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Rapid recovery of Patagonian plant–insect associations after the end-Cretaceous extinction

The Southern Hemisphere may have provided biodiversity refugia after the Cretaceous/Palaeogene (K/Pg) mass extinction. However, few extinction and recovery studies have been conducted in the terrestrial realm using well-dated macrofossil sites that span the latest Cretaceous (late Maastrichtian) and early Palaeocene (Danian) outside western interior North America (WINA). Here, we analyse insect-feeding damage on 3,646 fossil leaves from the latest Maastrichtian and three time slices of the Danian in Chubut, Patagonia, Argentina (palaeolatitude approximately 50° S). We test the southern refugial hypothesis and the broader hypothesis that the extinction and recovery of insect herbivores, a central component of terrestrial food webs, differed substantially from WINA at locations far south of the Chicxulub impact structure in Mexico. We find greater insect-damage diversity in Patagonia than in WINA during both the Maastrichtian and Danian, indicating a previously unknown insect richness. As in WINA, the total diversity of Patagonian insect damage decreased from the Cretaceous to the Palaeocene, but recovery to pre-extinction levels occurred within approximately 4 Myr compared with approximately 9 Myr in WINA. As for WINA, there is no convincing evidence for survival of any of the diverse Cretaceous leaf miners in Patagonia, indicating a severe K/Pg extinction of host-specialized insects and no refugium. However, a striking difference from WINA is that diverse, novel leaf mines are present at all Danian sites, demonstrating a considerably more rapid recovery of specialized herbivores and terrestrial food webs. Our results support the emerging idea of large-scale geographic heterogeneity in extinction and recovery from the end-Cretaceous catastrophe.

a–l, Latest Cretaceous samples from the Lefipán Formation (a–c), and early Palaeocene samples8 from the Salamanca (d–i) and Peñas Coloradas (j–l) formations. a, Multiple, overlapping blotch mines containing centralized frass (DT299) on leaf morphotype LEF28 (LefW; MPEF-Pb 4776). b, Spheroidal galls with striated surfaces (DT303) on LEF2 (LefE; MPEF-Pb 4259). c, Margin feeding with thickened reaction tissue (DT12) on LEF23 (LefL; MPEF-Pb 4758). d, Serpentine mine with spheroidal terminal chamber (DT300) on Cissites patagonica (PL1; MPEF-Pb 6557). e, Elliptical gall positioned on the primary vein at the intersection with secondary veins (DT84) on Laurophyllum piatnitzkyi (PL1; MPEF-Pb 6555). f, Row of parallel-sided holes near the leaf margin (DT64) on Dryophyllum australis (PL1; MPEF-Pb 6560). g, Spheroidal galls with distinct outer rims positioned on the primary vein (DT117) of Cissites patagonica (PL2; MPEF-Pb 6567). h, Concentric rings of piercing and sucking marks surrounded by dark reaction tissue (DT118) on SA19 (PL2; MPEF-Pb 4072). i, Hole feeding surrounded by a wide rim of blotched reaction tissue (DT113) on SA43 (PL2; MPEF-Pb 6561). j, Serpentine mines that transition to blotch mines with internal, intestiniform trails (DT301) on Fagophyllum duseni (LF; MPEF-Pb 6547). k, Elongate, curvilinear patches of skeletonized tissue (DT20) on SA70 (LF; MPEF-Pb 6549). l, Deeply incised margin feeding damage (DT15) on Dryophyllum australis (LF; MPEF-Pb 6546). DT, damage type27 (new DTs defined in Supplementary Discussion).

