Sampling bias and the robustness of ecological metrics for plant-damage-type association networks.

Plants and their insect herbivores have been a dominant component of the terrestrial ecological landscape for the past 410 million years and feature intricate evolutionary patterns and co-dependencies. A complex systems perspective allows for both detailed resolution of these evolutionary relationships as well as comparison and synthesis across systems. Using proxy data of insect herbivore damage (denoted by the damage type or DT) preserved on fossil leaves, functional bipartite network representations provide insights into how plant-insect associations depend on geological time, paleogeographical space, and environmental variables such as temperature and precipitation. However, the metrics measured from such networks are prone to sampling bias. Such sensitivity is of special concern for plant-DT association networks in paleontological settings where sampling effort is often severely limited. Here, we explore the sensitivity of functional bipartite network metrics to sampling intensity and identify sampling thresholds above which metrics appear robust to sampling effort. Across a broad range of sampling efforts, we find network metrics to be less affected by sampling bias and/or sample size than richness metrics, which are routinely used in studies of fossil plant-DT interactions. These results provide reassurance that cross-comparisons of plant-DT networks offer insights into network structure and function and support their widespread use in paleoecology. Moreover, these findings suggest novel opportunities for using plant-DT networks in neontological terrestrial ecology to understand functional aspects of insect herbivory across geological time, environmental perturbations, and geographic space.

Correction: Insect herbivory on Catula gettyi gen. et sp. nov. (Lauraceae) from the Kaiparowits Formation (Late Cretaceous, Utah, USA).

[This corrects the article DOI: 10.1371/journal.pone.0261397.].

Insect herbivory on Catula gettyi gen. et sp. nov. (Lauraceae) from the Kaiparowits Formation (Late Cretaceous, Utah, USA).

The Upper Cretaceous (Campanian Stage) Kaiparowits Formation of southern Utah, USA, preserves abundant plant, invertebrate, and vertebrate fossil taxa. Taken together, these fossils indicate that the ecosystems preserved in the Kaiparowits Formation were characterized by high biodiversity. Hundreds of vertebrate and invertebrate species and over 80 plant morphotypes are recognized from the formation, but insects and their associations with plants are largely undocumented. Here, we describe a new fossil leaf taxon, Catula gettyi gen et. sp. nov. in the family Lauraceae from the Kaiparowits Formation. Catula gettyi occurs at numerous localities in this deposit that represent ponded and distal floodplain environments. The type locality for C. gettyi has yielded 1,564 fossil leaf specimens of this species, which provides the opportunity to circumscribe this new plant species. By erecting this new genus and species, we are able to describe ecological associations on C. gettyi and place these interactions within a taxonomic context. We describe an extensive archive of feeding damage on C. gettyi caused by herbivorous insects, including more than 800 occurrences of insect damage belonging to five functional feeding groups indicating that insect-mediated damage on this taxon is both rich and abundant. Catula gettyi is one of the best-sampled host plant taxa from the Mesozoic Era, a poorly sampled time interval, and its insect damage is comparable to other Lauraceae taxa from the younger Late Cretaceous Hell Creek Flora of North Dakota, USA.

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 (c. 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.

Late Cretaceous domatia reveal the antiquity of plant-mite mutualisms in flowering plants.

Mite houses, or acarodomatia, are found on the leaves of over 2000 living species of flowering plants today. These structures facilitate tri-trophic interactions between the host plant, its fungi or herbivore adversaries, and fungivorous or predaceous mites by providing shelter for the mite consumers. Previously, the oldest acarodomatia were described on a Cenozoic Era fossil leaf dating to 49 Myr in age. Here, we report the first occurrence of Mesozoic Era acarodomatia in the fossil record from leaves discovered in the Upper Cretaceous Kaiparowits Formation (76.6-74.5 Ma) in southern UT, USA. This discovery extends the origin of acarodomatia by greater than 25 Myr, and the antiquity of this plant-mite mutualism provides important constraints for the evolutionary history of acarodomatia on angiosperms.

The importance of sampling standardization for comparisons of insect herbivory in deep time: a case study from the late Palaeozoic.

Sampling standardization has not been fully addressed for the study of insect herbivory in the fossil record. The effects of sampling within a single locality were explored almost a decade ago, but the importance of sampling standardization for comparisons of herbivory across space and time has not yet been evaluated. Here, we present a case study from the Permian in which we evaluate the impact of sampling standardization on comparisons of insect herbivory from two localities that are similar in age and floral composition. Comparisons of insect damage type (DT) diversity change dramatically when the number of leaves examined is standardized by surface area. This finding suggests that surface area should always be taken into account for comparisons of DT diversity. In addition, the three most common metrics of herbivory-DT diversity, proportion of leaves herbivorized and proportion of leaf surface area herbivorized-are inherently decoupled from each other. The decoupling of the diversity and intensity of insect herbivory necessitates a reinterpretation of published data because they had been conflated in previous studies. Future studies should examine the divergent ecological factors that underlie these metrics. We conclude with suggestions to guide the sampling and analysis of herbivorized leaves in the fossil record.