Ecology shapes metabolic and life history scalings in termites

Abstract

1. Metabolic rate (B) is a fundamental property of organisms, and scales with body mass (M) as B = αMβ. There has been much debate on whether scaling parameters should be viewed as constants or variables. However, there is increasing evidence that ecological differentiation can affect both α and β. 2. In colonial organisms such as social insects, individual metabolism is integrated at the colony level. Theory and data suggest that whole‐colony metabolism partly reflects individual‐level metabolic and life‐history scalings, but whether these have been affected by ecological diversification is little known. 3. Here, this issue was addressed using termites. Data from the literature were assembled to assess the interspecific scalings of individual metabolic rate with individual mass, and of individual mass with colony mass. Concurrently, it was tested whether such scalings were affected by two key ecological traits: lifestyle and diet. 4. Individual‐level metabolic scaling was affected by diet, with β = 1.02 in wood feeders and 0.60 in soil feeders. However, there was no difference in α. Further, individual mass scaled to the 0.25 power with colony mass, but forager species had larger colonies and smaller individuals relative to wood‐dwelling, sedentary ones, thus producing a grade shift. 5. Our results show that ecological diversification has affected fundamental metabolic and life‐history scalings in termites. Thus, theory on the energetics and evolution of colonial life should account for this variability.

Rediscovering and Reviving Old Observations and Explanations of Metabolic Scaling in Living Systems

“…These include models or hypotheses invoking the effects of four-dimensional geometry, sometimes including biological time as the fourth dimension [17,[77][78][79][80][81][82][83][84], the relative effects of resource supply versus demand (e.g., [19,20,46,70,[85][86][87][88][89][90]), the biological regulation of metabolic rate (e.g., [20,87,[90][91][92][93][94][95][96][97][98]), and various adaptive effects resulting from interactions with ecological factors (e.g., [19,20,46,[99][100][101][102][103][104][105][106][107]). Here I focus on four major, much-discussed theoretical approaches encompassed by the 'contextual multimodal theory' (CMT) of metabolic scaling ( Figure 1) recently proposed in this journal [20].…”

“…Many investigators (but surprisingly not Kleiber himself, a founder of the 3/4-power law) rejected the thermoregulatory surface-area model of metabolic scaling, because it seemed incapable of explaining 3/4-power scaling, especially in ectothermic organisms that do not actively maintain constant body temperatures (see also [20]). Furthermore, the metabolic scaling slope does not necessarily approximate the theoretical values of 2/3 or 3/4, but may vary extensively between ~0 and >1, in association with differences in taxonomic affiliation, lifestyle, developmental stage, physiological status, and various ecological factors (e.g., [19,20,23,24,26,27,32,34,39,[44][45][46][47][48][49][54][55][56][57][58][59][60][61][72][73][74][75][76][99][100][101][102][103][104][105][106][107][117][118][119][120][121]). …”

“…A major limitation of the cell-based RD approach is that it cannot explain by itself why the hypometric scaling of cellular metabolic rate is lost in cells cultured in vivo (reviewed in [20,97]). Nor can it explain by itself why the metabolic scaling slope varies in relation to body shape, developmental stage, physiological condition, and various ecological factors (e.g., [19,20,46,56,103,105,107,132,133]). The cell-based RD approach focuses on proximate causes at the cellular level, but ignores proximate systemic causes and ultimate (evolutionary) causes of metabolic scaling relationships (also see [20]).…”

“…In short, extrinsic (ecological) factors may have primary effects on metabolic scaling [20,[98][99][100][101][102][103][104][105][106][107], rather than merely secondary effects, as postulated by models based on intrinsic physical and biological properties [63,64,[158][159][160][161][162]. Glazier and colleagues [105] have recommended the development of an "ecological theory of metabolism" (ETM), as an alternative (or complement) to the MTE (cf.…”

“…In keeping with the overall theme of my article, this discovery of metabolic scaling diversity was rediscovered many times during the 1900s (e.g., [23,32,[261][262][263]), but largely ignored in favor of a 3/4-power law. Only during the last two decades, has a true appreciation of the broad diversity of metabolic scaling relationships been spreading widely (see e.g., [19,20,24,26,27,33,34,39,44,46,50,[54][55][56][57][58]103,[105][106][107]117,118,121,132,142,143,147,149,153,182,193,219,225,260,264,265]), thus helping to stimulate the development of multi-mechanistic explanatory models (see Section 3.1). The recognition of diversity is not necessarily a hindrance to the development of general theory, as sometimes thought (cf.…”