Effect of posterior gut reduction on the evolution of rhynchonelliform brachiopods

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Brachiopods are a group of animals known since the Early Cambrian and thrived in the Paleozoic. After the Permian–Triassic extinction, there was a significant reduction in the taxonomic diversity of brachiopods. According to one hypothesis, in the Mesozoic, brachiopods with blind gut could not reinstate their numbers due to the predominance of shelly plankton. We assume that the terebratulids, the most widespread group of modern brachiopods, were able to adapt to the changed composition of food due to a more efficient filtration mechanism of the plectolophous lophophore. Extant rhynchonellids have a blind–closed bulbus end of digestive tract, which is probably used for crushing and digesting shelly plankton.

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А. Selischeva

Lomonosov Moscow State University

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Email: selav21@mail.ru
俄罗斯联邦, Moscow

参考

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2. Fig. 1. Scheme of brachiopod anatomy based on representatives of the order Terebratulida, lateral view (gonads, muscles and metanephridia are not shown; after: James et al., 1992, with modifications). Designations: vv – ventral valve, ds – dorsal valve, l – lophophore, mp – mantle cavity, n – stalk, ps – digestive system, tc – trunk coelom.

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3. Fig. 2. Generic diversity of brachiopods in paleontological history (after Carlson, 2016, with modifications).

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4. Fig. 3. Relationship between the generic diversity of bivalves and brachiopods and the qualitative composition of phytoplankton in the Phanerozoic (after Zezina, 2008, with modifications). The vertical axis for graphs 1 and 2 indicates the number of genera, and the horizontal axis for 1–7 indicates paleontological periods. Designations: 1 – bivalves, 2 – brachiopods, 3 – diatoms, 4 – coccolithophores, 5 – dinoflagellates, 6 – green algae, 7 – cyanobacteria; k – Cambrian, o – Ordovician, s – Silurian, d – Devonian, ka – Carboniferous, p – Permian, t – Triassic, ju – Jurassic, m – Cretaceous, pa – Paleogene, n – Neogene, pl – Pleistocene.

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5. Fig. 4. Evolution of rhynchonelliform brachiopods (after Carlson, 2016, with modifications) and diagrams of the structure of the digestive system of representatives of the extinct orders Chileida (ventral view; after Zhang et al., 2007b, with modifications), Kutorginida (ventral view; after Zhang et al., 2007c, with modifications) and modern orders Rhynchonellida, Terebratulida, Thecideida (lateral view; after Nielsen, 1991, with modifications). The red dot indicates the anus, the cross indicates the blind closure of the intestine. Taxonomy of brachiopods after: Carlson, 2016; Harper et al., 2017.

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6. Fig. 5. Schemes of the structure of the hinge structures of the rhynchonelliform brachiopod shell on the ventral valve (left column) and dorsal valve (right column): a – strophic surfaces of Chile sp. (Chileata; after Popov, Holmer, 2000a, with modifications); b – primitive hinge of Obolella sp. (Obolellata; after Popov, Holmer, 2000b, with modifications); c – astrophic surfaces of Kutorgina sp. (Kutorginata; Popov, Williams, 2000, with modifications); d – deltidiodont hinge of Hesperorthis sp., Hebertella sp. (Rhynchonellata; after Rudwick, 1970, with modifications); d – cyrtomatodont hinge of Magellania sp. (Rhynchonellata; after Clarkson, 1979, with modifications).

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7. Fig. 6. The location of the mantle cavity (highlighted in pink) and the trunk coelom (highlighted in blue) inside the brachiopod shell (after Rowell, Caruso, 1985; James et al., 1992; with modifications): a, b – Lingula anatina (Linguliformea): a – dorsal view, b – lateral view; c – Nisusia sulcata (Rhynchonelliformea: Kutorginata), lateral view; d, d – Magellania sp. (Rhynchonelliformea: Rhynchonellida): d – dorsal view, e – lateral view. The anal opening of the intestine is marked with red dots, the blind closure of the intestine is marked with a cross.

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8. Fig. 7. Size range of particles found in the digestive tract of the rhynchonelliform brachiopods Hemithiris psittacea and Terebratalia septentrionalis collected at depths of up to 40 m in the photic zone (after McCammon, 1981). The y-axis shows the proportion of detected particles out of the total number of organic particles as a percentage, and the x-axis shows the particle diameter in µm.

