Abstract
Collaea insignis, a new species from Midwestern of Brazil, is described and illustrated from plants recognized as C. speciosa or misinterpreted as C. aschersoniana and C. stenophylla. However, the association of the morphological (e.g., morphology of leaves, flowers and indument types), leaf anatomical (see below), and geographical (allopatric distribution) features led us to recognized such species, and also propose four lectotypes and a synonym within this Collaea group. The leaf anatomy of Collaea species is described here for the first time, and it is noteworthy that all species present stomata in crypts, a rare feature in plants, and not described in the American Fabaceae. Other characters such as indumented leaflets, thick cuticle, palisade parenchyma with 2 or 3 layers of cells, spongy parenchyma with 1–3 layers of loosened cells, cortex in the midrib, petiole, pulvinus and pulvinules with rhombohedral crystals, bicollateral vascular bundles in the midrib and collateral in the petiole and petiole, and common epidermal cells with different shapes and sizes between the abaxial, and adaxial surfaces are also provided for the first time for the genus. In addition to several vegetative and reproductive characters that can be used to separate the new species from morphologically similar congeners. The studied species can be anatomically differentiated by a set of characters such as contour of the midrib, pulvinus, and puvinules, presence or absence of petiole, type of the vascular bundles of the mesophyll, midrib, and pulvinules, type of sheath extension surrounding the vascular bundles in the mesophyll and its direction, as well as the number of parenchyma and collenchyma layers in the cortex of the midrib, pulvinus and pulvinules. In addition to the taxonomic, and macro and micromorphological novelties, new interpretations about the leaf of the genus are proposed.
References
Araújo, M.G.P. & Mendonça, M.S. (1998) Escleromorfismo foliar de Aldina heterophylla Spruce ex Benth (Leguminosae: Papilionoideae) em três campinas da amazônia central. Acta Amazônica 28: 353–371.
Bachman, S., Moat, J., Hill, A.W., de la Torre, J. & Scott, B. (2011) Supporting Red List threat assessments with GeoCAT: geospatial conservation assessment tool. ZooKeys 150: 117–126. https://doi.org/10.3897/zookeys.150.2109.
Barroso, G.M., Guimarães, E.F., Ichaso, C.L.F., Costa, C.G., Peixoto, A.L. & Lima, H.C. (1991) Sistemática das Angiospermas do Brasil. v. 2. Viçosa, Editora da Universidade Federal de Viçosa. 377 pp.
Bentham, G. (1837) Commentationes de Leguminosarum Generibus. Zollinger, Vienna, 121 pp.
Bentham, G. (1841) Notes on Mimoseae, with a short Synopsis of Species. Journal of botany: being a second series of the Botanical miscellany 1841: 243–392.
Bentham, G. (1859) Leguminosae 1, Papilionaceae. In: Martius, C.F.P., Endlicher, S. & Urban, I. (Eds.) Flora Brasiliensis v. 15, pt. 1. Monachii, Lipsiae, pp. 1–332.
Bentham. G. (1862) Leguminosae 1, Papilionaceae 2. In: Martius, C.F.P., Endlicher, S. & Urban, I. (Eds.) Flora Brasiliensis v. 15, pt. 1B. Monachii, Lipsiae, pp. 1–350.
Bieras, A.C. & Sajo, M.G. (2009) Leaf structure of the cerrado (Brazilian savanna) woody plants. Trees 23: 451–471. https://doi.org/10.1007/s00468-008-0295-7
Brodribb, T. & Hill, R.S. (1997) Imbricacy and stomatal wax plugs reduce maximum leaf conductance in Southern Hemisphere conifers. Australian Journal of Botany 45: 657–668.
Browne, P. (1756) The civil and natural history of Jamaica in three parts. London, Printed by the author, 503 pp.
Burkart, A. (1952) Las leguminosas argentinas silvestres y cultivadas. 2ª edição. Buenos Aires, ACME, 569 pp.
Burkart, A. (1971) El género Galactia (Leg. Phaseoleae) en Sudamérica con especial referencia a la Argentina y paises vecinos. Darwiniana 16: 663–796.
Bukatsch, F. (1972) Bemerkungen zur Doppelfärbung Astrablau-Safranin. Mikrokosmos 61: 255.
