Hostname: page-component-77c89778f8-m8s7h Total loading time: 0 Render date: 2024-07-20T01:48:46.333Z Has data issue: false hasContentIssue false
  • English
  • Français

Ancient Bug Bites on Ancient Plants Record Forest Ecosystem Response to Environmental Perturbations

Published online by Cambridge University Press:  21 July 2017

Ellen D. Currano
Ellen D. Currano*
Affiliation:
Department of Geology and Environmental Earth Science, Miami University, 114 Shideler Hall, Oxford, OH 45056 USA
Get access

Abstract

Leaf-compression fossils with insect feeding traces are unique in providing rich, direct evidence of two levels in a fossil food web. Plant-insect associations dominate terrestrial trophic interactions, emphasizing the need to understand their ecological and evolutionary history. This paper first discusses methods of recognizing insect herbivore damage on fossil leaves and quantifying fossil insect herbivory. By conducting an unbiased insect damage census, damage frequency (percent of leaves with insect feeding damage), percent of leaf surface area removed by insects, and damage diversity (the number of discrete damage morphotypes, or DTs, found on a fossil flora or individual host plant) can all be measured. Three examples of responses of past plant-insect trophic interactions to environmental stresses are examined. In the first case study, late Oligocene fossil floras from Ethiopia document forest response to local perturbation and key characteristics to recognize disturbance in the plant fossil record. The second case study considers the terrestrial ecosystem response to the catastrophic global perturbation at the Cretaceous–Paleogene boundary. In the third case study, the impact of past global warming events—including the Paleocene–Eocene Thermal Maximum—on insect herbivory is discussed. Productive avenues for further research include: insect damage studies conducted outside the North American Cretaceous and Paleogene, actualistic and taphonomic studies of insect herbivory, and tighter collaboration across paleobotany, paleoentomology, botany, and entomology.

Type
Research Article
Information
The Paleontological Society Papers , Volume 19: Ecosystem Paleobiology and Geobiology , October 2013 , pp. 157 - 174
Copyright
Copyright © 2013 by The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adams, J. M., Ahn, S., Ainuddin, N., and Lee, M.-L. 2011. A further test of a palaeoecological thermometer: Tropical rainforests have more herbivore damage diversity than temperate forests. Review of Palaeobotany and Palynology, 164:60–66.CrossRefGoogle Scholar
Adams, J. M., Zhang, Y. X., Basri, M., and Shukor, N. 2009. Do tropical forest leaves suffer more insect herbivory? A comparison of tropical versus temperate herbivory, estimated from leaf litter. Ecological Research, 24:1381–1392.CrossRefGoogle Scholar
Bale, J. S., Masters, G. J., Hodkinson, I. D., Awmack, C., Bezemer, T. M., Brown, V. K., Butterfield, J., Buse, A., Coulson, J. C., Farrar, J., Good, J. E. G., Harrington, R., Hartley, S., Jones, T. H., Lindroth, R. L., Press, M. C., Symrnioudis, I., Watt, A. D., and Whittaker, J. B. 2002. Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Global Change Biology, 8:1–16.CrossRefGoogle Scholar
Barone, J. A. 2000. Comparison of herbivores and herbivory in the canopy and understory for two tropical tree species. Biotropica, 32:307–317.CrossRefGoogle Scholar
Bazzaz, F. A. 1990. The Response of natural ecosystems to the rising global CO2 levels. Annual Review of Ecology and Systematics, 21:167–196.CrossRefGoogle Scholar
Beck, A. L., and Labandeira, C. C. 1998. Early Permian insect folivory on a gigantopteriddominated riparian flora from north-central Texas. Palaeogeography, Palaeoclimatology, Palaeoecology, 142:139–173.CrossRefGoogle Scholar
Bernays, E. A., and Chapman, R. F. 1994. Host-Plant Selection by Phytophagous Insects. Chapman and Hall, London.CrossRefGoogle Scholar
