Surviving winter on the Qinghai-Tibetan Plateau: Pikas suppress energy demands and exploit yak feces to survive winter

Abstract

The Qinghai-Tibetan Plateau, with low precipitation, low oxygen partial pressure, and temperatures routinely dropping below −30 °C in winter, presents several physiological challenges to its fauna. Yet it is home to many endemic mammalian species, including the plateau pika (Ochotona curzoniae). How these small animals that are incapable of hibernation survive the winter is an enigma. Measurements of daily energy expenditure (DEE) using the doubly labeled water method show that pikas suppress their DEE during winter. At the same body weight, pikas in winter expend 29.7% less than in summer, despite ambient temperatures being approximately 25 °C lower. Combined with resting metabolic rates (RMRs), this gives them an exceptionally low metabolic scope in winter (DEE/RMRt = 1.60 ± 0.30; RMRt is resting metabolic rate at thermoneutrality). Using implanted body temperature loggers and filming in the wild, we show that this is achieved by reducing body temperature and physical activity. Thyroid hormone (T3 and T4) measurements indicate this metabolic suppression is probably mediated via the thyroid axis. Winter activity was lower at sites where domestic yak (Bos grunniens) densities were higher. Pikas supplement their food intake at these sites by eating yak feces, demonstrated by direct observation, identification of yak DNA in pika stomach contents, and greater convergence in the yak/pika microbiotas in winter. This interspecific coprophagy allows pikas to thrive where yak are abundant and partially explains why pika densities are higher where domestic yak, their supposed direct competitors for food, are more abundant.

Differential Expression of Metabolism-Related Genes in Plateau Pika (Ochotona curzoniae) at Different Altitudes on the Qinghai–Tibet Plateau

“…It inhabits the alpine regions at an altitude of 3,100–5,300 m above sea level and is well adapted to extreme hypoxia, cold, and food deprived environments ( Cao et al, 2017 ). In this scenario, plateau animals including plateau pika face severe energetic challenges to maintain their core body temperature ( Van Sant and Hammond, 2008 ; Zhang et al, 2012 ; Speakman et al, 2021 ). Previous studies have found that at different altitudes, the life history strategies and personalities of plateau pika varied significantly ( Liu et al, 2012 ; Qu et al, 2013 ; Qu et al, 2019 ; Tan et al, 2020 ), accompanied by differences in fat accumulation and metabolic rate ( Yang et al, 2006 ).…”

Sympatric Yaks and Plateau Pikas Promote Microbial Diversity and Similarity by the Mutual Utilization of Gut Microbiota

“…It is possible that horizontal transmission significantly increases microbial diversity [ 44 ] and that the host acquires gut microbiota from other species to maintain a significantly greater species richness and biodiversity than non-gut environments [ 45 , 46 ]. Moreover, pikas eat the feces of yaks [ 24 , 47 ], which could increase the gut microbial diversity of pikas that live with yaks. Likewise, the soil-ingestion behavior of yaks may increase their gut microbial diversity when they live with pikas, as pikas excrete hard solid fecal pellets throughout the field [ 3 , 48 ].…”

“…Alternatively, another interpretation is that the stronger tolerance to toxic plant secondary metabolites (PSMs) of plateau pikas, compared with that of other herbivores, results in its outbreak in degraded regions, which are widely colonized by poisonous plants [ 21 , 22 , 23 ]. However, we have found that plateau pikas survive in winter by eating yak feces when food is short, and horizontal transmission of gut microbiota occurred during this process [ 24 ]; these scenes made us question if pikas eat yak feces in summer, or if horizontal transmission of gut microbiota also occurred in summer.…”

Analysis of the Impacts of Environmental Factors on Rat Hole Density in the Northern Slope of the Tienshan Mountains with Satellite Remote Sensing Data

“…However, compared with NTXJ, throughout other alpine meadows, or grassland areas in the world [51][52][53], longer grazing durations may indeed have a more significant impact on the population density of rodents. In addition, in alpine meadows, small rodents such as pika may spend the winter by eating yak feces [54], so the population density and grazing intensity may also show a positive correlation.…”