Skip to main content
SpringerLink
Log in

Pollen evolution and its taxonomic significance in Cuscuta (dodders, Convolvulaceae)

  • Original Article
  • Published:
Plant Systematics and Evolution Aims and scope Submit manuscript

Abstract

The pollen morphology of 148 taxa (135 species and 13 varieties) of the parasitic plant genus Cuscuta (dodders, Convolvulaceae) was examined using scanning electron microscopy. Six quantitative characters were coded using the gap-weighting method and optimized onto a consensus tree constructed from three large-scale molecular phylogenies of the genus based on nuclear internal transcribed spacer (ITS) and plastid trn-LF sequences. The results indicate that 3-zonocolpate pollen is ancestral, while grains with more colpi (up to eight) have evolved only in two major lineages of Cuscuta (subg. Monogynella and clade O of subg. Grammica). Complex morphological intergradations occur between species when their tectum is described using the traditional qualitative types—imperforate, perforate, and microreticulate. This continuous variation is better expressed quantitatively as “percent perforation,” namely the proportion of perforated area (puncta or lumina) from the total tectum surface. Tectum imperforatum is likely the ancestral condition, while pollen grains with increasingly larger perforation areas have evolved multiple times. The reticulated tectum, unknown in other Convolvulaceae, has evolved in Cuscuta only in two lineages (subg. Monogynella, and clade O of subg. Grammica). Overall, the morphology of pollen supports Cuscuta as a sister to either the “bifid-style” Convolvulaceae clade (Dicranostyloideae) or to one of the members of this clade. Pollen characters alone are insufficient to reconstruct phylogenetic relationships; however, palynological information is useful for the species-level taxonomy of Cuscuta.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics Intl 11:36–42

    Google Scholar 

  • Austin DF (1973a) The American Erycibeae (Convolvulaceae). Maripa, Dicranostyles and Lysiostyles. I. Systematics. Ann Missouri Bot Gard 60:306–412

    Article  Google Scholar 

  • Austin DF (1973b) The American Erycibeae (Convolvulaceae). Maripa, Dicranostyles and Lysiostyles. II. Palynology. Pollen Spores 15:203–226

    Google Scholar 

  • Austin DF (1998) Parallel and convergent evolution in the Convolvulaceae. In: Mathews P, Sivadasan M (eds) Biodiversity and taxonomy of tropical flowering plants. Mentor Books, Calicut, pp 201–234

    Google Scholar 

  • Blackmore S, Crane PR (1998) The evolution of apertures in the spores and pollen grains of embryophytes. In: Owens SJ, Rudall PJ (eds) Reproductive biology. Royal Botanic Garden, Kew, pp 159–182

    Google Scholar 

  • Borsch T, Barthlott W (1998) Structure and evolution of metareticulate pollen. Grana 37:68–78

    Article  Google Scholar 

  • Costea M (2007-onwards) Digital atlas of Cuscuta (Convolvulaceae). Wilfrid Laurier University Herbarium, Ontario, Canada. https://www.wlu.ca/page.php?grp_id=2147&p=8968 (accessed 2 June 2009)

  • Costea M, Stefanović S (2009a) Cuscuta jepsonii (Convolvulaceae), an invasive weed or an extinct endemic? Am J Bot 96:1744–1750

    Article  Google Scholar 

  • Costea M, Stefanović S (2009b) Molecular phylogeny of Cuscuta californica complex (Convolvulaceae) and a new species from New Mexico and Trans-Pecos. Syst Bot 34:570–579

    Article  Google Scholar 

  • Costea M, Tardif FJ (2006) Biology of Canadian weeds. Cuscuta campestris Yuncker, C. gronovii Willd. ex Schult., C. umbrosa Beyr. ex Hook., C. epithymum (L.) L. and C. epilinum Weihe. Can J Plant Sci 86:293–316

    Google Scholar 

  • Costea M, Nesom GL, Stefanović S (2006a) Taxonomy of Cuscuta gronovii and Cuscuta umbrosa (Convolvulaceae). Sida 22:197–207

    Google Scholar 

  • Costea M, Nesom GL, Stefanović S (2006b) Taxonomy of the Cuscuta pentagona complex (Convolvulaceae) in North America. Sida 22:151–175

    Google Scholar 

  • Costea M, Nesom GL, Stefanović S (2006c) Taxonomy of the Cuscuta indecora (Convolvulaceae) complex in North America. Sida 22:209–225

    Google Scholar 

  • Costea M, Nesom GL, Stefanović S (2006d) Taxonomy of the Cuscuta salina-californica complex (Convolvulaceae). Sida 22:176–195

    Google Scholar 

  • Costea M, Aiston F, Stefanvović S (2008a) Species delimitation, phylogenetic relationships, and two new species in the Cuscuta gracillima complex (Convolvulaceae). Botany 86:670–681

    Article  CAS  Google Scholar 

  • Costea M, García-Ruiz I, Welsh M (2008b) A new species of Cuscuta (Convolvulaceae) from Michoacan Mexico. Brittonia 3:235–239

    Google Scholar 

  • Cox PA (1988) Hydrophilous pollination. Annu Rev Ecol Syst 19:261–279

    Article  Google Scholar 

  • Dajoz I, Till-Bottraud I, Gouyon PH (1991) Evolution of pollen morphology. Science 253:66–68

