Seeing the world through the nose Seeing the world through the nose of a bird: exploring the sensory of a bird: exploring the sensory

ecology of Procellariiform seabirdsecology of Procellariiform seabirdsDr. Gabrielle Nevitt, Associate ProfessorDr. Gabrielle Nevitt, Associate Professor

University of California, DavisUniversity of California, Davis

Logistical support and funding provided by:Logistical support and funding provided by:

CNRS / IPEV (France); BAS (UK)CNRS / IPEV (France); BAS (UK)NSF Polar Programs and NSF Sensory Biology (USA)NSF Polar Programs and NSF Sensory Biology (USA)

Some publications pertinent to this Some publications pertinent to this talk:talk:

Nevitt, GA, Veit RR, and Kareiva P. 1995. Dimethyl sulfide as a Nevitt, GA, Veit RR, and Kareiva P. 1995. Dimethyl sulfide as a foraging cue for Antarctic procellariiform seabirds. foraging cue for Antarctic procellariiform seabirds. NatureNature 376, 680- 376, 680-682. 682.

Nevitt, GA. 2000. Olfactory Foraging by Antarctic Procellariiform Nevitt, GA. 2000. Olfactory Foraging by Antarctic Procellariiform Seabirds: Life at High Reynolds Numbers. Seabirds: Life at High Reynolds Numbers. Biological BulletinBiological Bulletin, 198, , 198, 245-253245-253

Nevitt GA, Reid K and Trathan P. 2004. Testing olfactory foraging Nevitt GA, Reid K and Trathan P. 2004. Testing olfactory foraging strategies in an Antarctic seabird assemblage. strategies in an Antarctic seabird assemblage. Journal of Journal of Experimental BiologyExperimental Biology, 207, 3537-3544, 207, 3537-3544

Silverman ED, Veit RR and Nevitt GA. 2004. Nearest neighbors as Silverman ED, Veit RR and Nevitt GA. 2004. Nearest neighbors as foraging cues: information transfer in a patchy environment. foraging cues: information transfer in a patchy environment. Marine Ecology Progress SeriesMarine Ecology Progress Series, 277, 25-35, 277, 25-35

Bonadonna F and Nevitt GA. 2004. Partner-specific odor recognition Bonadonna F and Nevitt GA. 2004. Partner-specific odor recognition in an Antarctic Seabird. in an Antarctic Seabird. ScienceScience, 306, 835 , 306, 835

http://www.npb.ucdavis.edu/npbdirectory/nevitt.html

Some Antarctic Some Antarctic procellariiform seabirdsprocellariiform seabirds

The procellariiforms:The procellariiforms: (petrels, albatrosses and shearwaters)(petrels, albatrosses and shearwaters)

Olfactory systems are well Olfactory systems are well developed.developed.

Species are highly pelagic.Species are highly pelagic. Food resources are patchily Food resources are patchily

distributed over vast areas so…distributed over vast areas so… Many species commonly forage Many species commonly forage

and navigate over extreme and navigate over extreme distances.distances.

Nearly all procellariiforms have Nearly all procellariiforms have highly developed olfactory systemhighly developed olfactory system

(Bang 1966)(Bang 1966)Cross section through Cross section through

the the peripheral olfactory peripheral olfactory

systemsystem

krillkrillfishfishsquidsquid

SQUIDKRILL FISH

WANDERING ALBATROSSSOUTH GEORGIA BREEDING SEASON

(CROXALL 1984)

BLACK BROWED ALBATROSSSOUTH GEORGIA BREEDING SEASON

(CROXALL 1984)

SQUIDKRILLFISHOTHER

Procellariiform seabirds routinely travel extreme Procellariiform seabirds routinely travel extreme distances over featureless oceandistances over featureless ocean

Wilson’s storm petrelWilson’s storm petrel

South GeorgiaSouth Georgia

KergeulenKergeulen

Wandering albatross

Movement Patterns of Wandering Albatrosses

EastEast

Sou

thS

outh

South

Africa

(Shaffer et al. 2001, 2003)

CommutingCommuting

ScavengingScavenging

Different large-scale foraging strategiesDifferent large-scale foraging strategies

Procellariiforms have different life history characteristics

Can birds detect odors emitted Can birds detect odors emitted from their prey?from their prey?

