Symbiosis between Cretaceous dinosaurs and feather-feeding beetles.

Extant terrestrial vertebrates, including birds, have a panoply of symbiotic relationships with many insects and arachnids, such as parasitism or mutualism. Yet, identifying arthropod-vertebrate symbioses in the fossil record has been based largely on indirect evidence; findings of direct association between arthropod guests and dinosaur host remains are exceedingly scarce. Here, we present direct and indirect evidence demonstrating that beetle larvae fed on feathers from an undetermined theropod host (avian or nonavian) 105 million y ago. An exceptional amber assemblage is reported of larval molts (exuviae) intimately associated with plumulaceous feather and other remains, as well as three additional amber pieces preserving isolated conspecific exuviae. Samples were found in the roughly coeval Spanish amber deposits of El Soplao, San Just, and Peñacerrada I. Integration of the morphological, systematic, and taphonomic data shows that the beetle larval exuviae, belonging to three developmental stages, are most consistent with skin/hide beetles (family Dermestidae), an ecologically important group with extant keratophagous species that commonly inhabit bird and mammal nests. These findings show that a symbiotic relationship involving keratophagy comparable to that of beetles and birds in current ecosystems existed between their Early Cretaceous relatives.

Arthropods in modern resins reveal if amber accurately recorded forest arthropod communities.

Amber is an organic multicompound derivative from the polymerization of resin of diverse higher plants. Compared with other modes of fossil preservation, amber records the anatomy of and ecological interactions between ancient soft-bodied organisms with exceptional fidelity. However, it is currently suggested that ambers do not accurately record the composition of arthropod forest paleocommunities, due to crucial taphonomic biases. We evaluated the effects of taphonomic processes on arthropod entrapment by resin from the plant Hymenaea, one of the most important resin-producing trees and a producer of tropical Cenozoic ambers and Anthropocene (or subfossil) resins. We statistically compared natural entrapment by Hymenaea verrucosa tree resin with the ensemble of arthropods trapped by standardized entomological traps around the same tree species. Our results demonstrate that assemblages in resin are more similar to those from sticky traps than from malaise traps, providing an accurate representation of the arthropod fauna living in or near the resiniferous tree, but not of entire arthropod forest communities. Particularly, arthropod groups such as Lepidoptera, Collembola, and some Diptera are underrepresented in resins. However, resin assemblages differed slightly from sticky traps, perhaps because chemical compounds in the resins attract or repel specific insect groups. Ground-dwelling or flying arthropods that use the tree-trunk habitat for feeding or reproduction are also well represented in the resin assemblages, implying that fossil inclusions in amber can reveal fundamental information about biology of the past. These biases have implications for the paleoecological interpretation of the fossil record, principally of Cenozoic amber with angiosperm origin.

First record of Jacobsoniidae (Coleoptera) on the African continent in Holocene copal from Tanzania: biogeography since the Cretaceous.

Neither fossil nor living Jacobsoniidae are found in abundance. Derolathrus cavernicolus Peck, 2010 is recorded here preserved in Holocene copal from Tanzania with an age of 210 ± 30 BP years. This leads us to three interesting conclusions: (1) This is the first time the family was found on the African continent, extending the family's distribution range to hitherto unknown localities. Derolathrus cavernicolus in Holocene copal from Tanzania expands the known distribution of the species, previously only recorded in the USA (Hawaii and Florida), Barbados, and Japan, both spatially and temporally. (2) All fossil specimens of the family have been found preserved in amber, which might be due to the small size of the specimens that prevents their discovery in other types of deposits. However, we here add a second aspect, namely the occurrence of this cryptic and currently scarce family of beetles in resinous environments, where they live in relationship with resin-producing trees. (3) The discovery of a new specimen from a family unknown on the African continent supports the relevance of these younger resins in preserving arthropods that lived in pre-Anthropocene times. Although we cannot demonstrate their extinction in the region, since it is possible that the family still survives in the already fragmented coastal forests of East Africa, we are detecting a loss of local biodiversity during the so-called Anthropocene, probably due to human activity.

A new genus of dance fly (Diptera: Empidoidea: Hybotidae) from Cretaceous Spanish ambers and introduction to the fossiliferous amber outcrop of La Hoya (Castellón Province, Spain).

