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Plant Biol (Stuttg) 2006; 8(6): 748-757
DOI: 10.1055/s-2006-924706
Review Article

Georg Thieme Verlag Stuttgart KG · New York

Recent Progress in Understanding the Evolution of Carnivorous Lentibulariaceae (Lamiales)

K. F. Müller1 , T. Borsch1 , L. Legendre2 , S. Porembski3 , W. Barthlott1
  • 1Nees-Institut für Biodiversität der Pflanzen, Rheinische Friedrich-Wilhelms-Universität Bonn, Meckenheimer Allee 170, 53111 Bonn, Germany
  • 2Laboratory of Plant Biology of Aromatic and Medicinal Herbs, Faculty of Science and Technology, University Jean Monnet, Rue Dr Paul Michelon, 42023 Saint Etienne, France
  • 3Institute of Biodiversity Research, Department of Botany, University of Rostock, Wismarsche Straße 8, 18051 Rostock, Germany
Further Information

Publication History

Received: June 30, 3006

Accepted: October 9, 2006

Publication Date:
03 January 2007 (online)

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Abstract

Carnivorous plants have emerged as model systems for addressing many ecological and evolutionary questions, and since Lentibulariaceae comprise more than half of all known carnivorous species (325 spp.), they are of particular interest. Studies using various molecular markers have established that Lentibulariaceae and their three genera are monophyletic with Pinguicula being sister to a Genlisea-Utricularia-clade, while the closest relatives of the family remain uncertain. Character states of the carnivorous syndrome in related proto-carnivorous lamialean families apparently emerged independently. In Utricularia, the terrestrial habit has been reconstructed as plesiomorphic, and an extension of subgenus Polypompholyx is warranted. In the protozoan-attracting Genlisea, subgenus Tayloria is revealed as basal lineage. In Pinguicula, the six major lineages found reflect radiations in clearly defined geographic regions, whereas most previously recognized subgeneric taxa are non-monophyletic. Genlisea and Utricularia exhibit substitutional rates that rank among the highest in angiosperms for the molecular markers analyzed. One possible explanation for this lies in selective constraints on a wide range of genomic regions that may have been lowered due to the use of an alternative mode of acquiring nutrients.

Key words

Carnivorous plants - Lentibulariaceae - Utricularia - Genlisea - Pinguicula - phylogeny - substitutional rates - molecular evolution.

