Early Cretaceous mealybug herbivory on a laurel highlights the deep-time history of angiosperm-scale insect associations.

● Insect fluid-feeding on fossil vascular plants is an inconspicuous and underappreciated mode of herbivory that can provide novel data on the evolution of deep-time ecological associations and indicate the host-plant preferences of ancient insect herbivores. Previous fossil studies have documented piercing-and-sucking herbivory but often are unable to identify culprit insect taxa. ● One line of evidence are punctures and scale-insect impression marks made by piercing-and-sucking insects that occasionally provide clues to the systematic identities and relationships of particular insect herbivores. ● We report here the earliest occurrences of piercing and sucking on early angiosperms as evidenced by scale insect covers, impression marks, punctures, and body fossils, notably a mealybug, from the Lower Cretaceous Rose Creek Flora of the Dakota Formation (ca. 103 Ma), in southeastern Nebraska, USA. The mealybug, two other scale insect taxa, and several distinctive damage types on laurel leaves and seed-plant stems at Rose Creek document a diverse guild of piercing-and-sucking insects on early angiosperms. ● The discovery of an Early Cretaceous female mealybug indicates an early herbivorous association with a laurel host. These data provide direct evidence for co-associations and possible coevolution of scale insects and their plant hosts during early angiosperm diversification.

[1]  Shaoli Wang,et al.  Whitefly hijacks a plant detoxification gene that neutralizes plant toxins , 2021, Cell.

[2]  S. Maccracken,et al.  A new Late Cretaceous leaf mine Leucopteropsa spiralae gen. et sp. nov. (Lepidoptera: Lyonetiidae) represents the first confirmed fossil evidence of the Cemiostominae , 2021 .

[3]  G. Poinar,et al.  A mid-Cretaceous female scale insect (Hemiptera: Sternorrhyncha: Coccomorpha) in Burmese amber. , 2020, Zootaxa.

[4]  Yue-Qing Hu,et al.  Global synthesis of effects of plant species diversity on trophic groups and interactions , 2020, Nature Plants.

[5]  G. Stathas,et al.  The scale insect Coccus pseudomagnoliarum (Kuwana) (Hemiptera: Coccomorpha: Coccidae) on citrus in Greece , 2020, Hellenic Plant Protection Journal.

[6]  M. T. D. Castro,et al.  Mulberry (Morus nigra L., Moraceae) Hosting Scale Insects Crypticerya brasiliensis (Hempel, 1900) (Hemiptera: Monophlebidae) and Pseudaulacaspis pentagona (Targioni-Tozzetti, 1886) (Hemiptera: Diaspididae) in the Federal District, Brazil , 2020 .

[7]  C. Labandeira,et al.  The History of Herbivory on Sphenophytes: A New Calamitalean with an Insect Gall from the Upper Pennsylvanian of Portugal and a Review of Arthropod Herbivory on an Ancient Lineage , 2020, International Journal of Plant Sciences.

[8]  S. Maccracken,et al.  The Middle Permian South Ash Pasture Assemblage of North-Central Texas: Coniferophyte and Gigantopterid Herbivory and Longer-Term Herbivory Trends , 2020, International Journal of Plant Sciences.

[9]  R. Corlett,et al.  Plastid phylogenomics improve phylogenetic resolution in the Lauraceae , 2020, Journal of Systematics and Evolution.

[10]  C. Labandeira The Fossil Record of Insect Mouthparts: Innovation, Functional Convergence, and Associations with Other Organisms , 2019, Insect Mouthparts.

[11]  W. Judd,et al.  Early Eudicot flower and fruit: Dakotanthus gen. nov. from the Cretaceous Dakota Formation of Kansas and Nebraska, USA , 2018 .

[12]  C. Labandeira,et al.  Williamson Drive: Herbivory from a north-central Texas flora of latest Pennsylvanian age shows discrete component community structure, expansion of piercing and sucking, and plant counterdefenses , 2018 .

[13]  Dave Clarke,et al.  Molecular phylogeny of Macrosiphini (Hemiptera: Aphididae): An evolutionary hypothesis for the Pterocomma-group habitat adaptation. , 2018, Molecular phylogenetics and evolution.

