Spatial heterogeneity within an evergreen conifer promotes foliage-age dietary mixing by a specialist herbivore

Animal Behaviour

Volumn 80, Issue 4, 2010, Pages 659-666

  Johns, Rob ^a,b   Quiring, Dan ^b  

^a LAURENTIAN FORESTRY CENTRE   (Canada)

^b UNIVERSITY OF NEW BRUNSWICK   (Canada)

Author keywords

Complementary diet; Intra tree variation; Ontogeny; Picea mariana; Pikonema alaskensis; Sawfly; Spatiotemporal

Indexed keywords

AGE CLASS; CONIFEROUS FOREST; DEFOLIATION; DIETARY OVERLAP; EVERGREEN FOREST; FOLIAGE; HERBIVORE; HETEROGENEITY; HOST PLANT; INSECT; INTRASPECIFIC VARIATION; LARVA; ONTOGENY; PLANT-HERBIVORE INTERACTION; SPATIAL ANALYSIS; SPATIOTEMPORAL ANALYSIS; SPECIALIST;

ANIMALIA; CONIFEROPHYTA; HYMENOPTERA; PICEA MARIANA; PIKONEMA ALASKENSIS; TENTHREDINIDAE;

EID: 77956616998     PISSN: 00033472     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anbehav.2010.06.027     Document Type: Article

References (60)

