squirrels versus rattlesnakes: the evolution of unique antipredator behavior barbara clucas, phd...
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Squirrels versus Squirrels versus Rattlesnakes: Rattlesnakes:
the Evolution of Unique the Evolution of Unique Antipredator BehaviorAntipredator Behavior
Barbara Clucas, PhDCollege of the EnvironmentUniversity of Washington
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Animal BehaviorAnimal Behavior
• The study of how animals use behavior to survive and reproduce
• How and why behavior evolves
• Social, reproductive, movement, antipredator
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Animal BehaviorAnimal Behavior
• The study of how animals use behavior to survive and reproduce
• How and why behavior evolves
• Social, reproductive, movement, antipredator
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Antipredator BehaviorAntipredator Behavior
• Reduce the risk of predation
• Most animals are prey
• Evolution of a vast array of antipredator behavior
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Antipredator BehaviorAntipredator Behavior
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Ground Squirrels Ground Squirrels ((SpermophilusSpermophilus))
• Diverse genus of species
• Worldwide distribution (except Australia and Antarctica)
• Live in burrows in the ground
• Species vary in habitats and sociality
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Ground squirrel predatorsGround squirrel predators
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Ground squirrel predatorsGround squirrel predators
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Rattlesnakes Rattlesnakes ((CrotalusCrotalus))
• Warning rattle• Venomous• Skilled rodent predators
– Lethal venom– Acute sense of sight and
smell– Pit organs can sense
temperature changes
rattle
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Ground squirrel defensesGround squirrel defenses
• Venom resistant • Harass, attack
rattlesnakes• Tail-flagging
– visual and infrared signal
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Rattlesnakes are still predators…Rattlesnakes are still predators…
• Ground squirrel pups– Not large enough to be
venom resistant– Anti-snake behavior not
fully developed– Depend on adults for
protection (especially their mothers)
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Recent discoveryRecent discovery
• Another unique snake-related behavior found in certain species of ground squirrels
• “Snake scent application”
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Snake Scent ApplicationSnake Scent Application
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Snake Scent Application (SSA)Snake Scent Application (SSA)
1. Why are squirrels applying rattlesnake scent?• Test 3 functional hypotheses
2. Evolutionary history• Phylogenetic comparative methods
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Functional hypotheses of SSAFunctional hypotheses of SSA
1. Antipredator
2. Social
3. Ectoparasitic defense
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1. Antipredator1. Antipredator
• SSA disguises squirrel odor– Rattlesnakes
may bypass burrows with snake-scented squirrels
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2. Social2. Social
• Conspecific deterrence
• SSA deters rivals– Snake-scented
squirrels win more aggressive encounters
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3. Ectoparasite defense3. Ectoparasite defense
• SSA reduces fleas
– Flea host-finding behavior affected by snake scent
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Testing hypotheses of functionTesting hypotheses of function
• Study 1: Time spent applying snake scent
– Which squirrels apply more?
• Study 2: Series of experiments directly testing targets
– What are the effects of snake scent?
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Study 1: Study 1: Which squirrels SSA more?Which squirrels SSA more?
Study species
• California ground squirrel, (S. beecheyi)
– Winters, California
• Rock squirrel, (S. variegatus) – Caballo, New Mexico
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• Trapped and marked squirrels
• Recorded:– sex– age– flea load
Study 1: Study 1: Which squirrels SSA more?Which squirrels SSA more?
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• Staked out shed rattlesnake skins
• Filmed individual squirrels
• Recorded duration of SSA
Quantifying application behaviorQuantifying application behavior
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PredictionsPredictions
1. Antipredator• adult females & pups > adult males
2. Conspecific deterrence• adult males > adult females & pups
3. Ectoparasite defense• time spent related to flea load• pups > adults
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Adult females & pups > adult malesAdult females & pups > adult males
*P < 0.005; Error bars = SE Clucas et al. 2008, Anim Behav
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SSA not related to flea loadSSA not related to flea load
None Low Med High
Spearman rank correlation: rs: -0.033, N=45, P=0.829 Clucas et al. 2008, Anim Behav
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Study 1:Study 1: Antipredator hypothesis supportedAntipredator hypothesis supported
• Pups most susceptible to predation, adult females share burrows with and protect their pups
• No support for alternative hypotheses– squirrels with more fleas do not apply more– most aggressive squirrels (adult males) do
not SSA the most
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Study 2: What are the effects of snake scent?Study 2: What are the effects of snake scent?
