Reef-building corals farm and feed on their photosynthetic symbionts

Jörg Wiedenmann, Cecilia D’Angelo, M. Loreto Mardones, Shona Moore, Cassandra E. Benkwitt, Nicholas A.J. Graham, Bastian Hambach, Paul A. Wilson, James Vanstone, Gal Eyal, Or Ben-Zvi, Yossi Loya, Amatzia Genin

Research output: Contribution to journalArticlepeer-review

41 Scopus citations

Abstract

Coral reefs are highly diverse ecosystems that thrive in nutrient-poor waters, a phenomenon frequently referred to as the Darwin paradox1. The energy demand of coral animal hosts can often be fully met by the excess production of carbon-rich photosynthates by their algal symbionts2,3. However, the understanding of mechanisms that enable corals to acquire the vital nutrients nitrogen and phosphorus from their symbionts is incomplete4–9. Here we show, through a series of long-term experiments, that the uptake of dissolved inorganic nitrogen and phosphorus by the symbionts alone is sufficient to sustain rapid coral growth. Next, considering the nitrogen and phosphorus budgets of host and symbionts, we identify that these nutrients are gathered through symbiont ‘farming’ and are translocated to the host by digestion of excess symbiont cells. Finally, we use a large-scale natural experiment in which seabirds fertilize some reefs but not others, to show that the efficient utilization of dissolved inorganic nutrients by symbiotic corals established in our laboratory experiments has the potential to enhance coral growth in the wild at the ecosystem level. Feeding on symbionts enables coral animals to tap into an important nutrient pool and helps to explain the evolutionary and ecological success of symbiotic corals in nutrient-limited waters.

Original languageEnglish
Pages (from-to)1018-1024
Number of pages7
JournalNature
Volume620
Issue number7976
DOIs
StatePublished - 23 Aug 2023
Externally publishedYes

Bibliographical note

Publisher Copyright:
© 2023, The Author(s).

Funding

Funding was provided by NERC (NE/T001364/1), Infrastructure Improvement Funding (University of Southampton), the Royal Society (URF\R\201029) and the Bertarelli Foundation contributing to the Bertarelli Programme in Marine Science. Fieldwork was conducted under permit numbers 0004SE18, 0001SE19, 0003SE20, and 0002SE21. We thank G. Clarke and R. Robinson for their support in maintaining the Experimental Coral Aquarium Facility at the University of Southampton; M. Cooper for the analysis of P content; M. Wilding for technical help with the stable isotope analyses; J. Gittins for support of the molecular work of J.V.; and C. Dumousseaud for dissolved inorganic N and PO concentration analysis. We acknowledge the work of postgraduate (R. Gracie) and undergraduate (M.-M. Baker and N. Burt) students who analysed subsets of the data for their dissertations during the COVID 19-related lockdown. 4 Funding was provided by NERC (NE/T001364/1), Infrastructure Improvement Funding (University of Southampton), the Royal Society (URF\R\201029) and the Bertarelli Foundation contributing to the Bertarelli Programme in Marine Science. Fieldwork was conducted under permit numbers 0004SE18, 0001SE19, 0003SE20, and 0002SE21. We thank G. Clarke and R. Robinson for their support in maintaining the Experimental Coral Aquarium Facility at the University of Southampton; M. Cooper for the analysis of P content; M. Wilding for technical help with the stable isotope analyses; J. Gittins for support of the molecular work of J.V.; and C. Dumousseaud for dissolved inorganic N and PO4 concentration analysis. We acknowledge the work of postgraduate (R. Gracie) and undergraduate (M.-M. Baker and N. Burt) students who analysed subsets of the data for their dissertations during the COVID 19-related lockdown.

FundersFunder number
Fondation Bertarelli0002SE21, 0003SE20, 0004SE18, 0001SE19
Natural Environment Research CouncilNE/T001364/1
Royal SocietyURF\R\201029
University of Southampton

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