Testing for the effects and consequences of mid paleogene climate change on insect herbivory

Background

The Eocene, a time of fluctuating environmental change and biome evolution, was generally driven by exceptionally warm temperatures. The Messel (47.8 Ma) and Eckfeld (44.3 Ma) deposits offer a rare opportunity to take a census of two, deep-time ecosystems occurring during a greenhouse system. An understanding of the long-term consequences of extreme warming and cooling events during this interval, particularly on angiosperms and insects that dominate terrestrial biodiversity, can provide insights into the biotic consequences of current global climatic warming.

Methodology/Principal Findings

We compare insect-feeding damage within two middle Eocene fossil floras, Messel and Eckfeld, in Germany. From these small lake deposits, we studied 16,082 angiosperm leaves and scored each specimen for the presence or absence of 89 distinctive and diagnosable insect damage types (DTs), each of which was allocated to a major functional feeding group, including four varieties of external foliage feeding, piercing- and-sucking, leaf mining, galling, seed predation, and oviposition. Methods used for treatment of presence–absence data included general linear models and standard univariate, bivariate and multivariate statistical techniques.

Conclusions/Significance

Our results show an unexpectedly high diversity and level of insect feeding than comparable, penecontemporaneous floras from North and South America. In addition, we found a higher level of herbivory on evergreen, rather than deciduous taxa at Messel. This pattern is explained by a ca. 2.5-fold increase in atmospheric CO₂ that overwhelmed evergreen antiherbivore defenses, subsequently lessened during the more ameliorated levels of Eckfeld times. These patterns reveal important, previously undocumented features of plant-host and insect-herbivore diversification during the European mid Eocene.     

Fossil water striders from the Middle Eocene fossil sites of Eckfeld and Messel,Germany (Hemiptera,Gerromorpha)

Water striders (Hemiptera, Gerromorpha) are a very distinct ecological group specially adapted for life on the water surface. The present paper reports on four species of Gerromorpha from the Middle Eocene fossil sites of Eckfeld and Messel describingLutetiabates eckfeldensis n. gen. et n. sp.,Cylindrobates messelensis n. gen. et n. sp. (both Gerridae), and two nymphs most probably of the genusGerris. The record of two new members of Gerridae from the Paleogene as well as the hitherto known Gerromorpha from fossiliferous resins document a distinctly higher diversity of water striders within die European Paleogene than today. Lastly, comments are made on the fossil history as well as on the palaeobiological and palaeobiogeographical significance of the faunas.     

Fossil water‐penny beetles (Coleoptera: Psephenidae: Eubrianacinae) from the Eocene of Europe,with remarks on their phylogenetic position and biogeography

Abstract: A species of water‐penny beetles is recorded from larval instars from the Middle Eocene Messel pit fossil site in Germany. This species clearly belongs to the psephenid subfamily Eubrianacinae, but its precise systematic affinities remain unclear. It is the second fossil species of this taxon recorded from Europe. The holotype of the first fossil species, Eubrianax vandeli Bertrand and Laurentiaux, 1963, is lost. The high number of fossil specimens from Messel allowed discussion of stratigraphic and spatial occurrence of the eubrianacine species in the Messel pit, but its larval ontogeny could not be unravelled. Because of the high number of fossils and their wide occurrence, it is inferred that the species from Messel gen. sp. 1 was an autochthonous faunal element of the Eocene Lake Messel, which might indicate that some parts of the former Lake Messel had a shore area with stones. The analysis of the phylogenetic position of both Eocene eubrianacine species showed that their phylogenetic placement cannot be resolved because preservational influences limit the evaluation of characters. The historical biogeography of Psephenidae and Eubrianacinae is analysed and discussed. The fossil record shows that psephenid beetles have fossil members occurring outside their current distribution range, so interpretations of their biogeography based only on extant members can be misleading.     

