Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology
The standard metabolic rate of a land snail (Cepaea hortensis) is a repeatable trait and influences winter survival
Graphical abstract
Introduction
The energy metabolism of a living organism is of obvious vital importance for all bodily functions, and as such is expected to correlate with phenotypical traits which are necessary to staying alive (Husak, 2016; Pettersen et al., 2018). Consequently, in the recent years there has been an increased interest in the factors underlying metabolic variation, both interspecific and intraspecific, and the physiological significance of such variation (Biro and Stamps, 2010; Boratynski et al., 2013; Burton et al., 2011; Pettersen et al., 2018; White and Kearney, 2013). This interest is also clearly illustrated through the recently developed Metabolic Theory of Ecology (see Sibly et al., 2012 and references therein). Most studies on the evolutionary biology of metabolic rate has been performed on vertebrates. When Nespolo and Franco (2007) summarised the available data on the repeatability of metabolic rate (a prerequisite for metabolism being targeted by natural selection), only eight (17%) of the 47 datasets in their meta-analysis were from invertebrates. Later, when White et al. (2013) summarised the literature on the effect on time on the repeatability of metabolic rate, 27 out of their 132 data-points (20%) were from invertebrates. Only two of these were from molluscs. Hence, there is still a lack of information on repeatability of metabolic rate in invertebrate species, and also information on the degree to which metabolic rate is related to fitness parameters. If natural selection should work on metabolic rate, one should expect metabolic rate to correlate with fitness parameters. However, surprisingly few studies have been able to show a relationship between metabolic rate and such central fitness proxies as survival and reproduction (Pettersen et al., 2018). This is especially true for invertebrates, since only 3 of the 13 studies reporting a relationship between metabolic rate and survival or reproductive output compiled by Pettersen et al. (2018) were from invertebrates.
Natural selection on metabolic rates could be on either the minimum rate (basal or standard metabolic rate in endotherms and ectotherms, respectively), or the maximum rate of metabolism. The minimum metabolic rate might however constitute a substantial portion of the total energy expenditure of many organisms (see McNab, 2002), which make selection on both minimum and maximum rates plausible. When SMR constitutes a substantial part of the total metabolic rate, this may consequently leave less energy available for important life-history activities such as activity, growth and reproduction. This is especially important for organisms which are constrained by metabolically expensive traits. One such group of animals is the shell-bearing molluscs, in which the costs of shell building could be expensive (Palmer, 1992; Czarnoleski et al., 2008; Watson et al., 2017) and in which also the cost of moving is among the most expensive in the animal kingdom (Denny, 1980). Hence, one could predict that shell-bearing molluscs should be especially economic in their energy use, and that large variation in metabolic rate might incur biological costs.
Only a few studies have investigated the effect of individual variations in metabolic rate of molluscs on fitness parameters. Artacho and Nespolo (2009b) studied the survival of juvenile Garden snails (Cornu aspesum) throughout the Austral summer period and found the variation in SMR among the individuals to result in a stabilization or a negative directional selection on SMR. Bartheld et al. (2015) later found a stabilizing selection on SMR in adult individuals of the same species during 1 year of exposure to natural conditions. Hence, data on metabolic selection is only available from this species within the gastropods, showing a selection on low to medium rates of metabolism. In the present study we complement these few data from gastropods by investigating the effect of individual variation in SMR on the probability of winter-survival in the white-lipped snail (Cepaea hortensis), a shell-bearing gastropod from Northern Europe.
A significant repeatability of metabolic rate has been reported in several species, but mostly reported in vertebrates (Nespolo and Franco, 2007; White et al., 2013) and rarely in non-vertebrates. The few data on repeatability of SMR in invertebrates has normally been measured over periods shorter than 30 days. Only in one invertebrate, a South American harvestman (Pachylus paessleri), was a significant repeatability over a longer period of 5 months measured (Lardies et al., 2008). In order to potentially be targeted by natural selection, the repeatability should be significant across such a long time period that selection has time to influence fitness traits such as reproduction or survival. In gastropods, Gaitan-Espitia et al. (2012) reported a significant repeatability in the slug Limax maximus. Likewise, in the garden snail, significant repeatabilites in SMR have been reported (Artacho and Nespolo, 2009a; Bartheld et al., 2015). However, in both cases, repeatability was only measured across a period of up to 1 month. Hence, an additional aim of the present study was to test if SMR in the white-lipped snail is a repeatable trait over a time period, which would increase the chance of SMR being targeted by natural selection. To this end, we estimated the repeatability of SMR across the entire winter period when snails would normally stay dormant.
Section snippets
Materials and methods
All national (Norwegian) guidelines for the care and use of animals were followed.
