Unimodal size scaling of phytoplankton growth and the size dependence of nutrient uptake and use

doi:10.1111/ELE.12052

Home
/
Papers
/
Unimodal size scaling of phytoplankton growth and the size dependence of nutrient uptake and use

Journal Article•DOI•

Unimodal size scaling of phytoplankton growth and the size dependence of nutrient uptake and use

Emilio Marañón¹, Pedro Cermeño¹, Daffne C. López-Sandoval¹, Tamara Rodríguez-Ramos¹, Cristina Sobrino¹, María Huete-Ortega¹, José María Blanco², Jaime Rodríguez² - Show less +4 more•Institutions (2)

University of Vigo¹, University of Málaga²

01 Mar 2013-Ecology Letters (John Wiley & Sons, Ltd)-Vol. 16, Iss: 3, pp 371-379

TL;DR: It is suggested that the unimodal size scaling of phytoplankton growth arises from taxon-independent, size-related constraints in nutrient uptake, requirement and assimilation.

read less

Abstract: Phytoplankton size structure is key for the ecology and biogeochemistry of pelagic ecosystems, but the relationship between cell size and maximum growth rate (μ(max) ) is not yet well understood. We used cultures of 22 species of marine phytoplankton from five phyla, ranging from 0.1 to 10(6) μm(3) in cell volume (V(cell) ), to determine experimentally the size dependence of growth, metabolic rate, elemental stoichiometry and nutrient uptake. We show that both μ(max) and carbon-specific photosynthesis peak at intermediate cell sizes. Maximum nitrogen uptake rate (V(maxN) ) scales isometrically with V(cell) , whereas nitrogen minimum quota scales as V(cell) (0.84) . Large cells thus possess high ability to take up nitrogen, relative to their requirements, and large storage capacity, but their growth is limited by the conversion of nutrients into biomass. Small species show similar volume-specific V(maxN) compared to their larger counterparts, but have higher nitrogen requirements. We suggest that the unimodal size scaling of phytoplankton growth arises from taxon-independent, size-related constraints in nutrient uptake, requirement and assimilation.

...read moreread less

Citations

PDF

Open Access

More filters

Journal Article•DOI•

Cell Size as a Key Determinant of Phytoplankton Metabolism and Community Structure

[...]

Emilio Marañón¹•Institutions (1)

University of Vigo¹

05 Jan 2015-Annual Review of Marine Science

TL;DR: Evidence indicates that biomass-specific production and growth rates are similar in both small and large cells but peak at intermediate cell sizes, and the superior ability of intermediate-size cells to exploit high nutrient concentrations explains their biomass dominance during blooms.

...read moreread less

Abstract: Phytoplankton size structure controls the trophic organization of planktonic communities and their ability to export biogenic materials toward the ocean's interior. Our understanding of the mechanisms that drive the variability in phytoplankton size structure has been shaped by the assumption that the pace of metabolism decreases allometrically with increasing cell size. However, recent field and laboratory evidence indicates that biomass-specific production and growth rates are similar in both small and large cells but peak at intermediate cell sizes. The maximum nutrient uptake rate scales isometrically with cell volume and superisometrically with the minimum nutrient quota. The unimodal size scaling of phytoplankton growth arises from ataxonomic, size-dependent trade-off processes related to nutrient requirement, acquisition, and use. The superior ability of intermediate-size cells to exploit high nutrient concentrations explains their biomass dominance during blooms. Biogeographic patterns in phytopla...

...read moreread less

325 citations

Cites background or methods from "Unimodal size scaling of phytoplank..."

