Implications for the mesopelagic microbial gardening hypothesis as determined by experimental fragmentation of Antarctic krill fecal pellets

Detritivores need to upgrade their food to increase its nutritional value. One method is to fragment detritus promoting the colonization of nutrient‐rich microbes, which consumers then ingest along with the detritus; so‐called microbial gardening. Observations and numerical models of the detritus‐do...

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Published in:Ecology and Evolution
Main Authors: Cavan, EL, Kawaguchi, S, Boyd, PW
Format: Article in Journal/Newspaper
Language:English
Published: John Wiley & Sons Ltd 2021
Subjects:
Online Access:https://eprints.utas.edu.au/37158/
https://eprints.utas.edu.au/37158/1/142964%20-%20Implications%20for%20the%20mesopelagic%20microbial%20gardening%20hypothesis%20as%20determined.pdf
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spelling ftunivtasmania:oai:eprints.utas.edu.au:37158 2023-05-15T13:31:53+02:00 Implications for the mesopelagic microbial gardening hypothesis as determined by experimental fragmentation of Antarctic krill fecal pellets Cavan, EL Kawaguchi, S Boyd, PW 2021 application/pdf https://eprints.utas.edu.au/37158/ https://eprints.utas.edu.au/37158/1/142964%20-%20Implications%20for%20the%20mesopelagic%20microbial%20gardening%20hypothesis%20as%20determined.pdf en eng John Wiley & Sons Ltd https://eprints.utas.edu.au/37158/1/142964%20-%20Implications%20for%20the%20mesopelagic%20microbial%20gardening%20hypothesis%20as%20determined.pdf Cavan, EL orcid:0000-0003-1099-6705 , Kawaguchi, S and Boyd, PW orcid:0000-0001-7850-1911 2021 , 'Implications for the mesopelagic microbial gardening hypothesis as determined by experimental fragmentation of Antarctic krill fecal pellets' , Ecology and Evolution, vol. 11, no. 2 , pp. 1023-1036 , doi:10.1002/ece3.7119 <http://dx.doi.org/10.1002/ece3.7119>. carbon sink fecal pellets krill mesopelagic zone microbial gardening zooplankton Article PeerReviewed 2021 ftunivtasmania https://doi.org/10.1002/ece3.7119 2021-09-13T22:20:35Z Detritivores need to upgrade their food to increase its nutritional value. One method is to fragment detritus promoting the colonization of nutrient‐rich microbes, which consumers then ingest along with the detritus; so‐called microbial gardening. Observations and numerical models of the detritus‐dominated ocean mesopelagic zone have suggested microbial gardening by zooplankton is a fundamental process in the ocean carbon cycle leading to increased respiration of carbon‐rich detritus. However, no experimental evidence exists to demonstrate that microbial respiration rates are higher on recently fragmented sinking detrital particles. Using aquaria‐reared Antarctic krill fecal pellets, we showed fragmentation increased microbial particulate organic carbon (POC) turnover by 1.9×, but only on brown fecal pellets, formed from the consumption of other pellets. Microbial POC turnover on un‐ and fragmented green fecal pellets, formed from consuming fresh phytoplankton, was equal. Thus, POC content, fragmentation, and potentially nutritional value together drive POC turnover rates. Mesopelagic microbial gardening could be a risky strategy, as the dominant detrital food source is settling particles; even though fragmentation decreases particle size and sinking rate, it is unlikely that an organism would remain with the particle long enough to nutritionally benefit from attached microbes. We propose “communal gardening” occurs whereby additional mesopelagic organisms nearby or below the site of fragmentation consume the particle and the colonized microbes. To determine how fragmentation impacts the remineralization of sinking carbon‐rich detritus and to parameterize microbial gardening in mesopelagic carbon models, three key metrics from further controlled experiments and observations are needed; how particle composition (here, pellet color/krill diet) impacts the response of microbes to the fragmentation of particles; the nutritional benefit to zooplankton from ingesting microbes after fragmentation along with identification of which essential nutrients are being targeted; how both these factors vary between physical (shear) and biological particle fragmentation. Article in Journal/Newspaper Antarc* Antarctic Antarctic Krill University of Tasmania: UTas ePrints Antarctic Ecology and Evolution 11 2 1023 1036
institution Open Polar
collection University of Tasmania: UTas ePrints
op_collection_id ftunivtasmania
language English
topic carbon sink
fecal pellets
krill
mesopelagic zone
microbial gardening
zooplankton
spellingShingle carbon sink
fecal pellets
krill