    Article  PubMed  CAS  Google Scholar 

  • Das S, Banerji ML (1966) Pollen morphology of a new species of Cuscuta. Curr Sci (India) 35:105–106

    Google Scholar 

  • Dawson JH, Musselman LJ, Wolswinkel P, Dorr I (1994) Biology and control of Cuscuta. Rev Weed Sci 6:265–317

    Google Scholar 

  • Doyle JA (2005) Early evolution of angiosperm pollen as inferred from molecular and morphological phylogenetic analyses. Grana 44:227–251

    Article  Google Scholar 

  • Doyle JA (2008) Evolutionary significance of granular exine structure in the light of phylogenetic analyses. Rev Palaeobot Palynol. doi:10.1016/j.revpalbo.2008.08.001

  • Engelmann G (1859) Systematic arrangement of the species of the genus Cuscuta with critical remarks on old species and descriptions of new ones. Trans Acad Sci St Louis 1:453–523

    Google Scholar 

  • Erdtman G (1966) Sporoderm morphology and morphogenesis. A collocation of data and suppositions. Grana Palynol 6:317–323

    Article  Google Scholar 

  • Ferguson FLS, Skvarla JJ (1982) Pollen morphology in relation to pollinators in Papilionoideae (Leguminosae). Bot J Linn Soc 84:183–193

    Article  Google Scholar 

  • Ferguson K, Verdcourt B, Poole MM (1977) Pollen morphology in the genera Merremia and Operculina (Convolvulaceae) and its taxonomic significance. Kew Bull 31:763–773

    Article  Google Scholar 

  • Fogelberg SO (1938) The cytology of Cuscuta. Bull Torrey Bot Club 65:631–645

    Article  Google Scholar 

  • García MA, Castroviejo S (2003) Estudios citotaxonómicos en las especies ibéricas del género Cuscuta (Convolvulaceae). Anales Jard Bot Madrid 60:33–44

    Google Scholar 

  • García MA, Martin MP (2007) Phylogeny of Cuscuta subgenus Cuscuta (Convolvulaceae) based on nrDNA ITS and chloroplast trnL intron sequences. Sys Bot 32:899–916

    Google Scholar 

  • García-Cruz J, Sosa V (2006) Coding quantitative character data for phylogenetic analysis: a comparison of five methods. Sys Bot 31:302–309

    Article  Google Scholar 

  • Gibbs PE, Ferguson IK (1987) Correlations between pollen exine sculpturing and angiosperm self-incompatibility systems—a reply. Plant Syst Evol 157:143–159

    Article  Google Scholar 

  • Hallier H (1893) Versuch einer natuerlichen Gliederung der Convolvulaceen auf morphologischer und anatomischer Grundlage. Bot Jahrb Syst Pflanzengesch Pflanzengeogr 16:453–591

    Google Scholar 

  • Harley MM, Ferguson IK (1990) The role of the SEM in pollen morphology and plant systematics. In: Claugher D (ed) Scanning electron microscopy in taxonomy and functional morphology. Oxford University Press, Oxford, pp 45–68

    Google Scholar 

  • Hesse M (2000) Pollen wall stratification and pollination. Plant Syst Evol 222:1–17

    Article  Google Scholar 

  • Hsiao LC, Kuoh CS (1995) Pollen morphology of the Ipomea (Convolvulaceae) in Taiwan. Taiwania 40:229–316

    Google Scholar 

  • Jain RK, Nanda S (1966) Pollen morphology of some recent plants of Pilani, Rajasthan. Palynol Bull Lucknow, II and III:56–69

  • Kaul MLH, Bhan AK (1977) Cytogenetics of polyploids VI. Cytology of tetraploid and hexaploid Cuscuta reflexa Roxb. Cytologia 42:125–136

    Google Scholar 

  • Leite K, Simao-Bianchini R, Santos F (2005) Morphology pollen of species genus Merremia Dennst. (Convolvulaceae) occurring in Bahia State, Brazil. Acta Bot Bras 19:313–321

    Article  Google Scholar 

  • Lewis WH (1971) Pollen differences between Stylisma and Bonamia. Brittonia 23:331–334

    Article  Google Scholar 

  • Lewis WH, Oliver RL (1965) Realignment of Calystegia and Convolvulus (Convolvulaceae) in Taiwan. Ann Missouri Bot Gard 52:217–222

    Article  Google Scholar 

  • Liao GI, Chen MY, Huoh CS (2005) Pollen morphology of Cuscuta (Convolvulaceae) in Taiwan. Bot Bull Acad Sin 46:75–81

    Google Scholar 

  • Lienau K, Straka H, Friedrich B (1986) Palynologia Madagassica et Mascarenica. Fam. 167–181. Akademie der Wissenschaften und der Literatur, Mainz and Franz Steiner Verlag, Wiesbaden

  • Lisci M, Tanda C, Pacini E (1994) Pollination ecophysiology of Mercurialis annua L. (Euphorbiaceae), an anemophilous species flowering all year round. Ann Bot 74:125–135

    Article  Google Scholar 

  • Maddison DR, Maddison WP (2000) MacClade 4: analysis of phylogeny and character evolution. Sinauer Associates, Sunderland

    Google Scholar 

  • Maddison WP, Donoghue MJ, Maddison DR (1984) Outgroup analysis and parsimony. Syst Zool 33:83–103

