Why Did Terrestrial Insect Diversity Not Increase During the Angiosperm Radiation? Mid-Mesozoic, Plant-Associated Insect Lineages Harbor Clues

  • Conrad LabandeiraEmail author


Several studies provided evidence that family-level insect diversity remained flat throughout the initial mid-Cretaceous angiosperm radiation 125–90 million years ago. As this result has engendered considerable commentary, a reanalysis was done of a new dataset of 280 plant-associated insect families spanning the 174 million year interval of the Jurassic–Paleogene periods from 201 to 23 million years ago. Lineage geochronologic ranges were determined, and feeding attributes were characterized by: (i) dominant feeding guild (herbivore, pollinator, herbivore–pollinator, pollinator–mimic, xylophage); (ii) membership in one of eight functional feeding groups; and (iii) dominant plant host or host transition (cryptogam/fern only, cryptogam/fern → angiosperm, gymnosperm only, gymnosperm → angiosperm, angiosperm only). A time-series plot of insect lineages and their dominant plant–host affiliations resulted in four conclusions. First, insect lineages with dominant gymnosperm hosts reached a level of 95 families in the 35 million years preceding the initial angiosperm radiation. Second, earlier insect lineages with gymnosperm → angiosperm host transitions and newly originated insect lineages that developed dominant associations with emerging angiosperms rapidly diversified during the angiosperm radiation, later establishing a plateau of 110 families during a 20 million year interval after the initial angiosperm radiation. Third, these two diversity maxima were separated during the angiosperm radiation by a diversity minimum, the Aptian–Albian gap, indicating major turnover and time-lag effects associated with the extirpation and acquisition of plant associations. Last, insect lineages most affected during this interval were herbivores and pollinators, exophagous feeders, and those hosting gymnosperms, angiosperms and gymnosperm → angiosperm transitions. These data largely explain the flat or even decreased level of insect diversity immediately before, during, and after the initial angiosperm radiation.


Aptian–albian gap Cretaceous Feeding guild Fern Functional feeding group Gymnosperm Host–plant preference Plant–insect interactions Stasis Time lags 



Thanks go to Pierre Pontarotti for inviting CCL to attend the Seventeenth Evolutionary Biology meeting in Marseille France. Finnegan Marsh adroitly crafted the figures. We are grateful for the Missouri Botanical Garden (St. Louis, Missouri), Wang Chen (Capital Normal University, Beijing), and Enrique Peñalver (Museo Geominero, Madrid) for use of images in Fig. 13.4. An anonymous reviewer improved the manuscript. Use of the online Paleobiology Data Base (PBDB) is acknowledged. This is contribution 263 to the Evolution of Terrestrial Ecosystems consortium at the National Museum of Natural History, in Washington, D.C.


  1. Alekseev AC, Dmitriev VY, Ponomarenko AG (2001) The evolution of taxonomic diversity. Geos, MoscowGoogle Scholar
  2. Barreda VD, Cúneo NR, Wilf P, Currano ED, Scasso RA, Brinkhuis H (2012) Cretaceous/Paleogene floral turnover in Patagonia: drop in diversity, low extinction, and a Classopollis spike. PLoS ONE 7(12):e52455PubMedCentralPubMedCrossRefGoogle Scholar
  3. Bell CD, Soltis DE, Soltis PS (2010) The age and diversification of the angiosperms re-revisited. Am J Bot 97:1296–1303PubMedCrossRefGoogle Scholar
  4. Buatois LA, Labandeira CC, Cohen AC, Mángano G, Voigt S (2015) The fossil history of continental aquatic taxa and the Mesozoic lacustrine revolution. In: Buatois LA, Mángano G (eds) The trace-fossil record of major evolutionary events, in review. Springer, Berlin (in review)Google Scholar
