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Pollen morphology of Crotonoideae (Euphorbiaceae) from Seasonally Dry Tropical Forests, Northeastern Brazil

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Abstract

Crotonoideae is a subfamily of Euphorbiaceae, a plant family that is characterized by the presence of laticifers and pollen grains with Croton pattern exine. We analysed 48 species of Crotonoideae from Seasonally Dry Tropical Forests within Caatinga vegetation aiming to contribute to the pollen morphology of this subfamily, focusing on endemics to these forests. Pollen samples were obtained from specimens of the herbarium. Pollen grains were acetolyzed, measured, photographed and described using light and scanning electron microscopy methods. Three pollen types and seven subtypes were recognized based on aperture type, polarity, shape, size and details of the exine sculpture. The exine ornamentation and the type and number of apertures are the most important characteristics for recognizing genera in Crotonoideae. Inaperturate pollen grains with surface pila plicate were observed in representatives of Croton and Jatropha; 4–8 pantoporate pollen grains and a 3-colpate one with psilate pila were observed in Cnidoscolus, and 10–22 pantoporate pollen grains with rugulate pila were observed in Manihot. Due to the high diversity of Crotonoideae pollen morphology, we highlighted its eurypalynous properties, in addition to its taxonomic relevance, for the identification of groups.

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Acknowledgments

The authors thank the curators and staff of the CEPEC, HUEFS, HUNEB and SP herbaria for providing specimens; Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the fellowship granted to the first author; Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for supporting the senior author; Fundação Instituto Osvaldo Cruz (FIOCRUZ)-Centro de pesquisa Gonçalo Moniz for SEM facilities; and Laboratório de Palinologia da Universidade do Estado da Bahia (Campus VII) laboratory facilities with light microscopy, PPBio Project (457427/2012-4) and the Flora of Bahia (483909/2012-2).

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Authors and Affiliations

  1. Programa de Pós-Graduação em Botânica, Laboratório de Micromorfologia Vegetal, Departamento de Ciências Biológicas, Universidade Estadual de Feira de Santana, Av. Universitária, s/n., Feira De Santana, 44031-460, BA, Brazil

    Lidian R. de Souza, Daniela S. Carneiro-Torres & Francisco de A. R. dos Santos

  2. Universidade do Estado da Bahia, Campus VII, Senhor Do Bonfim, BA, Brazil

    Marileide D. Saba

Authors
  1. Lidian R. de Souza
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  2. Daniela S. Carneiro-Torres
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  3. Marileide D. Saba
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  4. Francisco de A. R. dos Santos
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Corresponding author

Correspondence to Lidian R. de Souza.

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This study was conducted following the accepted principles of ethics and professional conduct.

Conflict of interest

Author Lidian Ribeiro de Souza has received research grant from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (BR). Author Francisco de Assis Ribeiro dos Santos has received research grant from Conselho Nacional de Desenvolvimento Científico e Tecnológico (BR) (#303862/2013-0).

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Handling editor: Hervé Sauquet.

Appendix: specimens investigated

Appendix: specimens investigated

Cnidoscolus hamosus Pohl. Brazil: Bahia, Irecê, 20 Jan 1984, G. Fotius 3705 (HUEFS). Cnidoscolus infestus Pax & K.Hoffm. Brazil: Bahia, Conceição de Feira, Jun 1980, Grupo Pedra do Cavalo 225 (HUEFS).

Cnidoscolus pubescens Pohl. Brazil: Bahia, Bendengó, 23 Feb 2000, A.M. Giulietti 1775 and R.M. Harley (HUEFS); Bahia, Itaberaba, 23 Oct 2005, E. Mello 4144 et al. (HUEFS); Bahia, Paulo Afonso, 29 Nov 2005, R.M. Castro 1277 et al. (HUEFS). Cnidoscolus quercifolius Pohl ex Baill. Brazil: Bahia, Rodelas, 30 Oct 2009, E. Melo 6971 et al. (HUEFS); Bahia, Rodelas, 30 Oct 2009, E. Melo 7006 (HUEFS); Bahia, Rodelas, 13 Nov 2011, E. Melo 10684 et al. (HUEFS).

