Evidence That Dimethyl Sulfide Facilitates a Tritrophic Mutualism Between Marine Primary Producers and Top Predators
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Evidence that dimethyl sulfide facilitates a tritrophic mutualism between marine primary producers and top predators Matthew S. Savocaa,b and Gabrielle A. Nevitta,b,1 aGraduate Group in Ecology, University of California, Davis, CA 95616; and bDepartment of Neurobiology, Physiology, and Behavior, College of Biological Sciences, University of California, Davis, CA 95616 Edited by May R. Berenbaum, University of Illinois at Urbana–Champaign, Urbana, IL, and approved February 3, 2014 (received for review September 10, 2013) Tritrophic mutualistic interactions have been best studied in plant– in this regard, and many species have been shown to detect and insect systems. During these interactions, plants release volatiles respond to biogenic concentrations of DMS in foraging contexts in response to herbivore damage, which, in turn, facilitates pre- (24, 25). Members of this order share highly pelagic lifestyles and dation on primary consumers or benefits the primary producer by are central-place foragers associated with land only during in- providing nutrients. Here we explore a similar interaction in the cubation and chick rearing (26). Procellariiformes routinely range Southern Ocean food web, where soluble iron limits primary pro- thousands of kilometers to forage (27) and have large olfactory ductivity. Dimethyl sulfide has been studied in the context of bulbs compared with other avian clades (28), and some species global climate regulation and is an established foraging cue for marine top predators. We present evidence that procellariiform have been shown to track their prey using their sense of smell (29). seabird species that use dimethyl sulfide as a foraging cue selec- Some procellariiform species are attracted to DMS, whereas others tively forage on phytoplankton grazers. Their contribution of ben- are not (24, 30) (Fig. 1); however, the relationship between DMS eficial iron recycled to marine phytoplankton via excretion suggests behavioral sensitivity and the consumption of herbivorous crusta- a chemically mediated link between marine top predators and oce- cea has not previously been shown. anic primary production. The Southern Ocean is the largest marine ecosystem in the world, with the polar front forming a distinct northern boundary any plant species interact with carnivores to gain pro- to this ecoregion (31). Our rationale for using this system is Mtection from herbivory. Such mutualistic tritrophic inter- twofold: (i) A majority of the world’s procellariiform species actions have been studied extensively in plant–insect systems, breed or forage in the Southern Ocean (32), and (ii) food web and are frequently mediated by plant volatiles released in re- relationships are relatively simple by comparison with other sponse to insect feeding (1). One example that has received marine systems. Phaeocystis antarctica and several siliceous di- detailed study is the interaction between the phytophagous two- atom species are the dominant DMS-producing phytoplankton Tetranychus urticae spotted spider mite , the lima bean plant species in this ecosystem, and Antarctic krill (Euphasia superba) Phaseolus lunatus, and the predatory mite Phytoseiulus persimilis and other small crustaceans (copepods, decapods, amphipods, (2, 3). In this model system, grazing by the herbivorous spider mite has been demonstrated to elicit a cascade of biochemical etc.) are their major consumers. reactions within the afflicted plants, stimulating the release of Here we take advantage of a 50-y dietary database of Southern a suite of volatile terpenoids such as (E)-4,8-dimethyl-l,3, Ocean seabirds (33) to explore whether DMS mediates a mutual- 7-nonatriene, (E)-β-ocimene, and (E,E)-4,8,12-trimethyl-1,3,7, istic tritrophic interaction in the Southern Ocean pelagic ecosys- 11-tridecatetraene (3). These volatiles attract olfactory-searching tem. If this is the case, then we predict that (i) carnivorous species, P. persimilis that prey upon herbivorous spider mites. such as seabirds, that are attracted to this infochemical should spe- The possibility of tritrophic mutualisms involving plant vola- cialize on primary consumers, such as crustaceans, and (ii)primary tiles has received considerable attention in terrestrial commu- producers should gain some benefit from this interaction. nities (2–5); however, similar interactions have rarely been suggested for marine systems (6). Dimethyl sulfide (DMS) and its Significance precursor dimethylsulfoniopropionate (DMSP) are well-established infochemicals in the marine environment, and as such are good This study demonstrates that dimethyl sulfide, a chemical cue candidate molecules for mediating tritrophic