Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-26T19:35:12.909Z Has data issue: false hasContentIssue false
  • English
  • Français

When conifers took flight: a biomechanical evaluation of an imperfect evolutionary takeoff

Published online by Cambridge University Press:  12 March 2015

Robert A. Stevenson ,
Dennis Evangelista  and
Cindy V. Looy
Robert A. Stevenson
Affiliation:
Department of Integrative Biology, University of California, Berkeley, 3060 Valley Life Sciences Building #3140, Berkeley, California 94720, U.S.A.
Dennis Evangelista
Affiliation:
Department of Integrative Biology, University of California, Berkeley, 3060 Valley Life Sciences Building #3140, Berkeley, California 94720, U.S.A.
Cindy V. Looy
Affiliation:
Department of Integrative Biology and Museum of Paleontology, University of California, Berkeley, 3060 Valley Life Sciences Building #3140, Berkeley, California 94720, U.S.A. E-mail: [email protected].
Get access Rights & Permissions [Opens in a new window]

Abstract

Manifera talaris, a voltzian conifer from the late early to middle Permian (ca. 270 Ma) of Texas, is the earliest known conifer to produce winged seeds indicative of autorotating flight. In contrast to autorotating seeds and fruits of extant plants, the ones of M. talaris are exceptional in that they have variable morphology. They bore two wings that produced a range of wing configurations, from seeds with two equal-sized wings to single-winged specimens, via various stages of underdevelopment of one of the wings. To examine the effects of various seed morphologies on aerodynamics and dispersal potential, we studied the flight performance of paper models of three morphotypes: symmetric double-winged, asymmetric double-winged, and single-winged. Using a high-speed camera we identified the mode of descent (plummeting, gliding, autorotation) and quantified descent speed, autorotation frequency, and other flight characteristics. To validate such modeling as an inferential tool, we compared descent of extant analogues (kauri; Agathis australis) with descent of similarly constructed seed models. All three seed morphotypes exhibited autorotating flight behavior. However, double-winged seeds, especially symmetric ones, failed to initiate slow autorotative descent more frequently than single-winged seeds. Even when autorotating, symmetric double-winged seeds descend faster than asymmetric double-winged ones, and descent is roughly twice as fast compared to single-winged seeds. Moreover, the relative advantage that (effectively) single-winged seeds have in slowing descent during autorotation becomes larger as seed weight increases. Hence, the range in seed wing configurations in M. talaris produced a wide variation in potential dispersal capacity. Overall, our results indicate that the evolutionarily novel autorotating winged seeds must have improved conifer seed dispersal, in a time when animal vectors for dispersion were virtually absent. Because of the range in wing configuration, the early evolution of autorotative flight in conifers was a functionally imperfect one, which provides us insight into the evolutionary developmental biology of autorotative seeds in conifers.

