Conrad C. Labandeira

Impact of the terminal Cretaceous event on plant-insect associations.

Evidence for a major extinction of insect herbivores is provided by presence–absence data for 51 plant–insect associations on 13,441 fossil plant specimens, spanning the Cretaceous/Paleogene boundary in southwestern North Dakota. The most specialized associations, which were diverse and abundant during the latest Cretaceous, almost disappeared at the boundary and failed to recover in younger strata even while generalized associations regained their Cretaceous abundances. These results are consistent with a sudden ecological perturbation that precipitated a diversity bottleneck for insects and plants.

A Probable Pollination Mode Before Angiosperms: Eurasian, Long-Proboscid Scorpionflies

Long-Lost Pollinators The rise of angiosperms in the Early Cretaceous (∼140 million years ago) was accompanied by coevolution of a variety of insects, including flies, bees, and wasps required for pollination. Ren et al. (p. 840; see the Perspective by Ollerton and Coulthard) show that three families of scorpionflies had already evolved specialized mouth parts for feeding on the nectar of gymnosperms, as early as the Middle Jurassic (∼170 million years ago). The diversity and specialization of these insects and related plant structures suggests that they were also involved in pollination. These families died out later in the Cretaceous as angiosperms began to dominate. Prior to the coevolution of angiosperms and pollinating insects, scorpionflies may have been pollinating gymnosperms. The head and mouthpart structures of 11 species of Eurasian scorpionflies represent three extinct and closely related families during a 62-million-year interval from the late Middle Jurassic to the late Early Cretaceous. These taxa had elongate, siphonate (tubular) proboscides and fed on ovular secretions of extinct gymnosperms. Five potential ovulate host-plant taxa co-occur with these insects: a seed fern, conifer, ginkgoopsid, pentoxylalean, and gnetalean. The presence of scorpionfly taxa suggests that siphonate proboscides fed on gymnosperm pollination drops and likely engaged in pollination mutualisms with gymnosperms during the mid-Mesozoic, long before the similar and independent coevolution of nectar-feeding flies, moths, and beetles on angiosperms. All three scorpionfly families became extinct during the later Early Cretaceous, coincident with global gymnosperm-to-angiosperm turnover.

Sharply increased insect herbivory during the Paleocene–Eocene Thermal Maximum

The Paleocene–Eocene Thermal Maximum (PETM, 55.8 Ma), an abrupt global warming event linked to a transient increase in pCO2, was comparable in rate and magnitude to modern anthropogenic climate change. Here we use plant fossils from the Bighorn Basin of Wyoming to document the combined effects of temperature and pCO2 on insect herbivory. We examined 5,062 fossil leaves from five sites positioned before, during, and after the PETM (59–55.2 Ma). The amount and diversity of insect damage on angiosperm leaves, as well as the relative abundance of specialized damage, correlate with rising and falling temperature. All reach distinct maxima during the PETM, and every PETM plant species is extensively damaged and colonized by specialized herbivores. Our study suggests that increased insect herbivory is likely to be a net long-term effect of anthropogenic pCO2 increase and warming temperatures.

New data from the Middle Jurassic of China shed light on the phylogeny and origin of the proboscis in the Mesopsychidae (Insecta: Mecoptera)

BackgroundThe Mesopsychidae is an extinct family of Mecoptera, comprising eleven described genera from Upper Permian to Lower Cretaceous deposits. In 2009, several well-preserved mesopsychids with long proboscides were reported from the mid Mesozoic of Northeastern China, suggesting the presence of pollination mutualisms with gymnosperm plants and highlighting their elevated genus-level diversity. Since that time, additional mesopsychid taxa have been described. However, the phylogeny of genera within Mesopsychidae has not been studied formally, attributable to the limited number of well-preserved fossils.ResultsHere, we describe two new species, Lichnomesopsyche prochorista sp. nov. and Vitimopsyche pristina sp. nov. and revise the diagnosis of Lichnomesopsyche daohugouensis Ren, Labandeira and Shih, 2010, based on ten specimens from the latest Middle Jurassic Jiulongshan Formation of Inner Mongolia, China. After compiling data from these new fossil species and previously reported representative taxa, we conducted phylogenetic analyses and geometric morphometric studies that now shed light on the taxonomy and phylogeny of Mesopsychidae. We also evaluate the recurring origin of the siphonate proboscis in the Mecoptera and propose an evolutionary developmental model for its multiple origins.ConclusionsPhylogenetic and geometric morphometric results confirm the establishment of two new species, each to Lichnomesopsyche and Vitimopsyche. Vitimopsyche pristina sp. nov. extends the existence of the genus Vitimopsyche Novokshonov and Sukacheva, 2001, from the mid Lower Cretaceous to the latest Middle Jurassic. Two methods of analyses indicate an affiliation of Mesopsyche dobrokhotovae Novokshonov, 1997 with Permopsyche Bashkuev, 2011. A phylogenetic analysis of the Mesopsychidae supports: 1), Mesopsychidae as a monophyletic group; 2), Mesopsyche as a paraphyletic group, to be revised pending future examination of additional material; and 3), the independent origin of the proboscis in the Pseudopolycentropodidae, its subsequent loss in earliest Mesopsychidae such as Epicharmesopsyche, its re-origination in the common ancestor (or perhaps independently) in the Vitimopsyche and Lichnomesopsyche clades of the Mesopsychidae. The third conclusion indicates that the proboscis originated four or five times within early Mecoptera, whose origin is explained by an evolutionary developmental model.

