Canadian Journal of Zoology Estimating the energy expenditure of endotherms at the species level Journal: Canadian Journal of Zoology Manuscript ID cjz-2020-0035 Manuscript Type: Article Date Submitted by the 17-Feb-2020 Author: Complete List of Authors: McNab, Brian; University of Florida, Biology Is your manuscript invited for consideration in a Special Not applicable (regular submission) Issue?: Draft arvicoline rodents, BMR, Anatidae, energy expenditure, endotherms, Keyword: Meliphagidae, Phyllostomidae © The Author(s) or their Institution(s) Page 1 of 42 Canadian Journal of Zoology Estimating the energy expenditure of endotherms at the species level Brian K. McNab B.K. McNab, Department of Biology, University of Florida 32611 Email for correspondence: [email protected] Telephone number: 1-352-392-1178 Fax number: 1-352-392-3704 The author has no conflict of interest Draft © The Author(s) or their Institution(s) Canadian Journal of Zoology Page 2 of 42 McNab, B.K. Estimating the energy expenditure of endotherms at the species level. Abstract The ability to account with precision for the quantitative variation in the basal rate of metabolism (BMR) at the species level is explored in four groups of endotherms, arvicoline rodents, ducks, melaphagid honeyeaters, and phyllostomid bats. An effective analysis requires the inclusion of the factors that distinguish species and their responses to the conditions they encounter in the environment. These factors are implemented by changes in body composition and are responsible for the non-conformity of species to a scaling curve. Two concerns may limit an analysis. The factors correlatedDraft with energy expenditure often correlate with each other, which usually prevents them from being included together in an analysis, thereby preventing a complete analysis, implying the presence of factors other than mass. Many of the relevant factors, such as food habits and an island residence, are qualitative, which complicates their inclusion in a quantitative analysis, a difficulty that is solved by ANCOVA. The precision of an analysis, based on an inclusive equation, can be determined by comparing its estimates to measurements of the performance of species. Without this comparison, the effectiveness of an analysis cannot be determined, which then simply becomes a suggestion. A proposed standard for a precise estimate is for it to be within 10% of the measured rate. Key words: arvicoline rodents, BMR, ducks, energy expenditure, endotherms, meliphagid honeyeaters, phyllostomid bats © The Author(s) or their Institution(s) Page 3 of 42 Canadian Journal of Zoology 1 Estimating the energy expenditure of endotherms at the species level 2 INTRODUCTION 3 The goal of this article is to determine the extent to which the basal rate of 4 metabolism (BMR) of birds and mammals can be estimated with precision. This can 5 be accomplished through an equation that includes the various factors that correlate 6 with basal rate. The reason why BMR is worthy of consideration is that data are 7 available from >1400 species, which gives an enhanced view of biological diversity. 8 And many aspects of species’ performance correlate with BMR, including their 9 thermal biology, environmental tolerance, reproductive output, and field energy 10 expenditure (McNab 2013, 2015). 11 A series of operative factorsDraft determine basal rate, including body mass, body 12 composition, and tissue activity, as reflected in their correlations with food habits, 13 climate, substrate, and an island or continental distribution (Raichlen et al. 2010; 14 McNab, 2015, 2019b). These observations go beyond demonstrating correlations of 15 basal rate with various ecological and behavioral factors. It goes to their 16 implementation and collective action. Correlations are not determinative, they 17 reflect and introduce the action of the mechanisms that determine basal rate 18 (McNab 2019b). The rate of endotherms stands at the interface between energy 19 income and expenditure and therefore accounts for the restriction or expansion of 20 the behavior of endotherms. 21 The consequences of the correlates of basal rate have not been pursued. This 22 article deals with whether the information that we have on the correlatives of basal 23 rate can collectively account for its variance at the species level. Without this 1 © The Author(s) or their Institution(s) Canadian Journal of Zoology Page 4 of 42 24 approach we do not know the extent to which we understand how basal rates are 25 determined and we are left with the superficiality of correlations (McNab 2019b). 