Olfactory foraging in temperate waters: Sensitivity to dimethylsulphide of shearwaters in the Atlantic Ocean and Mediterranean Sea

Journal of Experimental Biology

Volumn 217, Issue 10, 2014, Pages 1701-1709

  Dell'Ariccia, Gaia ^a   Célérier, Aurélie ^a   Gabirot, Marianne ^a   Palmas, Pauline ^a   Massa, Bruno ^b   Bonadonna, Francesco ^a  

^a CENTRE D ECOLOGIE FONCTIONNELLE ET EVOLUTIVE   (France)

^b UNIVERSITY OF PALERMO   (Italy)

Author keywords

DMS; Foraging; Odour cues; Olfaction; Petrels; Procellariiform seabirds

Indexed keywords

AVES; CALONECTRIS; CALONECTRIS DIOMEDEA; PROCELLARIIDAE; PROCELLARIIFORMES;

DIMETHYL SULFIDE; SULFIDE; WATER;

ANALYSIS; ANIMAL; ASSOCIATION; ATLANTIC OCEAN; BIRD; FEEDING BEHAVIOR; MEDITERRANEAN SEA; METABOLISM; ODOR; PHYSIOLOGY; SEA;

ANIMALS; ATLANTIC OCEAN; BIRDS; CUES; FEEDING BEHAVIOR; MEDITERRANEAN SEA; OCEANS AND SEAS; ODORS; SMELL; SULFIDES; WATER;

EID: 84908293027     PISSN: 00220949     EISSN: 14779145     Source Type: Journal    
DOI: 10.1242/jeb.097931     Document Type: Article

References (103)