Cnidoscolus ulei (Pax) Pax. Brazil: Bahia, Caetité, 8 Feb 1997, M.L. Guedes 5212 et al. (HUEFS); Bahia, Caetité, 18 Dec 2009, L.J. Alves 122 et al. (HUEFS); Bahia, Mucugê, 14 Feb 1992, L.P. Queiroz 2629 (HUEFS).

Cnidoscolus urnigerus Pax. Brazil: Bahia, Casa Nova, 9 Feb 2004, L.P. Queiroz 9153 et al. (HUEFS); Bahia, Livramento do Brumado, 15 Jun 2002, L.P. Queiroz 7069 et al. (HUEFS); Bahia, Maracás, 22 Jan 2004, D.S. Carneiro-Torres 302 et al. (HUEFS). Croton adamantinus Müll.Arg. Brazil: Bahia, Campo Formoso, 13 Apr 2006, R.D. Souza 17 et al. (HUEFS); Bahia, Mucugê, 20 Dec 2007, M. Ibrahim 55 and S.F. Conceição (HUEFS); Bahia, Pindobaçú, 16 Dec 2008, L.A. Sousa 210 (HUNEB); Bahia, Rio de Contas, 6 Sep 2003, R.M. Harley 54674 and A.M. Giulietti (HUEFS). Croton adenocalyx Baill. Brazil: Ceará, Aiubá, 21 Mar 1980, Gomes s.n. (HUEFS); Bahia, Aiuaba, 21 Mar 1980, A. Gomes s.n. (HUEFS); Bahia, Cratéus, 27 Feb 2002, F.S. Araujo 1346 (HUEFS).

Croton anisodontus Müll.Arg. Brazil: Ceará, Capistrano, 27 Apr 1994, J.B.L.P. Medeiros 51 and M.A. Figueiredo (HUEFS); Ceará, Guaraciaba do Norte, 6 May 1984, A. Fernandes s.n. and Matos (HUEFS); Ceará, Guaraciaba do Norte, 6 May1984, A. Fernandes s.n. and Matos (HUEFS).

Croton arenosus Carn.-Torres & Cordeiro. Brazil: Bahia, Canudos, 18 Feb 2004, E.B. Miranda 613 et al. (HUEFS).

Croton argyrophylloides Müll.Arg. Brazil: Bahia, Itaberaba, 15 Feb 1984, G.C. Pereira-Pinto 544184 (HUEFS); Bahia, Itambé, 9 Jan 1986, A.M. Carvalho 2118 A. Chautems (HUEFS); Bahia, Tucano, 19 Jan 1964, A.L. Costa 2050 (HUEFS).

Croton betulaster Müll.Arg. Brazil: Bahia, Érico Cardoso, 4 Jul 2001, M.P. Bautista 3286 et al. (HUEFS); Bahia, Rio de Contas, 18 Jan 2003, A.M. Miranda 4054 et al. (HUEFS); Bahia, Rio de Contas, 16 Aug 2006, A.K.A. Santos 846 et al. (HUEFS). Croton blanchetianus Baill. Brazil: Ceará, Aiuaba, 9 Jan 1997, L.V. Lima-Verde 368 et al. (HUEFS).

Croton catinganus Müll.Arg. Brazil: Piauí, Amarante, 24 Jan 1970, L.T. Eiten 1036 G. Eiten (SP).

Croton cordiifolius Baill. Brazil: Bahia, Abaíra, 27 Dec 1992, D.J.N. Hind 50467 et al. (HUEFS); Bahia, Rio de Contas, 24 Jan1994, W. Ganev 2873 (HUEFS); Bahia, Rui Barbosa, 17 Jan 2006, L.P. Queiroz 12041 and D. Cardoso (HUEFS).