Burnham, R. J. 1994. Paleoecological and floristic heterogeneity in the plant-fossil record; an analysis based on the Eocene of Washington. U. S. Geological Society Bulletin, 2085-B:B1–B36.Google Scholar
Burnham, R. J., Wing, S. L., and Parker, G. G. 1992. The reflection of deciduous forest communities in leaf litter; implications for autochthonous litter assemblages from the fossil record. Paleobiology, 18:30–49.CrossRefGoogle Scholar
Clyde, W. C., and Gingerich, P. D. 1998. Mammalian community response to the latest Paleocene thermal maximum: an isotaphonomic study in the northern Bighorn Basin, Wyoming. Geology, 26:1011–1014.2.3.CO;2>CrossRefGoogle Scholar
Coley, P. D., and Barone, J. A. 1996. Herbivory and plant defenses in tropical forests. Annual Review of Ecology and Systematics, 27:305–335.CrossRefGoogle Scholar
Coley, P. D., Bryant, J. P., and Chapin, F. S. 1985. Resource availability and plant antiherbivore defense. Science, 230:895–899.CrossRefGoogle ScholarPubMed
Coope, G. R., and Wilkins, A. S. 1994. The response of insect faunas to glacial-interglacial climatic fluctuations. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences, 344:19–26.Google Scholar
Cross, A. T., and Taggart, R. E. 1982. Causes of short-term sequential changes in fossil plant assemblages: Some considerations based on a Miocene flora of the northwest United States. Annals of the Missouri Botanical Garden, 69:676–734.CrossRefGoogle Scholar
Cui, Y. L., Kump, L. R., Ridgwell, A. J., Junium, C. K., Diefendorf, A. F., Freeman, K. H., Urban, N. M., and Harding, I. C. 2011. Slow release of fossil carbon during the Paleocene–Eocene Thermal Maximum. Nature Geoscience, 4:481–485.CrossRefGoogle Scholar
Currano, E. D. 2009. Patchiness and long-term change in early Eocene insect feeding damage. Paleobiology, 35:484–498.CrossRefGoogle Scholar
Currano, E. D., Jacobs, B. F., Pan, A. D., and Tabor, N. J. 2011a. Inferring ecological disturbance in the fossil record: A case study from the late Oligocene of Ethiopia. Palaeogeography, Palaeoclimatology, Palaeoecology, 309:242–252.CrossRefGoogle Scholar
Currano, E. D., Kattler, K. R., and Flynn, A. 2011b. Paleogene insect herbivory as a proxy for pCO2 and ecosystem stress in the Bighorn Basin, Wyoming, USA. Climate and Biota of the Early Paleogene Conference Program and Abstracts 61, Salzburg, Austria.Google Scholar
Currano, E. D., Labandeira, C. C., and Wilf, P. 2010. Fossil insect folivory tracks paleotemperature for six million years. Ecological Monographs, 80:547–567.CrossRefGoogle Scholar
Currano, E. D., Wilf, P., Wing, S. L., Labandeira, C. C., Lovelock, E. C., and Royer, D. L. 2008. Sharply increased insect herbivory during the Paleocene–Eocene Thermal Maximum. Proceedings of the National Academy of Sciences of the United States of America, 105:1960–1964.CrossRefGoogle ScholarPubMed
Deconto, R. M., Galeotti, S., Pagani, M., Travy, D., Schaefer, K., Zhang, T., Pollard, D., and Beerling, D. J. 2012. Past extreme warming events linked to massive carbon release from thawing permafrost. Nature, 484:87–91.CrossRefGoogle ScholarPubMed
Dickens, G. R., O'Neil, J. R., Rea, D. K., and Owen, R. M. 1995. Dissociation of oceanic methane hydrate as a cause of the carbon isotope excursion at the end of the Paleocene. Paleoceanography, 10:965–971.CrossRefGoogle Scholar
DiMichele, W. A., Pfefferkorn, H. W., and Gastaldo, R. A. 2001. Response of Late Carboniferous and early Permian plant communities to climate change. Annual Review of Earth and Planetary Sciences, 29:461–487.CrossRefGoogle Scholar
Dyer, L. A., Singer, M. S., Lill, J. T., Stireman, J. O., Gentry, G. L., Marquis, R. J., Ricklefs, R. E., Greeney, H. F., Wagner, D. L., Morais, H. C., Diniz, I. R., Kursar, T. A., and Coley, P. D. 2007. Host specificity of Lepidoptera in tropical and temperate forests. Nature, 448:696–699.CrossRefGoogle ScholarPubMed