1. Belviso, S., Sciandra, A. and Copin-Monté gut, C. (2003). Mesoscale features of surface water DMSP and DMS concentrations in the Atlantic Ocean off Morocco and in the Mediterranean Sea. Deep Sea Res. Part I Oceanogr. Res. Pap. 50, 543-555.
2. Belviso, S., Moulin, C., Bopp, L. and Stefels, J. (2004). Assessment of a global climatology of oceanic dimethylsulfide (DMS) concentrations based on SeaWiFS imagery (1998-2001). Can. J. Fish. Aquat. Sci. 61, 804-816.
3. Bonadonna, F. and Nevitt, G. A. (2004). Partner-specific odor recognition in an Antarctic seabird. Science 306, 835.
4. Bonadonna, F. and Sanz-Aguilar, A. (2012). Kin recognition and inbreeding avoidance in wild birds: the first evidence for individual kin-related odour recognition. Anim. Behav. 84, 509-513.
5. Bonadonna, F., Caro, S., Jouventin, P. and Nevitt, G. A. (2006). Evidence that blue petrel, Halobaena caerulea, fledglings can detect and orient to dimethyl sulfide. J. Exp. Biol. 209, 2165-2169.
6. Brooke, M. (2004). Albatrosses and Petrels Across the World. Oxford: Oxford University Press.
7. Buitron, D. and Nuechterlein, G. L. (1985). Experiments on olfactory detection of food caches by black-billed magpies. Condor 87, 92-95.
8. Cantin, G., Levasseur, M., Gosselin, M. and Michaud, S. (1996). Rol e of zooplankton in the mesoscale distribution of surface dimethylsulfide concentrations in the Gulf of St. Lawrence, Canada. Mar. Ecol. Prog. Ser. 141, 103-117.
9. Cecere, J. G., Catoni, C., Maggini, I., Imperio, S. and Gaibani, G. (2013). Movement patterns and habitat use during incubation and chick-rearing of Cory Shearwater (Calonectris diomedea) from Central Mediterranean: influence of seascape and breeding stage. Italian Journal of Zoology 80, 82-89.
10. Clark, L. and Shah, P. S. (1992). Information content of prey odour plumes: what do foraging Leach's storm petrels know? In Chemical Signals in Vertebrates VI (ed. R. L. Doty and D. Müller-Schwarze), pp. 421-427. New York, NY: Plenum Press.
11. Cunningham, G. B. and Nevitt, G. A. (2005). The sense of smell in procellariiforms-an overview and new directions. In Chemical Signals in Vertebrates 10 (ed. R. T. Mason, M. P. LeMaster and D. Müller-Schwarze), pp. 403-408. New York, NY: Springer.
12. Cunningham, G. B., Van Buskirk, R. W., Bonadonna, F., Weimerskirch, H. and Nevitt, G. A. (2003). A comparison of the olfactory abilities of three species of procellariiform chicks. J. Exp. Biol. 206, 1615-1620.
13. Cunningham, G. B., Van Buskirk, R. W., Hodges, M. J., Weimerskirch, H. and Nevitt, G. A. (2006). Behavioural responses of blue petrel chicks (Halobaena caerulea) to food-related and novel odours in a simple wind tunnel. Antarct. Sci. 18, 345-352.
14. Cunningham G. B.,Strauss V.,Ryan, PG. 2008). African penguins (Spheniscus demersus) can detect dimethyl sulphide, a prey-related odour J. Exp. Biol. 211, 3123-3127.
15. Dacey, J. W. H. and Wakeham, S. G. (1986). Oceanic dimethylsulfide: production during zooplankton grazing on phytoplankton. Science 233, 1314-1316.
16. DeBose, J. L. and Nevitt, G. (2007). Investigating the association between pelagic fish and dimethylsulfoniopropionate in a natural coral reef system. Mar. Freshw. Res. 58, 720-724.
17. DeBose, J. L., Lema, S. C. and Nevitt, G. A. (2008). Dimethylsulfoniopropionate as a foraging cue for reef fishes. Science 319, 1356.
18. del Hoyo, J., Elliott, A. and Sargatal, J. (1992). Handbook of the Birds of the World. Barcelona: Lynx Edicions.
19. Dell'Ariccia, G., Dell'Omo, G., Massa, B. and Bonadonna, F. (2010). First GPStracking of Cory's shearwater in the Mediterranean Sea. Italian Journal of Zoology 77, 339-346.
