Mechanistic Drivers of Flexibility in Summit Metabolic Rates of Small Birds

Abstract

Flexible metabolic phenotypes allow animals to adjust physiology to better fit ecological or environmental demands, thereby influencing fitness. Summit metabolic rate (Msum = maximal thermogenic capacity) is one such flexible trait. Skeletal muscle and heart masses and myocyte metabolic intensity are potential drivers of Msum flexibility in birds. We examined correlations of skeletal muscle and heart masses and pectoralis muscle citrate synthase (CS) activity (an indicator of cellular metabolic intensity) with Msum in house sparrows (Passer domesticus) and dark-eyed juncos (Junco hyemalis) to determine whether these traits are associated with Msum variation. Pectoralis mass was positively correlated with Msum for both species, but no significant correlation remained for either species after accounting for body mass (Mb) variation. Combined flight and leg muscle masses were also not significantly correlated with Msum for either species. In contrast, heart mass was significantly positively correlated with Msum for juncos and nearly so (P = 0.054) for sparrows. Mass-specific and total pectoralis CS activities were significantly positively correlated with Msum for sparrows, but not for juncos. Thus, myocyte metabolic intensity influences Msum variation in house sparrows, although the stronger correlation of total (r = 0.495) than mass-specific (r = 0.378) CS activity with Msum suggests that both pectoralis mass and metabolic intensity impact Msum. In contrast, neither skeletal muscle masses nor pectoralis metabolic intensity varied with Msum in juncos. However, heart mass was associated with Msum variation in both species. These data suggest that drivers of metabolic flexibility are not uniform among bird species.

Acute cold and exercise training upregulate similar aspects of fatty acid transport and catabolism in house sparrows, Passer domesticus

“…However, migratory (Driedzic et al, 1993) and seasonal (Dawson and Marsh, 1989;Swanson, 2010) stability in pectoralis CS activities are also common in birds. The increases in mass-specific pectoralis CS activities for both training protocols in this study, along with the significant positive correlations between pectoralis CS activities and organismal metabolic capacities, are consistent with other house sparrow data, as total pectoralis CS activity increases in winter relative to summer (Liknes and Swanson, 2011) and pectoralis CS activity is positively correlated with M sum (Swanson et al, 2014a). Collectively, these studies suggest that increases in pectoralis CS activities are important to increased organismal capacities for exercise and shivering in house sparrows.…”

“…Positive correlations of pectoralis CS activity with both M sum and MMR for sparrows in the present study suggest that cellular metabolic intensity contributes to training effects for house sparrow. This is not necessarily the case for birds generally, as previous studies showed that M sum was also positively correlated with pectoralis CS activity in house sparrows, but not for other birds Swanson et al, 2014a). In addition, MMR was only significantly positively correlated with pectoralis CS activities in male red junglefowl (Gallus gallus), but not in female red junglefowl or house sparrows (Hammond et al, 2000;Buttemer et al, 2010).…”

“…We used house sparrows as our study species, since the same population of house sparrows exhibited winter increases in summit metabolic rate (maximum thermogenic metabolic rate; M sum ) (Swanson and Liknes, 2006) and a positive correlation between M sum and CS activities in pectoralis (Swanson et al, 2014a). Bird collection, training protocols and tissue dissection methods have been discussed in detail by Zhang et al (2015a).…”

31° South: The physiology of adaptation to arid conditions in a passerine bird

“…Given the absence of regional differences in maximum thermogenic capacity (Ribeiro, Prats, et al, ), the wider metabolic expansibility observed in populations experiencing lower winter temperatures (Central and Inland populations; mean minimum temperature in winter <2°C) inescapably stems from the lower BMR. Thus, as opposed to northern‐temperate climates, where highly variable climates select for higher maximum thermogenic capacity (Swanson, Zhang, & King, ), subtropical and highly variable climates should select for lower BMR.…”

31° South: phenotypic flexibility in adaptive thermogenesis among conspecific populations of an arid-endemic bird - from organismal to cellular level

“…While shivering thermogenesis results from cellular processes, namely the activation of 44 energetic metabolism pathways to burn cellular fuels to power skeletal muscle contraction 45 (Hothola 2004), it can be quantified at the organism-level as the maximum thermoregulatory 46 metabolic capacity (M sum ; (Thompson 2010)). In fact, several studies showed that cold 47 temperatures lead to increases in M sum (Vezina et al 2011) (Swanson et al 2014a). One 48 explanation for this flexibility in maximum metabolic capacity is the cold adaptation hypothesis, 49 which posits that birds wintering in cold climates should have higher M sum than those in warmer 50 climates, and hence high M sum is critical for overwinter survival in very cold regions (Marsh and 51 pectoralis muscle which is the primary thermogenic organ (Vézina et al 2006) (Swanson et al 59 2014a); iii) increase in enzymatic activity in oxidative metabolic pathways (Vézina et al 2006) 60 (Zheng et al 2014) (Liknes and Swanson 2011a); and iv) increase in fat catabolism (Dawson et 61 al.…”