Arboreal environments impose strong physical constraints on vertebrate morphology and locomotor adaptations, due to the diversity of supports varying in orientation, diameter, and compliance. For arboreal mammals, the ability to navigate sloping and vertical trunks, branches, and lianas is essential, as these constitute the most available supports in trees. Climbing on vertical supports is a key aspect of arboreal locomotion in both fully arboreal and scansorial species, enabling access to the canopy from the ground, diverse food sources, enhanced vigilance, predator avoidance, and secure resting and nesting sites (Hildebrand, 1995). Climbing abilities in mammals date back to the Jurassic (Zheng et al., 2013; Bi et al., 2014; Meng et al., 2015) and have played a central role in the evolution of euarchontoglires, especially primates (Wood Jones, 1916; Cartmill, 1985; Hunt et al., 1996; Hirasaki et al., 2000; Isler, 2005; Hanna et al., 2008; Hanna et al., 2017; Karantanis et al., 2018; Nyakatura, 2019). Adaptations for climbing vertical supports have been identified in early Paleogene primates through postcranial fossil analyses (Dagosto, 2007; Gebo, 2011; Boyer et al., 2017; Yapuncich et al., 2019). Frequent vertical climbing may have been a prerequisite for the development of hallucal and pollical grasping in early primates (Szalay and Dagosto, 1988; Toussaint et al., 2020), and has been proposed as an alternative scenario to the hypothesis of cautious displacements on narrow branches of angiosperm tree peripheries (Bloch and Boyer, 2002; Cartmill, 1992; Sussman et al., 2013).

Several extant mammal species have been proposed as models for early primate arboreal adaptations, including small strepsirrhines (Toussaint et al., 2015; Shapiro et al., 2016), platyrrhines (Nyakatura, 2019; Toussaint et al., 2020; Kirk et al., 2008), treeshrews (Sargis, 2007), rodents (Urbani and Youlatos, 2013; Orkin and Pontzer, 2011; Byron et al., 2011), carnivorans (McClearn, 1992), and marsupials (Toussaint et al., 2020; Youlatos, 2008; Lemelin and Schmitt, 2007; Shapiro and Young, 2010; Shapiro et al., 2014; Youlatos et al., 2018). While not all arboreal mammals travel on narrow terminal branches, all rely on vertical supports to navigate canopy strata. However, few comparative studies have examined vertical climbing in non-primate arboreal mammals, and most have focused on ascents (Hanna et al., 2017; Preuschoft, 2002; Antunes et al., 2016; Clemente et al., 2019). Although behaviors, such as dropping, jumping, or gliding allow arboreal animals to move to lower tree layers, the ability to safely descend sloping and vertical supports remains critical, yet largely understudied (Birn-Jeffery and Higham, 2014).

Non-primate arboreal mammals often adopt a head-first posture when descending vertical supports, as reported in some rodents (Karantanis et al., 2018; Youlatos, 2011; Youlatos and Panyutina, 2014) and procyonid carnivorans (McClearn, 1992; Jenkins and McClearn, 1984). This strategy relies on reversed feet and functional claws that enable secure gripping of tree bark during descent. Head-first descent is also common in prehensile-tailed mammals, such as certain platyrrhine primates (Youlatos and Gase, 1994; Garber and Rehg, 1999; Lawler and Stamps, 2002) and the kinkajou (McClearn, 1992). In species lacking a prehensile tail, and in primates that lack claws and use their digits to wrap around supports, alternative descent strategies are required. In a study of nine small to medium-sized strepsirrhines, Perchalski, 2021 found that lemurs under 1 kg predominantly used head-first descents regardless of support properties, whereas larger species (>1 kg) increasingly adopted tail-first postures on supports angled at 45° or more, depending on species. Both head-first and tail-first strategies involve orthograde postures with the body aligned parallel to the support (Hunt et al., 1996). Perchalski also recorded other descent behaviors, including leaping, dropping, and asymmetrical descents that did not fit into strict head-first or tail-first categories. These findings suggest that in strepsirrhines, body mass and locomotor adaptations influence the choice of descent posture. However, such behavioral variation also highlights the need for broader comparative data across arboreal mammals to fully understand the functional and ecological significance of vertical descent strategies in an evolutionary context.

