Can a marine infochemical facilitate a tritrophic mutualism between primary producers and top predators?

Background/Question/Methods

Tritrophic interactions have been best studied in plant–insect 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 (DMS) has been studied extensively in the context of global climate regulation, and has also been implicated as a key signal molecule in foraging cascades. It has been suggested, for example that procellariiform seabirds and other marine top predators use DMS released by depredated phytoplankton as a foraging cue to locate zooplankton prey. However, the dietary links between DMS attraction and trophic foraging level have never been explicitly demonstrated. Moreover, a marine tritrophic mutualism between primary producers and top predators has rarely been investigated. We addressed two hypotheses: 1) if DMS is an infochemical facilitating a tritrophic mutualism, then the diets of DMS-responsive procellariiform species would contain significantly higher proportions of primary consumers (e.g. crustaceans, including euphausiids, copepods, and decapods) than other food types (cephalopods and fish) and 2) phytoplankton may benefit from the addition of soluble iron recycled by forging seabirds.

Results/Conclusions

Our results strongly support the first hypothesis; DMS-responsive seabirds specialize on primary consumers (proportion crustacea: 0.814 ± 0.039, proportion cephalopod: 0.065 ± 0.019, proportion fish: 0.108 ± 0.024; F_5,274 = 42.67, P < 0.001). To address our second hypothesis, we estimated the iron throughput from seabirds nesting on South Georgia Island. We estimate that the ~31 million seabirds nesting on South Georgia ingest approximately 226 metric tons of iron annually in the krill they consume. Iron is toxic to vertebrates at high levels and ~90% of iron ingested by these seabirds is excreted on the surface layer of the ocean. Even though these seabirds forage and defecate over vast regions of the Southern Ocean, only 0.1-0.5 nM L^-1 of local iron enhancement is required to stimulate phytoplankton growth; therefore we believe it is possible for flocks of foraging seabirds to seed phytoplankton growth. These birds also forage sympatrically with marine mammals, leading to additive effects on localized fertilization.  Together, these results 1) provide evidence that DMS may facilitate a tritrophic mutualistic interaction in the pelagic marine environment and 2) suggest that a decline in seabird populations could negatively affect overall marine productivity.