Edirisooriya, G., and Dharmagunawardhane, H. A. 2013. Plant insect-interactions in Jurassic fossil flora from Sri Lanka. International Journal of Scientific and Research Publications, 3:1–12.Google Scholar
Falcon-Lang, H. J. 2004. Pennsylvanian tropical rain forests responded to glacial-interglacial rhythms. Geology, 32:689–692.CrossRefGoogle Scholar
Farrell, B. D., and Sequeira, A. S. 2004. Evolutionary rates in the adaptive radiation of beetles on plants. Evolution, 58:1984–2001.Google ScholarPubMed
Fricke, H. C., Clyde, W. C., O'Neil, J. R., and Gingerich, P. D. 1998. Evidence for rapid climate change in North America during the latest Paleocene thermal maximum: Oxygen isotope compositions of biogenic phosphate from the Bighorn Basin (Wyoming). Earth and Planetary Science Letters, 160:193–208.CrossRefGoogle Scholar
Gingerich, P. D. 1989. New earliest Wasatchian mammalian fauna from the Eocene of northwestern Wyoming: composition and diversity in a rarely sampled high-floodplain assemblage. University of Michigan Papers on Paleontology 28, Ann Arbor, Michigan.Google Scholar
Grubb, P. J., Jackson, R. V., Barberis, I. M., Bee, J. N., Coomes, D. A., Dominy, N. J., De La Fuente, M. A. S., Lucas, P. W., Metcalfe, D. J., Svenning, J.-C., Turner, I. M., and Vargas, O. 2008. Monocot leaves are eaten less than dicot leaves in tropical lowland rainforests: correlations with leaf toughness and leaf presentation. Annals of Botany, 101:1379–1389.CrossRefGoogle Scholar
Haddad, N. M., Tilman, D., Haarstad, J., Ritchie, M., and Knops, J. M. H. 2001. Contrasting effects of plant richness and composition on insect communities: a field experiment. American Naturalist, 158:17–35.CrossRefGoogle ScholarPubMed
Hawkins, B. A., and Porter, E. E. 2003. Does herbivore diversity depend on plant diversity? The case of the California butterflies. American Naturalist, 161:40–49.CrossRefGoogle ScholarPubMed
Heck, K. L., Van Belle, G., and Simberloff, D. 1975. Explicit calculation of the rarefaction diversity measurement and the determination of sufficient sample size. Ecology, 56:1459–1461.CrossRefGoogle Scholar
Hering, M. 1951. Biology of Leaf Miners. Den Hagen, Junk.CrossRefGoogle Scholar
Iglesias, A., Wilf, P., Johnson, K. R., Zamuner, A. B., Cuneo, N. R., Matheos, S. D., and Singer, B. S. 2007. A Paleocene lowland macroflora from Patagonia reveals significantly greater richness than North American analogs. Geology, 35:947–950.CrossRefGoogle Scholar
Johnson, K. R., Nichols, D. J., Attrep, M., and Orth, C. J. 1989. High-resolution leaf-fossil record spanning the Cretaceous/Tertiary boundary. Nature, 340:708–711.CrossRefGoogle Scholar
Jolivet, P. 1998. Interrelationship Between Insects and Plants. CRC Press, Boca Raton, Florida.CrossRefGoogle Scholar
Kennett, J. P., and Stott, L. D. 1991. Abrupt deep-sea warming, palaeoceanographic changes and benthic extinctions at the end of the Paleocene. Nature, 353:225–229.CrossRefGoogle Scholar
Koch, P. L., and Gingerich, P. D. 1992. Correlation between isotope records in marine and continental carbon reservoirs near the Paleocene/Eocene boundary. Nature, 358:319–322.CrossRefGoogle Scholar
Kursar, T. A., and Coley, P. D. 2003. Convergence in defense syndromes of young leaves in tropical rainforests. Biochemical Systematics and Ecology, 31:929–949.CrossRefGoogle Scholar
Kurtz, A. C., Kump, L. R., Arthur, M. A., Zachos, J. C., and Paytan, A. 2003. Early Cenozoic decoupling of the global carbon and sulfur cycles. Paleoceanography, 18:1090.CrossRefGoogle Scholar
Labandeira, C. C. 1998. Early history of arthropod and vascular plant associations. Annual Review of Earth and Planetary Sciences, 26:329–377.CrossRefGoogle Scholar
Labandeira, C. C. 2002. The history of associations between plants and animals, p. 26–74. In Herrara, C. M. and Pellmyr, O. (eds.), Plant-Animal Interactions: An Evolutionary Approach. Blackwell Science, London.Google Scholar
