ORIGINAL ARTICLE
Seed traits linked to differential survival of plants during the Cretaceous/Paleogene impact winter
| 1 | Science Department, Hoehne Re-3 School District, Hoehne, Colorado, 81046, USA |
Online publication date: 2020-12-30
Publication date: 2020-12-30
Acta Palaeobotanica 2020; 60(2): 307–322
KEYWORDS
ABSTRACT
In past investigations the pattern of differential survival of plants across the K/Pg boundary has
been viewed as incompatible with severe asteroid impact winter scenarios (i.e., an impact winter lasting more
than a few months), particularly the enigmatic survival of coryphoid palms and Pandanus (screw pine). Stateof-
the-art climate models based on soot, sulfate and nano-sized dust aerosols predict a global impact winter
that drastically reduced precipitation and resulted in a transient period of total darkness and permafrost conditions.
This suggests that the plants most likely to have been affected by the global mass-extinction event were
tropical phanerophytes that produce recalcitrant seeds, which by definition are desiccation-intolerant, survive
less than a year, and cannot survive freezing. However, this hypothesis has never been tested. In this study
I sampled over 100 plant species from the global fossil record that have a high probability of having produced
either recalcitrant seeds/disseminules (n1 = 58) or orthodox seeds (n2 = 59), based on their phylogenetic relationships
with extant taxa that either are monomorphic for these traits or specifically exhibit a genetic marker for
abscisic acid inhibition associated with seed dormancy and recalcitrance. A one-tailed z-test for the difference
between two proportions revealed that plant taxa with a high probability of having produced recalcitrant seeds
had significantly lower survivorship than plant taxa with a high probability of having produced orthodox seeds
(p < 0.0001). Based on these data, it can be concluded that plants which formed a frost-tolerant seed bank during
the latest Maastrichtian were significantly more likely to survive the K/Pg impact winter than plants which
did not (including palms). These data clearly indicate that the K/Pg impact winter probably lasted longer than
a year and that it selected for seed-based traits that effectively sorted correlated functional traits of mature
plants (i.e., leaf physiognomic features). This novel hypothesis stands as an alternative to J.A. Wolfe’s classic
hypothesis that a mild K/Pg impact winter selected for fast-growing angiosperms with deciduous leaves and did
not affect the plant communities of the Southern Hemisphere. Potential mechanisms for the rare survival of
tropical, recalcitrant-seeded plants are discussed.
REFERENCES (139)
1.
Alvarez, L.W., Alvarez, W., Asaro, F., Michel, H.V., 1980. Extraterrestrial cause for the Cretaceous-Tertiary extinction. Science 208, 1095–1108.
2.
Alvarez, W., Alvarez, L.W., Asaro, F., Michel, H.V., 1982. Current status of the impact theory for the terminal Cretaceous extinction. GSA Special Paper 190, 305–315.
3.
Andruchow-Colombo, A., Escapa, I.H., Cúneo, N.R., Gandolfo, M.A., 2018. Araucaria lefipanensis (Araucariaceae), a new species with dimorphic leaves from the Late Cretaceous of Patagonia, Argentina. American Journal of Botany 105, 1–21.
4.
Ash, S.R., Tidwell, W.D., 1976. Upper Cretaceous and Paleocene floras of the Raton Basin, Colorado and New Mexico. In: Ewing, R.C., and Kues, B.C. (eds) New Mexico Geological Society 27th Field Conference Guidebook. New Mexico Geological Society, Socorrow, pp. 197–203.
5.
Barbour, J.R., 2008. Serenoa repens (Bartr.) Small. In: Bonner, F.T., Karrfait, R.P. (eds) The Woody Plant Seed Manual, 1039–1042.
6.
Barclay, R.S., Johnson, K.R., Betterton, W.J., Dilcher, D.L., 2003. Stratigraphy and megaflora of a K/T boundary section in the eastern Denver Basin, Colorado: Rocky Mountain Geology 3, 45–71.
7.
Bardeen, C.G., Garcia, R.R., Toon, O.B., Conley, A.A., 2017. On transient climate change at the Cretaceous-Paleogene boundary due to atmospheric soot injections. Proceedings of the National Academy of Sciences USA 114, 7415–7424.
8.
Barreda, V.D., Cúneo, N.R., Wilf, P., Currano, E.D., Scasso, R.A., Brinkhuis, H., 2012. Cretaceous/Paleogene floral turnover in Patagonia: drop in diversity, low extinction, and a Classopollis spike. PLoSONE 7, 1–8.
