Corals Chemically Cue Mutualistic Fishes to Remove Competing Seaweeds

Dixson, Danielle L.; Hay, Mark E.

doi:10.1126/science.1225748

Cited by 62 publications

(57 citation statements)

References 33 publications

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“…Very similar values were obtained for the apogonids Apogon fragilis Smith (mean of 100 s), Ostorhinchus nigrofasciatus (Lachner) (66–143 s) and Nectamia similis Fraser (65–162 s) (Schubert et al . ; Dixson & Hay ). These relatively constant and high levels of toxicity suggest that predation pressure is generally high for coral gobies.…”

Section: Discussionmentioning

confidence: 99%

“…Different toxicity levels of the same species may reflect regional differences. The toxicity of gobies may also be enhanced by the ingestion of toxic algae (Dixson & Hay ). Additionally, the rapid drop in toxicity over time may play a role: our experiments revealed differences in species‐specific toxicity only until 10 min after mucus production.…”

Section: Discussionmentioning

confidence: 99%

“…; Wall & Herler ). They defend their host corals against coral predators or competitive algae (Pratchett ; Dirnwoeber & Herler ; Dixson & Hay ). Habitat specialisation (Munday et al .…”

Section: Introductionmentioning

confidence: 99%

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Skin toxins in coral‐associated Gobiodon species (Teleostei: Gobiidae) affect predator preference and prey survival

et al. 2014

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Predation risk is high for the many small coral reef fishes, requiring successful sheltering or other predator defence mechanisms. Coral-dwelling gobies of the genus Gobiodon live in close association with scleractinian corals of the genus Acropora. Earlier studies indicated that the low movement frequency of adult fishes and the development of skin toxins (crinotoxicity) are predation avoidance mechanisms. Although past experiments showed that predators refuse food prepared with goby skin mucus, direct predator–prey interactions have not been studied. The present study compares the toxicity levels of two crinotoxic coral gobies – Gobiodon histrio, representative of a conspicuously coloured species, and Gobiodon sp.3 with cryptic coloration – using a standard bioassay method. The results show that toxin levels of both species differ significantly shortly after mucus release but become similar over time. Predator preferences were tested experimentally in an aquarium in which the two gobies and a juvenile damselfish Chromis viridis were exposed to the small grouper Epinephelus fasciatus. Video-analysis revealed that although coral gobies are potential prey, E. fasciatus clearly preferred the non-toxic control fish (C. viridis) over Gobiodon. When targeting a goby, the predator did not prefer one species over the other. Contrary to our expectations that toxic gobies are generally avoided, gobies were often captured, but they were expelled quickly, repeatedly and alive. This unusual post-capture avoidance confirms that these gobies have a very good chance of surviving attacks in the field due to their skin toxins. Nonetheless, some gobies were consumed: the coral shelter may therefore also provide additional protection, with toxins protecting them mainly during movement between corals. In summary, chemical deterrence by crinotoxic fishes seems to be far more efficient in predation avoidance than in physical deterrence involving body squamation and/or strong fin spines.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Skin toxins in coral‐associated Gobiodon species (Teleostei: Gobiidae) affect predator preference and prey survival

et al. 2014

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“…Mutualisms typically involve organisms that provide food and shelter in return for protection from predators and competitors. Corals, for example, provide shelter and food to herbivorous fish in return for protection from enemies such as seaweeds (Dixson and Hay 2012). Ant nests are safe environments with ample of food sources and are consequently targeted by many organisms (Kronauer and Pierce 2011).…”

Section: Introductionmentioning

confidence: 99%

An apparent mutualism between Afrotropical ant species sharing the same nest

Parmentier

Yeo

Dekoninck

et al. 2017

Behav Ecol Sociobiol

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Social insects have a highly developed nestmate and species recognition system that is quite effective at keeping out unwanted intruders. Rare cases of Bparabiosis,^however, are known in some ants where two species apparently live peacefully alongside each other within the same nest. Here, we report on such an association between the tiny Afrotropical ant Strumigenys maynei and the large ant Platythyrea conradti. We demonstrated that both ants peacefully share the same arboreal nests in spite of the presence of clearly distinct nestmate recognition cues. Because of the large size differences, we hypothesized that each of the two species would benefit from specializing in carrying out particular tasks, in analogy to the size-related division of labor observed in species with size-polymorphic workers. In line with this theory, we found that the tiny ant S. maynei was highly efficient at nest defense against intranidal arthropods and alien ant intruders, whereas the large ant P. conradti was highly skilled in nest engineering. We argue that the described association is likely mutualistic, as P. conradti clearly benefited from the supreme defense capabilities of S. maynei, and that, conversely, S. maynei took advantage of small prey thriving in the organic nest material collected by P. conradti. Significance statementAssociations between social insects are typically parasitic in nature. A few cases, however, are known of beneficial associations between social insects. Here, we report such a rare association between two Afrotropical species that share the same nest even though they lack matching colony odors. The large ant Platythyrea conradti benefited from the presence of Strumigenys maynei as this tiny, but highly aggressive, ant was much more efficient in attacking intranidal and extranidal enemies. S. maynei in turn took advantage of P. conradti as this ant constructs a unique nest which attracts suitable prey.

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“…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)(8)(9)(10).…”

mentioning

confidence: 99%

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

Savoca

Nevitt

2014

Proc. Natl. Acad. Sci. U.S.A.

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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...

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Corals Chemically Cue Mutualistic Fishes to Remove Competing Seaweeds

Cited by 62 publications

References 33 publications

Skin toxins in coral‐associated Gobiodon species (Teleostei: Gobiidae) affect predator preference and prey survival

Skin toxins in coral‐associated Gobiodon species (Teleostei: Gobiidae) affect predator preference and prey survival

An apparent mutualism between Afrotropical ant species sharing the same nest

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

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