Microbial Cretaceous park: biodiversity of microbial fossils entrapped in amber

Microorganisms are the most ancient cells on this planet and they include key phyla for understanding cell evolution and Earth history, but, unfortunately, their microbial records are scarce. Here, we present a critical review of fossilized prokaryotic and eukaryotic microorganisms entrapped in Cretaceous ambers (but not exclusively from this geological period) obtained from deposits worldwide. Microbiota in ambers are rather diverse and include bacteria, fungi, and protists. We comment on the most important microbial records from the last 25 years, although it is not an exhaustive bibliographic compilation. The most frequently reported eukaryotic microfossils are shells of amoebae and protists with a cell wall or a complex cortex. Likewise, diverse dormant stages (palmeloid forms, resting cysts, spores, etc.) are abundant in ambers. Besides, viral and protist pathogens have been identified inside insects entrapped in amber. The situation regarding filamentous bacteria and fungi is quite confusing because in some cases, the same record was identified consecutively as a member of these phylogenetically distant groups. To avoid these identification errors in the future, we propose to apply a more resolute microscopic and analytical method in amber studies. Also, we discuss the most recent findings about ancient DNA repair and bacterial survival in remote substrates, which support the real possibility of ancient DNA amplification and bacterial resuscitation from Cretaceous resins.     

Wasps robbing food from ants: a frequent behavior?

Food robbing, or cleptobiosis, has been well documented throughout the animal kingdom. For insects, intrafamilial food robbing is known among ants, but social wasps (Vespidae; Polistinae) taking food from ants has, to the best of our knowledge, never been reported. In this paper, we present two cases involving social wasps robbing food from ants associated with myrmecophytes. (1) Polybioides tabida F. (Ropalidiini) rob pieces of prey from Tetraponera aethiops Smith (Formicidae; Pseudomyrmecinae) specifically associated with Barteria fistulosa Mast. (Passifloraceae). (2) Charterginus spp. (Epiponini) rob food bodies from myrmecophytic Cecropia (Cecropiaceae) exploited by their Azteca mutualists (Formicidae; Dolichoderinae) or by opportunistic ants (that also attack cleptobiotic wasps). We note here that wasps gather food bodies (1) when ants are not yet active; (2) when ants are active, but avoiding any contact with them by flying off when attacked; and (3) through the coordinated efforts of two to five wasps, wherein one of them prevents the ants from leaving their nest, while the other wasps freely gather the food bodies. We suggest that these interactions are more common than previously thought.     

Mammalian hairs in Early Cretaceous amber

Two mammalian hairs have been found in association with an empty puparium in a ∼100-million-year-old amber (Early Cretaceous) from France. Although hair is known to be an ancestral, ubiquitous feature in the crown Mammalia, the structure of Mesozoic hair has never been described. In contrast to fur and hair of some Jurassic and Cretaceous mammals preserved as carbonized filaments, the exceptional preservation of the fossils described here allows for the study of the cuticular structure. Results show the oldest direct evidence of hair with a modern scale pattern. This discovery implies that the morphology of hair cuticula may have remained unchanged throughout most of mammalian evolution. The association of these hairs with a possible fly puparium provides paleoecological information and indicates peculiar taphonomic conditions.     

Reduced Chitinase Activities in Ant Plants of the Genus Macaranga

Many plant species have evolved mutualistic associations with ants, protecting their host against detrimental influences such as herbivorous insects. Letourneau (1998) reported in the case of Piper that ants defend their plants principally against stem-boring insects and also reduce fungal infections on inflorescences. Macaranga plants that were experimentally deprived of their symbiotic Crematogaster ants suffered heavily from shoot borers and pathogenic fungi (Heil 1998). Here we report that ants seem to reduce fungal infections actively in the obligate myrmecophyte Macaranga triloba (Euphorbiaceae), while ant-free plants can be easily infected. We also found extremely low chitinase activity in Macaranga plants. The plants' own biochemical defense seems to be reduced, and low chitinase activity perhaps may represent a predisposition for the evolution of myrmecophytism. These plants are therefore highly dependent on their ants, which obviously function not only as an antiherbivore defense but also as an effective agent against fungal pathogens. Received: 5 August 1998 / Accepted in revised form: 18 November 1998     

Nest site selection and induced response in a dominant arboreal ant species

It is well known that arboreal ants, both territorially dominant species and plant ants (e.g., species associated with myrmecophytes or plants housing them in hollow structures), protect their host trees from defoliators. Nevertheless, the presence of an induced defense, suggested by the fact that the workers discovering a leaf wound recruit nestmates, is only known for plant ants. Based on the results from a field study, we show here (1) that colonies of Azteca chartifex, a territorially dominant, neotropical arboreal ant species, mostly selected Goupia glabra (Goupiaceae) trees in which to build their principal carton nests and (2) that plant signals induced workers to recruit nestmates, which patrol the leaves, likely providing the plant with a biotic defense. Furthermore, the number of recruited workers was clearly higher on G. glabra, their most frequently selected host tree species, than on other tree species. These results show that contrary to what was previously believed, induced responses are also found in territorially dominant arboreal ants and so are not limited to the specific associations between myrmecophytes and plant ants.     

