, in LS gaits, the touchdown of a forelimb takes place after less than half of the cycle following the touchdown of the ipsilateral hind limb. Diagonal sequence (DS) gaits are particular by being prevalent among primates, while most other mammals primarily make use of LS gaits (Hildebrand, 1967; Cartmill et al., 2007). Since DS gaits were initially only encountered in primates, they were thought to be superior to LS gaits in terms of stability during arboreal locomotion (Prost, 1965; Tomita, 1967; Prost & Sussman, 1969). However, this has been disproven and attributed to a neurological reorganization in the primate brain (Vilensky & Larson, 1989). In recent years, DS gaits have been shown to have convergently evolved in a number of other taxa, including some arboreal metatherians (White, 1990; Schmitt & Lemelin, 2002; Karantanis, Youlatos & Rychlik, 2015) and the arboreal carnivoran Potos flavus (Lemelin & Cartmill, 2010). Consequently, it seems improbable that the convergent evolution of DS gaits is unrelated to any adaptive significance. Cartmill et al. (2007) proposed that DS gaits are beneficial in that they assist in the inspection of new, unknown and possibly unstable substrates, while moving on terminal branches. Essentially, DS gaits may allow for the safe anchoring of a hind limb, while the diagonally opposite forelimb moves and tests the substrate. If something goes wrong, the animal can fall back to the safety of the previous substrate, assisted by the anchored hind limb, while keeping its centre of mass within a support polygon generated by the limbs, thus preventing it from toppling over. DS or LS gaits, with diagonality scores between 25 and 75, are referred to as diagonal couplet (DC) gaits. In these gaits, the footfalls of contralateral limbs are more concurrent than in lateral couplets gaits, with D scores >75 or < 25. Diagonal couplets (DC) in DS (DSDC) and LS (LSDC) gaits (Cartmill et al., 2002, 2007) may have different advantages for arboreality, relative to keeping the centre of mass within the support polygons produced by the limbs (Fig 1.4). This is of great importance as if the centre of mass leaves the support polygon, it may result in loss of balance (Fig. 1.5) (Cartmill et al., 2002, 2007; Lammers & Biknevicius, 2004; Lammers & Zurcher, 2011a, 2011b). DSDC gaits are associated with dynamic stability, i.e. the control and transfer of moments and torques imposed on the body axes (Lammers & Zurcher, 2011a). In DS gaits, the contralateral footfall pattern promotes a dynamic weight shift from side to side at any given moment of a stride cycle leading to increased dynamic stability. Simultaneously, the other two diagonally paired fore- and hind limbs take off and move forward, offsetting the motion on the transverse body axis (Cartmill et al., 2002, 2007). On the other hand, in arboreal locomotion, LSDC gaits may be preferable in terms of static stability during slower locomotion, as they enable the continuous placement of the centre of mass within the support polygon (Fig. 1.4) produced by the limbs (Gray, 1944; Tomita, 1967; Shapiro & Raichlen, 2005; Lammers & Zurcher, 2011a).
Figure 1.5. A male Apodemus flavicollis losing balance on an unstable, 2mm substrate.
Asymmetrical gaits (Fig. 1.6) are often used for achieving higher velocities (Hildebrand, 1977; Pridmore, 1994; Gasc, 2001; Young, 2009; Shapiro et al., 2016), and confer a number of advantages in comparison to symmetrical gaits. They can optimize the metabolic cost of locomotion (Hoyt & Taylor, 1981), or decrease the strain borne by the musculoskeletal system by decreasing peak substrate reaction forces (Farley & Taylor, 1991). Specifically in small mammals, asymmetrical gaits may also contribute by an energetic input to locomotion through the sagittal movements of their flexible spines and related muscles (Schilling & Hackert, 2006). Moreover, in arboreal locomotion, the use of asymmetrical gaits reduces peak vertical forces, constrain the movement of the centre of mass, and bring about shorter and more frequent strides, all of which contribute to arboreal stability (Young, 2009; Schmidt & Fischer, 2010; Shapiro et al., 2016).
Figure 1.6. Support patterns in symmetrical and asymmetrical gaits. Reproduced from Wikipedia. Permanent link at https://en.wikipedia.org/wiki/Gait#/media/File:Gait_graphs.jpg
Locomotor speed may also serve as an indicator of locomotor efficiency on arboreal substrates. For example, in some neotropical marsupials and rodents, arboreal species tend to display higher velocities than terrestrial species when using arboreal substrates (Delciellos & Vieira, 2006, 2007; Camargo et al., 2016), which may contribute to maintaining dynamic stability (Schmidt & Fischer, 2010). Velocity is a function of two parameters: stride frequency, i.e. number of strides per unit of time, and stride length, i.e. the distance covered within a single stride (Alexander, 1992; Hildebrand, 1995). Arboreal mammals may increase their velocity in a number of different ways: (i) increase stride frequency and decrease stride length (Delciellos & Vieira, 2006, 2007; Camargo et al., 2016); (ii) decrease stride frequency and increase stride length (Larson et al., 2000, 2001, Delciellos & Vieira, 2006, 2007); or (iii) increase primarily stride frequency, accompanied at a lesser rate by increase in stride length (Nyakatura et al., 2008; Karantanis et al., 2015). Increasing velocity through longer strides can be safer on arboreal substrates as they enable a farther reach by the forelimb and thus reduce involuntary branch sway (Demes et al., 1994). This method of velocity increase is often encountered in medium-sized and larger arboreal mammals, which may cause significant branch movement under their weight (Larson et al., 2000, 2001, Delciellos & Vieira, 2006, 2007). In contrast, increasing velocity by increasing stride frequency, although energetically costly (Reilly, McElroy & Biknevicius, 2007), decreases body oscillations, allows continuous progression, and may thus be more advantageous for smaller mammals, for which, branch sway may be insignificant, but body oscillations may disrupt continuous progression (Strang & Steudel, 1990; Delciellos & Vieira, 2007). In the arboreal niche, substrates are available at a great range of possible sizes, and are placed at any possible inclination, from horizontal (0°) to vertical (90°). Substrate size directly affects the width of the support polygons that can be obtained during locomotion (Cartmill et al., 2002, 2007; Lammers & Biknevicius, 2004; Lammers & Zurcher, 2011a). Moreover, ascending and descending locomotion affects how the weight is distributed towards the forelimbs and the hind limbs and consequent reaction forces developed at the contact points with the substrate (Lammers, Earls & Biknevicius, 2006; Lammers, 2007; Nyakatura et al., 2007; Schmidt, 2011; Schmidt & Fischer, 2011). Arboreal mammals, therefore, are expected to adjust their behaviour according to substrate properties, such as size and inclination, in ways that affect effectiveness and safety in the arboreal milieu.
Substrate size. The diameter of arboreal substrates may impose significant constraints on locomotion (Jenkins, 1974; Witte et al., 2002), as it has an immediate impact on the size of the support polygons during quadrupedal locomotion (Cartmill et al., 2002, 2007; Lammers & Biknevicius, 2004; Lammers & Zurcher, 2011a). DS gaits have been theorised to be useful towards achieving safe negotiation of smaller and potentially unstable substrates in the presence of grasping hind feet (Cartmill et al., 2007), which translates into an increase in diagonality or occurrence of DS gaits in small substrate. Nevertheless, existing results are contrasting. The kinkajou Potos flavus (Lemelin & Cartmill, 2010) does display a higher frequency of DS gaits on smaller substrates. In contrast, DS gaits are in fact less frequent in the majority of strepsirrhine primates examined (Stevens, 2008), the tamarin Saguinus fuscicollis (Nyakatura & Heymann, 2010), and the arboreal metatherian Petaurus breviceps (Shapiro & Young, 2010), and a lack of correlation between substrate size and DS gaits has been detected in free-ranging tamarins Saguinus mystax (Nyakatura & Heymann, 2010). In most arboreal mammals, DF, velocity and its regulating factors, stride frequency and stride length, are often lower on smaller substrates but gradually increase on larger substrates (Lammers & Biknevicius, 2004; Delciellos & Vieira, 2006; Shapiro & Young, 2012). When a quadruped moves on an arboreal substrate, the support polygons produced by the limbs are very narrow (Lammers & Zurcher, 2011a) increasing the risk of the centre of mass being placed outside them. Furthermore, each time a limb touches down, the torque produced further enhances the probability of losing balance (Lammers & Zurcher, 2011b). A slow, controlled walk, especially on the smallest of substrates, should minimize this possibility by reducing the produced torques, increasing the simultaneous contact points on the substrate at any given time, and providing longer periods to accommodate a stable and secure dynamic posture (Lammers & Zurcher, 2011a). In contrast, some neotropical arboreal rodents seem to walk faster on smaller substrates (Camargo et al., 2016), probably in order to achieve dynamic stability, which may be potentially related to lack of significant grasping abilities (Schmidt & Fischer, 2010). These results indicate a lack of consensus on how substrate size influences gait metrics. More importantly, it seems that different species with different morphologies have adapted to arboreal locomotion on narrow arboreal substrates with contrasting behavioural strategies. It is, therefore, of importance, to further study how substrate size affects gaits, especially in the absence of primate-like powerful grasping.
Substrate inclination. Moving upwards or downwards on an inclined substrate has a different effect on gait parameters, due to a more posterior distribution of body weight in ascents and a more anterior one in descents (Lammers et al., 2006; Lammers, 2007; Nyakatura et al., 2007; Schmidt, 2011; Schmidt & Fischer, 2011). In ascending locomotion, diagonality and duty factor index increase, thus signifying more diagonal gaits and a higher dependence on the hind limbs (Prost & Sussman, 1969; Lammers, 2007; Nyakatura et al., 2008; Nyakatura & Heymann, 2010; Shapiro & Young, 2010; Shapiro, Young & VandeBerg, 2014). This functions twofold, reducing yawing and lateral torques, while enhancing the potential to propel the body upwards (Vilensky, Moore & Libii, 1994; Lammers & Biknevicius, 2004; Stevens, 2006; Nyakatura et al., 2008; Nyakatura & Heymann, 2010). Results regarding velocity in ascending locomotion are contradictory. European red squirrels (Sciurus vulgaris) move with a higher velocity during ascents than in horizontal locomotion, possibly in an effort to achieve dynamic stability, whereas rats (Rattus norvegicus) tend to move more slowly, probably in order to maintain static stability (Schmidt & Fischer, 2011). During descents, diagonality and duty factor index are decreased in comparison to ascents, suggesting more lateral gaits and a reliance on forelimbs. This behavioural shift has been related to braking though a “stop-jolt” mechanism using the forelimbs (Rollinson & Martin, 1981; Nyakatura & Heymann, 2010). Furthermore, due to the anterior shift to the centre of mass, contact times between the forelimbs and the substrate are increased, resulting in a higher fraction of vertical impulse, which may enhance their supportive and regulatory role (Rollinson & Martin, 1981; Lee et al., 2004; Nyakatura et al., 2008; Young, 2012; Karantanis et al., 2015). In arboreal mammals, descents are often also characterised by a lower velocity compared to ascents and horizontal locomotion (Vilensky et al., 1994; Lammers et al., 2006; Lammers, 2007; Karantanis et al., 2015). A need for a higher control of speed for cautiousness brings about a higher frictional effect of the forefeet through pads and claws, combined with an anterior weight shift to the forelimbs and an emphasis on their braking role (Lammers et al., 2006; Lammers, 2007). However, arboreal primates appear not to adjust velocity to direction of movement, which has also been suggested to be related to the maintenance of dynamic stability (Nyakatura et al., 2008; Shapiro et al., 2016). To sum up, substrate inclination, and consequently, an ascending, descending, or horizontal direction of movement may affect gait parameters and metrics in various ways. It seems, though, that these effects are not similar in all species, and may depend on their individual needs for static or dynamic stability. However, there is both a general lack of data, as well as a disaccord on the causes of these differences. Therefore, the collection of more observations from different taxa is necessary in order to form more concise and clear hypotheses on how and why mammals modify gait metrics for different directions of movement.
