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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.

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Presentation on theme: "Seeing the world through the nose of a bird: exploring the sensory ecology of Procellariiform seabirds Dr. Gabrielle Nevitt, Associate Professor University."— Presentation transcript:

1 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)

2 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, 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. 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 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 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 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

3 Some Antarctic procellariiform seabirds

4 The procellariiforms: (petrels, albatrosses and shearwaters) Olfactory systems are well developed. Olfactory systems are well developed. Species are highly pelagic. Species are highly pelagic. Food resources are patchily distributed over vast areas so… Food resources are patchily distributed over vast areas so… Many species commonly forage and navigate over extreme distances. Many species commonly forage and navigate over extreme distances.

5 Nearly all procellariiforms have highly developed olfactory system (Bang 1966) Cross section through the peripheral olfactory system

6 krillfishsquid

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8 Procellariiform seabirds routinely travel extreme Procellariiform seabirds routinely travel extreme distances over featureless ocean Wilson’s storm petrel

9 South Georgia Kergeulen Wandering albatross

10 Movement Patterns of Wandering Albatrosses East South South Africa (Shaffer et al. 2001, 2003)

11 Commuting Scavenging Different large-scale foraging strategies

12 Procellariiforms have different life history characteristics

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14 Can birds detect odors emitted from their prey? This turns out to be the wrong question.

15 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.

16 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.

17 shelf breaks frontal zones sea mounts (Nevitt, et al. Nature 1995) New concept: Navigation by Olfactory Landscapes Scented compounds are predictably elevated where productivity is high

18 (Nevitt, 2000) navigation large scale small scale Olfactory Landscapes

19 Dimethyl sulphide (DMS) is an important signal molecule in the marine environment Latitude Longitude (Data from Kettle, et al. 1999) (nmol L -1 ) DMS Oceanic Concentrations 10.0 1.0 0.1

20 Chlorophyll concentrations around Kerguelen Like DMS, chlorophyll occurs in predictable Locations and is associated with productive areas of ocean Kerguelen 25 o S, 40 o -75 o E 54 o S, 40 o -75 o E (Courtesy of SeaWiFS Project data base)

21 OceanicDMS Metabolism and senescence Metabolism and excretion PHYTO PLANKTON (DMSP) ZOO PLANKTON (DMSP) DMSP DMS + Acrylic acid AtmosphericDMS (adapted from Dacey and Wakham, 1986)

22 OceanicDMS Metabolism and senescence Digestion and andexcretion PHYTO PLANKTON (DMSP) ZOO PLANKTON (DMSP) Ingestion DMSP DMS + Acrylic acid DMS hotspots

23 Variation in DMS seawater concentrations around a frontal zone (Sciare et al. 1999)

24 Kerguelen Africa Antarctic prion (Pachipitila desolata) The study system

25 The lab

26 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) Establishing physiological sensitivity to the odor cue: Cardiac monitoring

27 bird Cardiac monitoring

28 Mean change in heart rate (bpm) DMSControl 0 10 20 30 40 50 p<0.01 Cardiac Monitoring N=10 Antarctic prions respond to DMS at 3-4 nM concentrations (Nevitt and Bonadonna, submitted)

29 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)

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31 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)

32 Y-Maze Testing DMSControlNo choice % Choice 0 20 40 60 80 100 p<0.01 N=24 Antarctic prions respond to DMS at biogenic (< pM) concentrations (Nevitt and Bonadonna, submitted)

33 Can procellariiform seabirds detect DMS? Conclusions: Antarctic prion adults can detect DMS at biologically relevant levels.

