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Deep-time patterns of tissue consumption by terrestrial arthropod herbivores

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Abstract

A survey of the fossil record of land-plant tissues and their damage by arthropods reveals several results that shed light on trophic trends in host-plant resource use by arthropods. All 14 major plant tissues were present by the end of the Devonian, representing the earliest 20 % of the terrestrial biota. During this interval, two types of time lags separate the point between when tissues first originated from their earliest consumption by herbivorous arthropods. For epidermis, parenchyma, collenchyma and xylem, live tissue consumption was rapid, occurring on average 10 m.y. after the earliest tissue records. By contrast, structural tissues (periderm, sclerenchyma), tissues with actively dividing cells (apical, lateral, intercalary meristems), and reproductive tissues (spores, megagametophytes, integuments) experienced approximately a 9-fold (92 m.y.) delay in arthropod herbivory, extending well into the Carboniferous Period. Phloem similarly presents a delay of 85 m.y., but this incongruously long lag-time may be attributed to the lack of preservation of this tissue in early vascular plants. Nevertheless, the presence of phloem can be indicated from planar spaces adjacent well-preserved xylem, or inferred from a known anatomy of the same plant taxon in better preserved material, especially permineralisations. The trophic partitioning of epidermis, parenchyma, phloem and xylem increases considerably to the present, probably a consequence of dietary specialization or consumption of whole leaves by several herbivore functional feeding groups. Structural tissues, meristematic tissues and reproductive tissues minimally have been consumed throughout the fossil record, consistent with their long lags to herbivory during the earlier Paleozoic. Neither angiosperm dominance in floras nor global environmental perturbations had any discernible effect on herbivore trophic partitioning of plant tissues.

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Acknowledgments

This study is an outgrowth of a presentation at the fourth Euro Evo-Devo meeting in Lisbon during July of 2012. Thanks go to Finnegan Marsh for constructing Figs. 1 and 2. Two anonymous reviewers and especially Richard Bateman provided superb reviews. This is contribution 259 of the Evolution of Terrestrial Ecosystems consortium at the National Museum of Natural History, Washington, D.C.

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Correspondence to Conrad C. Labandeira.

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Communicated by: Beverley Glover

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Labandeira, C.C. Deep-time patterns of tissue consumption by terrestrial arthropod herbivores. Naturwissenschaften 100, 355–364 (2013). https://doi.org/10.1007/s00114-013-1035-4

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