  5. Carpenter FM (1992) Superclass Hexapoda. In: Moore RC, Kaesler RL, Brosius E, Keim J, Priesner J (eds) Treatise on invertebrate paleontology, part R Arthropoda 4, vol 3 and 4. Geological Society of America, Boulder, and University of Kansas, LawrenceGoogle Scholar
  6. Cocroft RB, Rodriguez RL, Hunt RE (2008) Host shifts, the evolution of communication, and speciation in the Enchenopa binotata species complex of treehoppers. In: Tillmon KJ (ed) Specialization, speciation, and radiation: the evolutionary biology of herbivorous insects. University of California Press, Berkeley, pp 88–100Google Scholar
  7. Crane PR (1987) Vegetational consequences of the angiosperm diversification. In: Friis EM, Chaloner WG, Crane PR (eds) The origins of angiosperms and their biological consequences. Cambridge, New York, p 107–144Google Scholar
  8. Crane PR, Friis EM, Pedersen KR (1995) The origin and early diversification of angiosperms. Nature 374:27–33CrossRefGoogle Scholar
  9. Currano ED, Labandeira CC, Wilf P (2009) Fossilized insect folivory tracks temperature for six million years. Ecol Mon 80:547–567CrossRefGoogle Scholar
  10. Davis RB, Baldauf SL, Mayhew PJ (2010) The origins of species richness in the Hymenoptera: insights from a family-level supertree. BMC Evol Biol 10:109PubMedCentralPubMedCrossRefGoogle Scholar
  11. Davis SR, Engel MS, Legalov A, Ren D (2013) Weevils of the Yixian Formation, China (Coleoptera: Curculionoidea): phylogenetic considerations and comparison with other Mesozoic faunas. Syst Entomol 11:399–429Google Scholar
  12. Ding Q, Labandeira CC, Ren D (2014) Distinctive insect leaf mines on Liaoningocladus boii (Coniferales) from the Early Cretaceous Yixian Formation of northeastern China. Arthro Syst Phylo (in review)Google Scholar
  13. Dmitriev VJ, Zherikhin VV (1988) Changes in the diversity of insect families from data of first and last occurrences. In: Ponomarenko AG (ed) The Mesozoic-Cenozoic crisis in the evolution of insects. Nauka, Moscow, pp 208–215 (in Russian)Google Scholar
  14. Dodd JR, Stanton (1990) Paleoecology: concepts and applications, 2nd edn. Wiley, New YorkGoogle Scholar
  15. Dolling WR (1991) The Hemiptera. Oxford, New YorkGoogle Scholar
  16. Dunne JA, Labandeira CC, Williams RJ (2014) Highly resolved middle Eocene food webs show early development of modern trophic structure after the end-Cretaceous extinction. Proc Roy Soc B 281.
  17. Engel MS (2000) A new interpretation of the oldest fossil bee (Hymenoptera: Apidae). Am Mus Novit 3296:1–11CrossRefGoogle Scholar
  18. Evenhuis NL (1994) Catalogue of the fossil flies of the world (Insecta: Diptera). Backhuys, LeidenGoogle Scholar
  19. Farrell BD (1998) “Inordinate fondness” explained: why are there so many beetles? Science 281:555–559PubMedCrossRefGoogle Scholar
  20. Friis EM, Pedersen KR, Crane PR (2010) Diversity in obscurity: fossil flowers and the early history of angiosperms. Phil Trans Roy Soc B 365:369–382CrossRefGoogle Scholar
  21. Friis EM, Crane PR, Pedersen KR (2011) Early flowers and angiosperm evolution. Cambridge, CambridgeCrossRefGoogle Scholar
  22. Gauld I, Bolton B (eds) (1988) The Hymenoptera. Oxford, New YorkGoogle Scholar
  23. Goulet H, Huber JT (eds) (1993) Hymenoptera of the world: an identification guide to families. Agriculture Canada, OttawaGoogle Scholar
  24. Gradstein FM, Ogg JG, Schmitz MD, Ogg G (2012) The geologic time scale 2012. Elsevier, BostonGoogle Scholar
  25. Grimaldi D, Engel MS (2005) Evolution of the insects. Cambridge, New YorkGoogle Scholar
  26. Harris TM (1942) Wonnacottia, a new Bennettitalean microsporophyll. Ann Bot 6:577–592Google Scholar
  27. Hartkopf-Fröder C, Rust J, Wappler T, Friis EM, Viehofen A (2011) Mid-Cretaceous charred flowers reveal direct observation of arthropod feeding strategies. Biol Lett 8:295–298PubMedCentralPubMedCrossRefGoogle Scholar
