Growth form evolution in Piperales and its Relevance for understanding angiosperm diversification: An integrative approach combining plant architecture, anatomy, and biomechanics

International Journal of Plant Sciences

Volumn 173, Issue 6, 2012, Pages 610-639

  Isnard, Sandrine ^a,b   Prosperi, Juliana ^c   Wanke, Stefan ^b   Wagner, Sarah T ^b   Samain, Marie Stéphanie ^d   Trueba, Santiago ^a   Frenzke, Lena ^b   Neinhuis, Christoph ^b   Rowe, Nick P ^e,f  

^a INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^c CIRAD   (France)

^d GHENT UNIVERSITY   (Belgium)

^e UNIV MONTPELLIER   (France)

^f CNRS   (France)

Author keywords

Anatomy; Architecture; Biomechanics; Evolution; Growth form; Piperales

Indexed keywords

ANATOMY; BIOMECHANICS; CLIMBING PLANT; DICOTYLEDON; EPIPHYTE; GROWTH FORM; HERB; MORPHOLOGY; PHYLOGENY; PLANT ARCHITECTURE; RHIZOME; SHRUB; SPECIES DIVERSITY; SPECIES RICHNESS;

ARISTOLOCHIACEAE; MAGNOLIIDAE; MAGNOLIIDS; MAGNOLIOPHYTA; PIPERACEAE; PIPERALES; SARUMA; SAURURACEAE;

EID: 84862122227     PISSN: 10585893     EISSN: None     Source Type: Journal    
DOI: 10.1086/665821     Document Type: Review

References (122)

