An official website of the United States government
Synopsis Metabolism is a fundamental attribute of all organisms that influences how species affect and are affected by their natural environment. Differences between sexes in ectothermic species may substantially alter metabolic scaling patterns, particularly in viviparous or live-bearing species where females must support their basal metabolic costs and that of their embryos. Indeed, if pregnancy is associated with marked increases in metabolic demand and alters scaling patterns between sexes, this could in turn interact with natural sex ratio variation in nature to affect population-level energy demand. Here, we aimed to understand how sex and pregnancy influence metabolic scaling and how differences between sexes affect energy demand in Gambusia affinis (Western mosquitofish). Using the same method, we measured routine metabolic rate in the field on reproductively active fish and in the laboratory on virgin fish. Our data suggest that changes in energy expenditure related to pregnancy may lead to steeper scaling coefficients in females (b = 0.750) compared to males (b = 0.595). In contrast, virgin females and males had similar scaling coefficients, suggesting negligible sex differences in metabolic costs in reproductively inactive fish. Further, our data suggest that incorporating sex differences in allometric scaling may alter population-level energy demand by as much as 20–28%, with the most pronounced changes apparent in male-biased populations due to the lower scaling coefficient of males. Overall, our data suggest that differences in energy investment in reproduction between sexes driven by pregnancy may alter allometric scaling and population-level energy demand.
more »
« less
Metabolic scaling as an emergent outcome of variation in metabolic rate
The allometric scaling of metabolic rate and what drives it are major questions in biology with a long history. Since the metabolic rate at any level of biological organization is an emergent property of its lower-level constituents, it is an outcome of the intrinsic heterogeneity among these units and the interactions among them. However, the influence of lower-level heterogeneity on system-level metabolic rate is difficult to investigate, given the tightly integrated body plan of unitary organisms. In this context, social insects such as honeybees can serve as important model systems because unlike unitary organisms, these superorganisms can be taken apart and reassembled in different configurations to study metabolic rate and its various drivers at different levels of organization. This commentary discusses the background of such an approach and how combining it with artificial selection to generate heterogeneity in metabolic rate with an analytical framework to parse out the different mechanisms that contribute to the effects of heterogeneity can contribute to the various models of metabolic scaling. Finally, the absence of the typical allometric scaling relationship among different species of honeybees is discussed as an important prospect for deciphering the role of top-down ecological factors on metabolic scaling. This article is part of the theme issue ‘The evolutionary significance of variation in metabolic rates’.
more »
« less
- Award ID(s):
- 2241230
- PAR ID:
- 10560269
- Publisher / Repository:
- Royal Society Publishing
- Date Published:
- Journal Name:
- Philosophical Transactions of the Royal Society B: Biological Sciences
- Volume:
- 379
- Issue:
- 1896
- ISSN:
- 0962-8436
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Coloniality may grant colony members an energetic advantage in the form of lower individual respiration rates as colony size increases. If this occurs it should be apparent as negative allometric scaling of respiration with colony size, and colonial organisms should have scaling factors < 1. However, colonial members from phylum Rotifera have yet to be examined. To test if colonial rotifers possess allometric scaling relationships between respiration rate and colony size, we measured respiration rates for four solitary and three colonial rotifer species; from these respiration rates we estimated scaling factors. We found mixed evidence for allometric scaling of respiration rate in colonial rotifers. Both rotifers with allometric scaling of respiration rate,Conochilus hippocrepisandLacinularia flosculosa, have extensive mucilaginous coverings. These coverings may represent an investment of colony members into a shared structure, lowering individual metabolic costs and thus respiratory needs. Additionally, we determined which traits are associated with allometric scaling of respiration. We compiled known scaling factors for animal phyla from a wide phylogenetic spectrum with colonial representatives and conducted a hierarchical mixed regression that included attributes of colonies. Traits associated with allometric scaling in colonial animals included colony shape, the presence of shared extrazooidal structures, and planktonic lifestyle. There are many other colonial rotifers and animal taxa for which allometric scaling factors have yet to be estimated, knowing these may enhance our understanding of the benefits of coloniality in animals.more » « less
-