The four phases of plant-arthropod associations in deep time

Vascular-plant hosts, their arthropod herbivores, and associated functional feeding groups are distributed spatiotemporally into four major herbivore expansions during the past 420 m.y. They are: (1) a Late Silurian to Late Devonian (60 m.y.) phase of myriapod and apterygote, hexapod (perhaps pterygote) herbivores on several clades of primitive vascular-plant hosts and a prototaxalean fungus; (2) a Late Mississippian to end-Permian (85 m.y.) phase of mites and apterygote and basal pterygote herbivores on pteridophyte and basal gymnospermous plant hosts; (3) a Middle Triassic to Recent (245 m.y.) phase of mites, orthopteroids (in the broadest sense) and hemipteroid and basal holometabolan herbivores on pteridophyte and gymnospermous plant hosts; and (4) a mid Early Cretaceous to Recent (115 m.y.) phase of modern-aspect orthopteroids and derived hemipteroid and holometabolous herbivores on angiospermous plant hosts. These host-plant and herbivore associations are mediated by seven functional feeding groups: a) external foliage feeding, b) piercing-and-sucking, c) boring (Phase 1 origins); d) galling, e) seed predation, f) nonfeeding oviposition (Phase 2 origins); and leaf mining (early Phase 3 origin). Within about 20 m.y. of each herbivore expansion, there is a biota that expresses the nearly full spectrum of later plant-arthropod associations. These four associational phases may be linked to the paleoclimatologic variables of greenhouse/icehouse cycles and atmospheric O2 and CO2 levels by uncertain causes, although some relationship probably is present. The 7 functional feeding groups persist through most of the sampled interval but harbor host-plants and arthropod herbivores that are spatiotemporally ephemeral. Poor understanding of associations in Phases 1 to 3 is attributed to disproportionate focus on the angiosperm and holometabolan insect associations of Phase 4.

Oribatid mites and the decomposition of plant tissues in Paleozoic coal-swamp forests

Although oribatid mites are essential to the decomposition of plant tissues in modern temperate forests by assisting conversion of primary productivity to soil organic matter, little is known of their paleoecologic history. Previously there has been scattered and anecdotal evidence documenting oribatid mite detritivory in Pennsylvanian plant tissues. This study evaluates the incidence of oribatid mite damage for seven major coal-ball deposits from the Illinois and Appalachian sedimentary basins, representing a 17 million year interval from the Euramerican tropics. Although this interval contains the best anatomically preserved plant tissues with oribatid mite borings in the fossil record, coeval oribatid mite body-fossils are absent. By contrast, the known body-fossil record of oribatid mites commences during the Middle Devonian, but does not reappear until the Early Jurassic, at which time mite taxa are modern in aspect. All major plant taxa occurring in Pennsylvanian coal swamps, including lycopsids, sphenopsids, ferns, seed ferns and cordaites, were consumed by oribatid mites. Virtually every type of plant tissue was used by mites, notably indurated tissues such as bark, fibrovascular bundles and especially wood, as well as softer seed megagametophytic and parenchymatic tissues within stems, roots and leaves. Significant evidence also exists for secondary consumption by mites of tissues in macroarthropod coprolites. Our data indicate that oribatid mites consumed dead, aerially-derived plant tissues at ground level, as well as root-penetrated tissues substantially within the peat. Oribatid mites were important arthropod decomposers in Pennsylvanian coal swamps of Euramerica. The wood boring functional-feeding-guild was expanded by insects into above-ground, live trees during the early Mesozoic. New food resources for insect borers resulted from penetration of live tissues such as cambium and phloem, and the invasion of heartwood and other hard tissues mediated by insect-fungus symbioses. Termites and holometabolous insects were prominent contributors to this second wave of wood-boring, exploiting gymnosperms and angiosperms as both detritivores and herbivores. An earlier emplacement of oribatid mites as detritivores of dead plant tissues continued to the present, but without a documented trace-fossil record.