This turns out to be the This turns out to be the wrong question.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.

•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

(Nevitt, 2000)(Nevitt, 2000)

navigation large scale small navigation large scale small scalescale

Olfactory LandscapesOlfactory Landscapes

Dimethyl sulphide (DMS) is an Dimethyl sulphide (DMS) is an important signal molecule in the important signal molecule in the marine environmentmarine environment

Lat

itud

e

Longitude(Data from Kettle, et al. 1999)

(nmol L-1)DMS Oceanic ConcentrationsDMS Oceanic Concentrations

10.0

1.0

0.1

Chlorophyll concentrations around Chlorophyll concentrations around Kerguelen Kerguelen Like DMS, chlorophyll occurs in predictable Like DMS, chlorophyll occurs in predictable

Locations and is associated with productive areas of oceanLocations and is associated with productive areas of ocean

Kerguelen

25oS, 40o-75oE

54oS, 40o-75oE

(Courtesy of SeaWiFS Project data base)

OceanicOceanicDMSDMS

MetabolismMetabolism

and and senescencesenescence

Metabolism Metabolism andand

excretionexcretion

PHYTO PLANKTONPHYTO PLANKTON(DMSP)(DMSP)

ZOO PLANKTONZOO PLANKTON(DMSP)(DMSP)

DMSPDMSP DMS + Acrylic acid DMS + Acrylic acid

AtmosphericAtmosphericDMSDMS

(adapted from Dacey and Wakham, 1986)

OceanicOceanicDMSDMS

MetabolismMetabolism

and and senescencesenescence

DigestionDigestion and and

excretionexcretion

PHYTO PLANKTONPHYTO PLANKTON(DMSP(DMSP))

ZOO PLANKTONZOO PLANKTON(DMSP)(DMSP)

IngestionIngestion

DMSPDMSP DMS + Acrylic acid DMS + Acrylic acid

DMS hotspotsDMS hotspots

Variation in DMS seawater Variation in DMS seawater concentrations around a concentrations around a frontal zonefrontal zone

(Sciare et al. 1999)

KerguelenAfrica

Antarctic prion (Antarctic prion (Pachipitila desolataPachipitila desolata))

The study systemThe study system

The lab

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 Establishing physiological sensitivity to the odor cue: odor cue: Cardiac monitoringCardiac monitoring

birdbird

Cardiac monitoringCardiac monitoring

Mea

n ch

ange

in h

eart

rat

e (b

pm)

DMS Control

0

10

20

30

40

50p<0.01

Cardiac MonitoringCardiac Monitoring

N=10N=10

Antarctic prions respond to DMSAntarctic prions respond to DMSat 3-4 nM concentrationsat 3-4 nM concentrations

(Nevitt and Bonadonna, submitted)(Nevitt and Bonadonna, submitted)

Behavioral orientation to the odor cueBehavioral orientation to the odor cue: : Y maze testingY maze testing

TEST ODOR:DMS in ethylene glycol

CONTROL ODOR:ethylene glycol

(e.g., Bonadonna and Nevitt, 2004)

Behavioral orientation to the odor cueBehavioral orientation to the odor cue: : Y maze testingY maze testing

TEST ODOR:DMS in ethylene glycol

CONTROL ODOR:ethylene glycol

(e.g., Bonadonna and Nevitt, 2004)

Y-Maze TestingY-Maze Testing

DMS Control No choice

% C

hoic

e

0

20

40

60

80

100

p<0.01

N=24N=24

Antarctic prions respond to DMSAntarctic prions respond to DMSat biogenic (< pM) concentrationsat biogenic (< pM) concentrations

(Nevitt and Bonadonna, submitted)(Nevitt and Bonadonna, submitted)

Can procellariiform seabirds Can procellariiform seabirds detect DMS?detect DMS?

Conclusions: Conclusions:

Antarctic prion adults can Antarctic prion adults can detect DMS at biologically detect DMS at biologically relevant levels. relevant levels.

What about at sea?What about at sea?