The best of two worlds: ecology and evolution of ambophilous plants

Ambophily, the mixed mode of wind and insect pollination is still poorly understood, even though it has been known to science for over 130 years. While its presence has been repeatedly inferred, experimental data remain regrettably rare. No specific suite of morphological or ecological characteristics has yet been identified for ambophilous plants and their ecology and evolution remain uncertain. In this review we summarise and evaluate our current understanding of ambophily, primarily based on experimental studies. A total of 128 ambophilous species – including several agriculturally important crops – have been reported from most major habitat types worldwide, but this probably represents only a small subset of ambophilous species. Ambophilous species have evolved both from wind- and insect-pollinated ancestors, with insect-pollinated ancestors mostly representing pollination by small, generalist flower visitors. We compiled floral and reproductive traits for known ambophilous species and compared our results to traits of species pollinated either by wind or by small generalist insects only. Floral traits were found to be heterogeneous and strongly overlap especially with those of species pollinated by small generalist insects, which are also the prominent pollinator group for ambophilous plants. A few ambophilous species are only pollinated by specialised bees or beetles in addition to pollination by wind. The heterogeneity of floral traits and high similarity to generalist small insect-pollinated species lead us to conclude that ambophily is not a separate pollination syndrome but includes species belonging to different insect- as well as wind-pollination syndromes. Ambophily therefore should be regarded as a pollination mode. We found that a number of ecological factors promoted the evolution of ambophily, including avoidance of pollen limitation and self-pollination, spatial flower interference and population density. However, the individual ecological factors favouring the transition to ambophily vary among species depending on species distribution, habitat, population structure and reproductive system. Finally, a number of experimental studies in combination with observations of floral traits of living and fossil species and dated phylogenies may indicate evolutionary stability. In some clades ambophily has likely prevailed for millions of years, for example in the castanoid clade of the Fagaceae.     

The Morphology of Pollen Tetrads and Viscin Threads in Some Tertiary,Rhododendron-Like Ericaceae

The morphology of pollen tetrads and viscin threads is described in fossil Ericaceae pollen from various Eocene/Oligocene/Miocene localities in Europe (Germany, Austria), North America (eastern U.S.A.), and Asia (eastern China). The typical characters of the tetrad configuration, the exine ornamentation and sculpturing, and especially the viscin thread morphology are extremely similar to or even indistinguishable from that in extant members of Rhododendron. All these pollen morphological features strongly suggest that all the investigated material can be assigned to a modern taxon of the Ericaceae: either to Rhododendroideae or even to Rhododendron itself.     

Synonymy and actual affinities of the putative Middle Eocene “New World vulture” Eocathartes Lambrecht , 1935 and “hornbill” Geiseloceros Lambrecht , 1935 (Aves, Ameghinornithidae)

The taxonomy and phylogenetic affinities of the putative “New World vulture”Eocathartes robustus,Lambrecht, 1935 and the “hornbill”Geiseloceros robustus Lambrecht, 1935 from the Middle Eocene of the Geisel Valley in Germany are revised. It is shown that the holotype specimens belong to a single individual, whose osteology closely resembles that ofStrigogyps sapea (Peters, 1987) from the Middle Eocene of Messel (Germany). The species is classified intoStrigogyps robustus (Lambrecht, 1935), n. comb., and provides further evidence for the great similarity between the Eocene avifaunas of the Geisel Valley and Messel.Strigogyps is a representative of the Ameghinornithidae whose phylogenetic affinities are uncertain; there is no fossil record of either Cathartidae (New World vultures) or Bucerotidae (hornbills) from the Geisel Valley.     

Mechanisms of pollen deposition by insect pollinators

Summary Studies of pollen dispersal in insect-pollinated plants have often documented highly leptokurtic patterns of pollen deposition that can increase the likelihood of long-distance mating. To examine potential causes of highly leptokurtic deposition, we introduce four functions that arise when (1) the duration of pollinator visits to pollen sources is limited, (2) the rate of pollen deposition varies randomly among pollinators and/or among visits, (3) the rate of pollen deposition changes monotonically over time or (4) pollen is carried in layers or compartments on the pollinator's body that differ in deposition rate. Maximum likelihood techniques were used to fit deposition functions to data obtained from honey bees (Apis mellifera L.) visiting mustard plants (Brassica campestris L.) that contained a marker gene. Each of the alternative leptokurtic functions fit the experimental data better than a simple exponential function and the best-fit function predicted a mean pollen dispersal distance more than three times greater than the exponential. We argue that studies of pollen deposition need to test a broader range of deposition models to assess outcrossing distance in plant populations accurately.     