Late Paleocene fossils from the Cerrejón Formation, Colombia, are the earliest record of Neotropical rainforest

Neotropical rainforests have a very poor fossil record, making hypotheses concerning their origins difficult to evaluate. Nevertheless, some of their most important characteristics can be preserved in the fossil record: high plant diversity, dominance by a distinctive combination of angiosperm families, a preponderance of plant species with large, smooth-margined leaves, and evidence for a high diversity of herbivorous insects. Here, we report on an ≈58-my-old flora from the Cerrejón Formation of Colombia (paleolatitude ≈5 °N) that is the earliest megafossil record of Neotropical rainforest. The flora has abundant, diverse palms and legumes and similar family composition to extant Neotropical rainforest. Three-quarters of the leaf types are large and entire-margined, indicating rainfall >2,500 mm/year and mean annual temperature >25 °C. Despite modern family composition and tropical paleoclimate, the diversity of fossil pollen and leaf samples is 60–80% that of comparable samples from extant and Quaternary Neotropical rainforest from similar climates. Insect feeding damage on Cerrejón fossil leaves, representing primary consumers, is abundant, but also of low diversity, and overwhelmingly made by generalist feeders rather than specialized herbivores. Cerrejón megafossils provide strong evidence that the same Neotropical rainforest families have characterized the biome since the Paleocene, maintaining their importance through climatic phases warmer and cooler than present. The low diversity of both plants and herbivorous insects in this Paleocene Neotropical rainforest may reflect an early stage in the diversification of the lineages that inhabit this biome, and/or a long recovery period from the terminal Cretaceous extinction.

Decoupled Plant and Insect Diversity After the End-Cretaceous Extinction

Food web recovery from mass extinction is poorly understood. We analyzed insect-feeding damage on 14,999 angiosperm leaves from 14 latest Cretaceous, Paleocene, and early Eocene sites in the western interior United States. Most Paleocene floras have low richness of plants and of insect damage. However, a low-diversity 64.4-million-year-old flora from southeastern Montana shows extremely high insect damage richness, especially of leaf mining, whereas an anomalously diverse 63.8-million-year-old flora from the Denver Basin shows little damage and virtually no specialized feeding. These findings reveal severely unbalanced food webs 1 to 2 million years after the end-Cretaceous extinction 65.5 million years ago.

Insect herbivory, plant defense, and early Cenozoic climate change

Insect damage on fossil leaves from the Central Rocky Mountains, United States, documents the response of herbivores to changing regional climates and vegetation during the late Paleocene (humid, warm temperate to subtropical, predominantly deciduous), early Eocene (humid subtropical, mixed deciduous and evergreen), and middle Eocene (seasonally dry, subtropical, mixed deciduous and thick-leaved evergreen). During all three time periods, greater herbivory occurred on taxa considered to have short rather than long leaf life spans, consistent with studies in living forests that demonstrate the insect resistance of long-lived, thick leaves. Variance in herbivory frequency and diversity was highest during the middle Eocene, indicating the increased representation of two distinct herbivory syndromes: one for taxa with deciduous, palatable foliage, and the other for hosts with evergreen, thick-textured, small leaves characterized by elevated insect resistance. Leaf galling, which is negatively correlated with moisture today, apparently increased during the middle Eocene, whereas leaf mining decreased.

Confirmation of Romer's Gap as a low oxygen interval constraining the timing of initial arthropod and vertebrate terrestrialization

The first terrestrialization of species that evolved from previously aquatic taxa was a seminal event in evolutionary history. For vertebrates, one of the most important terrestrialized groups, this event was interrupted by a time interval known as Romers Gap, for which, until recently, few fossils were known. Here, we argue that geochronologic range data of terrestrial arthropods show a pattern similar to that of vertebrates. Thus, Romers Gap is real, occupied an interval from 360 million years before present (MYBP) to 345 MYBP, and occurred when environmental conditions were unfavorable for air-breathing, terrestrial animals. These model results suggest that atmospheric oxygen levels were the major driver of successful terrestrialization, and a low-oxygen interval accounts for Romers Gap. Results also show that terrestrialization among members of arthropod and vertebrate clades occurred in two distinct phases. The first phase was a 65-million-year (My) interval from 425 to 360 MYBP, representing an earlier, prolonged event of complete arthropod terrestrialization of smaller-sized forms (425–385 MYBP) and a subsequent, modest, and briefer event of incipient terrestrialization of larger-sized, aquatic vertebrates (385–360 MYBP). The second phase began at 345 MYBP, characterized by numerous new terrestrial species emerging in both major clades. The first and second terrestrialization phases bracket Romers Gap, which represents a depauperate spectrum of major arthropod and vertebrate taxa before a major Late Paleozoic colonization of terrestrial habitats.