Labandeira, C. C. 2006. The four phases of plant-arthropod associations in deep time. Geologica Acta, 4:409–438.Google Scholar
Labandeira, C. C., and Currano, E. D. 2013. The fossil record of plant-insect dynamics. Annual Reviews of Earth and Planetary Sciences, 41:13.1–13.25.CrossRefGoogle Scholar
Labandeira, C. C., Johnson, K. R., and Lang, P. 2002a. Preliminary assessment of insect herbivory across the Cretaceous–Tertiary boundary: Major extinction and minimum rebound, p. 297–327. In Hartman, J. H., Johnson, K. R., and Nichols, D. J. (eds.), The Hell Creek Formation and the Cretaceous–Tertiary Boundary in the Northern Great Plains: An Integrated Continental Record of The End of The Cretaceous. Geological Society of America Special Paper 361, Denver, CO.CrossRefGoogle Scholar
Labandeira, C. C., Johnson, K. R., and Wilf, P. 2002b. Impact of the terminal Cretaceous event on plant-insect associations. Proceedings of the National Academy of Sciences of the United States of America, 99:2061–2066.CrossRefGoogle ScholarPubMed
Labandeira, C. C., and Phillips, T. L. 1996. A Carboniferous insect gall: Insight into early ecologic history of the Holometabola. Proceedings of the National Academy of Sciences of the United States of America, 93:8470–8474.CrossRefGoogle ScholarPubMed
Labandeira, C. C., and Sepkoski, J. J. 1993. Insect diversity in the fossil record. Science, 261:310–315.CrossRefGoogle ScholarPubMed
Labandeira, C. C., Wilf, P., Johnson, K. R., and Marsh, F. 2007. Guide to Insect (and Other) Damage Types on Compressed Plant Fossils. Version 3.0: Smithsonian Institution, Washington, D.C. http://paleobiology.si.edu/insects Google Scholar
Lincoln, D. E., Fajer, E. D., and Johnson, R. H. 1993. Plant insect herbivore interactions in elevated CO2 environments. Trends in Ecology & Evolution, 8:64–68.CrossRefGoogle Scholar
Lowman, M. D. 1987. Relationships between leaf growth and holes caused by herbivores. Australian Journal of Ecology, 12:189–191.CrossRefGoogle Scholar
Lowman, M. D. 1992. Herbivory in Australian rain forests, with particular reference to the canopies of Doryphora sassafras (Monimaceae). Biotropica, 24:263–272.CrossRefGoogle Scholar
Lowman, M. D., and Heatwole, H. 1992. Spatial and temporal variability in defoliation of australian eucalypts. Ecology, 73:129–142.CrossRefGoogle Scholar
McInerney, F. A., and Wing, S. L. 2011. The Paleocene–Eocene Thermal Maximum: A perturbation of carbon cycle, climate, and biosphere with implications for the future. Annual Review of Earth and Planetary Sciences, 39:489–516.CrossRefGoogle Scholar
Nichols, D. J. 2002. Palynology and palynostratigraphy of the Hell Creek Formation in North Dakota: A microfossil record of plants at the end of Cretaceous time, p. 393–456. In Hartman, J. H., Johnson, K. R., and Nichols, D. J. (eds.), The Hell Creek Formation and the Cretaceous–Tertiary Boundary in the Northern Great Plains: An Integrated Continental Record of The End of The Cretaceous. Geological Society of America Special Paper 361, Denver, CO.CrossRefGoogle Scholar
Novotny, V., Drozd, P., Miller, S. E., Kulfan, M., Janda, M., Basset, Y., and Weiblen, G. D. 2006. Why are there so many species of herbivorous insects in tropical rainforests? Science, 313:1115–1118.CrossRefGoogle ScholarPubMed
Novotny, V., Miller, S. E., Hulcr, J., Drew, R. A. I., Basset, Y., Janda, M., Setliff, G. P., Darrow, K., Stewart, A. J. A., Auga, J., Isua, B., Molem, K., Manumbor, M., Tamtiai, E., Mogia, M., and Weiblen, G. D. 2007. Low beta diversity of herbivorous insects in tropical forests. Nature, 448:692–697.CrossRefGoogle ScholarPubMed
Price, P. W. 1991. Patterns in communities along latitudinal gradients, p. 51–69. In Price, P. W., Lewinsohn, T. M., Fernandes, G. W., and Benson, W. W. (eds.), Plant-Animal Interactions: Evolutionary Ecology in Tropical and Temperate Regions. Wiley, New York.Google Scholar
Price, P. W. 2002. Resource-driven terrestrial interaction webs. Ecological Research, 17:241–247.CrossRefGoogle Scholar