...…expressed as a fraction of photosynthetically fixed carbon) are relatively low (<5% for exudation and <15% for respiration) in exponentially growing algal cultures and, in addition, remain relatively constant across the whole cell size range (López-Sandoval et al. 2013, Marañón et al. 2013)....
[...]
...In contrast, the time required to consume all initial nutrients by equally dense batch cultures is relatively similar and varies only by a factor of 2–3 across a cell size range of 0.1–106 μm3 (Marañón et al. 2013)....
[...]
...Some evidence also suggests that the carbon-to-nitrogen ratio tends to be lower in the smallest phytoplankton (Raven 1994, Marañón et al. 2013)....
[...]
...The determination, following standardized protocols, of maximum nitrogen uptake (VmaxN) in 22 species spanning more than seven orders of magnitude in cell size (Figure 3a) has revealed that nutrient uptake in phytoplankton scales isometrically with cell volume (Marañón et al. 2013)....
[...]
...…however, unimodality does not seem to arise from changes in cell organization (e.g., a transition from prokaryotes to eukaryotes), because the decrease in growth rate with decreasing cell size is also observed in the smallest eukaryotic algae (Bec et al. 2008, Marañón et al. 2013) (Figure 2c,d)....
[...]

Journal Article•DOI•

Marine mixotrophy increases trophic transfer efficiency, mean organism size, and vertical carbon flux

[...]

Ben A. Ward¹, Michael J. Follows²•Institutions (2)

University of Bristol¹, Massachusetts Institute of Technology²

15 Mar 2016-Proceedings of the National Academy of Sciences of the United States of America

TL;DR: This work removes the strict distinction between phytoplankton and zooplankon from a global model of the marine plankton food web and allows the emergence of a realistic trophic network with increased fidelity to empirical estimates of plankton community structure and elemental stoichiometry.

...read moreread less

Abstract: Mixotrophic plankton, which combine the uptake of inorganic resources and the ingestion of living prey, are ubiquitous in marine ecosystems, but their integrated biogeochemical impacts remain unclear. We address this issue by removing the strict distinction between phytoplankton and zooplankton from a global model of the marine plankton food web. This simplification allows the emergence of a realistic trophic network with increased fidelity to empirical estimates of plankton community structure and elemental stoichiometry, relative to a system in which autotrophy and heterotrophy are mutually exclusive. Mixotrophy enhances the transfer of biomass to larger sizes classes further up the food chain, leading to an approximately threefold increase in global mean organism size and an ∼35% increase in sinking carbon flux.

...read moreread less

214 citations

Journal Article•DOI•

Growth Rates of Microbes in the Oceans

[...]

David L. Kirchman¹•Institutions (1)

University of Delaware¹

08 Jan 2016-Annual Review of Marine Science

TL;DR: Data from 16S rRNA and other approaches are used to speculate about the growth rate and the life history strategy of SAR11, the most abundant clade of heterotrophic bacteria in the oceans, and these strategies are explored using genomic data.

...read moreread less

Abstract: A microbe's growth rate helps to set its ecological success and its contribution to food web dynamics and biogeochemical processes. Growth rates at the community level are constrained by biomass and trophic interactions among bacteria, phytoplankton, and their grazers. Phytoplankton growth rates are approximately 1 d−1, whereas most heterotrophic bacteria grow slowly, close to 0.1 d−1; only a few taxa can grow ten times as fast. Data from 16S rRNA and other approaches are used to speculate about the growth rate and the life history strategy of SAR11, the most abundant clade of heterotrophic bacteria in the oceans. These strategies are also explored using genomic data. Although the methods and data are imperfect, the available data can be used to set limits on growth rates and thus on the timescale for changes in the composition and structure of microbial communities.

...read moreread less

193 citations

Journal Article•DOI•

Characteristic Sizes of Life in the Oceans, from Bacteria to Whales*

[...]