References

  • 1 Albach D. C., Soltis P. S., Soltis D. E., Olmstead R. G.. Phylogenetic analysis of asterids based on sequences of four genes.  Annals of the Missouri Botanical Garden. (2001);  88 163-212
    PubMedGoogle Scholar
  • 2 Albach D. C., Martinez-Ortega M. M., Fischer M. A., Chase M. W.. A new classification of the tribe Veroniceae - problems and a possible solution.  Taxon. (2004);  53 429-452
    PubMedGoogle Scholar
  • 3 Albach D. C., Meudt H. M., Oxelman B.. Piecing together the “new” Plantaginaceae.  American Journal of Botany. (2005);  92 297-315
    PubMedGoogle Scholar
  • 4 Albert V. A., Williams S. E., Chase M. W.. Carnivorous plants: phylogeny and structural evolution.  Science. (1992);  257 1491-1495
    PubMedGoogle Scholar
  • 5 APG2 . An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II.  Botanical Journal of the Linnean Society. (2003);  141 399-436
    CrossrefPubMedGoogle Scholar
  • 6 Barraclough T. G., Savolainen V.. Rate of rbcL gene sequence evolution and species diversification in flowering plants (angiosperms).  Proceedings of the Royal Society B, Biological Sciences. (1996);  263 589-591
    CrossrefPubMedGoogle Scholar
  • 7 Barraclough T. G., Savolainen V.. Evolutionary rates and species diversity in flowering plants.  Evolution. (2001);  55 677-683
    PubMedGoogle Scholar
  • 8 Barthlott W., Porembski S., Fischer E., Gemmel B.. First protozoa-trapping plant found.  Nature. (1998);  392 447
    PubMedGoogle Scholar
  • 9 Barthlott W., Porembski S., Seine R., Theisen I.. Karnivoren. Biologie und Kultur fleischfressender Pflanzen. Stuttgart; Ulmer (2004)
    Google Scholar
  • 10 Baum D. A.. Combining trees as a way of combining datasets for phlylogenetic inference, and the desirability of combining gene trees.  Taxon. (1992);  41 3-10
    CrossrefPubMedGoogle Scholar
  • 11 Bello M. A., Chase M. W., Olmstead R. G., Rønsted N., Albach D. C.. The pàramo endemic Aragoa is the sister genus of Plantago (Plantaginaceae, Lamiales): evidence from plastid rbcL and nuclear ribosomal ITS sequence data.  Kew Bulletin. (2002);  57 585-597
    PubMedGoogle Scholar
  • 12 Bininda-Emonds O. R. P., Sanderson M. J.. Assessment of the accuracy of matrix representation with parsimony analyses.  Systematic Biology. (2001);  47 497-508
    PubMedGoogle Scholar
  • 13 Borsch T., Löhne C., Müller K., Hilu K. W., Wanke S., Worberg A., Barthlott W., Neinhuis C., Quandt D.. Towards understanding basal angiosperm diversification: recent insights using rapidly evolving genomic regions.  Nova Acta Leopoldina NF. (2005);  342 85-110
    PubMedGoogle Scholar
  • 14 Bremer B., Bremer K., Heidari N., Erixon P., Olmstead R. G.. Phylogenetics of asterids based on 3 coding and 3 non-coding chloroplast DNA markers and the utility of non-coding DNA at higher taxonomic levels.  Molecular Phylogenetics and Evolution. (2002);  24 274-301
    CrossrefPubMedGoogle Scholar
  • 15 Brugger J., Rutishauser R.. Bau und Entwicklung landbewohnender Utricularia-Arten.  Botanica Helvetica. (1989);  99 91-146
    PubMedGoogle Scholar
  • 16 Casper S. J.. Monographie der Gattung Pinguicula L.  Bibliotheca Botanica. (1966);  127/128 1-209
    PubMedGoogle Scholar
  • 17 Chevalier A.. Novitates Florae Africanae. Lentibulariaceae.  Mémoire de la Societé Botanique France. (1912);  8 186-188
    PubMedGoogle Scholar
