Transcript DMS

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
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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)
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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.
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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