Do canal-cutting behaviours facilitate host-range expansion by insect herbivores?

Biological Journal of the Linnean Society

Volumn 96, Issue 4, 2009, Pages 715-731

  Dussourd, David E ^a  

^a UNIVERSITY OF CENTRAL ARKANSAS   (United States)

Author keywords

Adaptive zone; Co evolution; Exudate; Herbivore offence; Insect plant interaction; Laticifer; Plant defence; Resin duct; Secretory canals; Vein cutting

Indexed keywords

ADAPTATION; BUTTERFLY; COEVOLUTION; EVOLUTION; HERBIVORE; HOST RANGE; PLANT DEFENSE; PLANT-HERBIVORE INTERACTION; RANGE EXPANSION; SECRETION;

HEXAPODA; NYMPHALIDAE; PAPILIONOIDEA;

EID: 63849208896     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/j.1095-8312.2008.01168.x     Document Type: Article

References (119)

1. Abe F, Yamauchi T, Honda K, Omura H, Hayashi N. 2001. Sequestration of phenanthroindolizidine alkaloids by an Asclepiadaceae-feeding danaid butterfly, Ideopsis similis. Phytochemistry 56 : 697 701.
2. Ackery PR, Vane-Wright RI. 1984. Milkweed butterflies: their cladistics and biology. Ithaca, NY : Cornell University Press.
3. Agrawal AA. 2004. Resistance and susceptibility of milkweed: competition, root herbivory, and plant genetic variation. Ecology 85 : 2118 2133.
4. Agrawal AA. 2006. Macroevolution of plant defense strategies. Trends in Ecology and Evolution 22 : 103 109.
5. Agrawal AA, Lajeunesse MJ, Fishbein M. 2008. Evolution of latex and its constituent defensive chemistry in milkweeds (Asclepias): a phylogenetic test of plant defense escalation. Entomologia Experimentalis et Applicata 128 : 126 138.
6. Agrawal AA, Lau JA, Hambäck PA. 2006. Community heterogeneity and the evolution of interactions between plants and insect herbivores. Quarterly Review of Biology 81 : 349 376.
7. Albanese G, Nelson MW, Vickery PD, Sievert PR. 2007. Larval feeding behavior and ant association in frosted elfin, Callophrys irus (Lycaenidae). Journal of the Lepidopterists Society 61 : 61 66.
8. Andrade I, Benson WW. 1997. Eurema dina leuce (Pieridae) feeds on a lactiferous host plant in eastern Brazil. Journal of the Lepidopterists Society 51 : 358 359.
9. Angiosperm Phylogeny Group. 2003. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Botanical Journal of the Linnean Society 141 : 399 436.
10. Arribére MC, Cortadi AA, Gattuso MA, Bettiol MP, Priolo NS, Caffini NO. 1998. Comparison of Asclepiadaceae latex proteases and characterization of Morrenia brachystephana Griseb. cysteine peptidases. Phytochemical Analysis 9 : 267 273.
11. Becerra JX. 2003. Synchronous coadaptation in an ancient case of herbivory. Proceedings of the National Academy of Sciences of the United States of America 100 : 12804 12807.
12. Becerra JX. 1994. Squirt-gun defense in Bursera and the chrysomelid counterploy. Ecology 75 : 1991 1996.
13. Becerra JX, Venable DL, Evans PH, Bowers WS. 2001. Interactions between chemical and mechanical defenses in the plant genus Bursera and their implications for herbivores. American Zoologist 41 : 865 876.
14. Berg CC. 1978. Cecropiaceae a new family of the Urticales. Taxon 27 : 39 44.
15. Bernath J, ed. 1998. Poppy: the genus Papaver. Amsterdam : Harwood Academic.
16. Bernays EA, Chapman RF. 1994. Host-plant selection by phytophagous insects. New York : Chapman and Hall.