New fossil ants in French Cretaceous amber (Hymenoptera: Formicidae)

Recent studies on the ant phylogeny are mainly based on the molecular analyses of extant subfamilies and do not include the extinct, only Cretaceous subfamily Sphecomyrminae. However, the latter is of major importance for ant relationships, as it is considered the most basal subfamily. Therefore, each new discovery of a Mesozoic ant is of high interest for improving our understanding of their early history and basal relationships. In this paper, a new sphecomyrmine ant, allied to the Burmese amber genus Haidomyrmex, is described from mid-Cretaceous amber of France as Haidomyrmodes mammuthus gen. and sp. n. The diagnosis of the tribe Haidomyrmecini is emended based on the new type material, which includes a gyne (alate female) and two incomplete workers. The genus Sphecomyrmodes, hitherto known by a single species from Burmese amber, is also reported and a new species described as S. occidentalis sp. n. after two workers remarkably preserved in a single piece of Early Cenomanian French amber. The new fossils provide additional information on early ant diversity and relationships and demonstrate that the monophyly of the Sphecomyrminae, as currently defined, is still weakly supported.     

Ant-lepidopteran associations along African forest edges

Working along forest edges, we aimed to determine how some caterpillars can co-exist with territorially dominant arboreal ants (TDAAs) in tropical Africa. We recorded caterpillars from 22 lepidopteran species living in the presence of five TDAA species. Among the defoliator and/or nectarivorous caterpillars that live on tree foliage, the Pyralidae and Nymphalidae use their silk to protect themselves from ant attacks. The Notodontidae and lycaenid Polyommatinae and Theclinae live in direct contact with ants; the Theclinae even reward ants with abundant secretions from their Newcomer gland. Lichen feeders (lycaenid; Poritiinae), protected by long bristles, also live among ants. Some lycaenid Miletinae caterpillars feed on ant-attended membracids, including in the shelters where the ants attend them; Lachnocnema caterpillars use their forelegs to obtain trophallaxis from their host ants. Caterpillars from other species live inside weaver ant nests. Those of the genus Euliphyra (Miletinae) feed on ant prey and brood and can obtain trophallaxis, while those from an Eberidae species only prey on host ant eggs. Eublemma albifascia (Erebidae) caterpillars use their thoracic legs to obtain trophallaxis and trophic eggs from ants. Through transfer bioassays of last instars, we noted that herbivorous caterpillars living in contact with ants were always accepted by alien conspecific ants; this is likely due to an intrinsic appeasing odor. Yet, caterpillars living in ant shelters or ant nests probably acquire cues from their host colonies because they were considered aliens and killed. We conclude that co-evolution with ants occurred similarly in the Heterocera and Rhopalocera.     

Forest clearing and sex ratio in forest-dwelling wood ant <Emphasis Type="Italic">Formica aquilonia</Emphasis>

Sex ratios of ants have been shown to vary with food resource levels in several studies, but it is not known whether forest clear-cutting has any effect on sex ratio of aphid-tending forest-dwelling ants. We investigated whether the offspring sex ratio of the forest dwelling ant Formica aquilonia varied as a response to clear-cutting. We found that the proportion of males was smaller in clear-cuts than in adjacent forests. Our results are among the first showing that anthropogenic changes in forest structures may have a potential to modify sex ratios of social insects and other forest-dwelling animals.     

Cycads: their evolution,toxins, herbivores and insect pollinators

Palaeobiological evidence indicates that gymnosperms were wind-pollinated and that insect pollination began in angiosperms in the Lower Cretaceous (ca. 135 mya) leading to close associations between higher plants and their pollinators. Cycads, which were widespread and pervasive throughout the Mesozoic (250-65 mya) are among the most primitive living seed-plants found today. Because pollination by beetles and by thrips has now been detected in several modern cycads, it is attractive to speculate that some insects and cycads had already developed similar mutualistic interactions in the Triassic (250-205 mya), long before the advent of angiosperms. We also draw attention to another key factor in this insect-plant relationship, namely secondary, defensive plant substances which must always have controlled interspecific interactions. Cycads mainly produce toxic azoglucosides and neurotoxic non-protein amino acids (e.g. BMAA), which apparently are crucial elements in the development and maintenance of mutualism (pollination) and parasitism (herbivory) by cycad-linked herbivores. We now add new results on the uptake and storage of the main toxin, cycasin, of the Mexican cycad Zamia furfuracea by its pollinator, the weevil Rhopalotria mollis, and by a specialist herbivore of Zamia integrifolia, the aposematic Atala butterfly Eumaeus atala.     