Ramírez-Carvalho, M., Wilf, P., Barrios, H., Currano, E. D., Jaramillo, C., Labandeira, C. C., and Windsor, D. M. 2009. Is insect damage diversity correlated with insect diversity? Preliminary results from the Panama canopy cranes and implications for plant-insect associational diversity in the fossil record. Geological Society of America Annual Meeting Abstracts with Programs, 41:162.Google Scholar
Röhl, U., Westerhold, T., Bralower, T. J., and Zachos, J. C. 2007. On the duration of the Paleocene–Eocene Thermal Maximum (PETM). Geochemistry, Geophysics, Geosystems, 8:Q12002.CrossRefGoogle Scholar
Rose, K. D. 1981. The Clarkforkian Land-Mammal Age and Mammalian Faunal Composition Across the Paleocene–Eocene Boundary. University of Michigan Papers on Paleontology 26, Ann Arbor, Michigan.Google Scholar
Royer, D. L., Sack, L., Wilf, P., Lusk, C. H., Jordan, G. J., Niinemets, U., Wright, I. J., Westoby, M., Cariglino, B., Coley, P. D., Cutter, A. D., Johnson, K. R., Labandeira, C. C., Moles, A. T., Palmer, M. B., and Valladares, F. 2007. Fossil leaf economics quantified: calibration, Eocene case study, and implications. Paleobiology, 33:574–589.CrossRefGoogle Scholar
Secord, R., Bloch, J. I., Chester, S. G. B., Boyer, D. M., Wood, A. R., Wing, S. L., Kraus, M. J., McInerney, F. A., and Krigbaum, J. 2012. Evolution of the earliest horses driven by climate change in the Paleocene–Eocene Thermal Maximum. Science, 335:959–962.CrossRefGoogle ScholarPubMed
Siemann, E., Tilman, D., and Haarstad, J. 1996. Insect species diversity, abundance and body size relationships. Nature, 380:704–706.CrossRefGoogle Scholar
Smith, D. M. 2008. A comparison of plant-insect associations in the middle Eocene Green River Formation and the Upper Eocene Florissant Formation and their climatic implications, p. 89–103. In Meyer, H. W., and Smith, D. M. (eds.), Paleontology of the Upper Eocene Florissant Formation, Colorado. Geological Society of America Special Paper 435. The Geological Society of America, Boulder, Colorado.Google Scholar
Smith, D. M., and Nufio, C. R. 2004. Levels of herbivory in two Costa Rican rain forests: Implications for studies of fossil herbivory. Biotropica, 36:318–326.Google Scholar
Smith, J. J., Hasiotis, S. T., Kraus, M. J., and Woody, D. T. 2009. Transient dwarfism of soil fauna during the Paleocene–Eocene Thermal Maximum. Proceedings of the National Academy of Sciences of the United States of America, 106:17655–17660.CrossRefGoogle ScholarPubMed
Svensen, H., Planke, S., Malthe-Sorenssen, A., Jamtveit, B., Myklebust, R., Eidem, T. R., and Rey, S. S. 2004. Release of methane from a volcanic basin as a mechanism for initial Eocene global warming. Nature, 429:542–545.CrossRefGoogle ScholarPubMed
Termonia, A., Hsiao, T. H., Pasteels, J. M., and Milinkovitch, M. C. 2001. Feeding specialization and host-derived chemical defense in Chrysomeline leaf beetles did not lead to an evolutionary dead end. Proceedings of the National Academy of Sciences of the United States of America, 98:3909–3914.CrossRefGoogle ScholarPubMed
Vajda, V., Raine, J. I., and Hollis, C. J. 2001. Indication of global deforestation at the Cretaceous–Tertiary boundary by New Zealand fern spike. Science, 294:1700–1702.CrossRefGoogle ScholarPubMed
Wappler, T., Currano, E. D., Wilf, P., Rust, J., and Labandeira, C. C. 2009. No post-Cretaceous ecosystem depression in European forests? Rich insect-feeding damage on diverse middle Palaeocene plants, Menat, France. Proceedings of the Royal Society B-Biological Sciences, 276:4271–4277.CrossRefGoogle ScholarPubMed
Wappler, T., and Denk, T. 2011. Herbivory in early Tertiary Arctic forests. Palaeogeography, Palaeoclimatology, Palaeoecology, 310:283–295.CrossRefGoogle Scholar
Watt, A. D., Whittaker, J. B., Docherty, M., Brooks, G., Lindsay, E., and Salt, D. T. 1995. The impact of elevated atmospheric CO2 on insect herbivores, p. 198–217. In Harrington, R. and Stork, N. (eds.), Insects in a Changing Environment. Academic Press, San Diego.Google Scholar