Type
Featured Article
Information
Paleobiology , Volume 41 , Issue 2 , March 2015 , pp. 205 - 225
Copyright
Copyright © 2015 The Paleontological Society. All rights reserved. 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Augspurger, C. K. 1986. Morphology and dispersal potential of wind-dispersed diaspores of neotropical trees. American Journal of Botany 73:353–363.Google Scholar
Azuma, A., and Okuno, Y.. 1987. Flight of a samara, Alsomitra macrocarpa. Journal of Theoretical Biology 129:263–274.Google Scholar
Azuma, A., and Yasuda, K.. 1989. Flight performance of rotary seeds. Journal of Theoretical Biology 138:23–53.Google Scholar
Benkman, C. W. 1995. Wind dispersal capacity of pine seeds and the evolution of different seed dispersal modes in pines. Oikos 73:221–224.Google Scholar
Bergman, N. M., Lenton, T. M., and Watson, A. L.. 2004. COPSE: a new model of biogeochemical cycling over Phanerozoic time. American Journal of Science 304:397–437.Google Scholar
Berner, R. A. 2009. GEOCARBSULF: Phanerozoic atmospheric oxygen: new results using the GEOCARBSULF model. American Journal of Science 309:603–606.Google Scholar
Burrows, F. M. 1975. Wind-borne seed and fruit movement. New Phytologist 75:405–418.CrossRefGoogle Scholar
Call, V. B., and Dilcher, D. L.. 1997. The fossil record of Eucommia (Eucommiaceae) in North America. American Journal of Botany 84:798–814.Google Scholar
Chaney, D. S., and DiMichele, W. A.. 2007. Paleobotany of the classic redbeds (Clear Fork Group - Early Permian) of North Central Texas. Pp. 357-366 In T. Wong, ed. Proceedings of the XVth International Congress on Carboniferous and Permian Stratigraphy (Utrecht, 10-16 August 2003). Royal Netherlands Academy of Arts and Sciences, Amsterdam.Google Scholar
Childress, S., Vandenberghe, N., and Zhang, J.. 2006. Hovering of a passive body in an oscillating airflow. Physics of Fluids 18:117103.Google Scholar
Clark, J. S. 1998. Why trees migrate so fast: confronting theory with dispersal biology and the paleorecord. American Naturalist 152:204–224.Google Scholar
Clement-Westerhof, J. A. 1984. Aspects of Permian palaeobotany and palynology. IV. The conifer Ortiseia Florin from the Val Gardena Formation of the Dolomites and Vicentinian Alps (Italy) with special reference to a revised concept of the Walchiaceae (Göppert) Schimper. Review of Palaeobotany and Palynology 41:51–166.CrossRefGoogle Scholar
Clement-Westerhof, J. A 1987. Aspects of Permian paleobotany and palynology, VII. The Majonicaceae, a new family of Late Permian conifers. Review of Palaeobotany and Palynology 52:375–402.CrossRefGoogle Scholar
Clement-Westerhof, J. A 1988. Morphology and phylogeny of Palaeozoic conifers. Pp. 298–337in C. Beck, ed. Origin and evolution of gymnosperms. Columbia University Press, New York.Google Scholar
DiMichele, W. A., Mamay, S. H., Chaney, D. S., Hook, R. W., and Nelson, J. W.. 2001. An Early Permian flora with Late Permian and Mesozoic affinities from north-central Texas. Journal of Paleontology 75:449–460.Google Scholar
DiMichele, W. A., Tabor, N. J., Chaney, D. S., and Nelson, W. J.. 2006. From wetlands to wet spots: environmental tracking and the fate of Carboniferous elements in the Early Permian tropical floras. In S. F. Greb and W. A. DiMichele, eds. Wetlands through time. Geological Society of America Special Paper 399: 223–248.Google Scholar
Dudley, R. 1998. Atmospheric oxygen, giant Paleozoic insects, and the evolution of aerial locomotor performance. Journal of Experimental Biology 201:1043–1050.Google Scholar
Dudley, R., and Chai, P.. 1996. Animal flight mechanics in physically variable gas mixtures. Journal of Experimental Biology 199:1881–1885.Google Scholar
