Metabolic trait diversity shapes marine biogeography

Deutsch, Curtis; Penn, Justin L.; Seibel, Brad A.

doi:10.1038/s41586-020-2721-y

Cited by 176 publications

(253 citation statements)

References 49 publications

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“…This would entail developing models that can be used to predict the gill surface area from gill slit height obtained from either physical specimens or field guide illustrations. Subsequently, this gill surface area can be used to then infer energy expenditure, life history and even connect to the broader goals of macrophysiology—predicting ecological dynamics such as biogeography from physiology ( Bigman et al , 2018 ; Healy et al , 2019 ; Deutsch et al , 2020 ). Finally, we chose to focus on just one field guide because Ebert et al .…”

Section: Discussionmentioning

confidence: 99%

Gill slits provide a window into the respiratory physiology of sharks

VanderWright¹,

Bigman

Elcombe

et al. 2020

Conservation Physiology

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Metabolically important traits, such as gill surface area and metabolic rate, underpin life histories, population dynamics and extinction risk, as they govern the availability of energy for growth, survival and reproduction. Estimating both gill surface area and metabolic rate can be challenging, especially when working with large-bodied, threatened species. Ideally, these traits, and respiratory physiology in general, could be inferred from external morphology using a faster, non-lethal method. Gill slit height is quick to measure on live organisms and is anatomically connected to the gill arch. Here, we relate gill slit height and gill surface area for five Carcharhiniform sharks. We compared both total and parabranchial gill surface area to mean and individual gill slit height in physical specimens. We also compared empirical measurements of relative gill slit height (i.e. in proportion to total length) to those estimated from field guide illustrations to examine the potential of using anatomical drawings to measure gill slit height. We find strong positive relationships between gill slit height and gill surface area at two scales: (i) for total gill surface area and mean gill slit height across species and (ii) for parabranchial gill surface area and individual gill slit height within and across species. We also find that gill slit height is a consistent proportion of the fork length of physical specimens. Consequently, relative gill slit height measured from field guide illustrations proved to be surprisingly comparable to those measured from physical specimens. While the generality of our findings needs to be evaluated across a wider range of taxonomy and ecological lifestyles, they offer the opportunity that we might only need to go to the library and measure field guide illustrations to yield a non-lethal, first-order approximation of the respiratory physiology of sharks.

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Section: Discussionmentioning

confidence: 99%

Gill slits provide a window into the respiratory physiology of sharks

VanderWright¹,

Bigman

Elcombe

et al. 2020

Conservation Physiology

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“…Our global database and analysis of OGP in marine bivalves confirms that growth increases with decreasing latitude (Moss et al., 2016; Pörtner et al., 2005), but we reveal that the form of this relationship is nonlinear and depends on biogeographical context. Latitudinal variation of physiological parameters has previously been associated with seasonality and genetic adaptations to a specific temperature range (Yamahira & Conover, 2002), although temperature dependent hypoxia may also have a major role in determining biogeographical patterns (Deutsch et al, 2020). Regional disparities observed here can, however, be linked to specific circumstances; for example, the lower mean OGP found in the Mediterranean is likely related to growth limitation through lower food availability in this largely oligotrophic region (Siokou‐Frangou et al., 2010), a view supported by laboratory experiments on bryzoans (Svensson & Marshall, 2015) and Antarctic bivalves (Román‐González et al., 2017).…”

Section: Discussionmentioning

confidence: 99%

“…The nonlinear relationship of OGP with temperature and latitude suggests that other ecological and phylogenetic constraints will exist across a latitudinal gradient and between ecological realms (Parmesan & Yohe, 2003), but these may be underestimated or ignored when traditional assumptions on thermal relationships are applied in isolation (Spence & Tingley, 2020). This carries implications for the way we assess physiological responses to climate change scenarios (Clarke, 2003; Feder et al., 2000) as the consequences of climate change will differ at local scales (Stuart‐Smith et al., 2015), or across species distributions (Deutsch et al, 2020). Climate change is not consistently expressed across latitude ranges and while experimental approaches have persistently shown the greatest severity of warming on physiology to be within tropical (Deutsch et al., 2008; Tewksbury et al., 2008) and across both polar realms (Peck et al., 2004; Pörtner et al., 2007), contradictory linear relationships with greatest thermal capacity at the tropics have also been identified (Seebacher et al., 2014).…”

