Conspecific chemical cues drive density-dependent metabolic suppression independently of resource intake

Lovass, Melanie K.; Marshall, Dustin J.; Ghedini, Giulia

doi:10.1242/jeb.224824

Cited by 6 publications

(5 citation statements)

References 44 publications

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“…Metabolic suppression is stronger in response to conspecifics than heterospecifics (Armitage, 2016; Ghedini, Malerba, et al., 2020), similarly to competition for resources (Adler et al., 2018; Weis et al., 2007; Weisser et al., 2017) as we also observe for most species (Figure 4d). Since metabolic suppression occurs even when resources are not limiting (Lovass et al., 2020), mixtures initially produce net energy and biomass faster because each species competes with fewer conspecifics. But as biomass accumulates, communities suffer stronger metabolic suppression (shallower slopes of energy flux with biovolume) which reduces production.…”

Section: Discussionmentioning

confidence: 99%

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Phytoplankton diversity affects biomass and energy production differently during community development

2021

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Biodiversity determines the productivity and stability of ecosystems but some aspects of biodiversity–ecosystem functioning relationships remain poorly resolved. One key uncertainty is the inter‐relationship between biodiversity, energy and biomass production as communities develop over time. Energy production drives biomass accumulation but the ratio of the two processes can change during community development. How biodiversity affects these temporal patterns remains unknown. We empirically assessed how species diversity mediates the rates of increase and maximum values of biomass and net energy production in experimental phytoplankton communities over 10 days in the laboratory. We used five phytoplankton species to assemble three levels of diversity (monocultures, bicultures and communities) and we quantify their changes in biomass production and energy fluxes (energy produced by photosynthesis, consumed by metabolism, and net energy production as their difference) as the cultures move from a low density, low competition system to a high density, high competition system. We find that species diversity affects both biomass and energy fluxes but in different ways. Diverse communities produce net energy and biomass at faster rates, reaching greater maximum biomass but with no difference in maximum net energy production. Bounds on net energy production seem stronger than those on biomass because competition limits energy fluxes as biomass accumulates over time. In summary, diversity initially enhances productivity by diffusing competitive interactions but metabolic density dependence reduces these positive effects as biomass accumulates in older communities. By showing how biodiversity affects both biomass and energy fluxes during community development, our results demonstrate a mechanism that underlies positive biodiversity effects and offer a framework for comparing biodiversity effects across systems at different stages of development and disturbance regimes. A free Plain Language Summary can be found within the Supporting Information of this article.

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Section: Discussionmentioning

confidence: 99%

“…Since our experiment only covered ~10 generations, evolutionary changes probably played a minor role. But we cannot preclude phenotypic changes in metabolism because resource use and metabolic rates are plastic (Lovass et al., 2020; Poulson‐Ellestad et al., 2014; Svanbäck & Bolnick, 2007).…”

Section: Discussionmentioning

confidence: 99%

Phytoplankton diversity affects biomass and energy production differently during community development

2021

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“…Although these classic drivers of metabolism are well recognized, it has become apparent that population density also alters metabolic rates. From bacteria to metazoans, organisms at higher densities tend to have lower metabolic rates than conspecifics at lower densities ( DeLong et al, 2014 ; Ghedini et al, 2017 ; Lovass et al, 2020 ; Malerba et al, 2017 ; Marshall et al, 2022 ). The ultimate driver for this negative association between density and metabolism is unclear, but increased competition for resources is the most commonly proposed explanation ( Amundsen et al, 2007 ; Auer et al, 2015 ; DeLong et al, 2014 ).…”

Section: Introductionmentioning

confidence: 99%

“…Studies of density-dependent regulation of metabolism in multicellular and unicellular organisms have proliferated over recent years ( DeLong and Hanson, 2009 ; DeLong et al, 2014 ; Ghedini et al, 2017 ; Lovass et al, 2020 ; Malerba et al, 2017 ), but the idea was actually first proposed almost a century ago, and specifically in relation to sperm. In a series of papers starting in the 1920s, Gray (1928a , b , c ) showed that sea urchin sperm at high concentrations had lower per capita (individual sperm) metabolic rates and suffered less senescence than sperm in lower concentrations.…”

