The Cretaceous insects: A promising state of the art

A short review of the state of the art of research on insects from the Cretaceous period is given. The recent achievements and priorities for future efforts are indicated. © 2014 Elsevier Ltd. All rights reserved. The Cretaceous, the geologic period from circa 145 to 66 million years (Ma) ago is a complex time period in Earth's history (Gale, 2000; Keller, 2008; Cohen et al., 2013). Generally speaking, the climate of the Cretaceous was much warmer than at present, perhaps the warmest on a worldwide basis than at any other time during the Phanerozoic. However, going into details, the Cretaceous saw episodes of abrupt greenhouse warming and cooling, repeated platform drowning, major excursions in the carbon isotope record, episodic oceanic anoxic events, and increased volcanic activity forming large igneous provinces (Gale, 2000; Keller, 2008). The Cretaceous was a period of changes in vegetation, during which the gymnospermand fern-dominated flora of the Mesophytic were replaced by angiosperm-dominated communities of the Cainophytic (Vakrameev, 1988, 1991; Krassilov, 2003; Friis et al., 2010). All these factors and events, together with changing biotic conditions, availability of new ecological niches influenced strongly the evolution of insects. The insects of the Cretaceous period witnessed the major global change e The Mid Cretaceous Biosphere Re-organization or the Mid Cretaceous Biotic Crisis (Zherikhin, 1978, 1993, 2002; Rasnitsyn, 1988; Krassilov, 2003). The endCretaceous extinction attracts much attention as one of the most dramatic in the history of life. Themid-Cretaceous biological events are somewhat less widely known but no less important. It was of (J. Szwedo), [email protected] ., Nel, A., The Cretaceous inse greater importance in insect history than the Mesozoic/Cenozoic boundary with its famous dinosaur extinction event. The state of the art on Cretaceous insects changed during last 110 years. Only 11 pages were concerned by the Cretaceous insects among the 1430 pages of the considerable compendium of Handlirsch (1906e1908). At that time the Cretaceous insect faunas were extremely badly known, for the main reason that only the Western European and North American fossil insects were investigated, areas thatwere in great part under the seas at that time.More recently, Hennig (1981: 79) indicated that ‘One of the most regrettable gaps in our knowledge of insect phylogeny is the almost complete absence of fossils from the Cretaceous.’ Fortunately the situation has greatly improved during the 34 last years with the discoveries of numerous Cretaceous insect Konservat-Lagerst€ atten. The studies on theEarlyCretaceous compression faunas fromformer Soviet Union, Montsec and Las Hoyas (Spain), Crato Formation (Brazil), Liaoning Province (China), Koonwarra Fossil Bed in Queensland (Australia) gave a crucial increase of information in the years 1980e2000. During the years 1990e2014, very rich new outcrops with amber inclusions were discovered and/or studied in Spain, France, Myanmar, USA (New Jersey amber), Siberia, and overall in Lebanon. These studies resulted into complementary sets of information because, as a general rule amber entomofaunas concern small animals (minute flies, wasps, beetles, etc.) while compression fossils are larger animals (Odonata, large Neuroptera, Orthoptera, etc.). The important difficulty related to the relatively poor quality of the Cretaceous resins, opaque or darkened by gas bubbles, is now partly solved by the new use of X-ray computer microtomography. If this technique remains expensive and of delicate use, considerable progressesweremade in the lastfive years, as cts: A promising state of the art, Cretaceous Research (2014), http:// J. Szwedo, A. Nel / Cretaceous Research xxx (2014) 1e3 2 it is now possible to make virtual dissections of insects and to observe thewings of the insects embedded in opaque amber pieces. The resulting current image is the existence of extremely complex and diverse Lower Cretaceous entomofaunas, characterized by their ‘modernity’ and by very widespread and frequent families (the Neuroptera Allopteridae, the Odonata Aeschnidiidae or Stenophlebioptera), present in what are now the South America, Spain, England, France, and China. The oldest records of the majority of the modern insect families, known in the Palaeogene only before 1981, are now Cretaceous. It is especially the case for the eusocial insects (termites, ants, social wasps and bees). These animals were unknown or known by only one or two Mesozoic fossils 30 years ago, while dozens of genera and species of these groups described now. The oldest records of these eusocial insects concern the termites, well represented in the earliest Early Cretaceous, while the oldest eusocial Hymenoptera are latest Early Cretaceous, in AlbianeCenomanian amber outcrops. No ant is known in the Lower Cretaceous Lebanese amber for instance. After the emergence and first important diversification of the modern eusocial insects, the second crucial change that occurred in the Cretaceous entomofaunas is the major turnover around the boundary between the Early and the Late Cretaceous (AlbianeCenomanianeTuronian) characterized by the extinction during the Cenomanian of many families that appeared in the Jurassic (the most emblematic being the Aeschnidiidae, a very diverse dragonfly family distributed all over the world in the Lower Cretaceous, but whose most recent representative is Cenomanian), and by the diversification and/or oldest records of many modern clades (bees, ants, libellulid dragonflies, Strepsiptera, etc.). It is currently considered that the turnover (replacement of a gymnosperm-dominated flora by an angiosperm-dominated one) that affected the terrestrial plants between the end of the Early Cretaceous and the beginning of the Late Cretaceous was the crucial event that caused these changes in the entomofaunas all over the world. It is particularly well visible among plant-sucking insects e whiteflies, coccids, aphids, planthoppers and leafhoppers (von Dohlen & Moran, 2000; Koteja, 2001; Szwedo, 2008; Huang X.