The effect of body size on gaits has been involved in a long-standing debate. In terms of velocity, for instance, Hill (1950) constructed a model predicting that, due to geometric similarity, locomotor speed should be independent of body size. Nevertheless, other scaling models suggest that large animals move (run, swim or fly) faster than small animals, especially when converting velocity to dimensionless measures (Alexander & Jayes, 1983; Garland, 1983; Alexander & Maloiy, 1984; Alexander, 1992; Donovan & Gleeson, 2008). Unfortunately, the majority of studies on locomotor performance and efficiency have focused on terrestrial locomotion. However, arboreal locomotion may pertain to body size in different manners than in terrestrial species, as arboreal substrates are highly flexible and the risk of losing balance is increased (Grand, 1972, 1984). Regardless of their phylogeny, small mammals perceive substrates as wider and flatter, distances as longer, and obstacles, such as small rocks on the ground or small protrusions on tree branches, as larger than large mammals (Cartmill, 1974b; Jenkins, 1974). Moreover, in an arboreal context, larger animals tend to display increased below-branch, suspensory locomotion, and cross discontinuities with bridging more often than leaping (Cartmill & Milton, 1977a; Fleagle & Mittermeier, 1980). On the other hand, smaller mammals view discontinuities in the canopy as larger (Cartmill & Milton, 1977b), therefore engaging in more frequent leaping (Fleagle & Mittermeier, 1980). In this way, compared to larger mammals, smaller mammals tend to be faced with similar locomotor constraints, regardless of the specific microhabitat they use (Jenkins, 1974). In order to cope with their size-related convergent challenges in locomotion, small mammals share features that differentiate them even from their larger phylogenetically close relatives. They usually walk and run with a crouched limb posture, while larger mammals run with a more upright posture (Biewener, 1989a, 1989b, 1990). Moreover, they often move in quick bursts of intermittent locomotion, likely contributing to vigilance and predator avoidance (McAdam & Kramer, 1998). Their kinematics, such as the increased contribution and combined operation of proximal limb segments, more flexible spine, pelvic movements, and overall locomotor performance are convergently similar, compared to those of their larger relatives (Biewener, 1989a; Fischer et al., 2002; Iriarte-Díaz, 2002). Studying small arboreal and scansorial extant mammals is of importance in discussions of mammalian evolution because of the central role of small body size therein. Many Mesozoic early mammals, the first known metatherian (Luo et al., 2003) and the two oldest eutherians (Ji et al., 2002; Luo et al., 2011) were small, clawed, agile climbers, which likely utilized both terrestrial and arboreal substrates. Furthermore, the early ancestors of the order Primates, the mammalian order where humans are placed, have also been hypothesised to have been very small, clawed climbers, which shifted to a more confined use of a fine-branch niche (Cartmill, 1974a, 1992; Sussman, 1991; Gebo, 2004). Even though the limited available data on the effects of body size on locomotion in arboreal mammals has centred primarily around primates and their origin, they show that body size may significantly impact locomotor preferences, substrate use, and interplays adaptively with morphology (Fleagle & Mittermeier, 1980; Fleagle, 1985). For instance, in terms of substrate use, larger monkeys tend to use larger substrates, which can better support their weight (Fleagle & Mittermeier, 1980). Yet, by shifting to suspensory locomotion, they can readily exploit smaller substrates (Cartmill & Milton, 1977b; Fleagle & Mittermeier, 1980; Cant, 1992). Furthermore, body size is especially relevant to how animals approach vertical locomotion. Large and smaller vertical substrates enable rapid vertical ranging within the canopy, permitting arboreal mammals to exploit a wider range of forest strata. Smaller mammals tend to encounter larger vertical substrates, but can easily negotiate them via clawed locomotion, by interlocking with irregularities or crevices on the surface of tree trunks (Cartmill, 1974b, 1985; Youlatos, 1999b; Samaras & Youlatos, 2010; Orkin & Pontzer, 2011). Conversely, larger mammals are more prone to use prehensile grasping, utilising friction via expanded apical pads, as vertical clawed locomotion is biomechanically and physiologically disproportionately costly (Soligo and Martin 2006). These morpho-behavioural differences indicate divergent responses of small and large mammals to arboreal constraints. On the other hand, gait parameters related to arboreal stability, such as diagonality, seem to be independent of body size. Among smaller mammals, DS gaits are encountered in some arboreal primates (Shapiro et al., 2016), and some arboreal metatherians (Schmitt & Lemelin, 2002), whereas LS gaits are exhibited by other arboreal primates (Nyakatura et al., 2008; Stevens, 2008; Nyakatura & Heymann, 2010), few metatherians (Shapiro & Young, 2010), and scansorial rodents (Schmidt & Fischer, 2011). In larger mammals, terrestrial, arboreal, and scansorial primates (Cartmill et al., 2007) and an arboreal carnivore (Lemelin & Cartmill, 2010) exhibit DS gaits, whereas some arboreal metatherians (White, 1990) display LS gaits. Consequently, DS and LS gait distribution among arboreal mammals is particularly difficult to interpret, as many factors, such as phylogeny, habitat use, and substrate handling may play important roles. Apart from diagonality, data on other gait parameters, such as duty factor and duty factor index, are largely lacking. In terms of velocity, past research on both terrestrial and arboreal marsupials and rodents found only very weak to no correlations between body size and relative velocity (Delciellos & Vieira, 2006; Camargo et al., 2016), leading to conjectures that locomotor competence is better predicted by the ecological correlates of a species, rather than body size or phylogeny (Camargo et al., 2016). However, smaller mammals tend to regulate velocity primarily via stride frequency, which reduces disrupting body oscillations (Delciellos & Vieira, 2006; Nyakatura et al., 2008). In contrast, larger mammals display a higher contribution of stride length in the increase of velocity, which reduces branch sway which poses a more significant problem at a larger body size (Larson et al., 2001; Delciellos & Vieira, 2006). Hence, to clarify how small body size relates to the utilization of arboreal substrates, studying both clawed and non-clawed arboreal and scansorial mammals is essential. This would help elucidate the locomotor constraints related to any transition between terrestriality, scansoriality and arboreality, which may be confounded at a small body size (Jenkins, 1974). Although many small to mid-size therians follow similar locomotor patterns regardless of evolutionary history and phylogeny (Jenkins, 1974; Fischer et al., 2002; Schmidt, 2005), they can also differ in at least some aspects, such as gait patterns and the use of symmetrical and asymmetrical gaits (e.g. Schmitt & Lemelin, 2002; Shapiro & Young, 2010; Shapiro et al., 2016). It is thus important to identify any similarities or divergences in locomotor behaviour of small scansorial and arboreal mammals, as well as their adaptive value in the relevant microhabitats they exploit.
Even though we possess extensive information on gait parameters used during arboreal locomotion, most studied species are primates, or have been examined in relation to primate evolution. Furthermore, there is a significant lack of observations at the lower end of the mammalian size range. However, small clawed arboreal and scansorial mammals hold a special position, as they face much similar arboreal challenges (Jenkins, 1974). This leads to convergent locomotor responses that differ from those of their larger phylogenetically close relatives (Fischer et al., 2002). As ancestral therians (Ji et al., 2002; Luo et al., 2011) and possibly ancestral primates (Gebo, 2004) were purportedly equally small-sized and scansorially/arboreally adapted, they would have faced comparable challenges in arboreal locomotion. This renders extant small arboreal and scansorial mammals suitable models for identifying behavioural adaptive patterns in the evolution of mammalian arboreality. In order to achieve successful arboreal locomotion, mammals must cope with the properties of the arboreal milieu. This translates into moving on a mesh of branches ranging from very narrow to very wide, and placed at any possible angle. Mammals, therefore, must possess behavioural mechanisms which will increase arboreal stability and safety, and which will likely be related to the properties of the substrates they move on, such as substrate diameter and inclination, and the direction of locomotion (ascending, descending, or horizontal locomotion). However, previous research has demonstrated differential responses to substrate diameter or inclination, which may relate to the specific needs for arboreal locomotion. Nevertheless, it is likely that small body size may impose convergent behavioural effects, regardless of phylogeny. Regardless of convergences or dissimilarities, I expect to observe behaviours which will enhance stability and contribute to safe and secure body displacement. Towards this end, this study will address three goals: The first research goal is to examine how small mammals adjust gait parameters in relation to substrate diameter. On narrower substrates, animals are expected to adjust their gaits to increase stability and safety. For enhanced safety, study subjects, at least those which possess grasping hind feet, are expected to display higher diagonality on narrower substrates. As narrow substrates represent dangerous, unstable situations in a naturalistic setting, this would theoretically allow the forelimb to test novel substrates, while the contralateral hind limb remains anchored on the previous, stable substrate. To achieve better arboreal stability, duty factor is expected to increase on narrow substrates and velocity to decrease, as a slow, controlled walk should minimize instability by reducing the produced torques, increasing the simultaneous contact points on the substrate at any given time, and providing longer time periods to accomplish a stable and secure dynamic posture. On the other hand, subjects should be able to move faster on wider substrates, which would allow them to move swiftly to safety and avoid exposure to dangers in a natural setting. Hence, duty factor should decrease and velocity should increase as substrates become larger. Moreover, the use of asymmetrical gaits is expected to be more frequent on larger substrates, assisting in the increase of velocity. The second goal is to assess if and how substrate inclination and consequent ascending, descending or horizontal directions of movement affect gaits. During descents, there is an increased requirement for control of locomotion for safety, further marked by an anterior shift of the weight. Thus, the breaking and supportive role of the forelimbs should be enhanced and this may be expressed by a lower duty factor index, which should also be accompanied by a decrease in gait diagonality to assist in breaking. Furthermore, to assist in maintaining control of progression and safety, the velocity is expected to be lower than any other direction of movement. During ascents, animals need to generate propulsion to carry their body upwards, while maintaining stability. This propulsion is expected to be mainly produced by the hind limbs, leading to a higher duty factor index, also assisted by higher diagonality. Moreover, in maintenance of dynamic stability, ascents are expected to be characterised by higher velocity than descents or horizontal locomotion. The third goal is to diagnose whether gait metrics relate to any degree of arboreality in small mammals. More arboreal mammals are expected to be better adjusted to the challenges of arboreal locomotion and should be able to enhance locomotor stability and safety through their more specialised morphology and behaviour. On the other hand, less arboreal species are expected to be more cautious in their arboreal locomotion to minimise the chances of losing stability. In terms of gait parameters, this will likely lead to higher values of diagonality, higher velocity and possibly lower duty factor in more arboreal species. To expand our knowledge on the interplay of substrate characteristics and gaits in the arboreal locomotion of small mammals, this study will use an experimental approach of simulated arboreal settings, attempting to isolate substrate parameters and compare how different small mammals approach arboreal locomotion. Gait parameters, such as diagonality, duty factor, duty factor index, velocity, stride length, and stride frequency, which possibly all relate to arboreality, will be recorded in relation to the properties of the substrates. This research is broken down into case studies, addressing the behaviour of either a single, or comparing more than one species. Discovered trends, or lack thereof, similarities or divergences between species will be reviewed and will be linked to arboreal locomotion. Finally, I anticipate that this thesis will ultimately provide more insight into the arboreal behaviour of mammals, and serve as a valuable resource for future researchers.
This chapter is presented in full as its own standalone publication: Arboreal Gaits in Three Sympatric Rodents Apodemus agrarius, Apodemus flavicollis (Rodentia, Muridae) and Myodes glareolus (Rodentia, Cricetidae).
This chapter is presented in full as its own standalone publication: Vertical Locomotion in Micromys minutus (Rodentia: Muridae): Insights Into the Evolution of Eutherian Climbing.
This chapter is presented in full as its own standalone publication: Arboreal Locomotion in Eurasian Harvest Mice Micromys minutus (Rodentia: Muridae): The Gaits of Small Mammals.
This chapter is presented in full as its own standalone publication: Arboreality in Acacia Rats (Thallomys paedulcus; Rodentia, Muridae): Gaits and Gait Metrics.
This chapter is presented in full as its own standalone publication: Comparing the Arboreal Gaits of Muscardinus avellanarius and Glis glis (Gliridae, Rodentia): A First Quantitative Analysis.
This chapter is presented in full as its own standalone publication: Diagonal Gaits in the Feathertail Glider Acrobates pygmaeus (Acrobatidae, Diprotodontia): Insights for the Evolution of Primate Quadrupedalism.
The results obtained from the case studies show that gaits relate to arboreality in various ways, which are often not uniform. Arboreal species display behaviours which maximize their abilities to efficiently utilize arboreal substrates. More terrestrial species may not be as able to negotiate slender substrates, however, they modify their behaviour appropriately to cope with the challenges of arboreality. In this last section, the results from the previous chapters will be comparatively discussed to uncover any trends related to substrate size and direction of movement (i.e. ascent, descent, or horizontal locomotion). Moreover, I proceeded to a meta-analysis of selected trends in an attempt to link gait parameters to an animal’s degree of arboreality, which would provide insights on common patterns for an arboreal lifestyle among mammals.
Substrate size. Overall, the effect of substrate size on gaits, across the small mammals examined, was rather uniform (Table 8.1), except for diagonality (D). Duty factor (DF) was reduced on narrower substrates whereas duty factor index (DFI) was not affected by substrate size across the tested species. Diagonality (D) was the only parameter subject to variability across species. Only Acrobates pygmaeus increased D on narrow substrates in contrast to Apodemus agrarius, A. flavicollis and Micromys minutus in which D decreased. Thallomys paedulcus and Myodes glareolus showed no effect of substrate size on D, and among the two glirids, Glis glis made exclusive use of asymmetrical gaits, while Muscardinus avellanarius used LS symmetrical gaits only on the narrowest substrates, switching to asymmetrical gaits on all other. Similar results for most gait parameters, excluding D, reported for other mammals of various taxa and body sizes (Lammers & Biknevicius, 2004; Stevens, 2006; Nyakatura et al., 2008; Shapiro et al., 2016), indicate that the effect of substrate size on these gait parameters may be conserved across mammalian groups.
Table 8.1. Effect of substrate size on various gait metrics for each species examined, as determined by ANCOVA tests (See respective chapters for exact results). Positive indicates that the metric increases on larger substrates. Negative indicate a decrease in the metric on larger substrates. Positive and negative results are significant at p<0.05. None indicates no significant relationship (p>0.05), and Unknown means that there is not enough data to compute relationships.