Croton echioides Baill. Brazil: Pernambuco, Moreilândia, 4 Mar 1995, E. Silveira s.n. (HUEFS); Bahia, Cafarnaum, 14 Jan 2012, J.G. Carvalho-Sobrinho 3227 et al. (HUEFS).

Croton glandulosodentatus Pax & K.Hoffm. Brazil: Bahia, Canudos, 18 Feb 2004, E.B. Miranda 622 et al. (HUEFS); Piauí, São Raimundo Nonato, 19 Dec 1978, A. Fundes s.n. (HUEFS).

Croton grewioides Baill. Brazil: Bahia, Jaguarari, 10 Nov 2005, A.A. Conceição 1608 et al. (HUEFS); Bahia, Jequié, 5 Nov 2009, J.C Nascimento 21 and R.M. Aguiar (HUEFS); Bahia, Jequié, 5 Nov 2009, J.C. Nascimento 20 and R.M. Aguiar (HUEFS); Bahia, Pindobaçú, 16 Nov 2008, L.A. Sousa 213 (HUNEB).

Croton harleyi Carn.-Torres & Cordeiro. Brazil: Bahia, Casa Nova, 29 Feb 2008, C. Correia 428 (HUEFS); Bahia, Morro do Chapéu, 1 Feb 2008, F.B.L. Silva 79 and F. França (HUEFS); Piauí, Sertão de Dentro, 1 Mar 1980, M. Del Arco s.n. (HUEFS).

Croton imbricatus L.R.Lima & Pirani. Brazil: Bahia, Caetité, 20 Nov 2006, M.M. Silva-Castro 1052 (HUEFS); Bahia, Rio de Contas, 20 Apr 2003, A.C. Serrão-Neto 16 et al. (HUEFS); Bahia, Rio de Contas, 12 Jun 2003, M.M. Silva-Castro 681 et al. (HUEFS).

Croton jacobinensis Baill. Brazil: Bahia, Campo Formoso, 5 Dec 2003, E.B. Miranda 601 et al. (HUEFS); Bahia, Pindobaçú, 24 May 2008, L.A. Sousa 85 (HUNEB); Ceará, Crato, 13 Feb 2007, D.S. Carneiro-Torres 873 et al. (HUEFS).

Croton japirensis Müll.Arg. Brazil: Pernambuco, Petrolina, 21 Mar 1984, G. Fotius 3804 (HUEFS); Bahia, Casa Nova, 8 Feb 2004, L.P. Queiroz 9109 (HUEFS); Bahia, Macaúbas, 12 Jan 2008, A. Rapini 1500 et al. (HUEFS).

Croton laceratoglandulosus Caruzo & Cordeiro. Brazil: Bahia, São Félix do Coribe, 11 Apr 2007, L.P. Queiroz 12818 (HUEFS); Bahia, São Félix do Coribe, 9 Jan 2008, A. Rapini 1432 et al. (HUEFS); Bahia, São Félix do Coribe, 11 Jan 2008, R.F. Souza-Silva 300 et al. (HUEFS).

Croton limae A.P.S.Gomes, M.F.Sales and P.E.Berry. Brazil: Bahia, Abaíra, 20 Dec 1991, R.M. Harley 50157 et al. (HUEFS); Bahia, Abaíra, 28 Dec 1992, R.M. Harley 50514 et al. (HUEFS); Bahia, Rio de Contas, 23 Jan 2008, R.M. Harley 55788 et al. (HUEFS).

Croton luetzelburgii Pax & K.Hoffm. Brazil: Bahia, Abaíra, 26 Oct 1992, W. Ganev 1377 (HUEFS 12441); Bahia, Lençóis, 3 Oct 2007, A.A. Conceição 2614 (HUEFS); Bahia, Palmeiras, 8 Aug 2007, T.F.B. Pastore 2162 et al. (HUEFS 127624).