A review of early gadiform evolution and diversification: first record of a rattail fish skull (Gadiformes, Macrouridae) from the Eocene of Antarctica, with otoliths preserved in situ

Codfishes, the Gadiformes, are quite abundant in modern temperate and polar waters with a fossil record ranging back into the Palaeogene. The oldest records are from the Danian and Selandian of Europe and South Australia. The bipolar distribution early in their evolutionary history implies that their origin must have occurred quite early in the Palaeocene, or even in the Late Cretaceous with subsequent rapid diversification. By the Eocene, gadiforms were highly abundant and widespread. With the exception of gadiforms, no Eocene Antarctic teleostean group is present in the modern Antarctic fauna. Here, we review the early evolution and diversification of gadiforms in general and of macrouroids in particular. We also describe the undoubtedly oldest skeletal macrourid specimen with otoliths preserved in situ. It is the first definitive record of this group from the Eocene of Antarctica filling a gap in its stratigraphic distribution. The fossil record of gadiforms in general and macrouroids in particular indicates that the origin of both was in shallow shelf environments but with adaptations to deep-water settings early in their evolution. While gadoids seemingly originated in the earliest Palaeogene and rapidly experienced a first major radiation event in the eastern North Atlantic and/or North Sea Basin, macrouroids evolved in the Southern Ocean and migrated northwards into the South Atlantic before the establishment of the circum-Antarctic current and subsequent isolation of the Antarctic fish fauna. These two timely and regional separated adaptive radiation events in the Palaeogene gave rise to their modern taxonomic diversity and global distribution.     

Amphimixis and the individual in evolving populations: does Weismann’s Doctrine apply to all,most or a few organisms?

The German biologist August Weismann (1834–1914) proposed that amphimixis (sexual reproduction) creates variability for natural selection to act upon, and hence he became one of the founders of the Neo-Darwinian theory of biological evolution. He is perhaps best known for what is called “Weismann’s Doctrine” or “Weismann’s Barrier” (i.e. the irreversible separation of somatic and germ cell functionalities early during ontogeny in multicellular organisms). This concept provided an unassailable argument against “soft inheritance” sensu Lamarck and informed subsequent theorists that the only “individual” in the context of evolution is the mature, reproductive organism. Herein, we review representative model organisms whose embryology conforms to Weismann’s Doctrine (e.g. flies and mammals) and those that do not (e.g. freshwater hydroids and plants) based on this survey and the Five Kingdoms of Life scheme; we point out that most species (notably bacteria, fungi, protists and plants) are “non-Weismannian” in ways that make a canonical definition of the “individual” problematic if not impossible. We also review critical life history functional traits that allow us to create a matrix of all theoretically conceivable life cycles (for eukaryotic algae, embryophytes, fungi and animals), which permits us to establish where this scheme Weismann’s Doctrine holds true and where it does not. In addition, we argue that bacteria, the dominant organisms of the biosphere, exist in super-cellular biofilms but rarely as single (planktonic) microbes. Our analysis attempts to show that competition among genomic variants in cell lineages played a critical part in the evolution of multicellularity and life cycle diversity. This feature was largely ignored during the formulation of the synthetic theory of biological evolution and its subsequent elaborations.     

Which insect species numerically respond to allochthonous inputs?

Herons (Ardeidae) frequently breed in inland forests and provide organic material in the form of carcasses of prey (that they drop) and chicks (that die) to the forest floor. Such allochthonous inputs of organic materials are known to increase arthropod populations in forests. However, the exact species that show numerical responses to allochthonous inputs in heron breeding colonies remains unclear. Very few studies have clarified which factors determine numerical responses in individual species. We used pitfall and baited traps to compare the densities of arthropods between forest patches in heron breeding colonies (five sites) and areas outside of colonies (five sites) in central Japan. The density of all arthropods was not significantly different between colonies and non-colony areas. However, significant differences between colonies and non-colony areas were found in four arthropod groups. Earwigs (Dermaptera: Anisolabididae), hister beetles (Coleoptera: Histeridae), and carrion beetles (Coleoptera: Silphidae) were more abundant in colonies, while ants (Hymenoptera: Formicidae) were less abundant in colonies. We detected numerical responses to heron breeding in two earwig, one histerid, five silphid, and one ant species. Chick and prey carcasses from herons may have directly led to increases in consumer populations such as earwigs, histerids, and silphids in colonies, while microenvironmental changes caused by heron breeding may have reduced ant abundance. In the Silphidae, five species showed numerical responses to allochthonous inputs, and the other two species did not. Numerical responses in individual species may have been determined by life history traits such as reproductive behaviour.     