9.
Berry, E.W., 1922. Additions to the flora of the Wilcox Group. USGS Professional Paper 91, 1–20.
10.
Berry, K., 2018a. Paleontological evidence against a major geographic barrier at about the paleolatitude of Colorado, USA, during the Late Campanian (Late Cretaceous): the conspicuous absence of endemic subclades of chasmosaurine ceratopsid (horned) dinosaurs and its significance. The Mountain Geologist 55, 5–18.
11.
Berry, K., 2018b. Icacinaceae in the early middle Paleocene Raton Formation, Colorado. The Mountain Geologist 55, 75–86.
12.
Berry, K., 2019a. Linking fern foliage with spores at the K/Pg boundary section in the Sugarite coal zone, New Mexico, USA, while questioning the orthodoxy of the global pattern of plant succession across the K/Pg boundary. Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen 291, 159–169.
13.
Berry, K., 2020. A thelypteridaceous fern from the early Paleocene Raton Formation, south-central Colorado, and its importance in interpreting the climate of the region. The Mountain Geologist 57, 5–20.
14.
Berry, K., in press. The first plants to recolonize western North America following the Cretaceous/Paleogene (K/Pg) mass-extinction event. International Journal of Plant Sciences 182. DOI: https://doi.org/10.1086/711847.
15.
Blonder, B., Royer, D.L., Johnson, K.R., Miller, I., Enquist, B.J., 2014. Plant ecological strategies shift across the Cretaceous-Paleogene boundary. PLoSONE 12, 1–7.
16.
Bowen, M.R., Whitmore, T.C., 1980. A second look at Agathis. CFI Occasional Paper 13, Commonwealth Forestry Institute, Oxford, pp. 1–19.
17.
Britton, M.R., Watkins, J.E., Jr., 2016. The economy of reproduction in dimorphic ferns. Annals of Botany 118, 1139–1149.
18.
Brodribb, T.J., Piterrman, J., Coomes, D.A., 2012. Elegance vs. speed: examining the competition between conifer and angiosperm trees. International Journal of Plant Sciences 173, 673–694.
19.
Brown, R.W., 1962. Paleocene flora of the Rocky Mountains and Great Plains. USGS Professional Paper 375, 1–119.
20.
Brugger, J., Feulner, G., Petri, S., 2017. Baby, it’s cold outside: climate model simulations of the effects of the asteroid impact at the end of the Cretaceous. Geophysical Research Letters 44, 419–427.
21.
Carpenter, K.J., 2005. Stomatal architecture and evolution in basal angiosperms. American Journal of Botany 92, 1595–1615.
22.
Carpenter, W.J., 1987. Temperature and imbibition effects on seed germination of Sabal palmetto and Serenoa repens. Horticulture Science 22, 660–661.
23.
Chanderbali, A.S., Van der Werff, H., Renner, S.S., 2001. Phylogeny and historical biogeography of Lauraceae: evidence from the chloroplast and nuclear genomes. Annals of the Missouri Botanical Gardens 88, 104–134.
24.
Chen, Y.-C., Li, C., Zhao, Y.-X., Gao, M., Wang, J.-Y., Liu, K.-W., Wang, K., Wu, Li.-W., Jiao, Y.-L., Xu, Z.-L., He, W.-G., Zhang, Q.-Y., Liang, C.-K., Hsiao, Y.-Y., Zhang, D.-Y., Lan, S.-R., Huang, L., Xu, W., Tsai, W.-C., Liu, Z.-J., Van de Peer, Y., Wang, D.-W., 2020. The Litsea genome and the evolution of the laurel family. Nature Communications 11, 1–14.
25.
Chin, K., Pearson, D., Ekdale, A.A., 2013. Fossil worm burrows reveal very early terrestrial animal activity and shed light on trophic resources after the end-Cretaceous mass extinction. PLoSONE 8, 1–8.
26.
Chiarenza, A.A., Farnsworth, A., Mannion, P.D., Lunt, D.J., Valdes, P.J., Morgan, J.V., Allison, P.A., 2020. Asteroid impact, not volcanism, caused the end-Cretaceous dinosaur extinction. Proceedings of the National Academy of Sciences, USA, 117, 17084–17093.
27.
Christopher, R.A., Prowell, D.C., 2002. A palynological biozonation for the Maastrichtian Stage (Upper Cretaceous) of South Carolina, USA. Cretaceous Research 23, 639–669.