  28. Hill RS, Carpenter RJ (1999) Ginkgo leaves from Paleogene sediments in Tasmania. Austral J Bot 47:717–724CrossRefGoogle Scholar
  29. Hughes N (1994) The enigma of angiosperm origins. Cambridge University Press, CambridgeGoogle Scholar
  30. Imada Y, Kawakita A, Kato M (2011) Allopatric distribution and diversification without niche shift in a bryophyte-feeding basal moth lineage (Lepidoptera: Micropterigidae). Proc Roy Soc B 278:3026–3033CrossRefGoogle Scholar
  31. Jarzembowski EA, Ross AJ (1993) Time flies: the geological record of insects. Geol Today 9:218–223CrossRefGoogle Scholar
  32. Jarzembowski EA, Ross AJ (1996) Insect origination and extinction in the Phanerozoic. In: Hart MB (ed) Biotic recovery from mass extinction events. Geol Soc Spec Publ 102:65–78Google Scholar
  33. Krassilov VA, Rasnitsyn AP, Afonin SA (2007) Pollen eaters and pollen morphology: co-evolution through the Permian and Mesozoic. Afr Invert 48:3–11Google Scholar
  34. Labandeira CC (1994) A compendium of fossil insect families. Milwaukee Publ Mus Contrib Biol Geol 88:1–71Google Scholar
  35. Labandeira CC (1997) Insect mouthparts: ascertaining the paleobiology of insect feeding strategies. Annu Rev Ecol Syst 28:153–193CrossRefGoogle Scholar
  36. Labandeira CC (1998) Early history of arthropod and vascular plant associations. Annu Rev Earth Planet Sci 26:329–377CrossRefGoogle Scholar
  37. Labandeira CC (2002) The paleobiology of predators, parasitoids, and parasites: accommodation and death in the fossil record of terrestrial invertebrates. In: Kowalewski M, Kelley PH (eds) The fossil record of predation. Paleontol Soc Pap 8:211–250Google Scholar
  38. Labandeira CC (2005) Fossil history and evolutionary ecology of Diptera and their associations with plants. In: Yeates DK, Wiegmann BM (eds) The evolutionary biology of flies. Columbia, New York, pp 217–273Google Scholar
  39. Labandeira CC (2006) Silurian to Triassic plant and insect clades and their associations: new data, a review, and interpretations. Arth Syst Phylo 64:53–94Google Scholar
  40. Labandeira CC (2007) The origin of herbivory on land: the initial pattern of live tissue consumption by arthropods. Ins Sci 14:259–274CrossRefGoogle Scholar
  41. Labandeira CC (2010) The pollination of mid Mesozoic seed plants and the early history of long-proboscid insects. Ann Missouri Bot Gard 97:469–513CrossRefGoogle Scholar
  42. Labandeira CC (2013) A paleobiological perspective on plant–insect interactions. Curr Opin Pl Biol 16:414–421CrossRefGoogle Scholar
  43. Labandeira CC, Allen EM (2007) Minimal insect herbivory for the lower Permian coprolite bone bed site of north-central Texas, USA, and comparison to other late Paleozoic floras. Palaeogeogr Palaeoclimatol Palaeoecol 247:197–219CrossRefGoogle Scholar
  44. Labandeira CC, Dilcher DL, Davis DR, Wagner DL (1994) Ninety-seven million years of angiosperm-insect association: paleobiological insights into the meaning of coevolution. Proc Natl Acad Sci USA 91:12278–12282PubMedCentralPubMedCrossRefGoogle Scholar
  45. Labandeira CC, Kvaček J, Mostovski MB (2007a) Pollination fluids, pollen, and insect pollination of Mesozoic gymnosperms. Taxon 56:663–695CrossRefGoogle Scholar
  46. Labandeira CC, Johnson KR, Wilf P (2002) Impact of the terminal Cretaceous event on plant–insect associations. Proc Natl Acad Sci USA 99:2061–2066PubMedCentralPubMedCrossRefGoogle Scholar
  47. Labandeira CC, Sepkoski JJ Jr (1993) Insect diversity in the fossil record. Science 261:310–315Google Scholar
  48. Labandeira CC, Wilf P, Johnson KR, Marsh F (2007b) Guide to insect (and other) damage types on compressed plant fossils. Version 3.0—Spring 2007). Smithsonian Institution, Washington.