Section: Introductionmentioning

confidence: 99%

Per capita sperm metabolism is density dependent

Potter,

White,

Marshall

2024

Journal of Experimental Biology

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From bacteria to metazoans, higher density populations have lower per capita metabolic rates than lower density populations. The negative covariance between population density and metabolic rate is thought to represent a form of adaptive metabolic plasticity. A relationship between density and metabolism was actually first noted 100 years ago, and was focused on spermatozoa, again it was postulated that adaptive plasticity drove this pattern. Since then, contemporary studies of sperm metabolism specifically assume that sperm concentration has no effect on metabolism and that sperm metabolic rates show no adaptive plasticity. We did a systematic review to estimate the relationship between sperm aerobic metabolism and sperm concentration, for 198 estimates spanning 49 species, from protostomes to humans from 88 studies. We found strong evidence that per capita metabolic rates are concentration-dependent: both within- and among-species, sperm have lower metabolisms in dense ejaculates but increase their metabolism when diluted. On average, a 10-fold decrease in sperm concentration increased per capita metabolic rate by 35 percent. Metabolic plasticity in sperm appears to be an adaptive response, whereby sperm maximise their chances of encountering eggs.

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“…Intuitively, energy acquisition (as estimated by food consumption, Jenkins et al., 1999) is expected to decline as the number of competitors in a habitat increase (Ban et al., 2008; DeLong & Vasseur, 2011). However, it is now recognised that energy expenditure (metabolic rate, as estimated by oxygen consumption; White, 2011) also scales negatively with population density in many cases (see table 1 in Delong et al., 2014), either as a direct response to reduced ingestion rates (DeLong & Hanson, 2009; Schmoker & Hernández‐León, 2003), or as a consequence of lowered activity levels (Waters et al., 2010), conspecific chemical cues (Lovass et al., 2020) or metabolic depression due to increased stress (Guppy & Withers, 1999). Depending on the relative strengths at which per capita energy intake and expenditure decline with the number of hosts in a population, either more or less energy is accessible for a host or its dependent pathogen at any given host population density (see Figure 1, modified from Ghedini et al., 2017).…”

Section: Introductionmentioning

confidence: 99%

Energetic scaling across different host densities and its consequences for pathogen proliferation

et al. 2020

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The spread of infectious disease is determined by the ability of a pathogen to proliferate within and spread between susceptible hosts. Processes that limit the performance of a pathogen thus occur at two scales: varying with both the availability of energy within a host, and the number of susceptible hosts in a patch. When the rate at which a host intakes and expends energy is density‐dependent, these two processes are intimately linked. By modifying how hosts compete for and expend resources, a shift in population density may contribute to differences in the flow of energy in a host–pathogen system, both in terms of the energy available for a host to grow, reproduce and fight infection, as well as the energy available for a pathogen to exploit. Energy flux, therefore, connects the two contrasting scales of within‐ and between‐host dynamics by directly linking the proliferation of a pathogen to the number of hosts circulating within a patch. We use the host Daphnia magna to explore the relationship between energy intake and expenditure at various population densities, as estimated by feeding and metabolic rates respectively. By infecting hosts with the bacterial pathogen Pasteuria ramosa, we then explore how infection changes the relative balance of energy intake and expenditure, and how this energy scope translates into production of transmission spores. Our work demonstrates that energy intake declines at a faster rate with density than does metabolic rate, leaving more excess energy (i.e. discretionary energy) available for both hosts and their dependent pathogens at low population densities. This energetic advantage translates positively into host and pathogen growth, with the production of mature transmission spores benefiting most from correlated changes in host body size, as well as a direct connection between energy scope and spore loads. Our findings reinforce how patch quality for a pathogen operates at two contrasting scales, with the within‐host proliferation of a pathogen being optimised in energy rich, low density host populations and opportunities for between‐host transmission likely maximised in dense populations. A free Plain Language Summary can be found within the Supporting Information of this article.

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Conspecific chemical cues drive density-dependent metabolic suppression independently of resource intake

Cited by 6 publications

References 44 publications

Phytoplankton diversity affects biomass and energy production differently during community development

Phytoplankton diversity affects biomass and energy production differently during community development

Per capita sperm metabolism is density dependent

Energetic scaling across different host densities and its consequences for pathogen proliferation

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