Carpenter, R.J., Mcloughlin, S., Hill, R.S. & Jordan, G.J. (2014) Early evidence of xeromorphy in angiosperms: Stomatal encryption in a new eocene species of Banksia (Proteaceae) from Western Australia. American Journal of Botany 101: 1486–1497. https://doi.org/10.3732/ajb.1400191
Carvalho, C.R.V., Soares, E.K.S. & Oliveira, A.B. (2019) Morfoanatomia foliar de Copaifera sabulicola J.A.S. Costa & L.P. Queiroz: uma planta com potencial medicinal. Hoehnea 46: e192018.
Cen, Y. & Bornman, J.F. (1993) The effect of exposure toenhanced UV-B radiation on the penetration of monochromatic and polychromatic UV-B radiation in leaves of Brassica napus. Physiologia Plantarum 87: 249–255.
Ceolin, G.B. & Miotto, S.T.S. (2009) O gênero Collaea DC. (Leguminosae, Papilionoideae) na Região Sul do Brasil. Acta Botanica Brasilica 23: 991–998. https://doi.org/10.1590/S0102-33062009000400009
Chodat, R.H. & Hassler, E. (1904) Plantae Hasslerianae. Bulletin de l’Herbier Bossier 2: 879–913.
Cole, M.M. (1986) The savannas: biogeography and geobotany. Academy Press, London, 438 pp.
Corrêa, M.M., Araújo, M.G.P. & Scudeller, V.V. (2018) Comparative leaf anatomy of twenty species of Chrysobalanaceae R. Br. Flora 249: 60–66. https://doi.org/10.1016/j.flora.2018.09.009
De Lucia, E.H., Nelson, K., Vogelmann, T.C. & Smith, W.K. (1996) Contribution of the intercelular reflectance to photosinthesis in shade leaves. Plant, Cell & Enviroment 19: 159–170. https:doi.org/10.1111/j.1365-3040.1996.tb00237.x.
De Candolle, A.P. (1825) Leguminosae. Prodromus Systematis Naturalis Regni Vegetabilis 2: 93–524.
Dickison, W.C. (2000) Integrative plant anatomy. Academic Press, Harcourt, 533 pp.
Durazzini, A. (1772) Sull’ Albero detto volgarmente Iulibrissin letta il dì 5, Agosto 1772 nella Società de’ Georgosili. Magazzino Toscano 3: 1–14.
Esau, K. (1965) Plant anatomy 2nd Ed.. J. Wiley and Sons, New York, London, Sydney, 767 pp.
Evert, R.F. (2006) Esau’s plant anatomy: meristems, cells and tissues of the plant body: their structure, function and development. 3 ed. Wiley, New Jersey, 601 pp.
Fahn, A. (1979) Secretory tissues in plants. Academic Press, London, 302 pp.
Fahn, A. & Cutler, D. (1992) Xerophytes. Gebruder Borntraeger, Berlin, 176 pp.
Ferreira, P.M. & Flores, A.S. (2013) Anatomia foliolar de espécies lenhosas de Leguminosae-Caesalpinioideae em uma área de savana em Roraima, Brasil. Boletim do Museu Integrado de Roraima 7: 69–76. https://doi.org/10.24979/bolmirr.v7i02.759.
Fleurat-Lessard, P. & Bonnemain, J.-L. (1978) Structural and ultrastructural characteristics of the vascular apparatus of the sensitive plant (Mimosa pudica L.). Protoplasma 94: 127–143.
Fleurat-Lessard, P. & Satter, R.L. (1985) Relationship between structure and motility of Albizzia motor organs: changes in ultrastructure of cortical cells during dark-induced closure. Protoplasma 128: 72–79.
Fleurat-Lessard, P. & Roblin, G. (1982) Comparative histocitology of the petiole and the main pulvinus in Mimosa pudica L. Annals of Botany 50: 83–92.
Fortunato, R.H. (1995) A new species of Collaea (Leguminosae: Papilionoideae: Phaseoleae: Diocleinae) from Brazil. Kew Bulletin 50: 795–799.
Grisebach, A. (1874) Plantae Lorentzianae. Abhandlungen der Königlichen Gesellschaft der Wissenschaften zu Göttingen 19: 77–78.
Hassiotou, F., Ludwig, M., Renton, M., Veneklaas, E. & Evans, J. (2009) Influence of leaf dry mass per area, CO2, and irradiance on mesophyll conductance in sclerophylls. Journal of Experimental Botany 60: 2303–2314. https://doi:10.1093/jxb/erp021
Haworth, M. & McElwain (2008) Hot, dry, wet, cold or toxic? Revisiting the ecological significance of leaf andcuticular micromorphology. Palaeogeography, Palaeoclimatology, Palaeoecology 262: 79–90.
