Plant Systematics and Evolution

, Volume 303, Issue 4, pp 531–558 | Cite as

Morphological characterization in the genus Passiflora L.: an approach to understanding its complex variability

  • John Ocampo Pérez
  • Geo Coppens d’Eeckenbrugge
Original Article


Morphological variation was studied in 124 accessions from 61 Passiflora L. species. Twenty-four quantitative descriptors selected for their high variation among subgenera were submitted to a principal component analysis. The first principal component (32% of total variance) was associated with flower length and secondarily with floral cup constriction, the second (27%) with flower width and bract shape, and the third (14%) with peduncle branching, stem width, and leaf length, which relates it to the differentiation of subgenera Astrophea and Deidamioides. The projection of accessions in the resulting tridimensional space consistently separates the four subgenera, as well as supersection Tacsonia of subgenus Passiflora. A neighbor joining analysis, on a selection of 32 qualitative traits and four categorized quantitative variables, clustered species according to their chromosome number and, within subgenus Passiflora, separated supersections Tacsonia (pollinated by the sword-billed hummingbird) and Distephana (pollinated by shorter-billed hummingbirds) from all other, bee-pollinated, species. Thus, the morphological study allows separating the effects of genome evolution from those of more recent and independent coevolutions concerning the pollination syndromes of supersections Tacsonia and Distephana. Within subgenus Decaloba, diverging subclusters are consistent with supersections and particular sections, with the partial exception of supersection Decaloba. Within supersection Tacsonia, subclusters correspond to one or two sections, pointing to overclassification in the current taxonomy. Among the bee-pollinated species of subgenus Passiflora, only supersection Laurifolia is clearly validated. Most of these results are consistent with molecular phylogenetic studies, except for interspecific relations among bee-pollinated species of subgenus Passiflora, which appear particularly difficult to classify.


Morphological descriptors Passifloraceae Plant genetic resources Principal component analysis Systematics 

Supplementary material

606_2017_1390_MOESM1_ESM.pdf (93 kb)
Supplementary material 1 (PDF 93 kb)


