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Physiological and morphological scaling enables gigantism in pelagic protists

Physiological and morphological scaling enables gigantism in pelagic protists
Physiological and morphological scaling enables gigantism in pelagic protists
Planktonic foraminifera are pelagic protists frequently used to study paleoenvironmental change. Many planktonic foraminifera, like other taxa in Rhizaria, reach gigantic proportions relative to other pelagic protists (> 600 μm), placing them in a size class dominated by metazoans. Here, we combine new and existing respiration rate measurements, micro-CT scans, and test size measurements to investigate allometric scaling of metabolic rates, relative biomass density, and mixotrophy in contributing to the ability of planktonic foraminifera to reach large sizes. Respiration rate increases with foraminiferal biovolume with a slope of 0.51 ± 0.18. This allometric scaling slope is lower than those reported in other plankton. Further, the basal respiration rates for planktonic foraminifera exceed those of other organisms in their size class when probable biomass, rather than test volume, is considered. Using the allometric regression on a published database of modern planktonic foraminifera from the Atlantic Ocean, we estimate that gigantic individuals account for 15.3–26.1% of foraminiferal community respiration in temperate and tropical/subtropical latitudes, despite making up only 4.5–8.3% of individuals. We hypothesize that shallow scaling of test size with metabolism and of test size to actual biomass is the key factor allowing for gigantism in planktonic foraminifera. Having a large test and broadcasting rhizopodial networks increases the functional volume of the organism, allowing higher passive prey encounter rates to support the elevated metabolic rates in planktonic foraminifera. Mixotrophy may act as a mitigating factor for metabolic challenges at low latitudes, accounting for the presence of large populations of giant, predominately mixotrophic Rhizarians in these assemblages.
0024-3590
461-476
Burke, Janet E.
826d61d1-4a1d-4ad0-afa5-f646edd9e3c7
Elder, Leanne E.
98ac4665-b68a-4fc0-896b-6fd2beca8f40
Maas, Amy E.
1b4c7577-2234-4d03-83b4-db53d82bc686
Gaskell, Daniel E.
bc30f812-ffcb-4653-aca3-46a96833c8c1
Clark, Elizabeth G.
8cc964d3-ff1e-414b-b3de-91c368aec536
Hsiang, Allison Y.
4d4d6e58-660d-49cd-8be2-ed3d7bf6039e
Foster, Gavin L.
fbaa7255-7267-4443-a55e-e2a791213022
Hull, Pincelli M.
071e549a-6172-448b-b339-9359c495c03c
Burke, Janet E.
826d61d1-4a1d-4ad0-afa5-f646edd9e3c7
Elder, Leanne E.
98ac4665-b68a-4fc0-896b-6fd2beca8f40
Maas, Amy E.
1b4c7577-2234-4d03-83b4-db53d82bc686
Gaskell, Daniel E.
bc30f812-ffcb-4653-aca3-46a96833c8c1
Clark, Elizabeth G.
8cc964d3-ff1e-414b-b3de-91c368aec536
Hsiang, Allison Y.
4d4d6e58-660d-49cd-8be2-ed3d7bf6039e
Foster, Gavin L.
fbaa7255-7267-4443-a55e-e2a791213022
Hull, Pincelli M.
071e549a-6172-448b-b339-9359c495c03c

Burke, Janet E., Elder, Leanne E., Maas, Amy E., Gaskell, Daniel E., Clark, Elizabeth G., Hsiang, Allison Y., Foster, Gavin L. and Hull, Pincelli M. (2025) Physiological and morphological scaling enables gigantism in pelagic protists. Limnology and Oceanography, 70 (2), 461-476. (doi:10.1002/lno.12770).

Record type: Article

Abstract

Planktonic foraminifera are pelagic protists frequently used to study paleoenvironmental change. Many planktonic foraminifera, like other taxa in Rhizaria, reach gigantic proportions relative to other pelagic protists (> 600 μm), placing them in a size class dominated by metazoans. Here, we combine new and existing respiration rate measurements, micro-CT scans, and test size measurements to investigate allometric scaling of metabolic rates, relative biomass density, and mixotrophy in contributing to the ability of planktonic foraminifera to reach large sizes. Respiration rate increases with foraminiferal biovolume with a slope of 0.51 ± 0.18. This allometric scaling slope is lower than those reported in other plankton. Further, the basal respiration rates for planktonic foraminifera exceed those of other organisms in their size class when probable biomass, rather than test volume, is considered. Using the allometric regression on a published database of modern planktonic foraminifera from the Atlantic Ocean, we estimate that gigantic individuals account for 15.3–26.1% of foraminiferal community respiration in temperate and tropical/subtropical latitudes, despite making up only 4.5–8.3% of individuals. We hypothesize that shallow scaling of test size with metabolism and of test size to actual biomass is the key factor allowing for gigantism in planktonic foraminifera. Having a large test and broadcasting rhizopodial networks increases the functional volume of the organism, allowing higher passive prey encounter rates to support the elevated metabolic rates in planktonic foraminifera. Mixotrophy may act as a mitigating factor for metabolic challenges at low latitudes, accounting for the presence of large populations of giant, predominately mixotrophic Rhizarians in these assemblages.

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Revised_PF_Scaling_2024_Resubmit_Manuscript_clean - Accepted Manuscript
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Accepted/In Press date: 29 November 2024
Published date: 17 January 2025
Additional Information: Publisher Copyright: © 2025 Association for the Sciences of Limnology and Oceanography.

Identifiers

Local EPrints ID: 498039
URI: http://eprints.soton.ac.uk/id/eprint/498039
ISSN: 0024-3590
PURE UUID: ebd42975-d694-4287-8b40-1a5d2a1e0924
ORCID for Gavin L. Foster: ORCID iD orcid.org/0000-0003-3688-9668

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Date deposited: 06 Feb 2025 17:38
Last modified: 14 May 2025 01:44

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Contributors

Author: Janet E. Burke
Author: Leanne E. Elder
Author: Amy E. Maas
Author: Daniel E. Gaskell
Author: Elizabeth G. Clark
Author: Allison Y. Hsiang
Author: Gavin L. Foster ORCID iD
Author: Pincelli M. Hull

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