The physical properties of an animal’s environment have a strong influence on the energetic cost of movement; the energetic constraints of a landscape help drive the evolution of specialised morphology for a given species’ environment (Parker et al. 1984; Telfer and Kelsall 1979). For species endemic to locations with adverse climatic conditions, physiological demands (i.e., maintaining metabolic homeostasis and energetic balance) are high, and resources often limited; therefore, survival is strongly dependent on an optimal balance between energy acquisition and allocation (Tolkamp 2002). In the context of rapid climate change, some species are incurring heightened energetic costs, most notably amongst those species that inhabit polar regions where changes are particularly dramatic (LaPoint et al. 2020; Parmesan 2006; Pecl et al. 2017). For many vertebrates, the rapidity of environmental and climate change limits available responses to behavioural plasticity or dispersal to a habitat with a more suitable climate (Ignacio 2013; Parmesan 2006). Whilst large-scale poleward shifts in home range have been documented on all continents and major oceans in mammals, amphibians, insects, fish, and birds in response to warming (Crick 2004; Parmesan 2006), range-restricted species are ultimately constrained to the environmental change within their home ranges. These species tend to be particularly susceptible to climate change; therefore, a biomechanical understanding of how variation in the physical properties of a changing environment is linked to their energetic cost of locomotion can provide insight into how they may cope with change.
Locomotion is energetically expensive and is a major contributor to the energy budget of many animals (Cavagna et al. 1977; Zera and Harshman 2001). The physical properties of the landscape an animal traverses, as well as how an animal biomechanically interacts with these properties, can substantially influence the metabolic cost of terrestrial locomotion (Shaw 2020). The metabolic cost of locomotion rises concomitantly with substrate penetrability, as the animal requires more work to push into and deform the substrate (Shepherd et al. 2013). Importantly, an animal’s morphology can mitigate these effects. For example, many animals endemic to regions with high annual snow cover (and therefore greater variation in substrate penetrability) exhibit morphological adaptations, such as longer limbs (Telfer and Kelsall 1979) and increased foot surface area in ungulates (Telfer and Kelsall 1979), birds (Hohn 1977) and canids (Murray and Larivière 2002), that facilitate a reduced metabolic cost of locomotion in response to penetrable substrates (Parker et al. 1984). In fact, foot load is directly linked to geographical range, whereby animals at higher latitudes with high rates of annual snow cover often have increased body mass to foot area ratios (Parker et al. 1984). Snow is a complex medium with a range of structural properties, whereby snow density, depth, stiffness, and thickness, factors are continually changing due to interactions with environmental variables such as temperature, precipitation, and wind (Fierz et al. 2009). Because snow varies greatly in structural composition, it forms a component of the landscape that is continually changing in degree of penetrability. Therefore, snow condition has been shown to strongly affect the metabolic cost of terrestrial locomotion in ungulates (Parker et al. 1984; Telfer and Kelsall 1979; Fancy and White 1987) and canids (Crête and Larivière, 2003). The amount of force production required for locomotion in snow increases with snow depth, density, and compliance, due to the added costs associated with deforming a penetrable substrate.
Although the effect of changing snow properties on the energetics of locomotion has been well-documented in ungulates, there is a lack of understanding of this effect in terrestrial birds that regularly engage in ground locomotion. As the world’s northernmost resident bird that frequently relies on terrestrial locomotion over snow to feed, the Svalbard rock ptarmigan (Lagopus muta hyperborea) provides an ideal model for examining foot loading in the context of fluctuating snow properties. The Svalbard rock ptarmigan is a ground-dwelling, resident (non-migratory) bird endemic to the high-Arctic archipelago of Svalbard, their range restriction thus limiting them to immediate resources and environmental conditions and contributing in part to their susceptibility to climate change (Pedersen 2017). In response to substantial seasonal variation in environmental conditions (where winters deliver sub-zero average temperatures and a snowy, icy landscape contrasted against a bare, rocky summer landscape), Svalbard rock ptarmigan display significant seasonal variation in physiology, morphology and behaviour (i.e., Mortensen et al. 1985; Mortensen and Blix 1986; Pedersen 2005; Stokkan 1992). Notably, to cope with extreme winter conditions, Svalbard rock ptarmigan double their body mass through the deposition of fat stores, in parallel with the regrowth of more heavily feathered feet and thicker, wider claws (Stejneger 1884; Stokkan et al. 1986; Nord et al. 2023). Interestingly, Svalbard rock ptarmigan can carry their additional body mass for no increase in the metabolic cost of transport (Lees 2010), an adaptation not reported in any other avian species and only known to occur in a few mammalian species (Baudinette and Biewener 1998; Heglund 1995; Maloiy et al. 1986; Taylor 1980). The reduced cost of locomotion in winter despite added body mass is suggested to be in part a product of the greater feathered surface area of the Svalbard rock ptarmigan foot, and the subsequent expected lowering of their foot load (Lees et al. 2010). Notably, Hohn (1977) found that the feathered winter foot of willow (Lagopus lagopus) and rock (Lagopus muta) ptarmigan experience a reduced foot track depth of about 50% compared to a plucked foot. In combination with Lees et al. (2010), the results of Hohn (1977) suggests that the increases in foot surface area of a feathered winter foot may facilitate energy savings during terrestrial locomotion, functioning as an effective ‘snowshoe’.
While the presence of an effective snowshoe in the feathered Svalbard rock ptarmigan foot has been suggested to support winter locomotion in snow, the only published account of the effect of feathering on foot sink depth in snow did not include the Svalbard rock ptarmigan (Hohn 1977). Hohn (1977) compared feathered and plucked feet in two lower-latitude ptarmigan species to test for a difference in foot sink depth but did not further address how adaptive morphology performs under variation in snow hardness. Here, we test the relative performance of feathered winter feet of the Svalbard rock ptarmigan and Norwegian mainland rock and willow ptarmigan across varying snow properties (soft to stiff) to determine foot track depth (as a proxy for the energetic cost of locomotion). The cadaveric feet (extending from the tarsometatarsus to the foot) of three ptarmigan species were attached to a force rig, which pressed feet into the snow to measure displacement. We hypothesised that the Svalbard rock ptarmigan, with its denser foot feathering, would have lower foot track depth than the other ptarmigan species for equivalent reaction forces, and that this effect would be greater with increasing snow softness.