28.
Clarke, R.T., 1963. Palynology of the Vermejo Formation coals (Upper Cretaceous) in the Cañon City coal field, Fremont County, Colorado. Ph.D. Thesis, University of Oklahoma.
29.
Clout, M.N., Tilley, J.A.V., 1992. Germination of miro (Prumnopitys ferruginea) seeds after consumption by New Zealand pigeons (Hemiphaga novaeseelandiae). New Zealand Journal of Botany 30, 25–28.
31.
Davies, R., Pritchard, H., 1998. Seed storage and germination of the palms Hyphaene thebaica, H. petersiana and Medemia argun. Seed Science and Technology 26, 823–828.
32.
Denk, T., Oh, I.-C., 2006. Phylogeny of Schisandraceae based on morphological data: evidence from modern plants and the fossil record. Plant Systematics and Evolution 256, 113–145.
33.
Dickie, J.B., Smith, R.D., 1995. Observations on the survival of seeds of Agathis spp. stored at low moisture contents and temperatures. Seed Science Research 5, 5–14.
34.
Dickie, J.B., Pritchard, H.W., 2002. Systematic and evolutionary aspects of desiccation tolerance in seeds. In: Black, M., Pritchard, H.W. (eds) Desiccation and Survival in Plants: Drying without Dying. CABI Publications, New York, pp. 239–260.
35.
Dickie, J.B., Balick, M.J., Linington, I.M., 1993. Studies on the practicality of ex situ preservation of palm seeds. Principes 37, 94–98.
36.
Dorf, E., 1939. Fossil plants from the Upper Cretaceous Aguja Formation of Texas. American Museum Novitates 1015, 1–9.
37.
Duman, J.G., Olsen, T.M., 1993. Thermal hysteresis protein activity in bacteria, fungi, and phylogenetically diverse plants. Cryobiology 30, 322–328.
38.
Ellis, R.H., Hong, T.D., Roberts, E.H., 1990. An intermediate category of seed storage behaviour? I. COFFEE. Journal of Experimental Botany 41, 1167–1174.
39.
El-Soughier, M.I., Mehrotra, R.C., Zhou, Z.-Y., Shi G., 2019. Nypa fruits and seeds from the Maastrichtian-Danian sediments of Bir Abu Minqar, South Western Desert, Egypt. Palaeoworld 20, 75–83.
40.
Escapa, I.H., Iglesias, A., Wilf, P., Catalano, S.A., Caraballo-Ortiz, M.A., Cúneo, N.R., 2018. Agathis trees of Patagonia’s Cretaceous-Paleogene death landscapes and their evolutionary significance. American Journal of Botany 105, 1345–1368.
41.
Farnsworth, E., 2000. The ecology and physiology of viviparous and recalcitrant seeds. Annual Review of Ecology and Systematics, 107–138.
42.
Field, D.J., Bercovici, A., Berv, J.S., Dunn, R., Fastovsky, D.E., Lyson, T.R., Vajda, V., Gauthier, J.A., 2018. Early evolution of modern birds structured by global forest collapse at the end-Cretaceous mass extinction. Current Biology 28, 1–7.
43.
Franchi, G.G., Piotto, B., Nepi, M., Baskin, C.C., Baskin, J.M., Pacini, E., 2011. Pollen and seed desiccation tolerance in relation to degree of developmental arrest, dispersal, and survival. Journal of Experimental Botany 62, 5267–5281.
44.
Frederiksen, N.O., 1980. Sporomorphs from the Jackson Group (Upper Eocene) and adjacent strata of Mississippi and Western Alabama. USGS Professional Paper 1084, 1–75.
45.
Futuyma, D.J., 1989. Speciational trends and the role of species in macroevolution. The American Naturalist 134, 318–321.
46.
Greenwood, D.R., West, C.K., 2016. A fossil coryphoid palm from the Paleocene of western Canada. Review of Palaeobotany and Palynology 239, 55–65.
47.
Greenwood, D.R., Wing, S.L., 1995. Eocene continental climates and latitudinal temperature gradients. Geology 23, 1044–1048.
48.
Harley, M.M., 2006. A summary of fossil records for Arecaceae. Botanical Journal of the Linnean Society 151, 39–67.
49.
Hofmann, P., Steiner, A.M., 1989. An updated list of recalcitrant seeds. Landwirtschaftliche Forschung 42, 310–323.