17. Bernays EA, Singer MS, Rodrigues D. 2004. Trenching behavior by caterpillars of the Euphorbia specialist, Pygarctia roseicapitis: a field study. Journal of Insect Behavior 17 : 41 52.
18. Blaser HW. 1945. Anatomy of Cryptostegia grandiflora with special reference to the latex system. American Journal of Botany 32 : 135 141.
19. Brower AVZ. 2000. Phylogenetic relationships among the Nymphalidae (Lepidoptera) inferred from partial sequences of the wingless gene. Proceedings of the Royal Society of London B 267 : 1201 1211.
20. Chemsak JA. 1963. Taxonomy and bionomics of the genus Tetraopes (Cerambycidae: Coleoptera). University of California Publications in Entomology 30 : 1 89.
21. Clarke AR, Zalucki MP. 2000. Foraging and vein-cutting behaviour of Euploea core corinna (W. S. Macleay) (Lepidoptera: Nymphalidae) caterpillars feeding on latex-bearing leaves. Australian Journal of Entomology 39 : 283 290.
22. Cohen JA, Brower LP. 1983. Cardenolide sequestration by the dogbane tiger moth (Cycnia tenera: Arctiidae). Journal of Chemical Ecology 9 : 521 532.
23. Compton SG. 1987. Aganais speciosa and Danaus chrysippus (Lepidoptera) sabotage the latex defences of their host plants. Ecological Entomology 12 : 115 118.
24. Compton SG. 1989. Sabotage of latex defences by caterpillars feeding on fig trees. South African Journal of Science 85 : 605 606.
25. Covell CV. 1984. A field guide to moths of Eastern North America. Boston : Houghton Mifflin.
26. Darling C. 2007. Holey aroids: circular trenching behavior by a leaf beetle in Vietnam. Biotropica 39 : 555 558.
27. DeVries PJ. 1987. The butterflies of Costa Rica and their natural history. Princeton, NJ : Princeton University Press.
28. DeVries PJ. 1991. Foam barriers, a new defense against ants for milkweed butterfly caterpillars (Nymphalidae: Danainae). Journal of Research on the Lepidoptera 30 : 261 266.
29. Demarco D, Kinoshita LS, Castro M. 2006. Laticíferos articulados anastomosados - novos registros para Apocynaceae. Revista Brasileira de Botânica 29 : 133 144.
30. Dillon PM, Lowrie S, McKey D. 1983. Disarming the 'Evil Woman': petiole constriction by a sphingid larva circumvents mechanical defenses of its host plant, Cnidoscolus urens (Euphorbiaceae). Biotropica 15 : 112 116.
31. Downie NM, Arnett RH. 1996. The beetles of northeastern North America Vol. II. Polyphaga (cont.), Superfamily Bostrichoidea, thru Curculionoidea. Gainesville, FL : Sandhill Crane Press.
32. Dussourd DE. 1993. Foraging with finesse: caterpillar adaptations for circumventing plant defenses. In : Stamp NE, Casey TM, eds. Caterpillars: ecological and evolutionary constraints on foraging. New York : Chapman and Hall, 92 131.
33. Dussourd DE. 1995. Entrapment of aphids and whiteflies in lettuce latex. Annals of the Entomological Society of America 88 : 163 172.
34. Dussourd DE. 1997. Plant exudates trigger leaf-trenching by cabbage loopers, Trichoplusia ni. Oecologia 112 : 362 369.
35. Dussourd DE. 1999. Behavioral sabotage of plant defense: do vein cuts and trenches reduce insect exposure to exudate? Journal of Insect Behavior 12 : 501 515.
36. Dussourd DE. 2003. Chemical stimulants of leaf-trenching by cabbage loopers: natural products, neurotransmitters, insecticides, and drugs. Journal of Chemical Ecology 29 : 2023 2047.
37. Dussourd DE. 2005. In the trenches: bioprospecting with a caterpillar probe. Wings: Essays in Invertebrate Conservation 28 : 20 24.