1. Barthélémy D, Y Caraglio 2007 Plant architecture: a dynamic, multilevel and comprehensive approach to plant form, structure and ontogeny. Ann Bot 99:375-407.
2. Barthélémy D, C Edelin, F Hallé 1989 Architectural concepts for tropical trees. Pages 89-100 in LB Holm-Nielsen, H Balslev, eds. Tropical forests: botanical dynamics, speciation and diversity. Academic Press, London.
3. Barthélémy D, C Edelin, F Hallé 1991 Canopy architecture. Pages 1-20 in A Raghavendra, ed. Physiology of trees. Wiley, Chichester.
4. Bateman RM 1994 Evolutionary-developmental change in the growth architecture of fossil rhizomorphic lycopsids: scenarios constructed on cladistic foundations. Biol Rev 69:527-597.
5. Bateman RM, PR Crane, WA DiMichele, PR Kenrick, NP Rowe, T Speck, WE Stein 1998 Early evolution of land plants: phylogeny, physiology, and ecology of the primary terrestrian radiation. Annu Rev Ecol Syst 29:263-292.
6. Bateman RM, WA DiMichele 1994 Saltational evolution of form in vascular plants: a neoGoldschmidtian synthesis. Pages 63-102 in DS Ingram, A Hudson, eds. Shape and form in plants and fungi. Academic Press, London.
7. Blanc P 1986 Edification d'arbres par croissance d'établissement de type monocotyledonien: L'exemple de Chloranthaceae. Colloque international sur l'arbre, Montpellier, France, 9-14 septembre. Nat Monspel Vol h.s.:101-123.
8. Blanc P, K Andraos 1983 Remarques sur la dynamique de croissance dans le genre Piper L. (Piperaceoe) et les genres affines. Bull Mus Natl Hist Nat Sect B Adansonia 5:259-282.
9. Blanc P, K Andraos 1984 Remarques sur la dynamique de croissance dans le genre Peperomia Ruiz & Pau. (Piperaceae). Bull Mus Natl Hist NatSect B Adansonia 6:41-56.
10. Boyce CK, TJ Brodribb, TS Feild, MA Zwieniecki 2009 Angiosperm leaf vein evolution was physiologically and environmentally transformative. Proc R Soc B 276:1771-1776.
11. Brodribb TJ, TS Feild 2010 Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification. Ecol Lett 13:175-183.
12. Busch S, R Seidel, O Speck, T Speck 2010 Morphological aspects of self-repair of lesions caused by internal growth stresses in stems of Aristolochia macrophylla and Aristolochia ringens. Proc R Soc B 277:2113-2120.
13. Carlquist S 1990 Wood anatomy and relationships of Lactoridaceae. Am J Bot 77:1498-1505.
14. Carlquist S 1991 Anatomy of vine and liana stems: a review and synthesis. Pages 53-71 in FE Putz, HA Mooney, eds. The biology of vines. Cambridge University Press, Cambridge.
15. Carlquist S 1993 Wood and bark anatomy of Aristolochiaceae: systematic and habital correlations. IAWA J 14:341-357.
16. Carlquist S 1995 Wood and stem anatomy of Saururaceae with reference to ecology, phylogeny, and origin of the monocotyledons. IAWA J 16:133-150.
17. Carlquist S 1999 Wood and bark anatomy of Schisandraceae: implications for phylogeny, habit, and vessel evolution. Aliso 18:45-55.
18. Carlquist S 2009 Xylem heterochrony: an unappreciated key to angiosperm origin and diversifications. Bot J Linn Soc 161:26-65.
19. Carlquist S, EL Schneider 2009 Do tracheid microstructure and the presence of minute crystals link Nymphaeaceae, Cabombaceae and Hydatellaceae? Bot J Linn Soc 159:572-582.
20. Carlquist S, EL Schneider, CB Hellquist 2009 Xylem of early angiosperms: Nuphar (Nymphaeaceae) has novel tracheid microstructure. Am J Bot 96:207-215.
21. Civeyrel L, NP Rowe 2001 Phylogenetic relationships of Secamonoideae based on the plastid gene matK, morphology and biomechanics. Ann Mo Bot Gard 88:583-602.
22. Coiffard C, B Gomez, J Kvacek, F Thevenard 2006 Early angiosperm ecology: evidence from the Albian-Cenomanian of Europe. Ann Bot 98:495-502.
23. Coiffard C, B Gomez, F Thevenard 2007 Early Cretaceous angiosperm invasion of western Europe and major environmental changes. Ann Bot 100:545-553.
24. Cremers G 1973 Architecture de quelques lianes d'Afrique Tropicale. Candollea 28:249-280.
25. Cremers G 1974 Architecture de quelques lianes d'Afrique Tropicale (2). Candollea 29:57-110.