• Experiment 1: Rattlesnake foraging behavior
• Experiment 2: Squirrel behavior before and after
applying
• Experiment 3: Flea host choice
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Rattlesnake Foraging BehaviorRattlesnake Foraging Behavior
Experiment 1Experiment 1
N = 8
C. oreganus oreganus
• 3 scent-type trials1. Ground squirrel2. Ground squirrel
+Rattlesnake3. Rattlesnake
• Water control
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Rattlesnake Foraging BehaviorRattlesnake Foraging Behavior
• Behavior scored– Time spent over– Tongue-flicking
Experiment 1Experiment 1
N = 8
C. oreganus oreganus
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Repeated measures GLM: F2,14=4.667, P = 0.028; planned
comparisons: all P<0.05
Experiment 1Experiment 1
Spent more time over ‘squirrel’Spent more time over ‘squirrel’
888 888N =
Scent Type
Squirrel+RattlesnakeRattlesnakeSquirrel
Tim
e O
ver
(sec
on
ds)
+/-
SE
250
200
150
100
50
0
- 50
Scent
Water
Clucas et al. 2008, PRSL
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Repeated measures GLM: F2,14=4.478, P = 0.031;
planned comparisons: Sq>R P=0.03, Sq>S+R P=0.07
Experiment 1Experiment 1
Tongue flicked more over ‘squirrel’Tongue flicked more over ‘squirrel’
888 888N =
Scent Type
Squirrel+RattlesnakeRattlesnakeSquirrel
Ton
gue
Flic
ks +
/- S
E
100
80
60
40
20
0
- 20
Scent
Water
Clucas et al. 2008, PRSL
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Experiment 2Experiment 2
Before and After SSA behaviorBefore and After SSA behavior
SCENTED
Pre-trial SSA trial Post-trial
CONTROLS
Pre-trial No SSA trial Post-trial
24-48 hours 24-48 hours
24-48 hours 24-48 hours
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Experiment 2Experiment 2
Before and After SSA behaviorBefore and After SSA behavior
• Recorded:– Social interactions (aggressive or tolerant)
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CONTROLS
* No differences between before and after
Experiment 2Experiment 2
Social InteractionsSocial Interactions
SCENTED
* No differences between before and after
Repeated Measures GLM; P>0.05 Clucas et al. 2008, PRSL
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Flea host choiceFlea host choice
• Juvenile ground squirrels as hosts
• Fleas – Removed from
ground squirrels
Experiment 3Experiment 3
Control Flea SSA Squirrel starting Squirrel point
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Flea host choiceFlea host choice
• Flea behavior recorded– Choice– Latency to move– Choice latency
Experiment 3Experiment 3
Control Flea SSA Squirrel starting Squirrel point
??
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Fleas not affected by snake scentFleas not affected by snake scent
• No significant difference in choice (2
1=0.455, N=56, P=0.500)
• Latencies did not differ by choice
– Latency to move: t53=0.661, P=0.512
– Choice latency: t53=-0.030, P=0.976
Experiment 3Experiment 3
==
Clucas et al. 2008, PRSL
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Study 2: Antipredator hypothesis supportedStudy 2: Antipredator hypothesis supported
• Rattlesnake foraging behavior affected by snake scent
• No support for alternative hypotheses– Neither conspecific behavior nor flea
behavior affected by snake scent
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Function of Applying Function of Applying Snake ScentSnake Scent
• All evidence supports an antipredator function
• Olfactory camouflage– Snakes did not avoid
rattlesnake scent, rather showed low foraging behavior
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Evolutionary history Evolutionary history
• Explore the origins of applying snake scent
– When did it evolve?
– What caused it to evolve?
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Studying evolutionary historyStudying evolutionary history
• Phylogenetic comparative methods
• Phylogenetic tree
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Evolutionary history Evolutionary history
?Common Ancestor
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Evolutionary history Evolutionary history
?
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Ground Ground squirrel squirrel
phylogenyphylogeny
• Molecular (cytochrome b)
• Divergence times– Time (in
million of years) when species diverged
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Comparative studyComparative study
• Tested multiple ground squirrel and chipmunk species with rattlesnake scent
• Recorded presence/absence of application behavior
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When did scent application originate?When did scent application originate?
• Ancestor state reconstruction
– estimate whether squirrel ancestors possessed the scent application trait using maximum likelihood analysis
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Ancestral State Reconstruction
• Common ancestor likely had behavior
• Behavior lost several times
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What caused SSA to evolve?What caused SSA to evolve?