Metabolic rate
Of the 127 snails measured twice during the autumn of 2014, and placed in individual containers for the winter, 14 individuals were found to be dead when checked during the spring. One individual was unfortunately not retrieved during the inspection process, leaving 112 individuals to be alive when inspected again in the spring of 2015. In addition, one of the spring metabolic measurements was unsuccessful, producing a total of 111 successful VCO2-measurements during the spring period. The SMR
Metabolic rate
The values of CO2-production measured compare well with values measured earlier in gastropods. Vladimirova (2001) presents a general equation for estimating the SMR of gastropods and our mean data from the four measuring events (Table 1) span from 77% to 166% of the predicted value from this equation. There are only few available SMR data from shell-bearing pulmonated land snails to which our data can be compared. In the larger Cornu aspersumGaitan-Espitia et al., 2013a, Gaitan-Espitia et al.,
Funding
This research did not receive any specific grant from funding agencies in the public or commercial sectors.
Declaration of competing interest
No conflicts of interest!
Acknowledgements
The present study started out as a student project in connection with a field course in Zoophysiology (BI2025) at the Department of Biology at the Norwegian University of Science and Technology in Trondheim. We thank the other lectures at the course (Tor Jørgen Almaas and Kjell J. Nilssen) as well as fellow students (Vegard M. Ambjørndalen, Øystein H. Gjelsvik, Ida W. Lindefjeld, Elise Midtbust, Trym E. Norstein, Adeline Perciot, Nora Sunde and Ingvild K. Øverland) for help during the initial
References (41)
- et al.
Do consistent individual differences in metabolic rate promote consistent individual differences in behaviour?
Trends Ecol. Evol.
(2010) - et al.
Intraspecific variation in the metabolic scaling exponent in ectoterms: testing the effect of latidudinal cline, ontogeny and transgenerational change in the land snail Cornu aspersum
Comp. Biochem. Physiol. A
(2013) - et al.
Interpopulation variation in the standard metabolism of a terrestrial mollusc: repeatability of the CO2 production in the land snail Helix aspersa
Physiol. Biochem. Zool.
(2009) - et al.
Natural selection reduces energy metabolism in the garden snail, Helix aspersa (Cornu aspersum)
Evolution
(2009) - et al.
Energy expenditure and body size are targets of natural selection across a wide geographic range, in a terrestrial invertebrate
Funct. Ecol.
(2015) - et al.
The standard metabolic rate of a land snail (Cepaea hortensis) is a repeatable trait and influences winter survival
Dryad, Dataset
(2020) - et al.
Quantitative genetics and fitness effects of basal metabolism
Evol. Ecol.
(2013) - et al.
What causes intraspecific variation in resting metabolic rate and what are its ecological consequences?
Proc. R. Soc. Lond. B
(2011) Behavioural ecology, on doing the right thing, in the right time, in the right place at the right time
- et al.
Scaling of metabolism in Helix aspersa snails: changes through ontogeny and response to selection for increased size
J. Exp. Biol.
(2008)
Locomotion: the costs of gastropod crawling
Science
The energetics cost of humoral immunity in the Collared Dove, Streptopelia decaocto: is the magnitude sufficient to force energy-based trade-offs?
Funct. Ecol.
Repeatability of energy metabolism and resistance to dehydration in the invasive slug Limax maximus
Invertebr. Biol.
Varieation in thermal sensitivity and thermal tolerances in an invasive species across a climate gradient: lessons from the land snail Cornu aspersum
PLOS ONE
Beyond the “3/4-power law”: variation in the intra- and interspecific scaling of metabolic rate in animals
Biol. Rev.
A unifying explanation for diverse metabolic scaling in animals and plants
Biol. Rev.
Metabolic consequences of overlapping food deprivation and cell-mediated immune response in a long-distance migratory shorebird, the little ringed plover Charadrius dubius
J. Avian Biol.
Measuring selection on physiology in the wild and manipulating phenotypes (in terrestrial nonhuman vertebrates)
Compr. Physiol.
A Field Guide to the Land Snails of Britain and Northwestern Europe
Predation promotes survival of beetles with lower resting metabolic rates
Ent. Exp. Appl.
Cited by (2)
Synergistic effects of pesticides and environmental variables on earthworm standard metabolic rate
2022, Comparative Biochemistry and Physiology Part - C: Toxicology and PharmacologyCitation Excerpt :The standard metabolic rate (SMR) in ectotherms is defined as the minimum metabolism that supports the animal life of non-reproductive, unstressed, and not digesting food conditions (Norin and Metcalfe, 2019). This biomarker has been proposed as a complementary indicator of the organism's fitness (Bech et al., 2020). Past studies with non-mammal vertebrates have used this integrative physiological marker to assess to what extent pollutant-exposed organisms face energy requirements for pollutant toxicity and detoxification, and for maintaining normal physiological processes (Ward et al., 2006; Verreault et al., 2007; Blévin et al., 2017).
Meta-analysis reveals that resting metabolic rate is not consistently related to fitness and performance in animals
2021, Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology
- 1
Present address: Faculty of Environmental Sciences and Natural Resources Management, Norwegian University of Life Sciences, NO-1430 Ås, Norway.