    Article  Google Scholar 

  • Manitz H (1970) Beiträge zur Pollenmorphologie und Systematik der Convolvulaceen-Gattungen Maripa und Mouroucoa. Feddes Repert 82:167–181

    Article  Google Scholar 

  • Martin HA (2001) The family Convolvulaceae in the tertiary of Australia: evidence from pollen. Aust J Bot 49:221–234

    Article  Google Scholar 

  • McNeal JR, Arumugunathan K, Kuehl JV, Boore JL, dePamphilis CW (2007) Systematics and plastid genome evolution of the cryptically photosynthetic parasitic plant genus Cuscuta (Convolvulaceae). BMC Biol 5:55. doi:10.1186/1741-7007-5-55

    Article  PubMed  CAS  Google Scholar 

  • Menemen Y, Jury SL (2002) Pollen studies on some species of the genus Convolvulus L. (Convolvulaceae) from Morocco. Turk J Bot 26:141–148

    Google Scholar 

  • Mignot A, Hoss C, Dajoz I, Leuret C, Henry JP, Druillaux JM, Heberle-Bors E, Till-Bottraud I (1994) Pollen aperture polymorphism in the angiosperms; importance, possible causes and consequences. Acta Bot Gallica 141:109–122

    Google Scholar 

  • Muller J (1970) Palynological evidence on early differentiation of angiosperms. Biol Rev 54:417–450

    Article  Google Scholar 

  • Parker C, Riches C (1993) Parasitic weeds of the world: biology and control. CABA, Wallingford

    Google Scholar 

  • Pazy B, Plitmann U (1995) Chromosome divergence in the genus Cuscuta and its systematic implications. Caryologia 48:173–180

    Google Scholar 

  • Pichon M (1947) Le genre Humbertia. Notulae Systematicae 13:13–25

    Google Scholar 

  • Punt W, Hoen PP, Blackmore S, Nilsson S, Le Thomas A (2007) Glossary of pollen and spore terminology. Rev Paleobot Palyno 143:1–81

    Article  Google Scholar 

  • Rao AN, Lee YK (1970) Studies on Singapore pollen. Pac Sci 24:255–268

    Google Scholar 

  • Ressayre A, Godelle B, Raquin C, Gouyon PH (2002) Aperture pattern ontogeny in angiosperms. J Exp Zoo 294:122–135

    Article  Google Scholar 

  • Ressayre A, Dreyer L, Triki-Teurtroy S, Forchioni A, Nadot S (2005) Post-meiotic cytokinesis and pollen aperture pattern ontogeny: comparison of development in four species differing in aperture pattern. Am J Bot 92:576–583

    Article  Google Scholar 

  • Robertson KR (1971) The genus Jacquemontia (Convolvulaceae) in North and Central America and the West Indies. Ph.D. dissertation. Washington University

  • Robertson KR (1982) Odonellia, a new genus of Convolvulaceae from tropical America. Brittonia 34:417–423

    Article  Google Scholar 

  • Schols P, Dessein S, D’hondt C, Huysmans S, Smets E (2002) CARNOY: a new digital measurement tool for palynology. Grana 41:124–126

    Article  Google Scholar 

  • Schols P, D’hondt C, Geuten K, Merckx V, Jamssens S, Smets E (2004) MorphoCode: coding quantitative data for phlyogenetic analysis. PhyloInformatics 4:1–4

    Google Scholar 

  • Sengupta S (1972) On the pollen morphology of Convolvulaceae with special reference to its taxonomy. Rev Palaeobot Palyno 13:157–212

    Article  Google Scholar 

  • Staples GW, Carine M, Austin DF (2009) Convolvulaceae pollen atlas. University of Arizona Herbarium. http://ag.arizona.edu/herbarium/assoc/projects/convolv/Convolvulaceae_Pollen_Atlas.htm (accessed 5 April 2009)

  • Stefanović S, Olmstead RG (2004) Testing the phylogenetic position of a parasitic plant (Cuscuta, Convolvulaceae, Asteridae): Bayesian inference and the parametric bootstrap on data drawn from three genomes. Syst Biol 53:384–399

    Article  PubMed  Google Scholar 

  • Stefanović S, Krueger L, Olmstead RG (2002) Monophyly of the Convolvulaceae and circumscription of their major lineages based on DNA sequences of multiple chloroplast loci. Am J Bot 89:1510–1522

    Article  Google Scholar 

  • Stefanović S, Austin D, Olmstead RG (2003) Classification of the Convolvulaceae: a phylogenetic approach. Syst Bot 28:791–806

    Google Scholar 

  • Stefanović S, Kuzmina M, Costea M (2007) Delimitation of major lineages within Cuscuta subgenus Grammica (Convolvulaceae) using plastid and nuclear DNA sequences. Am J Bot 94:568–589

    Article  Google Scholar 

  • Stuessy TF (2008) Plant taxonomy: the systematic evaluation of comparative data, 2nd edn. Columbia University Press, New York

    Google Scholar 

  • Swiderski DL, Zelditch ML, Fink WL (1998) Why morphometrics is not special: coding quantitative data for phylogenetic analysis. Syst Biol 47:508–519

    CAS  PubMed  Google Scholar 

  • Tanaka N, Uehara K, Murata J (2004) Correlation between pollen morphology and pollination mechanisms in the Hydrocharitaceae. J Plant Res 117:265–276

    Article  PubMed  Google Scholar 

  • Tellería MC, Daners G (2003) Pollen types in southern New World Convolvulaceae and their taxonomic significance. Plant Syst Evol 243:99–118