Hill, R.S. (1998) Fossil evidence for the onset of xeromorphy and scleromorphy in Australian Proteaceae. Australian Systematic Botany 11: 391–400.
Holtzmeier, M.A., Stern, W.L. & Judd, W.S. (1998) Comparative anatomy and systematics of Senghas’s cushion species of Maxillaria (Orchidaceae). Botanical Journal of the Linnean Society 127: 43–82.
Holmes, M.G. & Keiller, D.R. (2002) Effects of pubescence and waxes on the reflectance of leaves in the ultraviolet and photosynthetic wavebands: a comparison of a range of species. Plant Cell Environment 25: 85–93.
Hooker, W.J. & Arnott, G.A.W. (1833) Contributions towards a flora of South America and the islands of the Pacific. Botanical Miscellany 3: 129–212.
IUCN (2017) Standards and Petitions Subcommittee. Guidelines for using the IUCN Red List Categories and Criteria. Version 13. Prepared by the Standards and Petitions Subcommittee.
Johansen, D.A. (1940) Plant Microtecnique. 2.ed. Tata McGraw-Hill, New York, 532 pp.
Jordan, G.J., Dillon, R.A. & Weston, P.H. (2005) Solar radiation as a factor in the evolution of scleromorphic leaf anatomy in Proteaceae. American Journal of Botany 92: 789–796.
Krauss, P., Markstädter, C. & Riederer, M. (1977) Attenuation of UV radiation by plant cuticles from woody species. Plant Cell Environment 20: 1079–1085. https://doi.org/10.1111/j.1365-3040.1997.tb00684.x
Larcher, W. (2006) Ecofisiologia Vegetal. 3ª ed. Editora RiMa. São Carlos, São Paulo, 529 pp.
Linnaeus, C. (1753) Species Plantarum 1. Laurentii Salvius, Stockolm, 560 pp.
Loiseleur-Deslongchamps, J.L.A. (1812). Nouveau Duhamel ou Traité des arbres et arbustes que l’on cultive en France (Nouvelle edition) 7: 160. 516 pp.
LPWG (The Legume Phylogeny Working Group) (2017) A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny. Taxon 66: 44–77. https://doi.org/10.12705/661.3.
Machado, S.R. & Rodrigues, T.M. (2004) Anatomia e ultra-estrutura do pulvino primário de Pterodon pubescens Benth. (Fabaceae - Faboideae). Brazilian Journal of Botany 1: 135–147.
Matos, R.G., Souza, A.O., Santos, I.S. & Silva, M.J. (2020) Leaf anatomy and macro-morphological data support a new species of the legume genus Chamaecrista (Fabaceae, Caesalpinioideae) from Goiás, Brazil. Phytotaxa 443 (2): 167–178. https://doi.org/10.11646/phytotaxa.443.2.4
Martius, C.F.P. (1826) Vochysiaceae. In: Martius, C.F.P. & Zuccarini, J.G. (Eds.) Nova genera et species plantarum 1. Typis Lindaueri, Munich, pp. 123–154.
Mendes, K.R., Fortuna-Perez, A.P. & Rodrigues, T.M. (2019) Leaflet anatomy of Poiretia Vent. (Leguminosae, Papilionoideae, Dalbergieae) with emphasis on internal secretory structures in support of taxonomy. Flora 260: 151484. https://doi.org/10.1016/j.flora.2019.151484
Metcalfe, C.R. & Chalk, L. (1950) Anatomy of the Dicotyledons: Leaves, Stem, and Wood in Relation to Taxonomy with Notes on Economic Uses. v.2. Claredon Press, Oxford.
Metcalfe, C.R. & Chalk, L. (1979) Anatomy of the Dicotyledons. Vol I. Systematic Anatomy of the Leaf and Stem, Ed 2. Clarendon Press, Oxford, 288 pp.
Moysset, L. & Simón, E. (1991) Secondary pulvinus of Robinia pseudoacacia (Leguminosae): structural and ultrastructural features. American Journal of Botany 78: 1467–1486.
Morretes, B.L. & Ferri, M.G. (1959) Contribuição ao estudo da anatomia das folhas de plantas do cerrado. Boletim da Faculdade de Filosofia, Ciências e Letras da USP 243, Botânica 16: 7–70.
