Underestimating the benefits of marine protected areas for the replenishment of fished populations

Authors: Dustin J Marshall, Steven Gaines, Robert Warner, Diego R Barneche, and Michael Bode

Published in: Frontiers in Ecology and the Environment

Abstract

Marine protected areas (MPAs) are important tools for managing marine ecosystems. MPAs are expected to replenish nearby exploited populations through the natural dispersal of young, but the models that make these predictions rely on assumptions that have recently been demonstrated to be incorrect for most species of fish.

A meta‐analysis showed that fish reproductive output scales “hyperallometrically” with fish mass, such that larger fish produce more offspring per unit body mass than smaller fish. Because fish are often larger inside MPAs, they should exhibit disproportionately higher reproductive output as compared to fish outside of MPAs.

We explore the consequences of hyperallometric reproduction for a range of species for population replenishment and the productivity of exploited species.

We show that the reproductive contribution of fish inside MPAs has been systematically underestimated and that fisheries yields can be enhanced by the establishment of reservoirs of larger, highly fecund fish.

Marshall DJ, Gaines S, Warner R, Barneche DR, Bode M (2019) Underestimating the benefits of marine protected areas for the replenishment of fished populations. Frontiers in Ecology and the Environment PDF DOI

Size‐abundance rules? Evolution changes scaling relationships between size, metabolism and demography

Authors: Martino E Malerba and Dustin J Marshall

Published in: Ecology Letters

Abstract

Body size often strongly covaries with demography across species. Metabolism has long been invoked as the driver of these patterns, but tests of causal links between size, metabolism and demography within a species are exceedingly rare.

We used 400 generations of artificial selection to evolve a 2,427% size difference in the microalga Dunaliella tertiolecta. We repeatedly measured size, energy fluxes and demography across the evolved lineages. Then, we used standard metabolic theory to generate predictions of how size and demography should covary based on the scaling of energy fluxes that we measured.

The size dependency of energy remained relatively consistent in time, but metabolic theory failed to predict demographic rates, which varied unpredictably in strength and even sign across generations.

Classic theory holds that size affects demography via metabolism – our results suggest that both metabolism and size act separately to drive demography and that among‐species patterns may not predict within‐species processes.

Malerba ME, Marshall DJ (2019) Size-abundance rules? Evolution changes scaling relationships between size, metabolism and demography. Ecology Letters PDF DOI

The origin and maintenance of metabolic allometry in animals

Authors: Craig R White, Dustin J Marshall, Lesley A Alton, Pieter A Arnold, Julian E Beaman, Candice L Bywater, Catriona Condon, Taryn S Crispin, Aidan Janetzki, Elia Pirtle, Hugh S Winwood-Smith, Michael J Angilletta Jr, Stephen F Chenoweth, Craig E Franklin, Lewis G Halsey, Michael R Kearney, Steven J Portugal, and Daniel Ortiz-Barrientos

Published in: Nature Ecology & Evolution

Abstract

Organisms vary widely in size, from microbes weighing 0.1 pg to trees weighing thousands of megagrams — a 1021-fold range similar to the difference in mass between an elephant and the Earth.

Mass has a pervasive influence on biological processes, but the effect is usually non-proportional; for example, a tenfold increase in mass is typically accompanied by just a four- to sevenfold increase in metabolic rate.

Understanding the cause of allometric scaling has been a long-standing problem in biology. Here, we examine the evolution of metabolic allometry in animals by linking microevolutionary processes to macroevolutionary patterns.

We show that the genetic correlation between mass and metabolic rate is strong and positive in insects, birds and mammals.

We then use these data to simulate the macroevolution of mass and metabolic rate, and show that the interspecific relationship between these traits in animals is consistent with evolution under persistent multivariate selection on mass and metabolic rate over long periods of time.

White CR, Marshall DJ, Alton LA, Arnold PA, Beaman JE, Bywater CL, Condon C, Crispin TS, Janetzki A, Pirtle E, Winwood-Smith HS, Angilletta MJ, Chenoweth SF, Franklin CE, Halsey LG, Kearney MR, Portugal SJ, Ortiz-Barrientos D (2019) The origin and maintenance of metabolic allometry in animals, Nature Ecology & Evolution PDF DOI

Influence of food, body size, and fragmentation on metabolic rate in a sessile marine invertebrate

Authors: Lukas Schuster, Craig R White, and Dustin J Marshall

Published in: Invertebrate Biology

Abstract

Metabolic rates vary among individuals according to food availability and phenotype, most notably body size. Disentangling size from other factors (e.g., age, reproductive status) can be difficult in some groups, but modular organisms may provide an opportunity for manipulating size experimentally. While modular organisms are increasingly used to understand metabolic scaling, the potential of feeding to alter metabolic scaling has not been explored in this group.