Section: Discussionmentioning

confidence: 99%

“…Further, some fundamental physiological assumptions, such as variation in life span (Moss et al., 2016), metabolic rates (Heilmayer et al., 2004), growth (Pörtner et al., 2005), and acclimation capacity (Seebacher et al., 2014) over wide geographical ranges are based on data with poor spatial resolution and/or are fitted with curvilinear models that do not adequately account for variation in regional environmental conditions. However, incorporation of local processes is vital, as environmental history and setting affects how individuals respond to altered environmental conditions (Calosi et al., 2016; Deutsch et al, 2020; Gladstone‐Gallagher et al., 2019; Spence & Tingley, 2020) and affects ecosystem functioning (Godbold & Solan, 2013; Wohlgemuth et al., 2016).…”

Section: Introductionmentioning

confidence: 99%

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Growth of marine ectotherms is regionally constrained and asymmetric with latitude

Reed

Godbold

Grange

et al. 2020

Global Ecol. Biogeogr.

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Aim Growth rates of organisms are routinely used to summarize physiological performance, but the consequences of local evolutionary history and ecology are largely missed by analyses on wide biogeographical scales. This broad approach has been commonly applied to other physiological parameters across terrestrial and aquatic environments. Here, we examine growth rates of marine bivalves across all biogeographical realms, latitude, and temperature, with analyses to determine regional effects on growth on global scales. Location Global: marine ecosystems. Time period 1930–2018. Major taxa Bivalves. Methods We use a comprehensive data set of bivalve growth parameters (n = 966, 243 species) representing all biogeographical realms to calculate overall growth performances. We use these data with environmental temperature to analyse global patterns in growth, accounting for regional primary productivity and phylogeny using general additive mixed and linear models. The Arrhenius relationship and corresponding activation energies are used to quantify the sensitivity to temperature in each biogeographical realm and province. Results Our analyses show that bivalve growth demonstrates latitudinal asymmetry and exhibits nonlinear relationships with latitude. We find that overall growth performance is affected by temperature and particulate organic carbon, but the form of these relationships differs with phylogeny. Growth is slower and more sensitive to increasing temperature in the Antarctic than it is in the Arctic, and decreases with increasing temperature in some tropical realms, a previously unidentified and fundamental difference in growth and physiological sensitivity. Main conclusions Our findings provide compelling evidence that the widely used curvilinear relationship between temperature and growth rates in marine ectotherms is an inappropriate descriptor of thermal sensitivity, because it normalizes regional variations in physiological performance. Without a more detailed assessment of global physiological patterns, the responses of species to local variations associated with climate change will be under‐appreciated in global assessments of climate risk, minimizing the effectiveness of management and conservation.

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“…Metabolic scaling is also applied in influential size-based models predicting animal responses to climate change (Cheung et al 2013;Deutsch et al 2015Deutsch et al , 2020, and in metabolic growth models predicting the maximum biomass that can be sustainably harvested from exploited populations (e.g. stock assessments in fisheries; von Bertalanffy 1957; Andersen 2019).…”

Section: Introductionmentioning

confidence: 99%

Fast ontogenetic growth drives steep evolutionary scaling of metabolic rate

Norin

2021

Preprint

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Metabolic rate (MR) changes with body mass (BM) as MR = aBMb, where a is a normalisation constant (log–log intercept) and b the scaling exponent (log–log slope). This scaling relationship is fundamental to biology and widely applied, yet a century of research has provided little consensus on why and how steeply metabolic rate scales with body mass. I here show that ontogenetic (within-individual) b can be strongly and positively related to growth rates of juvenile fish when food availability is naturally restricted, with fast growing individuals having steep and near-isometric metabolic scaling (b ≈ 1). I suggest that the steep evolutionary (among-species) scaling also found for fishes (b also approaching 1) is a by-product of natural selection for these fast growing individuals early in ontogeny, and that a weaker relationship between metabolic scaling and growth later in life causes variation in b at lower taxonomic levels (within orders or species). I support these ideas by showing that b within fish orders is linked to natural mortality rates of fish larvae.

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Metabolic trait diversity shapes marine biogeography

Cited by 176 publications

References 49 publications

Gill slits provide a window into the respiratory physiology of sharks

Gill slits provide a window into the respiratory physiology of sharks

Growth of marine ectotherms is regionally constrained and asymmetric with latitude

Fast ontogenetic growth drives steep evolutionary scaling of metabolic rate

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