| Species | Diagonality | Duty Factor | Duty Factor Index | Velocity | Stride Length | Stride Frequency |
|---|---|---|---|---|---|---|
| Acrobates pygmaeus | Negative | Negative | None | Positive | Positive | Positive |
| Muscardinus avellanarius | Unknown | Negative | None | Positive | Positive | Positive |
| Glis glis | Unknown | None | None | None | None | None |
| Myodes glareolus | None | Negative | None | Positive | Positive | None |
| Apodemus agrarius | Positive | Negative | None | Positive | Positive | Positive |
| Apodemus flavicollis | Positive | Negative | None | Positive | Positive | Positive |
| Micromys minutus | Positive | Negative | None | Positive | Positive | Positive |
| Thallomys paedulcus | None | Negative | None | Positive | Positive | Positive |
These observations have immediate implications for theories regarding gait adaptations during arboreal locomotion. It has been hypothesised that the diagonal-sequence diagonal couplet (DSDC) footfall pattern (i.e. increased D) is favourable to arboreal mammals. It allows them to explore new, potentially unstable substrates with their forelimbs, while their safely anchored contralateral grasping hind limbs permit them to withdraw in case of instability, keeping their centre of mass within the support polygon of the limbs (Cartmill et al., 2007). Consequently, the frequency of DS gaits should increase on fine branches, which are more prone to bending or breakage. On one hand, D was indeed found to increase on narrow substrates in the arboreal specialist A. pygmaeus, characterized by grasping hind and forefeet (Rosenberg & Rose, 1999), overall faster locomotion, and a predominant use of DS gaits, contrary to the LS gaits of the other species examined here. Although testing new substrates through DS gaits seems improbable during high speed locomotion (Nyakatura et al., 2008), the diagonally paired limbs of DS gaits may confer better dynamic stability (i.e. during fast locomotion), allowing possibly a better control and transfer of moments and torques across the body axes (Lammers & Zurcher, 2011a). Increased D on narrow branches, as exemplified by A. pygmaeus, with DSDC gaits, produces medially-oriented forces (Schmitt, 2003b; Lammers & Biknevicius, 2004; Schmidt & Fischer, 2010), and allow animals to seize the branch and increase the force applied, and consequently friction, which makes slipping less likely (Lammers & Zurcher, 2011a). Moreover, opposing mediolateral and angular impulses generated by the contralateral limbs may reduce mediolateral deviations from the long axis of the branch (Shapiro & Raichlen, 2007). Although the previous explanation for DS gaits focuses on grasping hind feet (Cartmill et al., 2007), this highlights that powerful or at least strong grasping forelimb capacity may be integral for effective DS gaits, as the combined function of fore- and hind limbs would contribute to increasing stability. Muscardinus avellanarius, for instance, moves even faster than A. pygmaeus at the narrowest substrates, hence requiring good dynamic stability utilised LSDC gaits, however. Although both animals possess grasping hind feet (Stafford, Rosenberger & Beck, 1994; Haffner, 1998), A. pygmaeus is further differentiated by its increased forelimb grasping ability (Rosenberg & Rose, 1999). However, further research is required regarding the contribution of grasping forelimbs in DS gaits to test this hypothesis. Lastly, the gaits of A. pygmaeus are also often ambles, in which D is over 50, and DF below 50, and at least one limb is on the substrate (Schmitt et al., 2006). The lack of an aerial phase in ambling gaits limits the dorsal and ventral accelerations of the centre of mass, thus reducing peak vertical forces, which in turn reduce the vertical oscillations of narrow branches (Young, 2009) on which A. pygmaeus specialises. Conversely, most of the sampled species displayed lower D on narrower substrates, regardless of the presence of grasping hind feet [in T. paedulcus (De Graaff, 1978), M. minutus (Haffner, 1998), and A. flavicollis (Krattli, 2001)], or lack of hind foot grasping ability [in A. agrarius and M. glareolus (Krattli, 2001; Zefferer, 2002)]. This prevalent use of LS gaits by most scansorial and arboreal small mammals examined, as well as the decrease of D on narrow substrates, implies behavioural adaptations for increased static stability (slow locomotion) on arboreal substrates. This is due to the fact that the centre of gravity always passes through the support polygon during LS gaits, provided that three or four limbs are in contact with the substrate, hence at high DFs (Lammers & Zurcher, 2011a), as was observed in most of the examined scansorial species. For an animal that habitually uses LS gaits, it is therefore possible that lower D combined with a high DF is preferable, and optimises arboreal stability compared to gaits of higher D. Moreover, this strategy may be best suited for mammals that do not possess strong grasping abilities of the hind or forefeet and possibly cannot apply very strong contralateral forces during arboreal locomotion. Duty factor (DF) increased progressively on narrower substrates for most of the examined species. The shortening of swing phases relative to stance phases was in all cases accompanied by a predicted decrease in velocity, suggesting cautiousness in locomotion on narrow substrates. These results are in line with observations in arboreal metatherians and primates (Delciellos & Vieira, 2006; Nyakatura & Heymann, 2010). On the other hand, some arboreal neotropical rodents seem to increase velocity on narrow substrates (Camargo et al., 2016), possibly enhancing their dynamic stability (Schmidt & Fischer, 2011) by producing non-zero angular momentum through small distortions of their body such as the rotation of the limbs around the hip joint or the centre of rotation of the scapula (Lammers & Zurcher, 2011a). Nevertheless, the reduction of velocity seems to provide different advantages. Narrow substrates impose a more mid-sagittal placement of the limbs than wider substrates, producing narrower support polygons (Cartmill et al., 2007; Lammers & Zurcher, 2011a). As a result, there is an increased probability of the centre of mass being positioned outside the support polygon due to the laterally-directed destabilising torques at touchdown (Lammers & Zurcher, 2011b). The observed higher DFs and lower velocities increase the number of simultaneous contact points and the relative contact time with the substrate, assisting in counteracting the destabilising torques (Lammers & Gauntner, 2008; Lammers & Zurcher, 2011b). Moreover, the inverse correlation between D and DF, observed in most species examined here and in other arboreal mammals which habitually employ LSDC gaits, has been shown to optimise the support polygons produced during a stride cycle (Cartmill et al., 2002, 2007). This further adds to the argument that LSDC gaits may be preferable in terms of static stability (i.e. slower locomotion), reducing the danger of toppling over and maximizing safe navigation at lower speeds (Lammers & Zurcher, 2011a). The duty factor index (DFI) is unaffected by changes in substrate diameter in all species examined (Table 8.2). Even though DFI indicates some interspecific variation, implying elevated dominance of the forelimbs or hind limbs in different species, it seems that the roles of the two sets of limbs remain constant regardless of the narrowness of substrates. This is similar to findings in primates (Nyakatura et al., 2008) and rats (Schmidt & Fischer, 2010), and this was partly expected, as any anterior or posterior weight distribution does not depend on substrate diameter, but on substrate inclination and ascending or descending locomotion (Preuschoft et al., 1995; Preuschoft, 2002). Moreover, it highlights that despite the grasping capabilities of the hind limbs of many of the species studied, the hind limbs may not be biomechanically involved in increasing stability on narrower substrates by an increased stance to swing phase ratio. In contrast, when small mammals are on larger substrates, they maximise their locomotor competence by increasing velocity, and swing to stance ratios of the limbs (lower DF). As a result, small mammals, which are often exposed to high predation pressures, are able to move swiftly between stops, minimising exposure and maximising vigilance for predators (McAdam & Kramer, 1998). Often, this increase in velocity is achieved by switching to asymmetrical gaits (Hildebrand, 1977; Gasc, 2001; Young, 2009; Shapiro et al., 2016), as displayed by A. flavicollis, T. paedulcus, and M. avellanarius. Overall, asymmetrical gaits may be of high importance for improving arboreal locomotion (Flaherty et al., 2010). Their role in an arboreal context has been overlooked, but they have been gaining attention recently (i.e. Young, 2009; Shapiro et al., 2016). Asymmetrical gaits may confer a few advantages compared to symmetrical gaits at higher velocities. For instance, the transition from symmetrical trots to asymmetrical gallops in horses has been shown to contribute to decreasing peak substrate reaction forces, which in turn significantly reduces the considerable strain born by the musculoskeletal system during high-speed locomotion (Farley & Taylor, 1991). The same transition, from trot to gallop, may also reduce metabolic costs, making asymmetrical gaits more economical at a higher velocity (Hoyt & Taylor, 1981). Moreover, when asymmetrical gaits are used in an arboreal context, they have several characteristics that increase stability. Marmosets, squirrel monkeys, and red tree squirrels, all avoid full-body suspension phases, increase the duration during which limbs are in contact with the substrate, and also increase the time interval between the touchdown of trailing and leading limbs during asymmetrical gaits (Young, 2009; Schmidt & Fischer, 2011; Shapiro et al., 2016). These special characteristics of arboreal asymmetrical gaits contribute to arboreal stability of small mammals at higher velocities. To sum up, small mammals tend to respond to substrate diameter in various ways, all of which tend to increase their stability and safety. The mechanisms which are common among most species are the use of LS gaits concurrently with an increased DF and a reduction in velocity, all of which increase the static stability of locomotion. On the other hand, DFI is not affected, implying maintenance of the roles of fore- and hind limbs in locomotion regardless of substrate diameter. Last, the use of DS gaits displayed by A. pygmaeus may relate to dynamic stability and an increased degree of arboreality, especially when accompanied by enhanced grasping capacities in both fore- and hind limbs.
Direction of movement. Results regarding the relationship of gait metrics to ascending, descending, and horizontal locomotion were not as clear cut as was observed for substrate diameter (Table 8.2). In most species for which symmetrical gaits were recorded direction of movement had no effect on D, except for A. pygmaeus and M. minutus. In A. pygmaeus D was higher during horizontal locomotion than during descents or ascents, which scored similarly. In M. minutus, D was lower in horizontal locomotion than during descents or ascents, which also scored similarly. DFI was in most cases higher in ascents, followed by horizontal locomotion, and descents. No effect of the direction of movement on DFI was observed in M. glareolus and T. paedulcus. The duty factor (DF) was, in most cases, higher in horizontal compared to descending locomotion. However, A. flavicollis and T. paedulcus did not adjust DF according to their direction of movement. During ascents, DS gaits along with a higher DFI are thought to assist in generating additional propulsion (Nyakatura et al., 2008). In these gaits, the hind limbs touch down shortly before their contralateral forelimbs. As a result, a considerable proportion of the hind limbs’ stance phase has elapsed before the touchdown of the diagonal forelimbs. This temporal spacing brings the hind foot spatially closer to the pivot of the extremity which is producing propulsion, or may have already started contributing to propulsion itself. As a result, an increased D during ascents may have an adaptive advantage, by reducing the retarding role of the forelimbs in the first part of their stance phase, while the autopodium is still anterior to the pivot of the extremities (Nyakatura et al., 2008). However, none of the species studied increased D in ascents, except for M. minutus. On the other hand, the higher DFI observed in most species during ascents, i.e. a higher DF of the hind limbs in relation to the DF of the forelimbs, confirms that during ascents there is a higher reliance on hind limbs for propulsion due to a posterior weight shift (Preuschoft et al., 1995; Preuschoft, 2002). In an opposite manner, downward locomotion causes an anterior weight shift, which in some species such as A. pygmaeus, A. flavicollis, and M. minutus, caused a reduction in DFI, suggesting a higher reliance on the forelimbs. This is due to a higher portion of vertical impulse transferred to the forelimbs which enhances their regulative and supportive role (Rollinson & Martin, 1981; Nyakatura et al., 2008). However, in some species (e.g. M. glareolus and T. paedulcus), DFI remained constant, regardless of the direction of locomotion. The lack of changes in the DFI implies that the roles of the two sets of limbs in locomotion may not be affected by the inclination of the substrate, as has been proposed based on similar results in rats and European red squirrels (Schmidt & Fischer, 2011). In most studied species, velocity increased during ascents compared to horizontal locomotion or descents. This observation contrasts previous results in a number of mammalian and non-mammalian vertebrates moving on inclines (Birn-Jeffery & Higham, 2014). Our observations, however, may relate to the specific challenges of arboreal locomotion. Velocity increase on inclines has been also observed in European red squirrels (Sciurus vulgaris), and has been functionally related to the maintenance of dynamic stability (Schmidt & Fischer, 2011) by non-zero angular momentums (Lammers & Zurcher, 2011a). On the other hand, T. paedulcus was slower in ascents, which may promote static stability during arboreal locomotion (Schmidt & Fischer, 2011) through more controlled, cautious locomotion. Moreover, for those species for which descents were recorded, velocity was higher compared to that of horizontal locomotion. This may possibly indicate that animals take advantage of gravity when descending, in order to reduce their energy expenditure (Birn-Jeffery & Higham, 2014).
Table 8.2. Effect of the direction of movement on various gait metrics for each species examined, as determined by ANCOVA tests (See respective chapters for exact results). Comparisons between descents (Des), horizontal locomotion (Hor) and ascents (Asc) at the p<0.05 level of significance. ( “=” stands for similar; “>” stands for larger; “≥” stands for larger but insignificant; “unknown“ stands for lack of data).
| Species | Diagonality | Duty Factor | Duty Factor Index | Velocity | Stride Length | Stride Frequency |
|---|---|---|---|---|---|---|
| Acrobates pygmaeus | Hor > Des = Asc | Hor > Des = Asc | Asc > Hor > Des | Asc = Des > Hor | Des = Hor = Asc | Des = Asc > Hor |
| Muscardinus avellanarius | Unknown | Unknown | Unknown | Unknown | Unknown | Unknown |
| Glis glis | Unknown | Unknown | Unknown | Unknown | Unknown | Unknown |
| Myodes glareolus | Des = Hor | Hor > Des | Des = Hor | Des > Hor | Des = Hor | Des > Hor |
| Apodemus agrarius | Des = Hor | Hor > Des | Hor > Des | Des ≥ Hor | Des = Hor | Des > Hor |
| Apodemus flavicollis | Des = Hor = Asc | Des = Hor = Asc | Asc > Hor > Des | Asc > Hor > Des | Des = Hor = Asc | Asc > Hor > Des |
| Micromys minutus | Des = Asc > Hor | Hor = Asc > Des | Asc (=Des) > Hor (=Des) | Des = Asc > Hor | Des = Asc > Hor | Des (=Asc) > Hor (=Asc) |
| Thallomys paedulcus | Hor = Asc | Hor = Asc | Hor = Asc | Hor > Asc | Hor > Asc | Hor = Asc |
In order to diagnose whether the degree of arboreality and gait metrics relate, the eight species examined were initially ranked by degree of arboreality based on existing ecological data. The metatherian A. pygmaeus is exclusively arboreal (Goldingay & Kavanagh, 1995), and although it is possible, I have not found any reports of them descending to the ground. The two glirids, M. avellanarius and G. glis, are extensively arboreal, staying primarily on trees and bushes, but also occasionally descent to the ground to burrow (Juškaitis, 2008; Kryštufek, 2010). Thallomys paedulcus relies heavily on arboreal locomotion on acacia trees, however also digs burrows and finds shelter among the roots of trees (Earl & Nel, 1976; De Graaff, 1978). Micromys minutus is primarily arboreal during the breeding season, but also spends extensive periods on the ground (Nordvig et al., 2001). Among the remaining rodents, A. flavicollis often climbs on trees (Borowski, 1962; Montgomery, 1980), while M. glareolus is an occasional climber (Montgomery, 1980), though both are primarily terrestrial. Lastly, A. agrarius is possibly exclusively terrestrial (Böhme, 1978), as there are no reports of it being captured or observed on on trees or bushes. An ANCOVA was carried out for the gait metrics (diagonality, duty factor, duty factor index, dimensionless velocity, dimensionless stride length, and dimensionless stride frequency) to explore if significant differences exist between species. As ascending and descending locomotion was missing for some species, only data on horizontal locomotion were used. Furthermore, in order to compensate for differences in body size, substrate diameters were divided by the mean head-body length of each species, to obtain a measure of adjusted dimensionless substrate size (Alexander, 1977). The adjusted substrate size was inserted as covariate into the ANCOVA model for all tests. All obtained ANCOVA results were significant at p<0.001 (Fig. 8.1, Table 8.3). Moreover, a Principal Component Analysis (PCA) was performed using mean gait parameters (diagonality, duty factor, duty factor index, dimensionless velocity, dimensionless stride length, and dimensionless stride frequency) for each species on each substrate used. Glis glis was excluded from the analysis (exclusively asymmetrical gaits, therefore lack of data on diagonality). In the PCA, the first two axes explained 86.16% of the observed variance (axis 1: 60.86%; axis 2: 23.50%) and all observations were subsequently plotted and examined in the space described by these two axes (Fig. 8.2; Table 8.4). Among the metrics examined, duty factor was lower (N=7, F(7,434)=143.084, p<0.001) and stride frequency higher (Ν=7, F(7,434)=100.482) in more arboreal species, and both seemed to be most consistent in predicting the degree of arboreality (Fig. 8.1). Duty factor and dimensionless stride frequency were also the primary contributors to Factor 1 of the PCA which separated arboreal species from terrestrial ones (Table 8.4; Fig. 8.2). Diagonality (Ν=6, F(6,323)=8.166) was an adequate predictor of arboreality in the most arboreal species, and was overall positively linked with levels of arboreality. However, the pattern of higher diagonality for increased arboreality did not hold in the most terrestrial species (Fig. 8.1). All remaining metrics, although significantly different between species, did not seem to relate to the degree of arboreality. Moreover, dimensionless velocity, although overall higher in more arboreal than in more terrestrial species (Delciellos & Vieira, 2006; Camargo et al., 2016), was not a reliable predictor of their degree of arboreality (Fig. 8.1; Table 8.3).