The fossil pollen record of Araceae

The fossil record of Araceae pollen beginning in the late Early Cretaceous and peaking in the Paleocene/Eocene is very sparse up to now, consisting of three highly distinctive types: zona-aperturate pollen of the Monstera or Gonatopus type (very similar to Proxapertites operculatus), an ulcerate-spiny type typical for Limnobiophyllum, and a polyplicate, omniaperturate pollen type (an ephedroid pollen with non-gnetalean affinities) which was recently reported from the late Early Cretaceous (Mayoa portugallica). An extensive literature search has shown that some distinctive Ephedripites forms (the Paleogene Ephedripites vanegensis, and the Late Cretaceous Ephedripites elsikii) are very similar to pollen of Spathiphyllum and both species are here transferred from Ephedripites to Spathiphyllum (as comb. nov.). We also add new fossil findings to the Araceae record. The new findings include a zona-aperturate, microperforate to microreticulate pollen type from the Palaeocene of Colombia, highly similar to extant Gonatopus or Zamioculcas or Monstera pollen (Araceae) and to fossil Proxapertites operculatus, which is currently seen as a fossil equivalent; and, an ulcerate, spiny pollen from the Eocene of Stolzenbach, Germany, extending the range of Limnobiophyllum (Pandaniidites), which is thought to be an extinct member of extant Araceae. The three pollen types add considerably to the reliable fossil record of the family that now contains more than 20 records of these three pollen types: with the zona-aperturate type recorded from the tropical or subtropical regions of Northern and Southern America, Central Africa, Southern and Central Europe, from the Indian subcontinent and the Malayan Archipelago; the ulcerate type occurring in North America and Europe; and the polyplicate type mainly occurring in South America and South-West Europe. Now we have good evidence that some of the aroid subfamilies were already in existence in the Cretaceous, increasing in diversity and worldwide distribution in the Paleogene. Dedicated to Prof. Dr. Stefan Vogel on the occasion of his 80th birthday.     

Squamate reptiles from the middle Eocene of Lissieu (France). A landmark in the middle Eocene of Europe

In Europe, faunas of squamates (lizards and snakes) from the middle Eocene are very poorly known, with the exception of those from the level MP 16 (latest middle Eocene). From the MP 11-MP 15 interval, squamates were previously reported only from Messel (MP 11, earliest middle Eocene) and from the untere and obere Mittelkohle of Geiseltal (MP 12 and MP 13 respectively) in Germany. The present report describes the middle Eocene assemblage of squamates from Lissieu (France), the first fauna reported from the level MP 14. Whereas fossils from Messel and Geiseltal are mostly articulated skeletons, fossils from Lissieu are represented by disarticulated bones; such fossils may be more easily compared to those from other Cenozoic localities, in which bones are almost always disarticulated. The fauna from Lissieu is more diverse than those from the Geiseltal sites and approximately as diverse as that from Messel as they are presently known; it is comprised of 17 distinct taxa. These taxa cannot be all identified to the species or genus level. They belong to iguanids, gekkonids, lacertids, anguids, thecoglossan platynotans, ophidians incertaesedis, boids, ?tropidophiines, “tropidophiids” incertaesedis, booids incertaesedis, and perhaps russellophiids. The fauna includes several new taxa but only a presumed tropidophiine snake may be named on the basis of the available material. The fauna from Lissieu is a mixture of taxa restricted to the middle Eocene and taxa known from older or younger levels. Taxa shared by Lissieu and the few other localities from the middle Eocene of Europe are rare. This fauna from Lissieu represents a stratigraphical landmark for the middle Eocene.     

The implications of the numerical dating of the Messel fossil deposit (Eocene, Germany) for mammalian biochronology

Radiometric dating of volcaniclastic material from a borehole below the Middle Eocene Messel Formation leads to a revised numerical age of the Messel fossil deposit. Accordingly, the Grauvian/Geiseltalian boundary moves up from about 49 to 47.5 ma. The consequences of this change as well as the necessity of the Geiseltalian European Land Mammal Mega-Zone (ELMMZ)¹ for mammalian biochronology are discussed.     

Studies on Cenozoic crocodiles: 8.Bergisuchus dietrichbergi Kuhn (Sebecosuchia: Bergisuchidae n. fam.) from the Middle Eocene of Germany, some new systematic and biological conclusions

Bergisuchus dietrichbergi Kuhn is redescribed as a member of its own family, Bergisuchidae n. fam., within the Sebecosuchia. At present, two fragmentary specimens ofBergisuchus are known: the holotype ofBergisuchus, a partial rostrum, comes from the lower part of the Middle Eocene of the Messel pit, near Darmstadt; and a recently discovered fragmentary mandible from the middle part of the Middle Eocene of Geiseltal in an opencast coal-mining pit near Halle (Saale).Bergisuchus shows similarities with species ofSebecus which are known from the Paleocene to Miocene from South America. All palaeoecological and biomechanical data support the hypothesis ofBergisuchus as a small, mainly terrestrial crocodile, which did not build its nests near either of the fossil localities from which it has been collected.     

