Sunday, 1 December 2019

Angimordella burmitina: A pollen-associated Tumbling Flower Beetle from Cretaceous Burmese Amber.

Angiosperms, Flowering Plants, are the most diverse group of Land Plants. The earliest unequivocal pollen and macrofossils of Angiosperms are generally thought to date from the early Hauterivian (about 130 million years ago) and early Aptian (about 125 million years ago), respectively, despite claims based on other fossils and molecular analyses. The apparently rapid and tremendous evolutionary diversification of Angiosperms during the Cretaceous was the great 'abominable mystery' mentioned by Darwin and continues to be an active and sometimes a controversial area of research. Insect pollination (entomophily) is generally considered to be a key contributor to the Cretaceous radiation of Angiosperms. It is generally thought to be the dominant pollination mode of Angiosperms during the early mid-Cretaceous with specialisation increasing during the angiosperm radiation, supported by basal flower morphology, palynological data, and phylogenetic inferences. Some Cretaceous Insects are palynivores of Angiosperms based on their pollen- or nectar-feeding mouthparts, gut contents, or coprolites. However, a palynivore is not equivalent to a pollinator. Only direct evidence (pollen-carrying behaviour and pollen-feeding mouthparts) can provide unambiguous demonstration of ancient Insect pollination. Until now, direct evidence of Cretaceous Insect pollination supports Insect-Gymnosperm pollination, such as that involving Thrips, True Flies, Beetles, and Scorpionflies. Although both Insects and Angiosperms were common during the mid-Cretaceous, direct evidence for Cretaceous Insect-Angiosperm pollination mode has been absent.

In a paper published in the Proceedings of the National Accademy of Sciences of the USA on 11 November 2019, Tong Bao of the State Key Laboratory of Palaeobiology and Stratigraphy at the Nanjing Institute of Geology and Palaeontology, the Center for Excellence in Life and Paleoenvironment of the Chinese Academy of Sciences, and the Institut für Geowissenschaften at Universität Bonn, Bo Wang, also of the State Key Laboratory of Palaeobiology and Stratigraphy at the Nanjing Institute of Geology and Palaeontology, the Center for Excellence in Life and Paleoenvironment of the Chinese Academy of Sciences, and of the Key Laboratory of Zoological Systematics and Evolution at the Institute of Zoology of the Chinese Academy of Sciences, Jianguo Li, again of the State Key Laboratory of Palaeobiology and Stratigraphy at the Nanjing Institute of Geology and Palaeontology, the Center for Excellence in Life and Paleoenvironment of the Chinese Academy of Sciences, and David Dilcher of the Department of Geology and Atmospheric Science at Indiana University, describe a new species of Tumbling Flower Beetle, Mordellidae, from a pieces of Burmese Amber, with associated Angiosperm pollen, which they argue provides the first direct evidence of Insect pollination of Angiosperms in the Cretaceous.

Beetles constitute almost a quarter of all Animal species on Earth, and are among the most prominent pollinators of Angiosperms. More than 77 000 beetle species are estimated to visit flowers. Among these flower-visiting Beetles, Tumbling Flower Beetles are one of the most species-rich families, and adults are easily recognised by their humpbacked body, deflexed head, pointed abdomen, and stout hind legs. The majority of extant adult Mordellids feed on Angiosperm pollen Cretaceous Mordellids have been hypothesised to be Angiosperm pollinators, but direct evidence of this has been lacking.

Cretaceous ‘Burmese Amber’ has been extensively worked at several sites across northern Myanmar (though mostly in Kachin State) in the last 20 years. The amber is fairly clear, and often found in large chunks, providing an exceptional window into the Middle Cretaceous Insect fauna. This amber is thought to have started out as the resin of a Coniferous Tree, possibly a Cypress or an Araucaria, growing in a moist tropical forest. This amber has been dated to between 105 and 95 million years old, based upon pollen inclusions, and to about 98.8 million years by uranium/lead dating of ash inclusions in the amber.

The new species is named  Angimordella burmitina, where 'Angimordella' is a combination of Angiosperm, for Flowering Plant, and Mordella, the genus name from which Mordellidae is derived, and 'burmitina' is a mineralogical name used for Burmese Amber. The species is described from a single specimen, a complete Beetle with left side visible but its right side covered by abundant microbubbles. A Thrips is near the maxillary palpi of the Beetle on the left side. This Beetle is small, about 4.25 mm in length, with serrated antennae, abundant wrinkles and folds on the protonum (backplate covering the abdomen) and elytra (wingcases), but not the legs.

Cretaceous Tumbling Flower beetle Angimordella burmitina. (A) Habitus. (B) Drawing. (C) Prothorax and pronotum highlighted by red dashed lines. (D) Microtomographic reconstruction of the head. Maxillary palpi highlighted in yellow. (E) Abdomen, I−IV represent first to fifth abdominal ventrites. (F) Hind leg, I−IV represent first to fourth metatarsomeres. an, antennae; cl, claw; mp, maxillary palp; py, pygidium; sp, spines on metatibiae and metatarsi; tr, trochanter. Bao et al. (2019).