  1. Abrahamczyk S, Souto-Vilarós D, Renner SS (2014) Escape from extreme specialization: passionflowers, bats and the sword-billed hummingbird. Proc Roy Soc Edinburgh B 281:1–7. doi:10.1098/rspb.2014.0888 Google Scholar
  2. Brummitt RK, Powell CE (1992) Authors of plant names. A list of authors of scientific names of plants, with recommended standard form of their names including abbreviations. Royal Botanic Gardens, KewGoogle Scholar
  3. Buzato S, Franco ALM (1992) Tetrastylis ovalis: a second case of bat-pollinated passionflower (Passifloraceae). Pl Syst Evol 181:261–267. doi:10.1007/BF00937450 CrossRefGoogle Scholar
  4. Cerqueira-Silva CBM, Faleiro FG, Jesus ON, Santos ESL, Souza AP (2016) The genetic diversity, conservation, and use of passion fruit (Passiflora spp.). In: Ahuja MR, Jain SM (eds) Genetic diversity and erosion in plants, sustainable development and biodiversity 8. Springer, Switzerland. doi:10.1007/978-3-319-25954-3_5
  5. Coppens d’Eeckenbrugge G (2003) Exploração da diversidade genética das passifloras. Sexto Simpósio Brasileiro sobre a Cultura do Maracujazeiro. November 24-27, Campos de Goytacazes (Brazil). Available at: Accessed 10 Oct 2016
  6. Coppens d’Eeckenbrugge G, Barney VE, Møller Jørgensen P, MacDougal JM (2001) Passiflora tarminiana, a new cultivated species of Passiflora subgenus Tacsonia (Passifloraceae). Novon 11:8–15. doi:10.2307/3393199 CrossRefGoogle Scholar
  7. De Jussieu AL (1805) Second Mémoire sur la famille des Passiflorées, et particulièrement sur quelques espèces nouvelles du genre Tacsonia. Ann Mus Natl Hist Nat 6:388–396Google Scholar
  8. De Melo F, Guerra M (2003) Variability of 5S and 45S rDNA sites in Passiflora L. species with distinct base chromosome numbers. Ann Bot (Oxford) 92:309–316. doi:10.1093/aob/mcg138 CrossRefGoogle Scholar
  9. De Melo F, Cervi A, Guerra M (2001) Karyology and cytotaxonomy of the genus Passiflora L. (Passifloraceae). Pl Syst Evol 226:69–84. doi:10.1007/s006060170074 CrossRefGoogle Scholar
  10. De Oliviera Plotze R, Falvo M, Gomes J, Bernacci L, Carneiro M, Oliveira G, Martinez O (2005) Leaf shape analysis using the multiscale Minkowski fractial dimension, a new morphometric method: a study with Passiflora (Passifloraceae). Canad J Bot 83:287–301. doi:10.1139/b05-002 CrossRefGoogle Scholar
  11. Escobar LK (1988) Monografía No 10. Passifloraceae. Passiflora. Subgéneros: Tacsonia, Rathea, Manicata and Distephana. Universidad Nacional de Colombia, Bogotá D.E.Google Scholar
  12. Escobar LK (1989) A new subgenus and five new species in Passiflora (Passifloraceae) from South America. Ann Missouri Bot Gard 76:877–885. doi:10.1590/S1415-47572012000600019 CrossRefGoogle Scholar
  13. Escobar LK (1990) A taxonomic revision of Passiflora Subgenus Astrophea (Passifloracae). Universidad de Antioquia and University of Texas, Antioquia, AustinGoogle Scholar
  14. Escobar LK (1994) Two new species and a key to Passiflora subg. Astrophea. Syst Bot 19:203–210. doi:10.2307/2419596 CrossRefGoogle Scholar
  15. Fajardo D, Angel F, Grum M, Tohmé J, Lobo M, Roca W, Sánchez I (1998) Genetic variation analysis of the genus Passiflora L. using RAPD markers. Euphytica 101:341–347. doi:10.1023/A:1018395229851 CrossRefGoogle Scholar
  16. FAO (2011) Committee on commodity problems, intergovernmental group on bananas and tropical fruits, Yaoundé (Cameroon), 3–5 May 2011, Tropical Fruits Compendium. Available at: Accessed 10 Oct 2016
  17. Feuillet C, MacDougal JM (2003) A new infrageneric classification of Passiflora L. (Passifloraceae). Passiflora 13:34–38Google Scholar
  18. Hansen AK, Lawrence G, Simpson BB, Downie SR, Stephen R, Cervi AC, Jansen RK (2006) Phylogenetic relationships and chromosome number evolution in Passiflora. Syst Bot 31:138–150. doi:10.1600/036364406775971769 CrossRefGoogle Scholar
  19. Hansen AK, Escobar LK, Lawrence E, Gilbert E, Jansen K (2007) Paternal, maternal and biparental inheritance of chloroplast genome in Passiflora (Passifloraceae). Amer J Bot 94:42–46. doi:10.3732/ajb.94.1.42 CrossRefGoogle Scholar
  20. Hill T, Lewicki P (2006) STATISTICS methods and applications. StatSoft, Tulsa. doi:10.1007/s10260-015-0341-8 Google Scholar
