The ant-pollination system of Cytinus hypocistis (Cytinaceae), a Mediterranean root holoparasite

Annals of Botany

Volumn 103, Issue 7, 2009, Pages 1065-1075

  De Vega, Clara ^a   Arista, Montserrat ^b   Ortiz, Pedro L ^b   Herrera, Carlos M ^a   Talavera, Salvador ^b  

^a DEPARTMENT OF CONSERVATION BIOLOGY   (Spain)

^b UNIVERSITY OF SEVILLE   (Spain)

Author keywords

Ant; Breeding system; Cytinaceae; Cytinus hypocistis; Flies; Insects; Mediterranean Basin; Parasitic plant; Pollination; Rafflesiaceae

Indexed keywords

ANT; ECOSYSTEM MODELING; FRUIT PRODUCTION; INTERSPECIFIC VARIATION; PARASITIC PLANT; POLLINATION; REPRODUCTIVE STRATEGY; SEED PRODUCTION; SPATIAL VARIATION; TEMPORAL VARIATION;

ANGIOSPERM; ARTICLE; GROWTH, DEVELOPMENT AND AGING; PARASITOLOGY; PHYSIOLOGY; PLANT ROOT; POLLEN; POLLINATION; SOUTHERN EUROPE;

ANGIOSPERMS; MEDITERRANEAN REGION; PLANT ROOTS; POLLEN; POLLINATION;

INDIAN OCEAN; INDIAN OCEAN ISLANDS; MADAGASCAR; MEDITERRANEAN REGION; MEDITERRANEAN SEA;

CYTINACEAE; CYTINUS; CYTINUS HYPOCISTIS; FORMICIDAE; HEXAPODA; MAMMALIA; RAFFLESIACEAE;

EID: 65349125478     PISSN: 03057364     EISSN: 10958290     Source Type: Journal    
DOI: 10.1093/aob/mcp049     Document Type: Article

References (77)