Napp-Zinn, K. (1973) Anatomie des Blattes. II Blattanatomie der Angiospermen. In: Linsbauer, K. (Ed.) Handbuch der Planzenanatomie. Gebrüder Borntraeger, Berlin, 1424 pp.
Oguchi, R., Hikosaka, K. & Hirose, T. (2005) Leaf anatomy as a constraint for photosynthetic acclimation: differential responses in leaf anatomy to increasing growth irradiance among three deciduous trees. Plant Cell Environment 28: 916–927.
Oliveira, A.C.S. & Queiroz, L.P. (2020) Collaea in Flora do Brasil 2020. Jardim Botânico do Rio de Janeiro. [https://floradobrasil2020.jbrj.gov.br/FB29549]
Paviani, T.I. (1974) Sobre a ocorrência de fibras gelatinosas em Plathymenia reticulata Benth. Ciência e Cultura 26: 783–786.
Pyykkö, M. (1966) The leaf anatomy of East Patagonian xerophytic plants. Annales Botanici Fennici 3: 453–622.
Rossatto, D.R., Kolb, R.M. & Franco, A.C. (2015) Leaf anatomy is associated with the type of growth form in Neotropical savanna plants. Botany 93: 507–518. https://doi.org/10.1139/cjb-2015-0001
Roth-Nebelsick, A. (2007) Computer-based studies of diffusion through stomata of different architecture. Annals of Botany 100: 23–32. https://doi.org/10.1093/aob/mcm075
Queiroz, L.P., Fortunato, R.H. & Giulietti, A.M. (2003) Phylogeny of the Diocleinae (Papilionoideae: Phaseoleae) based on morphological characters. In: Klitgaard, B.B. & Bruneau, A. (Eds.) Advances in legume systematics, part 10, Higher Level Systematics. Royal Botanic Gardens, Kew, pp. 303–324.
Queiroz, L.P., Pastore, J.F.B., Cardoso, D., Snak, C., Lima, A.L.C., Gagnon, E., Vatanparast, M., Holland, A.E. & Egan, A.N. (2015) A multilocus phylogenetic analysis reveals the monophyly of a recircumscribed papilionoid legume tribe Diocleae with well-supported generic relationships. Molecular Phylogenetics and Evolution 90: 1–19. https://doi.org/10.1016/j.ympev.2015.04.016.
Queiroz, L.P. & Snak, C. (2020) Revisiting the taxonomy of Dioclea and related genera (Leguminosae, Papilionoideae), with new generic circumscriptions. Phytokeys 164: 67–114. https://doi.org/10.3897/phytokeys.164.55441
Sajo, M.G. & Rudall, P.J. (2002) Leaf and stem anatomy of Vochysiaceae in relation to subfamilial systematics. Botanical Journal of the Linnean Society 126: 237–260.
Sede, S.M., Tosto, D., Gottlieb, A.M., Poggio, L. & Fortunato, R. (2008) Genetic relationships in the Galactia – Camptosema–Collaea complex (Leguminosae) inferred from AFLP markers. Plant Systematics and Evolution 276: 261–270. https://doi.org/10.1007/s00606-008-0100-5.
Schrire, B.D. (2005) Tribe Phaseoleae. In: Lewis, G., Schrire, B., Mackinder, B. & Lock, M. (Eds.) Legumes of the world. Royal Botanic Gardens, Kew, pp. 393–431.
Silva, M.J., Souza, A.O. & Alonso, A.A. (2017) Chamaecrista belladonna (Fabaceae, Caesalpinioideae, Cassieae), a new threatened endemic species from Goiás, Brazil. Brittonia 69: 544–552. https://doi.org/10.1007/s12228-017-9489-x
Silva, M.J., Souza, A.O. & Alonso, A.A. (2019) A new species for the legume genus Chamaecrista (Fabaceae, Caesalpinioideae) supported by molecular, morphological, and anatomical data. Plant Systematics and Evolution 305: 325–340. https://doi.org/10.1007/s00606-019-01569-3
Taubert, P.H.W. (1894) Leguminosae. Die Natürlichen Pflanzenfamilien 3 (3): 70–396.
Taubert, P.H.W. (1896) Beiträge zur Kenntnis der Flora des centralbrasilianischen Staates Goyaz. Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie 21: 402–457.