[14]  C. Labandeira,et al.  Expansion of Arthropod Herbivory in Late Triassic South Africa: The Molteno Biota, Aasvoëlberg 411 Site and Developmental Biology of a Gall , 2018 .

[15]  M. Kaydan,et al.  Evolution of sensory antennal structures in the ensign scale insects (Hemiptera Coccomorpha Ortheziidae) , 2017 .

[16]  K. Golan,et al.  The phenology of Pulvinaria floccifera Westwood (Hemiptera: Coccomorpha: Coccidae), a new invasive pest on ornamentals outdoors in Poland , 2017 .

[17]  C. Labandeira,et al.  Floral Assemblages and Patterns of Insect Herbivory during the Permian to Triassic of Northeastern Italy , 2016, PloS one.

[18]  A. Dale,et al.  Tuliptree Scale Toumeyella liriodendri (Gmelin) (Insecta: Hemiptera: Coccoidea: Coccidae) , 2016, EDIS.

[19]  L. Osborne,et al.  Host Plants and Natural Enemies of Rugose Spiraling Whitefly (Hemiptera: Aleyrodidae) in Florida , 2016, Florida Entomologist.

[20]  D. Grimaldi,et al.  Putting scales into evolutionary time: the divergence of major scale insect lineages (Hemiptera) predates the radiation of modern angiosperm hosts , 2016, Scientific Reports.

[21]  Douglass R. Miller,et al.  ScaleNet: a literature-based model of scale insect biology and systematics , 2016, Database J. Biol. Databases Curation.

[22]  T. Kondo,et al.  Scale insects (Hemiptera: Coccoidea) associated with avocado crop, Persea americana Mill. (Lauraceae) in Valle del Cauca and neighboring departments of Colombia , 2016 .

[23]  C. Labandeira,et al.  Insect herbivory, plant-host specialization and tissue partitioning on mid-Mesozoic broadleaved conifers of Northeastern China , 2015 .

[24]  C. Labandeira,et al.  Insect herbivory from early Permian Mitchell Creek Flats of north-central Texas: Opportunism in a balanced component community , 2015 .

[25]  Jacek Szwedo,et al.  Brood care in a 100-million-year-old scale insect , 2015, eLife.

[26]  C. Labandeira,et al.  Evolution of a complex behavior: the origin and initial diversification of foliar galling by Permian insects , 2015, The Science of Nature.

[27]  Luis F. Aristizábal,et al.  Biology and Management of Maconellicoccus hirsutus (Hemiptera: Pseudococcidae) on Ornamental Plants , 2015 .

[28]  C. Hodgson,et al.  A review of the phylogeny of Palaearctic mealybugs (Hemiptera: Coccoidea: Pseudococcidae) , 2015, Arthropod Systematics & Phylogeny.

[29]  C. Labandeira,et al.  Plant-Insect Interactions from Early Permian (Kungurian) Colwell Creek Pond, North-Central Texas: The Early Spread of Herbivory in Riparian Environments , 2014, International Journal of Plant Sciences.

[30]  C. Labandeira,et al.  Middle Devonian liverwort herbivory and antiherbivore defence. , 2014, The New phytologist.

[31]  C. Hodgson Phenacoleachia, Steingelia, Pityococcus and Puto - Neococcoids or Archaeococcoids? An Intuitive Phylogenetic Discussion Based on Adult Male Characters , 2014 .

[32]  C. Hodgson,et al.  The phylogeny of the superfamily Coccoidea (Hemiptera: Sternorrhyncha) based on the morphology of extant and extinct macropterous males , 2013 .

[33]  M. Moghaddam A review of the mealybugs (Hemiptera: Coccoidea: Pseudococcidae, Putoidae and Rhizoecidae) of Iran, with descriptions of four new species and three new records for the Iranian fauna. , 2013, Zootaxa.

[34]  P. Bhagawati,et al.  Hypersensitive reaction and anatomical changes of young tea leaf (Camellia sinensis, clone TV1) during feeding by tea mosquito bug (Helopeltis theivora Waterhouse: Hemiptera: Miridae) , 2013 .

[35]  M. Kaydan,et al.  A taxonomic revision of the mealybug genus Ferrisia fullaway (Hemiptera: Pseudococcidae), with descriptions of eight new species and a new genus , 2012 .