  • 18 Cieslack T., Polepalli J. S., White A., Müller K., Borsch T., Barthlott W., Steiger J., Marchand A., Legendre L.. Phylogenetic analysis of Pinguicula (Lentibulariaceae): chloroplast DNA sequences and morphology support several geographically distinct radiations.  American Journal of Botany. (2005);  92 1723-1736
    PubMedGoogle Scholar
  • 19 Darwin C.. Insectivorous Plants. London; Murray (1875)
    Google Scholar
  • 20 De Candolle A. P.. Prodromus Systematis Naturalis Regni Vegetabilis VIII. Paris; S. G. Mason (1844)
    Google Scholar
  • 21 Dixon K. W., Pate J. S., Bailey W. J.. Nitrogen nutrition of the tuberous sundew Drosera erythrorhiza Lindl. With special reference to catch of arthropod fauna by its glandular leaves.  Australian Journal of Botany. (1980);  28 283-297
    PubMedGoogle Scholar
  • 22 Dörrstock S., Seine R., Porembski S., Barthlott W.. First record of the American Utricularia juncea (Lentibulariaceae) from Africa.  Kew Bulletin. (1996);  579-583
    PubMedGoogle Scholar
  • 23 Farris J. S., Albert V. A., Källersjö M., Lipscomb D., Kluge A. G.. Parsimony jackknifing outperforms neighbor-joining.  Cladistics. (1996);  12 99-124
    CrossrefPubMedGoogle Scholar
  • 24 Felsenstein J.. Confidence limits on phylogenies: an approach using the bootstrap.  Evolution. (1985);  39 783-791
    PubMedGoogle Scholar
  • 25 Fischer E., Porembski S., Barthlott W.. Revision of the genus Genlisea (Lentibulariaceae) in Africa and Madagascar with notes on ecology and phytogeography.  Nordic Journal of Botany. (2000);  20 291-318
    PubMedGoogle Scholar
  • 26 Fischer E., Barthlott W., Seine R., Theisen I.. Lentibulariaceae. Kubitzki, K., ed. The Families and Genera of Vascular Plants. Berlin; Springer (2004)
    Google Scholar
  • 27 Fromm-Trinta E.. Tayloria Fromm-Trinta - nova seca do genere Genlisea St.‐Hil. Boletim do Museu Nacional Rio de Janeiro.  Botanica. (1977);  44 1-4
    PubMedGoogle Scholar
  • 28 Fromm-Trinta E.. Revisao das especies do genero Genlisea St.‐Hil das regioes sudeste e sul do Brasil. In Dissertacao de Mestrado apresentada a Coordenacao do Curso de Pos-Graduacao em Botanica da UFRJ. (1978)
    Google Scholar
  • 29 Fromm-Trinta E.. Revisao do genero Genlisea St.‐Hil. das regioes sudeste e sul do Brasil.  Rodriguésia. (1979);  31 17-139
    PubMedGoogle Scholar
  • 30 Fromm-Trinta E.. Revisao do genero Genlisea St.‐Hil. do Brasil. Boletim do Museu Nacional Rio de Janeiro.  Botanica. (1981);  61 1-21
    PubMedGoogle Scholar
  • 31 Fromm-Trinta E., Taylor P.. Genlisea pallida Fromm-Trinta and Taylor, P. - una nova especie para o genero Genlisea St.‐Hil.  Bradea. (1985);  4 176-179
    PubMedGoogle Scholar
  • 32 Ghebrehiwet M., Bremer B., Thulin M.. Phylogeny of the tribe Antirrhineae (Scrophulariaceae) based on morphological and ndhF sequence data.  Plant Systematics and Evolution. (2000);  220 223-239
    PubMedGoogle Scholar
  • 33 Good R.. New tropical African Lentibulariaceae.  Journal of Botany. (1924);  62 165
    PubMedGoogle Scholar
  • 34 Greilhuber J., Borsch T., Müller K., Worberg A., Porembski S., Barthlott W.. Smallest angiosperm genomes found in Lentibulariaceae, with chromosomes of bacterial size.  Plant Biology. (2006);  8 770-777
    Article in Thieme ConnectPubMedGoogle Scholar
  • 35 Hedges S. B.. The number of replications needed for accurate estimation of the bootstrap p value in phylogenetic studies.  Molecular Biology and Evolution. (1992);  9 366-369
    PubMedGoogle Scholar
  • 36 Hédren M., Chase M. W., Olmstead R. G.. Relationships in the Acanthaceae and related families as suggested by cladistic analysis of rbcL nucleotide sequences.  Plant Systematics and Evolution. (1995);  194 93-109