• Is rattlesnake presence related to scent application?– Test with correlated
trait evolution analysis
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SSA Correlated with rattlesnake presenceSSA Correlated with rattlesnake presence
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Correlated Trait Evolution Correlated Trait Evolution Snake Scent Application (SSA)Snake Scent Application (SSA)
Transition qij Independent model
Dependent model
No Pred, No SSA to No Pred, SSA q12 0.06681 0.07035 Gain SSA Pred, No SSA to Pred, SSA q34 5.46777
No Pred, SSA to Pred, SSA q24 12.26164 Retain SSA Pred, SSA to No Pred, SSA q42 0.000002
No Pred, SSA to No Pred, No SSA q21 0.04732 1.36796 Lose SSA Pred, SSA to Pred, No SSA q43 0.06255
Pred, No SSA to No Pred, No SSA q31 0.04732 14.32849 No SSA No Pred, No SSA to Pred, No SSA q13 0.06681 0.0000003
L(I)
L(D)
L(R)
-11.5970 -5.1190 12.95 p<0.02
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However…However…
• Current predator presence
• What about historical co-occurrence?
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Historical predator presenceHistorical predator presence
• Fossil records – established
squirrel and rattlesnake co-occurrence in the past
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Historical predator presenceHistorical predator presence
• First squirrel fossil about 30 mya
• First squirrel-rattlesnake co-occurrence about 15 mya
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Squirrel and rattlesnake ancestors
• Behavior evolved before co-occurrence
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Original sources of selectionOriginal sources of selection
• Snake scent application evolved at least 28 mya– Rattlesnake ancestor not
present until 15 mya
• Original source of selection may have been older snake species (e.g., Boavus spp.)
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More Recent Past: 10-400 More Recent Past: 10-400 thousand years agothousand years ago
• Presently existing squirrel species
– Species that do not SSA did not historically co-occur with rattlesnakes
– Species that do SSA did historically co-occur with rattlesnakes
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Past and PresentPast and Present
• Typically species had both historic and present co-occurrence with rattlesnakes
• However, there were several exceptions…
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Interesting exceptions…Interesting exceptions…
• California ground squirrels in Davis, CA– Historically had
rattlesnakes – Ended about 9000 years
ago
• Do not apply snake scent
• Behavior rapidly lost
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Interesting exceptions…Interesting exceptions…
• Belding’s ground squirrels in MWR, OR– Did not have rattlesnakes
historically
– Currently do co-occur • Do not apply snake scent• Behavior not regainable?
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Final ConclusionsFinal Conclusions
• Squirrels apply predator scents to reduce predation risk
• Predator scent application is an evolutionarily ancient trait in squirrels
• Original source of selection unknown• Recent past, behavior maintained by
rattlesnake presence, dependent on historic co-occurrence
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Antipredator behavior: Antipredator behavior: applications for conservationapplications for conservation
• Captive breeding programs– Will individuals in captivity maintain
antipredator behavior?
• Reintroductions of predators– Will individuals from predator-naïve
populations be able to defend themselves?
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Black tailed prairie dogs Black tailed prairie dogs
• 98% decline in North America
• Candidate species for Endangered Species Act listing
• Translocating individuals to boost small or extirpated populations
• Low survival rates after translocations
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Prairie Dog Prairie Dog Antipredator BehaviorAntipredator Behavior
• Alarm calls denote certain predators – Mammalian (e.g., coyotes)– Hawks– Snakes
• Different alarm calls refer to different response behavior and urgency
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Prairie Dog Prairie Dog Antipredator BehaviorAntipredator Behavior
• Pre-release predator training for captive-born juveniles– Paired presentation of
predators with appropriate alarm calls
• Enhanced antipredator behavior and increased post-release survival
Shier & Owings 2006
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Predator ReintroductionPredator Reintroduction
• Wolves reintroduced in areas in Wyoming after 30-year absence
• Moose calf death rate increased
• But… tested moose that lost calves to wolf predation and showed hypersensitivity to wolf vocalizations
Berger et al. 2001
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Animal Behavior and Animal Behavior and ConservationConservation
• Understanding behavior can lead to better conservation of wildlife
• Taking historic information into account may be important
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AcknowledgementsAcknowledgementsDon OwingsMatt RoweTim Caro
Jamie CorneliusAnnie LeonardTerry OrdGeorge & Maria ClucasDick CossDoug DineroTom HahnAnn HedrickPeter MarlerLori MiyasatoLarry RabinAaron Rundus
ABGG students 2002-2008, Pat & Roy Arrowood, Stan Bursten, Marian Bilheimer, Jenn DeBose, Taylor Chapple, John Hammond, Tyson Schmidt, Aysha Taff, 2008 Bodega Phylogenetics Workshop (especially Brian O’Meara), Fred Armstrong, Gwen Bachman, Gretchen Baker, Duane Davis, Karen Hughes, Michael Magnuson, Phillip McClelland, Sonia Navarro Perez, Richard Roy, Donna Stovall, Renee West, Sebastian, Batman, Sugar, the Celtic soccer team, and the countless people who donated shed snake skins
NSF UC Davis Animal Behavior
Graduate GroupAnimal Behaviour SocietyAmerican Society of
MammalogyUCMexusUC Davis College of
Agricultural & Environmental Sciences