50.
Hong, T.D., Linington, S., Ellis, R.H., 1997. Seed storage behavior: a compendium. Handbook for Genebanks: No. 4. International Plant Genetic Resources Institute, Rome. 104 p.
51.
Huegele, I.B., Manchester, S.R., 2020. An Early Paleocene carpoflora from the Denver Basin of Colorado, USA, and its implications for plant-animal interactions and fruit size evolution. International Journal of Plant Sciences 181, 646–665.
53.
Iglesias, A., Wilf, P., Johnson, K.R., Zamuner, A.B., Cúneo, N.R., Matheos, S.D., 2007. A Paleocene lowland macroflora from Patagonia reveals significantly greater richness than North American analogs. Geology 35, 947–950.
54.
Iglesias, A., Artabe, A.E., Morel, E.M., 2011. The evolution of Patagonian climate and vegetation from the Mesozoic to the present. Biological Journal of the Linnean Society 103, 409–422.
55.
Jablonski, D., 2008. Species selection: theory and data. Annual Review of Ecology, Evolution, and Systematics 39, 501–524.
56.
Jaganathan, G.K., Li, J., Yang, Y., Han, Y., Liu, B., 2019. Complexities in identifying seed storage behavior of hard seed-coated species: a special focus on Lauraceae. Botany Letters 166, 1–9.
57.
Johnson, K.R., 1996. Description of seven common fossil leaf species from the Hell Creek Formation (Upper Cretaceous: Upper Maastrichtian), North Dakota, South Dakota, and Montana. Proceedings of the Denver Museum of Natural History 3, 1–48.
58.
Johnson, K.R., 2002. Megaflora of the Hell Creek and lower Fort Union Formations in the western Dakotas: Vegetational response to climate change, the Cretaceous-Tertiary boundary event, and rapid marine transgression. GSA Special Paper 361, 329–391.
59.
Johnson, K.R., Reynolds, M.L., Werth, K.W., Thomasson, J.R., 2003. Overview of the Late Cretaceous, early Paleocene, and early Eocene megafloras of the Denver Basin, Colorado. Rocky Mountain Geology 38, 101–120.
60.
Jud, N.A., Gandolfo, M.A., Iglesias, A., Wilf, P., 2018. Fossil flowers from the early Paleocene, Argentina, with affinity to Schizomerieae (Cunoniaceae). Annals of Botany 121, 431–442.
61.
Kauffman, E.G., Upchurch, G.R., Nichols, D.J., 1990. The Cretaceous-Tertiary boundary interval at south table mountain, near Golden, Colorado. In: Kauffman, E.G., Walliser, O.H. (eds) Extinction Events in Earth History. Lecture Notes in Earth Sciences, vol 30. Springer, Berlin, Heidelberg., pp. 365–392.
62.
Knowlton, F.H., 1930. The flora of the Denver and associated formations of Colorado. USGS Professional Paper 155, 1–142.
63.
Lee, W.T., Knowlton, F.H., 1917. Geology and paleontology of the Raton Mesa and other regions, Colorado and New Mexico. USGS Professional Paper, 101, 1–435.
64.
Leppe, M., Mihoc, M., Varela, N., Stinnesbeck, W., Mansilla, H., Bierma, H., Cisterna, K., Frey, E., Jujihara, T., 2012. Evolution of the Austral-Antarctic flora during the Cretaceous: new insights from a paleobiogeographic perspective. Revista Chilena de Historia Natural 85, 369–392.
65.
Lesquereux, L., 1873. Lignitic formation and fossil flora. In: Hayden F.V. (ed.) Sixth annual report of the United States Geological Survey of the Territories: Part II. Special reports on geology and paleontology, pp. 315–428.
66.
Li, L., Li, J., Rohwer, J.G., Van Der Werff, H., Wang, Z.-H., and Li, H.-W., 2011. Molecular phylogenetic analysis of the Persea group (Lauraceae) and its biogeographic implications on the evolution of tropical and subtropical amphi-Pacific disjunctions. American Journal of Botany 98, 1520–1536.
67.
Lloyd, R.M., Klekowski, E.J., 1970. Spore germination and viability in Pteridophyta: evolutionary significance of chlorophyllous spores. Biotropica 2, 129–137.
68.
