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

Emma L Cavan,Philip W Boyd,So Kawaguchi

doi:10.1002/ece3.7119

Emma L Cavan, Philip W Boyd + Show 1 more

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https://doi.org/10.1002/ece3.7119

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Abstract

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.

Highlights

Sinking detrital particulate organic carbon (POC) in the ocean is a vital sink for atmospheric carbon, without which there would be 50% more CO2 in the atmosphere than at present (Parekh et al, 2005; Volk & Hoffert, 1985)
We experimentally tested the first step in the microbial gardening hypothesis that fragmentation of sinking particles increases microbial activity and the dissolution of POC associated with smaller particles, using krill fecal pellets as a representative detrital particle
The brown pellets were mostly present in our aquaria fragmentation experiment once the phytoplankton food source had been depleted, and we propose that brown pellets occur due to krill feeding on other pellets when fresh algal concentrations are low (Figure 3) as is the case in the mesopelagic (Figure 4)

Summary

Introduction

Sinking detrital particulate organic carbon (POC) in the ocean is a vital sink for atmospheric carbon, without which there would be 50% more CO2 in the atmosphere than at present (Parekh et al, 2005; Volk & Hoffert, 1985). Microbes rapidly colonize smaller particles (Kiørboe, 2003; Kiørboe et al, 2002), and these microbes are rich in essential nutrients (e.g., unsaturated fatty acids) (Okuyama et al, 2008; Russell & Nichols, 1999; Shulse & Allen, 2010) some of which zooplankton cannot synthesize (De Carvalho & Caramujo, 2012; Moi et al, 2018; Okuyama et al, 2008) This process of fragmentation to nurture consume nutritionally enriched food (i.e., microbes plus detrital POC) is termed microbial gardening (Fenchel, 1970; Mayor et al, 2014). Such gardening can be seen as a gamble by choosing to fragment rather than ingest food in the food-poor mesopelagic (Iversen, 2014)

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