1. All J.N., Benjamin D.M. Influence of needle maturity on larval feeding preference and survival of Neodiprion swainei and N. rugifrons on jack pine, Pinus banksiana. Annual Review of the Entomological Society of America 1975, 68:579-584.
2. Barbosa P., Martinat P., Waldvogel M. Development, fecundity, and survival of the herbivore Lymantria dispar and the number of plant species in its diet. Ecological Entomology 1986, 11:1-6.
3. Bartelt R.J., Kulman H.M., Jones R.L. Effects of temperature on diapausing cocoons of the yellowheaded spruce sawfly, Pikonema alaskensis. Annals of the Entomological Society of America 1981, 74:472-477.
4. Behmer S.T. Insect herbivore nutrient regulation. Annual Review of Entomology 2009, 54:165-187.
5. Behmer S.T., Simpson S.J., Raubenheimer D. Herbivore foraging in chemically heterogeneous environments: nutrients and secondary metabolites. Ecology 2002, 83:2489-2501.
6. Behmer S.T., Raubenheimer D., Simpson S.J. The effects of distance between foods on nutrient regulation in a highly mobile insect herbivore. Animal Behaviour 2003, 66:665-675.
7. Bernays E.A., Chapman R.F. Host Plant Selection in Phytophagous Insects 1994, Chapman & Hall, New York.
8. Bernays E.A., Minkenberg P.J.M. Insect herbivores: different reasons for being a generalist. Ecology 1997, 78:1157-1169.
9. Blüthgen N., Metzner A. Contrasting leaf age preferences of specialist and generalist stick insects (Phasmida). Oikos 2007, 116:1853-1862.
10. Carisey N., Bauce É Impact of balsam fir foliage age on sixth-instar spruce budworm growth, development, and food utilization. Canadian Journal of Forest Research 1997, 27:257-264.
11. Carroll A.L. Physiological adaptation to temporal variation in conifer foliage by a caterpillar. Canadian Entomologist 1999, 131:659-669.
12. Carroll A.L., Quiring D.T. Intra-tree variation in foliage development influences the foraging strategy of a caterpillar. Ecology 1994, 75:1978-1990.
13. Cates R.G. Feeding patterns of monophagous, oligophagous, and polyphagous insect herbivores: the effect of resource abundance and plant chemistry. Oecologia 1980, 46:22-31.
14. Codella S.G., Raffa K.F. Contributions of female oviposition patterns and larval behavior to group defense in conifer sawflies (Hymenoptera: diprionidae). Oecologia 1995, 103:24-33.
15. Denno R.F., McClure M.S. Variable Plants and Herbivores in Natural and Managed Systems 1983, Academic Press, New York.
16. Dethier V.G. The feeding behavior of a polyphagous caterpillar (Diacrisia virginica) in its natural habitat. Canadian Journal of Zoology 1988, 66:1280-1288.
17. Ernest K.A. Insect herbivory on a tropical understory tree: effects of leaf age and habitat. Biotropica 1989, 21:194-199.
18. Ewers F., Schmid R. Longevity of needle fascicles of Pinus longaveava (bristlecone pine) and other North American pines. Oecologia 1981, 51:107-115.
19. Fox L.R., Morrow P.A. Specialization: species property or local phenomenon?. Science 1981, 211:887-893.
20. Freeland W.J., Janzen D.H. Strategies in herbivory by mammals: the role of plant secondary compounds. American Naturalist 1974, 108:269-289.
21. Géri C., Allais J.P., Auger M.A. Effects of plant chemistry and phenology on sawfly behavior and development. Sawfly Life History Adaptations to Woody Plants 1993, 173-210. Academic Press, New York. M.R. Wagner, K.F. Raffa (Eds.).
22. Hochuli D.F. Insect herbivory and ontogeny: how do growth and development influence feeding behaviour, morphology and host use?. Austral Ecology 2001, 26:563-570.
23. Honkanen T., Haukioja E. Why does a branch suffer more after branch-wide than after tree-wide defoliation?. Oikos 1994, 71:441-450.
24. Honkanen T., Jormalainen V., Hemmi A., Mäkinen A., Heikkilä N. Feeding and growth of the isopod Idotea baltica on the brown alga Fucus vesiculosus: roles of inter-population and within-plant variation in plant quality. Ecoscience 2002, 9:332-338.
25. Houseweart M.W., Kulman H.M. Fecundity and parthenogenesis of the yellowheaded spruce sawfly, Pikonema alaskensis. Annals of the Entomological Society of America 1976, 69:748-750.
26. Johns R.C., Ostaff D.P., Quiring D.T. Sampling procedures for evaluating yellowheaded spruce sawfly density and defoliation in juvenile black spruce stands. Journal of the Acadian Entomological Society 2006, 2:1-12.
27. Johns R.C., Quiring D.T., Lapointe R., Lucarotti C.J. Foliage-age mixing within balsam fir increases the fitness of a generalist caterpillar. Ecological Entomology 2009, 34:624-631.
28. Johns R.C., Quiring D.T., Ostaff D.P. Sex biased intra-tree oviposition site selection and larval foraging behavior of a specialist herbivore. Entomologia Experimentalis et Applicata 2009, 132:264-274.
29. Johns R.C., Quiring D.T., Ostaff D.P., Bauce É. Intra-tree variation in foliage quality drives the adaptive sex-biased foraging behaviors of a specialist herbivore. Oecologia 2010, 163:935-947.
30. Katovich S.A., McCullough D.G., Haack R.A. Yellowheaded Spruce Sawfly: Its Ecology and Management. General Technical Report CTR NC-179 1995, United States Department of Agriculture, Forest Service, North Central Research Station, St Paul, Minnesota.