mesopelagic zone
microbial gardening
zooplankton
Cavan, EL
Kawaguchi, S
Boyd, PW
Implications for the mesopelagic microbial gardening hypothesis as determined by experimental fragmentation of Antarctic krill fecal pellets
topic_facet carbon sink
fecal pellets
krill
mesopelagic zone
microbial gardening
zooplankton
description Detritivores need to upgrade their food to increase its nutritional value. One method is to fragment detritus promoting the colonization of nutrient‐rich microbes, which consumers then ingest along with the detritus; so‐called microbial gardening. Observations and numerical models of the detritus‐dominated ocean mesopelagic zone have suggested microbial gardening by zooplankton is a fundamental process in the ocean carbon cycle leading to increased respiration of carbon‐rich detritus. However, no experimental evidence exists to demonstrate that microbial respiration rates are higher on recently fragmented sinking detrital particles. Using aquaria‐reared Antarctic krill fecal pellets, we showed fragmentation increased microbial particulate organic carbon (POC) turnover by 1.9×, but only on brown fecal pellets, formed from the consumption of other pellets. Microbial POC turnover on un‐ and fragmented green fecal pellets, formed from consuming fresh phytoplankton, was equal. Thus, POC content, fragmentation, and potentially nutritional value together drive POC turnover rates. Mesopelagic microbial gardening could be a risky strategy, as the dominant detrital food source is settling particles; even though fragmentation decreases particle size and sinking rate, it is unlikely that an organism would remain with the particle long enough to nutritionally benefit from attached microbes. We propose “communal gardening” occurs whereby additional mesopelagic organisms nearby or below the site of fragmentation consume the particle and the colonized microbes. To determine how fragmentation impacts the remineralization of sinking carbon‐rich detritus and to parameterize microbial gardening in mesopelagic carbon models, three key metrics from further controlled experiments and observations are needed; how particle composition (here, pellet color/krill diet) impacts the response of microbes to the fragmentation of particles; the nutritional benefit to zooplankton from ingesting microbes after fragmentation along with identification of which essential nutrients are being targeted; how both these factors vary between physical (shear) and biological particle fragmentation.
format Article in Journal/Newspaper
author Cavan, EL
Kawaguchi, S
Boyd, PW
author_facet Cavan, EL
Kawaguchi, S
Boyd, PW
author_sort Cavan, EL
title Implications for the mesopelagic microbial gardening hypothesis as determined by experimental fragmentation of Antarctic krill fecal pellets
title_short Implications for the mesopelagic microbial gardening hypothesis as determined by experimental fragmentation of Antarctic krill fecal pellets
title_full Implications for the mesopelagic microbial gardening hypothesis as determined by experimental fragmentation of Antarctic krill fecal pellets
title_fullStr Implications for the mesopelagic microbial gardening hypothesis as determined by experimental fragmentation of Antarctic krill fecal pellets
title_full_unstemmed Implications for the mesopelagic microbial gardening hypothesis as determined by experimental fragmentation of Antarctic krill fecal pellets
title_sort implications for the mesopelagic microbial gardening hypothesis as determined by experimental fragmentation of antarctic krill fecal pellets
publisher John Wiley & Sons Ltd
publishDate 2021
url https://eprints.utas.edu.au/37158/
https://eprints.utas.edu.au/37158/1/142964%20-%20Implications%20for%20the%20mesopelagic%20microbial%20gardening%20hypothesis%20as%20determined.pdf
geographic Antarctic
geographic_facet Antarctic
genre Antarc*
Antarctic
Antarctic Krill
genre_facet Antarc*
Antarctic
Antarctic Krill
op_relation https://eprints.utas.edu.au/37158/1/142964%20-%20Implications%20for%20the%20mesopelagic%20microbial%20gardening%20hypothesis%20as%20determined.pdf
Cavan, EL orcid:0000-0003-1099-6705 , Kawaguchi, S and Boyd, PW orcid:0000-0001-7850-1911 2021 , 'Implications for the mesopelagic microbial gardening hypothesis as determined by experimental fragmentation of Antarctic krill fecal pellets' , Ecology and Evolution, vol. 11, no. 2 , pp. 1023-1036 , doi:10.1002/ece3.7119 <http://dx.doi.org/10.1002/ece3.7119>.
op_doi https://doi.org/10.1002/ece3.7119
container_title Ecology and Evolution
container_volume 11
container_issue 2
container_start_page 1023
op_container_end_page 1036
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