  49. Lawrence JF, Ślipiński A (2013) Australian beetles: Morphology, classification and keys, vol 1. CSIRO, CollingwoodGoogle Scholar
  50. Lewis T (1973) Thrips: their biology, ecology and economic importance. Academic Press, LondonGoogle Scholar
  51. López-Vaamonde C, Wikström N, Labandeira CC, Goodman S, Godfray HCJ, Cook JM (2006) Fossil-calibrated molecular phylogenies reveal that leaf-mining moths radiated millions of years after their host plants. J Evol Biol 19:1314–1326PubMedCrossRefGoogle Scholar
  52. Magallón S (2010) Using fossils to break long branches in molecular dating: a comparison of relaxed clocks applied to the origin of angiosperms. Syst Biol 59:384–399PubMedCrossRefGoogle Scholar
  53. Marshall SA (2012) Flies: the natural history and diversity of Diptera. Firefly, BuffaloGoogle Scholar
  54. McAlpine JF, Peterson BV, Shewell GE, Teskey HJ, Vockeroth JR, Wood DW (eds) (1981–1989) Manual of Nearctic Diptera vols 1–3. Canadian Government Publishing Centre, Hull, QuebecGoogle Scholar
  55. McKenna DD, Sequeira AS, Marvaldi AE, Farrell BD (2009) Temporal lags and overlap in the diversification of weevils and flowering plants. Proc Natl Acad Sci USA 106:7083–7088PubMedCentralPubMedCrossRefGoogle Scholar
  56. McLoughlin S, Carpenter RJ, Jordan GJ, Hill RS (2008) Seed ferns survived the end-Cretaceous extinction in Tasmania. Am J Bot 95:465–471PubMedCrossRefGoogle Scholar
  57. McLoughlin S, Carpenter RJ, Pott C (2011) Ptilophyllum muelleri (Ettingsh.) comb. nov. from the Oligocene of Australia: last of the Bennettitales? Int J Plant Si 172:574–585CrossRefGoogle Scholar
  58. Miller NCE (1956) The biology of the Heteroptera. Leonard Hill, LondonGoogle Scholar
  59. Moran NA, Tran P, Gerardo NM (2005) Symbiosis and insect diversification: an ancient symbiont of sap-feeding insects from the bacterial phylum Bacteroidetes. Appl Environ Microbiol 71:8802–8810PubMedCentralPubMedCrossRefGoogle Scholar
  60. Naumann ID, Carne PB, Lawrence JF, Nielsen ES, Spradbery JP, Taylor RW, Whitten MJ, Littlejohn MJ (eds) (1991) The insects of Australia: A textbook for students and research workers, vols. 1, 2. Cornell, IthacaGoogle Scholar
  61. Nylin S, Wahlberg N (2008) Does plasticity drive speciation? Host-plant shifts and diversification in nymphaliine butterflies (Lepidoptera: Nymphalidae) during the Tertiary. Biol J Linn Soc 94:115–130CrossRefGoogle Scholar
  62. Paleobiology Database (2014) Last accessed 10 Feb 2014
  63. Pellmyr O, Seagraves K (2003) Pollinator divergence within an obligate mutualism: two yucca moth species (Lepidoptera: Prodoxidae: Tegeticula) on the Joshua tree (Yucca brevifolia; Agavaceae). Ann Entomol Soc Am 96:716–722CrossRefGoogle Scholar
  64. Peñalver E, Labandeira CC, Barrón E, Delclòs X, Nel A, Nel P, Taffoureau P, Soriano C (2012) Thrips pollination of Mesozoic gymnosperms. Proc Natl Acad Sci USA 109:8623–8628PubMedCentralPubMedCrossRefGoogle Scholar