[36]  Jun Wang,et al.  Permian Circulipuncturites discinisporis Labandeira, Wang, Zhang, Bek et Pfefferkorn gen. et spec. nov. (formerly Discinispora) from China, an ichnotaxon of a punch-and-sucking insect on Noeggerathialean spores , 2009 .

[37]  T. Wappler,et al.  Preservation of Armoured Scale Insects on Angiosperm Leaves from the Eocene of Germany , 2008 .

[38]  A. Rasnitsyn,et al.  Plant-Arthropod Interactions in the Early Angiosperm History: Evidence from the Cretaceous of Israel , 2008 .

[39]  L. Cook,et al.  Phylogeny and higher classification of the scale insects (Hemiptera: Sternorrhyncha: Coccoidea)* , 2007 .

[40]  Daphne E. Lee,et al.  Fossil scale insects (Hemiptera, Coccoidea, Diaspididae) in life position on an angiosperm leaf from an early Miocene lake deposit, Otago, New Zealand , 2007 .

[41]  C. Labandeira The four phases of plant-arthropod associations in deep time , 2006 .

[42]  M. Singer,et al.  The tri-trophic niche concept and adaptive radiation of phytophagous insects , 2005 .

[43]  D. Downie,et al.  Phylogenetic analysis of mealybugs (Hemiptera: Coccoidea: Pseudococcidae) based on DNA sequences from three nuclear genes, and a review of the higher classification , 2004 .

[44]  Seunghwan Lee,et al.  The genus Pseudococcus (Westwood) (Sternorrhyncha: Pseudococcidae) of Korea , 2002 .

[45]  U. Maschwitz,et al.  Acropyga and Azteca Ants (Hymenoptera: Formicidae) with Scale Insects (Sternorrhyncha: Coccoidea): 20 Million Years of Intimate Symbiosis , 2001 .

[46]  A. Chanderbali,et al.  Phylogeny and Historical Biogeography of Lauraceae: Evidence from the Chloroplast and Nuclear Genomes , 2001 .

[47]  Douglass R. Miller,et al.  Notes on a new mealybug (Hemiptera: Coccoidea: Pseudococcidae) pest in Florida and the Caribbean: the papaya mealybug, Paracoccus marginatus Williams and Granara de Willink , 1999 .

[48]  C. Labandeira,et al.  Response of plant-insect associations to paleocene-eocene warming , 1999, Science.

[49]  P. Gullan,et al.  Adaptations in scale insects. , 1997, Annual review of entomology.

[50]  C. Labandeira,et al.  Insect fluid-feeding on Upper Pennsylvanian tree ferns (Palaeodictyoptera, Marattiales) and the early history of the piercing-and-sucking functional feeding group , 1996 .

[51]  R. Denno,et al.  Local Adaptation in the Armored Scale Insect Pseudaulacaspis Pentagona (Homoptera: Diaspididae) , 1994 .

[52]  D. Dilcher,et al.  Cenomanian Angiosperm Leaf Megafossils, Dakota Formation, Rose Creek Locality, Jefferson County, Southeastern Nebraska , 1990 .

[53]  T. Wang A NEW SPECIES OF FORMICOCOCCUS TAKAHASHI FROM CHINA (HOMOPTERA: PSEUDOCOCCIDAE) , 1985 .

[54]  J. Lawton,et al.  Community Patterns and Competition in Folivorous Insects , 1981, The American Naturalist.

[55]  A. Dabbour Distribution of the scale insect Parlatoria blanchardi Targ. on date-palm trees. , 1981 .

[56]  Douglass R. Miller,et al.  Recent Advances in the Study of Scale Insects , 1979 .

[57]  P. Kevan,et al.  Interrelationships of early terrestrial arthropods and plants , 1975 .

[58]  O. Gottlieb Chemosystematics of the lauraceae , 1972 .

[59]  A. Dixon The Role of Aphids in Wood Formation. I. The Effect of the Sycamore Aphid, Dreopanosiphum platanoides (Schr.) (Aphididae), on the Growth of Sycamore, Acer pseudoplatanus (L.) , 1971 .

[60]  Denver P. Burns,et al.  Biology of the Tuliptree scale, Toumeyella liriodendri (Homoptera: Coccidae). , 1970 .