26. Debray F 1885 Etude comparative des caractères anatomiques et du parcours des faisceaux fibro-vasculaires des Pipéracées. Thèse de Doctorat d'Etat. Faculté des Sciences de Paris, France.
27. Dickison WC 1992 Morphology and anatomy of the flower and pollen of Saruma henryi Oliv., a phylogenetic relict of the Aristolochiaceae. Bull Torrey Bot Club 119:392-400.
28. Dickison WC 1996 Stem and leaf anatomy of Saruma henryi Oliv., including observations on raylessness in the Aristolochiaceae. Bull Torrey Bot Club 123:261-267.
29. Edelin C 1984 L'architecture monopodiale: l'exemple de quelques arbres d'Asie tropicale. Thèse de doctorat d'Etat. Université Montpellier 2, France.
30. Edelin C 1991 Nouvelles données sur l'architecture des arbres sympodiaux: le concept de plan d'organisation. Pages 127-154 in C. Edelin, ed. Colloque international sur l'arbre, Montpellier, France, 10-15 septembre. Nat Monspel Vol h.s. A7.
31. Eiten G 1991 What is a herb? Veroeff Geobot Inst Zurich 106:288-304.
32. Feild TS, NC Arens 2005 Form, function and environments of the early angiosperms: merging extant phylogeny and ecophysiology with fossils. New Phytol 166:383-408.
33. Feild TS, NC Arens 2007 The ecophysiology of early angiosperms. Plant Cell Environ 30:291-309.
34. Feild TS, NC Arens, JA Doyle, TE Dawson, MJ Donoghue 2004 Dark and disturbed: a new image of early angiosperm ecology. Paleobiology 30:82-107.
35. Feild TS, TJ Brodribb, T Jaffré, NM Holbrook 2001 Acclimation of leaf anatomy, photosynthetic light use, and xylem hydraulics to light in Amborella trichopoda (Amborellaceae). Int J Plant Sci 162: 999-1008.
36. Feild TS, DS Chatelet, L Balun, EE Schilling, R Evans 2012 The evolution of angiosperm lianescence without vessels-climbing mode and wood structure-function in Tasmannia cordata (Winteraceae). New Phytol 193:229-240.
37. Feild TS, DS Chatelet, TJ Brodribb 2009 Ancestral xerophobia: a hypothesis on the whole plant ecophysiology of early angiosperms. Geobiology 7:237-264.
38. Feild TS, PJ Franks, TL Sage 2003 Ecophysiological shade adaptation in the basal angiosperm, Austrobaileya scandens (Austrobaileyaceae). Int J Plant Sci 164:313-324.
39. Feild TS, PJ Hudson, L Balun, DS Chatelet, AA Patino, CA Sharma, K McLaren 2011a The ecophysiology of xylem hydraulic constraints by ''basal'' vessels in Canella winterana (Canellaceae). Int J Plant Sci 172:879-888.
40. Feild TS, GR Upchurch, DS Chatelet, TJ Brodribb, KC Grubbs, M-S Samain, S Wanke 2011b Fossil evidence for low gas exchange capacities for Early Cretaceous angiosperm leaves. Paleobiology 37: 195-213.
41. Friis EM, P Crane 2007 Botany: new home for tiny aquatics. Nature 446:269-270.
42. Frodin DG 2004 History and concepts of big plant genera. Taxon 53: 753-776.
43. Gentry AG 1991 The distribution and evolution of climbing plants. Pages 73-97 in FE Putz, HA Mooney, eds. The biology of vines. Cambridge University Press, Cambridge.
44. González F 1999a Inflorescence morphology and the systematics of Aristolochiaceae. Syst Geogr Plants 68:159-172.
45. González F 1999b A phylogenetic analyses of the Aristolochioideae (Aristolochiaceae). PhD diss. City University of New York.
46. González F, P Rudall 2001 The questionable affinities of Lactoris: evidence from branching pattern, inflorescence morphology, and stipule development. Am J Bot 88:2143-2150.
47. Gould SJ, ES Vrba 1982 Exaptation: a missing term in the science of form. Palaeobiology 8:4-15.
48. Hacke UG, JS Sperry, TS Feild, Y Sano, EH Sikkema, J Pittermann 2007 Water transport in vesselless angiosperms: conducting efficiency and cavitation safety. Int J Plant Sci 168:1113-1126.
49. Hallé F 2004 Architecture des plantes. JPC Edition, Palavas-les-Flots, 162 pp.
50. Hallé F, P Danton, C Perrier 2007 Architectures de plantes de l'Île Robinson Crusoe, archipel Juan Fernández, Chili. Adansonia, sér 3, 29:333-350.
51. Hallé F, RAA Oldeman 1970 Essai sur l'architecture et la dynamique de croissance des arbres tropicaux. Masson, Paris.