    Article  Google Scholar 

  • Thiele K (1993) The holy grail of the perfect character: the cladistic treatment of morphometric data. Cladistics 9:275–304

    Article  Google Scholar 

  • Till-Bottraud I, De Paepe R, Mignot A, Dajoz I (1995) Pollen heteromorphism in Nicotiana tabacum (Solanaceae). Am J Bot 82:1040–1048

    Article  Google Scholar 

  • Till-Bottraud I, Vincent M, Dajoz I, Mignot A (1999) Pollen aperture heteromorphism: variation in pollen type proportions along altitudinal transects in Viola calcarata (Violaceae). Comptes Rendus de L Académie des Sciences Serie 3. Sciences de la Vie 322:579–589

    CAS  PubMed  Google Scholar 

  • Van Campo M (1976) Patterns of pollen morphological variation within taxa. In: Ferguson IK, Muller J (eds) The evolutionary significance of the exine. Academic, London, pp 125–135

    Google Scholar 

  • Vezey EL, Skvarla JJ, Vanderpool SS (1991) Characterizing pollen sculpture of three closely related Capparaceae species using quantitative image analysis of scanning electron micrographs. In: Blackmore S, Barnes SH (eds) Pollen and spores—patterns of diversification. Clarendon, Oxford, pp 291–300

    Google Scholar 

  • Vezey EL, Shah VP, Skvarla JJ (1992) A numerical approach to pollen sculpture terminology. Plant Syst Evol 181:245–254

    Article  Google Scholar 

  • Vishnu-Mittre (1964) Contemporary thought in palynology. Phytomorph 14:135–147

    Google Scholar 

  • Wiens JJ (2001) Character analysis in morphological phylogenetics: problems and solutions. Syst Biol 50:689–699

    Article  CAS  PubMed  Google Scholar 

  • Wodehouse RP (1936) Evolution of pollen grains. Bot Rev 2:67–84

    Article  Google Scholar 

  • Yuncker TG (1932) The genus Cuscuta. Mem Torrey Bot Club 18:113–331

    Google Scholar 

  • Zavada MS (1984) The relation between pollen exine sculpturing and self-incompatibility mechanisms. Plant Syst Evol 147:63–78

    Article  Google Scholar 

  • Zavada MS (1990) Correlations between pollen exine sculpturing and angiosperm self-incompatibility systems—a rebuttal. Taxon 39:442–447

    Article  Google Scholar 

Download references

Acknowledgments

The authors warmly thank the curators and directors of AAU, ALTA, ARIZ, ASU, B, BAB, BOL, BRIT, CANB, CAS, CEN, CHR, CHSC, CIIDIR, CIMI, CTES, DAO, ENCB, F, G, GH, H, HUFU, IAC, IBUG, IEB, IND, J, JEPS, LL, LP, LPB, LPS, K, MEL, MERL, MEXU, MICH, MO, NMC, NU, NY, OKLA, OSU, OXF, PACA, PRE, QCNE, QFA, P, PACA, RB, RSA, SAM, S, SD, SGO, SI, SPF, TEX, TRT, UA, UB, UBC, UCR, UCT, UNB, UNM, UPRRP, UPS, US, USAS, VEN, WTU, and XAL for supplying plant material. We also thank Frédérique Guinel and two anonymous reviewers for their comments on an earlier version of the manuscript. Thierry Deroin provided the information about the pollen of Humbertia. This research was supported by Discovery grants from the Natural Sciences and Engineering Research Council (NSERC) of Canada to M. Costea (327013–06) and to S. Stefanović (326439–06).

Author information

Authors and Affiliations

  1. Department of Biology, Wilfrid Laurier University, Waterloo, ON, N2L 3C5, Canada

    Mark Welsh & Mihai Costea

  2. Department of Biology, University of Toronto Mississauga, Mississauga, ON, L5L 1C6, Canada

    Saša Stefanović

Authors
  1. Mark Welsh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Saša Stefanović
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mihai Costea
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mihai Costea.

Electronic supplementary material

Below is the link to the electronic supplementary material.

606_2009_259_MOESM1_ESM.jpg

Online resource 1: Pollen size optimized onto a summary consensus tree resulted from three molecular phylogenies of Cuscuta based on nuclear ITS and plastid trnL-F sequences (García and Martin 2007; Stefanović et al. 2007; Stefanović and Costea, personal communication). Pollen size is polymorphic but the species of subg. Monogynella have the largest pollen grains

Appendix

Appendix

Vouchers used for scanning electron microscopy. Species (arranged in alphabetical order), country, collector, collector number, herbarium acronym from Index Herbariorum.

