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Seeing the world through the nose of a bird: exploring the sensory ecology of Procellariiform seabirds Dr. Gabrielle Nevitt, Associate Professor University of California, Davis Logistical support and funding provided by: CNRS / IPEV (France); BAS (UK) NSF Polar Programs and NSF Sensory Biology (USA) Some publications pertinent to this talk: Nevitt, GA, Veit RR, and Kareiva P. 1995. Dimethyl sulfide as a foraging cue for Antarctic procellariiform seabirds. Nature 376, 680-682. Nevitt, GA. 2000. Olfactory Foraging by Antarctic Procellariiform Seabirds: Life at High Reynolds Numbers. Biological Bulletin, 198, 245-253 Nevitt GA, Reid K and Trathan P. 2004. Testing olfactory foraging strategies in an Antarctic seabird assemblage. Journal of Experimental Biology, 207, 3537-3544 Silverman ED, Veit RR and Nevitt GA. 2004. Nearest neighbors as foraging cues: information transfer in a patchy environment. Marine Ecology Progress Series, 277, 25-35 Bonadonna F and Nevitt GA. 2004. Partner-specific odor recognition in an Antarctic Seabird. Science, 306, 835 http://www.npb.ucdavis.edu/npbdirectory/nevitt.html Some Antarctic procellariiform seabirds The procellariiforms: (petrels, albatrosses and shearwaters) Olfactory systems are well developed. Species are highly pelagic. Food resources are patchily distributed over vast areas so… Many species commonly forage and navigate over extreme distances. Nearly all procellariiforms have highly developed olfactory system Cross section through the peripheral olfactory system (Bang 1966) krill fish squid BLACK BROWED ALBATROSS SOUTH GEORGIA BREEDING SEASON (CROXALL 1984) SQUID KRILL FISH OTHER WANDERING ALBATROSS SOUTH GEORGIA BREEDING SEASON (CROXALL 1984) SQUID KRILL FISH Procellariiform seabirds routinely travel extreme distances over featureless ocean Wilson’s storm petrel Wandering albatross South Georgia Kergeulen Movement Patterns of Wandering Albatrosses East (Shaffer et al. 2001, 2003) Different large-scale foraging strategies Commuting Scavenging Procellariiforms have different life history characteristics Can birds detect odors emitted from their prey? This turns out to be the wrong question. Several false assumptions have gotten in the way of thinking of odors as potential foraging and navigation cues: • Odor cues translate into concentration gradients over large distances. • Odors are ephemeral. • Transport is mediated by diffusion. Several false assumptions have gotten in the way of thinking of odors as potential foraging and navigation cues: • Odor cues translate into concentration gradients over large distances. • Odors are ephemeral. • Transport is mediated by diffusion. New concept: Navigation by Olfactory Landscapes Scented compounds are predictably elevated where productivity is high •shelf breaks •frontal zones •sea mounts (Nevitt, et al. Nature 1995) Olfactory Landscapes navigation large scale small scale (Nevitt, 2000) Dimethyl sulphide (DMS) is an important signal molecule in the marine environment DMS Oceanic Concentrations (nmol L-1) Latitude 10.0 1.0 0.1 Longitude (Data from Kettle, et al. 1999) Chlorophyll concentrations around Kerguelen Like DMS, chlorophyll occurs in predictable Locations and is associated with productive areas of ocean 25oS, 40o-75oE Kerguelen 54oS, 40o-75oE (Courtesy of SeaWiFS Project data base) Atmospheric DMS Metabolism and senescence PHYTO PLANKTON (DMSP) DMSP Oceanic DMS Metabolism and excretion ZOO PLANKTON (DMSP) DMS + Acrylic acid (adapted from Dacey and Wakham, 1986) DMS hotspots Metabolism and senescence PHYTO PLANKTON (DMSP) DMSP Oceanic DMS Ingestion Digestion and excretion ZOO PLANKTON (DMSP) DMS + Acrylic acid Variation in DMS seawater concentrations around a frontal zone (Sciare