38. Dussourd DE, Denno RF. 1991. Deactivation of plant defense: correspondence between insect behavior and secretory canal architecture. Ecology 72 : 1383 1396.
39. Dussourd DE, Denno RF. 1994. Host range of generalist caterpillars: trenching permits feeding on plants with secretory canals. Ecology 75 : 69 78.
40. Dussourd DE, Eisner T. 1987. Vein-cutting behavior: insect counterploy to the latex defense of plants. Science 237 : 898 901.
41. Dussourd DE, Hoyle AM. 2000. Poisoned plusiines: toxicity of milkweed latex and cardenolides to some generalist caterpillars. Chemoecology 10 : 11 16.
42. Eben A, Gamez-Virues S. 2007. Sharing the trench: a curious feeding behavior of Diabrotica porracea Harold (Chrysomelidae: Galerucinae) in the presence of Epilachna tredecimnotata (Latreille) (Coccinellidae). Coleopterists Bulletin 61 : 57 64.
43. Ehrlich PR, Raven PH. 1964. Butterflies and plants: a study in coevolution. Evolution 18 : 586 608.
44. Esau K. 1940. Developmental anatomy of the fleshy storage organ of Daucus carota. Hilgardia 13 : 175 209.
45. Esau K. 1965. Plant anatomy. New York : John Wiley and Sons.
46. Evans PH, Becerra JX, Venable DL, Bowers WS. 2000. Chemical analysis of squirt-gun defense in Bursera and counterdefense by chrysomelid beetles. Journal of Chemical Ecology 26 : 745 754.
47. Fahn A. 1979. Secretory tissues in plants. New York : Academic Press.
48. Fahn A, Evert RF. 1974. Ultrastructure of the secretory ducts of Rhus glabra L. American Journal of Botany 61 : 1 14.
49. Farrell BD. 2001. Evolutionary assembly of the milkweed fauna: cytochrome oxidase I and the age of Tetraopes beetles. Molecular Phylogenetics and Evolution 18 : 467 478.
50. Farrell BD, Dussourd DE, Mitter C. 1991. Escalation of plant defense: do latex and resin canals spur plant diversification? American Naturalist 138 : 881 900.
51. Farrell BD, Mitter C. 1998. The timing of insect/plant diversification: might Tetraopes (Coleoptera: Cerambycidae) and Asclepias (Asclepiadaceae) have co-evolved? Biological Journal of the Linnean Society 63 : 553 577.
52. Farrell BD, Mitter C, Futuyma DJ. 1992. Diversification at the insect-plant interface. Bioscience 42 : 34 42.
53. Fatope MO, Zeng L, Ohayaga JE, Shi G, McLaughlin JL. 1996. Selectively cytotoxic diterpenes from Euphorbia poisonii. Journal of Medicinal Chemistry 39 : 1005 1008.
54. Fitzgerald TD. 1995. Caterpillars roll their own. Natural History 4/95 : 30 37.
55. Fordyce JA, Malcolm SB. 2000. Specialist weevil, Rhyssomatus lineaticollis, does not spatially avoid cardenolide defenses of common milkweed by ovipositing into pith tissue. Journal of Chemical Ecology 26 : 2857 2874.
56. French JC. 1988. Systematic occurrence of anastomosing laticifers in Araceae. Botanical Gazette 149 : 71 81.
57. Fukuda H, Hama E, Kuzuya T, Takahashi A, Takahashi M, Tanaka B, Tanaka H, Wakabayashi M, Watanabe Y. 1982. The life histories of butterflies of Japan. Volume 1. Osaka, Japan : Hoikusha.
58. Gangwere SK. 1961. A monograph on food selection in Orthoptera. Transactions of the American Entomological Society 87 : 67 230.
59. Harris P. 1972. Food-plant groups of the Semanophorinae (Lepidoptera: Sphingidae): a possible taxonomic tool. Canadian Entomologist 104 : 71 80.