Ken Haste Andersen¹, Terje Berge², Rodrigo J. Gonçalves, Martin Hartvig³, Martin Hartvig², Martin Hartvig¹, Jan Heuschele¹, Samuel Hylander¹, Samuel Hylander⁴, Nis Sand Jacobsen¹, Christian Lindemann¹, Erik A. Martens², Erik A. Martens¹, Anna B. Neuheimer⁵, Anna B. Neuheimer², Anna B. Neuheimer¹, Karin H. Olsson¹, Artur Palacz¹, A. E. F. Prowe¹, A. E. F. Prowe⁶, Julie Sainmont¹, Sachia J. Traving², André W. Visser¹, Navish Wadhwa¹, Thomas Kiørboe¹ - Show less +21 more•Institutions (6)

Technical University of Denmark¹, University of Copenhagen², University of Göttingen³, Linnaeus University⁴, University of Hawaii⁵, Leibniz Institute of Marine Sciences⁶

08 Jan 2016-Annual Review of Marine Science

TL;DR: This work collate and review data on size-based scaling laws for resource acquisition, mobility, sensory range, and progeny size for all pelagic marine life, from bacteria to whales, and divides life in the ocean into seven major realms based on trophic strategy, physiology, and life history strategy.

...read moreread less

Abstract: The size of an individual organism is a key trait to characterize its physiology and feeding ecology. Size-based scaling laws may have a limited size range of validity or undergo a transition from one scaling exponent to another at some characteristic size. We collate and review data on size-based scaling laws for resource acquisition, mobility, sensory range, and progeny size for all pelagic marine life, from bacteria to whales. Further, we review and develop simple theoretical arguments for observed scaling laws and the characteristic sizes of a change or breakdown of power laws. We divide life in the ocean into seven major realms based on trophic strategy, physiology, and life history strategy. Such a categorization represents a move away from a taxonomically oriented description toward a trait-based description of life in the oceans. Finally, we discuss life forms that transgress the simple size-based rules and identify unanswered questions.

...read moreread less

180 citations

Journal Article•DOI•

Industrial-strength ecology: trade-offs and opportunities in algal biofuel production

[...]

Jonathan B. Shurin¹, Rachel L. Abbott², Rachel L. Abbott¹, Michael S. Deal¹, Garfield T. Kwan¹, Elena Litchman³, Robert C. McBride, Shovon Mandal¹, Val H. Smith⁴ - Show less +5 more•Institutions (4)

University of California, San Diego¹, Cornell University², Michigan State University³, University of Kansas⁴

01 Nov 2013-Ecology Letters

TL;DR: It is argued that a community engineering approach that manages microalgal diversity, species composition and environmental conditions may lead to more robust and productive biofuel ecosystems.

...read moreread less

Abstract: Microalgae represent one of the most promising groups of candidate organisms for replacing fossil fuels with contemporary primary production as a renewable source of energy. Algae can produce many times more biomass per unit area than terrestrial crop plants, easing the competing demands for land with food crops and native ecosystems. However, several aspects of algal biology present unique challenges to the industrial-scale aquaculture of photosynthetic microorganisms. These include high susceptibility to invading aquatic consumers and weeds, as well as prodigious requirements for nutrients that may compete with the fertiliser demands of other crops. Most research on algal biofuel technologies approaches these problems from a cellular or genetic perspective, attempting either to engineer or select algal strains with particular traits. However, inherent functional trade-offs may limit the capacity of genetic selection or synthetic biology to simultaneously optimise multiple functional traits for biofuel productivity and resilience. We argue that a community engineering approach that manages microalgal diversity, species composition and environmental conditions may lead to more robust and productive biofuel ecosystems. We review evidence for trade-offs, challenges and opportunities in algal biofuel cultivation with a goal of guiding research towards intensifying bioenergy production using established principles of community and ecosystem ecology.

...read moreread less

175 citations

1
2
3
4
…
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
61

Collapse

References

PDF

Open Access

More filters

Journal Article•DOI•

Toward a metabolic theory of ecology

[...]

James H. Brown¹, James H. Brown², James F. Gillooly¹, Andrew P. Allen¹, Van M. Savage³, Van M. Savage², Geoffrey B. West³, Geoffrey B. West² - Show less +4 more•Institutions (3)

University of New Mexico¹, Santa Fe Institute², Los Alamos National Laboratory³

01 Jul 2004-Ecology

TL;DR: This work has developed a quantitative theory for how metabolic rate varies with body size and temperature, and predicts how metabolic theory predicts how this rate controls ecological processes at all levels of organization from individuals to the biosphere.