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9. Fig. 8. Organization of the brachiopod lophophore: a – cross-section through the lophophore tentacles (after: Kuzmina, Malakhov, 2007); b – cross-section through the brachial axis of the spirolophore (after: Kuzmina et al., 2018, with modifications); c – the predominant role of the internal and external tentacles in the process of accepting and rejecting particles. Designations: bo – brachial axis, bs – brachial fold, vshch – internal tentacles, rl – lateral cilia, ns – external tentacles, pzh – food groove, fr – frontal cilia. Arrows indicate the direction of water flow. The frontal ciliary zone is shown in blue, the lateral zone in green, the abfrontal zone in pink, and the sensitive latero-frontal ciliary cells in yellow.

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10. Fig. 9. Organization of the spirolophore (a) and plectolophore (b) lophophores (cross-section through the shell; after Rudwick, 1970, with modifications). Designations: bo – brachial axis of the lophophore, VP – outflow, VC – ventral valve, VHP – inflow, DS – dorsal valve; arrows indicate the directions of water flow, the excretory chamber is shaded gray, the inflow chamber is yellow.

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11. Fig. 10. Direction of water flow during filtration in a plectolophore lophophore (after Williams et al., 1997, with modifications). Key: bo – brachial axis, lar – lateral arm, mr – medial arm, ol – base of the lophophore, r – mouth; incoming flow is shown by red arrows, outgoing flow – by blue ones.

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12. Fig. 11. Scheme of the proposed mechanism of particle sorting in the spirolophore and plectolophore types of lophophore (according to Rudwick, 1970, with changes): a – entry of a suspension of particles of different sizes into the mantle cavity, b – particle sorting. Large and small particles in the spirolophore enter the internal spirals with equal probability. In the plectolophore, most large particles are retained in the lateral arms. Designations: CP – large particles, FP – small particles, WA – water flow.

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13. Fig. 12. Cross-section through the brachial axis of the spirolophore (a) and plectolophore (b) lophophores (after: Temereva, Kuzmina, 2017; Kuzmina, Temereva, 2018). The internal structure of the tentacles is not shown. Designations: ac – abfrontal side, intr – internal tentacles, lf – lateral cilia, ns – external tentacles, fs – frontal side.

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14. Fig. 13. Morphology of the digestive system of brachiopods (after Nielsen, 1991, with modifications): a – Hemithiris psittacea (Rhynchonelliformea: Rhynchonellida), blindly closed intestine with a dilation at the end (original diagram); b – Rhynchonelliformea: Terebratulida, blindly closed intestine without dilation (original diagram); c – Novocrania anomala (Craniiformea), the intestine is through and opens through the anus on the posterior side of the body (after Chuang, 1960); d – Lingula anatina (Linguliformea), U-shaped through intestine opens through the anus into the mantle cavity to the right of the mouth (after Chuang, 1959). The mouth and pharynx are marked in orange, the esophagus is marked in yellow, the stomach is marked in green, the digestive gland is marked in red, the pyloric section is marked in blue, and the posterior section of the intestine is marked in purple. The arrows point to the mouth opening, and the dots indicate the anus of the intestine.

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15. Fig. 14. Features of the microscopic anatomy of the intestinal tube of the rhynchonellid Hemithiris psittacea (according to Punin, 1981, with changes): a – ultrastructure of cells of the blind expansion of the pyloric section, b – ultrastructure of digestive cells of the digestive gland, c – ultrastructure of secretory cells of the digestive gland, g – cross-section through the middle part of the pyloric section of the intestine, d – cross-section of the blind expansion of the pyloric section. The boundaries of the cells in Figs. g, d are not indicated. Designations: ag – Golgi apparatus, azpc – apical zone of vesicles and tubules, bm – basement membrane, bp – basal plate, vac – vacuole, vacm – invaginations of apical cytoplasmic membrane, gl – lipofuscin granule, d – desmosome, kn – rootlet thread, l – lipid inclusion, MV – microvilli, mit – mitochondrion, mo – muscular sheath, pp – pinocytotic vesicle, ppo – lumen of the pyloric region, pcr – lumen of the blind expansion of the pyloric region, p – cilium, sg – secretory granule, e – epithelium, n – nucleus, n – nucleolus.

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16. Fig. 15. Hypothesis of the evolution of rhynchonelliform brachiopods.

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