Elucidating the affinities and habitat of ancient, widespread Cyperaceae: Volkeria messelensis gen. et sp. nov., a fossil mapanioid sedge from the Eocene of Europe

The sedges (family Cyperaceae) are an economically and ecologically important monocot group dating back at least to the Paleocene. While modern genera are mostly unknown before the Oligocene, several extinct taxa are recognized as the earliest sedges. Their affinities have been unclear until now, because they are found as isolated, often abraded fruits or endocarps. Exceptionally preserved sedge fossils from the Middle Eocene of Messel, Germany yield more characters for identification. Fossil cyperacean infructescences with in situ pollen are recognized for the first time and show features of the early-divergent mapanioid sedges. Pollen resembles that of tribe Hypolytreae. Comparisons with extant taxa suggest the closest affinities with Hypolytrum and Mapania. However, the Messel fossils represent a distinct taxon, Volkeria messelensis gen. et sp. nov. Without the additional characters of infructescence and pollen, the Messel fruits would have been placed in the extinct genus Caricoidea, a typical Eocene sedge that was widespread across Eurasia. Similarities of fruit structure suggest that Caricoidea was also a mapanioid sedge. Mapanioid sedges are found today in tropical wet forests and swamps, a distribution suggesting that early sedges occupied a similar habitat, unlike many modern sedges, and were not precursors to open grassland vegetation.     

Generalized host‐plant feeding can hide sterol‐specialized foraging behaviors in bee–plant interactions

Host‐plant selection is a key factor driving the ecology and evolution of insects. While the majority of phytophagous insects is highly host specific, generalist behavior is quite widespread among bees and presumably involves physiological adaptations that remain largely unexplored. However, floral visitation patterns suggest that generalist bees do not forage randomly on all available resources. While resource availability and accessibility as well as nectar composition have been widely explored, pollen chemistry could also have an impact on the range of suitable host‐plants. This study focuses on particular pollen nutrients that cannot be synthesized de novo by insects but are key compounds of cell membranes and the precursor for molting process: the sterols. We compared the sterol composition of pollen from the main host‐plants of three generalist bees: Anthophora plumipes, Colletes cunicularius, and Osmia cornuta, as well as one specialist bee Andrena vaga. We also analyzed the sterols of their brood cell provisions, the tissues of larvae and nonemerged females to determine which sterols are used by the different species. Our results show that sterols are not used accordingly to foraging strategy: Both the specialist species A. vaga and the generalist species C. cunicularius might metabolize a rare C₂₇ sterol, while the two generalist species A. plumipes and O. cornuta might rather use a very common C₂₈ sterol. Our results suggest that shared sterolic compounds among plant species could facilitate the exploitation of multiple host‐plants by A. plumipes and O. cornuta whereas the generalist C. cunicularius might be more constrained due to its physiological requirements of a more uncommon dietary sterol. Our findings suggest that a bee displaying a generalist foraging behavior may sometimes hide a sterol‐specialized species. This evidence challenges the hypothesis that all generalist free‐living bee species are all able to develop on a wide range of different pollen types.     

New fossil ants of the subfamily Myrmeciinae (Hymenoptera, Formicidae) from Germany

Two new fossil members of the subfamily Myrmeciinae are described: Archimyrmex wedmannae, sp. nov (Grube Messel, Germany, Middle Eocene) and Prionomyrmex wappleri, sp. nov. (Rott, Germany, Late Oligocene). Members of the genus Archimyrmex were known earlier from Eocene deposits of the United States and Argentina, and members of the genus Prionomyrmex were known from Late Eocene Baltic amber.     

The mangrove palm Nypa in the geologic past of the New World

The paleontological history of Nypa, known today as the mangrovepalm, is traced through geological time back to the Late Cretaceous. Emphasis is laid on the New World occurrences, especially in NorthAmerica, where Nypa is known from fossil fruits and pollen. In SouthAmerica, the stratigraphic range of this palm extends from theMaastrichtian to the late Eocene, whereas in North America, Nypa isrestricted to only the Eocene. Nypa occurs as pollen all along theAmerican Gulf Coast from the early Eocene (Ypresian) to the late Eocene(Priabonian), while fruit records come from the early and middle Eoceneof Maryland and Texas, respectively. The floristics of these Eocenemangroves, including possible mangrove associates, and the developmentof mangrove vegetation in the neotropics through the Tertiary andQuaternary, are discussed. New paleobotanical evidence from a middleEocene faunal and floral assemblage in Texas, the Casa Blanca flora (LaredoFormation, Claiborne Group), which contains fossil Nypa pollen andfruits, is described in detail.     