...read moreread less

Abstract: Metabolism provides a basis for using first principles of physics, chemistry, and biology to link the biology of individual organisms to the ecology of populations, communities, and ecosystems. Metabolic rate, the rate at which organisms take up, transform, and expend energy and materials, is the most fundamental biological rate. We have developed a quantitative theory for how metabolic rate varies with body size and temperature. Metabolic theory predicts how metabolic rate, by setting the rates of resource uptake from the environment and resource allocation to survival, growth, and reproduction, controls ecological processes at all levels of organization from individuals to the biosphere. Examples include: (1) life history attributes, including devel- opment rate, mortality rate, age at maturity, life span, and population growth rate; (2) population interactions, including carrying capacity, rates of competition and predation, and patterns of species diversity; and (3) ecosystem processes, including rates of biomass production and respiration and patterns of trophic dynamics. Data compiled from the ecological literature strongly support the theoretical predictions. Even- tually, metabolic theory may provide a conceptual foundation for much of ecology, just as genetic theory provides a foundation for much of evolutionary biology.

...read moreread less

6,017 citations

"Unimodal size scaling of phytoplank..." refers background or methods in this paper

...The decrease in maximum intrinsic population growth rate (lmax) and mass-specific metabolic rates (RM) with increasing body size (M) is one of the most pervasive patterns in biology (Fenchel 1974) and has major implications for the ecology and evolution of all organisms (Brown et al. 2004)....
[...]
...We used cultures of 22 species of marine phytoplankton from five phyla, ranging from 0.1 to 106 lm3 in cell volume (Vcell), to determine experimentally the size dependence of growth, metabolic rate, elemental stoichiometry and nutrient uptake....
[...]
...Because population growth requires the synthesis of new biomass, lmax is expected to be closely related to metabolic rate (Fenchel 1974; Brown et al. 2004)....
[...]

Book•

Recherches sur la croissance des cultures bactériennes

[...]

Jacques Monod, Jules Jean Baptiste Vincent Bordet

01 Jan 1942

1,360 citations

"Unimodal size scaling of phytoplank..." refers background in this paper

...In contrast, small cells have a comparatively small storage capacity and therefore their growth is tightly linked to the rate of external nutrient supply, as represented by Monod’s model of microbial growth (Monod 1942)....
[...]

Journal Article•DOI•

Phytoplankton in a changing world: cell size and elemental stoichiometry

[...]

Zoe V. Finkel¹, John Beardall², Kevin J. Flynn³, Antonietta Quigg⁴, Antonietta Quigg⁵, T. Alwyn V. Rees⁶, John A. Raven⁷ - Show less +3 more•Institutions (7)

Mount Allison University¹, Monash University², Swansea University³, Texas A&M University⁴, Texas A&M University at Galveston⁵, University of Auckland⁶, Scottish Crop Research Institute⁷

01 Jan 2010-Journal of Plankton Research

TL;DR: It is suggested that cell size and elemental stoichiometry are promising ecophysiological traits for modelling and tracking changes in phytoplankton community structure in response to climate change.

...read moreread less

Abstract: Global increases in atmospheric CO2 and temperature are associated with changes in ocean chemistry and circulation, altering light and nutrient regimes. Resulting changes in phytoplankton community structure are expected to have a cascading effect on primary and export production, food web dynamics and the structure of the marine food web as well the biogeochemical cycling of carbon and bio-limiting elements in the sea. A review of current literature indicates cell size and elemental stoichiometry often respond predictably to abiotic conditions and follow biophysical rules that link environmental conditions to growth rates, and growth rates to food web interactions, and consequently to the biogeochemical cycling of elements. This suggests that cell size and elemental stoichiometry are promising ecophysiological traits for modelling and tracking changes in phytoplankton community structure in response to climate change. In turn, these changes are expected to have further impacts on phytoplankton community structure through as yet poorly understood secondary processes associated with trophic dynamics.