et al. 1999) The study system Africa Kerguelen Antarctic prion (Pachipitila desolata) The lab Establishing physiological sensitivity to the odor cue: Cardiac monitoring Hypothesis: Birds respond to an odor presentation with a change in resting heart rate Methods: Establish resting heart rate Present test subject with either odor (DMS) or control (water) stimulus using a vapor dilution olfactometer Record heart rate. (e.g., Benvenuti, et al. 1992) Cardiac monitoring bird Antarctic prions respond to DMS at 3-4 nM concentrations Mean change in heart rate (bpm) Cardiac Monitoring 50 p<0.01 40 N=10 30 20 10 0 DMS (Nevitt and Bonadonna, submitted) Control Behavioral orientation to the odor cue: Y maze testing TEST ODOR: DMS in ethylene glycol CONTROL ODOR: ethylene glycol (e.g., Bonadonna and Nevitt, 2004) Behavioral orientation to the odor cue: Y maze testing TEST ODOR: DMS in ethylene glycol CONTROL ODOR: ethylene glycol (e.g., Bonadonna and Nevitt, 2004) Antarctic prions respond to DMS at biogenic (< pM) concentrations Y-Maze Testing 100 % Choice 80 p<0.01 N=24 60 40 20 0 DMS (Nevitt and Bonadonna, submitted) Control No choice Can procellariiform seabirds detect DMS? Conclusions: Antarctic prion adults can detect DMS at biologically relevant levels. What about at sea? Behavioral experiments at sea A good day Attraction to Scented Slicks Experimental Design ship 100 meters control slick wind odor slick Basic Behavior Assumptions: odor olfactory wind visual % increase in bird sightings after odor deployment SAMPLE DATA 350 Wilson’s storm-petrel 300 250 ODOR 200 150 100 CONTROL 50 0 -50 0 1 2 3 4 5 6 7 8 9 10 11 12 Time (min) (Nevitt, Reid and Trathan, 2004) Species Blue Petrel White-chinned Petrel Blk-bellied Storm-Petrel Unid. prion Wilson’s Storm-Petrel Unid. diving-petrel Black-browed Albatross Unid. giant petrel Wandering Albatross Cape Petrel Grey-headed Albatross Antarctic Fulmar Kerguelen Petrel % Krill in Diet 75 47-59 45 1-87 40-85 15-78 35-39 5-33 10 2-85 15-17 2-90 <2 Response Comparison DMS PYR Cod X X X X X 0 0 0 0 0 0 ND ND X X 0 0 0 0 X X X X 0 X X (0 = no response; X= positive response; ND = no data) X X X X X 0 X X X X 0 X X Some key observations (South Georgia) Some species respond to visual cues and macerated krill Other species track DMS and… Feeding frenzy! (Photo by G. Robertson) At small scales, Procellariiforms use different olfactory foraging strategies to find prey DMS DMSP DMS DMSP DMS DMSP PYR DMS DMSP PYR DMS DMSP DIFFERENTSENSORY FORAGING STRATEGIES “opportunistic olfactory vs. multimodal” Opportunistic: DMS RESPONDERS • are cryptically colored / smaller • tend to nest in burrows • are more vulnerable to predation Multimodal: KRILL / VISUAL RESPONDERS • tend to be highly visible / larger • nest above ground • are less vulnerable to predation Could differences be shaped by life history? Surface nester Burrow nester Could chicks be learning other information as well? Dr. Rich VanBuskirk (he’s the one on the left) Shearwaters Prions Fulmars Gadflys Nunn & Stanley 1998 Parsimony consensus tree 1143 bases of cytochrome b (mitochondrial DNA) Diving petrels Storm Petrels Albatross Tree pruned to species tested at sea for response to odors Species Nesting DMS Krill Cod Daption capense S - + + Fulmarus glacialis S - + + Fulmarus glacialoides S n/a - n/a Macronectes giganteus S - + + Halobaena caerulea B + + + Pachyptila desolata B + - + Procellaria aequinoctialis B + + + Puffinus griseus B + + + Pelecanoides urinatrix B - - - Diomedea chionoptera S - - + Thalassarche chrysostoma S - - - Thalassarche melanophris S - + + Fregetta tropica B + - + Oceanites oceanicus B + - + Oceanodroma leucorhoa B + + + Evidence for Correlated Trait Evolution Likelihood ratio test of independent vs. dependent trait evolution