A good dayA good day

Behavioral experiments at Behavioral experiments at seasea

ship

control slick

odor slick

wind

100 meters

Attraction to Scented SlicksExperimental Design

wind

odor

visual

olfactory

Basic Behavior Assumptions:

0 1 2 3 4 5 6 7 8 9 10 11 12-50

0

50

100

150

200

250

300

350%

incr

ease

in

bir

d s

igh

tin

gs

afte

r o

do

r d

eplo

ymen

t

Time (min)

CONTROLCONTROL

ODORODOR

Wilson’s storm-petrelWilson’s storm-petrel

SAMPLE DATASAMPLE DATA

Response Comparison Species % Krill

in Diet DMS PYR Cod

Blue Petrel 75 X X X White-chinned Petrel 47-59 X X X Blk-bellied Storm-Petrel 45 X 0 X Unid. prion 1-87 X 0 X Wilson’s Storm-Petrel 40-85 X 0 X Unid. diving-petrel 15-78 0 0 0 Black-browed Albatross 35-39 0 X X Unid. giant petrel 5-33 0 X X Wandering Albatross 10 0 X X Cape Petrel 2-85 0 X X Grey-headed Albatross 15-17 0 0 0 Antarctic Fulmar 2-90 ND X X Kerguelen Petrel <2 ND X X

(0 = no response; X= positive response; ND = no data)

(Nevitt, Reid and Trathan, 2004)(Nevitt, Reid and Trathan, 2004)

Some species respond to

visual cues and macerated krill

Other species track DMS

Some key observations (South Georgia)Some key observations (South Georgia)

andand……

Feeding frenzy!Feeding frenzy!

(Photo by G. Robertson)

At small scales, Procellariiforms

use different olfactory foraging

strategies to find prey

DMS

DMSP

DMSP

DMS

DMS

DMSP

DMSP

PYR

DMS

DMSP

PYRDMS

DIFFERENTSENSORY FORAGING STRATEGIESDIFFERENTSENSORY FORAGING STRATEGIES““opportunistic olfactory vs. opportunistic olfactory vs. multimodal” multimodal”

Opportunistic: DMS RESPONDERSOpportunistic: DMS RESPONDERS• are cryptically colored / smallerare cryptically colored / smaller• tend to nest in burrowstend to nest in burrows• are more vulnerable to predationare more vulnerable to predation

Multimodal: KRILL / VISUAL RESPONDERSMultimodal: KRILL / VISUAL RESPONDERS• tend to be highly visible / largertend to be highly visible / larger• nest above groundnest above ground• are less vulnerable to predationare less vulnerable to predation

Could differences be shaped bylife history?

Surface Surface nesternester

BurrowBurrow nesternester

Could chicks be learning other Could chicks be learning other information as well?information as well?

Dr. Rich VanBuskirkDr. Rich VanBuskirk

(he’s the one on the left)(he’s the one on the left)

Prions

Shearwaters

Fulmars GadflysAlbatross

Storm PetrelsDivingpetrels

Nunn & Stanley 1998Parsimony consensus tree1143 bases of cytochrome b(mitochondrial DNA)

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 + + +

Tree pruned to species tested at sea for response to odors

White-chinned Petrel

Blue Petrel

Antarctic Prion

Sooty Shearwater

Cape PetrelNorthern Fulmar

Giant Petrel

Comm. Diving-Petrel

Wandering Albatross

Grey-head. Albatross

Black-brow AlbatrossBlack-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.

Present Absent

Nesting habit and DMS Nesting habit and DMS sensitivity show evidence forsensitivity show evidence for

correlated traitcorrelated traitevolution, but we don’t know evolution, but we don’t know

which came firstwhich came first

ConclusionsConclusions

(VanBuskirk and Nevitt, submitted)(VanBuskirk and Nevitt, submitted)

European rabbitsEuropean rabbits FerretsFerrets HumansHumans ChickensChickens

Petrels fledge and forage without aid or Petrels fledge and forage without aid or instruction from parents. instruction from parents. Could odors Could odors brought in by the parents provide them brought in by the parents provide them with information about their foraging with information about their foraging habitat?habitat?

Babies can be pre-tuned to prey-related scents via Babies can be pre-tuned to prey-related scents via interactions with their parents.interactions with their parents.

RESPONSE TO PEA?RESPONSE TO PEA?

RESPONSE TO PEA?RESPONSE TO PEA?

eggegg ~3 weeks~3 weeks

Does pre-exposure to an odor influence behavior?Does pre-exposure to an odor influence behavior?

