Olfactory foraging in temperate waters: Sensitivity to dimethylsulfide by shearwaters in the Atlantic Ocean and Mediterranean Sea

Abstract

Many procellariiforms use olfactory cues to locate food patches over the seemingly featureless ocean surface. In particular, some of them are able to detect and are attracted by dimethylsulphide (DMS), a volatile compound naturally occurring over worldwide oceans in correspondence with productive feeding areas. However, current knowledge is restricted to sub-Antarctic species and to only one study realized under natural conditions at sea. Here, for the first time, we investigated the response to DMS in parallel in two different environments in temperate waters, the Atlantic Ocean and the Mediterranean Sea, employing Cory's (Calonectris borealis) and Scopoli's (Calonectris diomedea) shearwaters as models. To test whether these birds can detect and respond to DMS, we presented them with this substance in a Y-maze. Then, to determine whether they use this molecule in natural conditions, we tested the response to DMS at sea. The number of birds that chose DMS in the Y-maze and that were recruited at DMS-scented slicks at sea suggests that these shearwaters are attracted to DMS in both non-foraging and natural contexts. Our findings show that the use of DMS as a foraging cue may be a strategy adopted by procellariiforms across oceans but that regional differences may exist, giving a worldwide perspective to previous hypotheses concerning the use of DMS as a chemical cue.

Comment on “Marine plastic debris emits a keystone infochemical for olfactory foraging seabirds” by Savoca et al.

“…They described DMS as a “keystone infochemical” with wide implications because this volatile compound occurs particularly in productive habitats where there is intensive grazing by phytoplankton feeders and functions as an attractant for some seabirds (for example, some petrels and penguins), which probably use it as a cue to locate foraging patches ( 2 – 5 ). Savoca et al ( 1 ) hypothesized that emission of DMS by biota on plastics may represent an olfactory trap for foraging seabirds and that it explained patterns of plastic ingestion among procellariiform seabirds.…”

“…A. tenuirostris and A. grisea respond to fish oil and ammonia, but the abstract cited to support the claim that these species respond to DMS states, “responses to dimethyl sulphide and pyrazene were much less robust” ( 8 ), and gives no details on statistical analyses or results. Savoca et al ( 1 ) also included among the non–DMS-responders several species that respond to other odors linked to foraging, but those, as far as we are aware, have not been tested for DMS [ Macronectes giganteus , Macronectes halli , Pelecanoides magellani , Pelecanoides georgicus , Pagodroma nivea , and Thalassoica antarctica ( 5 , 7 , 8 , 11 , 12 )]. The reclassification of all these species is likely to change the model results, including the statistical significance of some of the factors being tested.…”

“…The reclassification of all these species is likely to change the model results, including the statistical significance of some of the factors being tested. At a more fundamental level, odor responsiveness in procellariiform seabirds is not clear-cut [for a comprehensive review, see the study of Dell’Ariccia et al ( 5 )], and the binary classification of Savoca et al ( 1 ) is an oversimplification of the complex ecology of these species in a heterogeneous marine environment that should have been at least considered in their discussion.…”

“…The authors justify the exclusion of these factors by the questionable arguments that prey “capture strategy does not align with ‘species’ among seabirds” and that “DMS tracking is an adaptation for foraging on crustaceans.” However, on average, those Procellariiformes with the widest dietary niches ingest around double the amount of plastic than those that feed mainly on crustaceans or fish and almost four times than those that feed on cephalopods ( 13 ). Fulmarine petrels eat substantial proportions of krill ( 14 , 15 ) but do not respond to DMS ( 8 ), whereas Calonectris borealis is responsive to DMS ( 5 ) but hardly ever eats crustaceans (although it often preys on fish that graze on phytoplankton) ( 16 ). A more parsimonious explanation for the supposedly higher incidence of plastics in the stomach contents of DMS-sensitive species is that small plastic fragments are visually more similar to crustaceans than to other typical prey of seabirds (fish and cephalopods).…”

Chemical labels differ between two closely related shearwater taxa

“…This anatomical development is thought to be related to the nocturnal and colonial ecology of these seabirds during the breeding season, which could exert selective pressures favouring the evolution of refined olfactory mechanisms (Healy and Guilford , Bonadonna and Bretagnolle ). Accordingly, many Procellariiform species possess good olfactory capabilities that are used in different behavioural contexts such as foraging (Nevitt , Dell'Ariccia et al ), homing (Gagliardo et al ) and both intra (Bonadonna and Nevitt , Bonadonna et al , Bonadonna and Mardon ) and interspecific discrimination/recognition (Mardon et al ).…”