...read moreread less

919 citations

Additional excerpts

...Ecology Letters (2013) 16: 371–379...
[...]

Journal Article•DOI•

Some thoughts on nutrient limitation in algae1

[...]

M. R. Droop

01 Sep 1973-Journal of Phycology

TL;DR: An empirical relation relating specific growth, rate in steady state systems to nutrient status with respect to more than one nutrient simultaneously is proposed, based on 3 experimentally verifiable postulates.

...read moreread less

Abstract: SUMMARY An empirical relation relating specific growth, rate in steady state systems to nutrient status with respect to more than one nutrient simultaneously is proposed, based on 3 experimentally verifiable postulates: (1) that uptake depends on the external substrate concentration; (2) that growth depends on the interval substrate concentration; and (3) in a steady state system specific rate of uptake (in the absence of significant, excretion) is necessarily the product of the specific growth rate and internal substrate concentration. The implications of this model are discussed in particular in respect to the concept of luxury consumption and Liebig's law of minimum. Some aspects of uptake in transient situations are also discussed.

...read moreread less

817 citations

"Unimodal size scaling of phytoplank..." refers background in this paper

...The variability in Q over time is given by the balance between nutrient uptake rate (V) and nutrient assimilation (Nassim = l Q) into biomass (Droop 1973): dQ dt ¼ V lQ ð2Þ V depends on external nutrient concentration and the nutrient halfsaturation constant, following Michaelis–Menten kinetics....
[...]
...The variability in Q over time is given by the balance between nutrient uptake rate (V) and nutrient assimilation (Nassim = l Q) into biomass (Droop 1973):...
[...]
...The high storage capacity of the largest cells allows them to uncouple their growth from the dynamics of external nutrient supply, a scenario described by Droop’s model (Droop 1973)....
[...]
...…be described as a function of the cellular quota of the limiting nutrient (Q) and the minimum nutrient quota (Qmin), below which cells cannot grow (Droop 1973): 1Departamento de Ecolog ıa y Biolog ıa Animal, Universidad de Vigo, 36210, Vigo, Spain 2Departamento de Ecolog ıa, Universidad de M…...
[...]
...Following Droop’s model, and assuming there is no mortality, phytoplankton growth rate (l) can be described as a function of the cellular quota of the limiting nutrient (Q) and the minimum nutrient quota (Qmin), below which cells cannot grow (Droop 1973):...
[...]

Journal Article•DOI•

Global Biodiversity, Biochemical Kinetics, and the Energetic-Equivalence Rule

[...]

Andrew P. Allen¹, James H. Brown¹, James F. Gillooly¹•Institutions (1)

University of New Mexico¹

30 Aug 2002-Science

TL;DR: In this paper, the authors show that the average energy flux of populations is temperature invariant and derive a model that quantitatively predicts how species diversity increases with environmental temperature, supported by data for terrestrial, freshwater, and marine taxa along latitudinal and elevational gradients.

...read moreread less

Abstract: The latitudinal gradient of increasing biodiversity from poles to equator is one of the most prominent but least understood features of life on Earth. Here we show that species diversity can be predicted from the biochemical kinetics of metabolism. We first demonstrate that the average energy flux of populations is temperature invariant. We then derive a model that quantitatively predicts how species diversity increases with environmental temperature. Predictions are supported by data for terrestrial, freshwater, and marine taxa along latitudinal and elevational gradients. These results establish a thermodynamic basis for the regulation of species diversity and the organization of ecological communities.

...read moreread less

785 citations

"Unimodal size scaling of phytoplank..." refers methods in this paper

...According to models based on the kinetics of biochemical reactions, metabolic rate is a major factor controlling diversity (Allen et al. 2002) and rate of speciation (Allen et al....
[...]
...According to models based on the kinetics of biochemical reactions, metabolic rate is a major factor controlling diversity (Allen et al. 2002) and rate of speciation (Allen et al. 2006)....
[...]