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Squirrels versus Rattlesnakes: the Evolution of Unique Antipredator Behavior

Squirrels versus Rattlesnakes: the Evolution of Unique Antipredator Behavior. Barbara Clucas, PhD College of the Environment University of Washington. Animal Behavior. The study of how animals use behavior to survive and reproduce How and why behavior evolves

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Squirrels versus Rattlesnakes: the Evolution of Unique Antipredator Behavior

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  1. Squirrels versus Rattlesnakes: the Evolution of Unique Antipredator Behavior Barbara Clucas, PhD College of the Environment University of Washington

  2. Animal Behavior • The study of how animals use behavior to survive and reproduce • How and why behavior evolves • Social, reproductive, movement, antipredator

  3. Animal Behavior • The study of how animals use behavior to survive and reproduce • How and why behavior evolves • Social, reproductive, movement, antipredator

  4. Antipredator Behavior • Reduce the risk of predation • Most animals are prey • Evolution of a vast array of antipredator behavior

  5. Antipredator Behavior

  6. Ground Squirrels (Spermophilus) • Diverse genus of species • Worldwide distribution (except Australia and Antarctica) • Live in burrows in the ground • Species vary in habitats and sociality

  7. Ground squirrel predators

  8. Ground squirrel predators

  9. Rattlesnakes (Crotalus) • Warning rattle • Venomous • Skilled rodent predators • Lethal venom • Acute sense of sight and smell • Pit organs can sense temperature changes rattle

  10. Ground squirrel defenses • Venom resistant • Harass, attack rattlesnakes • Tail-flagging • visual and infrared signal

  11. 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)

  12. Recent discovery • Another unique snake-related behavior found in certain species of ground squirrels • “Snake scent application”

  13. Snake Scent Application

  14. Snake Scent Application (SSA) • Why are squirrels applying rattlesnake scent? • Test 3 functional hypotheses • Evolutionary history • Phylogenetic comparative methods

  15. Functional hypotheses of SSA • Antipredator • Social • Ectoparasitic defense

  16. 1. Antipredator • SSA disguises squirrel odor • Rattlesnakes may bypass burrows with snake-scented squirrels

  17. 2. Social • Conspecific deterrence • SSA deters rivals • Snake-scented squirrels win more aggressive encounters

  18. 3. Ectoparasite defense • SSA reduces fleas • Flea host-finding behavior affected by snake scent

  19. Testing 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?

  20. Study 1: Which squirrels SSA more? Study species • California ground squirrel, (S. beecheyi) • Winters, California • Rock squirrel, (S. variegatus) • Caballo, New Mexico

  21. Study 1: Which squirrels SSA more? • Trapped and marked squirrels • Recorded: • sex • age • flea load

  22. Quantifying application behavior • Staked out shed rattlesnake skins • Filmed individual squirrels • Recorded duration of SSA

  23. Predictions • Antipredator • adult females & pups > adult males • Conspecific deterrence • adult males > adult females & pups • Ectoparasite defense • time spent related to flea load • pups > adults

  24. Adult females & pups > adult males *P < 0.005; Error bars = SE Clucas et al. 2008, Anim Behav

  25. SSA 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

  26. Study 1:Antipredator 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

  27. 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

  28. Experiment 1 Rattlesnake Foraging Behavior • 3 scent-type trials • Ground squirrel • Ground squirrel +Rattlesnake • Rattlesnake • Water control C. oreganus oreganus N = 8

  29. Experiment 1 Rattlesnake Foraging Behavior • Behavior scored • Time spent over • Tongue-flicking C. oreganus oreganus N = 8

  30. Experiment 1 Spent more time over ‘squirrel’ Repeated measures GLM: F2,14=4.667, P = 0.028; planned comparisons: all P<0.05 Clucas et al. 2008, PRSL

  31. Experiment 1 Tongue flicked more over ‘squirrel’ Repeated measures GLM: F2,14=4.478, P = 0.031; planned comparisons: Sq>R P=0.03, Sq>S+R P=0.07 Clucas et al. 2008, PRSL

  32. Experiment 2 Before and After SSA behavior SCENTED Pre-trial SSA trial Post-trial 24-48 hours 24-48 hours CONTROLS Pre-trial No SSA trial Post-trial 24-48 hours 24-48 hours

  33. Experiment 2 Before and After SSA behavior • Recorded: • Social interactions (aggressive or tolerant)

  34. Experiment 2 Social Interactions SCENTED * No differences between before and after CONTROLS * No differences between before and after Repeated Measures GLM; P>0.05 Clucas et al. 2008, PRSL

  35. Experiment 3 Flea host choice • Juvenile ground squirrels as hosts • Fleas • Removed from ground squirrels Control Flea SSA Squirrel starting Squirrel point

  36. ? ? Experiment 3 Flea host choice • Flea behavior recorded • Choice • Latency to move • Choice latency Control Flea SSA Squirrel starting Squirrel point

  37. = = Experiment 3 Fleas not affected by snake scent • No significant difference in choice (21=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 Clucas et al. 2008, PRSL

  38. Study 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

  39. Function of Applying Snake Scent • All evidence supports an antipredator function • Olfactory camouflage • Snakes did not avoid rattlesnake scent, rather showed low foraging behavior

  40. Evolutionary history • Explore the origins of applying snake scent • When did it evolve? • What caused it to evolve?

  41. Studying evolutionary history • Phylogenetic comparative methods • Phylogenetic tree

  42. Evolutionary history ? Common Ancestor

  43. Evolutionary history ?

  44. Ground squirrel phylogeny • Molecular (cytochrome b) • Divergence times • Time (in million of years) when species diverged

  45. Comparative study • Tested multiple ground squirrel and chipmunk species with rattlesnake scent • Recorded presence/absence of application behavior

  46. When did scent application originate? • Ancestor state reconstruction • estimate whether squirrel ancestors possessed the scent application trait using maximum likelihood analysis

  47. Ancestral State Reconstruction • Common ancestor likely had behavior • Behavior lost several times

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