34 What about at sea?

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36 A good day Behavioral experiments at sea

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38 ship control slick odor slick wind 100 meters Attraction to Scented Slicks Experimental Design

39 wind odor visual olfactory Basic Behavior Assumptions:

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41 CONTROL ODOR Wilson’s storm-petrel SAMPLE DATA

42 (0 = no response; X= positive response; ND = no data) (Nevitt, Reid and Trathan, 2004)

43 Some species respond to visual cues and macerated krill Other species track DMS Some key observations (South Georgia) and… and…

44 Feeding frenzy! (Photo by G. Robertson)

45 At small scales, Procellariiforms use different olfactory foraging strategies to find prey

46 DMS DMSP

47 DMS

48 DMSP

49 PYR DMS

50 DMSP PYR DMS

51 DIFFERENTSENSORY FORAGING STRATEGIES “opportunistic olfactory vs. multimodal” Opportunistic: DMS RESPONDERS are cryptically colored / smaller are cryptically colored / smaller tend to nest in burrows tend to nest in burrows are more vulnerable to predation are more vulnerable to predation Multimodal: KRILL / VISUAL RESPONDERS tend to be highly visible / larger tend to be highly visible / larger nest above ground nest above ground are less vulnerable to predation are less vulnerable to predation

52 Could differences be shaped by life history?

53 Surfacenester Burrow nester nester

54 Could chicks be learning other information as well?

55 Dr. Rich VanBuskirk (he’s the one on the left)

56 Prions Shearwaters FulmarsGadflys Albatross Storm PetrelsDiving petrels Nunn & Stanley 1998 Parsimony consensus tree 1143 bases of cytochrome b (mitochondrial DNA)

57 SpeciesNestingDMSKrillCod Daption capenseS-++ Fulmarus glacialisS-++ Fulmarus glacialoidesSn/a- Macronectes giganteusS-++ Halobaena caeruleaB+++ Pachyptila desolataB+-+ Procellaria aequinoctialisB+++ Puffinus griseusB+++ Pelecanoides urinatrixB--- Diomedea chionopteraS--+ Thalassarche chrysostomaS--- Thalassarche melanophrisS-++ Fregetta tropicaB+-+ Oceanites oceanicusB+-+ Oceanodroma leucorhoaB+++ Tree pruned to species tested at sea for response to odors

58 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 Evidence for Correlated Trait Evolution Likelihood ratio test of independent vs. dependent trait evolution using Pagel’s (1994) Markov model. PresentAbsent

59 Nesting habit and DMS sensitivity show evidence for correlated trait evolution, but we don’t know which came first Conclusions (VanBuskirk and Nevitt, submitted)

60 European rabbits European rabbits Ferrets Ferrets Humans Humans Chickens 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? Babies can be pre-tuned to prey-related scents via interactions with their parents.

61 RESPONSE TO PEA? egg ~3 weeks Does pre-exposure to an odor influence behavior? (Thin-billed prions)

62 Fan vent Flow Straightener 60 cm 80 cm 60 cm START position odor Testing arena

63 PRE-EXPOSURE TREATMENT N=12 for PEA-exp group; N=11 for CONTROL-exp group Head Turns * *P<0.05, Wilcoxon signed-rank test (Nevitt et al, in prep) ns

64 Chicks may be able to learn about their foraging environment even before leaving the nest. So how do naïve chicks respond to biogenic odors? Conclusions

65

66 “... 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 - Samuel Taylor Coleridge “Rhyme of the Ancient Mariner” “Rhyme of the Ancient Mariner” The literature suggested that we shouldn’t do electrophysiology…

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68 Blue petrels (Wilcoxon signed rank test, p<0.05 and p<0.01, respectively; n=30) (Cunningham et al. 2003) (μm)

69 Common Diving Petrels No significant difference (Wilcoxon signed rank test, p = 0.22; n=28)No significant difference (Wilcoxon signed rank test, p = 0.22; n=28) (Cunningham et al. 2003) (μm) n=29

70 Blue petrels Chicks (unfed vs. fed) C pM nM  M.1 mM C pM nM  M.1 mM

71 Chicks are sensitive to DMS at biogenic concentrations. Conclusion

72 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)

73 Y-Maze Testing “Naïve” fledgling blue petrels also respond to DMS at biogenic (< pM) concentrations (Bonadonna et al., just off the boat) Blue petrel (Halobaena caerulea)

74 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.

75 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

76 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

77 THANK YOU! –S– CH3


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