52. Hallé F, RAA Oldeman, PB Tomlinson 1978 Tropical trees and forests: an architectural analysis. Springer, New York. 441 pp.
53. Heywood VH, RK Brummitt, A Culham, O Seberg 2007 Flowering plants families of the world. Royal Botanic Gardens, Kew. 424 pp.
54. Holttum RE 1955 Growth-habits of monocotyledons: variations on a theme. Phytomorphology 5:399-413.
55. Hou D 1981 Florae Malesianae praecursores LXII on the genus Thottea (Aristolochiaceae). Blumea 27:301-332.
56. Hudson PJ, J Razanatsoa, TS Feild 2010 Early vessel evolution and the diversification of wood function: insights from Malagasy Canellales. Am J Bot 97:80-93.
57. Isnard S, T Speck, NP Rowe 2003 Mechanical architecture and development in different growth forms of Clematis: implications for canalised evolution of growth forms. New Phytol 158:543-559.
58. Jansen RK, Z Cai, LA Raubeson, H Daniell, CW dePamphilis, J Leebens-Mack, KF Muller, et al 2007 Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proc Natl Acad Sci USA 104: 19369-19374.
59. Jaramillo MA, R Callejas-Posada 2004 A reappraisal of Trianaeopiper Trelease: convergence of dwarf habit in some Piper species of the Chocó. Taxon 53:269-278.
60. Jaramillo MA, R Callejas-Posada, C Davidson, J Smith, A Stevens, E Tepe 2008 A phylogeny of the tropical genus Piper using ITS and the chloroplast intron psbJ-petA. Syst Bot 33:647-660.
61. Jaramillo MA, PS Manos 2001 Phylogeny and patterns of floral diversity in the genus Piper (Piperaceae). Am J Bot 88:706-716.
62. Judd WS, CS Campbell, EA Kellogg, PF Stevens, MJ Donoghue 2002 Plant systematic: a phylogenetic approach. Sinauer, Sunderland, MA. 576 pp.
63. Kelly LM 1998 Phylogenetic relationships in Asarum (Aristolochiaceae) based on morphology and ITS sequences. Am J Bot 85:1454-1467.
64. Kwiatkowska D 1999 Formation of pseudowhorls in Peperomia verticillata (L.) A. Dietr. shoots exhibiting various phyllotactic patterns. Ann Bot 83:675-685.
65. Lahaye R, L Civeyrel, T Speck, NP Rowe 2005 Evolution of shrublike growth forms in the lianoid subfamily Secamonoideae (Apocynaceae s.l.) of Madagascar: phylogeny, biomechanics, and development. Am J Bot 92:1381-1396.
66. Levinton J 1988 Genetics, palaeontology and macroevolution. Cambridge University Press, Cambridge.
67. Mabberley DJ 2009 Mabberley's plant-book: a portable dictionary of plants, their classifications, and uses. Cambridge University Press, Cambridge.
68. Maddison WP, DR Maddison 2011 Mesquite: a modular system for evolutionary analysis. Version 2.75. http://mesquiteproject.org.
69. Magallón S, A Castillo 2009 Angiosperm diversification through time. Am J Bot 96:349-365.
70. Martínez-Colín MA, EM Engleman, SD Koch 2006 Contribution al conocimiento de Peperomia (Piperaceae): fruto y semilla. Bol Soc Bot Mex 78:83-94.
71. Masselter T, NP Rowe, J Galtier, T Speck 2009 Secondary growth and deformation of stem tissues in the Lower Carboniferous seed fern Calamopitys. Int J Plant Sci 170:1228-1239.
72. Masselter T, NP Rowe, T Speck 2007 Biomechanical reconstruction of the carboniferous seed fern Lyginopteris oldhamia: implications for growth form reconstruction and habit. Int J Plant Sci 168:1177-1189.
73. Masselter T, T Speck 2008 Quantitative and qualitative changes in primary and secondary stem organization of Aristolochia macrophylla during ontogeny: functional analysis and experiments. J Exp Bot 59:2955-2967.
74. Mathieu G, L Symmank, R Callejas, S Wanke, C Neinhuis, P Goetghebeur, M-S Samain 2011 New geophytic Peperomia (Piperaceae) species from Mexico, Belize and Costa Rica. Rev Mex Biodivers 82:357-382.
75. Metcalfe CR, L Chalk 1979 Anatomy of the dicotyledons. Oxford University Press, New York.
76. Moore MJ, CD Bell, PS Soltis, DE Soltis 2007 Using plastid genomescale data to resolve enigmatic relationships among basal angiosperms. Proc Natl Acad Sci USA 104:19363-19368.
77. Mori SA, G Cremers, CA Gracie, JJ De Granville, SV Heald, M Hoff, JD Mitchell 2002 Guide to the vascular plants of central French Guiana. New York Botanical Garden Press, New York. 775 pp.