A small, “wader-like” bird from the Early Eocene of Messel (Germany)

A small bird with a shorebird-like beak and a very long hind toe is described from the Early Eocene of Messel in Germany. Vanolimicola longihallucis, gen. et sp. nov. is one of the few candidate species for a “wading bird” from Messel, that is, a bird that may have foraged along the shoreline of the ancient lake. A few features indicate a relationship to charadriiform birds and Jacanidae (jacanas) in particular, but charadriiform affinities are only weakly supported. In the preserved skeletal elements, V. longihallucis also resembles the taxon Songzia from the Early Eocene of China, which is considered to be a representative of the Ralloidea (rails and allies). A potential biogeographic significance of the new Messel fossil is strengthened by similar fossils from the North American Green River Formation.     

The Oldest Beetle and Bee Ichnofossils from Mexico and their Paleoenvironmental Implications

ABSTRACT

Specimens of Fictovichnus gobiensis, Celliforma curvata, Celliforma rosellii, Celliforma germanica and Celliforma isp. were collected from paleosol horizons in a fluviolacustrine succession near Santiago Yolomécatl town, in northwestern Oaxaca, southern Mexico. These ichnofossils represent the oldest evidence of beetles and bees in Mexican localities. K–Ar ages and the record of the equid Miohippus assiniboiensis, an index fossil, indicate that the age of the deposits is late Eocene. Based on the presence of the insect ichnofossils, pedogenic carbonate isotopes and mammal proxies, the inferred type of vegetation present in the study area was scrubland/woodland, within subhumid to subarid conditions.     

POLLINATION AND POLLEN ENERGETICS IN MEDITERRANEAN ECOSYSTEMS

Most plants in Mediterranean ecosystems are insect pollinated, with pollen being the main reward to pollinators. The great majority of pollinators (70%) are bees and flies. We measured the energy content of pollen from 40 plant species in these ecosystems that represent abiotic and biotic pollination modes as well as the number of species of their pollinators. Pollen energy content correlates with pollinator diversity. Pollen of wind-pollinated plants contained less energy than that of insect-pollinated plants; there was no difference between insect-pollinated dicots and insect-pollinated monocots. The median date of flowering (from 1 January) estimated for each of the plant species did not vary significantly either with the number of pollinator species or with the energy content of pollen. The reasons for the differing values of pollen energy content are discussed; in particular, its relation to the type of pollen reserves, length of the flower style, and pollination enhancement.     

Partitioning of pollen resources by two stingless bee species in the north Bahia,Brazil

Analysing the pollen stored by stingless bees allows identification of the diversity of flowering plants visited by these bees while collecting resources during a given period. However, few studies have focused on investigating the sharing of resources between species of native bees that coexist in transitional plant formations, which support conservation efforts and increase colony productivity. This study aims to describe the partitioning of pollen resources among colonies of two species of stingless bees in the state of the Bahia (Brazil) through the analysis of stored pollen. The study was conducted in neighbouring vegetation zones of the relevant species Melipona quadrifasciata anthidioides and Melipona scutellaris by collecting monthly pollen samples stored by three colonies of each species over one year. The collected samples were treated using the acetolysis technique, and the partitioning of pollen resources between the two species was investigated through quali-quantitative analysis of the treated pollen. The results show that among the 16 pollen types belonging to a particular species or group identified in the Melipona quadrifasciata anthidioides samples and the 18 identified in the Melipona scutellaris samples, 13 were shared by both species. The two most common pollen types stored by both species were from Mimosa arenosa (Fabaceae, Mimosoidae) and Eucalyptus sp. (Myrtaceae). These results demonstrate the niche similarity of pollen pasture between these two species and suggest that conservation efforts for these bee species should focus on the plant families most visited by bees.     

Melissopalynology in an area of Atlantic Forest (northeast region,Brazil)

Apis mellifera is a bee that was introduced to Brazil and has adapted very well to the climate conditions and vast diversity of plants that exist in the country. In the northeast region of Brazil, beekeepers make use of the association between bees and plants by selling various bee products, notably honey. One way to identify species visited by bees in an area is by the pollen in its products. Based on this, 16 samples of honey were analysed, which were collected over a period of two years and obtained from an apiary in the Atlantic Forest biome in the municipality of Entre Rios (Bahia). In addition, climatic data (precipitation and temperature) of the region were obtained for the months sampled. The average temperature of the region during the collection months varied from 22 to 28 °C. The highest precipitation recorded in the region was 133.7 mm³ and the lowest was 0.3 mm³. Seventy pollen types were found. The family Fabaceae was notable, with ten pollen types, of which Mimosa pudica was the most important with a high frequency of occurrence and distribution. The Eucalyptus (Myrtaceae) pollen type also had a high frequency of occurrence and distribution. In addition, pollen types corresponding to species that supply nectar to bees were identified, which contributes to the large diversity of bee plants for Apis mellifera in the study area.