Fixed-Nitrogen Loss Associated with Sinking Zooplankton Carcasses in a Coastal Oxygen Minimum Zone (Golfo Dulce, Costa Rica)

Peter Stief,Bo Thamdrup,Ronnie N. Glud,Álvaro Morales-Ramírez,Ann Sofie B. Lundgaard

doi:10.3389/fmars.2017.00152

Abstract

Oxygen minimum zones (OMZs) in the ocean are of key importance for pelagic fixed-nitrogen loss (N-loss) through microbial denitrification and anaerobic ammonium oxidation (anammox). Recent studies document that zooplankton is surprisingly abundant in and around OMZs and that the microbial community associated with carcasses of a large copepod species mediates denitrification. Here, we investigate the complex N-cycling associated with sinking zooplankton carcasses exposed to the steep O2 gradient in a coastal OMZ (Golfo Dulce, Costa Rica). 15N-stable-isotope enrichment experiments revealed that the carcasses of abundant copepods and ostracods provide anoxic microbial hotspots in the pelagic zone by hosting intense anaerobic N-cycle activities even in the presence of ambient O2. Carcass-associated anaerobic N-cycling was clearly dominated by dissimilatory nitrate reduction to ammonium (DNRA) at up to 30.8 nmol NH4+ individual-1 d-1, followed by denitrification (up to 10.8 nmol N2-N individual-1 d-1), anammox (up to 1.6 nmol N2-N individual-1 d-1), and N2O production (up to 1.2 nmol N2O-N individual-1 d-1). In contrast, anaerobic N-cycling mediated by free-living bacteria proceeded mainly through anammox and denitrification in the anoxic bottom water, which underpins the distinctive microbial metabolism associated with zooplankton carcasses. Pelagic N-loss is potentially enhanced by zooplankton carcasses both directly through N2 and N2O production, and indirectly through NH4+ production that may fuel free-living anammox bacteria. We estimate that in the hypoxic water layer of Golfo Dulce, carcass-associated N2 and N2O production enhance N-loss as much as 1.4-fold at a relative carcass abundance of 36%. In the anoxic bottom water, however, N-loss is likely enhanced only marginally due to high ambient rates and low zooplankton abundance. Thus, zooplankton carcasses may enhance N-loss mainly at the hypoxic boundaries of OMZs which are usually more extensive in open-ocean than in coastal settings. Notably, these contributions by zooplankton carcasses to pelagic N-loss remain undetected by conventional, incubation-based rate measurements.

Highlights

Marine mesozooplankton, commonly dominated by copepods, is increasingly recognized to host unique microenvironments in the pelagic macroenvironment (Tang et al, 2010)
The 15N-incubation experiments conducted under different environmental conditions imply that the relative enhancement of pelagic nitrogen loss (N-loss) by zooplankton carcasses is greatest in oxic
Anaerobic N-cycling associated with zooplankton carcasses contributes to pelagic N-loss both directly via N2 and N2O production and indirectly via NH+4 production that may fuel free-living anammox bacteria in anoxic water layers

Summary

Introduction

Commonly dominated by copepods, is increasingly recognized to host unique microenvironments in the pelagic macroenvironment (Tang et al, 2010). In pelagic ecosystems, copepods and other mesozooplankton represent vastly abundant “microbial hotspots” with unique biogeochemical features (Tang, 2005; Tang et al, 2010; Nuester et al, 2014) In this sense, zooplankters, and in particular their carcasses, resemble sinking phytodetritus aggregates that host dense microbial communities within a low-oxygen microenvironment (Ploug et al, 1997; Glud et al, 2015; Klawonn et al, 2015; Stief et al, 2016). For marine habitats of tropical and subtropical regions, relative carcass abundances as high as 20–70% (Tang et al, 2009) and 10–90% (Elliott and Tang, 2009) are reported

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