Lyson, T.R., Miller, I.M., Bercovici, A.D., Weissenburger, K., Fuentes, A.J., Clyde, W.C., Hagadorn, J.W., Butrim, M.J., Johnson, K.R., Fleming, R.F., Barclay, R.S., MacCracken, S.A., Lloyd, B., Wilson, G.P., Krause, D.W., Chester, S.G.B., 2019. Exceptional continental record of biotic recovery after the Cretaceous/Paleogene mass extinction. Science 366, 977–983.
69.
Manchester, S.R., 2014. Revisions to Roland Brown’s North American Paleocene flora. Acta Musei Nationalis Pragae, Series B – Historia Naturalis 70, 153–210.
70.
Manchester, S.R., Lehman, T.M., Wheeler, E.A., 2010. Fossil palms (Arecaceae, Coryphoideae) associated with juvenile herbivorous dinosaurs in the Upper Cretaceous Aguja Formation, Big Bend National Park, Texas. International Journal of Plant Sciences 171, 679–689.
71.
Matsunaga, K.K.S., Manchester, S.R., Srivastava, R., Kapgate, D.K., Smith, S.Y., 2019. Fossil palm fruits from India indicate a Cretaceous origin of Arecaceae tribe Borasseae. Botanical Journal of the Linnean Society 190, 260–280.
72.
McIver, E.E., 1999. Paleobotanical evidence for ecosystem disruption at the Cretaceous-Tertiary boundary from Wood Mountain, Saskatchewan, Canada. Canadian Journal of Earth Sciences 36, 775–789.
73.
Morgan, J., Artemieva, N., Goldin, T., 2013. Revisiting wildfires at the K-Pg boundary. JGR Geosciences 118, 1508–1520.
74.
Morris, A.B., Bell, C.D., Clayton, J.W., Judd, W.S., Soltis, D.E., Soltis, P.S., 2007. Phylogeny and divergence time estimation in Illicium with implications for New World biogeography. Systematic Botany 32, 236–249.
75.
Nichols, D.J., Brown, J.L., 1992. Palynostratigraphy of the Tullock Member (lower Paleocene) of the Fort Union Formation in the Powder River Basin, Montana and Wyoming. USGS Bulletin 1917, 35 p.
76.
Nichols, D.J., Johnson, K.R., 2002. Palynology and microstratigraphy of Cretaceous-Tertiary boundary sections in southwestern North Dakota. GSA Special Paper 361, 95–143.
77.
Nichols, D.J., Jarzen, D.M., Orth, C.J., Oliver, P.Q., 1986. Palynological and iridium anomalies at Cretaceous-Tertiary boundary, south-central Saskatchewan. Science 231, 714–717.
78.
Nie, Z.-L., Wen, J., Sun, H., 2007. Phylogeny and biogeography of Sassafras (Lauraceae) disjunct distributions between eastern Asia and eastern North America. Plant Systematics and Evolution 267, 191–203.
79.
Noblick, L.R., Tucker Lima, J.M., Valdes, I.R., 2018. Nypa fruits in the Western Atlantic: potential for recolonization? Palms 62, 175–184.
80.
Offord, C.A., Porter, C.L., Meagher, P.F., Errington, G., 1999. Sexual reproduction and early plant growth of the Wollemi Pine (Wollemia nobilis), a rare and threatened Australian conifer. Annals of Botany 84, 1–9.
81.
Olson, D.F. Jr., Barnes, R.L., Karrfalt, R.P., 2008. Sabal palmetto. In: Bonner, F.T., Karrfalt, R.P. (eds) The Woody Plant Seed Manual. USDA, Washington, D.C., pp. 997–999.
82.
Orozco-Segovia, A., Batis, A.I., Rojas-Aréchiga, M., Mendoza, A., 2003. Seed biology of palms: a review. Palms 47, 79–94.
83.
Orth, C.J., Gilmore, J.S., Knight, J.D., Pillmore, C.L., Tschudy, R.H., Fassett, J.E., 1981. An Ir abundance anomaly at the palynological Cretaceous-Tertiary boundary in northern New Mexico. Science 214, 1341–1343.
84.
Pillmore, C.L., Nichols, D.J., Fleming, R.F., 1999. Field guide to the continental Cretaceous-Tertiary boundary in the Raton Basin, Colorado and New Mexico. GSA Field Guides 1, 135–155.
85.
Pole, M., 2008. The record of Araucariaceae macrofossils in New Zealand. Alcheringa 32, 405–426.
86.
Pole, M., Vajda, V., 2009. A new terrestrial Cretaceous-Paleogene site in New Zealand – turnover in macroflora confirmed by palynology. Cretaceous Research 30, 917–938.