Cuscuta acuta Engelm. Ecuador, Galapagos Islands, Anderson 1853 (S); Fagerlind & Wibom 3401 (S); Howell 10140 (G). C. acutiloba Engelm.: Bolivia, Mardon 1481 (G); Peru, Pennell 13242 (USM). C. africana Thumb.: South Africa, Beyers 6968 (NBG); Oliver 11852 (NBG). C. americana L.: USA, Florida, Small et al. 11596 (NY); Mexico, Van Devender and Reina-G 2000-745 (WLU); Bahamas, Correll 45030 (NY); Cuba, Britton et al. 5917 (NY). C. angulata Engelm.: South Africa, Beyers 6968/13 (NBG); Orchard 460 (NU). C. appendiculata Engelm.: South Africa, Hofmeyr s.n. (GRA); Burrows 4666 (J); Bohnen 7827 (NBG). C. applanata Engelm. USA, New Mexico, Casteller 7339 (UNM); Mexico, Van Devender 2001-710 et al. (WLU). C. approximata Bab.: USA, California, Abrams 457 (CAS); Mexico, Henrickson 13083a (RSA); Puebla, McKee 11042 (MEXU). C. argentiniana Yunck.: Argentina, Krapovickas & Schinini 36049, 36757 (CTES); Brücher s.n. (S); Meyer 12467 (UPS). C. aurea Liebm.: Mexico, Palmer 87 (S); Guerrero, Duran & Garcia 634 (MEXU). C. australis R. Br. var. australis: New Caledonia, Bonati 737 (S); Australia, Conveny 756 (RSA). C. australis var. tinei (Insenga) Yunck.: Hungary, Simonkai 2635 (NY); Karkovány s.n. (WLU). C. bella Yunck.: Peru, Killip & Smith 21827 (US). C. boldinghii Urb.: Mexico, Van Devender 92-31 et al. (ARIZ); Sinaloa, Vega 2630 (MEXU). C. boliviana Yunck.: Argentina, Hunzinker 2676 (S); Ruiz Leal 14817 (MERL), Burkart 12503 (CTES). C. brachycalyx Yunck.: USA, California, Ahart 9856 (CHICO); Colwell AC 04-305 (YM/WLU). C. burrelli Yunck.: Brazil, Heringer et al. 43 (UB); Alvarenga-Pereira 766 (RB). C. californica Hook. & Arn: USA, California, Sanders 25122 (UCR); Pinzl 7238a (NY); White 5033 (ASU). C. campestris Yunck.: USA, Iowa, Fay 4568 (UC); Oklahoma, Lipscomb 1894 (SMU); Puerto Rico, Liogier & Martorell 13908 (UPRRP); Venezuela, Killip & Tamayo 37010 (GH). C. cassytoides Nees: South Africa, Balkwill 6968 (NU); Alexandre 2407 (NBG). C. cephalanthi Engelm.: USA, Illinois, McDonald s.n. (NMS); Missouri, Steyermark 79977(MO); Nebraska, Churchill 4560 (MO). C. chapalana Yunck.: Mexico, Garcia-Ruiz 7942 (CIMI); Jalisco, Carrillo-Reyes & al. 468 (CIMI). C. chilensis Ker Gawl.: Chile, Anderson 84-189 (S); Buchtien s.n. (S); Valeutey 94 (S). C. chinensis Lam.: Australia, Carter 628 (CANB); China, Wang Wen-Tsai 2378 (RSA). C. choisiana Yunck.: Mexico, Véase 490 (MEXU). C. cockerellii Yunck.: Peru, Vargas 2600 (CUS). C. colombiana Yunck.: Colombia, Haught 4535 (NY); Venezuela, Aristeguieta 4500 (VEN); Tamayo 4432 (VEN). C. compacta Juss.: USA Mississippi, McDaniel 27291 (MO); Maryland, Hill 17349 (MO); New Jersey, Moldenke & Moldenke 25129 (NY). C. corniculata Engelm.: Brazil, Stannard et al. 51861 (G); Colombia, Pennell 1453 (GH). C. coryli Engelm.: USA, Arkansas, Demaree 19603 (CAS); Maryland, Killip 31293 (NY); Michigan, Hanes 548 (NY); Nebraska, Reynolds 2727; Tennessee, Rydberg 8179 (NY). C. corymbosa Ruiz & Pav. var. grandiflora Engelm.: Mexico, Garcia-Ruiz et al. 7572 (CIMI, WLU); Iltis & Guzman 29077 (MEXU); Galván & Galván 4681 (MEXU). C. corymbosa var. stylosa (Choisy) Engelm.: Mexico, Rzedowski 28752 (UCR); Bopp 206 (MEXU); Pringle s.n. (MEXU). C. costaricensis Yunck.: Mexico, Reina-G. et al. 2006-1049 (ARIZ, WLU); Van Devender 98-1789 (ARIZ); Wiens 96-125 et al. (WLU). C. cotijana Costea & I. García: Mexico, García Ruiz7412 (CIMI,); García Ruiz et al. 7557 (CIMI); Carranza et al. 7316 (IEB). C. cozumeliensis Yunck.: Guatemala, Kellerman 6580 (F); Mexico, Calzade & Nivea 9427 (XAL); Vazquez 176 (MEXU). C. cristata Engelm.: Meyer 10669 (CTES); Argentina, Cabrera 7144 (NY); Hunzinker 4927 (S); Burkart 14000 (SI). C. cuspidata Engelm.: USA, Arkansas, Demaree 15522 (RSA); Texas, Higgins 12480 (NY); Runyon 2828 (SMU). C. decipiens Yunck.: Mexico, Henrickson 