Table 8.3. Estimates of gait metric means (and SD given in brackets) based on ANCOVA for all study species ordered by degree of arboreality. ANCOVA F values and significance levels are also reported for each metric. “Dim.” means dimensionless values of the respective gait metrics.
| Arboreality Rank | Species | N | Diagonality | Duty Factor | Duty Factor Index | Dim. Velocity | Dim. Stride Length | Dim. Stride Frequency |
|---|---|---|---|---|---|---|---|---|
| 1 | Acrobates pygmaeus | 6 | 52.7 (0.80) | 42.12 (0.84) | 99.80 (1.52) | 1.637 (0.049) | 2.452 (0.047) | 0.654 (0.014) |
| 2 | Muscardinus avellanarius | 1 | 39.0 (2.62) | 44.00 (1.39) | 109.51 (2.52) | 2.109 (0.081) | 3.417 (0.078) | 0.599 (0.023) |
| 3 | Glis glis | 1 | No symmetrical gaits | 55.26 (1.60) | 111.06 (2.90) | 0.887 (0.094) | 1.946 (0.090) | 0.453 (0.026) |
| 4 | Thallomys paedulcus | 12 | 33.0 (1.63) | 64.28 (1.25) | 100.06 (2.28) | 1.249 (0.074) | 2.698 (0.070) | 0.423 (0.020) |
| 5 | Micromys minutus | 6 | 32.1 (1.01) | 70.64 (1.06) | 92.57 (1.92) | 0.536 (0.062) | 2.073 (0.059) | 0.251 (0.017) |
| 6 | Apodemus flavicollis | 2 | 32.9 (1.63) | 69.65 (1.70) | 99.12 (3.08) | 0.771 (0.065) | 2.852 (0.063) | 0.265 (0.018) |
| 7 | Myodes glareolus | 2 | 25.0 (1.52) | 72.89 (1.59) | 105.90 (2.88) | 0.527 (0.093) | 2.084 (0.089) | 0.249 (0.026) |
| 8 | Apodemus agrarius | 2 | 32.3 (1.07) | 75.43 (1.12) | 100.01 (2.02) | 0.491 (0.065) | 2.213 (0.063) | 0.217 (0.018) |
| ANCOVA | F(6,323)=8.166, p<0.001 | F(7,434)=143.084, p<0.001 | F(7,434)=6.636, p<0.001 | F(7,434)=73.939, p<0.001 | F(7,434)=44.449, p<0.001 | F(7,434)=100.482, p<0.001 |
Figure 8.1. Gait metric means for all studied species as estimated through ANCOVAs. Estimates were predicted using dimensionless conversions of substrate diameters and inserting them as covariates in the ANCOVA model. In the diagonality graph, Glis glis is absent, due to lack of symmetrical gaits. Jacknives on each bar represent estimates of standard deviation. Species are ordered in decreasing arboreality from left to right.
Table 8.4. Principal components obtained from the covariance matrix of gait parameters. Cases used for the principal component analysis were mean gait parameters (diagonality, duty factor, duty factor index, dimensionless velocity, dimensionless stride length, and dimensionless stride frequency) for each species on each substrate diameter used.
| Factor 1 | Factor 2 | |
|---|---|---|
| Diagonality | -0.375 | -0.396 |
| Duty Factor | 0.503 | -0.007 |
| Duty Factor Index | 0.0734 | 0.738 |
| Dimensionless Velocity | -0.496 | 0.175 |
| Dimensionless Stride Length | -0.330 | 0.505 |
| Dimensionless Stride Frequency | -0.496 | -0.110 |
| Eigenvalue | 3.652 | 1.410 |
| % of variance explained | 60.86 | 23.50 |
Figure 8.2. Projection of variables used in the the PCA (top) and of species (bottom) on the plane described by the first two factors. Species are represented using initials (AP: Acrobates pygmaeus:; AA: Apodemus agrarius; AF: Apodemus flavicollis; GG: Glis glis; MM: Micromys minutus; MA: Muscardinus avellanarius; MG: Myodes glareolus; TP: Thallomys paedulcus). Each point corresponds to each substrate diameter cateogory with observations for given species. A higher duty factor represents larger percentages of a gait cycle in which the limbs are on the substrate. It accommodates arboreal stability by reducing touchdown torques, increasing simultaneous contact points and contact periods with the substrate (Lammers & Zurcher, 2011b). The increased duty factor in more terrestrial species implies that this may be a behavioural response to increase stability on narrow substrates for which they are not well-adapted. On the other hand, arboreal species, adapted to the challenges of the arboreal milieu, maintained longer swing phases relative to stance phases. Towards increasing stability and safety, less arboreal mammals are also characterised by lower stride frequency, which along with the higher DF, and an overall lower velocity than more arboreal mammals, indicate a more cautious locomotion. Cautiousness may be essential for arboreal locomotion because of the lack of morphological or behavioural mechanisms that specifically facilitate arboreal stability in less arboreal mammals. This would then also translate to longer reaction times to avoid obstacles, and a consequent reduced likelihood for potentially fatal errors. On the other hand, mammals that are more inclined to use the arboreal milieu may have ultimately developed morphological adaptations that allow them to move more rapidly and decrease their DF. Moreover, hip and scapular mobility, often encountered among more arboreal mammals (Cartmill, 1985), combined with a higher velocity may assist in increasing stability by counteracting the torques generated at limb touchdown (Lammers & Gauntner, 2008; Lammers & Zurcher, 2011b). The counteraction of torques is achieved by generating non-zero angular momentums through small movements in their body, such as rotations of the limbs around the hip joint or the scapula, ultimately increasing dynamic stability on arboreal substrates (Lammers & Gauntner, 2008; Lammers & Zurcher, 2011a). Moreover, more arboreal mammals display a higher stride frequency which essentially implies more frequent contact with the substrate. This enables a greater control of movement, allowing easier halts and swifter changes of direction when obstacles are encountered (Kram & Taylor, 1990; Hoyt, Wickler & Cogger, 2000; Hanna, 2006; Hanna & Schmitt, 2011b). The facilitation of obstacle avoidance may be of adaptive importance on arboreal substrates which are characterised by irregularities on their surface such as protrusions of branches, branch stubs, and crevices in the bark. Moreover, branches are mobile, both around and perpendicularly to their longitudinal axis, and leaves or other branches may block an animals’ path. During fast locomotion, these distractions require swift action, coupled with minimising the possibility of correcting errors and may induce a lack of stability. Furthermore, stride frequency is a more significant factor to velocity increase than stride length in all the small mammals examined here, regardless of their degree of arboreality. Regulation of velocity by stride frequency decreases body oscillations, which may disrupt continuous progression and may thus be more advantageous for smaller arboreal and scansorial mammals (Strang & Steudel, 1990; Delciellos & Vieira, 2007). Lastly, in some scansorial and arboreal mammals, the increase in velocity is further facilitated by the use of asymmetrical gaits on larger substrates. Fast asymmetrical gaits may be favourable over fast symmetrical gaits for arboreal locomotion (Young, 2009; Flaherty et al., 2010; Schmidt & Fischer, 2011; Shapiro et al., 2016) as they may cause less strain on the muscles and bones and result in a lower energetic expenditure (Farley & Taylor, 1991; Wickler et al., 2003). Nevertheless, more research on the detailed kinematics of asymmetrical gaits is required in order to understand how small mammals specifically use and adapt these gaits on arboreal substrates where a loss of balance is dangerous. Another common pattern observed here is that small clawed scansorial and terrestrial mammals primarily opted for lateral-sequence (LS) gaits during arboreal locomotion. Moreover, even on the narrowest substrates utilised they reduced D rather than increasing it (i.e. using DS gaits). Most mammalian species examined, terrestrial or scansorial, as well as most reptiles, display LS footfall patterns (Hildebrand, 1976; Cartmill et al., 2002; Witte et al., 2002; McElroy, Hickey & Reilly, 2008), contrary to the DS footfall pattern most often observed among arboreal mammals (Cartmill et al., 2002, 2007). The most parsimonious hypothesis, therefore, is that LS gaits likely represent an ancestral state, whereas DS gaits are derived. The retention of the ancestral LS footfall pattern, along with a reduction in the relative swing phases of the limbs, can confer competent arboreal stability by keeping the centre of mass always within the support polygon (Lammers & Zurcher, 2011a). On the other hand, the most arboreal A. pygmaeus was isolated from other species on the negative side of the PC axes (Fig. 8.2). This placement was related to high dimensionless stride length, stride frequency, velocity, and diagonality (Fig. 8.2, Table 8.3). Feathertail gliders were the only species in this study that habitually employed diagonal-sequence diagonal couplets (DSDC) gaits. However, contrary to A. pygmaeus, the similarly sized and highly arboreal M. avellanarius used equally narrow substrates, moved at higher velocities than A. pygmaeus, and utilized LSDC gaits. The highly arboreal M. avellanarius was isolated on the positive side of axis 2 and the negative side of axis 1, due to their high stride length, stride frequency, velocity, and DFI (Fig. 8.2, Table 8.3). Among other things, M. avellanarius differs from A. pygmaeus in the lack of increased grasping abilities of the forelimb (Haffner, 1998). As argued earlier, it is possible that grasping by both the manus and the pes is required to make DSDC more useful than LSDC gaits in an arboreal setting. If grasping forefeet are present, and arboreality is a primary component in an animal’s ecology, the evolution of DS gaits may be favourable, as they produce medially-oriented forces (Schmitt, 2003b; Lammers & Biknevicius, 2004; Schmidt & Fischer, 2010) and allow animals to apply contralateral pressure on substrates and consequently increase friction, making slipping less likely (Lammers & Zurcher, 2011a). However, the results from this research cannot support this hypothesis. Future research into the forces applied by both clawed and non-clawed mammals which utilise both DS and LS gaits and especially in relation to substrate use may be more informative in relation to this question. Nevertheless, as D is not the most reliable predictor of arboreality in the meta-analysis carried out it seems that DSDC gaits may not be essential for successful arboreal locomotion as its occurrence does not increase with increased arboreality. Scansorial mammals can be also successful in achieving arboreal stability by using LS gaits, and utilise other mechanisms alongside this footfall pattern, such as increased DF and lower stride frequency. Levels of arboreality have no overall effect on the duty factor index. Most of the studied scansorial/arboreal mammals displayed an increased hind limb to forelimb duty factor ratio (DFI) when ascending, with the opposite trend observed while descending. The higher DFI observed during ascents indicates a higher reliance on the hind limbs for propulsion due to a posterior weight shift (Preuschoft et al., 1995; Preuschoft, 2002). On the other hand, the anterior shift in weight during descents causes more vertical impulse on the forelimbs which then assume a more pronounced regulatory and support role (Rollinson & Martin, 1981; Nyakatura et al., 2008). Moreover, as exhibited by M. minutus, this compartmentalisation in fore- and hind limb use may also be of great importance during vertical climbing. The separation in the roles of the fore- and hind limbs may be especially significant for both scansorial and arboreal mammals as perfectly horizontal substrates are rarely encountered. Similarly, the high duty factor index observed during above-branch locomotion in both glirids, M. avellanarius and Glis glis, implies hind limb dominance in locomotion. Both glirid species examined here are primarily arboreal animals which often move vertically between the canopy strata, yet also descend to the ground for burrowing (Juškaitis, 2008; Kryštufek, 2010). Thus, they engage in frequent climbing, hanging and clambering, facilitated by the possession of long digits, curved claws, a tendon-locking mechanism, and pedal grasping (Haffner, 1996, 1998; Krattli, 2001; Zefferer, 2002). Their ecology and morphological adaptations highlight a possible hind limb dominance which has been functionally linked to habitual vertical climbing (Preuschoft, 2002). A high duty factor index was also observed in the highly terrestrial M. glareolus. Even though their gross morphology is linked with digging and terrestrial locomotion, some Myodes species, including bank voles, occasionally vertically climb arboreal substrates (Buesching et al., 2008; Nations & Olson, 2015) and would thus benefit from an elevated duty factor index. Nevertheless, the observed hind limb dominance may relate to other aspects of their ecology, as they are much more terrestrial in their locomotor habits (Buesching et al., 2008). However, since the present study lacks adequate data, especially vertical locomotion observations, this is speculative and requires further research. Most other species displayed duty factor indices close to 100 which may be an indication of different but equal contributions by the forelimbs and the hind limbs to locomotion (Schmidt & Fischer, 2011). The data on DFI that I have collected here produce more questions than answers and more observations, as well as more individuals tested, in arboreal small mammals are essential to determine how and why forelimbs and hind limbs participate in arboreal locomotion. Interestingly, the four studied murid rodents (A. agrarius, A. flavicollis, M. minutus, T. paedulcus), as well as the cricetid M. glareolus, were more or less clustered closely together in the PCA (Fig. 8.1). They appear to be characterised by higher duty factor, but lower velocity, stride length and stride frequency than more arboreal species (Table 8.3, Fig. 8.1). The more terrestrial A. agrarius, along with M. glareolus, were placed at the positive end of this cluster, on the opposite side to the arboreal A. pygmaeus and M. avellanarius, probably in relation to their higher duty factors (Fig. 8.1). On the other hand, the more arboreal T. paedulcus, M. minutus, and A. flavicollis were located at the centre of the axes, between the most arboreal and the most terrestrial species, possibly implying an intermediate degree of arboreality. However, besides the lower duty factor and stride higher frequency of the more arboreal murids, T. paedulcus, M. minutus, and A. flavicollis did not differ greatly from the terrestrial representatives. Although arboreal and terrestrial murids differ substantially in appendicular morphology (Krattli, 2001; Zefferer, 2002; Samuels & Van Valkenburgh, 2008; Kuncová & Frynta, 2009), our results suggest that gaits may be more or less conserved within the family. However, since both terrestrial and arboreal locomotion are implicated in most of the examined species it may also be that the terrestrial component is what shapes their gaits most strongly. For instance, all rodents use LS gaits which may be more stable in terrestrial locomotion than DS gaits (Lammers & Zurcher, 2011a). These common patterns also bear some implications for mammalian locomotor evolution. The oldest known eutherians (Ji et al., 2002; Luo et al., 2011) and metatherian (Luo et al., 2003) were small and scansorial suggesting that both characteristics may have also been featured in the common ancestor of the two lineages. As argued earlier, the LS footfall pattern may represent an ancestral state, being the most common pattern among mammals and reptiles (Hildebrand, 1976; Cartmill et al., 2002; Witte et al., 2002; McElroy et al., 2008). Moreover, most small mammals examined in this research, which are similarly sized to Eomaia (20-25 g), Juramaia (15-17 g), and Sinodelphys (~30 g), used LS gaits during arboreal locomotion as well. Thus, it is highly probable that the LS footfall pattern characterised early mammals as well. These ancestors were most probably able to climb on shrubs and trees and would also have engaged in above-branch locomotion. In order to increase their stability, we would expect them to shift to gaits of lower D, higher DF, and lower velocity, as substrates became narrower, as well as increase velocity by stride frequency. Ascents, whether inclined or vertical, would be facilitated by increased input of propulsion by their hind limbs rather than the forelimbs. On the other hand, descents would place an emphasis on regulation and control of locomotion by their forelimbs. Thus, they would be able to ascend from the ground up to trees and bushes as fast as possible and descend head-first, being able to safely control their motion and scan the ground for dangers or food. To conclude, small clawed mammals are integral in understanding how arboreality has evolved throughout mammalian history. Despite limitations, they can be used as living models to understand morpho-behavioural adaptations in extinct and ancestral mammalian species. Moreover, they represent different adaptive scenarios compared to larger mammals which tend to possess special morphological adaptations in order to navigate the arboreal milieu. Moreover these large mammals are much more derived than ancestral mammalian morphotypes, such as Eomaia and Juramaia. This research, though by far non-exhaustive, shows that several small mammals display similar patterns in their gait which tend to optimize their ability to utilise arboreal substrates. Nevertheless, there is still much to be done. One important future addition would be more extended studies on the vertical locomotion of scansorial mammals, as climbing is a very demanding and important aspect of their ecology. Furthermore, the parameters studied herein effectively demonstrate some overall patterns and assist in constructing a gross locomotor profile of these species in relation to substrate properties. More detailed kinematic analyses of how small mammals adapt their gait and limb movements for arboreal locomotion is essential, however. Especially, higher resolution data on the spatial placement of the limbs on different substrates, as well as adjustments in the motion of joints coupled to measurements of locomotor forces and pressures would be insightful. Lastly, due to the small differences in size this study is not informative on the differences between smaller and larger mammals. Further comparative research on gait differences in animals of different body sizes can inform us on how size affects quadrupedal arboreal locomotion, an issue that has not been addressed adequately thus far.