Dudley, R., Byrnes, G., Yanoviak, S. P., Borrell, B., Brownand, R. M., and McGuire, J. A.. 2007. Gliding and the functional origins of flight: biomechanical novelty or necessity? Annual Review of Ecology, Evolution, and Systematics 38:179–201.Google Scholar
Eckenwalder, J. E. 2009. Conifers of the world. Timber, Portland, Ore.Google Scholar
Eriksson, O., Friis, E. M., and Löfgren, P.. 2000. Seed size, fruit size, and dispersal systems in angiosperms from the Early Cretaceous to the Late Tertiary. American Naturalist 156:47–58.Google Scholar
Escapa, I., Iglesias, A., Wilf, P., and Cuneo, N.. 2013. Oldest macrofossil record of Agathis (Araucariaceae), early Paleocene of Patagonia, Argentina, and its evolutionary significance. Botanical Society of America 2013 Meeting, New Orleans, Louisiana, Abstracts, p. 378.Google Scholar
Evangelista, D. J. 2013. Aerial righting, directed aerial descent, and maneuvering in the evolution of flight in birds. Ph.D. thesis. University of California, Berkeley.Google Scholar
Evangelista, D., Hotton, S., and Dumais, J.. 2011. The mechanics of explosive dispersal and self-burial in the seeds of the filaree, Erodium cicutarium (Geraniaceae). Journal of Experimental Biology 214:521–529.Google Scholar
Evangelista, D., Cam, S., Huynh, T., Krivitskiy, I., and Dudley, R.. 2014a. Ontogeny of aerial righting and wing flapping in juvenile birds. Biology Letters 10:20140497.Google Scholar
Evangelista, D., Cam, S., Huynh, T., Kwong, A., Mehrabani, H., Tse, K., and Dudley, R.. 2014b. Shifts in stability and control effectiveness during evolution of Paraves support aerial maneuvering hypotheses for flight origins. PeerJ 2:e632.Google Scholar
Farjon, A. 1990. Pinaceae. Koeltz Scientific Books, Koenigstein, Germany.Google Scholar
Farjon, A 2005. A monograph of Cupressaceae and Sciadopitys. Royal Botanic Gardens, Kew.Google Scholar
Farjon, A 2010. A handbook of the world’s conifers. Brill Academic, Leiden, the Netherlands.CrossRefGoogle Scholar
Givnish, T. J. 1980. Ecological constraints on the evolution of breeding systems in seed plants: dioecy and dispersal in gymnosperms. Evolution 34:959–972.Google Scholar
Graham, J. B., Dudley, R., Aguilar, N. M., and Gans, C.. 1995. Implications of the late Palaeozoic oxygen pulse for physiology and evolution. Nature 375:117–120.Google Scholar
Green, D. S. 1980. The terminal velocity and dispersal of spinning samaras. American Journal of Botany 67:1218–1224.CrossRefGoogle Scholar
Greene, D. F., and Johnson, E. A.. 1989. A model of wind dispersal of winged or plumed seeds. Ecology 70:339–347.Google Scholar
Greene, D. F., and Johnson, E. A.. 1990. The aerodynamics of plumed seeds. Functional Ecology 4:117–125.Google Scholar
Greene, D. F., and Johnson, E. A.. 1992. Can the variation in samara mass and terminal velocity on an individual plant affect the distribution of dispersal distances? American Naturalist 139:825–838.Google Scholar
Greene, D. F., and Johnson, E. A.. 1993. Seed mass and dispersal capacity in wind-dispersed diaspores. Oikos 67:69–74.Google Scholar
Greene, D. F., and Quesada, M.. 1992. Seed size, dispersal, and aerodynamic constraints within the Bombacaceae. American Journal of Botany 92:998–1005.CrossRefGoogle Scholar
Hedrick, T. L., Cheng, B., and Deng, X.. 2009. Wingbeat time and the scaling of passive rotational damping in flapping flight. Science 324:252–255.Google Scholar
Horn, H. S., Nathan, R., and Kaplan, S. R.. 2001. Long-distance dispersal of tree seeds by wind. Ecological Research 16:877–885.Google Scholar
Howe, H. F., and Miriti, M. N.. 2004. When seed dispersal matters. Bioscience 54:651–660.Google Scholar
Howe, H. F., and Smallwood, J.. 1982. Ecology of seed dispersal. Annual Review of Ecology and Systematics 13:201–228.Google Scholar