60. Haupt I. 1976. Separation of the sites of synthesis and accumulation of 3,4-dihydroxyphenylalanine in Euphorbia lathyris L. Nova Acta Leopoldina, Supplement 7 : 129 132.
61. Helmus MR, Dussourd DE. 2005. Glues or poisons: which triggers vein cutting by monarch caterpillars? Chemoecology 15 : 45 49.
62. Heppner JB. 2003. Arthropods of Florida and neighboring land areas. Volume 17. Lepidoptera of Florida. Gainesville, FL : Florida Department of Agriculture and Consumer Sciences.
63. Hirai N, Ishii M. 2002. Egg placement of the tachinid fly Sturmia bella on leaves of the evergreen milkvine Marsdenia tomentosa and the feeding habit of its host butterfly Parantica sita. Entomological Science 5 : 153 159.
64. Hodges RW. 1971. The moths of America north of Mexico. Fasc. 21. Sphingoidea. Washington, DC : Wedge Entomological Research Foundation.
65. Huwer RK, McFadyen RE. 1999. Biology and host range of the hawk moth Nephele densoi Keferstein (Lep.: Sphingidae), a potential agent for the biological control of rubbervine Cryptostegia grandifora R. Br. (Asclepiadaceae). Biocontrol Science and Technology 9 : 79 88.
66. Ide JY. 2004. Leaf trenching by Indian red admiral caterpillars for feeding and shelter construction. Population Ecology 46 : 275 280.
67. Isely FB. 1941. Researches concerning Texas Tettigoniidae. Ecological Monographs 11 : 457 475.
68. Janz N, Nylin S. 2008. The oscillation hypothesis of host-plant range and speciation. In : Tilman KJ, ed. Specialization, speciation, and radiations: the evolutionary biology of herbivorous insects. Berkeley, CA : University of California Press, 203 215.
69. Janz N, Nylin S, Wahlberg N. 2006. Diversity begets diversity: host expansions and the diversification of plant-feeding insects. BioMed Central Evolutionary Biology 6 : 4.
70. Janzen DH. 1985. Plant defences against animals in the Amazonian rainforest. In : Prance GT, Lovejoy TE, eds. Amazonia. New York : Pergamon, 207 217.
71. Jolivet P. 1998. Interrelationship between insects and plants. New York : CRC Press.
72. Karban R, Agrawal AA. 2002. Herbivore offense. Annual Review of Ecology and Systematics 33 : 641 664.
73. Kaur H, Sirohi SS. 1995. Developmental studies on laticifers of family Apocynaceae. Acta Botanica Indica 23 : 211 213.
74. Kong C, Liang W, Yang X, Zhang M, Hu F. 2004. Mechanism of Aulacophora femoralis chinensis Weise feeding behavior and chemical response of host Cucumis sativus L. Chinese Science Bulletin 49 : 1485 1489.
75. Konno K, Hirayama C, Nakamura M, Tateishi K, Tamura Y, Hattori M, Kohno K. 2004. Papain protects papaya trees from herbivorous insects: role of cysteine proteases in latex. The Plant Journal 37 : 370 378.
76. Konno K, Ono H, Nakamura M, Tateishi K, Hirayama C, Tamura Y, Hattori M, Koyama A, Kohno K. 2006. Mulberry latex rich in antidiabetic sugar-mimic alkaloids forces dieting on caterpillars. Proceedings of the National Academy of Sciences of the United States of America 103 : 1337 1341.
77. Lafontaine JD, Poole RW. 1991. The moths of America north of Mexico. Fasc. 25.1. Noctuoidea, Noctuidae (part). Washington, DC : Wedge Entomological Research Foundation.
78. Leineweber K, Schulz A, Thompson GA. 2000. Dynamic transitions in the translocated phloem filament protein. Australian Journal of Plant Physiology 27 : 733 741.