Alexander, R.M. (1977). Terrestrial locomotion. In Mechanics and Energetics of Animal Locomotion: 168–203. Alexander, R.M. & Goldspink, G. (Eds). London: Chapman & Hall.
Alexander, R.M. (1992). Exploring Biomechanics: Animals in Motion. New York: Scientific American Library.
Alexander, R.M., Dimery, N.J. & Ker, R.F. (1985). Elastic structures in the back and their role in galloping in some mammals. Journal of Zoology 207, 467–482.
Alexander, R.M. & Jayes, A.S. (1983). A dynamic similarity hypothesis for the gaits of quadrupedal mammals. Journal of Zoology 201, 135–152.
Alexander, R.M. & Maloiy, G.M.O. (1984). Stride lengths and stride frequencies of primates. Journal of Zoology 202, 577–582.
Algeo, T.J., Scheckler, S.E. & Maynard, B.J. (2002). Effects of the middle to late devonian spread of vascular land plants on weathering regimes, marine biotas, and global climate. In Plants Invade the Land: Evolutionary and Environmental Perspectives: 213– 236. Gensel, P.G. & Edwards, D. (Eds). New York: Columbia University Press.
Altman, J. & Sudarshan, K. (1975). Postnatal development of locomotion in the laboratory rat. Animal Behaviour 23, 896–920.
Andrzejewski, R. & Wrocławek, H. (1961). Mass occurrence of Apodemus agrarius (Pallas, 1771) and variations in the number of associated Muridae. Acta Theriologica 5, 173– 184.
Argot, C. (2001). Functional-adaptive anatomy of the forelimb in the Didelphidae, and the paleobiology of the Paleocene marsupials Mayulestes ferox and Pucadelphys andinus. Journal of Morphology 247, 51–79.
ASAB/ABS. (2012). Guidelines for the treatment of animals in behavioural research and teaching. Animal Behaviour 83, 301–309.
Bajpai, S., Kay, R.F., Williams, B.A., Das, D.P., Kapur, V. V & Tiwari, B.N. (2008). The oldest Asian record of Anthropoidea. Proceedings of the National Academy of Sciences, USA 105, 11093–11098.
Balát, F. & Pelikán, J. (1959). On Apodemus flavicollis (Melch.) occupying nest boxes for birds. Zoologické Listy 3, 257–287.
Beard, K.C. (1993). Origin and evolution of gliding in early Cenozoic Dermoptera (Mammalia, Primatomorpha). In Primates and Their Relatives in Phylogenetic Perspective: 63–90. MacPhee, R.D.E. (Ed). Boston, MA: Springer US.
Beck, C.B. (1960). The identity of Archaeopteris and Callixylon. Brittonia 12, 351–368.
Belsky, A.J. (1994). Influences of trees on savanna productivity: Tests of shade, nutrients, and tree-grass competition. Ecology 75, 922–932.
Bence, S.L., Stander, K. & Griffiths, M. (2003). Habitat characteristics of harvest mouse nests on arable farmland. Agriculture, Ecosystems & Environment 99, 179–186.
Bennici, A. (2008). Origin and early evolution of land plants: Problems and considerations. Communicative & Integrative Biology 1, 212–218.
Bensley, A.B. (1901). On the question of an arboreal ancestry of the Marsupialia, and the interrelationships of the mammalian subclasses. The American Naturalist 35, 117– 138.
Berkum, F.H. Van, Huey, R.B., Tsuji, J.S. & Garland, T. (1989). Repeatability of individual differences in locomotor performance and body size during early ontogeny of the lizard Sceloporus occidentalis. Functional Ecology 3, 97–105.
Bertram, J.E.A. & Gutmann, A. (2009). Motions of the running horse and cheetah revisited: fundamental mechanics of the transverse and rotary gallop. Journal of the Royal Society Interface 6, 549–59.
Bi, S., Wang, Y., Guan, J., Sheng, X. & Meng, J. (2014). Three new Jurassic euharamiyidan species reinforce early divergence of mammals. Nature 514, 579–584.
Biewener, A.A. (1989a). Mammalian terrestrial locomotion and size. BioScience 39, 776– 783.
Biewener, A.A. (1989b). Scaling body support in mammals: limb posture and muscle mechanics. Science (New York, N.Y.) 245, 45–8.
Biewener, A.A. (1990). Biomechanics of mammalian terrestrial locomotion. Science (New York, N.Y.) 250, 1097–103.
Biewener, A.A. (2005). Animal Locomotion. Oxford: Oxford University Press.
Biknevicius, A.R., Reilly, S.M., McElroy, E.J. & Bennett, M.B. (2013). Symmetrical gaits and center of mass mechanics in small-bodied, primitive mammals. Zoology 116, 67–74.
Birn-Jeffery, A. V & Higham, T.E. (2014). The scaling of uphill and downhill locomotion in legged animals. Integrative and comparative biology 54, 1159–72.
Bloch, J.I. & Boyer, D.M. (2007). New skeletons of Paleocene-Eocene Plesiadapiformes: A diversity of arboreal positional behaviors in early primates. In Primate Origins: Adaptations and Evolution: 535–581. Ravosa, M.J. & Dagosto, M. (Eds). Springer US.
Bloch, J.I., Silcox, M.T., Boyer, D.M. & Sargis, E.J. (2007). New Paleocene skeletons and the relationship of plesiadapiforms to crown-clade primates. Proceedings of the National Academy of Sciences, USA 104, 1159–1164.
Böhme, W. (1978). Apodemus agrarius (Pallas, 1771) – Brandmaus. In Handbuch der Säugetiere Europas, Band I., Nagetiere 1: 368–381. Niethammer, J. & Krapp, F. (Eds). Wiesbaden: Akademische Verlagsgesellschaft.
Borowski, S. (1962). Apodemus flavicollis (Melchior, 1834) in the tops of tall trees. Acta Theriologica 6, 314–314.
Boyer, D.M., Prasad, G.V.R., Krause, D.W., Godinot, M., Goswami, A., Verma, O. & Flynn, J.J. (2010). New postcrania of Deccanolestes from the Late Cretaceous of India and their bearing on the evolutionary and biogeographic history of euarchontan mammals. Naturwissenschaften 97, 365–377.
Brown, D. (2009). Tracker Video Analysis and Modeling Tool.
Buesching, C.D., Newman, C., Twell, R. & Macdonald, D.W. (2008). Reasons for arboreality in wood mice Apodemus sylvaticus and bank voles Myodes glareolus. Mammalian Biology - Zeitschrift für Säugetierkunde 73, 318–324.
Butet, A. & Delettre, Y.R. (2011). Diet differentiation between European arvicoline and murine rodents. Acta Theriologica 56, 297–304.
Camargo, N.F., Ribeiro, J.F., Gurgel-Gonçalves, R., Palma, A.R.T., Mendonça, A.F. & Vieira, E.M. (2012). Is footprint shape a good predictor of arboreality in sigmondontine rodents from a neotropical savanna? Acta Theriologica 57, 261–267.
Camargo, N.F., Sano, N.Y., Ribeiro, J.F. & Vieira, E.M. (2016). Contrasting the realized and fundamental niche of the arboreal walking performance of neotropical rodents. Journal of Mammalogy 97, 155–166.
Cant, J.G.H. (1992). Positional behavior and body size of arboreal primates: A theoretical framework for field studies and an illustration of its application. American Journal of Physical Anthropology 88, 273–283.
Carrier, D.R. (1996). Ontogenetic limits on locomotor performance. Physiological Zoology 69, 467–488.
Carrizo, L. V, Tulli, M.J., Dos Santos, D.A. & Abdala, V. (2014). Interplay between postcranial morphology and locomotor types in Neotropical sigmodontine rodents. Journal of Anatomy 224, 469–81.
Cartmill, M. (1972). Arboreal adaptations and the origin of the order Primates. In The Functional and Evolutionary Biology of Primates: 3–35. Tuttle, R.H. (Ed). Chicago: Aldine-Atherton.
Cartmill, M. (1974a). Rethinking primate origins. Science 184, 436–443.
Cartmill, M. (1974b). Pads and claws in arboreal locomotion. In Primate Locomotion: 45– 83. Jenkins Jr, F.A. (Ed). New York: Academic Press.
Cartmill, M. (1985). Climbing. In Functional Vertebrate Morphology: 73–88. Hildebrand, M., Bramble, D.M., Liem, K.F. & Wake, D.B. (Eds). Cambridge, MA: Belknap Press.
Cartmill, M. (1992). New views on primate origins. Evolutionary Anthropology: Issues, News, and Reviews 1, 105–111.
Cartmill, M., Lemelin, P. & Schmitt, D. (2002). Support polygons and symmetrical gaits in mammals. Zoological Journal of the Linnean Society 136, 401–420.
Cartmill, M., Lemelin, P. & Schmitt, D. (2007). Primate gaits and primate origins. In Primate Origins: Adaptations and Evolution: 403–435. Ravosa, M. & Dagosto, M. (Eds). New York: Springer.
Cartmill, M. & Milton, K. (1977a). The lorisiform wrist joint and the evolution of “brachiating” adaptations in the Hominoidea. American Journal of Physical Anthropology 47, 249–272.
Cartmill, M. & Milton, K. (1977b). The lorisiform wrist joint and the evolution of “brachiating” adaptations in the hominoidea. American Journal of Physical Anthropology 47, 249–272.
Chełkowska, H., Walkowa, W. & Adamczyk, K. (1985). Spatial relationships in sympatric populations of the rodents: Clethrionomys glareolus, Microtus agrestis and Apodemus agrarius. Acta Theriologica 30, 51–78.
Chen, M. & Wilson, G.P. (2015). A multivariate approach to infer locomotor modes in Mesozoic mammals. Paleobiology 41, 280–312.
Chester, S.G.B., Sargis, E.J., Szalay, F.S., Archibald, J.D. & Averianov, A.O. (2010). Mammalian distal humeri from the Late Cretaceous of Uzbekistan. Acta Palaeontologica Polonica 55, 199–211.
Chester, S.G.B., Sargis, E.J., Szalay, F.S., Archibald, J.D. & Averianov, A.O. (2012). Therian femora from the Late Cretaceous of Uzbekistan. Acta Palaeontologica Polonica 57, 53–64.
Churchfield, S. (1990). The Natural History of Shrews. Bromley: Christopher Helm (Publishers) Ltd.
Corbet, G.B. & Ovenden, D. (1980). Mammals of Britain and Europe. London: Wm Collins Sons & Co Ltd.
Czeszczewik, D.C., Walankiewicz, W.W. & Stańska, M.S. (2008). Small mammals in nests of cavity-nesting birds: Why should ornithologists study rodents? Canadian Journal of Zoology 86, 286–293.
Dagosto, M. (1988). Implications of postcranial evidence for the origin of euprimates. Journal of Human Evolution 17, 35–56.
Dagosto, M. (2007). The postcranial morphotype of Primates. In Primate Origins: Adaptations and Evolution: 489–534. Ravosa, M. & Dagosto, M. (Eds). New York: Springer.
Dean, W.R.J., Milton, S.J. & Jeltsch, F. (1999). Large trees, fertile islands, and birds in arid savanna. Journal of Arid Environments 41, 61–78.
Delany, M.J. (1972). The ecology of small rodents in tropical Africa. Mammal Review 2, 1– 42.
Delciellos, A.C. & Vieira, M.V. (2006). Arboreal walking performance in seven didelphid marsupials as an aspect of their fundamental niche. Austral Ecology 31, 449–457.
Delciellos, A.C. & Vieira, M.V. (2007). Stride lengths and frequencies of arboreal walking in seven species of didelphid marsupials. Acta Theriologica 52, 101–111.
Demes, B., Jungers, W.L. & Nieschalk, U. (1990). Size- and speed- related aspects of quadrupedal walking in slender and slow lorises. In Gravidity, Posture and Locomotion in Primates: 175–198. Jouffroy, F.K., Stack, M.H. & Niemitz, C. (Eds). Florence: Il Sedicesimo.
Demes, B., Larson, S.G., Stern Jr, J.T., Jungers, W.L., Biknevicius, A.R. & Schmitt, D. (1994). The kinetics of primate quadrupedalism: “hindlimb drive” reconsidered. Journal of Human Evolution 26, 353–374.
Dickman, C.R. & Doncaster, C.P. (2009). Responses of small mammals to Red fox ( Vulpes vulpes ) odour. Journal of Zoology 204, 521–531.
Donovan, E.R. & Gleeson, T.T. (2008). Scaling the duration of activity relative to body mass results in similar locomotor performance and metabolic costs in lizards. Journal of Experimental Biology 211, 3258–3265.
Dor, M. (1937). La Morphologie de la Queue des Mammifères. Paris: Pierre Andre.
Doran, D.M. (1997). Ontogeny of locomotion in mountain gorillas and chimpanzees. Journal of Human Evolution 32, 323–344.
Driese, S.G. & Mora, C.I. (2002). Diversification of siluro-devonian plant traces in paleosols and influence on estimates of paleoatmospheric CO2 levels. In Plants Invade the Land: Evolutionary and Environmental Perspectives: 237–253. Gensel, P.G. & Edwards, D. (Eds). New York: Columbia University Press.
Dzulhelmi, M.N. & Abdullah, M.T. (2009). An ethogram construction for the Malayan Flying Lemur ( Galeopterus variegatus ) in Bako National Park, Sarawak, Malaysia. Joural of Tropical Biology and Conservation 5, 31–42.
Earl, Z. & Nel, J.A.J. (1976). Climbing behavior in three African rodent species. Zoologica Africana 11, 183–192.
Eilam, D. (1997). Postnatal development of body architecture and gait in several rodent species. Journal of Experimental Biology 200, 1339–1350.
Emmons, L.H. (2000). Tupai: A field study of Bornean treeshrews. Berkeley, California: University of California Press.
Emmons, L.H. & Gentry, A.H. (1983). Tropical forest structure and the distribution of gliding and prehensile-tailed vertebrates. The American Naturalist 121, 513–524.
Essner, R.L. (2003). Locomotion, morphology, and habitat use in arboreal squirrels (Rodentia: Sciuridae).
Fabre, A.-C., Cornette, R., Perrard, A., Boyer, D.M., Prasad, G.V.R., Hooker, J.J. & Goswami, A. (2014). A three-dimensional morphometric analysis of the locomotory ecology of Deccanolestes, a eutherian mammal from the Late Cretaceous of India. Journal of Vertebrate Paleontology 34, 146–156.
Farley, C.T. & Taylor, C.R. (1991). A mechanical trigger for the trot-gallop transition in horses. Science 253, 306–8.
