Benthic foraminifera and gromiids from oxygen-depleted environments – survival strategies, biogeochemistry and trophic interactions

Abstract. The oceans are losing oxygen (O2), and oxygen minimum zones are expanding due to climate warming (lower O2 solubility) and eutrophication related to agriculture. This trend is challenging for most marine taxa that are not well adapted to O2 depletion. For other taxa this trend might be advantageous because they can withstand low O2 concentrations or thrive under O2-depleted or even anoxic conditions. Benthic foraminifera are a group of protists that include taxa with adaptations to partly extreme environmental conditions. Several species possess adaptations to O2 depletion that are rare amongst eukaryotes, and these species might benefit from ongoing ocean deoxygenation. In addition, since some foraminifera can calcify even under anoxic conditions, they are important archives for paleoceanographic reconstruction in O2-depleted environments. This paper reviews the current state of knowledge about foraminifera from low-O2 environments. Recent advances in our understanding of specific survival strategies of foraminifera to withstand O2 depletion are summarized and discussed. These adaptations include an anaerobic metabolism, heterotrophic denitrification, symbiosis with bacteria, kleptoplasty and dormancy and have a strong impact on their preferred microhabitat in the sediments, especially the ability of some benthic foraminiferal species to denitrify. Benthic foraminifera also differ regarding their trophic strategies, which has an additional impact on the selection of their microhabitat. For example, some species are strict herbivores that feed exclusively on fresh phytodetritus and live close to the sediment surface, while some species are non-selective detrivores that occupy intermediate to deep infaunal habitats. There is evidence that foraminifers have the capacity to undergo phagocytosis, even under anoxia, and some foraminiferal species which can withstand low-O2 conditions seem to prey on meiofauna. Also, due to their high abundances in O2-depleted environments and their metabolic adaptations, benthic foraminifera are key players in marine nutrient cycling, especially within the marine N and P cycles. This review summarizes the denitrification rates for the species that are known to denitrify and the intracellular nitrate concentrations of the species that are known to intracellularly store nitrate. Finally, equations are provided that can be used to estimate the intracellular nutrient storage and denitrification rates of foraminifera and might be integrated into biogeochemical models.