  65. Rasnitsyn AP (1980) The origin and evolution of hymenopterous insects. Trans Paleontol Inst 174:1–192 (in Russian)Google Scholar
  66. Rasnitsyn AP (1988) Principles and methods of phylogenetic reconstruction. In: Ponomarenko AG (ed) The Mesozoic-Cenozoic crisis in the evolution of insects. Nauka, Moscow, pp 191–207 (in Russian)Google Scholar
  67. Rasnitsyn AP, Krassilov VA (2000) The first documented occurrence of phyllophagy in pre-Cretaceous insects: leaf tissues in the gut of Upper Jurassic insects from southern Kazakhstan. Paleontol J 34:301–309Google Scholar
  68. Rasnitsyn AP, Quicke DLJ (eds) (2002) History of insects. Kluwer, DordrechtGoogle Scholar
  69. Ratzel SR, Rothwell GW, Mapes G, Mapes RH, Doguzhaeva LA (2001) Pityostrobus hokodzensis, a new species of pinaceous cone from the Cretaceous of Russia. J Paleontol 75:895–900CrossRefGoogle Scholar
  70. Ren D (1998) Flower-associated Brachycera flies as fossil evidence for Jurassic angiosperm origins. Science 280:85–88PubMedCrossRefGoogle Scholar
  71. Ren D (ed) (2010) Current research on palaeoentomology. Acta Geol Sin 84(4):655–1010Google Scholar
  72. Ren D, Labandeira CC, Santiago-Blay JA, Rasnitsyn AP, Shih CK, Bashkuev A, Logan MAV, Hotton CL, Dilcher DL (2009) A probable pollination mode before angiosperms: Eurasian, long-proboscid scorpionflies. Science 326:840–847PubMedCentralPubMedCrossRefGoogle Scholar
  73. Ross AJ, Jarzembowski EA (1993) Arthropoda (Hexapoda; Insecta). In: Benton MJ (ed) The fossil record 2. Chapman & Hall, London, pp 363–426Google Scholar
  74. Schachat S, Labandeira CC, Gordon J, Chaney D, Levi S, Halthore MS, Alvarez J (2014) Plant–insect interactions from the Early Permian (Kungurian) Colwell Creek Pond, North-Central Texas: the early spread of herbivory in riparian environments. Int J Pl Sci 175: in pressGoogle Scholar
  75. Schuh RT, Slater JA (1995) True bugs of the world (Hemiptera: Heteroptera). Cornell, IthacaGoogle Scholar
  76. Sinitshenkova ND (2002) Ecological history of the aquatic insects. In: Rasnitsyn AP, Quicke DLJ (eds) History of insects. Kluwer, Dordrecht, pp 388–426Google Scholar
  77. Sohn J-C, Labandeira CC, Davis D, Mitter C (2012) An annotated catalog of fossil and subfossil Lepidoptera (Insecta: Holometabola) of the world. Zootaxa 3286:1–132Google Scholar
  78. Sukatcheva ID (1991) The Late Cretaceous stage in the history of the caddisflies (Trichoptera). Acta Hydroentom Lat 1:68–85Google Scholar
  79. Taylor TN, Taylor EL, Krings M (2009) Paleobotany: the biology and evolution of fossil plants, 2nd edn. Elsevier, AmsterdamGoogle Scholar
  80. Wang B, Szwedo J, Zhang H (2012a) New Jurassic Cercopoidea from China and their evolutionary significance (Insecta: Hemiptera). Palaeontology 55:1223–1243CrossRefGoogle Scholar
  81. Wang B, Zhang H, Jarzembowski EA (2013) Early Cretaceous angiosperms and beetle evolution. Front Pl Sci 4:360Google Scholar