Taubert, P.H.W. (1889) Leguminosae novae v. minus cognitae austro-americanae. Flora 72: 421–430. Available from: http://www.botanicus.org/item/31753002307384 (accessed 10 October 2022)
Thiers, B. (continuously updated) (2022) Index Herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium, New York. Available from: https://sweetgum.nybg.org/science/ih/ (accessed 10 October 2022)
Valkama, E., Koricheva, J., Salminen, J.-P., Helander, M., Saloniemi, I., Saikkonen, K. & Pihlaja, K. (2005) Leaf surface traits: Overlooked determinants of birch resistance to herbivores and foliar micro-fungi? Trees 19: 191–197. https://doi.org/10.1007/s00468-004-0380-5
Ventenat, E.P. (1907) Notice sur les plantes qui seront publiées dans les cinq dernières livraision de l’ouvrage intitulée “Choix des plantes” Mémoires de la Classe des Sciences, Mathematique et Physique d l’Institut National de France 1: 1–6.
Bachman, S., Moat, J., Hill, A.W., de la Torre, J. & Scott, B. (2011) Supporting Red List threat assessments with GeoCAT: geospatial conservation assessment tool. ZooKeys 150: 117–126. https://doi.org/10.3897/zookeys.150.2109.
Barroso, G.M., Guimarães, E.F., Ichaso, C.L.F., Costa, C.G., Peixoto, A.L. & Lima, H.C. (1991) Sistemática das Angiospermas do Brasil. v. 2. Viçosa, Editora da Universidade Federal de Viçosa. 377 pp.
Bentham, G. (1837) Commentationes de Leguminosarum Generibus. Zollinger, Vienna, 121 pp.
Bentham, G. (1841) Notes on Mimoseae, with a short Synopsis of Species. Journal of botany: being a second series of the Botanical miscellany 1841: 243–392.
Bentham, G. (1859) Leguminosae 1, Papilionaceae. In: Martius, C.F.P., Endlicher, S. & Urban, I. (Eds.) Flora Brasiliensis v. 15, pt. 1. Monachii, Lipsiae, pp. 1–332.
Bentham. G. (1862) Leguminosae 1, Papilionaceae 2. In: Martius, C.F.P., Endlicher, S. & Urban, I. (Eds.) Flora Brasiliensis v. 15, pt. 1B. Monachii, Lipsiae, pp. 1–350.
Bieras, A.C. & Sajo, M.G. (2009) Leaf structure of the cerrado (Brazilian savanna) woody plants. Trees 23: 451–471. https://doi.org/10.1007/s00468-008-0295-7
Brodribb, T. & Hill, R.S. (1997) Imbricacy and stomatal wax plugs reduce maximum leaf conductance in Southern Hemisphere conifers. Australian Journal of Botany 45: 657–668.
Browne, P. (1756) The civil and natural history of Jamaica in three parts. London, Printed by the author, 503 pp.
Burkart, A. (1952) Las leguminosas argentinas silvestres y cultivadas. 2ª edição. Buenos Aires, ACME, 569 pp.
Burkart, A. (1971) El género Galactia (Leg. Phaseoleae) en Sudamérica con especial referencia a la Argentina y paises vecinos. Darwiniana 16: 663–796.
Bukatsch, F. (1972) Bemerkungen zur Doppelfärbung Astrablau-Safranin. Mikrokosmos 61: 255.
Carpenter, R.J., Mcloughlin, S., Hill, R.S. & Jordan, G.J. (2014) Early evidence of xeromorphy in angiosperms: Stomatal encryption in a new eocene species of Banksia (Proteaceae) from Western Australia. American Journal of Botany 101: 1486–1497. https://doi.org/10.3732/ajb.1400191
Carvalho, C.R.V., Soares, E.K.S. & Oliveira, A.B. (2019) Morfoanatomia foliar de Copaifera sabulicola J.A.S. Costa & L.P. Queiroz: uma planta com potencial medicinal. Hoehnea 46: e192018.
Cen, Y. & Bornman, J.F. (1993) The effect of exposure toenhanced UV-B radiation on the penetration of monochromatic and polychromatic UV-B radiation in leaves of Brassica napus. Physiologia Plantarum 87: 249–255.
Ceolin, G.B. & Miotto, S.T.S. (2009) O gênero Collaea DC. (Leguminosae, Papilionoideae) na Região Sul do Brasil. Acta Botanica Brasilica 23: 991–998. https://doi.org/10.1590/S0102-33062009000400009
Chodat, R.H. & Hassler, E. (1904) Plantae Hasslerianae. Bulletin de l’Herbier Bossier 2: 879–913.
