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, 16 (3), e2001663
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Late Maastrichtian Pterosaurs From North Africa and Mass Extinction of Pterosauria at the Cretaceous-Paleogene Boundary

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Late Maastrichtian Pterosaurs From North Africa and Mass Extinction of Pterosauria at the Cretaceous-Paleogene Boundary

Nicholas R Longrich et al. PLoS Biol.

Erratum in

Abstract

Pterosaurs were the first vertebrates to evolve powered flight and the largest animals to ever take wing. The pterosaurs persisted for over 150 million years before disappearing at the end of the Cretaceous, but the patterns of and processes driving their extinction remain unclear. Only a single family, Azhdarchidae, is definitively known from the late Maastrichtian, suggesting a gradual decline in diversity in the Late Cretaceous, with the Cretaceous-Paleogene (K-Pg) extinction eliminating a few late-surviving species. However, this apparent pattern may simply reflect poor sampling of fossils. Here, we describe a diverse pterosaur assemblage from the late Maastrichtian of Morocco that includes not only Azhdarchidae but the youngest known Pteranodontidae and Nyctosauridae. With 3 families and at least 7 species present, the assemblage represents the most diverse known Late Cretaceous pterosaur assemblage and dramatically increases the diversity of Maastrichtian pterosaurs. At least 3 families-Pteranodontidae, Nyctosauridae, and Azhdarchidae-persisted into the late Maastrichtian. Late Maastrichtian pterosaurs show increased niche occupation relative to earlier, Santonian-Campanian faunas and successfully outcompeted birds at large sizes. These patterns suggest an abrupt mass extinction of pterosaurs at the K-Pg boundary.

Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. A) Map showing the location of the phosphate mines in Morocco, (B) map showing Sidi Daoui and Sidi Chennane mines, and (C) stratigraphic column for the phosphates of the Sidi Daoui area (after [40]).
Abbreviations: PETM, Paleocene-Eocene Thermal Maximum.
Fig 2
Fig 2. T. regalis FSAC-OB 1, holotype left humerus.
In (A), ventral view, (B) dorsal view, (C) anterior view, (D) distal view, and (E) proximal view. Abbreviations: dpc, deltopectoral crest; ect, ectepicondyle; ent, entepicondyle; lc, lateral condyle; mc, medial condyle; pf, pneumatic fossa/foramen; scpr, supracondylar process; uc, ulnar crest; ut, ulnar tubercle.
Fig 3
Fig 3. T. regalis FSAC-OB 1, deltopectoral crest.
In (A), distal view, (B) apical view, and (C) proximal view. Abbreviations: apx, apex of deltopectoral crest; dis, distal margin of deltopectoral crest; prx, proximal margin of deltopectoral crest; uc, ulnar crest.
Fig 4
Fig 4. cf. T. regalis FSAC-OB 199 and 200, ulnae.
(A) Right ulna FSAC-OB 199 in posterior view; (B) right ulna FSAC-OB 200 in posterior view.
Fig 5
Fig 5. cf. T. regalis FSAC-OB 201 and 201 hindlimb elements.
(A) Right femur FSAC-OB 201 in anterior view; (B) left femur and tibia FSAC-OB 202 in posterior view. Abbreviations: fem, femur; fh, femoral head; gt, greater trochanter; lc, lateral condyle; mc, medial condyle; tib, tibia.
Fig 6
Fig 6. A. elainus FSAC-OB 2, holotype partial skeleton and FSAC-OB 217, metacarpal IV.
(A) Holotype right humerus in anterior view, (B) holotype right ulna and radius in anterior view, respectively, (C) holotype sternum in left lateral view, (D) referred metacarpal IV, (E) holotype, distal end of left metacarpal IV and left scapulocoracoid, and (F) holotype right femur in posterior view. Abbreviations: co, coracoid; cr, cristospine; dc, distal condyle; dpc, deltopectoral crest; ect, ectepicondyle; fh, femoral head; gl, glenoid; gt, greater trochanter; hh, humeral head; hum, humerus; mcIV, metacarpal IV, pc, proximal cotyle; pf, pneumatic foramen; rad, radius; scpr, supracondylar process; ste, sternum; uln, ulna.
Fig 7
Fig 7. A. elainus FSAC-OB 156 mandible.
Abbreviations: dgr, dorsal groove; ocl, occlusal ridge; sym, symphysis.
Fig 8
Fig 8. Alcione FSAC-OB 4, partial right wing.
Humerus in ventral view, ulna and radius in posterior view, and metacarpal IV and phalanx IV-1 in ventral view. Abbreviations: dpc, deltopectoral crest; ect, ectepicondyle; ent, entepicondyle; hum, humerus; lc, lateral condyle; mc, medial condyle; mcIV, metacarpal IV; IV-1, first phalanx of digit IV; rad, radius; uln, ulna.
Fig 9
Fig 9. Alcione FSAC-OB 5, right humerus.
In (A), ventral view, (B) anterior view, (C) dorsal view; (D) distal view, and (E) proximal view. Abbreviations: dpc, deltopectoral crest; ect, ectepicondyle; ent, entepicondyle; hh, humeral head; lc, lateral condyle; mc, medial condyle; msc, muscle scar; uc, ulnar crest, vp, ventral ridge; vt, ventral tubercle.
Fig 10
Fig 10. FSAC-OB 7, holotype right humerus, S. robusta.
In (A), dorsal view, (B) ventral view, and (C) posterior view. Abbreviations: dpc, deltopectoral crest; msc, muscle scar; scpr, supracondylar process of the ectepicondyle; vp, ventral pillar; vt, ventral tubercle of the deltopectoral crest.
Fig 11
Fig 11. FSAC-OB 232, holotype skeleton of B. grandis.
(A) Left humerus in anterior view, (B) right femur in anterior view, (C) right radius and ulna in posterior view, (D) cervical vertebra in ventral view, (E) left scapulocoracoid in medial view, and (F) posterior ramus of the right mandible in medial view. Abbreviations: co, coracoid; cot, cotyle of mandible; cvr, cervical ribs; dm, dorsal margin of mandible; dpc, deltopectoral crest; gl, glenoid; fh, femoral head; gt, greater trochanter; hh, humeral head; hyp, hypapophysis; olp, olecranon process; pex, postexapophysis; pn, pneumatopore; rad, radius; sca, scapula; scp, supracondylar process of the ectepicondyle; uc, ulnar crest; uln, ulna; vm, ventral margin of mandible.
Fig 12
Fig 12. FSAC-OB 8, right humerus of B. grandis.
In (A), ventral view, (B) dorsal view, and (C) anterior view. Abbreviations: dpc, deltopectoral crest; hh, humeral head; uc, ulnar crest; pf, pneumatic foramen; vp, ventral pillar; vt, ventral tubercle.
Fig 13
Fig 13. FSAC-OB 12 P. mauritanicus cervical vertebra.
In (A), dorsal view, (B) ventral view, (C) left lateral view; (D) anterior view; (E) posterior view. Abbreviations: cot, cotyle; hyp, hypapophysis; nsp, neural spine; pex, postexapophysis; poz, postzygapophysis; prz, prezygapophysis.
Fig 14
Fig 14. FSAC-OB 14, aff. Quetzalcoatlus cervical vertebra.
In (A), dorsal view, (B) ventral view; (C), left lateral view, and (D), anterior view. Abbreviations: dlr, dorsolateral ridge; hyp, hypapophysis; nsp, neural spine; pex, postexapophysis; poz, postzygapophysis; prz, prezygapophysis; pzl, prezygapophyseal laminae; vfo, ventral fossa.
Fig 15
Fig 15. FSAC-OB 203, giant azhdarchid (?Arambourgiania) ulna.
Middle shaft and distal end of the left ulna, in posterior view. Abbreviations: ut, ulnar tubercle; vp, ventral process.
Fig 16
Fig 16. Time-calibrated phylogenetic analysis.
Tree showing placement of T. regalis, A. elainus, S. robusta, B. grandis, P. mauritanicus, and aff. Quetzalcoatlus. Maximum parsimony analysis of the character-taxon matrix (S1 Data) recovered 4 most parsimonious trees with length 1,126.651 (consistency index = 0.336, retention index = 0.793). Divergence dates are set at 1 Ma, and ranges show the resolution of stratigraphic dating.
Fig 17
Fig 17. Diversity curve showing taxic (raw) diversity and phylogenetic (with ghost lineages) diversity of pterosaurs over time (millions of years ago [MYA]).
Late Cretaceous taxic diversity remains relatively steady up to the Cretaceous–Paleogene (K-Pg) boundary following the mid-Cretaceous diversity drop. The slight decrease in phylogenetic diversity in the Late Cretaceous is the expected result of the Signor-Lipps Effect: ghost taxa cannot be inferred for the Late Maastrichtian because no post-Cretaceous pterosaurs exist to create ghost lineages; here phylogenetic diversity equals taxic diversity. Abbreviations: Tr-J, Triassic-Jurassic; J-K, Jurassic-Cretaceous.
Fig 18
Fig 18. Late Cretaceous pterosaur functional diversity.
Santonian-Campanian (blue) versus Maastrichtian (red) functional diversity, based on principal coordinates analysis of habitat, wingspan, jaw shape, and limb proportions (S2 Data). Axis 1 accounts for 54.4% of variation; axis 2, 11.2%; axis 3, 4.5%; axis 4, 3.0%, axis 5, 1.9%; axis 6, 1.4%; and axis 7, 1%.
Fig 19
Fig 19. Resampling of functional diversity.
Rarefaction of sum of ranges for the Maastrichtian (red) and Santonian-Campanian (blue), showing mean functional diversity (A) and 95% confidence intervals (B).
Fig 20
Fig 20. Size disparity of late Maastrichtian pterosaurs and birds.
Maastrichtian pterosaurs are larger than coeval birds in both marine (blue) and terrestrial/freshwater (orange) ecosystems. Wingspan estimates for pterosaurs are from S2 Data. Wingspans for terrestrial birds were made using estimated masses from Longrich et al. [74] and the equation for passeriformes from Norberg [75] or from reconstructions based on fossils [76,77].

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Grant support

Research was supported by a Leverhulme Trust Research Leadership award to NRL. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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