79. Lewinsohn TM. 1991. The geographical distribution of plant latex. Chemoecology 2 : 64 68.
80. Lewinsohn TM, Vasconcellos-Neto J. 2000. Como insetos sabotam defesas de plantas: o caso do látex. In : Martins RP, Lewinsohn TM, Barbeitos MS, eds. Ecologia e comportamento de insetos. Série Oecologia Brasiliensis, vol. VIII. Rio de Janeiro, Brazil : PPGE-UFRJ, 281 298.
81. Lewis PA, Metcalf RL. 1996. Behavior and ecology of Old World Luperini beetles of the genus Aulacophora (Coleoptera: Chrysomelidae). Chemoecology 7 : 150 155.
82. Mabberley DJ. 1998. The plant-book: a portable dictionary of the vascular plants. Cambridge : Cambridge University Press.
83. McCloud ES, Tallamy DW, Halaweish FT. 1995. Squash beetle trenching behaviour: Avoidance of cucurbitacin induction or mucilaginous plant sap? Ecological Entomology 20 : 51 59.
84. Mackay PA, Wellington WG. 1977. Notes on the life history and habits of the red-backed sawfly, Eriocampa ovata (Hymenoptera: Tenthredinidae). Canadian Entomologist 109 : 53 58.
85. Mahlberg PG. 1963. Development of non-articulated laticifer in seedling axis of Nerium oleander. Botanical Gazette 124 : 224 231.
86. Mahlberg PG. 1981. The nonarticulated laticifer cell in Asclepiadaceae. Askpelios 23 : 30 32.
87. Mahlberg PG. 1993. Laticifers: an historical perspective. Botanical Review 59 : 1 23.
88. Marsh NA, Clarke CA, Rothschild M, Kellett DN. 1977. Hypolimnas bolina (L.), a mimic of danaid butterflies, and its model Euploea core (Cram.) store cardioactive substances. Nature 268 : 726 728.
89. Mattos Filho A. 1971. Estudo comparativo de duas espécies de Leguminosae latescentes do Cerrado e da Caatinga. Rodriguesia 38 : 9 33.
90. Metcalfe CR, Chalk L. 1950. Anatomy of the dicotyledons. Oxford : Clarendon Press.
91. Metcalfe CR, Chalk L. 1983. Anatomy of the dicotyledons, Vol. II. Oxford : Clarendon Press.
92. Nishida R. 2002. Sequestration of defensive substances from plants by Lepidoptera. Annual Review of Entomology 47 : 57 92.
93. Nishida R, Fukami H. 1990. Sequestration of distasteful compounds by some pharmacophagous insects. Journal of Chemical Ecology 16 : 151 164.
94. Nitao JK, Zangerl AR. 2004. Microwave-facilitated extraction of furanocoumarins onto paper substrates: an imaging technique to analyse spatial distribution and abundance in leaves. Phytochemical Analysis 15 : 262 266.
95. Novotny V, Basset Y. 2005. Host specificity of insect herbivores in tropical forests. Proceedings of the Royal Society B 272 : 1083 1090.
96. Olson KC, Tibbitts TW, Struckmeyer BE. 1969. Leaf histogenesis in Lactuca sativa with emphasis upon laticifer ontogeny. American Journal of Botany 56 : 1212 1216.
97. Ravenscroft NOM. 1994. The feeding behaviour of Carterocephalus palaemon (Lepidoptera: Hesperiidae) caterpillars: does it avoid host defences or maximize nutrient intake? Ecological Entomology 19 : 26 30.
98. Richards AM, Filewood LW. 1990. Feeding behaviour and food preferences of the pest species comprising the Epilachna vigintioctopunctata (F.) complex (Col., Coccinellidae). Journal of Applied Entomology 110 : 501 515.
99. Rothschild M, Reichstein T. 1976. Some problems associated with the storage of cardiac glycosides by insects. Nova Acta Leopoldina Supplement 7 : 507 550.
100. Roy AT, De DN. 1992. Studies on differentiation of laticifers through light and electron microscopy in Calotropis gigantea (Linn.) R. Br. Annals of Botany 70 : 443 449.