Cole, M.M. (1986) The savannas: biogeography and geobotany. Academy Press, London, 438 pp.
Corrêa, M.M., Araújo, M.G.P. & Scudeller, V.V. (2018) Comparative leaf anatomy of twenty species of Chrysobalanaceae R. Br. Flora 249: 60–66. https://doi.org/10.1016/j.flora.2018.09.009
De Lucia, E.H., Nelson, K., Vogelmann, T.C. & Smith, W.K. (1996) Contribution of the intercelular reflectance to photosinthesis in shade leaves. Plant, Cell & Enviroment 19: 159–170. https:doi.org/10.1111/j.1365-3040.1996.tb00237.x.
De Candolle, A.P. (1825) Leguminosae. Prodromus Systematis Naturalis Regni Vegetabilis 2: 93–524.
Dickison, W.C. (2000) Integrative plant anatomy. Academic Press, Harcourt, 533 pp.
Durazzini, A. (1772) Sull’ Albero detto volgarmente Iulibrissin letta il dì 5, Agosto 1772 nella Società de’ Georgosili. Magazzino Toscano 3: 1–14.
Esau, K. (1965) Plant anatomy 2nd Ed.. J. Wiley and Sons, New York, London, Sydney, 767 pp.
Evert, R.F. (2006) Esau’s plant anatomy: meristems, cells and tissues of the plant body: their structure, function and development. 3 ed. Wiley, New Jersey, 601 pp.
Fahn, A. (1979) Secretory tissues in plants. Academic Press, London, 302 pp.
Fahn, A. & Cutler, D. (1992) Xerophytes. Gebruder Borntraeger, Berlin, 176 pp.
Ferreira, P.M. & Flores, A.S. (2013) Anatomia foliolar de espécies lenhosas de Leguminosae-Caesalpinioideae em uma área de savana em Roraima, Brasil. Boletim do Museu Integrado de Roraima 7: 69–76. https://doi.org/10.24979/bolmirr.v7i02.759.
Fleurat-Lessard, P. & Bonnemain, J.-L. (1978) Structural and ultrastructural characteristics of the vascular apparatus of the sensitive plant (Mimosa pudica L.). Protoplasma 94: 127–143.
Fleurat-Lessard, P. & Satter, R.L. (1985) Relationship between structure and motility of Albizzia motor organs: changes in ultrastructure of cortical cells during dark-induced closure. Protoplasma 128: 72–79.
Fleurat-Lessard, P. & Roblin, G. (1982) Comparative histocitology of the petiole and the main pulvinus in Mimosa pudica L. Annals of Botany 50: 83–92.
Fortunato, R.H. (1995) A new species of Collaea (Leguminosae: Papilionoideae: Phaseoleae: Diocleinae) from Brazil. Kew Bulletin 50: 795–799.
Grisebach, A. (1874) Plantae Lorentzianae. Abhandlungen der Königlichen Gesellschaft der Wissenschaften zu Göttingen 19: 77–78.
Hassiotou, F., Ludwig, M., Renton, M., Veneklaas, E. & Evans, J. (2009) Influence of leaf dry mass per area, CO2, and irradiance on mesophyll conductance in sclerophylls. Journal of Experimental Botany 60: 2303–2314. https://doi:10.1093/jxb/erp021
Haworth, M. & McElwain (2008) Hot, dry, wet, cold or toxic? Revisiting the ecological significance of leaf andcuticular micromorphology. Palaeogeography, Palaeoclimatology, Palaeoecology 262: 79–90.
Hill, R.S. (1998) Fossil evidence for the onset of xeromorphy and scleromorphy in Australian Proteaceae. Australian Systematic Botany 11: 391–400.
Holtzmeier, M.A., Stern, W.L. & Judd, W.S. (1998) Comparative anatomy and systematics of Senghas’s cushion species of Maxillaria (Orchidaceae). Botanical Journal of the Linnean Society 127: 43–82.
Holmes, M.G. & Keiller, D.R. (2002) Effects of pubescence and waxes on the reflectance of leaves in the ultraviolet and photosynthetic wavebands: a comparison of a range of species. Plant Cell Environment 25: 85–93.
Hooker, W.J. & Arnott, G.A.W. (1833) Contributions towards a flora of South America and the islands of the Pacific. Botanical Miscellany 3: 129–212.
