Evidence that dimethyl sulfide facilitates a tritrophic mutualism between marine primary producers and top predators

Abstract

Tritrophic mutualistic interactions have been best studied in plantinsect systems. During these interactions, plants release volatiles in response to herbivore damage, which, in turn, facilitates predation on primary consumers or benefits the primary producer by providing nutrients. Here we explore a similar interaction in the Southern Ocean food web, where soluble iron limits primary productivity. Dimethyl sulfide has been studied in the context of global climate regulation and is an established foraging cue for marine top predators. We present evidence that procellariiform seabird species that use dimethyl sulfide as a foraging cue selectively forage on phytoplankton grazers. Their contribution of beneficial iron recycled to marine phytoplankton via excretion suggests a chemically mediated link between marine top predators and oceanic primary production. Many plant species interact with carnivores to gain protection from herbivory. Such mutualistic tritrophic interactions have been studied extensively in plant-insect systems, and are frequently mediated by plant volatiles released in response to insect feeding (1). One example that has received detailed study is the interaction between the phytophagous twospotted spider mite Tetranychus urticae, the lima bean plant Phaseolus lunatus, and the predatory mite Phytoseiulus persimilis (2, 3). In this model system, grazing by the herbivorous spider mite has been demonstrated to elicit a cascade of biochemical reactions within the afflicted plants, stimulating the release of a suite of volatile terpenoids such as (E)-4,8-dimethyl-l,3, 7-nonatriene, (E)-β-ocimene, and (E,E)- 4,8,12-trimethyl-1,3,7, 11-tridecatetraene (3). These volatiles attract olfactory-searching P. persimilis that prey upon herbivorous spider mites.The possibility of tritrophic mutualisms involving plant volatiles has received considerable attention in terrestrial communities (2-5); however, similar interactions have rarely been suggested for marine systems (6). Dimethyl sulfide (DMS) and its precursor dimethylsulfoniopropionate (DMSP) are well-established infochemicals in the marine environment, and as such are good candidate molecules for mediating tritrophic interactions between phytoplankton and carnivores (7-10). DMS arises as a catabolic breakdown product of DMSP, and has been studied extensively for its putative role as a global climate regulator (11). DMSP is produced by marine algae, where it has been proposed to function as an osmolyte (12) and a cryoprotectant (13). When algal cells lyse, due to biotic or abiotic stress, one of the fates of DMSP is catabolism by the enzyme DMSP lyase to DMS and acrylic acid (14-16). This process may also occur during autocatalytic cell death (17). It has been proposed that acrylic acid is the biologically salient product of this reaction due to its antimicrobial properties (18). DMS production has also been shown to increase during zooplankton grazing (14). It has been previously proposed that this phytoplankton-derived odorant is an important infochemi...

Dimethylsulfoniopropionate in corals and its interrelations with bacterial assemblages in coral surface mucus

“…Our findings contribute to the established research field on the ecological roles of DMSP, to the emergent study of microbial mediated DMSP/DMS dynamics [64] and, in the larger context, to the understanding of multi-trophic level mutualisms in marine ecosystems. [65] …”

Vision on the high seas: spatial resolution and optical sensitivity in two procellariiform seabirds with different foraging strategies

“…One of the most studied olfactory info-chemicals in the marine environment is dimethyl sulphide (DMS) (Nevitt et al, 1995;Nevitt, 2011;Savoca and Nevitt, 2014). Some procellariiform species respond to experimental DMS deployments at sea by tracking it to the source (Nevitt et al, 1995).…”

“…At the same time, other primarily surface-nesting species do not show behavioural responses to it (Nevitt et al, 1995(Nevitt et al, , 2004Van Buskirk and Nevitt, 2008). As DMS can be associated with areas of high primary productivity, DMS responsiveness is an adaptation for locating foraging hotspots by olfactory cues alone (Nevitt, 2011;Savoca and Nevitt, 2014).…”

The raison d'être of chemical ecology

“…), with ecosystem-level consequences. Specifically, the DMSmediated foraging by these pelagic sea birds is a key driver of between-ecosystem nutrient transfer: their feces are inferred to promote the retention of limiting nutrients, especially iron, in the surface waters of the nutrient-poor Southern Ocean (Savoca and Nevitt 2014). During the nesting season, the nutrient transfer is from the ocean to land, with ramifications for microbial-mediated nutrient flux in terrestrial soils (Fukami et al 2006).…”