    PubMedGoogle Scholar
  • 37 Hoggard R. K., Kores P. J., Molvray M., Hoggard G. D., Broughton D. A.. Molecular systematics and biogeography of the amphibious genus Littorella (Plantaginaceae).  American Journal of Botany. (2003);  90 429-435
    PubMedGoogle Scholar
  • 38 Jobson R. W., Albert V. A.. Molecular rates parallel diversification contrasts between carnivorous plant lineages.  Cladistics. (2002);  18 127-136
    PubMedGoogle Scholar
  • 39 Jobson R. W., Playford J., Cameron K. M., Albert V. A.. Molecular phylogenetics of Lentibulariaceae inferred from plastid rps16 intron and trnL‐F DNA sequences: implications for character evolution and biogeography.  Systematic Botany. (2003);  28 157-171
    PubMedGoogle Scholar
  • 40 Jobson R. W., Nielsen R., Laakonen L., Wikström N., Albert V. A.. Adaptive evolution of cytochrome c oxidase: infrastructure for a carnivorous plant radiation.  Proceedings of the National Academy of Sciences of the USA. (2004);  101 18064-18068
    CrossrefPubMedGoogle Scholar
  • 41 Juniper B. E.. The path to plant carnivory. Juniper, B. E. and Southwood, R., eds. Insects and the Plant Surface. London; Echvard Annald (1986)
    Google Scholar
  • 42 Juniper B. E., Robins R. J., Joel D. M.. The Carnivorous Plants. London; Academic Press (1989)
    Google Scholar
  • 43 Kirkpatrick M., Slatkin M.. Searching for evolutionary patterns in the shape of a phylogenetic tree.  Evolution. (1993);  47 1171-1181
    CrossrefPubMedGoogle Scholar
  • 44 Le Strat-Broussaud F.. Organization and specificities of Utricularia traps.  Acta Botanica Gallica. (2000);  147 29-36
    PubMedGoogle Scholar
  • 45 Legendre L.. The genus Pinguicula L. (Lentibulariaceae): an overview.  Acta Botanica Gallica. (2000);  147 77-95
    PubMedGoogle Scholar
  • 46 Lloyd F. E.. Carnivorous plants. In Chronica Botanica Co. Massachusetts; Waltham (1942)
    Google Scholar
  • 47 Lüttge U.. Ecophysiology of carnivorous plants. Lange, O. L. et al., eds. Physiological Plant Ecology, Vol. III. Berlin, Heidelberg; Springer (1983)
    Google Scholar
  • 48 Marschner H.. Mineral Nutrition of Higher Plants. London; Academic Press (1995)
    Google Scholar
  • 49 Meimberg H., Wistuba A., Dittrich P., Heubl G.. Molecular phylogeny of Nepenthaceae based on cladistic analysis of plastid trnK intron sequence data.  Plant Biology. (2001);  3 164-175
    Article in Thieme ConnectPubMedGoogle Scholar
  • 50 Meyers D. G., Strickler R. J.. Capture enhancement in a carnivorous aquatic plant: function of antennae and bristles in Utricularia vulgaris.  Science. (1979);  203 1022-1025
    CrossrefPubMedGoogle Scholar
  • 51 Müller J., Müller K.. TreeGraph: automated drawing of complex tree figures using an extensible tree description format.  Molecular Ecology Notes. (2004);  4 786-788
    CrossrefPubMedGoogle Scholar
  • 52 Müller K., Borsch T., Legendre L., Porembski S., Barthlott W.. A phylogeny of Lentibulariaceae based on sequences of matK and adjacent non-coding regions.  American Journal of Botany. (2000);  87 S145-S146
    PubMedGoogle Scholar
  • 53 Müller K., Borsch T., Legendre L., Porembski S., Theisen I., Barthlott W.. Evolution of carnivory in Lentibulariaceae and the Lamiales.  Plant Biology. (2004);  6 477-490
    Article in Thieme ConnectPubMedGoogle Scholar
  • 54 Müller K.. SeqState-primer design and sequence statistics for phylogenetic DNA data sets.  Applied Bioinformatics. (2005 a);  4 65-69
