Reversal learning and risk-averse foraging behavior in the monarch butterfly, danaus plexippus (lepidoptera: Nymphalidae)

Ethology

Volumn 116, Issue 3, 2010, Pages 270-280

  Rodrigues, Daniela ^a   Goodner, Brad W ^b   Weiss, Martha R ^a  

^a GEORGETOWN UNIVERSITY   (United States)

^b HIRAM COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BEHAVIORAL ECOLOGY; BUTTERFLY; FLORAL TRAIT; FORAGING BEHAVIOR; LEARNING; NECTAR; POLLINATOR;

APOIDEA; DANAUS PLEXIPPUS; HEXAPODA; LEPIDOPTERA; NYMPHALIDAE; PAPILIONOIDEA;

EID: 77949878412     PISSN: 01791613     EISSN: 14390310     Source Type: Journal    
DOI: 10.1111/j.1439-0310.2009.01737.x     Document Type: Article

References (66)

1. Adler L S. Adaptative significance of toxic nectar. Oikos 2000, 91:409-420.
2. Adler L S, Irwin R E. Ecological costs and benefits of defenses in nectar. Ecology 2005, 86:2968-2978.
3. Andersson S, Dobson H E M. Behavioral foraging responses by the butterfly Heliconius melponeme to Lantana camara floral scent. J. Chem. Ecol. 2003, 29:2303-2318.
4. Baker H G, Baker I. Studies of nectar-constitution and pollinator-plant coevolution. Coevolution of Animals and Plants 1975, 100-40. Gilbert L E, Raven P H. In, eds, Univ. of Texas Press, Austin, pp
5. Banschbach V S, Waddington K D. Risk-sensitive foraging in honey bees: no consensus among individuals and no effect of colony honey stores. Anim. Behav. 1994, 47:933-941.
6. Berenbaum M R, Miliczky E. Mantids and milkweed bugs: efficacy of aposematic coloration against invertebrate predators. Am. Midl. Nat. 1984, 111:64-68.
7. Bernays E A. Aversion learning and feeding. Insect Learning: Ecological and Evolutionary Perspectives 1993, 1-17. Papaj D RLewis A C. In, eds, Chapman and Hall, New York, pp
8. Biernaskie J M, Cartar R V. Variation in rate of nectar production depends on floral display size: a pollinator manipulation hypothesis. Funct. Ecol. 2004, 18:125-129.
9. Biernaskie J M, Cartar R V, Hurly T A. Risk-averse inflorescence departure in hummingbirds and bumblebees: could plant benefit from variable nectar volumes? Oikos 2002, 98:98-104.
10. Blackiston D J. Learning and memory in larval and adult Lepidoptera 2007, Ph.D. Dissertation, Georgetown Univ., Washington, DC
11. Blackiston D J, Silva Casey E, Weiss M R. Retention of memory through metamorphosis: can a moth remember what it learned as a caterpillar? PLoS ONE 2008, 3:e1736.
12. Bowdish T I, Bultman T L. Visual cues used by mantids in learning aversion to aposematically colored prey. Am. Midl. Nat. 1993, 129:215-222.
13. Briscoe A D, Chittka L. The evolution of color vision in insects. Annu. Rev. Entomol. 2001, 46:471-510.
14. Brower L P. Avian predation on the monarch butterfly and its implications for mimicry theory. Am. Nat. 1988, 131:S4-S6.
15. Calvert W H, Brower L P. The location of the monarch butterfly (Danaus plexippus L.) overwintering colonies in Mexico in relation to topography and climate. J. Lep. Soc. 1986, 40:164-187.
16. Cartar R V. A test of risk sensitive foraging in wild bumble bees. Ecology 1991, 72:888-895.
17. Chittka L, Dyer A G, Dornhaus A. Bees trade off foraging speed for accuracy. Nature 2003, 424:388.
18. Cnaani J, Thompson J D, Papaj D R. Flower choice and learning in foraging bumblebees: effects in variation of flower nectar volume and concentration. Ethology 2005, 112:278-285.
