Response of plant-insect associations to paleocene-eocene warming

Science

Volumn 284, Issue 5423, 1999, Pages 2153-2156

  Wilf, Peter ^a,c   Labandeira, Conrad C ^a,b  

^a DEPARTMENT OF PALEOBIOLOGY   (United States)

^b University of Maryland   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HERBIVORY; PALEOCENE-EOCENE BOUNDARY; PALEOCLIMATE; PLANT-INSECT INTERACTION; WARMING;

ANIMAL BEHAVIOR; ARTICLE; BIODIVERSITY; ENVIRONMENTAL TEMPERATURE; FEEDING BEHAVIOR; FOSSIL; GEOGRAPHY; GEOLOGY; INSECT; NONHUMAN; PLANT; PRIORITY JOURNAL;

ANIMALIA; BETULACEAE; HEXAPODA; INSECTA;

EID: 0033603533     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.284.5423.2153     Document Type: Article

References (55)

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16. T. L. Erwin, Coleopt. Bull. 36, 74 (1982); P. D. Coley and T. M. Aide, in Plant Animal Interactions: Evolutionary Ecology in Tropical and Temperate Regions, P. W. Price, T. M. Lewinsohn, G. W. Fernandes, B. B. Benson, Eds. (Wiley, New York, 1991), pp. 25-49; P. D. Coley and J. A. Barone, Annu. Rev. Ecol. Syst. 27, 305 (1996); M. G. Wright and M. J. Samways, Oecologia 115, 427 (1998).
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18. Y. Basset, Acta Oecol. 15, 181 (1994).
19. 2 has been postulated as a cause of Paleocene-Eocene warming [D. K. Rea, J. C. Zachos, R. M. Owen, P. D. Gingerich, Palaeogeogr. Palaeoclimatol. Palaeoecol. 79, 117 (1990)], but this hypothesis is not yet supported by proxy and model data [E. Thomas, in Late Paleocene-Early Eocene Climatic and Biotic Events in the Marine and Terrestrial Records, M.-P. Aubry, S. G. Lucas, W. A. Berggren, Eds. (Columbia Univ. Press, New York, 1998), pp. 214-235].
20. 2 has been postulated as a cause of Paleocene-Eocene warming [D. K. Rea, J. C. Zachos, R. M. Owen, P. D. Gingerich, Palaeogeogr. Palaeoclimatol. Palaeoecol. 79, 117 (1990)], but this hypothesis is not yet supported by proxy and model data [E. Thomas, in Late Paleocene-Early Eocene Climatic and Biotic Events in the Marine and Terrestrial Records, M.-P. Aubry, S. G. Lucas, W. A. Berggren, Eds. (Columbia Univ. Press, New York, 1998), pp. 214-235].
21. 2 has been postulated as a cause of Paleocene-Eocene warming [D. K. Rea, J. C. Zachos, R. M. Owen, P. D. Gingerich, Palaeogeogr. Palaeoclimatol. Palaeoecol. 79, 117 (1990)], but this hypothesis is not yet supported by proxy and model data [E. Thomas, in Late Paleocene-Early Eocene Climatic and Biotic Events in the Marine and Terrestrial Records, M.-P. Aubry, S. G. Lucas, W. A. Berggren, Eds. (Columbia Univ. Press, New York, 1998), pp. 214-235].
22. 2 has been postulated as a cause of Paleocene-Eocene warming [D. K. Rea, J. C. Zachos, R. M. Owen, P. D. Gingerich, Palaeogeogr. Palaeoclimatol. Palaeoecol. 79, 117 (1990)], but this hypothesis is not yet supported by proxy and model data [E. Thomas, in Late Paleocene-Early Eocene Climatic and Biotic Events in the Marine and Terrestrial Records, M.-P. Aubry, S. G. Lucas, W. A. Berggren, Eds. (Columbia Univ. Press, New York, 1998), pp. 214-235].
23. P. Wilf, Geol. Soc. Am. Bull., in press.
24. The late Paleocene sample is sample 2 of (9), a lumped Clarkforkian assemblage. The Eocene sample, from the Cenozoic thermal maximum, is the middle Wasatchian Sourdough flora, Great Divide Basin, sample 5 of (9). The Paleocene sample is time-averaged over ∼0.5 million years, during which some temperature increase occurred (9, 12, 25), whereas the more diverse Eocene sample is not significantly time-averaged and is derived from fewer localities. A total leaf count was not made because not all identifiable specimens were collected from every locality. An unbiased measure is that 7511 leaves have been identified from the 15 localities that were censused on the outcrop (9); the total number of leaves examined from alt 80 localities was far greater. Although floras from intervening stratigraphic intervals are known (9), the two samples used here are among the best preserved and are derived from many more localities. Deciduous taxa were more abundant than evergreens in both samples, although evergreens were more diverse in the Eocene sample (9). "Species" is used here to indicate both described species and undescribed forms considered as operational species in (9). Voucher collections, from the 1994 to 1996 and 1998 field seasons, are housed at the U.S. National Museum of Natural History (USNM), with supplementary material at the Denver Museum of Natural History and the Florida Museum of Natural History (9).