    CrossrefPubMedGoogle Scholar
  • 55 Müller K.. The efficiency of different search strategies in estimating parsimony jackknife, bootstrap, and Bremer support.  BMC Evolutionary Biology. (2005 b);  5 58
    CrossrefPubMedGoogle Scholar
  • 56 Müller K., Borsch T.. Phylogenetics of Utricularia (Lentibulariaceae) and molecular evolution of the trnK intron in a lineage with high substitutional rates.  Plant Systematics and Evolution. (2005);  250 39-67
    CrossrefPubMedGoogle Scholar
  • 57 Müller K., Hilu K. W., Borsch T.. Phylogenetic utility of rapidly evolving DNA on high taxonomical levels: comparing three cpDNA datasets of basal angiosperms.  Molecular Phylogenetics and Evolution. (2006);  41 99-117
    CrossrefPubMedGoogle Scholar
  • 59 Oliver D.. On the Lentibulariaceae collected in Angola by Dr. Welwitsch, with an enumeration of the African species.  Journal of the Linnean Society, Botany. (1865);  9 145-146
    PubMedGoogle Scholar
  • 60 Olmstead R. G., Michaels H. J., Scott K. M., Palmer J. D.. Monophyly of the asteridae and identification of their major lineages inferred from DNA sequences of rbcL.  Annals of the Missouri Botanical Garden. (1992);  79 249-265
    CrossrefPubMedGoogle Scholar
  • 61 Olmstead R. G., Reeves P. A.. Evidence for the polyphyly of the Scrophulariaceae based on chloroplast rbcL and ndhF sequences.  Annals of the Missouri Botanical Garden. (1995);  82 176-193
    PubMedGoogle Scholar
  • 62 Olmstead R. G., Reeves G., Yen A. C.. Patterns of sequence evolution and implications for parsimony analysis of chloroplast DNA. Soltis, D. E. et al., eds. Molecular Systematics of Plants II: DNA Sequencing. Boston; Kluwer Academic Publishers (1998)
    Google Scholar
  • 63 Olmstead R. G., Kim K.-J., Jansen R. K., Wagstaff S. J.. The phylogeny of asteridae sensu lato based on chloroplast ndhF gene sequences.  Molecular Phylogenetics and Evolution. (2000);  16 96-112
    CrossrefPubMedGoogle Scholar
  • 64 Olmstead R. G., DePamphilis C. W., Wolfe A. D., Young N. D., Elisons W. J., Reeves P. A.. Disintegration of the Scrophulariaceae.  American Journal of Botany. (2001);  88 348-361
    PubMedGoogle Scholar
  • 65 Oxelman B., Backlund M., Bremer B.. Relationships of the Buddlejaceae s. l. investigated using parsimony jackknife and branch support analysis of chloroplast ndhF and rbcL sequence data.  Systematic Botany. (1999);  24 164-182
    PubMedGoogle Scholar
  • 66 Oxelman B., Kornhall P., Olmstead R. G., Bremer B.. Further disintegration of the Scrophulariaceae.  Taxon. (2005);  54 411-425
    PubMedGoogle Scholar
  • 67 Oyama R. K., Baum D. A.. Phylogenetic relationships of North American Antirrhinum (Veronicaceae).  American Journal of Botany. (2004);  91 918-925
    PubMedGoogle Scholar
  • 68 Porembski S., Fischer E., Gemmel B.. Genlisea barthlottii (Lentibulariaceae) - a new species from Guinean inselbergs.  Adansonia. (1996);  18 151-154
    PubMedGoogle Scholar
  • 69 Ragan M. A.. Phylogenetic inference based on matrix representation of trees.  Molecular Phylogenetics and Evolution. (1992);  1 53-58
    CrossrefPubMedGoogle Scholar
  • 70 Rahmanzadeh R., Müller K., Fischer E., Bartels D., Borsch T.. Linderniaceae and Gratiolaceae (Lamiales) are further lineages distinct from Scrophulariaceae.  Plant Biology. (2005);  7 67-78
    Article in Thieme ConnectPubMedGoogle Scholar