101. Rudall PJ. 1987. Laticifers in Euphorbiaceae - a conspectus. Botanical Journal of the Linnean Society 94 : 143 163.
102. Schluter D. 2000. The ecology of adaptive radiation. Oxford : Oxford University Press.
103. Shrestha T, Kopp B, Bisset NG. 1992. The Moraceae-based dart poisons of South America. Cardiac glycosides of Maquira and Naucleopsis species. Journal of Ethnopharmacology 37 : 129 143.
104. Singer MS. 2008. Evolutionary ecology of polyphagy. In : Tilman KJ, ed. Specialization, speciation, and radiations: the evolutionary biology of herbivorous insects. Berkeley, CA : University of California Press, 29 42.
105. Takeuchi M, Tamura M. 1993. Trenching behavior of the cucumber looper, Anadevidia peponis (Fab.) (Lepidoptera: Noctuidae) on cucurbit host plants. Japanese Journal of Applied Entomology and Zoology 37 : 221 226.
106. Tallamy DW. 1985. Squash beetle feeding behavior: an adaptation against induced cucurbit defenses. Ecology 66 : 1574 1579.
107. Tallamy DW. 1986. Behavioral adaptations in insects to plant allelochemicals. In : Brattsten LB, Ahmad S, eds. Molecular aspects of insect-plant associations. New York : Plenum, 273 300.
108. Thompson JN. 1994. The coevolutionary process. Chicago, IL : University of Chicago Press.
109. Tune R, Dussourd DE. 2000. Specialized generalists: constraints on host range in some plusiine caterpillars. Oecologia 123 : 543 549.
110. Vertrees GL, Mahlberg PG. 1978. Structure and ontogeny of laticifers in Cichorium intybus (Compositae). American Journal of Botany 65 : 764 771.
111. Vreede MC. 1949. Topography of the laticiferous system in the genus Ficus. Annals of the Royal Botanic Gardens, Buitenzorg 51 : 125 149.
112. Wagner DL. 2005. Caterpillars of eastern North America: a guide to identification and natural history. Princeton, NJ : Princeton University Press.
113. Ward LK, Spalding DF. 1993. Phytophagous British insects and mites and their food-plant families: total numbers and polyphagy. Biological Journal of the Linnean Society 49 : 257 276.
114. Warning WC. 1934. Anatomy of the vegetative organs of the parsnip. Botanical Gazette 96 : 44 72.
115. Winder JA. 1976. Ecology and control of Erinnyis ello and E. alope, important insect pests in the New World. Pest Articles and News Summaries 22 : 449 466.
116. Winkler IS, Mitter C. 2008. The phylogenetic dimension of insect-plant interactions: a review of recent evidence. In : Tilman KJ, ed. Specialization, speciation, and radiations: the evolutionary biology of herbivorous insects. Berkeley, CA : University of California Press, 240 263.
117. Young AM. 1978. The biology of the butterfly Aeria eurimedea agna (Nymphalidae: Ithomiinae: Oleriini) in Costa Rica. Journal of the Kansas Entomological Society 51 : 1 10.
118. Zalucki MP, Brower LP. 1992. Survival of first instar larvae of Danaus plexippus (Lepidoptera: Danainae) in relation to cardiac glycoside and latex content of Asclepias humistrata (Asclepiadaceae). Chemoecology 3 : 81 93.
119. Zalucki MP, Brower LP, Alonso MA. 2001. Detrimental effects of latex and cardiac glycosides on survival and growth of first-instar monarch butterfly larvae Danaus plexippus feeding on the sandhill milkweed Asclepias humistrata. Ecological Entomology 26 : 212 224.