  82. Wang Y, Labandeira CC, Ding Q, Shih CK, Zhao Y, Ren D (2012b) An extraordinary Jurassic mimicry between a hangingfly and ginkgo from China. Proc Natl Acad Sci USA 109:20514–20519PubMedCentralPubMedCrossRefGoogle Scholar
  83. Wang Y, Liu Z, Wang X, Shih C, Zhao Y, Engel MS, Ren D (2010) Ancient pinnate leaf mimesis among lacewings. Proc Natl Acad Sci USA 107:16212–16215PubMedCentralPubMedCrossRefGoogle Scholar
  84. Wappler T, Labandeira CC, Rust J, Frankenhäuser H, Wilde V (2012) Testing for the effects and consequences of mid-Paleogene climate change on insect herbivory. PLoS ONE 7:e40744PubMedCentralPubMedCrossRefGoogle Scholar
  85. Watson J (1977) Some Lower Cretaceous conifers of the Cheirolepidiaceae from the U.S.A. and England. Palaeontology 20:715–749Google Scholar
  86. Weingartner E, Wahlberg N, Nylin S (2006) Dynamics of host plant use and species diversity in Polygonia butterflies (Nymphalidae). J Evol Biol 19:483–491PubMedCrossRefGoogle Scholar
  87. Wilf P, Labandeira CC, Johnson KR, Cúneo NR (2005) Richness of plant–insect associations in Eocene Patagonia: a legacy for South American biodiversity. Proc Natl Acad Sci USA 102:8944–8948PubMedCentralPubMedCrossRefGoogle Scholar
  88. Wilf P, Labandeira CC, Johnson KR, Ellis B (2006) Decoupled plant and insect diversity after the end-Cretaceous extinction. Science 313:1112–1115PubMedCrossRefGoogle Scholar
  89. Winkler IS, Labandeira CC, Wappler T, Wilf P (2010) Diptera (Agromyzidae) leaf mines from the Paleogene of North America and Germany: implications for host use evolution and an early origin for the Agromyzidae. J Paleontol 84:935–954CrossRefGoogle Scholar
  90. Yeates DK, Wiegmann BM (eds) (2005) The evolutionary biology of flies. Columbia, New YorkGoogle Scholar
  91. Zhang W, Shih CK, Labandeira CC, Sohn JC, Davis DR, Santiago-Blay JA, Flint O, Ren D (2013) New fossil Lepidoptera (Insecta: Amphiesmenoptera) from the Middle Jurassic Jiulongshan Formation of Northeastern China. PLoS ONE 8(11):e79500PubMedCentralPubMedCrossRefGoogle Scholar
  92. Zherikhin VV, Mostovski MB, Vršanský P, Blagoderov VA, Lukashevich ED (1999) The unique lower Cretaceous locality Baissa and other contemporaneous fossil insect sites in North and West Transbaikalia. In: Proceedings of 1st International Palaeoentom Conference (Moscow, 1998). AMBA Projects, Bratislava, p 185–191Google Scholar
  93. Zhou Z, Zhang B (1989) A sideritic Protocupressinoxylon with insect borings and frass from the Middle Jurassic, Henan, China. Rev Palaeobot Palynol 59:133–143CrossRefGoogle Scholar

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© Springer International Publishing Switzerland 2014

Authors and Affiliations

  1. 1.Department of PaleobiologyNational Museum of Natural History, Smithsonian InstitutionWashingtonUSA
  2. 2.Department of Entomology and BEES ProgramUniversity of MarylandCollege ParkUSA
  3. 3.College of Life SciencesCapital Normal UniversityBeijingChina

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