Metabolic rate is negatively linked to adult survival but does not explain latitudinal differences in songbirds

Abstract

27Survival rates vary dramatically among species and predictably across latitudes, but causes of this 28 variation are unclear. The rate of living hypothesis posits that physiological damage from metabolism 29 causes species with faster metabolic rates to exhibit lower survival rates. However, whether increased 30 survival commonly observed in tropical and south temperate latitudes is associated with slower metabolic 31 rate remains unclear. We compared metabolic rates and annual survival rates across 46 species that we 32 measured, and 147 species from literature data across northern, southern, and tropical latitudes. High 33 metabolic rates were associated with lower survival but latitude had substantial direct effects on survival 34 independent of metabolism. The inability of metabolic rate to explain latitudinal variation in survival 35 suggests 1) that species may evolve physiological mechanisms that mitigate physiological damage from 36 cellular metabolism, and 2) a larger role of extrinsic environmental, rather than intrinsic metabolic, causes 37 of latitudinal differences in mortality. 38 39 Key words: physiology, adult survival, metabolism, life history theory, latitude, pace of life 48 telomere dynamics) may coevolve with metabolic rate (Brand 2000; Monaghan & Haussmann 2006; 49 Hulbert et al. 2007; Costantini 2008; Salin et al. 2015; Skrip & Mcwilliams 2016; Vagasi et al. 2018). 50 Furthermore, survival rates may be unrelated to the accumulation of physiological damage entirely. 51 Extrinsic sources of mortality, such as harsh weather or predation, may be more important in shaping 52 variation in survival. Consequently, whether metabolic rate explains variation in adult survival across 53 species remains unclear (Costantini 2008). 54 Comparative studies show that metabolic rate is negatively correlated with maximum observed 55 lifespan (MLS) in birds and mammals at broad taxonomic scales (Trevelyan et al. 1990; Hulbert et al. 56 2007). However, the overriding influence of mass on both lifespan and metabolism obscures the 57 independent effect of metabolic rate on lifespan in such studies (Speakman 2005). Moreover, other 58 comparisons raise questions about this relationship. Bats and birds have higher metabolic rates but are 59 longer-lived than terrestrial mammals of similar size, suggesting that metabolism and lifespan can be 60 decoupled, at least across broad taxonomic groups (Holmes & Austad 1995; Holmes et al. 2001; Munshi-61 South & Wilkinson 2010). Furthermore, measurements of MLS represent exceptional rather than an 62 average across individuals and are sensitive to variation in sample size, recapture probability and quality 63 of record keeping (Krementz et al. 1989; Promislow 1993). In addition, MLS is often based on captive 64 individuals that are well-fed and isolated from disease, predation and other extrinsic sources of mortality 65 that are ubiquitous in wild populations (i.e. de Magalhães & Costa 2009). Direct estimates of annual 84Here, we test whether metabolic rate explains variatio...

Latitudinal but not elevational variation in blood glucose level is linked to life history across passerine birds

“…In lowland species, our data showed lower G0 in the tropics compared to the temperate zone, supporting the conclusion of the slow physiological pace of life in tropical lowlands. The European and Afrotropical origin of our data strengthens the generality of such a conclusion, which until now was mostly based on macrophysiological data from the Americas (Jimenez et al 2014a) and more recently from Southeast Asia (Bushuev et al 2018;Boyce et al 2020). The path analysis indicated that the effect of latitude on G0 is both related and unrelated to fecundity.…”

“…The patterns observed in our study also identified interesting topics for future research such as the potential importance of glucose for avian thermogenic capacity and hypoxia adaptation at the macroevolutionary scale. Overall, our results show that macrophysiological research into baseline and stress-induced blood glucose levels has a great potential to advance the much needed (Chown & Gaston 2016;Boyce et al 2020;Tomášek et al 2021) understanding of mechanisms underpinning both life history variation and adaptation to diverse environmental conditions at large geographical scales.…”

“…Considering that species with similar life histories are expected to evolve suites of convergent physiological adaptations termed pace-of-life syndromes (POLS), corresponding large-scale geographical patterns of variation in POLS should also emerge (Ricklefs & Wikelski 2002). Research into such macrophysiological patterns is pressingly needed as their knowledge is essential to our understanding of the mechanisms underpinning global variation in demographic rates and life histories, species distribution and abundance, or physiological adaptation under diverse environmental conditions (Ricklefs & Wikelski 2002;Chown et al 2004;Chown & Gaston 2008Boyce et al 2020;Tomášek et al 2021).…”

Corticosterone mediates a growth‐survival tradeoff for an amphibian exposed to increased salinity

“…To account for this, we instead included wet mass as a covariate and ln-transformed CORT release rates (Archard et al, 2012). Additionally, mass influences survival (Boyce et al, 2020;Saether, 1989) and mass also independently influences CORT (Wingfield, 1994). Therefore, we ran survival models with and without mass as a covariate because of possible confounding effects of mass on CORT levels and survival.…”

Geographical bias in physiological data limits predictions of global change impacts

“…We gathered a total of 5,329 spatially explicit measurements of the physiological traits likely to dictate the responses of terrestrial animals to climate change: critical upper and lower thermal limits, supercooling temperature, optimal temperatures for performance, rates of metabolism, patterns of gas exchange and acclimation capacity (Table 1). The physiological traits we chose as means to identify studied environments define the range of temperatures over which animals can survive (critical upper and lower thermal limits, supercooling temperature), the rates at which they utilise energy and the demands they place on their environment (metabolic rate, which exhibits associations with survival and fitness that vary among environmental and ecological contexts: Boratyński & Koteja, 2009; Boyce et al., 2020; Pettersen et al., 2016, 2020), their susceptibility to desiccation stress (gas exchange patterns: Schimpf et al., 2012; White, Blackburn, Terblanche, et al., 2007), the temperatures at which functional performance (development, growth, and locomotion) is maximised, and their capacity to compensate physiologically for changes in the thermal environmental (acclimation capacity). The dataset includes records for 2,637 species, including insects, arachnids, fish, amphibians, reptiles, birds and mammals (Table 1).…”