IUCN (2017) Standards and Petitions Subcommittee. Guidelines for using the IUCN Red List Categories and Criteria. Version 13. Prepared by the Standards and Petitions Subcommittee.
Johansen, D.A. (1940) Plant Microtecnique. 2.ed. Tata McGraw-Hill, New York, 532 pp.
Jordan, G.J., Dillon, R.A. & Weston, P.H. (2005) Solar radiation as a factor in the evolution of scleromorphic leaf anatomy in Proteaceae. American Journal of Botany 92: 789–796.
Krauss, P., Markstädter, C. & Riederer, M. (1977) Attenuation of UV radiation by plant cuticles from woody species. Plant Cell Environment 20: 1079–1085. https://doi.org/10.1111/j.1365-3040.1997.tb00684.x
Larcher, W. (2006) Ecofisiologia Vegetal. 3ª ed. Editora RiMa. São Carlos, São Paulo, 529 pp.
Linnaeus, C. (1753) Species Plantarum 1. Laurentii Salvius, Stockolm, 560 pp.
Loiseleur-Deslongchamps, J.L.A. (1812). Nouveau Duhamel ou Traité des arbres et arbustes que l’on cultive en France (Nouvelle edition) 7: 160. 516 pp.
LPWG (The Legume Phylogeny Working Group) (2017) A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny. Taxon 66: 44–77. https://doi.org/10.12705/661.3.
Machado, S.R. & Rodrigues, T.M. (2004) Anatomia e ultra-estrutura do pulvino primário de Pterodon pubescens Benth. (Fabaceae - Faboideae). Brazilian Journal of Botany 1: 135–147.
Matos, R.G., Souza, A.O., Santos, I.S. & Silva, M.J. (2020) Leaf anatomy and macro-morphological data support a new species of the legume genus Chamaecrista (Fabaceae, Caesalpinioideae) from Goiás, Brazil. Phytotaxa 443 (2): 167–178. https://doi.org/10.11646/phytotaxa.443.2.4
Martius, C.F.P. (1826) Vochysiaceae. In: Martius, C.F.P. & Zuccarini, J.G. (Eds.) Nova genera et species plantarum 1. Typis Lindaueri, Munich, pp. 123–154.
Mendes, K.R., Fortuna-Perez, A.P. & Rodrigues, T.M. (2019) Leaflet anatomy of Poiretia Vent. (Leguminosae, Papilionoideae, Dalbergieae) with emphasis on internal secretory structures in support of taxonomy. Flora 260: 151484. https://doi.org/10.1016/j.flora.2019.151484
Metcalfe, C.R. & Chalk, L. (1950) Anatomy of the Dicotyledons: Leaves, Stem, and Wood in Relation to Taxonomy with Notes on Economic Uses. v.2. Claredon Press, Oxford.
Metcalfe, C.R. & Chalk, L. (1979) Anatomy of the Dicotyledons. Vol I. Systematic Anatomy of the Leaf and Stem, Ed 2. Clarendon Press, Oxford, 288 pp.
Moysset, L. & Simón, E. (1991) Secondary pulvinus of Robinia pseudoacacia (Leguminosae): structural and ultrastructural features. American Journal of Botany 78: 1467–1486.
Morretes, B.L. & Ferri, M.G. (1959) Contribuição ao estudo da anatomia das folhas de plantas do cerrado. Boletim da Faculdade de Filosofia, Ciências e Letras da USP 243, Botânica 16: 7–70.
Napp-Zinn, K. (1973) Anatomie des Blattes. II Blattanatomie der Angiospermen. In: Linsbauer, K. (Ed.) Handbuch der Planzenanatomie. Gebrüder Borntraeger, Berlin, 1424 pp.
Oguchi, R., Hikosaka, K. & Hirose, T. (2005) Leaf anatomy as a constraint for photosynthetic acclimation: differential responses in leaf anatomy to increasing growth irradiance among three deciduous trees. Plant Cell Environment 28: 916–927.
Oliveira, A.C.S. & Queiroz, L.P. (2020) Collaea in Flora do Brasil 2020. Jardim Botânico do Rio de Janeiro. [https://floradobrasil2020.jbrj.gov.br/FB29549]
Paviani, T.I. (1974) Sobre a ocorrência de fibras gelatinosas em Plathymenia reticulata Benth. Ciência e Cultura 26: 783–786.