20. Dias, M. P., Granadeiro, J. P., Phillips, R. A., Alonso, H. and Catry, P. (2011). Breaking the ro utine: individual Cory's shearwaters shift winter destinations between hemispheres and across ocean basins. Proc. Biol. Sci. 278, 1786-1793.
21. Fiaschi, V., Farina, M. and Ioalé , P. (1974). Homing experiments on swifts Apus apus (L.) deprived of olfactory perception. Monitore Zoologico Italiano 8, 235-244.
22. Gagliardo, A., Bried, J., Lambardi, P., Luschi, P., Wikelski, M. and Bonadonna, F. (2013). Oceanic navigation in Cory's shearwaters: evidence for a crucial role of olfactory cues for homing after displacement. J. Exp. Biol. 216, 2798-2805.
23. Granadeiro, J. P., Dias, M. P., Rebelo, R., Santos, C. D. and Catry, P. (2006). Numbers and population trends of Cory's shearwater Calonectris diomedea at Selvagem Grande, Northeast Atlantic. Waterbirds 29, 56-60.
24. Grubb, T. C. (1972). Smell and foraging in shearwaters and petrels. Nature 237, 404-405.
25. Hay, M. E. and Kubanek, J. (2002). Community and ecosystem level consequences of chemical cues in the plankton. J. Chem. Ecol. 28, 2001-2016.
26. Holland, R. A., Thorup, K., Gagliardo, A., Bisson, I. A., Knecht, E., Mizrahi, D. and Wikelski, M. (2009). Testing the role of sensory systems in the migratory heading of a songbird. J. Exp. Biol. 212, 4065-4071.
27. Hutchison, L. V. and Wenzel, B. M. (1980). Olfactory guidance in foraging by procellariiforms. Condor 82, 314-319.
28. Hutchison, L. V., Wenzel, B. M., Stager, K. E. and Tedford, B. L. (1984). Further evidence for olfactory foraging by sooty shearwaters and northern fulmars. In Marine Birds: Their Feeding Ecology and Commercial Fisheries Relationships (ed. D. N. Nettleship, G. A. Sanger and P. F.Springer), pp. 72-77. Ottawa, ON: Canadian Wildlife Service.
29. Jacobs, L. F. (2012). From chemotaxis to the cognitive map: the function of olfaction. Proc. Natl. Acad. Sci. USA 109 Suppl. 1, 10693-10700.
30. Jean, N., Bogé , G., Jamet, J.-L., Jamet, D. and Richard, S. (2009). Plankton origin of particulate dimethylsulfoniopropionate in a Mediterranean oligotrophic coastal and shallow ecosystem. Estuar. Coast. Shelf Sci. 81, 470-480.
31. Jouventin, P. (1977). Olfaction in Snow Petrels. Condor 79, 498-499.
32. Jouventin, P. and Robin, J. P. (1984). Olfactory experiments on some Antarctic birds. Emu 84, 46-48.
33. Kettle, A. J. and Andreae, M. O. (2000). Flux of dimethylsulfide from the oceans: a comparison of updated data sets and flux models. J. Geophys. Res. 105, 26793-26808.
34. Lequette, B ., Verheyden, C. and Jouventin, P. (1989). Olfaction in suantarctic seabirds:its phylogenetic and ecological significance. Condor 91, 732-735.
35. Massa B.,Lo Valvo, M. 1986 Biometrical and biological considerations on the Cory's shearwater Calonectris diomedea In Mediterranean Marine Avifauna (ed. M. X. Monbaillin) 293-313. Berlin; Heidelberg: Springer Verlag.
36. Bonadonna, F., Caro, S., Jouventin, P. and Nevitt, G. A. (2006). Evidence that blue petrel, Halobaena caerulea, fledglings can detect and orient to dimethyl sulfide. J. Exp. Biol. 209, 2165-2169.
37. Bro oke, M. (2004). Albatrosses and Petrels Across the World. Oxford: Oxford University Press.
38. Buitron, D. and Nuechterlein, G. L. (1985). Experiments on olfactory detection of food caches by black-billed magpies. Condor 87, 92-95.
39. Cantin, G., Levasseur, M., Gosselin, M. and Michaud, S. (1996). Role of zooplankton in the mesoscale distribution of surface dimethylsulfide concentrations in the Gulf of St. Lawrenc e, Canada. Mar. Ecol. Prog. Ser. 141, 103-117.