26 A common approach in the analysis of quantitative physiological data from a 27 variety of species is to examine a scaling relationship. An r2 0.85 mass accounts 28 for at least 85% of the interspecific variance of the basal rate of the species. The 29 problem with this conclusion is that r2 increases with the range in mass, thereby 30 obscuring the appearance of other factors that also may be determinative. If a group 31 of species has no difference in mass, an appreciable variance in expenditures usually 32 remains, which contributes to the residual variation around the scaling curve. This 33 implies that factors other than mass also determine energy expenditure. The 34 adequacy of an analysis can be determinedDraft by its ability to account for the basal 35 rates of species with precision, but it must include the factors responsible for the 36 residual variation. If a multifactorial analysis is effective, the residual variation 37 around a scaling curve would decrease, or even disappear. 38 The attempt to account for the variance in basal rate is complicated. When 39 relatives differ in behavior and/or face different environmental conditions, they 40 often have different expenditures. This has been seen in deer mice (McNab and 41 Morrison 1963; Mueller and Diamond 2001; McNab 2019a), heteromyid rodents 42 (McNab 2012), and larks (Tieleman et al. 2003) with regard to their position along a 43 mesic/xeric gradient. And when unrelated species converge on a behavior, their 44 basal rates are more similar than expected from ancestry, as seen in ant- and 45 termite-eating mammals, including a monotreme, a marsupial, and many unrelated 2 © The Author(s) or their Institution(s) Page 5 of 42 Canadian Journal of Zoology 46 eutherians (McNab 2012). A similar convergence in energy expenditure occurs 47 among arboreal folivores and fossorial rodents (McNab 2012). 48 Another complication is that a factor does not necessarily have a uniform 49 performance. Small frugivores may have high or low mass-independent basal rates, 50 but all frugivores that weigh > 0.5 kg have low rates, a decrease that increases with 51 mass (McNab 2015). We shall see the impact of climate on nectarivory. To what 52 extent can an analysis account for the variance in the basal rate of species? This is a 53 physiological question. It concerns the mechanisms by which performances are 54 implemented, not history. Occurrence is not performance. 55 Energy expenditure has often been demonstrated to correlate with 56 behavioral and ecological factors (McNabDraft and Morrison 1963, McNab 1969, Soriano 57 et al. 2002; McNab 2003b; Tieleman et al. 2003; McNab 2012, 2015). However, 58 these correlations have not been pursued to determine the extent to which they 59 account for the basal rate of individual species. 60 The ability to account for the variation of BMR with precision is addressed 61 here by examining four sets of species with different characteristics. One analysis is 62 of 34 arvicoline rodents, a behaviorally and ecologically uniform group. This 63 subfamily of the Cricetidae includes voles, lemmings, and muskrats. An assembly of 64 27 species of anatids, i.e., ducks and geese, demonstrates the consequences of factor 65 interactions. An analysis of data from 20 meliphagid honeyeaters is examined to see 66 the extent to which their basal rates can be estimated with precision. Finally the 67 basal rate of 30 phyllostomid bats, characterized by their great ecological and 68 behavioral diversity, is reexamined. Phyllostomids have the greatest range in food 3 © The Author(s) or their Institution(s) Canadian Journal of Zoology Page 6 of 42 69 habits of all mammalian families. Data from other families with large diversities in 70 factors are not available. 71 Some possible difficulties with estimation must be faced. One is that the 72 mutual correlation of some characters often prevents an analysis from being 73 completed. Many of the correlates are qualitative, which are difficult to include in a 74 quantitative analysis. Furthermore, the identity of relevant factors is not always 75 obvious. 76 77 METHODS 78 At first, a scaling relationship is described. Then the included species are put into 79 categories with respect to their positionDraft along the scaling curve, i.e., above, below, or 80 in agreement with the curve. This is the basis for judging whether a particular 81 species has a ‘high’ or ‘low’ mass-independent basal rate. Factors that have more 82 than one state may differentially influence energy expenditure, which is what 83 contributes to the diversity of species and the complexity of analysis. Here the goal 84 is to account for the deviation of a species’ basal rate from the scaling curve: why are 85 high species high and low species low? Can residual variation be reduced, or even 86 eliminated, by including influential factors other than mass? 87 The intent of this article is to compare measurements of basal rate with 88 estimates derived from an equation that includes mass and the other factors that 89 correlate with BMR. A difficulty with this approach is that many of the appropriate 90 factors to be included are qualitative, as in food habits, being volant or flightless, and 91 living on islands or continents. How they are to be included in an equation? 4 © The Author(s) or their Institution(s) Page 7 of 42 Canadian Journal of Zoology 92 The quantification of these factors is made by ANCOVA.