Pyykkö, M. (1966) The leaf anatomy of East Patagonian xerophytic plants. Annales Botanici Fennici 3: 453–622.
Rossatto, D.R., Kolb, R.M. & Franco, A.C. (2015) Leaf anatomy is associated with the type of growth form in Neotropical savanna plants. Botany 93: 507–518. https://doi.org/10.1139/cjb-2015-0001
Roth-Nebelsick, A. (2007) Computer-based studies of diffusion through stomata of different architecture. Annals of Botany 100: 23–32. https://doi.org/10.1093/aob/mcm075
Queiroz, L.P., Fortunato, R.H. & Giulietti, A.M. (2003) Phylogeny of the Diocleinae (Papilionoideae: Phaseoleae) based on morphological characters. In: Klitgaard, B.B. & Bruneau, A. (Eds.) Advances in legume systematics, part 10, Higher Level Systematics. Royal Botanic Gardens, Kew, pp. 303–324.
Queiroz, L.P., Pastore, J.F.B., Cardoso, D., Snak, C., Lima, A.L.C., Gagnon, E., Vatanparast, M., Holland, A.E. & Egan, A.N. (2015) A multilocus phylogenetic analysis reveals the monophyly of a recircumscribed papilionoid legume tribe Diocleae with well-supported generic relationships. Molecular Phylogenetics and Evolution 90: 1–19. https://doi.org/10.1016/j.ympev.2015.04.016.
Queiroz, L.P. & Snak, C. (2020) Revisiting the taxonomy of Dioclea and related genera (Leguminosae, Papilionoideae), with new generic circumscriptions. Phytokeys 164: 67–114. https://doi.org/10.3897/phytokeys.164.55441
Sajo, M.G. & Rudall, P.J. (2002) Leaf and stem anatomy of Vochysiaceae in relation to subfamilial systematics. Botanical Journal of the Linnean Society 126: 237–260.
Sede, S.M., Tosto, D., Gottlieb, A.M., Poggio, L. & Fortunato, R. (2008) Genetic relationships in the Galactia – Camptosema–Collaea complex (Leguminosae) inferred from AFLP markers. Plant Systematics and Evolution 276: 261–270. https://doi.org/10.1007/s00606-008-0100-5.
Schrire, B.D. (2005) Tribe Phaseoleae. In: Lewis, G., Schrire, B., Mackinder, B. & Lock, M. (Eds.) Legumes of the world. Royal Botanic Gardens, Kew, pp. 393–431.
Silva, M.J., Souza, A.O. & Alonso, A.A. (2017) Chamaecrista belladonna (Fabaceae, Caesalpinioideae, Cassieae), a new threatened endemic species from Goiás, Brazil. Brittonia 69: 544–552. https://doi.org/10.1007/s12228-017-9489-x
Silva, M.J., Souza, A.O. & Alonso, A.A. (2019) A new species for the legume genus Chamaecrista (Fabaceae, Caesalpinioideae) supported by molecular, morphological, and anatomical data. Plant Systematics and Evolution 305: 325–340. https://doi.org/10.1007/s00606-019-01569-3
Taubert, P.H.W. (1894) Leguminosae. Die Natürlichen Pflanzenfamilien 3 (3): 70–396.
Taubert, P.H.W. (1896) Beiträge zur Kenntnis der Flora des centralbrasilianischen Staates Goyaz. Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie 21: 402–457.
Taubert, P.H.W. (1889) Leguminosae novae v. minus cognitae austro-americanae. Flora 72: 421–430. Available from: http://www.botanicus.org/item/31753002307384 (accessed 10 October 2022)
Thiers, B. (continuously updated) (2022) Index Herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium, New York. Available from: https://sweetgum.nybg.org/science/ih/ (accessed 10 October 2022)
Valkama, E., Koricheva, J., Salminen, J.-P., Helander, M., Saloniemi, I., Saikkonen, K. & Pihlaja, K. (2005) Leaf surface traits: Overlooked determinants of birch resistance to herbivores and foliar micro-fungi? Trees 19: 191–197. https://doi.org/10.1007/s00468-004-0380-5
Ventenat, E.P. (1907) Notice sur les plantes qui seront publiées dans les cinq dernières livraision de l’ouvrage intitulée “Choix des plantes” Mémoires de la Classe des Sciences, Mathematique et Physique d l’Institut National de France 1: 1–6.