Foraging ants trade off further for faster: use of natural bridges and trunk trail permanency in carpenter ants

Trail-making ants lay pheromones on the substrate to define paths between foraging areas and the nest. Combined with the chemistry of these pheromone trails and the physics of evaporation, trail-laying and trail-following behaviours provide ant colonies with the quickest routes to food. In relatively uniform environments, such as that provided in many laboratory studies of trail-making ants, the quickest route is also often the shortest route. Here, we show that carpenter ants (Camponotus rufipes), in natural conditions, are able to make use of apparent obstacles in their environment to assist in finding the fastest routes to food. These ants make extensive use of fallen branches, twigs and lianas as bridges to build their trails. These bridges make trails significantly longer than their straight line equivalents across the forest floor, but we estimate that ants spend less than half the time to reach the same point, due to increased carriage speed across the bridges. We also found that these trails, mainly composed of bridges, are maintained for months, so they can be characterized as trunk trails. We suggest that pheromone-based foraging trail networks in field conditions are likely to be structured by a range of potentially complex factors but that even then, speed remains the most important consideration.     

Geographic variations in seed dispersal by ants: are plant and seed traits decisive?

The effect of local ant species on the dispersal success of a myrmecochorous plant, Helleborus foetidus, was analyzed in two populations of the Iberian Peninsula (Caurel and Cazorla, respectively). The contribution of the various local ant species to dispersal was very unequal. While 5 and 19 ant taxa visited the plants of Caurel and Cazorla, respectively, most removal activity (67 and 80%) was performed by two species only (Formica lugubris and Camponotus cruentatus, respectively). Visits by dispersers were also unequally distributed between neighboring plants. While some plants were always visited during the period of seed release, others were never visited. A regression model indicated that this pattern might be explained by two plant traits: ants preferred to visit plants that released more seeds and whose elaiosomes were richer in oleic acid. Although it has long been known that this compound triggers removal by ants, it is the first demonstration that quantitative variations in elaiosome traits contribute to variation in dispersal success. Finally, other variables being equal, morphological traits (seed size, elaiosome size, and elaiosome/seed size ratio) did not affect ant behavior. Although myrmecochory has long been considered a diffuse interaction, our results support the idea that, at local scale, a limited number of ant species may be decisive to its evolution.     

Genetic caste polymorphism and the evolution of polyandry in <Emphasis Type="Italic">Atta</Emphasis> leaf-cutting ants

Multiple mating by females with different males (polyandry) is difficult to explain in many taxa because it carries significant costs to females, yet benefits are often hard to identify. Polyandry is a derived trait in social insects, the evolutionary origins of which remain unclear. One of several leading hypotheses for its evolution is that it improves division of labour by increasing intra-colonial genetic diversity. Division of labour is a key player in the ecological success of social insects, and in many successful species of ants is based on morphologically distinct castes of workers, each with their own task specialisations. Atta leaf-cutting ants exhibit one of the most extreme and complicated forms of morphologically specialised worker castes and have been reported to be polyandrous but with relatively low mating frequencies (~2.5 on average). Here, we show for the first time that there is a significant genetic influence on worker size in Atta colombica leaf-cutting ants. We also provide the first estimate of the mating frequency of Atta cephalotes (four matings) and, by analysing much higher within-colony sample sizes, find that Atta are more polyandrous than previously thought (approximately six to seven matings). The results show that high polyandry and a genetic influence on worker caste are present in both genera of leaf-cutting ants and add weight to the hypothesis that division of labour is a potential driver of the evolution of polyandry in this clade of ants.     

