“Metabolic theory and the temperature size rule explain the temperature dependence of population carrying capacity”

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Joey R. Bernhardt, Jennifer M. Sunday, and Mary I. O’Connor (Dec 2018)

The DOI will be https://dx.doi.org/10.1086/700114

Carrying capacity declines with warming, as predicted by the metabolic theory of ecology and the temperature-size rule

Fewer when it’s warmer

The coastal waters of Vancouver Island, Canada, where the population of the green alga, Tetraselmis tetrahele, was collected. Bottom panel shows T. tetrahele cells as imaged by the FlowCAM, the instrument used to count and size the phytoplankton in this study.
(Credit: Joey Bernhardt)

Predicting population persistence and dynamics in the context of global change is a major challenge for ecology. Density of a population at carrying capacity is a key concept linking population dynamics to broader-scale patterns of biodiversity and population persistence. A widely held prediction is that population abundance at carrying capacity should decrease with warming. While it may seem counterintuitive that density should decrease when it’s warmer, the rationale is that as temperatures increase, individual metabolic rates are predicted to increase. If resource supply is limited and equal across all temperatures, then populations growing in warmer conditions should be able to support fewer individuals because each individual requires more metabolic resources to live. This prediction, which is based on the metabolic theory of ecology, has not been tested empirically.

Here, using experimental populations of the green alga, Tetraselmis tetrahele, Joey Bernhardt, Jenn Sunday, and Mary O’Connor tested empirically whether effects of temperature on short-term metabolic performance (rates of photosynthesis and respiration) translate directly to effects of temperature on population dynamics. They measured per-capita metabolic rates and population abundances at carrying capacity across a temperature gradient spanning 5°C – 38°C. They found that carrying capacity declined with temperature, and that this decline in abundance was predicted by metabolic theory models. The temperature dependence of individual metabolic performance translated to population abundance. Concurrent with declines in abundance, they observed a linear decline in cell size of approximately 2% per degree Celsius, which is consistent with broadly observed patterns in unicellular organisms, known as the temperature-size rule. Their results indicate that outcomes of population dynamics across a range of temperatures reflect organismal responses to temperature via metabolic scaling, providing a general basis for forecasting population responses to global change.

Graphical overview of the main findings of the study. (Credit: Joey Bernhardt)

Abstract

The temperature dependence of highly conserved subcellular metabolic systems affects ecological patterns and processes across scales, from organisms to ecosystems. Population density at carrying capacity plays an important role in evolutionary processes, biodiversity and ecosystem function, yet how it varies with temperature-dependent metabolism remains unclear. Though the exponential effect of temperature on intrinsic population growth rate, r, is well known, we still lack clear evidence that population density at carrying capacity, K, declines with increasing per-capita metabolic rate, as predicted by the metabolic theory of ecology (MTE). We experimentally tested whether temperature effects on photosynthesis propagate directly to population carrying capacity in a model species, the mobile phytoplankton Tetraselmis tetrahele. After maintaining populations at fixed resource supply and temperatures (6 levels) for 43 days, we found that carrying capacity declined with increasing temperature. This decline was predicted quantitatively when models included temperature-dependent metabolic rates and temperature-associated body size shifts. Our results demonstrate that warming reduces carrying capacity, and that temperature effects on body size and metabolic rate interact to determine how temperature affects population dynamics. These findings bolster efforts to relate metabolic temperature dependence to population and ecosystem patterns via MTE.