Fischer, M.S. (1994). Crouched posture and high fulcrum, a principle in the locomotion of small mammals: The example of the rock hyrax ( Procavia capensis ) (Mammalia: Hyracoidea). Journal of Human Evolution 26, 501–524.
Fischer, M.S., Schilling, N., Schmidt, M., Haarhaus, D. & Witte, H. (2002). Basic limb kinematics of small therian mammals. Journal of Experimental Biology 205, 1315– 1338.
Flaherty, E. a, Ben-David, M. & Smith, W.P. (2010). Quadrupedal locomotor performance in two species of arboreal squirrels: predicting energy savings of gliding. Journal of comparative physiology. B, Biochemical, systemic, and environmental physiology 180, 1067–1078.
Fleagle, J.G. (1985). Size and adaptation in primates. In Size and Scaling in Primate Biology: 1–19. Jungers, W.L. (Ed). New York: Plenum.
Fleagle, J.G. & Mittermeier, R.A. (1980). Locomotor behavior, body size, and comparative ecology of seven Surinam monkeys. American Journal of Physical Anthropology 52, 301–314.
Fröbisch, J. & Reisz, R.R. (2009). The Late Permian herbivore Suminia and the early evolution of arboreality in terrestrial vertebrate ecosystems. Proceedings of the Royal Society of London B: Biological Sciences 276, 3611–3618.
Gaetano, L.C. & Rougier, G.W. (2011). New materials of Argentoconodon fariasorum (Mammaliaformes, Triconodontidae) from the Jurassic of Argentina and its bearing on triconodont phylogeny. Journal of Vertebrate Paleontology 31, 829–843.
Galetti, M., Rodarte, R.R., Neves, C.L., Moreira, M. & Costa-Pereira, R. (2016). Trophic niche differentiation in rodents and marsupials revealed by stable isotopes. PLOS ONE 11, e0152494.
Garland, T. (1983). The relation between maximal running speed and body mass in terrestrial mammals. Journal of Zoology 199, 157–170.
Gasc, J.-P. (2001). Comparative aspects of gait, scaling and mechanics in mammals. Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology 131, 121–133.
Gebo, D.L. (2004). A shrew-sized origin for Primates. Primates 62, 40–62.
Gebo, D.L., Dagosto, M., Beard, K.C. & Qi, T. (2000). The smallest primates. Journal of Human Evolution 38, 585–594.
Gilbert, C.C. (2004). Dietary ecospace and the diversity of euprimates during the Early and Middle Eocene. American Journal of Physical Anthropology 126, 237–249.
Gingerich, P.D., Dashzeveg, D. & Russell, D.E. (1991). Dentition and systematic relationships of Altanius orlovi (Mammalia, Primates) from the early Eocene of Mongolia. Geobios 24, 637–646.
Gliwicz, J. (1981). Competitive interactions within a forest rodent community in central Poland. Oikos 37, 353–362.
Goldingay, R.L. & Kavanagh, R.P. (1995). Foraging behaviour and habitat use of the feathertail glider (Acrobates pygmaeus) at Waratah Creek, New South Wales. Wildlife Research 22, 457–469.
Goodenberger, K.E., Boyer, D.M., Orr, C.M., Jacobs, R.L., Femiani, J.C. & Patel, B.A. (2015). Functional morphology of the hallucal metatarsal with implications for inferring grasping ability in extinct primates. American Journal of Physical Anthropology 156, 327–348.
Goswami, A., Prasad, G.V.R., Upchurch, P., Boyer, D.M., Seiffert, E.R., Verma, O., Gheerbrant, E. & Flynn, J.J. (2011). A radiation of arboreal basal eutherian mammals beginning in the Late Cretaceous of India. Proceedings of the National Academy of Sciences, USA 108, 16333–16338.
De Graaff, G. (1978). Notes on the Southern African black-tailed tree rat Thallomys paedulcus (Sundevall, 1846) and its occurrence in the Kalahari Gemsbok National Park. Koedoe 21, 181–190.
Grand, T.I. (1972). A mechanical interpretation of terminal branch feeding. Journal of Mammalogy 53, 198–201.
Grand, T.I. (1984). Motion economy within the canopy: Four strategies for mobility. In Adaptations for Foraging in Nonhuman Primates: 54–72. Rodman, P.S. & Cant, J.G.H. (Eds). New York: Columbia University Press.
Gray, J. (1944). Studies in the mechanics of the tetrapod skeleton. Journal of Experimental Biology 20, 88–116.
Gurnell, J. (1985). Woodland rodent communities. Symposium of the Zoological Society of London 55, 337–411.
Haffner, M. (1996). A tendon-locking mechanism in two climbing rodents, Muscardinus avellanarius and Micromys minutus. Journal of Morphology 227, 219–227.
Haffner, M. (1998). A comparison of the gross morphology and micro-anatomy of the foot pads in two fossorial and two climbing rodents (Mammalia). Journal of Zoology 244, 287–294.
Haines, R.W. (1958). Arboreal or terrestrial ancestry of placental mammals. The Quarterly Review of Biology 33, 1–23.
Hamrick, M.W. (2001). Primate origins: evolutionary change in digital ray patterning and segmentation. Journal of Human Evolution 40, 339–351.
Hanna, J.B. (2006). Kinematics of vertical climbing in lorises and Cheirogaleus medius. Journal of Human Evolution 50, 469–478.
Hanna, J.B. & Schmitt, D. (2011a). Interpreting the role of climbing in primate locomotor evolution: Are the biomechanics of climbing influenced by habitual substrate use and anatomy? International Journal of Primatology 32, 430–444.
Hanna, J.B. & Schmitt, D. (2011b). Locomotor energetics in primates: gait mechanics and their relationship to the energetics of vertical and horizontal locomotion. American Journal of Physical Anthropology 145, 43–54.
Harrell, F.E. (2001). Regression Modeling Strategies: With Applications to Linear Models, Logistic Regression, and Survival Analysis. New York: Springer-Verlag.
Harris, S. (1970). The Secret Life of the Harvest Mouse. London: Hamlyn.
Harris, S. (1979). History, distribution, status and habitat requirements of the Harvest mouse ( Micromys minutus ) in Britain. Mammal Review 9, 159–171.
Heglund, N.C. & Taylor, C.R. (1988). Speed, stride frequency and energy cost per stride: how do they change with body size and gait? Journal of Experimental Biology 138, 301–318.
Heglund, N.C., Taylor, C.R. & McMahon, T.A. (1974). Scaling stride frequency and gait to animal size: Mice to horses. Science 186, 1112–1113.
Heroldova, M. (1994). Diet of four rodent species from Robinia pseudo-acacia stands in South Moravia. Acta Theriologica 39, 333–337.
Hildebrand, M. (1967). Symmetrical gaits of primates. American Journal of Physical Anthropology 26, 119–130.
Hildebrand, M. (1968). Symmetrical gaits of dogs in relation to body build. Journal of Morphology 124, 353–359.
Hildebrand, M. (1976). Analysis of tetrapod gaits: general considerations and symmetrical gaits. In Neural control of locomotion: 203–236. Herman, R.M., Grillner, S., Stein, P.S.G. & Stuart, D.G. (Eds). New York: Plenum Press.
Hildebrand, M. (1977). Analysis of asymmetrical gaits. Journal of Mammalogy 58, 131– 156.
Hildebrand, M. (1985). Walking and running. In Functional Vertebrate Morphology: 38– 57. Hildebrand, M., Bramble, D.M., Liem, K.F. & Wake, D.B. (Eds). Cambridge, MA and London, England: Harvard University Press.
Hildebrand, M. (1995). Analysis of Vertebrate Structure. 4th edn. New York: John Wiley & Sons, Inc.
Hill, A. V. (1950). The dimensions of animals and their muscular dynamics. Science progress 38, 209–230.
Hirasaki, E., Kumakura, H. & Matano, S. (2000). Biomechanical analysis of vertical climbing in the spider monkey and the Japanese macaque. American Journal of Physical Anthropology 113, 455–472.
Hof, A.L. (1996). Scaling gait data to body size. Gait & Posture 4, 222–223.
Holisova, V. (1967). The food of Apodemus agrarius (Pall.). Zoologické Listy 16, 1–14.
Holisova, V. (1969). Vertical movements of some small mammals in a forest. Zoologické Listy 18, 121–141.
Howe, H.F. & Smallwood, J. (1982). Ecology of seed dispersal. Annual Review of Ecology and Systematics 13, 201–228.
Hoyt, D.F. & Taylor, C.R. (1981). Gait and the energetics of locomotion in horses. Nature 292, 239–240.
Hoyt, D.F., Wickler, S.J. & Cogger, E.A. (2000). Time of contact and step length: the effect of limb length, running speed, load carrying and incline. Journal of Experimental Biology 203, 221–227.
Hu, Y. & Wang, Y. (2002). Sinobaatar gen. nov.: First multituberculate from the Jehol Biota of Liaoning, Northeast China. Chinese Science Bulletin 47, 933.
Hu, Y., Wang, Y., Luo, Z. & Li, C. (1997). A new symmetrodont mammal from China and its implications for mammalian evolution. Nature 390, 137–142.
Hunt, K.D. (1991). Positional behavior in the Hominoidea. International Journal of Primatology 12, 95–118.
Hurum, J.H. & Kielan-Jaworowska, Z. (2008). Postcranial skeleton of a Cretaceous multituberculate mammal Catopsbaatar. Acta Palaeontologica Polonica 53, 545–566.
Iriarte-Díaz, J. (2002). Differential scaling of locomotor performance in small and large terrestrial mammals. The Journal of Experimental Biology 205, 2897–908.
Irschick, D.J. (2000). Effects of behaviour and ontogeny on the locomotor performance of a West Indian lizard, Anolis lineatopus. Functional Ecology 14, 438–444.
Ishiwaka, R. & Mori, T. (1999). Early development of climbing skills in harvest mice. Animal Behaviour 58, 203–209.
Ivakhnenko, M.F. (1994). A new Late Permian dromasaurian (Anomodontia) from Eastern Europe. Paleontological Journal 28, 96–103.
Jackson, S.M. & Thorington, R.W. (2012). Gliding Mammals: Taxonomy of Living and Extinct Species. Smithsonian Contributions to Zoology 1–117.
Jędrzejewska, B. & Jędrzejewski, W. (1990). Antipredatory behaviour of bank voles and prey choice of weasels - enclosure experiments. Annales Zoologici Fennici.
Jędrzejewski, W., Rychlik, L. & Jędrzejewska, B. (1993). Responses of bank voles to odours of seven species of predators: experimental data and their relevance to natural predator-vole relationships. Oikos 68, 251.
Jenkins, F.A. (1974). Tree shrew locomotion and the origins of primate arborealism. In Primate Locomotion: 85–116. Jenkins Jr, F.A. (Ed). New York: Academic.
Jenkins, F.A. & McClearn, D. (1984). Mechanisms of hind foot reversal in climbing mammals. Journal of Morphology 182, 197–219.
Ji, Q., Luo, Z.-X., Yuan, C.-X., Wible, J.R., Zhang, J.-P. & Georgi, J.A. (2002). The earliest known eutherian mammal. Nature 416, 816–822.
Johnson, L. (2012). Biomechanics of Vertical Clinging and Grasping in Primates. Duke University, Durham NC, USA.
Jones, F.W. (1953). Some readaptations of the mammalian pes in response to arboreal habits. Proceedings of the Zoological Society of London 123, 33–41.
Juškaitis, R. (2002). Spatial distribution of the yellow-necked mouse ( Apodemus flavicollis ) in large forest areas and its relation with seed crop of forest trees. Mammalian Biology - Zeitschrift für Säugetierkunde 67, 206–211.
Juškaitis, R. (2008). The Common Dormouse Muscardinus avellanarius : Ecology, Population Structure and Dynamics. Vilnius: Institute of Ecology of Vilnius University Publishers.
Juškaitis, R. & Šiožinyte, V. (2008). Habitat requirements of the common dormouse ( Muscardinus avellanarius ) and the fat dormouse ( Glis glis ) in mature mixed forest in Lithuania. Ekológia 27, 143–151.
Kalos, M.H. & Whitlock, P.A. (2009). Monte Carlo Methods. New York: Wiley-Verlag.
Karantanis, N.-E., Rychlik, L., Herrel, A. & Youlatos, D. (2017a). Arboreal gaits in three sympatric rodents Apodemus agrarius, Apodemus flavicollis (Rodentia, Muridae) and Myodes glareolus (Rodentia, Cricetidae). Mammalian Biology - Zeitschrift für Säugetierkunde 83, 51–63.
Karantanis, N.-E., Rychlik, L., Herrel, A. & Youlatos, D. (2017b). Vertical locomotion in Micromys minutus (Rodentia: Muridae): insights into the evolution of eutherian climbing. Journal of Mammalian Evolution.
Karantanis, N.-E., Youlatos, D. & Rychlik, L. (2015). Diagonal gaits in the feathertail glider Acrobates pygmaeus (Acrobatidae, Diprotodontia): Insights for the evolution of primate quadrupedalism. Journal of Human Evolution 86, 43–54.
Karaseva, E. V, Tichonova, G.N. & Bogomilov, P.L. (1992). Distribution of the Striped field mouse ( Apodemus agrarius ) and peculiarities of its ecology in different parts of its range. Zoologicheskii Zhurnal 71, 106–115.
Kemp, T.S. (2005). The Origin and Evolution of Mammals. 1st edn. Oxford: Oxford University Press.
Kielan-Jaworowska, Z. (2013). In Pursuit of Early Mammals. Life of the Past. Bloomington: Indiana University Press.
Kimura, T., Okada, M. & Ishida, H. (1979). Kinesiological characteristics of primate walking: Its significance in human walking. In Environment, Behavior and Morphology: Dynamic Interactions in Primates: 297–311. Morbeck, M.E. & Preuschoft, H. (Eds). New York: Gustav Fisher.
Kingdon, J. (1984). East African Mammals: An Atlas of Evolution in Africa. Chicago: University of Chicago Press.
Kingston, A.K., Boyer, D.M., Patel, B.A., Larson, S.G. & Stern Jr, J.T. (2010). Hallucal grasping in Nycticebus coucang: further implications for the functional significance of a large peroneal process. Journal of Human Evolution 58, 33–42.
Kirk, E.C., Lemelin, P., Hamrick, M.W., Boyer, D.M. & Bloch, J.I. (2008). Intrinsic hand proportions of euarchontans and other mammals: implications for the locomotor behavior of plesiadapiforms. Journal of Human Evolution 55, 278–299.
Kram, R. & Taylor, C.R. (1990). Energetics of running: a new perspective. Nature 346, 265– 267.
Krattli, H. (2001). Struktur und funktion des extremitäteninteguments bei einheimischen mäuseartigen (Muridae, Rodentia). PhD Dissertation, University of Zurich.
Kryštufek, B. (2010). Glis glis (Rodentia: Gliridae). Mammalian Species 42, 195–206.
Kuncová, P. & Frynta, D. (2009). Interspecific morphometric variation in the postcranial skeleton in the genus Apodemus. Belgian Journal of Zoology 139, 133–146.