40. Cecere, J. G., Catoni, C., Maggini, I., Imperio, S. and Gaibani, G. (2013). Movement patterns and habitat use during incubation and chick-rearing of Cory Shearw ater (Calonectris diomedea) from Central Mediterranean: influence of seascape and breeding stage. Italian Journal of Zoology 80, 82-89.
41. Clark, L. and Shah, P. S. (1992). Information content of prey odour plumes : what do foraging Leach's storm petrels know? In Chemical Signals in Vertebrates VI (ed. R. L. Doty and D. Müller-Schwarze), pp. 421-427. New York, NY: Plenum Press.
42. Cunningham, G. B. and Nevitt, G. A. (2005). The sense of smell in procellariiforms-an overview and new directions. In Chemical Signals in Vertebrates 10 (ed. R. T. Mason, M. P. LeMaster and D. Müller-Schwarze), pp. 403-408. New York, NY: Springer.
43. Cunningham, G. B., Van Buskirk, R. W., Bonadonna, F., Weimerskirch, H. and Nevitt, G. A. (2003). A comparison of the olfactory abilities of three species of procellariiform chicks. J. Exp. Biol. 206, 1615-1620.
44. Cunningham , G. B., Van Buskirk, R. W., Hodges, M. J., Weimerskirch, H. and Nevitt, G. A. (2006). Behavioural responses of blue petrel chicks (Halobaena caerulea) to food-related and novel odours in a simple wind tunnel. Antarct. Sci. 18 , 345-352.
45. Cunningham, G. B., Strauss, V. and Ryan, P. G. (2008). African penguins (Spheniscus demersus) can detect dimethyl sulphide, a prey-related odour. J. Exp. Biol. 211, 3123-3127.
46. D acey, J. W. H. and Wakeham, S. G. (1986). Oceanic dimethylsulfide: production during zooplankton grazing on phytoplankton. Science 233, 1314-1316.
47. DeBose, J. L. and Nevitt, G. (2007). Investigating the association between pelagic fish and dimethylsulfoniopropionate in a natural coral reef system. Mar. Freshw. Res. 58, 720-724.
48. DeBose, J. L., Lema, S. C. and Nevitt, G. A. (2008). Dimethylsulfoniopropi onate as a foraging cue for reef fishes. Science 319, 1356.
49. del Hoyo, J., Elliott, A. and Sargatal, J. (1992). Handbook of the Birds of the World. Barcelona: Lynx Edicions.
50. Dell'Ariccia, G., Dell'Omo, G., Massa, B. and Bonadonna, F. (2010). First GPStracking of Cory's shearwater in the Mediterranean Sea. Italian Journal of Zoology 77, 339-346.
51. Dias, M. P., Granade iro, J. P., Phillips, R. A., Alonso, H. and Catry, P. (2011). Breaking the routine: individual Cory's shearwaters shift winter destinations between hemispheres and across ocean basins. Proc. Biol. Sci. 278, 1786-1793.
52. Fiaschi, V., Farina, M. and Ioalé , P. (1974). Homing experiments on swifts Apus apus (L.) deprived of olfactory perception. Monitore Zoologico Italiano 8, 235-244.
53. Gagliardo, A., Bried, J., L ambardi, P., Luschi, P., Wikelski, M. and Bonadonna, F. (2013). Oceanic navigation in Cory's shearwaters: evidence for a crucial role of olfactory cues for homing after displacement. J. Exp. Biol. 216, 2798-2805.
54. Granadeiro, J. P., Dias, M. P., Rebelo, R., Santos, C. D. and Catry, P. (2006). Numbers and population trends of Cory's shearwater Calonectris diomedea at Selvagem Grande, Northeast Atlantic. Waterbirds 29, 56-60.
55. Grubb, T. C. (1972). Smell and foraging in shearwaters and petrels. Nature 237, 404-405.
56. Hay, M. E. and Kubanek, J. (2002). Community and ecosystem level consequences of chemical cues in the plankton. J. Chem. Ecol. 28, 2001-2016.
57. Holland R. A.,Thorup K.,Gagliardo A.,Bisson I. A.,Knecht E.,Mizrahi D.,Wikelski, M. 2009 Testing the role of sensory systems in the migratory heading of a songbird J. Exp. Biol. 212, 4065-4071.