25. A. K. Behrensmeyer and R. W. Hook, in Terrestrial Ecosystems Through Time, A. K. Behrensmeyer et al., Eds. (Univ. of Chicago Press, Chicago, IL, 1992), pp. 15-136.
26. P. Wilf, K. C. Beard, K. S. Davies-Vollum, J. W. Norejko, Palaios 13, 514 (1998).
27. A damage type (Table 1) was assigned if a distinctive insect feeding mode, or ecotype, was represented. No damage was found on conifers, cycads, or aquatic angiosperms, and damage on ferns was rare.
28. The primary goal of initial collecting (1994 to 1996 field seasons) was to reconstruct floral diversity and leaf morphology, with some resulting collection bias against common species and consequently against their insect damage. The field censusing of insect damage (in 1998) allowed unbiased sampling of herbivory on all species to complement that known from collections and also permitted the observed damage frequencies to be related as directly as possible to the relative abundances of host plants in the source forests [R. J. Burnham, S. L. Wing, G. G. Parker, Paleobiology 18, 30 (1992)].
29. The Corylites sp., from the Paleocene sample only, was described as the presumed foliage of Palaeocarpinus aspinosa Manchester and Chen [S. R. Manchester and Z. Chen, Int. J. Plant Sci. 157, 644 (1996)]. The Alnus sp., undescribed, is known from leaves, female cones, and staminate inflorescences in early Eocene deposits of southern and northern Wyoming (9, 25). These taxa occurred at the largest number of localities (Fig. 5) and also were most frequently the dominant species at individual localities (9).
30. D. H. Janzen, Am. Nat. 102, 592 (1968); P. A. Opler, Am. Sci. 62, 67 (1974); P. P. Feeny, in Biochemical Interaction Between Plants and Insects, J. Wallace and R. L. Mansell, Eds. (Plenum, New York, 1976), pp. 1-40.
31. D. H. Janzen, Am. Nat. 102, 592 (1968); P. A. Opler, Am. Sci. 62, 67 (1974); P. P. Feeny, in Biochemical Interaction Between Plants and Insects, J. Wallace and R. L. Mansell, Eds. (Plenum, New York, 1976), pp. 1-40.
32. D. H. Janzen, Am. Nat. 102, 592 (1968); P. A. Opler, Am. Sci. 62, 67 (1974); P. P. Feeny, in Biochemical Interaction Between Plants and Insects, J. Wallace and R. L. Mansell, Eds. (Plenum, New York, 1976), pp. 1-40.
33. J. Reichholf, Waldhygiene 10, 247 (1974); J. M. Cobos-Suarez, Bol. Sanid. Veg. 14, 1 (1988); B. Gharadjedaghi, Anz. Schaedlingskd. Pflanz. Umweltschutz 70, 145 (1997); B. Gharadjedaghi, Forstwiss. Centralbl. 116, 158 (1997); J. Oleksyn et al., New Phytol. 140, 239 (1998).
34. J. Reichholf, Waldhygiene 10, 247 (1974); J. M. Cobos-Suarez, Bol. Sanid. Veg. 14, 1 (1988); B. Gharadjedaghi, Anz. Schaedlingskd. Pflanz. Umweltschutz 70, 145 (1997); B. Gharadjedaghi, Forstwiss. Centralbl. 116, 158 (1997); J. Oleksyn et al., New Phytol. 140, 239 (1998).
35. J. Reichholf, Waldhygiene 10, 247 (1974); J. M. Cobos-Suarez, Bol. Sanid. Veg. 14, 1 (1988); B. Gharadjedaghi, Anz. Schaedlingskd. Pflanz. Umweltschutz 70, 145 (1997); B. Gharadjedaghi, Forstwiss. Centralbl. 116, 158 (1997); J. Oleksyn et al., New Phytol. 140, 239 (1998).
36. J. Reichholf, Waldhygiene 10, 247 (1974); J. M. Cobos-Suarez, Bol. Sanid. Veg. 14, 1 (1988); B. Gharadjedaghi, Anz. Schaedlingskd. Pflanz. Umweltschutz 70, 145 (1997); B. Gharadjedaghi, Forstwiss. Centralbl. 116, 158 (1997); J. Oleksyn et al., New Phytol. 140, 239 (1998).