87.
Poole, I., Cantrill, D.J., 2006. Cretaceous and Cenozoic vegetation of Antarctica integrating the fossil wood record. Geological Society of London Special Publication 258, 63–82.
88.
Raymer, J.D., 2010. Cretaceous/Paleogene boundary biostratigraphy and palynofacies of the Alo-1 well, southeastern Nigeria. M.S. Thesis, Missouri University of Science and Technology, 67 p.
89.
Raymond, A., Phillips, M.K., Gennett, J.A., Comet, P.A., 1997. Palynology and paleoecology of lignites from the Manning Formation (Jackson Group) outcrop in the Lake Somerville spillway of east-central Texas. International Journal of Coal Geology 34, 195–223.
90.
Reichgelt, T., West, C.K., Greenwood, D.R., 2018. The relation between global palm distribution and climate. Scientific Reports 8, 1–11.
91.
Renne, P.R., Arenillas, I., Arz, J.A., Vajda, V., Gilabert, V., Bermúdez, H.D., 2018. Multi-proxy record of the Chicxulub impact at the Cretaceous-Paleogene boundary from Gorgonilla Island, Colombia. Geology 46, 547–550.
92.
Roberts, E.H., 1973. Predicting the storage life of seeds. Seed Science and Technology 1, 499–514.
93.
Robertson, D.S., Lewis, W.M., Sheehan, P.M., Toon, O.B., 2013. K-Pg extinction patterns in marine and freshwater environments: the impact winter model. Journal of Geophysical Research: Biogeosciences 118, 1006–1014.
94.
Romero, E., Amenábar, C.R., Zamaloa, M.C., Concheyro, A., 2019. Nothofagus and the associated palynoflora from the Late Cretaceous of Vega Island, Antarctica Peninsula. Polish Polar Research 40, 227–253.
95.
Rothwell, G.W., Stockey, R.A., 1991. Onoclea sensibilis in the Paleocene of North America, a dramatic example of structural and ecological stasis. Review of Palaeobotany and Palynology 70, 113–124.
96.
Royer, D.L., Sack, L., Wilf, P., Lusk, C.H., Jordan, G.H., Niinemets, U., Wright, I.J., Westoby, M., Cariglino, B., Coley, P.D., Cutter, A.D., Johnson, K.R., Labandeira, C.C., Moles, A.T., Palmer, M.B., Valladares, F., 2007. Fossil leaf economics quantified: calibration, Eocene case study, and implications. Paleobiology 33, 574–589.
97.
Sato, T., 1982. Adaptation to cold climate of ferns native to Hokkaido with reference to the alternation of generations. In: Li, P.H., Sakai, A. (eds) Plant Cold Hardiness and Freezing Stress: Mechanisms and Crop Implications 2, Academic Press, Inc., New York, pp. 447–458.
98.
Shen-Miller, J., 2002. Sacred lotus, the long-living fruits of China Antique. Seed Science Research 12, 131–143.
99.
Shen-Miller, J., Mudgett, M.B., Schopf, J.W., Clarke, S., Berger, R., 1995. Exceptional seed longevity and robust growth: ancient Sacred Lotus from China. American Journal of Botany 82, 1367–1380.
100.
Smiskova, A., Vlasinova, H., Havel, L., 2005. Somatic embryogenesis from zygotic embryos of Schisandra chinensis. Biologia Plantarum 49, 451–454.
101.
Snedaker, S.C., Getter, C.D., 1985. Coasts: coastal resources management guidelines. USDI, 205 p.
102.
Spicer, R.A., 1989. Plants at the Cretaceous-Tertiary boundary (and discussion). Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences 325, 291–305.
103.
Spicer, R.A., Collinson, M.E., 2014, Plants and floral change at the Cretaceous-Paleogene boundary: three decades on. GSA Special Paper 505, 117–132.
104.
Srivastava, R., Srivastava, G., Dilcher, D.L., 2014. Coryphoideae palm leaf fossils from the Maastrichtian-Danian of central India with remarks on the phytogeography of the Coryphoideae (Arecaceae). PLoSONE 9, 1–10.
105.
Stiles, E., Wilf, P., Iglesias, A., Gandolfo, M.A., Cúneo, N.R., 2020. Cretaceous-Paleogene plant extinction and recovery in Patagonia. Paleobiology 47, 1–25.
106.