58. Hutchison, L. V. and Wenzel, B. M. (1980). Olfactory guidance in fora ging by procellariiforms. Condor 82, 314-319.
59. Hutchison, L. V., Wenzel, B. M., Stager, K. E. and Tedford, B. L. (1984). Further evidence for olfactory foraging by sooty shearwaters and northern fulmars. In Marine Birds: Their Feeding Ecology and Commercial Fisheries Relationships (ed. D. N. Nettleship, G. A. Sanger and P. F. Springer), pp. 72-77. Ottawa, ON: Canadian Wildlife Service.
60. Jacobs, L. F. (2012). From chemotaxis to the cognitive map: the function of olfaction. Proc. Natl. Acad. Sci. USA 109 Suppl. 1, 10693-10700.
61. Jean, N., Bogé , G., Jamet, J.-L., Jamet, D. and Richard, S. (2009). Plankton origin of particulate dimethylsulfoniopropionate in a Mediterranean oligotrophic coastal and shallow ecosystem. Estuar. Coast. Shelf Sci. 81, 470-480.
62. Jouventin, P. (1977). Olfaction in Snow Petrels. Condor 79, 498-499.
63. Jouventin, P. and Robin, J. P. (1984). Olfactory experiments on some Antarctic birds. Emu 84, 46-48.
64. Kettle, A. J. and Andreae, M. O. (2000). Flux of dimethylsulfide from the oceans: a comparison of updated data sets and flux models. J. Geophys. Res. 105, 26793-26808.
65. Lequette, B., Verheyden, C. and Jouventin, P. (1989).Olfaction in suantarctic seabirds:its phylogenetic and ecological significance. Condor 91, 732-735.
66. Massa, B. and Lo Valvo, M. (1986). Biometrical and biological considerations on the Cory's shearwater C alonectris diomedea. In Mediterranean Marine Avifauna (ed. M. X. Monbaillin), pp. 293-313. Berlin; Heidelberg: Springer Verlag.
67. RESEARCH ARTICLE The Journal of Experimental Biology (2014) doi:10.1242/jeb.097931 The Journal of Experimental Biology
68. McDonald, J. H. (2009). Handbook of Biological Statistics, 2nd edn. Baltimore, MD: Sparky House Publishing.
69. Nevitt, G. A. (1994). Antarctic procellariiform seabirds can smell krill. Antarct. J. US 29, 168-169.
70. Nevitt, G. A. (1999 a ). Foraging by seabirds on an olfactory landscape. Am. Sci. 87, 46-53.
71. Nevitt, G. A. (1999 b). Olfactory foraging in Antarctic seabirds: a species-specific attraction to krill odors. Mar. Ecol. Prog. Ser. 177, 235-241.
72. Nevitt, G. A. (2000). Olfactory foraging by Antarctic procellariiform seabirds: life at high Reynolds numbers. Biol. Bull. 198, 245-253.
73. Nevitt, G. A. (2008). Sensory ecology on the high seas: the odor world of the procellariiform seabirds. J. Exp. Biol. 211, 1706-1713.
74. Nevitt, G. A. (2011). The neu roecology of dimethyl sulfide: a global-climate regulator turned marine infochemical. Integr. Comp. Biol. 51, 819-825.
75. Nevitt, G. A. and Bonadonna, F. (2005 a). Seeing the world through the nose of a bird: new develo pments in the sensory ecology of procellariiform seabirds. Mar. Ecol. Prog. Ser. 287, 292-295.
76. Nevitt, G. A. and Bonadonna, F. (2005 b). Sensitivity to dimethyl sulphide suggests a mechanism for olfactory navigation by seabirds. Biol. Lett. 1, 303-305.
77. Nevitt, G. A. and Haberman, K. (2003). Behavioral attraction of Leach's storm-petrels (Oceanodroma leucorhoa) to dimethyl sulfide. J. Exp. Biol. 206, 1497-1501.
78. Nevitt G. A.,Hunt, GL. 1996). Olfactory sensitivities of foraging procellariid seabirds in the Aleutian Islands. Chem. Senses 21, 649-650.
79. Nevitt, G. A. and Veit, R. R. (1999). Mechan isms of prey-patch detection by foraging seabirds. In Proceedings of the 22nd International Ornithological Congress (ed. by N. J. Adams and R. H. Slotow), pp. 2072-2082. Durban; Johannesburg: BirdLife South Africa.