Hughes, L., Dunlop, M., French, K., Leishman, M. R., Rice, B., Rodgerson, L., and Westoby, M.. 1994. Predicting dispersal spectra: a minimal set of hypotheses based on plant attributes. Journal of Ecology 82:933–950.Google Scholar
Kerp, J. H. F., Poort, R. J., Swinkels, H. A. J. M., and Verwer, R.. 1990. Aspects of Permian palaeobotany and palynology. IX. Conifer-dominated Rotliegend floras from the Saar-Nahe Basin (?Late Carboniferous–Early Permian; SW-Germany) with special reference to the reproductive biology of early conifers. Review of Palaeobotany and Palynology 62:205–248.Google Scholar
Kvaček, Z. 2002. Novelties on Doliostrobus (Doliostrobaceae), an extinct conifer genus of the European Palaeogene. Časopis Národního Muzea 171:131–175.Google Scholar
Labandeira, C. C. 2002. The history of associations between plants and animals. Pp. 26–74, 248–261 In C. Herrera, and O. Pellmyr, eds. Plant-animal interactions: an evolutionary approach, Blackwell Science, Oxford, England.Google Scholar
Lentink, D., Dickson, W. B., van Leeuwen, J. L., and Dickinson, M. H.. 2009. Leading-edge vortices elevate lift of autorotating plant seeds. Science 324:1438–1440.CrossRefGoogle ScholarPubMed
Leslie, A. B. 2011. Shifting functional roles and the evolution of conifer pollen producing and seed-producing cones. Paleobiology 37:587–602.Google Scholar
Leslie, A. B., Beaulieu, J. M., Crane, P. R., and Donoghue, M. J.. 2013. Explaining the distribution of breeding and dispersal syndromes in conifers. Proceedings of the Royal Society B 280:20131812. doi:10.1098/rspb.2013.1812 [Epub ahead of print].Google Scholar
Levin, S. A., Muller-Landau, H. C., Nathan, R., and Chave, J.. 2003. The ecology and evolution of seed dispersal: a theore tical perspective. Annual Review of Ecology, Evolution, and Systematics 34:575–604.Google Scholar
Looy, C. V. 2007. Extending the range of derived Late Paleozoic conifers: Lebowskia gen. nov. (Majonicaceae). International Journal of Plant Sciences 168:57–972.Google Scholar
Looy, C. V., and Stevenson, R. A.. 2014. Earliest occurrence of autorotating seeds in conifers: the Permian (Kungurian-Roadian) Manifera talaris gen. et sp. nov. International Journal of Plant Sciences 175:841–854.Google Scholar
McCay, M. G. 2003. Winds under the rain forest canopy: the aerodynamic environment of gliding tree frogs. Biotropica 35:94–102.Google Scholar
McCutchen, C. W. 1977. The spinning rotation of Ash and Tulip Tree samaras. Science 197:691–692.Google Scholar
Meijering, O. D., and Smal, I.. 2012. Methods for cell and particle tracking. Methods in Enzymology 504:182–200.Google Scholar
Minami, S., and Azuma, A.. 2003. Various flying modes of wind-dispersal in seeds. Journal of Theoretical Biology 225:1–14.Google Scholar
Mirams, R. V. 1957. Aspects of the natural regeneration of the Kauri (Agathis australis Salish.). Transactions of the Royal Society of New Zealand 84:661–680.Google Scholar
Montañez, I. P., Tabor, N. J., Niemeier, D., DiMichele, W. A., Frank, T. D., Fielding, C. R., Isbell, J. L., Birgenheier, L. P., and Rygel, M. C.. 2007. CO2-forced climate and vegetation instability during Late Paleozoic deglaciation. Science 315:87–91.Google Scholar
Nathan, R., and Muller-Landau, H. C.. 2000. Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends in Ecology and Evolution 15:278–285.CrossRefGoogle ScholarPubMed
Nathan, R., Safriel, U. N., and Noy-Meir, I.. 2001. Field validation and sensitivity analysis of a mechanistic model for tree seed dispersal by wind. Ecology 82:374–388.Google Scholar
Nathan, R., Katul, G. G., Horn, H. S., Thomas, S. M., Oren, R., Avissar, R., Pacala, S. W., and Levin, S. A.. 2002. Mechanisms of long-distance dispersal of seeds by wind. Nature 418:409–413.CrossRefGoogle ScholarPubMed