Wilf, P., and Johnson, K. R. 2004. Land plant extinction at the end of the Cretaceous: a quantitative analysis of the North Dakota megafloral record. Paleobiology, 30:347–368.2.0.CO;2>CrossRefGoogle Scholar
Wilf, P., and Labandeira, C. C. 1999. Response of plant-insect associations to Paleocene–Eocene warming. Science, 284:2153–2156.CrossRefGoogle ScholarPubMed
Wilf, P., Labandeira, C. C., Kress, W. J., Staines, C. L., Windsor, D. M., Allen, A. L., and Johnson, K. R. 2000. Timing the radiations of leaf beetles: Hispines on gingers from latest Cretaceous to recent. Science, 289:291–294.CrossRefGoogle ScholarPubMed
Wilf, P., Labandeira, C. C., Johnson, K. R., Coley, P. D., and Cutter, A. D. 2001. Insect herbivory, plant defense, and early Cenozoic climate change. Proceedings of the National Academy of Sciences of the United States of America, 98:6221–6226.CrossRefGoogle ScholarPubMed
Wilf, P., Labandeira, C. C., Johnson, K. R., and Ellis, B. 2006. Decoupled plant and insect diversity after the end-Cretaceous extinction. Science, 313:1112–1115.CrossRefGoogle ScholarPubMed
Wing, S. L., Alroy, J., and Hickey, L. J. 1995. Plant and mammal diversity in the Paleocene to early Eocene of the Bighorn Basin. Palaeogeography, Palaeoclimatology, Palaeoecology, 115:117–155.CrossRefGoogle Scholar
Wing, S. L., Bao, H., and Koch, P. L. 2000. An early Eocene cool period? Evidence for continental cooling during the warmest part of the Cenozoic, p. 197–237. In Huber, B. T., MacLeod, K. G., and Wing, S. L. (eds.), Warm Climates in Earth History. Oxford University Press, Cambridge.Google Scholar
Wing, S. L., Harrington, G. J., Smith, F. A., Bloch, J. I., Boyer, D. M., and Freeman, K. H. 2005. Transient floral change and rapid global warming at the Paleocene–Eocene boundary. Science, 310:993–996.CrossRefGoogle ScholarPubMed
Wing, S. L., Herrera, F., Jaramillo, C. A., Gómez-Navarro, C., Wilf, P., and Labandeira, C. C. 2009. Late Paleocene fossils from the Cerrejón Formation, Colombia, are the earliest record of Neotropical rainforest. Proceedings of the National Academy of Sciences of the United States of America, 106:18627–18632.CrossRefGoogle ScholarPubMed
Wing, S. L., and Currano, E. D. 2013. The response of plants to a global greenhouse event 56 million years ago. American Journal of Botany, 100:1234–1254.CrossRefGoogle ScholarPubMed
Winkler, I. S., Mitter, C., and Scheffer, S. J. 2009. Repeated climate-linked host shifts have promoted diversification in a temperate clade of leaf-mining flies. Proceedings of the National Academy of Sciences of the United States of America, 106:18103–18108.CrossRefGoogle Scholar
Winkler, I. S., Labandeira, C. C., Wappler, T., and Wilf, P. 2010. Distinguishing Agromyzidae (Diptera) leaf mines in the fossil record: New taxa from the Paleogene of North America and Germany and their evolutionary implications. Journal of Paleontology, 84:935–954.CrossRefGoogle Scholar
Wint, G. R. W. 1983. Leaf damage in tropical rain forest canopies, p. 229–239. In Sutton, S. L., Whitmore, C., and Chadwick, A. C. (eds.), Tropical Rain Forest: Ecology and Management. Blackwell, Boston.Google Scholar
Wright, M. G., and Samways, M. J. 1998. Insect species richness tracking plant species richness in a diverse flora: gall-insects in the Cape Floristic Region, South Africa. Oecologia, 115:427–433.CrossRefGoogle Scholar
Zachos, J. C., Wara, M. W., Bohaty, S., Delaney, M. L., Petrizzo, M. R., Brill, A., Bralower, T. J., and Premoli-Silva, I. 2003. A transient rise in tropical sea surface temperature during the Paleocene–Eocene Thermal Maximum. Science, 302:1551–1554.CrossRefGoogle ScholarPubMed
Zhang, Y., Adams, J. M., and Zhao, D. 2011. Does insect folivory vary with latitude among temperate deciduous forests? Ecological Research, 26:377–383.CrossRefGoogle Scholar