Florivory of Early Cretaceous flowers by functionally diverse insects: implications for early angiosperm pollination

Abstract

Florivory (flower consumption) occurs worldwide in modern angiosperms, associated with pollen and nectar consumption. However, florivory remains unrecorded from fossil flowers since their Early Cretaceous appearance. We test hypotheses that earliest angiosperms were pollinated by a diverse insect fauna by evaluating 7858 plants from eight localities of the latest Albian Dakota Formation from midcontinental North America, in which 645 specimens (8.2%) were flowers or inflorescences. Well-preserved specimens were categorized into 32 morphotypes, nine of which displayed 207 instances of damage from 11 insect damage types (DTs) by four functional-feeding groups of hole feeding, margin feeding, surface feeding and piercing-and-sucking. We assessed the same DTs inflicted by known florivores on modern flowers that also are their pollinators, and associated insect mouthpart types causing such damage. The diverse, Dakota florivore–pollinator community showed a local pattern at Braun's Ranch of flower morphotypes 4 and 5 having piercing-and-sucking as dominant and margin feeding as minor interactions, whereas Dakotanthus cordiformis at Rose Creek I and II had an opposite pattern. We found no evidence for nectar robbing. These data support the rapid emergence of early angiosperms of florivore and associated pollinator guilds expressed at both the local and regional community levels.

The Angiosperm Terrestrial Revolution and the origins of modern biodiversity

“…These in turn have their predators, including other insects such as the hyperdiverse parasitoid wasps (Labandeira & Li, 2021), a key element in structuring the ATR, along with reptiles, birds and mammals. Specialized insect–angiosperm pollination associations are known from fossils in the Cretaceous (Grimaldi & Engel, 2005; Hu et al ., 2008; Bao et al ., 2019; Tihelka et al ., 2021; Xiao et al ., 2021), confirming phylogenetic studies, including that insect pollination might have been present in ancestors of angiosperms (van der Niet & Johnson, 2012; Gervasi & Schiestl, 2017) as strongly suggested by fossil evidence from extinct gymnosperms (Labandeira, 2010). Indeed, experiments with angiosperms, pollinators, and herbivores show how these mutualisms stimulate rapid evolutionary change and diversification (Ramos & Schiestl, 2019).…”

Data, metrics, and methods for arthropod and fungal herbivory at the dawn of angiosperm diversification: The Rose Creek plant assemblage of Nebraska, U.S.A.

“… Type of data Photographic images; data matrices; univariate, bivariate, and multivariate plots; and tables. How data were acquired For herbivore damage on plant specimens, data capture was done visually with assistance of relevant plant literature for Cretaceous plants [2] , sources for DT determinations [3] , [4] , [5] , and experience of the coauthors. Light microscopy was used for examination and photographic documentation.…”

“…The stoichiometry of the major functional feeding groups – a composite ectophytic feeding, piercing and sucking, mining, and galling – was compared for the three most herbivorized Rose Creek taxa with five modern, well documented taxa. Relevant sources [1] , [2] , [3] , [4] , [5] informed many of these decisions. Data source location Rose Creek locality: South of the city of Fairbury, in Jefferson County, Nebraska, USA.…”

“…Appendices S1–S3 provide ancillary accounts at a global level of plant-organismic associations present during the Early Cretaceous pertaining to the Rose Creek locality. Appendix S4 displays the botanical context of the Rose Creek locality, whereas Appendices S5–S10 discuss the procedures for processing and databasing the Rose Creek plant assemblage, including criteria for establishing plant taxa, distinguishing herbivory from detritivory, rarefaction analyses of the plant specimens and damage types (DTs), and a recent study of arthropod damage on Rose Creek flowers [5] . The rarefaction analyses of plant specimens and damage types versus surface areas ( Appendix S9 ) indicate that sampling is adequate.…”

Florivory and Pollination Intersection: Changes in Floral Trait Expression Do Not Discourage Hummingbird Pollination

“…In addition to the advertisement, florivory might also have effects on floral resources. Although it is not expected that florivores deplete the nectar resource used by hummingbirds, since they often feed on floral tissues other than nectaries and not on nectar itself ( Xiao et al, 2021 ), the injuries caused by florivores could interfere with nectar secretion by altering plant physiological pathways. In fact, by feeding on plant tissues, herbivores can alter jasmonate pathways, which are involved in both plant defense ( Xie et al, 1998 ; Chrétien et al, 2018 ) and nectar secretion ( Radhika et al, 2010 ).…”