Nathan, R., Schurr, F. M., Spiegel, O., Steinitz, O., Trakhtenbrot, A., and Tsoar, A.. 2008. Mechanisms of long-distance seed dispersal. Trends in Ecology and Evolution 23:638–647.Google Scholar
Norberg, R. 1973. Autorotation, self-stability, and structure of single-winged fruits and seeds (samaras) with comparative remarks on animal flight. Biological Reviews 48:561–596.Google Scholar
Okubo, A., and Levin, S. A.. 1989. A theoretical framework for data analysis of wind dispersal of seeds and pollen ecology 70: 329–338.Google Scholar
Owens, J. N., Catalano, G. L., and Aitken-Christie, J.. 1997. The reproductive biology of Kauri (Agathis australis). IV. Late embryogeny, histochemistry, cone and seed morphology. International Journal of Plant Science 158:395–407.Google Scholar
Phillips, T. L., and DiMichele, W. A.. 1992. Comparative ecology and life-history biology of arborescent lycopods in Late Carboniferous swamps of Euramerica. Annals of the Missouri Botanical Garden 79:560–588.Google Scholar
R Development Core Team. 2013. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/.Google Scholar
Rothwell, G. W., Mapes, G., and Hernandez-Castillo, G. R.. 2005. Hanskerpia gen. nov. and phylogenetic relationships among the most ancient conifers (Voltziales). Taxon 54:733–750.Google Scholar
Royal Botanic Gardens Kew. 2008. Seed information database (SID), Version 7.1. http://data.kew.org/sid/, accessed September 2013.Google Scholar
Schippers, P., and Jongejans, E.. 2005. Release thresholds strongly determine the range of seed dispersal by wind. Ecological Modeling 185:93–103.Google Scholar
Schulz, C., Knopf, P., and Stützel, T. H.. 2005. Identification key to the Cypress family (Cupressaceae). Feddes Repertorium 116:96–146.CrossRefGoogle Scholar
Sipe, T. W., and Linnerooth, A. R.. 1985. Intraspecific variation in samara morphology and flight behavior in Acer saccharinum (Aceraceae). American Journal of Botany 82:1412–1419.Google Scholar
Soons, M. B., and Bullock, J. M.. 2008. Non-random seed abscission, long-distance wind dispersal and plant migration rates. Journal of Ecology 96:581–590.Google Scholar
Tiffney, B. H. 1986. Evolution of seed dispersal syndromes according to the fossil record. Pp. 273–305in D. R. Murray, ed. Seed dispersal. Academic Press, Sydney.Google Scholar
Tiffney, B. H 2004. Vertebrate dispersal of seed plants through time. Annual Review of Ecology, Evolution, and Systematics 35:1–29.Google Scholar
Tiffney, B. H., and Mazer, S. J.. 1995. Angiosperm growth habit, dispersal and diversification reconsidered. Evolutionary Ecology 9:93–117.Google Scholar
Uhl, D. 2007. Typification of the fossil conifer Pseudovoltzia liebeana (Geinitz) Florin. Taxon 53:185–186.Google Scholar
Van der Pijl, L. 1982. Principles of dispersal in higher plants. Springer, Berlin.Google Scholar
Varshney, K., Chang, S., and Wang, Z. J.. 2012. The kinematics of falling maple seeds and the initial transition to a helical motion. Nonlinearity 25:C1–C8.CrossRefGoogle Scholar
Wardlaw, B. R. 2005. Age assignment of the Pennsylvanian–Early Permian succession of North Central Texas. Permophiles 46:21–22.Google Scholar
Wickham, H. 2009. ggplot2: elegant graphics for data analysis. Springer, New York. http://had.co.nz/ggplot2/book.Google Scholar
Willson, M. F., and Traveset, A.. 2000. The ecology of seed dispersal. Pp. 85–110in M. Fenner, ed. Seeds: the ecology of regeneration in plant communities. CAB International, New York.Google Scholar
Yasuda, K., and Azuma, A.. 1997. The autorotation boundary in the flight of samaras. Journal of Theoretical Biology 185:313–320.Google Scholar
Zeng, Y. 2013. Aerial righting, directed aerial descent and maneuvering in stick insects. Ph.D. thesis. University of California, Berkeley.Google Scholar