interactions between involved in global climate regulation, mediates a tritrophic phytoplankton and carnivores (7–10). DMS arises as a catabolic mutualistic interaction between marine apex predators and breakdown product of DMSP, and has been studied extensively primary producers. Our results imply that marine top predators for its putative role as a global climate regulator (11). DMSP is play a critical role in maintaining both ocean health and global produced by marine algae, where it has been proposed to function climate. Our results highlight the need for more collaboration as an osmolyte (12) and a cryoprotectant (13). When algal cells and discussion between micro- and macroscale biologists lyse, due to biotic or abiotic stress, one of the fates of DMSP is working on global issues in the Southern Ocean. catabolism by the enzyme DMSP lyase to DMS and acrylic acid – (14 16). This process may also occur during autocatalytic cell Author contributions: M.S.S. and G.A.N. designed research; G.A.N. developed the initial death (17). It has been proposed that acrylic acid is the bi- dataset; M.S.S. performed research; M.S.S. analyzed data; and M.S.S. and G.A.N. wrote ologically salient product of this reaction due to its antimicrobial the paper. properties (18). Conflict of interest statement: The authors declare a conflict of interest (such as defined DMS production has also been shown to increase during by PNAS policy). zooplankton grazing (14). It has been previously proposed that This article is a PNAS Direct Submission. this phytoplankton-derived odorant is an important infochemical Freely available online through the PNAS open access option. 1 for marine apex predators including whale sharks (19), harbor To whom correspondence should be addressed. E-mail: [email protected]. ECOLOGY – seals (20), penguins (21 23), and procellariiform (tube-nosed) This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. seabirds (24). Procellariiform seabirds have been the best-studied 1073/pnas.1317120111/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1317120111 PNAS | March 18, 2014 | vol. 111 | no. 11 | 4157–4161 Downloaded by guest on September 25, 2021 Procellariiform species included in analysis alopods in the diet showed a positive overall relationship (Fig. 3B), but log-transformed weight was the only significant mor- Sphenisciformes phological predictor (βlog wt = 0.12 ± 0.055, P = 0.03; βDMS tracker = Oceanites oceanicus Hydrobatidae −0.10 ± 0.082, P = 0.23 and βaspect ratio = 0.06 ± 0.016, P = Fregetta tropica β = − ± P = Thalassarche melanophris 0.89; DMS tracker 0.03 0.076, 0.70). The multiple linear Thalassarche chrysostoma Diomedeidae regression for the proportion of fish in the diet exhibited Diomedea exulans a weakly positive overall relationship (Fig. 3C), but neither Pelecanoides urinatrix Pelecaniodidae morphological parameter was significant (βlog wt = 0.01 ± 0.049, Pagodroma nivea P = 0.89; βDMS tracker = −0.15 ± 0.073, P = 0.04 and βaspect ratio = Thalassoica antarctica 0.02 ± 0.015, P = 0.29; βDMS tracker = −0.10 ± 0.070, P = 0.16; Fig. Daption capense 3C). Taken together, these results suggest that DMS behavioral Macronectes halli Macronectes giganteus responsiveness is linked to the consumption of primary con- Fulmarus glacialoides sumers (crustacea) that forage on DMS-producing phytoplank- Pachyptila turtur Procellariidae ton. As a result, we argue that procellariiform seabirds are Pachyptila desolata playing a similar role to that played by carnivorous mutualists Pachyptila salvini (e.g., P. persimilis) in plant–insect interactions. outgroup Pachyptila belcheri For this chemically mediated, tritrophic interaction to be mu- DMS + Halobaena caerulea tualistic, it must also carry a benefit to phytoplankton (Fig. 4). Procellaria aequinoctialis DMS − Predatory release implies that phytoplankton are “rescued” from Fig. 1. Phylogenetic relationships between the species included in the meta- grazing pressure when primary consumers are ingested by car- analysis, mapped with DMS responsiveness. DMS responsiveness is thought to nivores. Our results support this hypothesis in that DMS res- be ancestral in this lineage (30). Certain species in the outgroup, sphenisci- ponders were found to preferentially consume phytoplankton formes (penguins), have also been shown to be responsive to DMS (21–23). grazers (Fig. 2). However, we also considered the possible fer- tilization benefits that foraging seabirds may provide to phyto- plankton. Iron is necessary for electron transfer and ATP pro- Results duction involved in phytoplankton growth (36), but the Southern To address our first prediction, we conducted a meta-analysis of Ocean is iron-limited (37). This is because the Southern Ocean diet composition relative to DMS behavioral sensitivity for dif- lacks major land masses