  21. Kay E (2001) Observations on the Pollination of Passiflora penduliflora. Biotropica 33:709–713. doi:10.1111/j.1744-7429.2001.tb00229.x Google Scholar
  22. Killip EP (1938) The American species of Passifloraceae. Field Museum of Natural History Publication. Bot Ser 19:613. doi:10.5962/bhl.title.2269 Google Scholar
  23. Krosnick SE, Freudestein JV (2005) Monophyly and floral character homology of Old Word Passiflora (Subgeneus Decaloba: supersection Disemma). Syst Bot 20:139–152. doi:10.1600/0363644053661959 CrossRefGoogle Scholar
  24. Krosnick SE, Ford AJ, Freudenstein JV (2009) Taxonomic revision of Passiflora subgenus Tetrapathea including the monotypic genera Hollrungia and Tetrapathea (Passifloraceae), and a new species of Passiflora. Syst Bot 34:375–385. doi:10.1600/03636440978860634 CrossRefGoogle Scholar
  25. Krosnick SE, Porter-Utley KE, MacDougal J, Møller Jørgensen P, McDade LA (2013) New insights into the evolution of Passiflora subgenus Decaloba (Passifloraceae): phylogenetic relationships and morphological synapomorphies. Syst Bot 38:692–713. doi:10.1600/036364413X670359 CrossRefGoogle Scholar
  26. MacDougal JM (1994) Revision of Passiflora section Decaloba, Pseudodysosmia (Passifloraceae). Syst Bot Monogr 14:146. doi:10.2307/25027834 Google Scholar
  27. MacDougal JM, Feuillet C (2004) Systematics. In: Ulmer T, MacDougal JM (eds) Passiflora: Passionflowers of the world. Timber Press Portland, OregonGoogle Scholar
  28. Møller P, Muchhala N, MacDougal JM (2012) Passiflora unipetala, a new bat-pollinated species of Passiflora supersect. Tacsonia (Passifloraceae). Novon 22:174–179. doi:10.3417/2011095 CrossRefGoogle Scholar
  29. Muschner V, Lorenz-Lemke A, Cervi AC, Bonatto S, Souza-Chies T, Salzano F, Freitas L (2003) A first molecular phylogenetic analysis of Passiflora (Passifloraceae). Amer J Bot 90:1229–1238. doi:10.3732/ajb.90.8.1229 CrossRefPubMedGoogle Scholar
  30. Muschner V, Lorenz-Lemke A, Vecchia M, Bonatto S, Salzano F, Freitas L (2006) Differential organellar inheritance in Passiflora’s (Passifloraceae) subgenera. Genetica 128:449–453. doi:10.1007/s10709-006-7726-4 Google Scholar
  31. Muschner V, Zamberlan PM, Bonatto S, Freitas L (2012) Phylogeny, biogeography and divergence times in Passiflora (Passifloraceae). Genet Molec Biol 35:1036–1043. doi:10.1600/036364413X670359 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Mutis JC, Uribe L (1955) Pasifloráceas y Begoniáceas de la Real Expedición Botánica del Nuevo Reino de Granada. Flora de la Real Expedición Botánica del Nuevo Reino de Granada (1783–1816). Ediciones Cultura Hispánica, MadridGoogle Scholar
  33. Nunes TS (2009) Estudos biosystemáticos em Passiflora L. subgênero Deidamioides (Harms) Killip (Passisfloraceae). PhD Thesis, Universidade Estadual de Feira de Santana-Bahia, Feira de Santana-BahiaGoogle Scholar
  34. Ocampo J, Coppens d’Eeckenbrugge G, Olano C, Schnell R (2004) AFLP analysis for the study of genetic relationships among cultivated Passiflora species of the subgenera Passiflora and Tacsonia. Proc Interamer Soc Trop Hort 47:72–76. doi:10.13140/RG.2.1.4623.8167 Google Scholar
  35. Ocampo J, Coppens d’Eeckenbrugge G, Restrepo M, Salazar M, Jarvis A, Caetano C (2007) Diversity of Colombian Passifloraceae: biogeography an updated list for conservation. Biota Col 8:1–45.
  36. Ocampo J, Coppens d’Eeckenbrugge G, Jarvis A (2010) Distribution of the genus Passiflora L. diversity in Colombia and its potential as an indicator for biodiversity management in the Coffee Growing Zone. Diversity 2:1158–1180. doi:10.3390/d2111158 CrossRefGoogle Scholar
  37. Ocampo J, Arias JC, Urrea R (2016) Interspecific hybridization between cultivated and wild species of genus Passiflora L. Euphytica 209:395–408. doi:10.1007/s10681-016-1647-9 CrossRefGoogle Scholar
  38. Perrier X, Flori A, Bonnot F (2003) Data analysis methods. In: Hamon P, Seguin M, Perrier X, Glaszmann JC (eds) Genetic diversity of cultivated tropical plants. Enfield, Science Publishers, Montpellier, pp 43–76. doi:10.1017/S0014479704252152
  39. Porter-Utley K (2014) A revision of Passiflora L. subgenus Decaloba (DC.) Rchb. supersection Cieca (Medik.) J. M. MacDougal & Feuillet (Passifloraceae). PhytoKeys 43:1–224. doi:10.3897/phytokeys.43.7804 CrossRefGoogle Scholar