  • 71 Reeves P. A., Olmstead R. G.. Evolution of novel morphological and reproductive traits in a clade containing Antirrhinum majus (Scrophulariaceae).  American Journal of Botany. (1998);  85 1047-1056
    CrossrefPubMedGoogle Scholar
  • 72 Richards J. H.. Bladder function in Utricularia purpurea (Lentibulariaceae): is carnivory important?.  American Journal of Botany. (2001);  88 170-176
    PubMedGoogle Scholar
  • 73 Rivadavia F., Kondo K., Kato M., Hasebe M.. Phylogeny of the sundews, Drosera (Droseraceae), based on chloroplast rbcL and nuclear 18S ribosomal DNA sequences.  American Journal of Botany. (2003);  90 123-130
    PubMedGoogle Scholar
  • 74 Rønsted N., Chase M., Albach D. C., Bello M. A.. Phylogenetic relationships within Plantago (Plantaginaceae): evidence from nuclear ribosomal ITS and plastid trnL‐F sequence data.  Botanical Journal of the Linnean Society. (2002);  139 323-338
    CrossrefPubMedGoogle Scholar
  • 75 Rutishauser R., Sattler R.. Complementary and heuristic value of contrasting models in structural botany. III. Case study on shoot-like “leaves” and leave-like “shoots” in Utricularia macrorhiza and U. purpurea (Lentibulariaceae).  Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie. (1989);  111 121-137
    PubMedGoogle Scholar
  • 76 Rutishauser R.. Polymerous leaf whorls in vascular plants: developmental morphology and fuzziness of organ identities.  International Journal of Plant Science. (1999);  160 S81-S103
    CrossrefPubMedGoogle Scholar
  • 77 Rutishauser R., Isler B.. Developmental genetics and morphological evolution of flowering plants, especially bladderworts (Utricularia): fuzzy arberian morphology complements classical morphology.  Annals of Botany. (2001);  88 1173-1202
    CrossrefPubMedGoogle Scholar
  • 78 Saint-Hilaire A.. Voyage dans le district des Diamans du Brésil. Paris; Librairie-Gide (1833)
    Google Scholar
  • 79 Salamin N., Hodkinson T. R., Savolainen V.. Building supertrees: an empirical assesment using the grass family.  Systems Biology. (2002);  51 136-150
    PubMedGoogle Scholar
  • 80 Sanderson M. J., Donoghue M. J.. Shifts in diversification rate with the origin of angiosperms.  Science. (1994);  264 1590-1593
    CrossrefPubMedGoogle Scholar
  • 81 Sanderson M. J., Donoghue M. J.. Reconstructing shifts in diversification rates on phylogenetic trees.  Trends in Ecology and Evolution. (1996);  11 15-20
    CrossrefPubMedGoogle Scholar
  • 82 Sanderson M. J., Wojciechowski M. F.. Diversification rates in a temperate legume clade: are there “so many species” of Astragalus (Fabaceae)?.  American Journal of Botany. (1996);  83 1488-1502
    CrossrefPubMedGoogle Scholar
  • 83 Sanderson M. J.. r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock.  Bioinformatics. (2003);  19 301-302
    CrossrefPubMedGoogle Scholar
  • 84 Savolainen V., Goudet J.. Rate of gene sequence evolution and species diversification in flowering plants: a re-evaluation.  Proceedings of the Royal Society B, Biological Sciences. (1998);  265 603-607
    CrossrefPubMedGoogle Scholar
  • 85 Schnepf E.. Zur Feinstruktur der Drüsen von Drosophyllum lusitanicum.  Planta. (1960);  54 641-674
    CrossrefPubMedGoogle Scholar
  • 86 Schnepf E.. Struktur und Funktion der Golgi-Elemente in Insektivoren-Drüsen.  Berichte der Deutschen Botanischen Gesellschaft. (1961);  74 269
    PubMedGoogle Scholar
  • 87 Seine R., Barthlott W.. Some proposals on the infrageneric classification of Drosera L.  Taxon. (1994);  43 583-589
    PubMedGoogle Scholar