a–l, Latest Cretaceous samples from the Lefipán Formation (a–c), and early Palaeocene samples8 from the Salamanca (d–i) and Peñas Coloradas (j–l) formations. a, Multiple, overlapping blotch mines containing centralized frass (DT299) on leaf morphotype LEF28 (LefW; MPEF-Pb 4776). b, Spheroidal galls with striated surfaces (DT303) on LEF2 (LefE; MPEF-Pb 4259). c, Margin feeding with thickened reaction tissue (DT12) on LEF23 (LefL; MPEF-Pb 4758). d, Serpentine mine with spheroidal terminal chamber (DT300) on Cissites patagonica (PL1; MPEF-Pb 6557). e, Elliptical gall positioned on the primary vein at the intersection with secondary veins (DT84) on Laurophyllum piatnitzkyi (PL1; MPEF-Pb 6555). f, Row of parallel-sided holes near the leaf margin (DT64) on Dryophyllum australis (PL1; MPEF-Pb 6560). g, Spheroidal galls with distinct outer rims positioned on the primary vein (DT117) of Cissites patagonica (PL2; MPEF-Pb 6567). h, Concentric rings of piercing and sucking marks surrounded by dark reaction tissue (DT118) on SA19 (PL2; MPEF-Pb 4072). i, Hole feeding surrounded by a wide rim of blotched reaction tissue (DT113) on SA43 (PL2; MPEF-Pb 6561). j, Serpentine mines that transition to blotch mines with internal, intestiniform trails (DT301) on Fagophyllum duseni (LF; MPEF-Pb 6547). k, Elongate, curvilinear patches of skeletonized tissue (DT20) on SA70 (LF; MPEF-Pb 6549). l, Deeply incised margin feeding damage (DT15) on Dryophyllum australis (LF; MPEF-Pb 6546). DT, damage type27 (new DTs defined in Supplementary Discussion).

Palaeontological evidence from both continental and marine deposits suggests that the Southern Hemisphere may have harboured biodiversity refugia in the wake of the bolide impact at Chicxulub, Mexico, 66.0 Myr ago (Ma)1,2,3,4. The extinction rate of Southern Hemisphere nannoplankton was lower than that of their Northern Hemisphere counterparts, and their populations recovered nearly immediately2. Nominally Mesozoic plant groups, including corystosperms and bennettitaleans, survived until at least the Palaeogene in Australia1,5. Palynological data from New Zealand revealed a sudden but short-lived disturbance, with low overall extinction rates6,7. In Patagonia, Argentina, palynomorphs from the latest Maastrichtian–early Danian Lefipán Formation exhibited low extinction, followed by the reappearances of Cretaceous pollen types3. Early Danian macrofloras from the Salamanca Formation in Patagonia are more diverse than comparable North American Palaeocene floras8,9,10. A number of surviving lineages from other plant3 and vertebrate11,12groups have also been identified, especially in Patagonia4, although marine invertebrate faunas in Antarctica underwent severe extinction13. K/Pg boundary sections in New Zealand have provided important insights into the response of terrestrial ecosystems6,7,14,15,16, but until recently there has not been a series of well-dated, heavily sampled continental macrofloral localities anywhere in the Southern Hemisphere that spans both the terminal Cretaceous and earliest Palaeogene.

Plant–insect interactions are fundamental components of terrestrial food webs, and their sensitivity to major environmental perturbations is well known from deep time as well as the modern world17,18,19,20. The diversity of insect-feeding damage on extant leaves in two tropical rainforests is positively correlated with the richness of insects that caused the damage, supporting the widespread use of insect damage on fossil leaves as a proxy for herbivorous insect diversity when suitable insect body fossils are absent21. In North Dakota, USA, insect-damage diversity on fossil leaves, especially specialized feeding such as mining and galling, declined considerably across the K/Pg boundary and remained low throughout WINA before increasing with the latest Palaeocene warming, approximately 9 Myr after the K/Pg boundary17,18,20. The only exception to this pattern is the early Palaeocene (about 65 Ma) Mexican Hat locality in south-eastern Montana, USA, which has typical low-diversity flora but anomalously high insect damage diversity for the time; this pattern is attributed to a short-lived interval of decoupled plant and insect diversity following the K/Pg mass extinction17,20.

Much less is known about the extinction and recovery of insect herbivores outside WINA. Late Palaeocene floras from Colombia are associated with low richness of plants and specialized insect-damage diversity as in Palaeocene WINA22, contrasting with high plant and insect-damage diversity on middle Palaeocene floras from France23 and Spitsbergen24. However, until now, no studies have investigated changes in insect-damage diversity based on terminal Cretaceous and early Palaeocene leaf floras from any non-WINA study area.

Full Text: http://www.nature.com/articles/s41559-016-0012

WFS,World Fossil Society,Riffin T Sajeev,Russel T sajeev

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