Hybotidae fly species, also known as dance flies, in Cretaceous ambers have been described from Lebanon, France, Myanmar, Russia, and Canada. Here we describe Grimaldipeza coelica gen. et sp. n., and recognize another two un-named species, in Spanish amber from the middle Albian El Soplao and lower Cenomanian La Hoya outcrops. The fore tibial gland is present in the new genus, which is characteristic of the family Hybotidae. We compare Grimaldipeza coelica gen. et sp. n. with the holotypes of Trichinites cretaceus Hennig, 1970 and Ecommocydromia difficilis Schlüter, 1978, and clarify some morphological details present in the latter two species. Further taxonomic placement beyond family of the here described new genus was not possible and remains incertae sedis within Hybotidae until extant subfamilies are better defined. We provide new paleoecological data of the hybotids, together with paleogeographical and life paleoenvironmental notes. A table with the known Cretaceous Hybotidae is provided. Furthermore, the La Hoya amber-bearing outcrop is described in detail, filling the information gap for this deposit.

Necrophagy by insects in Oculudentavis and other lizard body fossils preserved in Cretaceous amber.

When a vertebrate carcass begins its decay in terrestrial environments, a succession of different necrophagous arthropod species, mainly insects, are attracted. Trophic aspects of the Mesozoic environments are of great comparative interest, to understand similarities and differences with extant counterparts. Here, we comprehensively study several exceptional Cretaceous amber pieces, in order to determine the early necrophagy by insects (flies in our case) on lizard specimens, ca. 99 Ma old. To obtain well-supported palaeoecological data from our amber assemblages, special attention has been paid in the analysis of the taphonomy, succession (stratigraphy), and content of the different amber layers, originally resin flows. In this respect, we revisited the concept of syninclusion, establishing two categories to make the palaeoecological inferences more accurate: eusyninclusions and parasyninclusions. We observe that resin acted as a "necrophagous trap". The lack of dipteran larvae and the presence of phorid flies indicates decay was in an early stage when the process was recorded. Similar patterns to those in our Cretaceous cases have been observed in Miocene ambers and actualistic experiments using sticky traps, which also act as "necrophagous traps"; for example, we observed that flies were indicative of the early necrophagous stage, but also ants. In contrast, the absence of ants in our Late Cretaceous cases confirms the rareness of ants during the Cretaceous and suggests that early ants lacked this trophic strategy, possibly related to their sociability and recruitment foraging strategies, which developed later in the dimensions we know them today. This situation potentially made necrophagy by insects less efficient in the Mesozoic.

The mid-Miocene Zhangpu biota reveals an outstandingly rich rainforest biome in East Asia.

During the Mid-Miocene Climatic Optimum [MMCO, ~14 to 17 million years (Ma) ago], global temperatures were similar to predicted temperatures for the coming century. Limited megathermal paleoclimatic and fossil data are known from this period, despite its potential as an analog for future climate conditions. Here, we report a rich middle Miocene rainforest biome, the Zhangpu biota (~14.7 Ma ago), based on material preserved in amber and associated sedimentary rocks from southeastern China. The record shows that the mid-Miocene rainforest reached at least 24.2°N and was more widespread than previously estimated. Our results not only highlight the role of tropical rainforests acting as evolutionary museums for biodiversity at the generic level but also suggest that the MMCO probably strongly shaped the East Asian biota via the northern expansion of the megathermal rainforest biome. The Zhangpu biota provides an ideal snapshot for biodiversity redistribution during global warming.

Unravelling the mystery of "Madagascar copal": Age, origin and preservation of a Recent resin.

The loss of biodiversity during the Anthropocene is a constant topic of discussion, especially in the top biodiversity hotspots, such as Madagascar. In this regard, the study of preserved organisms through time, like those included in "Madagascar copal", is of relevance. "Madagascar copal" originated from the leguminous tree Hymenaea verrucosa, which produced and produces resin abundantly. In the last 20 years, interest has focused on the scientific study of its biological inclusions, mainly arthropods, described in dozens of publications. The age and origin of the deposits of "Madagascar copal" have not yet been resolved. Our objectives are to determine its age and geographical origin, and thus increase its scientific value as a source of biological/palaeobiological information. Although Hymenaea was established in Madagascar during the Miocene, we did not find geological deposits of copal or amber in the island. It is plausible that the evolution of those deposits was negatively conditioned by the type of soil, by the climate, and by the development of soil/litter microorganisms, which inhibit preservation of the resin pieces in the litter and subsoil over 300 years. Our results indicate that "Madagascar copal" is a Recent resin, up to a few hundred years old, that originated from Hymenaea trees growing in the lowland coastal forests, one of the most endangered ecosystems in the world. The included and preserved biota is representative of that ecosystem today and during historical times. Inclusions in this Recent resin do not have the palaeontological significance that has been mistakenly attributed to them, but they do have relevant implications for studies regarding Anthropocene biodiversity loss in this hottest hotspot.

Cretaceous amniote integuments recorded through a taphonomic process unique to resins.