19. Davis R L. Olfactory memory formation in Drosophila: from molecular to systems neuroscience. Annu. Rev. Neurosci. 2005, 28:275-302.
20. Drezner-Levy T, Shafir S. Parameters of variable reward distributions that affect risk sensitivity of honey bees. J. Exp. Biol. 2007, 210:269-277.
21. Dukas R. Ecological relevance of associative learning in fruit fly larvae. Behav. Ecol. Sociobiol. 1999, 45:195-200.
22. Dukas R. Evolutionary biology of insect learning. Annu. Rev. Entomol. 2008, 53:145-160.
23. Dukas R, Bernays E A. Learning improves growth rate in grasshoppers. Proc. Natl Acad. Sci. USA 2000, 97:2637-2640.
24. Dukas R, Real L A. Effects of nectar variance on learning by bumble bees. Anim. Behav. 1993, 45:37-41.
25. Dyer A G, Chittka L. Fine colour discrimination requires differential learning in bumblebees. Naturwissenchaften 2004, 91:224-227.
26. Gardener M C, Gillman M P. The taste of nectar: a neglected area of pollination ecology. Oikos 2002, 98:552-557.
27. Gegear R J, Manson J S, Thomson J D. Ecological context influences pollinator deterrence by alkaloids in floral nectar. Ecol. Lett. 2007, 10:375-382.
28. Goulson D, Cory J S. Flower constancy and learning in foraging preferences of the green-veined white butterfly Pieris napi. Ecol. Entomol. 1993, 18:315-320.
29. Gumbert A. Color choices by bumble bees (Bombus terrestris): innate preferences and generalization after learning. Behav. Ecol. Sociobiol. 2000, 48:36-43.
30. Harder L D, Real L A. Why are bumblebees risk averse? Ecology 1987, 68:1104-1108.
31. Hay-Roe M N, Lamas G, Nation J L. Pre- and post zygotic isolation and Haldane rule effects in reciprocal crosses of Danaus erippus and Danaus plexippus (Lepidoptera: Danainae), supported by differentiation of cuticular hydrocarbons, establish their status as separate species. Biol. J. Linn. Soc. 2007, 91:445-453.
32. Helmus M R, Dussourd D E. Glues or poisons: which triggers vein cutting by monarch caterpillars? Chemoecology 2005, 15:45-49.
33. Johnson S D, Hargreaves A L, Brown M. Dark, bitter-tasting nectar functions as filter of flower visitors in a bird-pollinated plant. Ecology 2006, 87:2709-2716.
34. Kandori I, Ohsaki N. The learning abilities of the white cabbage butterfly, Pieris rapae, foraging for flowers. Res. Pop. Ecol. 1996, 38:111-117.
35. Kelber A. Colour learning in the hawkmoth Macroglossum stelatarum. J. Exp. Biol. 1996, 199:1127-1131.
36. Kelber A. Pattern discrimination in a hawkmoth: innate preferences, learning performance and ecology. Proc. R. Soc. Lond. B 2002, 269:2573-2577.
37. Kinoshita M, Shimada N, Arikawa K. Colour vision of the foraging swallowtail butterfly Papilio xuthus. J. Exp. Biol. 1999, 202:95-102.
38. Landolt P J, Lenczewski B. Lack of evidence for the toxic nectar hypothesis: a plant alkaloid did not deter nectar feeding by Lepidoptera. Fla. Entomol. 1993, 76:556-566.
39. Laverty T M. Bumble bee learning and flower morphology. Anim. Behav. 1994, 47:531-545.
40. Lee J C, Bernays E A. Food tastes and toxic effects: associative learning by the polyphagous grasshopper Schistocerca americana (Drury) (Orthoptera: Acrididae). Anim. Behav. 1990, 39:163-173.
41. Malcolm S B. Milkweeds, monarch butterflies and the ecological significance of cardenolides. Chemoecology 1994/1995, 5/6:101-117.
42. Masters R A. Dual role of pyrrolizidine alkaloids in nectar. J. Chem. Ecol. 1991, 17:195-205.
43. Matsumoto Y, Mizunami M. Lifetime olfactory memory in the cricket Gryllus bimaculatus. J. Comp. Physiol. A. 2002, 188:295-299.