  • 88 Seine R., Porembski S., Balduin M., Theisen I., Wilbert N., Barthlott W.. Different prey strategies of terrestrial and aquatic species in the carnivorous genus Utricularia (Lentibulariaceae).  Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie. (2002);  124 71-76
    PubMedGoogle Scholar
  • 89 Sirova D., Adamec L., Vrba J.. Enzymatic activities in traps of four aquatic species of the carnivorous genus Utricularia.  New Phytologist. (2003);  159 669-675
    CrossrefPubMedGoogle Scholar
  • 90 Slowinski J. B., Guyer C.. Testing the stochasticity of patterns of organismal diversity: an improved null model.  American Naturalist. (1989);  134 907-921
    PubMedGoogle Scholar
  • 91 Slowinski J. B., Guyer C.. Testing whether certain traits have caused amplified diversification: an improved method based on a model of random speciation and extinction.  American Naturalist. (1993);  142 1019-1024
    PubMedGoogle Scholar
  • 92 Stapf O.. Lentibulariaceae. Thiselton-Dyer, W. T., ed. Flora of Tropical Africa IV, Vol. 2. Ashford, Kent; Reeve (1906): 468-499
    Google Scholar
  • 93 Stopp K.. Notiz über die Dehiszenzweise der Kapselfrüchte von Genlisea hispidula Stapf.  Beiträge zur Biologie der Pflanzen. (1958);  34 126-142
    PubMedGoogle Scholar
  • 94 Taylor P.. Lentibulariaceae. Hutchinson, J. and Dalziel, J. M., eds. Flora of West Tropical Africa, 2nd ed., Vol. 3. London; Crown Agents for Oversea Governments and Administrations (1955): 375-381
    Google Scholar
  • 95 Taylor P.. Lentibulariaceae. Maguire, B. et al., eds. Botany of the Guayana Highland, Vol. 7, Memoirs of the New York Botanical Garden. (1967): 201-228
    Google Scholar
  • 96 Taylor P.. Lentibulariaceae. In Flore d'Afrique Centrale (Zaire - Rwanda - Burundi), Vol. Spermatophytes. Meise; Jardin botanique national de Belgique (1972): 1-62
    Google Scholar
  • 97 Taylor P.. Lentibulariaceae. Flora of Tropical East Africa. Rotterdam; Balkema (1973): 1-26
    Google Scholar
  • 98 Taylor P., Fromm-Trinta E.. Una nova espécie para o género Genlisea St.‐Hil., Sect. Tayloria (Lentibulariaceae): Genlisea uncinata P. Taylor and Fromm-Trinta.  Bradea. (1983);  3 365-368
    PubMedGoogle Scholar
  • 99 Taylor P.. Lentibulariaceae. In Flora Zambesiaca, Vol. 8. London; Royal Botanic Gardens (1988): 9-42
    Google Scholar
  • 100 Taylor P.. The genus Utricularia: a taxonomic monograph. In Kew Bulletin Additional Series XIV. London; Royal Botanic Gardens (1989)
    Google Scholar
  • 101 Taylor P.. The genus Genlisea St. Hil. - an annotated bibliography.  Carnivorous Plant Newsletter. (1991);  20 27-33
    PubMedGoogle Scholar
  • 102 Vintejoux C., Shoar-Ghafari A.. Secretion of mucilages by an aquatic carnivorous plant: Utricularia neglecta L. (Lentibulariaceae).  Acta Botanica Gallica. (1997);  144 347-351
    PubMedGoogle Scholar
  • 103 Williams S. E., Albert V. A., Chase M. W.. Relationships of Droseraceae - a cladistic analysis of rbcL sequence and morphological data.  American Journal of Botany. (1994);  81 1027-1037
    CrossrefPubMedGoogle Scholar
  • 104 Wolfe A. D., Datwyler S. L., Randle C. P.. A phylogenetic and biogeographic analysis of the Cheloneae (Scrophulariaceae) based on ITS and matK sequence data.  Systematic Botany. (2002);  27 138-148
    PubMedGoogle Scholar

K. F. Müller

Nees Institute for Biodiversity of Plants
University of Bonn

Meckenheimer Allee 170

53111 Bonn

Germany

Email: kaimueller@uni-bonn.de

Editor: H. Rennenberg