From a locomotor perspective, speed and duty factor (DF, the percentage of stride duration a limb remains in contact with the support) are key indicators of arboreal locomotor performance (Cartmill et al., 2007a). Studies across tetrapods have shown that animals generally move more slowly on narrow supports than on wider ones (Lammers and Stakes, 2025; Schmitt and Lemelin, 2002). Small primates (Shapiro et al., 2016; Hesse et al., 2015; Nyakatura et al., 2008), rodents (Karantanis et al., 2018; Karantanis et al., 2017; Wölfer et al., 2021), and marsupials (Shapiro et al., 2014; Lammers et al., 2006) typically decrease speed and increase duty factor, especially for the forelimbs, during descents compared to ascents on inclined supports and compared to locomotion on horizontal supports. These mechanisms supposedly help enhance stability by allowing more cautious displacements (Birn-Jeffery and Higham, 2014; Lammers and Stakes, 2025; Wölfer et al., 2021).

Gait patterns also reflect arboreal adaptations, particularly in primates (Preuschoft, 2002; Cartmill et al., 2007a; Vilensky and Larson, 1989; Hildebrand, 1967). Vertical climbing employs both symmetrical (walk, trot, run) and asymmetrical (bound, half-bound, gallop) gaits, similar to above-branch locomotion. Symmetrical gaits are defined as locomotor patterns in which the footfalls of a girdle (a pair of fore- or hindlimbs) are evenly spaced in time, with the right and left limbs of a pair of limbs being approximately 50% out of phase with each other (Hildebrand, 1967; Hildebrand, 1966). Symmetrical gaits can be further divided into two types: diagonal-sequence gaits, in which a hindlimb footfall is followed by that of the contralateral forelimb, and lateral-sequence gaits, in which a hindlimb footfall is followed by that of the ipsilateral forelimb (Hildebrand, 1967; Shapiro and Raichlen, 2005; Cartmill et al., 2007b). In contrast, asymmetrical gaits are characterized by unevenly spaced footfalls within a girdle, with the right and left limbs moving in near synchrony (Hildebrand, 1977). Asymmetrical gaits, often used by small mammals at high speeds (Lammers and Stakes, 2025; Dunham et al., 2020), allow for an increase in the distance traveled but often include an aerial phase (Hildebrand, 1977), raising support reaction forces and potentially causing oscillations or breakage on narrow horizontal or sloping branches, complicating locomotor control and safety. Benefits of asymmetrical gaits have thus been proposed to be related to both body mass and support diameter (Chadwell and Young, 2015). On vertical supports, such as trunks or lianas, these risks are reduced due to different force distributions and gravity orientation. Symmetrical gaits are widespread in primates and have been linked to the use of the fine branch niche, as enhanced grasping and hindlimb dominance supposedly increase stability during cautious locomotion on narrow horizontal or sloping supports (Hildebrand, 1967; Cartmill et al., 2007b; Cartmill et al., 2002; Lemelin and Cartmill, 2010). Notably, primates adjust their symmetrical gaits with support inclination, favoring diagonal-sequence gaits during ascents and lateral-sequence gaits during descents (Nyakatura et al., 2008; Granatosky et al., 2019; Nyakatura and Heymann, 2010; Prost and Sussman, 1969; Rollinson and Martin, 1981; Shapiro et al., 2025). Symmetrical gaits are also common in rodents (Karantanis et al., 2018; Karantanis et al., 2017), scandentians (Granatosky et al., 2022), carnivorans (McClearn, 1992), and marsupials (Cartmill et al., 2020; Lemelin et al., 2003; Gaschk et al., 2019; Karantanis et al., 2015). However, most kinematic studies have focused on horizontal or moderately sloped supports (~45°), rarely addressing vertical (~90°) supports or analyzing both symmetrical and asymmetrical gaits comprehensively. As a result, comparative data on how vertical supports of varying diameters affect descent and ascent kinematics remain limited, hindering our understanding of this common arboreal behavior.