Stone, J.F., 1973. Palynology of the Almond Formation (Upper Cretaceous) Rock Springs Uplift, Wyoming. Bulletins of American Paleontology 64, 1–136.
107.
Su, T., Farnsworth, A., Spicer, R.A., Huang, J., Wu, F.-X., Liu, J., Li, S.-F., Wing, Y.-W., Huang, Y.-J., Deng, W.-Y.-D., Tang, H., Xu, C.-L., Zhao, F., Srivastava, G., Valdes, P.J., Deng, T., Zhou, Z.-K., 2019. No high Tibetan Plateau until the Neogene. Science Advances 5, 1–8.
108.
Subbiah, A., Ramdhani, S., Pammenter, N.W., Macdonald, A.H.H., Sershen, 2019. Towards understanding the incidence and evolutionary history of seed recalcitrance: an analytical review. Perspectives in Plant Ecology, Evolution, and Systematics 37, 11–19.
109.
Tabor, C.R., Bardeen, C.G., Otto-Bliesner, B.L., Garcia, R.R., Toon, O.B., 2020. Causes and climatic consequences of the impact winter at the Cretaceous-Paleogene Boundary. Geophysical Research Letters 47, 1–10.
110.
Takahashi, M.K., Horner, L.M., Kubota, T., Keller, N.A., Abrahamson, W.G., 2011. Extensive clonal spread and extreme longevity in saw palmetto, a foundation clonal plant. Molecular Ecology 18, 3730–3742.
111.
Tiffney, B.H., Manchester, S.R., 2001. The use of geological and paleontological evidence in evaluating phylogeographic hypotheses in the Northern Hemisphere Tertiary. International Journal of Plant Sciences 162, S3–S17.
112.
Tommasi, F., Paciolla, C., de Pinto, M.C., Gara, L.D., 2006. Effects of storage temperature on viability, germination and antioxidant metabolism in Ginkgo biloba L. seeds. Plant Physiology and Biochemistry 44, 359–368.
113.
Toon, O.B., Pollack, J.B., Ackerman, T.P., Turco, R.P., McKay, C.P., Liu, M.S., 1982. Evolution of an impact-generated dust cloud and its effects on the atmosphere. GSA Special Paper 190, 187–200.
114.
Tredici, P.D., 1992. Natural regeneration of Ginkgo biloba from downward growing cotyledonary buds (basal chichi). American Journal of Botany 79, 522–530.
115.
Tschudy, R.H., 1970. Two new pollen genera (Late Cretaceous and Paleocene) with possible affinity to the Illiciaceae. USGS Professional Paper 643-F, 1–13.
116.
Tschudy, R.H., Tschudy, B.D., 1986. Extinction and survival of plant life following the Cretaceous/Tertiary boundary event, Western Interior, North America. Geology 14, 667–670.
117.
Tschudy, R.H., Pillmore, C.L., Orth, C.J., Gillmore, J.S., Knight, J.D., 1984. Disruption of the terrestrial plant ecosystem at the Cretaceous-Tertiary boundary, Western Interior. Science 225, 1030–1032.
118.
Tweddle, J.C., Dickie, J.B., Baskin, C.C., Baskin, J.M., 2003. Ecological aspects of seed desiccation sensitivity. Journal of Ecology 91, 294–304.
119.
Upchurch, G.R., Jr., 1995. Dispersed angiosperm cuticles: their history, preparation, and application to the rise of angiosperms in Cretaceous and Paleocene coals, southern Western Interior of North America. International Journal of Coal Geology 28, 161–227.
120.
Upchurch, G.R., Jr., Askin, R.A., 1990. Latest Cretaceous and earliest Tertiary dispersed plant cuticles from Seymour Island, Antarctica. Antarctic Journal of the U.S. (1989 Review) 24, 7–10.
121.
Upchurch, G.R., Jr., Lomax, B.H., Beerling, D.J., 2007. Paleobotanical evidence for climate change across the Cretaceous-Tertiary boundary, North America: 20 years after Wolfe and Upchurch. Cour Forsch-Inst Senckenberg 258, 57–74.
122.
Vajda, V., Bercovici, A., 2012. Pollen and spore stratigraphy of the Cretaceous-Paleogene mass-extinction interval in the Southern Hemisphere. Stratigraphy 36, 153–164.
123.
Vajda, V., Bercovici, A., 2014. The global vegetation pattern across the Cretaceous-Paleogene mass extinction interval: a template for other mass extinction events. Global and Planetary Change 122, 29–49.