  40. Primot S, Coppens d’Eeckenbrugge G, Rioux V, Ocampo J, Garcin F (2005) Variación morfológica de tres especies de curubas (Passiflora tripartita var. mollissima, P. tarminiana y P. mixta) y sus híbridos en el Valle del Cauca (Colombia). Rev Brasil Frutic 27:467–471. doi:10.1590/S0100-29452005000300030
  41. Royal Horticultural Society (2001) RHS Colour Chart. Royal Horticultural Society and Flower Council of Holland, London and LeidenGoogle Scholar
  42. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molec Biol Evol 4:406–425.PubMedGoogle Scholar
  43. Sánchez I, Fajardo A, Grum M, Duque M, Lobo M, Tohme J, Roca W (1999) Variability of chloroplast DNA in the genus Passiflora L. Euphytica 106:15–26. doi:10.1023/A:1003465016168 CrossRefGoogle Scholar
  44. Sazima M, Sazima I (1978) Bat pollination of the passion flower, Passiflora mucronata, in Southeastern Brazil. Biotropica 10:100–109. doi:10.2307/2388012 CrossRefGoogle Scholar
  45. Schoenigger G (1986) La curuba: técnicas para el mejoramiento de su cultivo. Editora Guadalupe, BogotáGoogle Scholar
  46. Segura S, Coppens d’Eeckenbrugge G, Bohórquez A, Ollitrault P, Tohmé J (2002) An AFLP study of the genus Passiflora focusing on subgenus Tacsonia. Genet Resources Crop Evol 49:111–123. doi:10.1023/A:1014731922490 CrossRefGoogle Scholar
  47. Segura S, Coppens d’Eeckenbrugge G, López L, Grum M, Guarino L (2003) Mapping the potential distribution of five species of Passiflora in Andean countries. Genet Resources Crop Evol 50:555–566. doi:10.1023/A:1024424012134 CrossRefGoogle Scholar
  48. Segura S, Coppens d’Eeckenbrugge G, Ocampo CH, Ollitrault P (2005) Isozyme variation in Passiflora subgenus Tacsonia: geographic and interspecific differentiation among the three most common species. Genet Resources Crop Evol 52:455–463. doi:10.1007/s10722-005-2255-z CrossRefGoogle Scholar
  49. Snow N, MacDougal JM (1993) New chromosome reports in Passiflora (Passifloraceae). Syst Bot 18:261–273CrossRefGoogle Scholar
  50. Souza MM, Pereira TNS, Vieira MLC (2008) Cytogenetic studies in some species of Passiflora L. (Passifloraceae): a review emphasizing Brazilian species. Braz Arch Biol Technol 51:247–258. doi:10.1590/S1516-89132008000200003 CrossRefGoogle Scholar
  51. Ulmer T, MacDougal JM (2004) Passiflora: passionflowers of the world. Timber Press Portland, OregonGoogle Scholar
  52. Vanderplank J (2013) A revision of Passiflora section Dysosmia, Passifloraceae. Curtis’s Bot Mag 30:318–387. doi:10.1111/curt.12050 CrossRefGoogle Scholar
  53. Villacís L, Grum M, Coppens d’Eeckenbrugge G (1998) Morphological characterization of Andean Passifloras (Passiflora spp.) from Ecuador. Pl Genet Resources Newsl 115:51–55Google Scholar
  54. Yockteng R, Nadot S (2004a) Infrageneric phylogenies: a comparison of chloroplast-expressed glutamine synthetase, cytosol-expressed glutamine synthetase and cpDNA maturase K in Passiflora. Molec Phylogen Evol 31:397–402. doi:10.1016/S1055-7903(03)00276-8 CrossRefGoogle Scholar
  55. Yockteng R, Nadot S (2004b) Phylogenetic relationships among Passiflora species based on the glutamine synthetase nuclear gene expressed in chloroplast (ncpGS). Molec Phylogen Evol 31:379–396. doi:10.1016/S1055-7903(03)00277-X CrossRefGoogle Scholar
  56. Yockteng R, Coppens d’Eeckenbrugge G, Souza-Chies T (2011) Passiflora L. In: Chittaranjan Kole (ed) Wild crop relatives: genomic and breeding resources. Tropical and subtropical fruits. Springer, Berlin. doi:10.1007/978-3-642-20447-0
  57. Yotoko SC, Dornelas MC, Togni PD, Fonseca TC, Salzano FM, Bonatto SL, Freitas LB (2011) Does variation in genome sizes reflect adaptive or neutral processes? New clues from Passiflora. PLoS ONE 6:e18212. doi:10.1371/journal.pone.0018212.t001 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Wien 2017

Authors and Affiliations

  • John Ocampo Pérez
    • 1
  • Geo Coppens d’Eeckenbrugge
    • 2
  1. 1.Departamento de Ciencias BiológicasUniversidad Nacional de Colombia, sede Palmira (UNAL)/International Center for Tropical Agriculture (CIAT)PalmiraColombia
  2. 2.CIRAD, UMR AGAPMontpellierFrance

Personalised recommendations