Croton muscicapa Müll.Arg. Brazil: Bahia, Jacobina, 02 Apr 1999, R.M. Harley 53690 A.M. Giulietti (HUEFS); Bahia, Pindobaçú, 24 May 2008, L.A. Sousa 78 and R. B. Carvalho (HUNEB); Bahia, Pindobaçu, 26 Oct 2008, L.A Sousa 155 (HUEFS).

Croton nepetifolius Baill. Brazil: Ceará, Pedra Branca, 11 Feb 2007, Carneiro-Torres 849 (HUEFS); Piauí, Itaueira, 11 Nov 1979, Fernandes s.n. and Matos (HUEFS).

Croton paludosus Müll.Arg. Brazil: Bahia, Casa Branca, 8 Feb 2004, L.P. Queiroz 9100 et al. (HUEFS); Bahia, Pilão Arcado, 18 Mar 2006, D.S. Carneiro-Torres 620 (HUEFS); Bahia, Pilão Arcado, 19 Mar 2006, D.S. Carneiro-Torres 624 (HUEFS). Croton piauhiensis Müll.Arg. Brazil: Ceará, Crato, 12 Feb 2007, D.S. Carneiro-Torres 869 (HUEFS); Pernambuco, Brejo da Madre de Deus, 29 Feb 2000, L.M. Nascimento 327 and A.G. Silva (HUEFS); Pernambuco, Exu, 13 Feb 2007, D.S. Carneiro-Torres 876 (HUEFS).

Croton pulegiodorus Baill. Brazil: Bahia, Bom Jesus da Lapa, 9 Feb 2000, L.P. Queiroz 5776 et al. (HUEFS); Ceará, Morada Nova, 11 Mar 1983, E. Nunes s.n. et al. (HUEFS).

Croton pulegioides Müll.Arg. Brazil: Bahia, Feira de Santana, 13 Nov 1986, L.P. Queiroz 1022 J.M. Lemes (HUEFS); Bahia, Ipuaçu, Sep 1980, Grupo Pedra do Cavalo 749 (HUEFS).

Croton rhexiifolius Baill. Brazil: Bahia, Almadina, 12 Aug 2007, D. Cardoso 2128 et al. (HUEFS); Bahia, Almadina, 12 Aug 2007, R. Funch 603 (HUEFS); Bahia, Caetité, 28 Aug 1999, E. Melo 2863 et al. (HUEFS).

Croton rudolphianus Müll.Arg. Brazil: Bahia, Itatim, 28 Jan 1996, F. França 1543 et al. (HUEFS); Bahia, Itatim, 15 Dec 1996, E. Melo 1914 et al. (HUEFS); Bahia, Tucano, 4 Jan 2006, D. Cardoso 902 A. Amado (HUEFS).

Croton schultessi Müll.Arg. Brazil: Bahia, Rio de Contas, 18 Aug 2006, A.K.A Santos 865 et al. (HUEFS).

Croton sonderianus Müll.Arg. Brazil: Ceará, Aiuaba, 4 Feb1997, M.A. Figueiredo 690 and L.W. Lima-Verde (HUEFS); Brazil, s.loc., s.d., M.L. Guedes 15997 (HUEFS).

Croton tridentatus Mart. ex Müll.Arg. Brazil: Bahia, Pilão Arcado, 10 Nov 2005, A.A. Conceição 1582 et al. (HUEFS); Bahia, Sobradinho, 5 Aug 1985, G. Fotius 4096 (HUEFS); Pernambuco, Petrolina, 11 Aug 1983, G. Fotius 3544 et al. (HUEFS). Jatropha catingae Ule. Brazil: Bahia, Manoel Vitorino, s.d., A.S. Mori 11244 et al. (CEPEC).