Early succession arthropod community changes on experimental passion fruit plant patches along a land-use gradient in Ecuador

Many tropical landscapes are today characterized by small forest patches embedded in an agricultural mosaic matrix. In such highly fragmented landscapes, agroforests have already been recognized as refuges for biodiversity but few studies have investigated the potential of non-forested land-use types to contribute to overall biodiversity of functionally important taxa in the tropics. This study experimentally investigated species richness, abundance, and community similarity of arthropods on Yellow Passion fruit plants, planted in standardized patches in 30 sites along a land-use intensity gradient. The gradient comprised all major land-use types of the area: forest fragments, abandoned coffee agroforests, coffee agroforests managed under shade trees, pastures, and rice fields in Coastal Ecuador. We found a total of 2123 individuals belonging to 242 species. Overall arthropod species richness increased with light intensity and leaf-surface area and decreased with land-use intensity: forest fragments and abandoned coffee agroforests harboured significantly more species than rice or pastures. Overall diversity in managed coffee agroforests was intermediate between the intensively managed and more natural habitats. However, the three most abundant taxa of arthropods (ants, spiders, and beetles) had the highest number of species in managed coffee agroforests, while ant abundance was highest in abandoned coffee agroforests and spider abundance highest in managed coffee agroforests. Analyses of community similarity revealed that open (pasture, and rice) and shaded (forest, abandoned and managed coffee agroforests) land-use types had distinct arthropod communities. In conclusion, although open agricultural land-use types tend to have fewer species in lower numbers, all land-use types contribute to overall biodiversity of the agricultural matrix because of distinct communities in shaded vs. non-shaded land-use types.     

Adaptations for marine habitat and the effect of Triassic and Jurassic predator pressure on development of decompression syndrome in ichthyosaurs

Decompression syndrome (caisson disease or the “the bends”) resulting in avascular necrosis has been documented in mosasaurs, sauropterygians, ichthyosaurs, and turtles from the Middle Jurassic to Late Cretaceous, but it was unclear that this disease occurred as far back as the Triassic. We have examined a large Triassic sample of ichthyosaurs and compared it with an equally large post-Triassic sample. Avascular necrosis was observed in over 15?% of Late Middle Jurassic to Cretaceous ichthyosaurs with the highest occurrence (18?%) in the Early Cretaceous, but was rare or absent in geologically older specimens. Triassic reptiles that dive were either physiologically protected, or rapid changes of their position in the water column rare and insignificant enough to prevent being recorded in the skeleton. Emergency surfacing due to a threat from an underwater predator may be the most important cause of avascular necrosis for air-breathing divers, with relative frequency of such events documented in the skeleton. Diving in the Triassic appears to have been a “leisurely” behavior until the evolution of large predators in the Late Jurassic that forced sudden depth alterations contributed to a higher occurrence of bends.     

Indirect defense in a highly specific ant–plant mutualism

Although associations between myrmecophytes and their plant ants are recognized as a particularly effective form of protective mutualism, their functioning remains incompletely understood. This field study examined the ant-plant Hirtella physophora and its obligate ant associate Allomerus decemarticulatus. We formulated two hypotheses on the highly specific nature of this association: (1) Ant presence should be correlated with a marked reduction in the amount of herbivory on the plant foliage; (2) ant activity should be consistent with the "optimal defense" theory predicting that the most vulnerable and valuable parts of the plant are the best defended. We validated the first hypothesis by demonstrating that for ant-excluded plants, expanding leaves, but also newly matured ones in the long term, suffered significantly more herbivore damage than ant-inhabited plants. We showed that A. decemarticulatus workers represent both constitutive and inducible defenses for their host, by patrolling its foliage and rapidly recruiting nestmates to foliar wounds. On examining how these activities change according to the leaves’ developmental stage, we found that the number of patrolling ants dramatically decreased as the leaves matured, while leaf wounds induced ant recruitment regardless of the leaf’s age. The resulting level of these indirect defenses was roughly proportional to leaf vulnerability and value during its development, thus validating our second hypothesis predicting optimal protection. This led us to discuss the factors influencing ant activity on the plant’s surface. Our study emphasizes the importance of studying both the constitutive and inducible components of indirect defense when evaluating its efficacy and optimality.     

Ubiquitous occurrence of semi-volatile carbonyl compounds in tropospheric samples and their possible sources

The levels of semi-volatile aldehydes with 4–10 carbon atoms and a ketone identified as 6-methyl-5-hepten-2-one by mass spectrometry have been measured in some urban, suburban and forest areas together with important hydrocarbons emitted by man-made (benzene, toluene) and biogenic sources (α-pinene). The results obtained show the ubiquitous occurrence of these carbonyl compounds in the atmospheric environment. Diurnal profiles obtained at various sites and a vertical gradient measured in a pine forest seem to be consistent with their natural origin. Direct emission from plants seems to be a major source for these components in the atmospheric boundary layer. The levels measured indicate that they are among the most abundant gaseous organic components present in natural environments.