Fossil records of vertebrate integuments are relatively common in both rocks, as compressions, and amber, as inclusions. The integument remains, mainly the Mesozoic ones, are of great interest due to the panoply of palaeobiological information they can provide. We describe two Spanish Cretaceous amber pieces that are of taphonomic importance, one bearing avian dinosaur feather remains and the other, mammalian hair. The preserved feather remains originated from an avian dinosaur resting in contact with a stalactite-shaped resin emission for the time it took for the fresh resin to harden. The second piece shows three hair strands recorded on a surface of desiccation, with the characteristic scale pattern exceptionally well preserved and the strands aligned together, which can be considered the record of a tuft. These assemblages were recorded through a rare biostratinomic process we call "pull off vestiture" that is different from the typical resin entrapment and embedding of organisms and biological remains, and unique to resins. The peculiarity of this process is supported by actualistic observations using sticky traps in Madagascar. Lastly, we reinterpret some exceptional records from the literature in the light of that process, thus bringing new insight to the taphonomic and palaeoecological understanding of the circumstances of their origins.

A revised definition for copal and its significance for palaeontological and Anthropocene biodiversity-loss studies.

The early fossilization steps of natural resins and associated terminology are a subject of constant debate. Copal and resin are archives of palaeontological and historical information, and their study is critical to the discovery of new and/or recently extinct species and to trace changes in forests during the Holocene. For such studies, a clear, suitable definition for copal is vital and is herein established. We propose an age range for copal (2.58 Ma-1760 AD), including Pleistocene and Holocene copals, and the novel term "Defaunation resin", defined as resin produced after the commencement of the Industrial Revolution. Defaunation resin is differentiated from Holocene copal as it was produced during a period of intense human transformative activities. Additionally, the "Latest Amber Bioinclusions Gap" (LABG) since the late Miocene to the end of the Pleistocene is hereby newly defined, and is characterized by its virtual absence of bioinclusions and the consequent lack of palaeontological information, which in part explains the historical differentiation between amber and copal. Crucial time intervals in the study of resin production, and of the biodiversity that could be contained, are now clarified, providing a framework for and focusing future research on bioinclusions preserved in copal and resin.

DNA from resin-embedded organisms: Past, present and future.

Past claims have been made for fossil DNA recovery from various organisms (bacteria, plants, insects and mammals, including humans) dating back in time from thousands to several million years BP. However, many of these recoveries, especially those described from million-year-old amber (fossil resin), have faced criticism as being the result of modern environmental contamination and for lack of reproducibility. Using modern genomic techniques, DNA can be obtained with confidence from a variety of substrates (e.g. bones, teeth, gum, museum specimens and fossil insects) of different ages, albeit always less than one million years BP, and results can also be obtained from much older materials using palaeoproteomics. Nevertheless, new attempts to determine if ancient DNA (aDNA) is present in insects preserved in 40 000-year old sub-fossilised resin, the precursor of amber, have been unsuccessful or not well documented. Resin-embedded specimens are therefore regarded as unsuitable for genetic studies. However, we demonstrate here, for the first time, that although a labile molecule, DNA is still present in platypodine beetles (Coleoptera: Curculionidae) embedded in six-year-old and two-year-old resin pieces from Hymenaea verrucosa (Angiospermae: Fabaceae) collected in Madagascar. We describe an optimised method which meets all the requirements and precautions for aDNA experiments for our purpose: to explore the DNA preservation limits in resin. Our objective is far from starting an uncontrolled search for aDNA in amber as it was in the past, but to start resolving basic aspects from the DNA preservation in resin and search from the most modern samples to the ancient ones, step by step. We conclude that it is therefore possible to study genomics from resin-embedded organisms, although the time limits remain to be determined.

Ancient amino acids from fossil feathers in amber.

Ancient protein analysis is a rapidly developing field of research. Proteins ranging in age from the Quaternary to Jurassic are being used to answer questions about phylogeny, evolution, and extinction. However, these analyses are sometimes contentious, and focus primarily on large vertebrates in sedimentary fossilisation environments; there are few studies of protein preservation in fossils in amber. Here we show exceptionally slow racemisation rates during thermal degradation experiments of resin enclosed feathers, relative to previous thermal degradation experiments of ostrich eggshell, coral skeleton, and limpet shell. We also recover amino acids from two specimens of fossil feathers in amber. The amino acid compositions are broadly similar to those of degraded feathers, but concentrations are very low, suggesting that much of the original protein has been degraded and lost. High levels of racemisation in more apolar, slowly racemising amino acids suggest that some of the amino acids were ancient and therefore original. Our findings indicate that the unique fossilisation environment inside amber shows potential for the recovery of ancient amino acids and proteins.