6362, 13394, 22781 (RSA). C. deltoidea Yunck.: Mexico, Orcutt 4457 (MEXU); Pringle 5350 (US); García Ruíz 2516 (CIMI). C. dentatasquamata Yunck.: Mexico, Jones s.n. (RSA); USA, Arizona, Lemmon s.n. (UC). C. denticulata Engelm.: USA, Arizona, Peebles & Parker 14793 (NY); California, Thomas 8904 (UC); Nevada, Perish 10299 (CAS); Utah, Choong s.n. (NY). C. desmouliniana Yunck.: Mexico, Spellenberg 4943 (NMS); Van Devender & Reina-G 2002-23 (WLU); Van Devender 96-360 et al. (WLU). C. draconella Costea & Stefanović: USA, New Mexico, Spellenberg & Mahrt 10497 (NY); Wagner 3395 (UNM); Herman 462 (NY). C. epilinum Weihe: Canada, Quebec, Barabe 16914 (DAO); Sweden, Samuelson 1317 (RSA). C. epithymum (L.) L.: Argentina, Bana 14733 (CTES); USA, New York, Ahles 67695 (SMU); Belgium, Meulebrouck s.n. (WLU). C. erosa Yunck.: USA, Arizona, Jones s.n. (CAS); Mexico, Rebman 4275; Sánchez NF-172 et al. (WLU). C. europea L.: Finland, Alava et al. s.n. (OSU); Sweden, Holmgren 19784 (SD). C. exaltata Engelm.: USA, Texas, Snyder 472 (SMU); Carter 10584 (MO). C. floribunda aff. Kunth: Mexico, Prather & Soule 1221 (TEX). C. flossdorfii Hicken var. pampagrandensis Yunck.: Bolivia, Mendoza & Acebo 919 (MO). C. foetida Kunth var. foetida: Ecuador, Holm-Nielsen & Andrade 18480 (AAU); Holm-Nielsen et al. 5181 (AAU); Peru, Smith 1624 (MO). C. foetida var. pycnantha Yunck: Peru, Plowman et al. 14291 (F). C. friesii Yunck.: Argentina, Krapovickas et al. 21898 (CTES); Saravia Toledo et al. 12993 (CTES); Mulgura 1245 (SI). C. glabrior (Engelm.) Yunck.: USA Texas, Wolff 3270 (NY); Mexico, Marsh 1115 (SMU); Henrickson 13676 (RSA). C. globiflora Engelm.: Argentina, Mulgura et al. 1199 (MO); Bolivia, Plowman & Davis 5196 (GH); Peru, King et al. 247 (USM). C. globulosa Benth: Puerto Rico, Stahl 1064 (S); Urban855 (S); Liogier & Oquendo 180 (UPRRP). C. glomerata Choisy: USA, Texas, Barkley 13886 (RSA); Wolff 3321 (SMU). C. goyaziana Yunck.: Brazil, Macedo 3731 (NY). C. gracillima Engelm.: Mexico, Pringle 6716 (NML); Koch and Fryxell 82253 (NY); García Ruiz 7334 (CIMI, WLU). C. grandiflora Kunth: Argentina, Schinini et al. 34615 (CTES); Ecuador, Løjtnant et al. 11829 (AAU); Tipaz et al. 1563 (QCNE); Peru, Pennell 13613 (GH). C. gronovii Willd. ex Roem. & Schult. var. gronovii: Canada, Ontario, Catling 5111 (DAO). USA Alabama, Kpeooer et al. s.n. (NY); Georgia, Mellinger s.n. (SMU). C. gronovii var. latiflora Engelm.: USA, Missouri, Brant & Donnell 4813 (MO); Texas, Lundell 11721 (SMU); New York, Ferguson 6091 (NY). C. gymnocarpa Engelm. Galapagos Islands, Fagerlind & Wibom3658 (S); Werff 2068 (S); Werff 2136 (NY). C. harperi Small: USA, Alabama, Demaree 46295 (NY); Harper s.n. (NY). C. haughtii Yunck.: Ecuador, Asplund 15974 (S); Holm-Nielsen et al. 2308 (NY). C. howelliana Rubtzoff: USA, California, True 7407 (DS); Oswald & Ahart 7978 (JEPS); Reino & Alava 6809 (JEPS). C. hyalina Roth.: India, Pushpauder s.n. (CANB); Namibia, Bosch 25022 (BOL). C. incurvata Prog.: Paraguay, López et al. 243 (CTES); Anisits 2395 (S); Hassler 8170 (S). C. indecora Choisy var. indecora: USA, California, Wolf 4392 (UC); Louisiana, Allen 19239 (BRIT); New Mexico, Spellenberg et al. 3427 (NY). C. indecora var. attenuata (Waterf.) Costea: USA, Oklahoma, Waterfall 17496 (GH); Texas, Fisher 4118 (CAS); Mexico, Palmer 333 (F). C. indecora var. longisepala Yunck.: Argentina, Leal 7964 (NY); USA Texas, Runyon 2819 (NY). C. jalapensis Schltdl.: Mexico, Ton & Lopez 9826 (NY); Sharp 45380 (NY); Waterfall & Wallis 14213 (SMU). C. japonica Choisy: China, Bartholomew et al. 883 (NY); Japan, Furuse 6890 (RSA). C. jepsonii Yunck.: USA, California, Dudley 1774 (DS); Heller 5981 (UC); Tracy 2349 (UC). C. killimanjari Oliv.: Malawi, Lacroix 4559 (MO); Tanzania, Scheffler 434 (MEL); Zimbabwe, Eyles 352 (J). C. lehmanniana Bunge: Uzbekistan, Vvedensky s.n (MEL); Drobov 3763 (NY). C. leptantha Engelm.: Mexico, Wiggins 17125 (MEXU); Lindsay 2928 (SD); Sanders 7523 (UCR); Van Devender & Reina-G 2000-933 (WLU). C. lindsayi Wiggins: Mexico, Wiggins 13185 (MO). C. longiloba Yunck.: Brazil, Krapovickas & Schinini 31255 (CTES); Paraguay, Casas & Molero 4384 (MO). C. lupuliformis Krock.: Austria, Barta 2004-302 (NY); Netherlands, Lennhouts 2514 (CANB). C. macrocephala W. Schaffn. ex Yunck.: Mexico, Rebman 5743 (SD); Van Devender & Reina-G. 2006-872 (WLU); Reina-G. & Van Devender 2001-774 (WLU). C. mcvaughii Yunck.: Mexico, Hinton et al. 12098 (NY). C. micrantha Choisy: Chile, Philippi 489 (G); Skottsberg 995 (F). C. microstyla Engelm. var. bicolor Hunz.: Argentina, Boelcke et al. 10243 (CTES); Burkart et al. 6968 (SI); Prina et al. 2362 (CTES). C. mitriformis Engelm.: Mexico, Rzedowski 41379 (IEB); Bye 2011 (MEXU); Bye 50488 (UCR). C. monogyna Vahl: Grece, Greuter 11459 (NY); Turkmenistan, Sintenis 1240 (MO). C. natalensis Baker: South Africa, Rudatis 1319 (NBG); Rudatis 2412 (NBG). C. nevadensis I.M. Johnst.: USA, California, Raven 12865 (CAS); Peebles 263 (NY); Nevada, Brandegee s.n. (UC), LaRivers & Hancock 164 (NY). C. nitida E. Mey.: South Africa, Burgers 2649 and 3318 (NBG); Rogers 17342 (J). C. obtusiflora Kunth var. obtusiflora: Argentina, Arbo et al. 7973 (CTES); Bordódon s.n. (CTES). C. obtusiflora Kunth var. glandulosa Engelm.: Cuba, Wright 1659 (GH); USA, California, Parish 2110 (CAS); Delaware, collector illegible (“MC”) s.n. (CAS); Texas, Clare 2144 (CAS). C. occidentalis Millsp.: USA, California, Howell 48868 (CAS); Ertter 7326 (NY); Schoolcraft et al. 2220 (NY); Nevada, Tiehm 12257 (NY); Utah, Garrett 2170 (NY). C. odontolepis Engelm.: Mexico, White 2730 (GH); Van Devender & Reina-G 2006-869; 2006-467 (WLU). C. odorata Ruiz & Pav.: Ecuador, Jaramillo 10372 (AAU); Sparre 16186 (S); Peru, Hitchcock 20320 (GH); Ugent & Ugent5323 (MO). C. orbiculata Yunck.: Brazil, Alvaregna 93605 (RB); Bolivia, Krapovickas et al. 19221 (CTES). C. ortegana Yunck.: Mexico, Hinton et al. 16294 (MICH); Van Devender et al. 2006-74 (WLU). C. paitana Yunck.: Ecuador, Madsen 63940 (QCNE); Peru, Horton 11575 (GH). C. parodiana Yunck.: Argentina, Eyerdam 22423 (MO); Novara 7976 (S); Balegno 447 (SMU). C. partita Choisy: Brazil, Eiten & Eiten 3961 (US); Krapovickas et al. 38723 (CTES); Lindman 3481 (S). C. parviflora Engelm. var. elongata Engelm.: Brazil, Filgueiras 1476 (RB); Oliveira et al. 745 (US). C. pauciflora Phil.: Chile, Werdermann 1884 (SGO). C. pentagona Engelm.: USA, Alabama, Kral 31225 (SMU); Florida, Welch 1633 (NY); North Dakota, Stevens s.n. (NY); Virginia, Weatherby 4230 (NY). C. planiflora Ten.: Australia, Howitt & Zaicon-Kunesch s.n. (PERTH); Palestine, Musselman 10461 (RSA). C. plattensis A. Nelson: USA, Wyoming, Nelson 2741 (MO); Nelson 2768 (NY). C. platyloba Prog.: Argentina, Burkart 10554 (CTES); Brazil, Dusen 10005 (S); Paraguay, Montes 16599 (CTES). C. polygonorum Engelm.: USA Indiana, Yuncker 10836 (NY); Ohio, Core & Anderson s.n. (NY). C. polyanthemos Schaffn. ex Yunck.: Mexico, Wiggins 13153 (SD); Van Devender & Reina-G 2006-809 (WLU). C. potosina W. Schaffn. ex S. Wats. var. potosina: Mexico, Rose et al. 9650 (NY). C. potosina var. globifera W. Schaffn.: Mexico, Perez et al. 3707 (IEB); Pringle 6575 (MEXU); Van Devender 96-451 et al. (WLU); USA, Arizona, Gooding 290-61 (ASU). C. prismatica Pav. ex Choisy: Ecuador, Mille 112 (F); Hitchcock 20141 (GH). C. punana Costea & Stefanović: Ecuador, Madsen 63850 (AAU). C. purpurata Phil.: Chile, Dillon & Teillier 5104 (MO); Johnston 5170 (US); Morong 1143 (US). C. purpusii Yunck.: Mexico, Martinez 1093; (MEXU); Torres Colin 15864 (MEXU); Hendrickson 6608 (RSA). C. racemosa Mart. var. racemosa: Brazil, Pinheiro 55 (SPF). C. racemosa Mart. var. miniata (Mart.) Engelm.: Brazil, Menezes et al. 5100 (CTES); Name illegible 7835 (S); Rapini et al. 491 (WLU). C. reflexa Roxb.: India, Kanta s.n. (ASU); Cullelt s.n. (MEL); Koelz 21955 (NY). C. rostrata Shuttlw. ex Engelm. & A. Gray: USA, North Carolina, Bozeman et al. 45268 (OSU); Tennessee, Jennison 2824 (NY); Texas, Lundell 11480 (SMU). C. rubella Yunck.: Peru, Macbride & Featherstone 371 (NY). C. rugosiceps Yunck.: Mexico, Carranza & Silva 5997 (IEB); Taylor 21457 (SMU). C. runyonii Yunck. USA, Texas, Correll & Johnston 14906 (NY); Lundell 9840 (SMU). C. salina Engelm. var. salina: USA, Arizona, Hammond 10349 (NY); California, Bacigalupi & al. 2667 (DS); Nevada, Tiehm 5991 (CAS). C. salina var. major Yunck.: Canada, Kennedy & Ganders 4947 (UBC); USA, California, Dudley 267 (CAS); Moldenke 25731 (NY). C. sandwichiana Choisy: USA, Hawaii, Stern 8416 (CHICO); Fosberg 9822a (RSA). C. santapaui Banerji & Sitesh Das: Nepal, Nicolson 2796 (MO). C. serrata Yunck.: Brazil, Acevedo & Lopes 848 (RB); Smith 15049 (US). C. sidarum Liebm.: Guatemala, Standley 74614 (NY); Mexico, Ayala 1054 (TEX & LL); Palmer 51 (S); Nicaragua, Stevens & Krukoff 20950 (GH). C. squamata Engelm.: USA, New Mexico, Wooton & Standley 3355 (CAS); Wooton s.n. (NMC); Texas, Hutchins 643 (BRIT). C. stenolepis Engelm.: Ecuador, Jaramillo & Carvajal2307 (AAU); Nuñez et al. 2220 (QCNE); Asplund 6678 (NY). C. strobilacea Liebm.: Mexico, Gentry 5291 (ARIZ); Jones s.n. (RSA). C. suaveolens Ser.: Australia, Alcock 10415 (RSA); Chile, Rusby 2000 (NY); USA, California, Dudley s.n. (CAS). C. subinclusa Durand & Hilg.: USA, California, Dudley 1653 (DS); Ewan 11049 (NY); Mason 5766 (NY). C. suksdorfii Yunck.: USA, California, Oswald & Ahart 5874 (CHICO); Twisselmann 14603 (SD); Tracy 18430 (UC); Bailey & Bailey 2672a (UC). C. tasmanica Engelm.: Australia, Barker s.n. (CANB); Lepschi 908 (CAMB); Watts 1/86 (MEL). C. tinctoria Mart. ex Engelm.: Mexico, Ventura 4248 (IEB); Rzedowski 34596 (IEB); Van Devender 94-1008 et al. (WLU). C. tuberculata Brandegee: USA, Arizona, Beauchamp 3112 (SD); Mexico, Gunn & Felger 19998 (ARIZ); Rodriguez 1642 (MEXU); Reina-G. & Van Devender 2001-624 (WLU). C. umbellata Kunth var. umbellata: Mexico, Nabhan & Rea 167 (ARIZ); Moran 24758 (SD). C. umbellata var. reflexa Yunck.: USA, Arizona, Felger 92-707 (CAS); Mexico, Van Devender 93-1123 et al. (UCR); Van Devender 94-458 et al. (UCR); Van Devender & Reina-G. 2006-638 (WLU). C. umbrosa Beyr. ex Hook: Canada, Alberta, Allen 150 (DAO); Manitoba, Criddle s.n. (DAO); USA Utah, Jones s.n. (CAS); Colorado, Mulford s.n. (NY). C. vandevenderi Costea & Stefanović: Mexico, Van Devender et al. 2006-983; 98-1334 (WLU). C. veatchii Brandegee: Mexico, Porter 198 (MEXU); Rebman 3189 (SD). C. victoriana Yunck.: Australia, Cowie 9624 (CANB); Glennon 379 (CANB). C. werdermanii Yunck.: Chile, Werdermann 880 (SGO). C. woodsonii Yunck.: Guatemala, Molina & Molina 30020 (MO); Panama, Davidson 967 (GH). C. xanthochortos Mart. ex Englem. var. xanthochortos: Argentina, Arbo et al. 6953 (MO); Paraguay, Zardini & Vera 46124 (MO). C. xanthochortos var. carinata Yunck.: Paraguay, Bernardi 18758 (MO), Billiet & Jadin 3294 (MO). C. xanthochortos var. lanceolata Yunck.: Argentina, Schulz 7139 (CTES); Paraguay, Zardini & Villate 46371 (WLU). C. yucatana Yunck.: Mexico, Alava 1341 (CAS; TEX & LL); Nee & Taylor 29575 (MO); Breedlove & Smith 22017 (MO).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Welsh, M., Stefanović, S. & Costea, M. Pollen evolution and its taxonomic significance in Cuscuta (dodders, Convolvulaceae). Plant Syst Evol 285, 83–101 (2010). https://doi.org/10.1007/s00606-009-0259-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00606-009-0259-4

Keywords

Search

Navigation