80. Nevitt, G. A. , Veit, R. R. and Kareiva, P. (1995). Dimethyl sulphide as a foraging cue for Antarctic Procellariiform seabirds. Nature 376, 680-682.
81. Nevitt, G., Reid, K. and Trathan, P. (2004). Testing olfactory foraging strategies in an Antarctic seabird assemblage. J. Exp. Biol. 207, 3537-3544.
82. Nevitt, G. A., Bergstrom, D. M. and Bonadonna, F. (2006). The potential r ole of ammonia as a signal molecule for procellariiform seabirds. Mar. Ecol. Prog. Ser. 315, 271-277.
83. Paiva, V. H., Geraldes, P., Ramírez, I., Meirinho, A., Garthe, S. and Ramos, J. A. (2010). Forag ing plasticity in a pelagic seabird species along a marine productivity gradient. Mar. Ecol. Prog. Ser. 398, 259-274.
84. Papi, F. (1989). Pigeons use olfactory cues to navigate. Ethology Ecology & Evolution 1, 219-231.
85. Peron, C. and Gremillet, D. (2014). Habitats Maritimes des Puffins de France Métropolitaine: Approche par Balises et Analyses Isotopiques: Final Report. Brest, France: Agence des Aires Marines Protégé es.
86. R Development Core Team (2011). R: A Language And Environment For Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.
87. Ristow, D., Berthold, P., Hashmi, D. and Querner, U. (2000). Satellite tracking of Cory's shearwater migration. Condor 102, 696-699.
88. Roper, T. J. (1999). Olfaction in birds. Adv. Study Behav. 28, 247-332.
89. Sangster, G., Collinson, J. M., Cr ochet, P.-A., Knox, A. G., Parkin, D. T. and Votier, S. C. (2012). Taxonomic recommendations for British birds: eighth report. Ibis 154, 874-883.
90. Simó, R. (2001). Production of atmospheric sulfur by oceanic plankton: biogeochemical, ecological and evolutionary links. Trends Ecol. Evol. 16, 287-294.
91. Simó, R. and Grimalt, J. O. (1998). Spring-summe r emissions of dimethyl sulphide from the north-western Mediterranean Sea. Estuar. Coast. Shelf Sci. 47, 671-677.
92. Simó, R., Grimalt, J. O. and Albaigés, J. (1997). Dissolved dimethylsulphide, dimethylsulphoniopropionate and dimethylsulphoxide in western Mediterranean waters. Deep Sea Res. Part II Top Stud. Oceanogr. 44, 929-950.
93. Stager, K. E. (1964). The Role of Olfaction in Food Location by Turkey Vulture (Cathartes aura). Los An geles, CA: Los Angeles County Museum Contributions in Science.
94. Stager, K. E. (1967). Avian olfaction. Am. Zool. 7, 415-420.
95. Stephens, D. W. and Krebs, J. R. (1986). Monographs in Behavior and Ecology: Foraging Theory. Princeton, NJ: Princeton University Press.
96. Verheyden, C. and Jouventin, P. (1994). Olfactory behavior of foraging procellariiforms. Auk 111, 285-291.
97. Wallraff, H. G., Kiepen heuer, J., Neumann, M. F. and Streng, A. (1995). Homing experiments with starlings deprived of the sense of smell. Condor 97, 20-26.
98. Warham, J. (1990). The Petrels Their Ecology and Breeding System. London: Harcourt Brace Jovanovich.
99. Warham, J. (1996). The Behaviour, Population Biology and Physiology of The Petrels. London: Harcourt Brace & Company.
100. Wenzel B. M. 1971 Olfactory sensation in the kiwi and other birds. Ann. New York Acad. Sci. 188, 183-193.
101. Wenzel, B. M. (1986). The ecological and evolutionary challenges of procellariiform olfaction. In Chemical Signals in Vertebrates (ed. D. Duvall, D. Müller-Schwarze and R. M. Silverstein), pp. 357-368. New York, NY: Plenum Press.
102. Wright, K. L. B., Pichegru, L. and Ryan, P. G. (2011). Penguins are attracted to dimethyl sulphide at sea. J. Exp. Biol. 214, 2509-2511.
103. Zar, J. H. (1996). Biostatistical Analysis. Upper Saddle River, NJ: Prentice Hall.