Kuroe, M., Ohori, S., Takatsuki, S. & Miyashita, T. (2007). Nest-site selection by the harvest mouse Micromys minutus in seasonally changing environments. Acta Theriologica 52, 355–360.
Lammers, A.R. (2007). Locomotor kinetics on sloped arboreal and terrestrial substrates in a small quadrupedal mammal. Zoology 110, 93–103.
Lammers, A.R. & Biknevicius, A.R. (2004). The biodynamics of arboreal locomotion: the effects of substrate diameter on locomotor kinetics in the gray short-tailed opossum ( Monodelphis domestica ). The Journal of Experimental Biology 207, 4325–4336.
Lammers, A.R., Earls, K.D. & Biknevicius, A.R. (2006). Locomotor kinetics and kinematics on inclines and declines in the gray short-tailed opossum Monodelphis domestica. The Journal of Experimental Biology 209, 4154–4166.
Lammers, A.R. & Gauntner, T. (2008). Mechanics of torque generation during quadrupedal arboreal locomotion. Journal of Biomechanics 41, 2388–2395.
Lammers, A.R. & Zurcher, U. (2011a). Stability during arboreal locomotion. In Theoretical Biomechanics. Klika, V. (Ed). Available from: http://www.intechopen.com/books/theoretical-biomechanics/stability-duringarboreal-locomotion.
Lammers, A.R. & Zurcher, U. (2011b). Torque around the center of mass: dynamic stability during quadrupedal arboreal locomotion in the Siberian chipmunk ( Tamias sibiricus ). Zoology 114, 95–103.
Larson, S.G., Schmitt, D., Lemelin, P. & Hamrick, M. (2000). Uniqueness of primate forelimb posture during quadrupedal locomotion. American Journal of Physical Anthropology 112, 87–101.
Larson, S.G., Schmitt, D., Lemelin, P. & Hamrick, M. (2001). Limb excursion during quadrupedal walking: how do primates compare to other mammals? Journal of Zoology 255, 353–365.
Larson, S.G. & Stern, J.T. (2006). Maintenance of above-branch balance during primate arboreal quadrupedalism: Coordinated use of forearm rotators and tail motion. American Journal of Physical Anthropology 129, 71–81.
Leach, M. (1990). Mice of the British Isles. Aylesbury: Shire Publications Ltd.
Lee, D. V, Stakebake, E.F., Walter, R.M. & Carrier, D.R. (2004). Effects of mass distribution on the mechanics of level trotting in dogs. Journal of Experimental Biology 207, 1715– 1728.
Lemelin, P. (1995). Comparative and functional myology of the prehensile tail in new world monkeys. Journal of Morphology 224, 351–368.
Lemelin, P. (1999). Morphological correlates of substrate use in didelphid marsupials: implications for primate origins. Journal of Zoology 247, 165–175.
Lemelin, P. & Cartmill, M. (2010). The effect of substrate size on the locomotion and gait patterns of the kinkajou ( Potos flavus ). Journal of Experimental Zoology Part A: Comparative Experimental Biology 313A, 157–168.
Lemelin, P. & Schmitt, D. (2007). Origins of grasping and locomotor adaptations in Primates: Comparative and experimental approaches using an opossum model. In Primate Origins: Adaptations and Evolution: 329–380. Ravosa, M.J. & Dagosto, M. (Eds). Boston, MA: Springer US.
Lemelin, P., Schmitt, D. & Cartmill, M. (2003). Footfall patterns and interlimb coordination in opossums (Family Didelphidae): Evidence for the evolution of diagonal-sequence walking gaits in primates. Journal of Zoology 260, 423–429.
Lindenmayer, D. & Fischer, J. (2006). Habitat Fragmentation and Landscape Chang : An Ecological and Conservation Synthesis. Washington, D.C.: Island Press.
Linzey, A. V. & Kesner, M.H. (1997). Small mammals of a woodland-savannah ecosystem in Zimbabwe. I. Density and habitat occupancy patterns. Journal of Zoology 243, 137– 152.
Luo, Z.-X., Ji, Q., Wible, J.R. & Yuan, C.-X. (2003). An early Cretaceous tribosphenic mammal and Metatherian evolution. Science 302, 1934–1940.
Luo, Z.-X., Yuan, C.-X., Meng, Q.-J. & Ji, Q. (2011). A Jurassic eutherian mammal and divergence of marsupials and placentals. Nature 476, 442–445.
Marsh, A.C.W. & Harris, S. (2000). Partitioning of woodland habitat resources by two sympatric species of Apodemus: lessons for the conservation of the yellow-necked mouse ( A. flavicollis ) in Britain. Biological Conservation 92, 275–283.
Mazurkiewicz, M. (1994). Factors influencing the distribution of the bank vole in forest habitats. Acta Theriologica 39, 113–126.
McAdam, A.G. & Kramer, D.L. (1998). Vigilance as a benefit of intermittent locomotion in small mammals. Animal Behaviour 55, 109–117.
McClearn, D. (1992). Locomotion, posture, and feeding behavior of kinkajous, coatis, and raccoons. Journal of Mammalogy 73, 245–261.
McElroy, E.J., Hickey, K.L. & Reilly, S.M. (2008). The correlated evolution of biomechanics, gait and foraging mode in lizards. The Journal of Experimental Biology 211, 1029–40.
Meldrum, D.J. (1998). Tail-assisted hind limb suspension as a transitional behavior in the evolution of the platyrrhine prehensile tail. In Primate Locomotion: Recent Advances: 145–156. Strasser, E., Fleagle, J.G., Rosenberger, A.L. & McHenry, H.M. (Eds). Boston, MA: Springer US.
Meldrum, D.J., Dagosto, M. & White, J. (1997). Hindlimb suspension and hind foot reversal in Varecia variegata and other arboreal mammals. American Journal of Physical Anthropology 103, 85–102.
Meng, J., Hu, Y., Wang, Y., Wang, X. & Li, C. (2006). A Mesozoic gliding mammal from northeastern China. Nature 444, 889–893.
Meng, Q.-J., Ji, Q., Zhang, Y.-G., Liu, D., Grossnickle, D.M. & Luo, Z. (2015). An arboreal docodont from the Jurassic and mammaliaform ecological diversification. Science 347, 764–768.
Mills, M. & Hes, L. (1997). The Complete Book of Southern African Mammals. Cape Town: Struik Book Distributors.
Monadjem, A.R.A. (1999). Geographic distribution patterns of small mammals in Swaziland in relation to abiotic factors and human land-use activity. Biodiversity and Conservation 8, 223–237.
Montgomery, W.I. (1978). Studies on the distributions of Apodemus sylvaticus (L.) and A. flavicollis (Melchior) in Britain. Mammal Review 8, 177–184.
Montgomery, W.I. (1980). The use of arboreal runways by the woodland rodents, Apodemus sylvaticus (L.), A. flavicollis (Melchior) and Clethrionomys glareolus (Schreber). Mammal Review 10, 189–195.
Montgomery, W.I. & Gurnell, J. (1985). The behaviour of Apodemus. Symposia of the Zoological Society of London 55, 89–115.
Murúa, R. & González, L.A. (1982). Microhabitat selection in two Chilean cricetid rodents. Oecologia 52, 12–15.
Nakano, Y. (2002). The effects of substratum inclination on locomotor patterns in primates. Zeitschrift für Morphologie und Anthropologie 83, 189–199.
Napier, J.R. (1961). Prehensility and opposability in the hands of primates. Symposia of the Zoological Society of London 5, 115–132.
Napier, J.R. (1967). Evolutionary aspects of primate locomotion. American Journal of Physical Anthropology 27, 333–341.
Nations, J.A. & Olson, L.E. (2015). Climbing behavior of northern red-backed voles ( Myodes rutilus ) and scansoriality in Myodes (Rodentia, Cricetidae). Journal of Mammalogy 96, 957–963.
Niemitz, C. (2002). Kinematics and ontogeny of locomotion in monkeys and human babies. Zeitschrift für Morphologie und Anthropologie 83, 383–400.
Nordvig, K., Reddersen, J. & Jensen, T.S. (2001). Small mammal exploitation of upper vegetation strata in non-forest, mixed farmland habitats. Mammalian Biology - Zeitschrift für Säugetierkunde 66, 129–134.
Nowak, R.M. (1999). Walker’s Mammals of the World. 6th edn. The Johns Hopkins University Press.
Nyakatura, J.A., Fischer, M.S. & Schmidt, M. (2008). Gait parameter adjustments of cottontop tamarins ( Saguinus oedipus, Callitrichidae) to locomotion on inclined arboreal substrates. American Journal of Physical Anthropology 135, 13–26.
Nyakatura, J.A. & Heymann, E.W. (2010). Effects of support size and orientation on symmetric gaits in free-ranging tamarins of Amazonian Peru: implications for the functional significance of primate gait sequence patterns. Journal of Human Evolution 58, 242–251.
Nyakatura, J.A., Klinge, A., Fischer, M.S. & Schmidt, M. (2007). Locomotion on sloped arboreal substrates: A comparison of gait parameters in cotton-top tamarins and an arboreal australodelphid marsupial. Journal of Morphology 268, 1112.
Obrtel, R. & Holisova, V. (1974). Trophic niches of Apodemus flavicollis and Clethrionomys glareolus in low-land forest. Acta Scientarum Naturalium Academiae Scientiarum Bohemicae Brno 8, 1–37.
Olson, L.E., Sargis, E.J. & Martin, R.D. (2004). Phylogenetic relationships among treeshrews (Scandentia): A review and critique of the morphological evidence. Journal of Mammalian Evolution 11, 49–71.
Olszewski, J.L. (1968). Role of uprooted trees in the movements of rodents in forests. Oikos 19, 99–104.
Organ, J.M. (2008). The functional anatomy of prehensile and nonprehensile tails of the Platyrrhini (Primates) and Procyonidae (Carnivora). Johns Hopkins University.
Orkin, J.D. & Pontzer, H. (2011). The Narrow Niche hypothesis: gray squirrels shed new light on primate origins. American Journal of Physical Anthropology 144, 617–624.
Özkan, B., Yigit, N. & Colak, E. (2003). A study on Micromys minitus (Pallas, 1771) (Mammalia: Rodentia) in Turkish Thrace. Turkish Journal of Zoology 27, 55–60.
Panyutina, A., Korzun, L. & Kuznetsov, A. (2015). Flight of Mammals: From Terrestrial Limbs to Wings. New York: Springer.
Peters, S.E. (1983). Postnatal development of gait behaviour and functional allometry in the domestic cat (Felis catus). Journal of Zoology 199, 461–486.
Pontzer, H. (2005). A new model predicting locomotor cost from limb length via force production. Journal of Experimental Biology 208, 1513–1524.
Pontzer, H. (2007a). Effective limb length and the scaling of locomotor cost in terrestrial animals. Journal of Experimental Biology 210, 1752–1761.
Pontzer, H. (2007b). Predicting the energy cost of terrestrial locomotion: a test of the LiMb model in humans and quadrupeds. Journal of Experimental Biology 210, 484–494.
Preuschoft, H. (2002). What does “arboreal locomotion” mean exactly and what are the relationships between “climbing”, environment and morphology? Zeitschrift für Morphologie und Anthropologie 83, 171–188.
Preuschoft, H., Witte, H. & Fischer, M.S. (1995). Locomotion in nocturnal prosimians. In Creatures of the Dark: 453–472. Alterman, L., Doyle, G. & Izard, M. (Eds). New York: Plenum Press.
Pridmore, P.A. (1994). Locomotion in Dromiciops australis (Marsupialia, Microbiotheriidae). Australian Journal of Zoology 42, 679–699.
Prost, J.H. (1965). The methodology of gait analysis and gaits of monkeys. American Journal of Physical Anthropology 23, 215–240.
Prost, J.H. & Sussman, R.W. (1969). Monkey locomotion on inclined surfaces. American Journal of Physical Anthropology 31, 53–58.
Pucek, Z. (1981). Keys to Vertebrates of Poland, Mammals. Warszawa: PWN - Polish Scientific Publishers.
Rasmussen, D.T. & Sussman, R.W. (1990). Primates and Possums. World 775–803.
Rasmussen, D.T. & Sussman, R.W. (2007). Parallelisms among primates and possums. In Primate Origins: Adaptations and Evolution: 775–803. Ravosa, M.J. & Dagosto, M. (Eds). New York: Springer.
Reed, D.N. (2003). Micromammals Paleoecology: Past and Present Relationships between African Small Mammals and Their Habitats. SUNY, New York.
Reghem, E., Byron, C., Bels, V. & Pouydebat, E. (2012). Hand posture in the grey mouse lemur during arboreal locomotion on narrow branches. Journal of Zoology 288, 76– 81.
Reilly, S.M., McElroy, E.J. & Biknevicius, A.R. (2007). Posture, gait and the ecological relevance of locomotor costs and energy-saving mechanisms in tetrapods. Zoology 110, 271–289.
Reynolds, T.R. (1985). Mechanics of increased support of weight by the hindlimbs in primates. American Journal of Physical Anthropology 67, 335–349.
Rollinson, J.M. & Martin, R.D. (1981). Comparative aspects of primate locomotion, with special reference to arboreal cercopithecines. Symposia of the Zoological Society of London 48, 377–427.
Rose, K.D. (2006). The Beginning of the Age of Mammals. Baltimore: Johns Hopkins University Press.
Rosenberg, H.I. & Rose, R. (1999). Volar adhesive pads of the feathertail glider, Acrobates pygmaeus (Marsupialia; Acrobatidae). Canadian Journal of Zoology 77, 233–248.
Rybczynski, N. (2000). Cranial anatomy and phylogenetic position of Suminia getmanovi, a basal anomodont (Amniota: Therapsida) from the Late Permian of Eastern Europe. Zoological Journal of the Linnean Society 130, 329–373.
Samaras, A. & Youlatos, D. (2010). Use of forest canopy by European red squirrels Sciurus vulgaris in Northern Greece: Claws and the small branch niche. Acta Theriologica 55, 351–360.
Samuels, J.X. & Van Valkenburgh, B. (2008). Skeletal indicators of locomotor adaptations in living and extinct rodents. Journal of Morphology 269, 1387–1411.
Sargis, E.J. (2001). The grasping behaviour, locomotion and substrate use of the tree shrews Tupaia minor and T. tana (Mammalia, Scandentia). Journal of Zoology 253, 485–490.
Sargis, E.J. (2007). The postcranial morphology of Ptilocercus lowii (Scandentia, Tupaiidae) and its implications for Primate supraordinal relationships. In Primate Origins: Adaptations and Evolution: 51–82. Ravosa, M.J. & Dagosto, M. (Eds). Springer US.
Sargis, E.J., Boyer, D.M., Bloch, J.I. & Silcox, M.T. (2007). Evolution of pedal grasping in Primates.
Schilling, N. & Hackert, R. (2006). Sagittal spine movements of small therian mammals during asymmetrical gaits. The Journal of Experimental Biology 209, 3925–3939.