The semi-aquatic pondweed bugs of a Cretaceous swamp.

Pondweed bugs (Hemiptera: Mesoveliidae), considered a sister group to all other Gerromorpha, are exceedingly rare as fossils. Therefore, each new discovery of a fossil mesoveliid is of high interest, giving new insight into their early evolutionary history and diversity and enabling the testing of their proposed relationships. Here, we report the discovery of new mesoveliid material from Spanish Lower Cretaceous (Albian) amber, which is the first such find in Spanish amber. To date, fossil records of this family only include one species from French Kimmeridgian as compression fossils, two species in French amber (Albian-Cenomanian boundary), and one in Dominican amber (Miocene). The discovery of two males and one female described and figured as Glaesivelia pulcherrima Sánchez-García & Solórzano Kraemer gen. et sp. n., and a single female described and figured as Iberovelia quisquilia Sánchez-García & Nel, gen. et sp. n., reveals novel combinations of traits related to some genera currently in the subfamily Mesoveliinae. Brief comments about challenges facing the study of fossil mesoveliids are provided, showing the necessity for a revision of the existing phylogenetic hypotheses. Some of the specimens were studied using infrared microscopy, a promising alternative to the systematic study of organisms preserved in amber that cannot be clearly visualised. The new taxa significantly expand the fossil record of the family and shed new light on its palaeoecology. The fossils indicate that Mesoveliidae were certainly diverse by the Cretaceous and that numerous tiny cryptic species living in humid terrestrial to marginal aquatic habitats remain to be discovered. Furthermore, the finding of several specimens as syninclusions suggests aggregative behaviour, thereby representing the earliest documented evidence of such ethology.

Datziinae as a new subfamily name for the unavailable name Protopsychodinae Stebner et al., 2015, (Diptera: Psychodidae).

In a recent paper a new subfamily of Psychodidae was inadequately named Protopsychodinae. This nomenclatural act cannot be considered as a valid name under ICZN regulations because the subfamily name is not based on the type genus Datzia Stebner et al., 2015, and furthermore the fossil genus Protopsychoda Azar et al., 1999 was originally described under the subfamily Psychodinae. Therefore, the new family-group name Datziinae is herein proposed.

Moth flies and sand flies (Diptera: Psychodidae) in Cretaceous Burmese amber.

One new subfamily, four new genera and 10 new species of Psychodidae are described from Burmese amber which significantly increases our knowledge about this group in the Cretaceous. Protopsychodinae n. subfam. probably represents the oldest known ancestor of modern Psychodinae and includes three species within two genera: Datzia setosa gen. et sp. n., Datzia bispina gen. et sp. n., and Mandalayia beumersorum gen. et sp. n. Sycoracinae and Phlebotominae are represented by two genera each in the studied material, Palaeoparasycorax globosus gen. et sp. n., Palaeoparasycorax suppus gen. et sp. n., Parasycorax simplex sp. n., and Phlebotomites aphoe sp. n. and Phlebotomus vetus sp. n., respectively. Bruchomyiinae is represented by Nemopalpus quadrispiculatus sp. n. Furthermore, one genus of an incertae sedis subfamily, Bamara groehni gen. et sp. n., is described. The systematic positions of the new taxa are discussed.

Entrapment bias of arthropods in Miocene amber revealed by trapping experiments in a tropical forest in Chiapas, Mexico.

All entomological traps have a capturing bias, and amber, viewed as a trap, is no exception. Thus the fauna trapped in amber does not represent the total existing fauna of the former amber forest, rather the fauna living in and around the resin producing tree. In this paper we compare arthropods from a forest very similar to the reconstruction of the Miocene Mexican amber forest, and determine the bias of different trapping methods, including amber. We also show, using cluster analyses, measurements of the trapped arthropods, and guild distribution, that the amber trap is a complex entomological trap not comparable with a single artificial trap. At the order level, the most similar trap to amber is the sticky trap. However, in the case of Diptera, at the family level, the Malaise trap is also very similar to amber. Amber captured a higher diversity of arthropods than each of the artificial traps, based on our study of Mexican amber from the Middle Miocene, a time of climate optimum, where temperature and humidity were probably higher than in modern Central America. We conclude that the size bias is qualitatively independent of the kind of trap for non-extreme values. We suggest that frequent specimens in amber were not necessarily the most frequent arthropods in the former amber forest. Selected taxa with higher numbers of specimens appear in amber because of their ecology and behavior, usually closely related with a tree-inhabiting life. Finally, changes of diversity from the Middle Miocene to Recent time in Central and South America can be analyzed by comparing the rich amber faunas from Mexico and the Dominican Republic with the fauna trapped using sticky and Malaise traps in Central America.