31. Kulman H.M. Effects of insect defoliation on growth and mortality of trees. Annual Review of Entomology 1971, 16:289-324.
32. Lima S.L., Dill L.M. Behavioural decisions made under the risk of predation: a review and prospectus. Canadian Journal of Zoology 1990, 68:619-640.
33. Moreau G., Quiring D.T., Eveleigh E.S., Bauce É Advantages of a mixed diet: feeding on several foliar age classes increases the performance of a specialist insect herbivore. Oecologia 2003, 135:391-399.
34. Ohigashi H., Wagner M.R., Matsumura F., Benjamin D.M. Chemical basis of differential feeding behavior of the larch sawfly, Pristophora erichsonii (Hartig). Journal of Chemical Ecology 1981, 7:599-614.
35. Pinault L., Thurston G., Quiring D.T. The interaction of foliage and larval age influence the preference and performance of a geometrid caterpillar. Canadian Entomologist 2009, 141:136-144.
36. Pointing, P. J., 1957. Studies on the comparative ecology of two sawflies Pikonema alaskensis Roh. and Pikonema dimmockii Cress. (Tenthredinidae, Hymenoptera). Ph.D. thesis, University of Toronto.
37. Price P.W. Macroevolutionary Theory on Macroevolutionary Patterns 2003, Cambridge University Press, Cambridge.
38. Price P.W., Roininen H., Ohgushi T. Adaptive radiation into ecological niches with eruptive dynamics: a comparison of tenthredinid and diprionid sawflies. Journal of Animal Ecology 2005, 74:397-408.
39. Pulliam H.R. Diet optimization with nutrient constraints. American Naturalist 1975, 109:765-768.
40. Quiring D.T. Influence of intra-tree variation in the timing of budburst on herbivory and the behaviour and survivorship of Zeiraphera canadensis. Ecological Entomology 1993, 18:353-364.
41. Raubenheimer D., Bernays E.A. Patterns of feeding in the polyphagous grasshopper Taeniopoda eques: a field study. Animal Behaviour 1993, 45:153-167.
42. Raupp M.J., Denno R.F. Leaf age as a predictor of herbivore distribution. Variable Plants and Herbivores in Natural and Managed Systems 1983, 91-124. Academic Press, New York. R.F. Denno, M.S. McClure (Eds.).
43. Roa R. Design and analysis of multiple-choice feeding-preference experiments. Oecologia 1992, 89:509-515.
44. Roslin T., Gripenberg S., Salminen J.P., Karonen M., O'Hara R., Pihlaja K., Pulkkinen P. Seeing the trees for the leaves: oaks as mosaics for a host-specific moth. Oikos 2006, 113:106-120.
45. SAS Institute The SAS System. Version 8 for Windows 1999, SAS Institute, Cary, North Carolina.
46. Schultz J.C. Habitat selection and foraging tactics of caterpillars in heterogeneous trees. Variable Plants and Herbivores in Natural and Managed Systems 1983, 61-90. Academic Press, New York. R.F. Denno, M.S. McClure (Eds.).
47. Scriber J.M. The effects of sequentially switching food plants upon biomass and nitrogen utilization by polyphagous and stenophagous Papilio larvae. Entomologia Experimentalis et Applicata 1979, 25:203-215.
48. Simpson S.J., Raubenheimer D., Chambers P.G. The mechanisms of nutritional homeostasis. Regulatory Mechanisms in Insect Feeding 1995, 251-278. Chapman & Hall, New York. R.F. Chapman, G. de Boer (Eds.).
49. Singer M.S., Bernays E.A., Carrière Y. The interplay between nutrient balancing and toxin dilution in foraging by a generalist insect herbivore. Animal Behaviour 2002, 64:629-643.
50. Singer M.S., Rodrigues D., Stireman J.O., Carrière Y. Roles of food quality and enemy-free space in host use by a generalist insect herbivore. Ecology 2004, 85:2747-2753.
51. Stamp N.E., Bowers M.D. Variation in food quality and temperature constrains the foraging of gregarious caterpillars. Ecology 1990, 7:1031-1039.
52. Stoyenoff J.L., Witter J.A., Montogomery M.E., Chilcote C.A. Effects of host switching on gypsy moth (Lymantria dispar (L.)) under field conditions. Oecologia 1994, 97:143-157.
53. Vanderwerker G.K., Kulman H.M. Stadium and sex-determination of yellowheaded spruce sawfly larvae, Pikonema alaskensis. Annals of the Entomological Society of America 1974, 67:29-31.
54. Waldbauer G.P., Cohen R.W., Friedman S. Self-selection of an optimal nutrient mix from defined diets by larvae of the corn earthworm, Heliothis zea (Boddie). Physiological Zoology 1984, 57:590-597.
55. Westoby M. What are the biological bases of varied diets?. American Naturalist 1978, 112:627-631.
56. Whitham T.G. Host manipulation of parasites: within-plant variation as a defense against rapidly evolving pests. Variable Plants and Herbivores in Natural and Managed Systems 1983, 15-41. Academic Press, New York. R.F. Denno, M.S. McClure (Eds.).
57. Wilson L.F. Yellowheaded Spruce Sawfly. United States Department of Agriculture, Forest Service Pest Leaflet 69 1971, U.S. Government Printing Office, Washington, D.C.
58. Wrangham R.W., Waterman P.G. Feeding behaviour of vervet monkeys on Acacia tortilis and Acacia xanthophloea: with special reference to reproductive strategies and tannin production. Journal of Animal Ecology 1981, 50:715-731.
59. Yamasaki M., Kikuzawa K. Temporal and spatial variations in leaf herbivory within a canopy of Fagus crenata. Oecologia 2003, 137:226-232.
60. Zar J.H. Biostatistical Analysis 1984, Prentice Hall, Englewood Cliffs, New Jersey. 2nd edn.