Here, we perform a series of experiments to examine the drivers of metabolic rate in a modular marine invertebrate, the bryozoan Bugula neritina. We manipulated size and examined metabolic rate in either fed or starved individuals to test for interactions between size manipulation and food availability.

Field collected colonies of unknown age showed isometric metabolic scaling, but those colonies in which size was manipulated showed allometric scaling.

To further disentangle age effects from size effects, we measured metabolic rate of individuals of known age and again found allometric scaling. Metabolic rate strongly depended on access to food: starvation decreased metabolic rate by 20% and feeding increased metabolic rate by 43%.

In comparison to other marine invertebrates, however, the increase in metabolic rate, as well as the duration of the increase (known as specific dynamic action, SDA), were both low. Importantly, neither starvation nor feeding altered the metabolic scaling of our colonies.

Overall, we found that field‐collected individuals showed isometric metabolic scaling, whereas metabolic rate of size‐manipulated colonies scaled allometrically with body size. Thus, metabolic scaling is affected by size manipulation but not feeding in this colonial marine invertebrate.

Schuster L, White CR, Marshall DJ (2019) Influence of food, body size, and fragmentation on metabolic rate in a sessile marine invertebrate. Invertebrate Biology PDF DOI

Should we care if models are phenomenological or mechanistic?

Authors: Craig R White and Dustin J Marshall

Published in: Trends in Ecology & Evolution

Abstract

A recent meta-analysis of published data demonstrated that reproductive output increases disproportionately with size in fish.

Building on this observation, we hypothesised that growth slows as animals increase in size because of an increasing allocation of energy to reproduction, and we demonstrated that this hypothesis is plausible by fitting a simple model of energy allocation to growth, reproduction, and maintenance to weight-for-age data for a selection of fish species.

The fit of our model to growth data was indistinguishable from that of the well-known models of Pütter, von Bertallanfy, and the ontogenetic growth model (OGM) proposed by West and colleagues. However, these and other existing models of growth (e.g., dynamic energy budget (DEB) theory) fail to predict hyperallometric reproduction, and we therefore suggested that this disconnect between theory and data requires the revision of existing theory.

White CR, Marshall DJ (2019) Should we care if models are phenomenological or mechanistic? Trends in Ecology & Evolution PDF DOI 

Aquatic life history trajectories are shaped by selection, not oxygen limitation

Authors: Dustin J Marshall and Craig R White

Published in: Trends in Ecology & Evolution

Pauly1 argues that, as espoused in the gill-oxygen limitation theory (GOLT), growth slows as size increases because oxygen supply via the gills is unable to keep up with the oxygen demands of an increasingly large body. Thus, according to GOLT, growth determines the timing of reproduction, and fish reproduce when they become oxygen limited and growth starts to decline. GOLT has been critiqued on physiological grounds2,3 and we agree with those critiques. Large fish are no more oxygen limited than small fish, primarily because their respiratory surface area matches their metabolic demand for oxygen over a large size range…

Marshall DJ, White CR (2019) Aquatic life history trajectories are shaped by selection, not oxygen limitation, Trends in Ecology & Evolution. PDF DOI

Linking life-history theory and metabolic theory explains the offspring size-temperature relationship

Authors: Amanda K Pettersen, Craig R White, Robert J Bryson‐Richardson, and Dustin J Marshall

Published in: Ecology Letters

Abstract

Temperature often affects maternal investment in offspring. Across and within species, mothers in colder environments generally produce larger offspring than mothers in warmer environments, but the underlying drivers of this relationship remain unresolved.

We formally evaluated the ubiquity of the temperature–offspring size relationship and found strong support for a negative relationship across a wide variety of ectotherms. We then tested an explanation for this relationship that formally links life‐history and metabolic theories. We estimated the costs of development across temperatures using a series of laboratory experiments on model organisms, and a meta‐analysis across 72 species of ectotherms spanning five phyla.

We found that both metabolic and developmental rates increase with temperature, but developmental rate is more temperature sensitive than metabolic rate, such that the overall costs of development decrease with temperature. Hence, within a species’ natural temperature range, development at relatively cooler temperatures requires mothers to produce larger, better provisioned offspring.

Pettersen AK, White CR, Bryson-Richardson RJ, Marshall DJ (2019) Linking life-history theory and metabolic theory explains the offspring size-temperature relationship, Ecology Letters PDF DOI