In addition to body mass, limb proportions influence locomotor and postural strategies (Perchalski, 2021; Granatosky et al., 2019). The relative length of autopodials, particularly manual and pedal digits, is closely linked to grasping ability and thus affects locomotor performance in primates (Nyakatura, 2019; Toussaint et al., 2020; Cartmill, 1992; Kirk et al., 2008; Lemelin and Jungers, 2007) and small marsupials (Toussaint et al., 2020; Lemelin and Schmitt, 2007). Species with relatively short autopods may struggle to maintain a secure grip during vertical descent. Fore- and hindlimb length ratios have also been proposed as predictors of postural adaptation in vertical locomotion, with shorter forelimbs generating greater hindlimb traction during head-first descents (Preuschoft, 2002; Perchalski, 2021). Consequently, a lower intermembral index (forelimb-to-hindlimb length ratio) increases the risk of forward pitching when descending vertically head-first compared to tail-first (Perchalski, 2021).

Variation in weight distribution along the body, notably caused by head mass differences, may also influence postural strategies during vertical descent (i.e. head-first vs. tail-first). Primates exhibit the highest brain-to-body mass ratio among mammals (Boddy et al., 2012). This relative brain expansion, traced back to early primate evolution, is a key synapomorphy alongside a divergent hallux and pollex, nails replacing claws, elongated hindlimbs and autopods, and large convergent eyes (Cartmill, 1992; Szalay, 1968; Martin, 1990). However, the evolutionary sequence and interplay between locomotor and cognitive specializations remain unresolved, despite consensus on the small body size (Nyakatura, 2019; Dagosto et al., 2018) and arboreality (Upham et al., 2019; Hughes et al., 2021; Dunn et al., 2016) of primate ancestors. While brain enlargement likely increases relative head mass, its effects on arboreal locomotion have yet to be investigated in primates or other mammals. Given that head mass influences both the center of mass and moment of inertia, greater head mass may increase toppling risk during vertical head-first descent.

In this study, we aim to test (a) whether postural and kinematic adjustments during vertical descents versus ascents vary consistently across mammalian groups; (b) whether these strategies correlate with specific morphological parameters; and (c) whether such correlations can be used to infer descent postures in fossils, shedding light on the evolutionary history of vertical arboreal locomotion, particularly in primates. To address these questions, we analyzed locomotor sequences of descents and ascents on vertical supports in 21 small- to medium-sized arboreal mammal species, including taxa proposed as modern analogues of early primates. We first examined the effect of support diameter (small, medium, large) on postural strategies and kinematics (speed, duty factor, gait) during descents relative to ascents. We then assessed the relationships between descent strategies and morphological parameters (body mass, limb proportions, and relative head mass) for each species. These data allowed us to build a model incorporating seven significant morphological predictors, which we applied to infer vertical descent behavior in 13 extinct euarchontoglires, including adapiforms (early strepsirrhines), omomyiforms (early haplorhines), a sciuromorph (early rodent), and plesiadapiforms (stem primates).

We predict that:

(H1) Postural strategies: species under 1 kg and/or possessing a prehensile tail will exhibit head-first descent postures more frequently than larger species, which will favor tail-first postures (Perchalski, 2021).

(H2) Kinematic adjustments: animals will adopt more cautious locomotor patterns during vertical descents compared to ascents, characterized by reduced speed, increased duty factors, and a higher proportion of symmetrical gaits, particularly on narrow supports (Lammers and Stakes, 2025; Karantanis et al., 2017; Wölfer et al., 2021; Granatosky et al., 2019; Granatosky et al., 2022).

(H3) Morphological correlates: the intermembral index will positively correlate with the proportion of head-first descents, whereas relative autopod length and head size will correlate negatively with head-first descent frequency (Cartmill, 1992; Preuschoft, 2002; Perchalski, 2021).

(H4) Evolutionary implications: early euarchontoglires, due to their small size and generalized locomotor abilities, likely employed a high proportion of head-first descents (Karantanis et al., 2018; Wölfer et al., 2021), whereas early euprimates may have increasingly favored tail-first descents associated with larger body and brain, and elongated hindlimbs and autopods (Cartmill, 1992; Szalay, 1968; Martin, 1990).