37. J. Reichholf, Waldhygiene 10, 247 (1974); J. M. Cobos-Suarez, Bol. Sanid. Veg. 14, 1 (1988); B. Gharadjedaghi, Anz. Schaedlingskd. Pflanz. Umweltschutz 70, 145 (1997); B. Gharadjedaghi, Forstwiss. Centralbl. 116, 158 (1997); J. Oleksyn et al., New Phytol. 140, 239 (1998).
38. O. Q. Hendrickson, W. H. Fogal, D. Burgess, Can. J. Bot. 69, 1919 (1991).
39. P. D. Coley, Oecologia 74, 531 (1988).
40. Damage frequency in fossil floras has been significantly lower than modern values in several studies (5), as we find here. Although insect damage may well have increased through time, it is likely that several factors would make damage appear less prevalent in fossil assemblages, including taphonomic bias against damaged leaves, the rarity of complete fossil leaves, the inability to observe completely consumed leaves, and the low probability of preservation for minute damage types, such as piercing and sucking. We consider good preservation of leaves (highest order venation visible on the majority of specimens, more than half of the original leaf usually present) and a fine-grained matrix, as in this study, to be prerequisites for censusing of insect damage. Insect damage by its nature reduces the preservability of leaves by creating tear points, although this bias needs to be quantified in actualistic studies.
41. Corylites and Alnus fit well with the resource availability hypothesis [P. D. Coley, J. P. Bryant, F. S. Chapin III, Science 230, 895 (1985)) in which high herbivory rates are correlated with short leaf lifespan (Corylites and Alnus were deciduous), high growth rates and relatively early successional status (Corylites and Alnus had tiny, wind-or water-dispersed fruits and colonized disturbed environments on floodplains), and low concentrations of defensive compounds (implied).
42. G. Bond, in Symbiotic Nitrogen Fixation in Plants, P. S. Nutman, Ed. (Cambridge Univ. Press, Cambridge, 1976), pp. 443-474; C. P. Onuf, J. M. Teal, I. Valiela, Ecology 58, 514 (1977); W. J. Mattson Jr., Annu. Rev. Ecol. Syst. 11, 119 (1980); R. E. Ricklefs and K. K. Matthew, Can. J. Bot. 60, 2037 (1982); J. J. Furlow, in Magnoliophyta: Magnolildae and Hamamelidae, vol. 3 of Flora of North America, Flora of North America Editorial Committee, Ed. (Oxford Univ. Press, New York, 1997), pp. 507-538. Phylogenetic analysis of DNA sequences from the rbcL gene places all actinorhizal plants within a single clade, indicating that actinorhizal association is ancient [D. E. Soltis et al., Proc. Natl. Acad. Sci. U.S.A. 92, 2647 (1995)].
43. G. Bond, in Symbiotic Nitrogen Fixation in Plants, P. S. Nutman, Ed. (Cambridge Univ. Press, Cambridge, 1976), pp. 443-474; C. P. Onuf, J. M. Teal, I. Valiela, Ecology 58, 514 (1977); W. J. Mattson Jr., Annu. Rev. Ecol. Syst. 11, 119 (1980); R. E. Ricklefs and K. K. Matthew, Can. J. Bot. 60, 2037 (1982); J. J. Furlow, in Magnoliophyta: Magnolildae and Hamamelidae, vol. 3 of Flora of North America, Flora of North America Editorial Committee, Ed. (Oxford Univ. Press, New York, 1997), pp. 507-538. Phylogenetic analysis of DNA sequences from the rbcL gene places all actinorhizal plants within a single clade, indicating that actinorhizal association is ancient [D. E. Soltis et al., Proc. Natl. Acad. Sci. U.S.A. 92, 2647 (1995)].
44. G. Bond, in Symbiotic Nitrogen Fixation in Plants, P. S. Nutman, Ed. (Cambridge Univ. Press, Cambridge, 1976), pp. 443-474; C. P. Onuf, J. M. Teal, I. Valiela, Ecology 58, 514 (1977); W. J. Mattson Jr., Annu. Rev. Ecol. Syst. 11, 119 (1980); R. E. Ricklefs and K. K. Matthew, Can. J. Bot. 60, 2037 (1982); J. J. Furlow, in Magnoliophyta: Magnolildae and Hamamelidae, vol. 3 of Flora of North America, Flora of North America Editorial Committee, Ed. (Oxford Univ. Press, New York, 1997), pp. 507-538. Phylogenetic analysis of DNA sequences from the rbcL gene places all actinorhizal plants within a single clade, indicating that actinorhizal association is ancient [D. E. Soltis et al., Proc. Natl. Acad. Sci. U.S.A. 92, 2647 (1995)].