Schmidt, A. (2011). Functional differentiation of trailing and leading forelimbs during locomotion on the ground and on a horizontal branch in the European red squirrel (Sciurus vulgaris, Rodentia). Zoology 114, 155–164.
Schmidt, A. & Fischer, M.S. (2010). Arboreal locomotion in rats – the challenge of maintaining stability. Journal of Experimental Biology 213, 3615–3624.
Schmidt, A. & Fischer, M.S. (2011). The kinematic consequences of locomotion on sloped arboreal substrates in a generalized ( Rattus norvegicus ) and a specialized ( Sciurus vulgaris ) rodent. Journal of Experimental Biology 214, 2544–2559.
Schmidt, M. (2005). Hind limb proportions and kinematics: are small primates different from other small mammals? Journal of Experimental Biology 208, 3367–3383.
Schmidt, M. (2008). Forelimb proportions and kinematics: how are small primates different from other small mammals? Journal of Experimental Biology 211, 3775– 3789.
Schmitt, D. (2003a). Evolutionary implications of the unusual walking mechanics of the common marmoset ( C. jacchus ). American Journal of Physical Anthropology 122, 28– 37.
Schmitt, D. (2003b). Substrate size and primate forelimb mechanics : implications for understanding the evolution of primate locomotion. International Journal of Primatology 24, 1023–1036.
Schmitt, D., Cartmill, M., Griffin, T.M., Hanna, J.B. & Lemelin, P. (2006). Adaptive value of ambling gaits in primates and other mammals. Journal of Experimental Biology 209, 2042–2049.
Schmitt, D. & Lemelin, P. (2002). Origins of primate locomotion: Gait mechanics of the woolly opossum. American Journal of Physical Anthropology 118, 231–238.
Shapiro, L.J., Kemp, A.D. & Young, J.W. (2016). Effects of substrate size and orientation on quadrupedal gait kinematics in mouse lemurs ( Microcebus murinus ). Journal of Experimental Zoology Part A: Ecological Genetics and Physiology 325, 329–343.
Shapiro, L.J. & Raichlen, D.A. (2005). Lateral sequence walking in infant Papio cynocephalus: Implications for the evolution of diagonal sequence walking in primates. American Journal of Physical Anthropology 126, 205–213.
Shapiro, L.J. & Raichlen, D.A. (2006). Limb proportions and the ontogeny of quadrupedal walking in infant baboons (Papio cynocephalus). Journal of Zoology 269, 191–203.
Shapiro, L.J. & Raichlen, D.A. (2007). A response to Cartmill et al.: primate gaits and arboreal stability. American Journal of Physical Anthropology 133, 825–827.
Shapiro, L.J. & Young, J.W. (2010). Is primate-like quadrupedalism necessary for finebranch locomotion? A test using sugar gliders ( Petaurus breviceps ). Journal of Human Evolution 58, 309–319.
Shapiro, L.J. & Young, J.W. (2012). Kinematics of quadrupedal locomotion in sugar gliders ( Petaurus breviceps ): effects of age and substrate size. Journal of Experimental Biology 215, 4049–4049.
Shapiro, L.J., Young, J.W. & VandeBerg, J.L. (2014). Body size and the small branch niche: Using marsupial ontogeny to model primate locomotor evolution. Journal of Human Evolution 68, 14–31.
Shattuck, M.R. & Williams, S.A. (2010). Arboreality has allowed for the evolution of increased longevity in mammals. Proceedings of the National Academy of Sciences, USA 107, 4635–4639.
Simmons, N.B. (1995). Bat relationships and the origin of flight. In Ecology, Evolution and Behavior of Bats: 27–43. Racey, P.A. & Swift, S.M. (Eds). Symposium of the Zoological Society of London.
Skinner, J. & Chimimba, C. (2005). The Mammals of South Africa Subregion. Cambridge, UK: Cambridge University Press.
Smith, J.M. & Brown, R.L.W. (1986). Competition and body size. Theoretical Population Biology 30, 166–179.
Smith, J.M. & Smith, A.C. (2013). An investigation of ecological correlates with hand and foot morphology in callitrichid primates. American Journal of Physical Anthropology 152, 447–458.
Soligo, C. & Martin, R.D. (2006). Adaptive origins of primates revisited. Journal of Human Evolution 50, 414–430.
Soligo, C. & Müller, A.E. (1999). Nails and claws in primate evolution. Journal of Human Evolution 36, 97–114.
Stafford, B.J., Rosenberger, A.L. & Beck, B.B. (1994). Locomotion of free-ranging golden lion tamarins (Leontopithecus rosalia) at the National Zoological Park. Zoo Biology 13, 333–344.
Stalheim-Smith, A. (1989). Comparison of the muscle mechanics of the forelimb of three climbers. Journal of Morphology 202, 89–98.
Stein, W.E., Mannolini, F., Hernick, L.V., Landing, E. & Berry, C.M. (2007). Giant cladoxylopsid trees resolve the enigma of the Earth’s earliest forest stumps at Gilboa. Nature 446, 904–907.
Stevens, N.J. (2006). Stability, limb coordination and substrate type: the ecorelevance of gait sequence pattern in primates. Journal of Experimental Zoology Part A: Comparative Experimental Biology 305A, 953–963.
Stevens, N.J. (2008). The effect of branch diameter on primate gait sequence pattern. American Journal of Primatology 70, 356–362.
Storch, G. & Seiffert, C. (2007). Extraordinarily preserved specimen of the oldest known glirid from the middle Eocene of Messel (Rodentia). Journal of Vertebrate Paleontology 27, 189–194.
Strang, K.T. & Steudel, K. (1990). Explaining the scaling of transport costs: the role of stride frequency and stride length. Journal of Zoology 221, 343–358.
Surmacki, A., Gołdyn, B. & Tryjanowski, P. (2005). Location and habitat characteristics of the breeding nests of the harvest mouse ( Micromys minutus ) in the reed-beds of an intensively used farmland. Mammalia 69, 5–9.
Sussman, R.W. (1991). Primate origins and the evolution of angiosperms. American Journal of Primatology 23, 209–223.
Sustaita, D., Pouydebat, E., Manzano, A., Abdala, V., Hertel, F. & Herrel, A. (2013). Getting a grip on tetrapod grasping: form, function, and evolution. Biological Reviews 88, 380– 405.
Szalay, F.S. (1984). Arboreality: Is it homologous in Metatherian and Eutherian mammals? In Evolutionary Biology: 215–258. Hecht, M.K., Wallace, B. & Prance, G.T. (Eds). Springer US.
Szalay, F.S. (2007). Ancestral locomotor modes, placental mammals, and the origin of Euprimates: lessons from history. In Primate Origins: Adaptations and Evolution: 457–487. Ravosa, M.J. & Dagosto, M. (Eds). Boston, MA: Springer US.
Szalay, F.S. & Dagosto, M. (1980). Locomotor adaptations as reflected on the humerus of paleogene primates. Folia Primatologica 34, 1–45.
Szalay, F.S. & Dagosto, M. (1988). Evolution of hallucial grasping in the primates. Journal of Human Evolution 17, 1–33.
Szalay, F.S. & Sargis, E.J. (2006). Cretaceous Therian tarsals and the MetatherianEutherian dichotomy. Journal of Mammalian Evolution 13, 171–210.
Tattersall, F. & Whitbread, S. (1994). A trap-based comparison of the use of arboreal vegetation by populations of bank vole ( Clethrionomys glareolus ), woodmouse ( Apodemus sylvaticus ) and common dormouse ( Muscardinus avellanarius ). Journal of Zoology 233, 309–314.
Taylor, B.K. (1978). The anatomy of the forelimb in the anteater (Tamandua) and its functional implications. Journal of Morphology 157, 347–367.
Taylor, B.K. (1985). Functional anatomy of the forelimb in vermilinguas (anteaters). In The Evolution and Ecology of Armadillos, Sloths, and Vermilinguas: 151–162. Montgomer, G.G. (Ed). Washington, D.C.: Smithsonian Institution Press.
Taylor, M.E. (1989). Locomotor adaptation by carnivorans. In Carnivore Behavior, Ecology, and Evolution: 383–409. Gittleman, J.L. (Ed). New York: Cornell University Press.
Taylor, P. & Boitani, L. (2008). Thallomys paedulcus [WWW Document]. The IUCN Red List of Threatened Species 2008. URL http://dx.doi.org/10.2305/IUCN.UK.2008.RLTS.T21692A9309064.en
Thompson, D.W. (1910). A History of Animals. Oxford: Clarendon Press.
Thorington, R.W., Miller, A. & Anderson, C. (1998). Arboreality in tree squirrels (Sciuridae). In Ecology and Evolutionary Biology of Tree Squirrels: 119–130. Steele, M., Merritt, J. & Zegers, D. (Eds). Martinsville: VMNH.
Tomita, M. (1967). A study on the movement pattern of four limbs in walking [1]. Journal of Anthropological Society of Nippon 75, 120–146.
Trout, R.C. (1978a). A review of studies on captive Harvest mice ( Micromys minutus (Pallas)). Mammal Review 8, 159–175.
Trout, R.C. (1978b). A review of studies on populations of wild Harvest mice ( Micromys minutus (Pallas)). Mammal Review 8, 159–175.
Urbani, B. & Youlatos, D. (2013). Positional behavior and substrate use of Micromys minutus (Rodentia: Muridae): Insights for understanding primate origins. Journal of Human Evolution 64, 130–136.
Vázquez-Molinero, R., Martin, T., Fischer, M.S. & Frey, R. (2001). Comparative anatomical investigations of the postcranial skeleton of Henkelotherium guimarotae Krebs, 1991 (Eupantotheria, Mammalia) and their implications for its locomotion. Zoosystematics and Evolution 77, 207–216.
Vetaas, O.R. (1992). Micro-site effects of trees and shrubs in dry savannas. Journal of vegetation science 3, 337–344.
Vilensky, J.A., Gankiewicz, E. & Townsend, D.W. (1990). Effects of size on vervet (Cercopithecus aethiops) gait parameters: A longitudinal approach. American Journal of Physical Anthropology 81, 429–439.
Vilensky, J.A. & Larson, S.G. (1989). Primate locomotion: Utilization and control of symmetrical gaits. Annual Review of Anthropology 18, 17–35.
Vilensky, J.A., Moore, A.M. & Libii, J.N. (1994). Squirrel monkey locomotion on an inclined treadmill: implications for the evolution of gaits. Journal of Human Evolution 26, 375– 386.
Wagner, D.M., Feldhamer, G.A. & Newman, J.A. (2000). Microhabitat selection by golden mice (Ochrotomys nuttalli) at arboreal nest sites. The American Midland Naturalist 144, 220–225.
Ward, S.J. (1990). Life-history of the feathertail glider, Acrobates pygmaeus (Acrobatidae, Marsupialia) in South-Eastern Australia. Australian Journal of Zoology 38, 503–517.
Ward, S.J. & Woodside, D.P. (2008). Feathertail glider, Acrobates pygmaeus. In The Mammals of Australia: 261–264. Van Dyke, S. & Strahan, R. (Eds). Sydney, Australia: Reed New Holland.
Watts, C.H.S. (1968). The foods eaten by wood mice ( Apodemus sylvaticus ) and bank voles ( Clethrionomys glareolus ) in Wytham Woods, Berkshire. Journal of Animal Ecology 37, 25–41.
Wells, J.P. & Turnquist, J.E. (2001). Ontogeny of locomotion in rhesus macaques (Macaca mulatta): II. Postural and locomotor behavior and habitat use in a free-ranging colony. American Journal of Physical Anthropology 115, 80–94.
White, T.D. (1990). Gait selection in the brush-tail possum ( Trichosurus vulpecula ), the northern quoll ( Dasyurus hallucatus ), and the virginia opossum ( Didelphis virginiana ). Journal of Mammalogy 71, 79–84.
Wickler, S.J., Hoyt, D.F., Cogger, E.A. & Myers, G. (2003). The energetics of the trot-gallop transition. The Journal of Experimental Biology 206, 1557–64.
Williamson, T.E., Brusatte, S.L. & Wilson, G.P. (2014). The origin and early evolution of metatherian mammals: the Cretaceous record. ZooKeys 465, 1–76.
Witte, H., Preuschoft, H. & Fischer, M.S. (2002). The importance of the evolutionary heritage of locomotion on flat ground in small mammals for the development of arboreality. Zeitschrift für Morphologie und Anthropologie 83, 221–233.
Ylönen, H. (1990). Spatial avoidance between the bank vole Clethrionomys minutus and the harvest mouse Micromys minutus: an experimental study. Annales Zoologici Fennici 27, 313–320.
Youlatos, D. (1999a). The schizodactylous grasp of the howling monkey. Zeitschrift für Morphologie und Anthropologie 3, 187–198.
Youlatos, D. (1999b). Locomotor and postural behavior of Sciurus igniventris and Microsciurus flaviventer (Rodentia, Sciuridae) in eastern Ecuador. Mammalia 63, 405–416.
Youlatos, D. (2000). Functional anatomy of forelimb muscles in Guianan atelines (Platyrrhini : Primates). Annales Des Sciences Naturelles 21, 137–151.
Youlatos, D. (2003). Osteological correlates of tail prehensility in carnivorans. Journal of Zoology 259, 423–430.
Youlatos, D. (2008). Hallucal grasping behavior in Caluromys (Didelphimorphia: Didelphidae): Implications for primate pedal grasping. Journal of Human Evolution 55, 1096–1101.
Youlatos, D. (2010). Use of zygodactylous grasp by Caluromys philander (Didelphimorphia: Didelphidae). Mammalian Biology 75, 475–481.
Youlatos, D., Karantanis, N.E., Byron, C.D. & Panyutina, A. (2015). Pedal grasping in an arboreal rodent relates to above-branch behavior on slender substrates. Journal of Zoology 296, 239–248.
Youlatos, D., Karantanis, N.E. & Panyutina, A. (2016). Pedal grasping in the northern smooth-tailed treeshrew Dendrogale murina (Tupaiidae, Scandentia): insights for euarchontan pedal evolution. Mammalia.
Young, J.W. (2009). Substrate determines asymmetrical gait dynamics in marmosets ( Callithrix jacchus ) and squirrel monkeys ( Saimiri boliviensis ). American Journal of Physical Anthropology 138, 403–420.
Young, J.W. (2012). Gait selection and the ontogeny of quadrupedal walking in squirrel monkeys ( Saimiri boliviensis ). American Journal of Physical Anthropology 147, 580– 592.
Zefferer, M. (2002). Adaptation des terminalen zehengliedes an die fortbewegung bei kleinsaugern (Mammalia). Bachelor Thesis, Zoologisches Museum der Universitat Zurich.
Zejda, J. (1967). Habitat selection in Apodemus agrarius (Pallas, 1771) (Mammalia: Muridae) on the border of the area of its distribution. Zoologické Listy 16, 15–30.
Zheng, X., Bi, S., Wang, X. & Meng, J. (2013). A new arboreal haramiyid shows the diversity of crown mammals in the Jurassic period. Nature 500, 199–202.
The raw dataset underlying this dissertation is available at: https://figshare.com/s/4d496e3c0bc8eaac98f9