78. Musselman LJ, LJ Visser 1986 The strangest plant in the world! Veld Flora 71:109-111.
79. Neinhuis C, S Wanke, KW Hilu, K Muller, T Borsch 2005 Phylogeny of Aristolochiaceae based on parsimony, likelihood, and Bayesian analyses of trnL-trnF sequences. Plant Syst Evol 250:7-26.
80. Nickrent DL, A Blarer, Y-L Qiu, DE Soltis, PS Soltis, M Zanis 2002 Molecular data place Hydnoraceae with Aristolochiaceae. Am J Bot 89:1809-1817.
81. Niklas KJ 1989 Mechanical behavior of plant tissues as inferred from the theory of pressurized celllular solides. Am J Bot 76:929-937.
82. Niklas KJ 1992 Plant biomechanics: an engineering approach to plant form and function. University of Chicago Press, Chicago. 607 pp.
83. Niklas KJ 1997 The evolutionary biology of plants. University of Chicago Press, Chicago. 449 pp.
84. Niklas KJ 2000 The evolution of plant body plans: a biomechanical perspective. Ann Bot 85:411-438.
85. Oelschlagel B, S Wagner, K Salomo, NS Pradeep, TL Yao, S Isnard, NP Rowe, C Neinhuis, S Wanke 2011 Implications from molecular phylogenetic data for systematics, biogeography and growth form evolution of Thottea (Aristolochiaceae). Gard Bull 63:259-275.
86. Oldeman RAA 1974 L'architecture de la forêt guyanaise. Office de la Recherche Scientifique et Technique Outre-Mer, Paris. 204 pp.
87. Qiu Y-L, J Lee, F Bernasconi-Quadroni, DE Soltis, PS Soltis, M Zanis, EA Zimmer, Z Chen, V Savolainen, MW Chase 1999 The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes. Nature 402:404-407.
88. Quijano-Abril MA, R Callejas-Posada, DR Miranda-Esquivel 2006 Areas of endemism and distribution patterns for Neotropical Piper species (Piperaceae). J Biogeogr 33:1266-1278.
89. Ravindran PN, AB Remashree 1998 Anatomy of Piper colubrinum link. J Spices Aromat Crops 7:111-123.
90. Rowe NP, S Isnard, F Gallenmuller, T Speck 2006 Diversity of mechanical architectures in climbing plants: an ecological perspective. Pages 35-59 in A Herrel, T Speck, NP Rowe, eds. Ecology and biomechanics: a mechanical approach to the ecology of animals and plants. CRC, Boca Raton, FL.
91. Rowe NP, T Speck 2005 Plant growth forms: an ecological and evolutionary perspective. New Phytol 166:61-72.
92. Rowe NP, T Speck, J Galtier 1993 Biomechanical analysis of a Palaeozoic gymnosperm stem. Proc R Soc B 252:19-28.
93. Samain M-S 2008 Tackling Pandora's box: order out of chaos in the giant genus Peperomia. PhD Biology. Universiteit Gent.
94. Samain M-S, G Mathieu, P Guillermo, L Symmank, N Cieza, C Neinhuis, P Goetghebeur, S Wanke 2011 The geophytic Peperomia subgenus Tildenia (Piperaceae) in the Andes with the description of new species in a phylogenetic framework. Plant Ecol Evol 144:148-176.
95. Samain M-S, L Vanderschaeve, P Chaerle, P Goetghebeur, C Neinhuis, S Wanke 2009a Erratum: is morphology telling the truth about the evolution of the species rich genus Peperomia (Piperaceae)? Plant Syst Evol 280:251-254.
96. Samain M-S, L Vanderschaeve, P Chaerle, P Goetghebeur, C Neinhuis, S Wanke 2009b Is morphology telling the truth about the evolution of the species rich genus Peperomia (Piperaceae)? Plant Syst Evol 278: 1-21.
97. Samain M-S, A Vrijdaghs, M Hesse, P Goetghebeur, F Jiménez Rodriguez, A Stoll, C Neinhuis, S Wanke 2010 Verhuellia is a segregate lineage in Piperaceae: more evidence from flower, fruit and pollen morphology, anatomy and development. Ann Bot 105: 677-688.
98. Schenk H 1892 Beitrage zur Biologie und Anatomie der Lianen, im besonderen der in Brasilien einheimishe Arten. I. Theil: Beitrage zur Anatomie der Lianen. G Fischer, Jena. 246 pp.
99. Schenk H 1893 Beitrage zur Biologie und Anatomie der Lianen, im besonderen der in Brasilien einheimishe Arten. II. Theil: Beitrage zur Anatomie der Lianen. G Fischer, Jena. 271 pp.
100. Smith J, A Stevens, E Tepe, C Davidson 2008 Placing the origin of two species-rich genera in the Late Cretaceous with later species divergence in the tertiary: a phylogenetic, biogeographic and molecular dating analysis of Piper and Peperomia (Piperaceae). Plant Syst Evol 275:9-30.