44. McDade L A, Weeks J A. Nectar in hummingbird-pollinated neotropical plants I: patterns of production and variability in 12 species. Biotropica 2004, 36:196-205.
45. Motulsky H. Analysing Data with GraphPad Prism Software 1999, GraphPad Software, San Diego
46. Mouritsen H, Frost B J. Virtual migration in tethered flying monarch butterflies reveals their orientation mechanisms. Proc. Natl Acad. Sci. USA 2002, 99:10162-10166.
47. Possigham H P, Houston A I, McNamara J M. Risk-averse foraging in bees: a comment on the model of Harder and Real. Ecology 1990, 71:1622-1624.
48. Real L A. Uncertainty and pollinator-plant interactions: the foraging behavior of bees and wasps on artificial flowers. Ecology 1981, 62:20-26.
49. Real L A, Ott J, Silverfine E. On the tradeoff between the mean and the variance in foraging: effect of spatial distribution and color preference. Ecology 1982, 63:1617-1623.
50. Rhoades D F, Bergdahl J C. Adaptive significance of toxic nectar. Am. Nat. 1981, 117:798-803.
51. Ritland D B, Brower L P. The viceroy butterfly is not a batesian mimic. Nature 1991, 350:497-498.
52. Scott J A. The Butterflies of North America: A Natural History and Field Guide 1986, Stanford Univ. Press, Stanford
53. Shafir S. Color discrimination conditioning of a wasp, Polybia occidentalis (Hymenoptera: Vespidae). Biotropica 1996, 28:243-251.
54. Smallwood P D. An introduction to risk sensitivity: the use of Jensen's Inequality to clarify evolutionary arguments of adaptation and constraint. Am. Zool. 1996, 36:392-401.
55. Sokal R R, Rohlf F J. Biometry 1995, 3rd edn, Freeman, New York
56. Stephens D W. Learning and behavioral ecology: Incomplete information and environmental predictability. Insect Learning: Ecological and Evolutionary Perspectives 1993, 195-218. Papaj D RLewis A C. In, eds, Chapman and Hall, New York, pp
57. Stephenson A G. Iridoid glycosides in the nectar of Catalpa speciosa are unpalatable to nectar thieves. J. Chem. Ecol. 1982, 8:1025-1034.
58. Tully T, Quinn W C. Classical conditioning and retention in normal and mutant Drosophila melanogaster. J. Comp. Physiol. A. 1985, 157:263-277.
59. Vergoz V, Roussel E, Sandoz J C, Giurfa M. Aversive learning in honeybees revealed by the olfactory conditioning of the sting reflexion index. PLoS ONE 2007, 3:1-10.
60. Waddington K D. Bumblebees do not respond to variance in nectar concentration. Ethology 1995, 101:33-38.
61. Weiss M R. Associative colour learning in a nymphalid butterfly. Ecol. Entomol. 1995, 20:298-301.
62. Weiss M R. Innate colour preferences and flexible colour learning in the pipevine swallowtail. Anim. Behav. 1997, 53:1043-1052.
63. Weiss M R. Vision and learning in some neglected pollinators: Beetles, flies, moths, and butterflies. Cognitive Ecology of Pollination: Animal Behavior and Floral Evolution 2001, 171-190. Chittka LThomson J D. In, eds, Cambridge Univ. Press, Cambridge, pp
64. Weiss M R, Papaj D R. Colour learning in two behavioural contexts: how much can a butterfly keep in mind? Anim. Behav. 2003, 65:425-434.
65. Zalucki M P, Malcolm S B, Paine T D, Hanlon C C, Brower L P, Clarke A R. It's the first bites that count: Survival of first-instar monarchs on milkweeds. Austral Ecol. 2001, 26:547-555.
66. Zimmerman M, Pleasants J M. Competition among pollinators: quantification of available resources. Oikos 1982, 38:381-383.