124.
Vajda, V., McLoughlin, S., 2004, Fungal proliferation at the Cretaceous-Tetiary boundary. Science 303, 1489.
125.
Vajda, V., McLoughlin, S., 2007, Extinction and recovery patterns of vegetation across the Cretaceous-Paleogene boundary – a tool for unraveling the causes of the end-Permian mass extinction. Review of Palaeobotany and Palynology 144, 99–112.
126.
Vajda, V., Ocampo, A., Ferrow, E., Bender Koch, C., 2015. Nanoparticles as the primary cause for longterm sunlight suppression at high southern latitudes following the Chicxulub impact. Gondwana Research 27, 1079–1088.
127.
Vallati, P., Sosa Tomas, A.D., Casal, G., 2020. A Maastrichtian terrestrial palaeoenvironment close to the K/Pg boundary in the Golfo San Jorge basin, Patagonia, Argentina. Journal of South American Earth Sciences 97, 1–11.
128.
Villegente, M., Marmey, P., Job, C., Galland, M., Cueff, G., Godin, B., Rajou, L., Balliau, T., Zivy, M., Fogliani, B., Sarramegna-Burtet, V., Job, D., 2017. A combination of histological, physiological, and proteomic approaches shed light on seed desiccation tolerance of the basal angiosperm Amborella trichopoda. Proteomes 5, 1–16.
129.
Vrba, E.S., Gould, S.J., 1986. The hierarchical expansion of sorting and selection: sorting and selection cannot be equated. Paleobiology 12, 217–228.
130.
Whitmore, T.C., 1980. Utilization, potential, and conservation of Agathis, a genus of tropical Asian conifers. Economic Botany 34, 1–12.
131.
Wilf, P., Johnson, K.R., 2004. Land plant extinction at the end of the Cretaceous: a quantitative analysis of the North Dakota megafloral record. Paleobiology 30, 347–368.
132.
Wilf, P., Johnson, K.R., Huber, B.T., 2003. Correlated terrestrial and marine evidence for global climate changes before mass extinction at the Cretaceous-Paleogene boundary. PNAS 100, 599–604.
133.
Wolfe, J.A., 1975. Some aspects of plant geography of the Northern Hemisphere during the Late Cretaceous and Tertiary. Annals of the Missouri Botanical Garden 62, 264–279.
134.
Wolfe, J.A., 1987. Late Cretaceous-Cenozoic history of deciduousness and the terminal Cretaceous event. Paleobiology 13, 215–226.
135.
Wolfe, J.A., 1997. Relations of environmental change to angiosperm evolution during the Late Cretaceous and Tertiary. In: Iwatsuki, K., Raven, P.H. (eds) Evolution and the Diversification of Land Plants. Springer-Verlag, Tokyo, pp. 269–290.
136.
Wolfe, J.A., Upchurch, G.R., Jr., 1987. Leaf assemblages across the Cretaceous-Tertiary boundary in the Raton Basin, New Mexico and Colorado. Proceedings of the National Academy of Sciences, USA 84, 5096–5100.
137.
Wood, C.B., Vautier, H.J., Bin, W., Rakotondranony, L.G., Pritchard, H.W., 2006. Conservation biology for seven palm species from diverse genera. Aliso 22, 278–284.
138.
Wyse, S.V., Dickie, J.B., 2017. Predicting the global incidence of seed desiccation sensitivity. Journal of Ecology 107, 1082–1093.
139.
Zona, S., 1990. A monograph of Sabal. Aliso: A Journal of Systematic and Evolutionary Botany 12, 583–666.
CITATIONS (2):
1.
No Consistent Shift in Leaf Dry Mass per Area Across the Cretaceous—Paleogene Boundary
Matthew Butrim, Dana Royer, Ian Miller, Marieke Dechesne, Nicole Neu-Yagle, Tyler Lyson, Kirk Johnson, Richard Barclay
Frontiers in Plant Science
Matthew Butrim, Dana Royer, Ian Miller, Marieke Dechesne, Nicole Neu-Yagle, Tyler Lyson, Kirk Johnson, Richard Barclay
Frontiers in Plant Science
2.
Was the K/Pg boundary Classopollis ‘spike’ a singular event? A review of global palynological records suggests otherwise, with potentially broad implications
Keith Berry
Rocky Mountain Geology
Keith Berry
Rocky Mountain Geology
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