101. Soltis DE, CD Bell, S Kim, PS Soltis 2008 Origin and early evolution of angiosperms. Ann NY Acad Sci 1133:3-25.
102. Souza LA, IS Moscheta, JHG Oliveira 2004 Comparative morphology and anatomy of the leaf and stem of Peperomai dahlstedtii C. DC., Ottonia martiana Miq. and Piper diospyrifolium Kunth (Piperaceae). Gayana Bot 61:6-17.
103. Speck T, C Neinhuis, F Gallenmuller, NP Rowe 1997 Trees and shrubs in the mainly lianescent genus Aristolochia s.l.: secondary evolution of the self-supporting habit? Pages 201-208 in G Jeronimidis, JFV Vincent, eds. Plant biomechanics. University of Reading.
104. Speck T, NP Rowe 1994 Biomechanical analysis of Pitus dayi: early seed plant vegetative morphology and its implication on growth habit. J Plant Res 107:443-460.
105. Speck T, NP Rowe 1999 A quantitative approach for analytically defining size, growth form and habit in living and fossil plants. Pages 447-479 in MH Kurmann, AR Hemsley, eds. The evolution of plant architecture. Royal Botanic Gardens, Kew.
106. Speck T, NP Rowe, L Civeyrel, R Classen-Bockhoff, C Neinhuis, C Spatz 2003 The potential of plant biomechanics in functional biology and systematics. Pages 241-271 in TF Stuessy, V Mayer, E Horandl, eds. Deep morphology: toward a renaissance of morphology in plant systematics. Koeltz, Konigstein.
107. Speck T, D Vogellehner 1988 Biophysical examinations of the bending stability of various stele types and the upright axes of early ''vascular'' land plants. Bot Acta 101:262-268.
108. Sperry JS, UG Hacke, TS Feild, Y Sano, EH Sikkema 2007 Hydraulic consequences of vessel evolution in angiosperms. Int J Plant Sci 168: 1127-1139.
109. Sperry JS, UG Hacke, J Pittermann 2006 Size and function in conifer tracheids and angiosperm vessels. Am J Bot 93:1490-1500.
110. Spicer R, A Groover 2010 Evolution of development of vascular cambia and secondary growth. New Phytol 186:577-592.
111. Stevens PF 2001 onward Angiosperm Phylogeny website. http://www.mobot.org/MOBOT/research/APweb/.
112. Symmank L, M-S Samain, JF Smith, G Pino, A Stoll, P Goetghebeur, C Neinhuis, S Wanke 2011 The extraordinary journey of Peperomia subgenus Tildenia (Piperaceae): insights into diversification and colonization patterns from its cradle in Peru to the Trans-Mexican Volcanic Belt. J Biogeogr 38:2337-2349.
113. Tennakoon KU, JF Bolin, LJ Musselman, E Maass 2007 Structural attributes of the hypogeous holoparasite Hydnora triceps Drege & Meyer (Hydnoraceae). Am J Bot 94:1439-1449.
114. Tomlinson PB 1973 The monocotyledons: their evolution and comparative biology. VIII. Branching in monocotyledons. Q Rev Biol 48:458-466.
115. Tomlinson PB 1987 Architecture of tropical plants. Annu Rev Ecol Syst 18: 1-21.
116. Vermeij GJ 1987 Evolution and escalation. Princeton University Press, Princeton, NJ.
117. Wanke S, F González, C Neinhuis 2006 Systematics of pipevines: combining morphological and fast-evolving molecular characters to investigate the relationships within subfamily Aristolochioideae (Aristolochiaceae). Int J Plant Sci 167:1215-1227.
118. Wanke S, MA Jaramillo, T Borsch, M-S Samain, D Quandt, C Neinhuis 2007a Evolution of Piperales: matK gene and trnK intron sequence data reveal lineage specific resolution contrast. Mol Phylogenet Evol 42:477-497.
119. Wanke S, L Vanderschaeve, G Mathieu, C Neinhuis, P Goetghebeur, MS Samain 2007b From forgotten taxon to a missing link? The position of the genus Verhuellia (Piperaceae) revealed by molecules. Ann Bot 99:1231-1238.
120. Wilson JP, AH Knoll, NM Holbrook, CR Marshall 2008 Modeling fluid flow in Medullosa, an anatomically unusual carboniferous seed plant. Paleobiology 34:472-493.
121. Wu ZY, PH Raven, eds 1999 Flora of China. Vol 4. Cycadaceae through Fagaceae. Science Press, Beijing, and Missouri Botanical Garden Press, St. Louis. 110 pp.
122. Yuncker TG, WD Gray 1934 Anatomy of Hawaiian Peperomias. Bishop Mus Bull 10. 19 pp.