Jatropha hastifolia Fern.Casas. Brazil: Bahia, Carinhanha, 24 Nov 2007, L.M. Guedes 13957 et al. (HUEFS); Bahia, Paulo Afonso, 6 Jun 2006, M. Calaço 141 (HUEFS).

Jatropha mutabilis Baill. Brazil: Bahia, Barra, 19 May 2010, L.P. Queiroz 14658 et al. (HUEFS); Bahia, Glória, 10 Aug 2004, S. Leal 109 and L. Barreto (HUEFS); Bahia, Jaguarari, 26 Nov 2010, E. Melo 8909 et al. (HUEFS).

Jatropha ribifolia Baill. Brazil: Bahia, Glória, 5 Jun 2004, M.V.M. Oliveira 681 (HUEFS); Bahia, Morro do Chápeu, 14 Apr 2007, E. Melo 4702 et al. (HUEFS); Bahia, São Gabriel, 5 Apr 2009, R.F. Machado 203 et al. (HUEFS).

Manihot brachyandra Pax & K.Hoffm. Brazil: Bahia, Piatã, 19 Oct 1992, W. Ganev 1276 (HUEFS).

Manihot caerulescens Pohl. Brazil: Bahia, Correntina, 28 Apr 1995, R.C. Mendonça 2304 et al. (HUEFS); Bahia, Wanderley, 1 Dec 2011, A.M. Miranda 6478 and J. Ferraz (HUEFS).

Manihot catingae Ule. Brazil: Bahia, Queimadas, 16 Nov 1986, L.P. Queiroz 1146 et al. (HUEFS).

Manihot dichotoma Ule. Brazil: Bahia, Brumado, 16 Dec 1987, A.C. Allem 3720 and W.L. Werneck (HUEFS); Bahia, Caldeirão Grande, 8 Dec 1987, A.C. Allem 3726 and W.L. Werneck (HUEFS); Minas Gerais, Espinosa, 4 Dec 1987, A.C. Allem 3707 and W.L. Werneck (HUEFS).

Manihot epruinosa Pax & K.Hoffm. Brazil: Bahia, Itaberaba, 7 Feb 1995, A.C. Allem 4518 and V.S. Silva (HUEFS); Minas Gerais, Itacarambi, 3 Dec 1987, A.C. Allem 3595 and W.L. Werneek (HUEFS); Minas Gerais, Itacarambi, 3 Dec 1987, A.C. Allem 3697 and W.L. Werneek (HUEFS).

Manihot heptaphylla Ule. Brazil: Bahia, Barra, 26 Oct 2000, A.T.A. Rodarte 128 (HUEFS); Bahia, Lençóis, 7 Sep 1999, F.F. Focha 42 and L.S. Funch (HUEFS); Bahia, Palmeiras, 20 Nov 2003, A.A. Conceição 1149 (HUEFS).

Manihot maracasensis Ule. Brazil: Bahia, Itamaraju, 6 Dec 1981, A.M. Carvalho 915 and G.P. Lewis (HUEFS); Bahia, Rui Barbosa, 18 Dec 2004, L.P. Queiroz 9904 et al. (HUEFS); Tocantins, Tocantinópolis, 19 Feb 2005, G. Pereira-Silva 9368 et al. (HUEFS).

Manihot pseudoglaziovii Pax & K.Hoffm. Brazil: Pernambuco, Petrolina, 22 Jan 2009, Antunes 95 et al. (HUEFS); Pernambuco, Salgueiro, 19 Jan 2010, D. Araújo 1122 et al. (HUEFS); Brazil, s.loc., s.d., V.D. Silva 26 et al. (HUEFS).

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de Souza, L.R., Carneiro-Torres, D.S., Saba, M.D. et al. Pollen morphology of Crotonoideae (Euphorbiaceae) from Seasonally Dry Tropical Forests, Northeastern Brazil. Plant Syst Evol 302, 795–817 (2016). https://doi.org/10.1007/s00606-016-1300-z

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