(Thin-billed prions)(Thin-billed prions)

Fan vent

FlowStraightener

60 cm

80 cm

60 cm

STARTposition

odorodor

Testing arenaTesting arena

Response to control

PEA EXP CONT EXP

He

ad

tu

rns

/ m

in

0

1

2

Response to PEA

PEA EXP CONT EXP

He

ad

tu

rns

/ m

in

0

1

2

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)

nsns

Chicks may be able to Chicks may be able to learn about their foraging learn about their foraging environment even before environment even before

leaving the nest.leaving the nest.

So how do naïve chicks So how do naïve chicks respond to biogenic odors?respond to biogenic odors?

ConclusionsConclusions

““... And I had done a hellish thing... And I had done a hellish thingAnd it would work ‘em woe;And it would work ‘em woe;For all aver’d I had kill’d the birdFor all aver’d I had kill’d the birdThat made the breeze to blow.That made the breeze to blow.Ah, Wretch! said they, the bird to slayAh, Wretch! said they, the bird to slayThat made the breeze to blow!”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 weThe literature suggested that weshouldn’t do electrophysiology…shouldn’t do electrophysiology…

Blue petrels

Control DMS PEA

Ave

rage

Sco

re (

0-3)

0.0

0.5

1.0

1.5

2.0

*

**

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

(μm)(μm)

Common Diving Petrels

• No significant difference No significant difference (Wilcoxon signed rank test, (Wilcoxon signed rank test,

p = 0.22; n=28)p = 0.22; n=28)

Control DMS PEA

Ave

rage

Sco

re (

0-3)

0.0

0.5

1.0

1.5

2.0

(Cunningham et al. 2003)(Cunningham et al. 2003)

(μm)(μm)

n=29n=29

Blue petrels Chicks

(unfed vs. fed)

C fM pM nM uM

AV

ER

AG

E S

CO

RE

(0-

3)

0.0

0.5

1.0

1.5

C fM pM nM uM0.0

0.5

1.0

1.5

(A)

(B)

C pM nM C pM nM M .1 M .1 mMmM

C pM nM C pM nM M .1 M .1 mMmM

Chicks are sensitive to Chicks are sensitive to DMSDMS

at biogenic at biogenic concentrations.concentrations.

ConclusionConclusion

Behavioral orientation to the odor cueBehavioral orientation to the odor cue: : Y maze testingY maze testing

TEST ODOR:DMS in ethylene glycol

CONTROL ODOR:ethylene glycol

(e.g., Bonadonna and Nevitt, 2004)

Y-Maze TestingY-Maze Testing

““Naïve” fledgling blue petrels also respond to Naïve” fledgling blue petrels also respond to DMS at biogenic (< pM) concentrationsDMS at biogenic (< pM) concentrations

(Bonadonna et al., just off the boat)(Bonadonna et al., just off the boat)

DMS Control No Choice

% C

hoic

e

0

20

40

60

80

100p < 0.01

N=20

Blue petrel (Halobaena caerulea)

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.

EpiloguEpiloguee

“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 YOUTHANK YOUSouth Geogia :South Geogia : Peter Karieva, Peter Prince, Peter Karieva, Peter Prince, Keith Reid, Emily Silverman, Phil Trathan, Keith Reid, Emily Silverman, Phil Trathan, Richard VeitRichard Veit

Crozet / Kergeulen:Crozet / Kergeulen: Dana Bergstrom, Dana Bergstrom, Francesco Bonadonna, Greg Cunningham, Francesco Bonadonna, Greg Cunningham, Mark Hodges,Mark Hodges, Rich VanBuskirk, Henri Rich VanBuskirk, Henri WeimerskirchWeimerskirch

Elephant Island / Seal Island:Elephant Island / Seal Island: Danny Danny Grunbaum, Roger HewitGrunbaum, Roger Hewit

Unimak Pass, AK:Unimak Pass, AK: George Hunt George Hunt

Kent Island:Kent Island: Alexis Blackmer, Karen Alexis Blackmer, Karen Haberman,Haberman, Nathaniel Wheelwright Nathaniel Wheelwright

THANK YOU!THANK YOU!

–S–

CH3

CH3