-L. et al., 2012; Hodgson & Hardy, 2013; Drohojowska & Szwedo, 2014). Interestingly this turnover seems to have occurred earlier (during the Barremian) for the freshwater than for the strictly terrestrial palaeoenvironments (Sinitshenkova, 2002; Zherikhin, 2002). The currently proposed scenario for the replacements among the aquatic insects is linked to a phenomenon of eutrophisation of the lake waters due to the increasing quantity of vegetal organicmatter, but it seems that, at least, the changes were not very rapid as many ‘ancient’ clades were still present during the Cenomanian. The changes among the strictly terrestrial insects are easier to explain at least for the taxa directly linked to plants (phytophagous, pollinators), even if a crucial question remains concerning the potential co-evolutions between angiosperms and insects. It remains that all the recent progresses in the knowledge on the Cretaceous insects go in the same general direction: more andmore modern clades are recorded in the Cretaceous, significant diversifications affected these first representatives (it is especially clear for the ants and the termites), and major extinctions affected numerous taxa during the Cretaceous. The CretaceouseCenozoic crisis is supposed to have greatly affected all the terrestrial ecosystems, with catastrophic scenarios proposed (generalized ‘nuclear-like’winter, generalized fires, acidification of the soils and the air, etc.). These scenarios do not take into account the complex ecological interactions between insects and terrestrial plants and between insects themselves, which were certainly comparable to those in the modern biotas because of the presence of nearly all the modern morpho-functional types in the Late Cretaceous. Some Please cite this article in press as: Szwedo, J., Nel, A., The Cretaceous inse dx.doi.org/10.1016/j.cretres.2014.07.008 impacts of the crisis on the planteinsects interactions have been detected at the CretaceouseCenozoic boundary, mainly through the study of the traces of insect activities on plant remains, but there is no clear trace of an extinction of a major insect clade (family rank) that can be related to this event. This phenomenon is maybe due to the fact that, in general, an insect family contains hundreds (even thousands) of species having more or less different biologies, with some ‘generalists’ that are potentially less subject to extinction than the specialized forms. On the contrary, some extinction affected the insects few million years after the KePg (CretaceousePalaeogene) crisis. For instance a Cretaceous lineage of Neuroptera: Chrysopoidea was still present at the end of the Palaeocene, the Mesozoic clade of damseledragonfly Sieblosiidae was still present the Miocene. The problem of the impact of the KePg crisis on the insects is a major challenge of the history of Earth, as the insects are (andwere) one of the most diverse clade among the terrestrial organisms. A major difficulty to solve this question is the nearly complete absence of major insect Konservat-Lagerst€ atten for the CampanianeMaastrichtian, and the relatively few insect outcrops in the TuronianeSantonian compared to the Lower Cretaceous to Cenomanian, so that it is not possible to correctly estimate the insect diversity in the latest Cretaceous. This point will be the greatest challenge in our knowledge of the Cretaceous insects. Cretaceous insects are still underinvestigated regarding their taxonomic diversity, morphological disparity, and numerous other questions on their phylogenetic relationships, ecology and bionomics, habitats, relationships with environment, other insects, host plants, animal hosts, palaeobiogeographical distribution, etc. are still not sufficiently known. However, the contributions in this volume give new insights into some of these subjects. The newly described or revised taxa of various insects e dragonflies (Zheng et al., 2014); earwigs (Yang et al., 2014), psocids (Azar et al., 2014), hemipteranbugs (Chenet al., 2014;DrohojowskaandSzwedo, 2014; Homan et al., 2014; Szwedo and Ansorge, 2014; _ Zyła andWegierek, 2014); fleas (Huang D.-Y., 2014); lacewings (Makarkin, 2014; Shi et al., 2014a, b), snakeflies (Makarkin and Khramov, 2014); beetles (Cai and Huang, 2014; Cai et al., 2014; Liu et al., 2014; Jarzembowski et al., 2014; Kirejtshuk et al., 2014; Peris et al., 2014; Yu et al., 2014a, b), scorpion-flies (Krzemi nski et al., 2014b), flies (Azar and Salam e, 2014; Azar et al., 2014; Kania et al., 2014a, b; Krzemi nski et al., 2014a; Lukashevich and Przhiboro, 2014; Szadziewski et al., 2014), hymenopterans (Kopylov and Zhang, 2014; Perrichot, 2014; Wang et al., 2014; Zhang et al., 2014) are presented not only in their taxonomic context, but also with evolutionary and biogeographical aspects. Also the questions of taphonomy of fossils insects in the Cretaceous deposits (Barling et al., 2014), and presence of microorganisms inside the inclusions in fossilized resins (Poinar, 2014) are introduced in this volume. The papers presented above added some answers to numerous questions on the evolutionary traits of the insects during the Cretaceous. The data presented and their interpretations allowed a better understanding of the insects from this crucial period. However, newquestions are raised and the areas for future investigations necessary to resolve twisted traits of insect evolution are indicated.