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Assessing the Jarman–Bell Principle: Scaling of intake, digestibility, retention time and gut fill with body mass in mammalian herbivores


Müller, Dennis W H; Codron, Daryl; Meloro, Carlo; Munn, Adam; Schwarm, Angela; Hummel, Jürgen; Clauss, Marcus (2013). Assessing the Jarman–Bell Principle: Scaling of intake, digestibility, retention time and gut fill with body mass in mammalian herbivores. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 164(1):129-140.

Abstract

Differences in allometric scaling of physiological characters have the appeal to explain species diversification and niche differentiation along a body mass (BM) gradient - because they lead to different combinations of physiological properties, and thus may facilitate different adaptive strategies. An important argument in physiological ecology is built on the allometries of gut fill (assumed to scale to BM1.0) and energy requirements/intake (assumed to scale to BM0.75) in mammalian herbivores. From the difference in exponents, it has been postulated that the mean retention time (MRT) of digesta should scale to BM1.0-0.75 = BM0.25. This has been used to argue that larger animals have an advantage in digestive efficiency and hence can tolerate lower-quality diets. However, empirical data does not support the BM0.25 scaling of MRT, and the deduction of MRT scaling implies, according to physical principles, no scaling of digestibility; basing assumptions on digestive efficiency on the thus-derived MRT scaling amounts to circular reasoning. An alternative explanation considers a higher scaling exponent for food intake than for metabolism, allowing larger animals to eat more of a lower quality food without having to increase digestive efficiency; to date, this concept has only been explored in ruminants. Here, using data for 77 species in which intake, digestibility and MRT were measured (allowing the calculation of the dry matter gut contents DMC), we show that the unexpected shallow scaling of MRT is common in herbivores and may result from deviations of other scaling exponents from expectations. Notably, DMC have a lower scaling exponent than 1.0, and the 95% confidence intervals of the scaling exponents for intake and DMC generally overlap. Differences in the scaling of wet gut contents and dry matter gut contents confirm a previous finding that the dry matter concentration of gut contents decreases with body mass, possibly compensating for the less favourable volume-surface ratio in the guts of larger organisms. These findings suggest that traditional explanations for herbivore niche differentiation along a BM gradient should not be based on allometries of digestive physiology. In contrast, they support the recent interpretation that larger species can tolerate lower-quality diets because their intake has a higher allometric scaling than their basal metabolism, allowing them to eat relatively more of a lower quality food without having to increase digestive efficiency.

Abstract

Differences in allometric scaling of physiological characters have the appeal to explain species diversification and niche differentiation along a body mass (BM) gradient - because they lead to different combinations of physiological properties, and thus may facilitate different adaptive strategies. An important argument in physiological ecology is built on the allometries of gut fill (assumed to scale to BM1.0) and energy requirements/intake (assumed to scale to BM0.75) in mammalian herbivores. From the difference in exponents, it has been postulated that the mean retention time (MRT) of digesta should scale to BM1.0-0.75 = BM0.25. This has been used to argue that larger animals have an advantage in digestive efficiency and hence can tolerate lower-quality diets. However, empirical data does not support the BM0.25 scaling of MRT, and the deduction of MRT scaling implies, according to physical principles, no scaling of digestibility; basing assumptions on digestive efficiency on the thus-derived MRT scaling amounts to circular reasoning. An alternative explanation considers a higher scaling exponent for food intake than for metabolism, allowing larger animals to eat more of a lower quality food without having to increase digestive efficiency; to date, this concept has only been explored in ruminants. Here, using data for 77 species in which intake, digestibility and MRT were measured (allowing the calculation of the dry matter gut contents DMC), we show that the unexpected shallow scaling of MRT is common in herbivores and may result from deviations of other scaling exponents from expectations. Notably, DMC have a lower scaling exponent than 1.0, and the 95% confidence intervals of the scaling exponents for intake and DMC generally overlap. Differences in the scaling of wet gut contents and dry matter gut contents confirm a previous finding that the dry matter concentration of gut contents decreases with body mass, possibly compensating for the less favourable volume-surface ratio in the guts of larger organisms. These findings suggest that traditional explanations for herbivore niche differentiation along a BM gradient should not be based on allometries of digestive physiology. In contrast, they support the recent interpretation that larger species can tolerate lower-quality diets because their intake has a higher allometric scaling than their basal metabolism, allowing them to eat relatively more of a lower quality food without having to increase digestive efficiency.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:05 Vetsuisse Faculty > Veterinary Clinic > Department of Small Animals
Dewey Decimal Classification:570 Life sciences; biology
630 Agriculture
Language:English
Date:2013
Deposited On:05 Dec 2012 17:19
Last Modified:07 Dec 2017 16:34
Publisher:Elsevier
Series Name:Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology
ISSN:1095-6433
Publisher DOI:https://doi.org/10.1016/j.cbpa.2012.09.018

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