45. G. Bond, in Symbiotic Nitrogen Fixation in Plants, P. S. Nutman, Ed. (Cambridge Univ. Press, Cambridge, 1976), pp. 443-474; C. P. Onuf, J. M. Teal, I. Valiela, Ecology 58, 514 (1977); W. J. Mattson Jr., Annu. Rev. Ecol. Syst. 11, 119 (1980); R. E. Ricklefs and K. K. Matthew, Can. J. Bot. 60, 2037 (1982); J. J. Furlow, in Magnoliophyta: Magnolildae and Hamamelidae, vol. 3 of Flora of North America, Flora of North America Editorial Committee, Ed. (Oxford Univ. Press, New York, 1997), pp. 507-538. Phylogenetic analysis of DNA sequences from the rbcL gene places all actinorhizal plants within a single clade, indicating that actinorhizal association is ancient [D. E. Soltis et al., Proc. Natl. Acad. Sci. U.S.A. 92, 2647 (1995)].
46. G. Bond, in Symbiotic Nitrogen Fixation in Plants, P. S. Nutman, Ed. (Cambridge Univ. Press, Cambridge, 1976), pp. 443-474; C. P. Onuf, J. M. Teal, I. Valiela, Ecology 58, 514 (1977); W. J. Mattson Jr., Annu. Rev. Ecol. Syst. 11, 119 (1980); R. E. Ricklefs and K. K. Matthew, Can. J. Bot. 60, 2037 (1982); J. J. Furlow, in Magnoliophyta: Magnolildae and Hamamelidae, vol. 3 of Flora of North America, Flora of North America Editorial Committee, Ed. (Oxford Univ. Press, New York, 1997), pp. 507-538. Phylogenetic analysis of DNA sequences from the rbcL gene places all actinorhizal plants within a single clade, indicating that actinorhizal association is ancient [D. E. Soltis et al., Proc. Natl. Acad. Sci. U.S.A. 92, 2647 (1995)].
47. G. Bond, in Symbiotic Nitrogen Fixation in Plants, P. S. Nutman, Ed. (Cambridge Univ. Press, Cambridge, 1976), pp. 443-474; C. P. Onuf, J. M. Teal, I. Valiela, Ecology 58, 514 (1977); W. J. Mattson Jr., Annu. Rev. Ecol. Syst. 11, 119 (1980); R. E. Ricklefs and K. K. Matthew, Can. J. Bot. 60, 2037 (1982); J. J. Furlow, in Magnoliophyta: Magnolildae and Hamamelidae, vol. 3 of Flora of North America, Flora of North America Editorial Committee, Ed. (Oxford Univ. Press, New York, 1997), pp. 507-538. Phylogenetic analysis of DNA sequences from the rbcL gene places all actinorhizal plants within a single clade, indicating that actinorhizal association is ancient [D. E. Soltis et al., Proc. Natl. Acad. Sci. U.S.A. 92, 2647 (1995)].
48. Insect damage on the single dicot species that was abundant in both samples (Averrhoites affinis) increased from five types in the Paleocene to nine in the Eocene (Fig. 5).
49. Although the most specialized damage types are rare, sampling was intensive (10, 14), which supports our view that the inferred turnover of herbivores is not a sampling artifact. The percentages listed should be regarded as minima given the difficulty of evaluating the more generalized feeding groups.
50. S. L. Wing, H. Bao, P. L. Koch, in Warm Climates in Earth History, B. T. Huber, K. MacLeod, S. L. Wing, Eds. (Cambridge Univ. Press, Cambridge, 1999), pp. 197-237.
51. R. N. Coulson and J. A. Witter, Forest Entomology: Ecology and Management (Wiley, New York, 1984).
52. P. Wilf, Paleobiology 23, 373 (1997).
53. L. J. Webb, J. Ecol. 47, 551 (1959). The logarithmic mean area was used for each Webb category to estimate total leaf area [P. Wilf, S. L. Wing, D. R. Greenwood, C. L. Greenwood, Geology 26, 203 (1998)].
54. L. J. Webb, J. Ecol. 47, 551 (1959). The logarithmic mean area was used for each Webb category to estimate total leaf area [P. Wilf, S. L. Wing, D. R. Greenwood, C. L. Greenwood, Geology 26, 203 (1998)].
55. We thank A. Ash, R. Schrott, K. Werth, and others for field and laboratory assistance, Western Wyoming Community College for logistical support, and W. DiMichele, P. Dodson, R. Horwitt, B. Huber, S. Wing, and two anonymous reviewers for helpful comments on the manuscript. P.W. was supported by Smithsonian Institution predoctoral and postdoctoral fellowships, the Smithsonian's Evolution of Terrestrial Ecosystems Program (ETE), a University of Pennsylvania Dissertation Fellowship, the Geological Society of America, Sigma Xi, and the Paleontological Society. C.C.L. was supported by the Walcott Fund of the National Museum of Natural History. This is ETE contribution number 68.