using Pagel’s (1994) Markov model. White-chinned Petrel Blue Petrel Antarctic Prion Sooty Shearwater Cape Petrel Northern Fulmar Giant Petrel Comm. Diving-Petrel Wandering Albatross Grey-head. Albatross Black-brow Albatross Black-bel. StormPetrel Wilson’s StormPetrel Leach’s StormPetrel Burrow Nesting DMS Trackers Present Absent Conclusions Nesting habit and DMS sensitivity show evidence for correlated trait evolution, but we don’t know which came first (VanBuskirk and Nevitt, submitted) Babies can be pre-tuned to prey-related scents via interactions with their parents. European rabbits Ferrets Humans Chickens Petrels fledge and forage without aid or instruction from parents. Could odors brought in by the parents provide them with information about their foraging habitat? Does pre-exposure to an odor influence behavior? RESPONSE TO PEA? RESPONSE TO PEA? egg ~3 weeks (Thin-billed prions) Testing arena Flow Straightener 80 cm Fan vent 60 cm 60 cm START position odor Head Turns Response to PEA * 1 0 ns 2 Head turns / min Head turns / min 2 Response to control 1 0 PEA EXP CONT EXP PEA EXP CONT EXP PRE-EXPOSURE TREATMENT N=12 for PEA-exp group; N=11 for CONTROL-exp group *P<0.05, Wilcoxon signed-rank test (Nevitt et al, in prep) Conclusions Chicks may be able to learn about their foraging environment even before leaving the nest. So how do naïve chicks respond to biogenic odors? The literature suggested that we shouldn’t do electrophysiology… “... And I had done a hellish thing And it would work ‘em woe; For all aver’d I had kill’d the bird That made the breeze to blow. Ah, Wretch! said they, the bird to slay That made the breeze to blow!” - Samuel Taylor Coleridge “Rhyme of the Ancient Mariner” Average Score (0-3) Blue petrels 2.0 (μm) 1.5 ** * 1.0 0.5 0.0 Control DMS (Wilcoxon signed rank test, p<0.05 and p<0.01, respectively; n=30) PEA (Cunningham et al. 2003) Average Score (0-3) Common Diving Petrels 2.0 1.5 (μm) • No significant difference (Wilcoxon signed rank test, 1.0 p = 0.22; n=28) 0.5 0.0 Control DMS n=29 PEA (Cunningham et al. 2003) (A) 1.5 AVERAGE SCORE (0-3) Blue petrels Chicks (unfed vs. fed) 1.0 0.5 0.0 CC pM nM nM mM .1 mM fM pM uM (B) 1.5 1.0 0.5 0.0 CC pM mM fM nM pM mM nM .1uM Conclusion Chicks are sensitive to DMS at biogenic concentrations. Behavioral orientation to the odor cue: Y maze testing TEST ODOR: DMS in ethylene glycol CONTROL ODOR: ethylene glycol (e.g., Bonadonna and Nevitt, 2004) “Naïve” fledgling blue petrels also respond to DMS at biogenic (< pM) concentrations Y-Maze Testing Blue petrel (Halobaena caerulea) 100 p < 0.01 % Choice 80 N=20 60 40 20 0 DMS (Bonadonna et al., just off the boat) Control No Choice Talk Summary 1. We have found evidence that different species use different sensory strategies to forage. 2. We have found evidence for correlated trait evolution: Our combined results suggest that burrow- nesting species are super smellers 3. Experimental results suggest that chicks already have a well developed sense of smell before leaving the nest. 4. There is the potential for olfactory tuning. Chicks may be able to learn about their foraging environment even before leaving the nest. Epilogue “Doubt is not a pleasant condition, but certainty is absurd." -Voltaire “Never, never, never, never give up.” -Churchill “if a frog had wings, he wouldn’t hit his tail on the ground.” -Bush THANK YOU South Geogia : Peter Karieva, Peter Prince, Keith Reid, Emily Silverman, Phil Trathan, Richard Veit Crozet / Kergeulen: Dana Bergstrom, Francesco Bonadonna, Greg Cunningham, Mark Hodges, Rich VanBuskirk, Henri Weimerskirch Elephant Island / Seal Island: Danny Grunbaum, Roger Hewit Unimak Pass, AK: George Hunt Kent Island: Alexis Blackmer, Karen Haberman, Nathaniel Wheelwright THANK YOU! –S–CH3 CH3