The body of Angimordella burmitina is strongly convex, wedge-shaped, and widest near base of prothorax, becoming slightly narrowed anteriorly and posteriorly. The head is strongly declined, with mouthparts directly posteriorly, and compound eyes which are finely faceted and glabrous. The occipital regionis wide, and has a a surface covered with wrinkles and hairs, matching perfectly with anterior edge of the pronotum. The antennae are comparatively short, with 7 visible antennomeres, and obviously serrate, all features considered diagnostic of a Tumbling Flower Beetle

There are at least 62 pollen grains (from only the visible left side of the Beetle) in the amber in total, of which 24 pollen grains aggregate into two small clusters near the abdominal end of the Insect. Pollen grains in the amber are retitricolpate and highly uniform in morphology. The shape of the grains is approximately oblate spheroidal, and they  measure 30.95−22.08 μm × 20.68−13.93 μm in equatorial view, based on measurement of the 27 best preserved pollen grains. The pollen clump shape is irregular, and the pollen grains are well preserved, indicating that they are natural floral remains rather than coprolites. These pollen grains can be confidently attributed to the Eudicot monophyletic group (true Dicotyledons), members of which are distinguished from all other Angiosperms by their tricolpate pollen structure. Bao et al. do not assign the pollen to a taxon given the nature of this microscopic method conducted within amber.

Angimordella burmitina and tricolpate pollen grains. (A) Habitus. Pollen grains attached to the body are indicated by red dots, unattached are indicated by yellow dots, clumped pollen are indicated by blue squares. (B)−(H) Locations are highlighted in (A). (B) and (C) Pollen grains near the body. Yellow arrows point to colpi. (D) and (E) Pollen grains on the body. (F)−(H) Clumped pollen grains. (G) and (H) Locations are highlighted in (F) and (G), respectively. Blue arrows point to colpi. Bao et al. (2019).

Angimordella burmitina exhibits a series of specialized body structures related to its flower-visiting behavior, similar to its modern counterparts, which feed on various angiosperm pollen. It has the Mordella-type apical maxillary palpomere (part of the mouth), which is enlarged and securiform (axe-shaped). This maxillary palpomere is blocked by a Thrips, but the palpomere shape was revealed by micro-tomography. This specialised modification of the maxillary palpomere has been known to aid collecting and most likely transporting pollen grains. Angimordella burmitina has a curved and laterally compressed body with a strongly declined head, allowing for flexibility when feeding inside the flower. Its hind legs are well developed, with enlarged metacoxa and metafemora and spiny metatibiae and metatarsi, which make it easier to move on the corolla and from one flower to another. Moreover, Angimordella burmitina has fine hairs; the spacing and height of these hairs influence the ability of the hairs to carry pollen grains. Accordingly, the hairs on the Beetle’s thorax and abdominal sternites are distinctly longer than 30 μm, and the spacing between the hairs is consistent with the width of the coexistent pollen grains (about 20 μm) and is well-adapted for holding and transporting pollen grains. 

Angimordella burmitina is covered by abundant tricolpate pollen grains that are mainly distributed on the thorax and abdomen. Tricolpate pollen is both the defining and most important character of the Eudicots, a group which comprises about 75% of extant Angiosperm species. The earliest fossil record of tricolpate pollen is about 125 million years old, slightly older than the earliest Eudicot macrofossil. By 99 million years ago (i.e. Burmese Amber age), tricolpate pollen had become widespread worldwide and Eudicot macrofossils are reported from Burmese Amber. Many Cretaceous plants with tricolpate pollen are animal-pollinated and characterised by their ornamentation, size (10−300 μm), and clumping characteristics. Small Angiosperm pollen grains in amber, especially those buried under Insect body hairs, are often not visible under optical microscopy and, thus, could be easily overlooked. In Bao et al's study, the pollen grains between body hairs were detected by confocal laser scanning microscopy, which takes advantage of pollen fluorescence, which contrasts with the surrounding dark Insect cuticle. The tricolpate pollen grains found in Burmese amber exhibit remarkable zoophilous pollination features including their reticulate surface and presence of pollen clumping, thus providing more evidence to support beetle-mediated pollination. Interestingly, only one type of pollen was found on this Beetle. This could reflect that there were not very many different types of flowers during the mid-Cretaceous or that the Insect visited only one type of flower before it was trapped in the amber.

Ecological reconstruction of Angimordella burmitina. These Tumbling Flower Beetles are feeding on Eudicot flowers. The colour and morphology of flowers are artistic only. Bao et al. (2019).

The Mordellidae, comprising about 1500 extant species worldwide, are among the most basal group of Tenebrionoidea based on morphological analysis and molecular data. Although Mordellid-like beetles are reported from the Middle-Late Jurassic of China and Kazakhstan, the earliest true Mordellids (i.e. members of the extant subfamily) are known from the mid-Cretaceous Spanish and Burmese amber. Angimordella burmitina is among the earliest true Mordellids and indicates that Mordellid-Angiosperm pollination mutualisms have been present since at least 99 million years ago. These mutualisms may be an important driver for the radiation of true Mordellids.

Bao et al. believe this provides direct evidence of Cretaceous Insect pollination of Angiosperms, which is strongly supported by the flower-visiting body shape, specialised pollen-feeding mouthparts, and zoophilous pollen grains attached to the body. The prior earliest direct evidence of Insect pollination of Angiosperms was reported from several pollen-collecting Bees from the Middle Eocene of Eckfeld and Messel (48 and 45 million years old, respectively) in Germany. Their findings thereby extend the known geological range of direct evidence of Insect pollination of Angiosperms by at least 50 million years.

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