Abstract Metabolic rate (MR) usually changes (scales) out of proportion to body mass (BM) as MR = aBMb, where a is a normalisation constant and b is the scaling exponent that reflects how steep this change is. This scaling relationship is fundamental to biology, but over a century of research has provided little consensus on the value of b, and why it appears to vary among taxa and taxonomic levels. By analysing published data on fish and taking an individual-based approach to metabolic scaling, I show that variation in growth of fish under naturally restricted food availability can explain variation in within-individual (ontogenetic) b for standard (maintenance) metabolic rate (SMR) of brown trout (Salmo trutta), with the fastest growers having the steepest metabolic scaling (b ≈ 1). Moreover, I show that within-individual b can vary much more widely than previously assumed from work on different individuals or different species, from –1 to 1 for SMR among individual brown trout. The negative scaling of SMR for some individuals was caused by reductions in metabolic rate in a food limited environment, likely to maintain positive growth. This resulted in a mean within-individual b for SMR that was significantly lower than the across-individual (“static”) b, a difference that also existed for another species, cunner (Tautogolabrus adspersus). Interestingly, the wide variation in ontogenetic b for SMR among individual brown trout did not exist for maximum (active) metabolic rate (MMR) of the same fish, showing that these two key metabolic traits (SMR and MMR) can scale independently of one another. I also show that across-species (“evolutionary”) b for SMR of 134 fishes is significantly steeper (b approaching 1) than the mean ontogenetic b for the brown trout and cunner. Based on these interesting findings, I hypothesise that evolutionary and static metabolic scaling can be systematically different from ontogenetic scaling, and that the steeper evolutionary than ontogenetic scaling for fishes arises as a by-product of natural selection for fast-growing individuals with steep metabolic scaling (b ≈ 1) early in life, where size-selective mortality is high for fishes. I support this by showing that b for SMR tends to increase with natural mortality rates of fish larvae within taxa.more » « less
-
Metabolism energizes all biological processes, and its tempo may importantly influence the ecological success and evolutionary fitness of organisms. Therefore, understanding the broad variation in metabolic rate that exists across the living world is a fundamental challenge in biology. To further the development of a more reliable and holistic picture of the causes of this variation, we review several examples of how various intrinsic (biological) and extrinsic (environmental) factors (including body size, cell size, activity level, temperature, predation and other diverse genetic, cellular, morphological, physiological, behavioural and ecological influences) can interactively affect metabolic rate in synergistic or antagonistic ways. Most of the interactive effects that have been documented involve body size, temperature or both, but future research may reveal additional ‘hub factors’. Our review highlights the complex, intimate inter-relationships between physiology and ecology, knowledge of which can shed light on various problems in both disciplines, including variation in physiological adaptations, life histories, ecological niches and various organism-environment interactions in ecosystems. We also discuss theoretical and practical implications of interactive effects on metabolic rate and provide suggestions for future research, including holistic system analyses at various hierarchical levels of organization that focus on interactive proximate (functional) and ultimate (evolutionary) causal networks. This article is part of the theme issue ‘The evolutionary significance of variation in metabolic rates’.more » « less
-
ABSTRACT Body size profoundly affects organism fitness and ecosystem dynamics through the scaling of physiological traits. This study tested for variation in metabolic scaling and its potential drivers among corals differing in life history strategies and taxonomic identity. Data were compiled from published sources and augmented with empirical measurements of corals in Moorea, French Polynesia. The data compilation revealed metabolic isometry in broadcasted larvae, but size-independent metabolism in brooded larvae; empirical measurements of Pocillopora acuta larvae also supported size-independent metabolism in brooded coral larvae. In contrast, for juvenile colonies (i.e. 1–4 cm diameter), metabolic scaling was isometric for Pocillopora spp., and negatively allometric for Porites spp. The scaling of biomass with surface area was isometric for Pocillopora spp., but positively allometric for Porites spp., suggesting the surface area to biomass ratio mediates metabolic scaling in these corals. The scaling of tissue biomass and metabolism were not affected by light treatment (i.e. either natural photoperiods or constant darkness) in either juvenile taxa. However, biomass was reduced by 9–15% in the juvenile corals from the light treatments and this coincided with higher metabolic scaling exponents, thus supporting the causal role of biomass in driving variation in scaling. This study shows that metabolic scaling is plastic in early life stages of corals, with intrinsic differences between life history strategy (i.e. brooded and broadcasted larvae) and taxa (i.e. Pocillopora spp. and Porites spp.), and acquired differences attributed to changes in area-normalized biomass.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1098/rstb.2022.0495