1. Arista M, Talavera S. 1994. Pollen dispersal capacity and pollen viability of Abies pinsapo Boiss. Silvae Genetica 43: 155-158.
2. Ashman TL, King EA. 2005. Are flower-visiting ants mutualists or antagonists? A study in a gynodioecious wild strawberry. American Journal of Botany 92: 891-895.
3. Bänzinger H. 1996. Pollination of a flowering oddity: Rhizanthes zippelii (Blume) Spach (Rafflesiaceae). Natural History Bulletin of the Siam Society 44: 113-142.
4. Bänzinger H, Pape T. 2004. Flowers, faeces and cadavers: natural feeding and laying habits of flesh flies in Thailand (Diptera: Sarcophagidae, Sarcophaga spp.). Journal of Natural History 38: 1677-1694.
5. Barkman TJ, Lim SH, Salleh M, Nais J. 2004. Mitochondrial DNA sequences reveal the photosynthetic relatives of Rafflesia, the world's largest flower. Proceedings of the National Academic of Sciences of the USA 101: 787-792.
6. Barkman TJ, McNeal JR, Lim SH, et al. 2007. Mitochondrial DNA suggests at least 11 origins of parasitism in angiosperms and reveals genomic chi-merism in parasitic plants. BMC Evolutionary Biology 7: 248. doi:10.1186/1471-2148-7-248
7. Beaman RS, Decker PJ, Beaman JH. 1988. Pollination of Rafflesia (Rafflesiaceae). American Journal of Botany 75: 1148-1162.
8. Beattie AJ, Turnbull C, Knox RB, Williams EG. 1984. Ant inhibition of pollen function: a possible reason why ant pollination is rare. American Journal of Botany 71: 421-426.
9. Beattie AJ, Turnbull C, Hough T, Jobson S, Knox RB. 1985. The vulnerability of pollen and fungal spores to ant secretions: evidence and some evolutionary implications. American Journal of Botany 72: 606-614.
10. Beehler BM. 1994. Canopy-dwelling honeyeater aggressively defends terrestrial nectar resource. Biotropica 26: 459-461.
11. Bouman F, Meijer W. 1994. Comparative structure of ovules and seeds in Rafflesiaceae. Plant Systematics and Evolution 193: 187-212.
12. Burgoyne PM. 2006. A new species of Cytinus (Cytinaceae) from South Africa and Swaziland, with a key to the Southern African species. Novon 16: 315-319.
13. Davis CC, Latvis M, Nickrent DL, Wurdack KJ, Baum DA. 2007. Floral gigantism in Rafflesiaceae. Science 315: 1812.
14. Ferdy JB, Loriot S, Sandmeier M, Lefranc M, Raquin C. 2001. Inbreeding depression in a rare deceptive orchid. Canadian Journal of Botany 79: 1181-1188.
15. Fumero Cabán J, Meléndez-Ackerman E. 2007. Relative pollination effectiveness of floral visitors of Pitcairnia angustifolia (Bromeliaceae). American Journal of Botany 94: 419-424.
16. García MB, Antor RJ, Espadaler X. 1995. Ant pollination of the paleoen-demic dioecious Borderea pyrenaica (Dioscoreaceae). Plant Systematics and Evolution 198: 17-27.
17. García-Franco JG, Rico-Gray V. 1997. Reproductive biology of the holopar-asitic endophyte Bdallophyton bambusarum (Rafflesiaceae). Botanical Journal of the Linnean Society 123: 237-247.
18. Giménez-Benavides L, Dötterl S, Jürgens A, Escudero A, Iriondo JM. 2007. Generalist diurnal pollination provides greater fitness in a plant with nocturnal pollination syndrome: assessing the effects of a SileneHadena interaction. Oikos 116: 1461-1472.
19. Gómez JM. 2000. Effectiveness of ants as pollinators of Lobularia maritima: effects on main sequential fitness components of the host plant. Oecologia 122: 90-97.
20. Gómez JM, Zamora R. 1992. Pollination by ants: consequences of the quantitative effects on a mutualistic system. Oecologia 91: 410-418.
21. Gómez JM, Zamora R. 1999. Generalization vs. specialization in the pollination system of Hermantophylla spinosa (Crucifera). Ecology 80: 796-805.
22. Gómez JM, Zamora R, Hódar JA, García D. 1996. Experimental study of pollination by ants in Mediterranean high mountain and arid habitats. Oecologia 105: 236-242.
23. Gómez LD. 1983. Flora Costaricensis: Rafflesiaceae. Fieldiana Botany 13: 89-93.
24. Harms H. 1935. Rafflesiaceae, Tribe IV. Cytineae. In: Engler A, Harms H eds. Die Natürlichen Planzenfamilien. Leipzig: Wilhelm Engelman, 276-281.
25. Herrera CM. 1987. Components of pollinator 'quality': comparative analysis of a diverse insect assemblage. Oikos 50: 79-90.
26. Herrera CM. 1988. Variation in mutualism: the spatiotemporal mosaic of a pollinator assemblage. Biological Journal of the Linnean Society 35: 95-125.
27. Herrera CM. 1989. Pollinator abundance, morphology, and flower visitation rate: analysis of the 'quantity' component in a plant-pollinator system. Oecologia 80: 241-248.
28. Hickman JC. 1974. Pollination by ants: a low-energy system. Science 184: 1290-1292.
29. Hidayati SN, Meijer W, Baskin JM, Walck JL. 2000. A contribution to the life history of the rare Indonesian holoparasite Rafflesia patma (Rafflesiaceae). Biotropica 32: 408-414.
30. Hölldobler B, Engel-Siegel H. 1984. On the metapleural gland of ants. Psyche 91: 201-224.
31. Hull DA, Beattie AJ. 1988. Adverse effects on pollen exposed to Atta texana and other North American ants: implications for ant pollination. Oecologia 75: 153-155.
32. Ivey CT, Martinez P, Wyatt R. 2003. Variation in pollinator effectiveness in swamp milkweed (Asclepias incarnata). American Journal of Botany 90: 212-223.
33. Jersákova J, Johnson SD. 2006. Lack of floral nectar reduces self-pollination in a fly-pollinated orchid. Oecologia 147: 60-68.
34. Johnson SD, Burgoyne PM, Harder LD, Dötterl S. 2008. Evidence for pollination by small mammals in the parasitic plant Cytinus visseri (Cytinaceae). South African Journal of Botany 74: 369 [SAAB Annual Meeting Abstracts].
35. Kuijt J. 1969. The biology of parasitic flowering plants. Berkeley, CA: University of California Press.
36. Larsson M. 2005. Higher pollinator effectiveness by specialist than generalist flower-visitors of unspecialized Knautia arvensis (Dipsacaceae). Oecologia 146: 394-403.
37. Li P, Luo Y, Bernhardt P, Kou Y, Perner H. 2008. Pollination of Cypripedium plectrochilum (Orchidaceae) by Lasioglossum spp. (Halictidae): the roles of generalist attractants versus restrictive floral architecture. Plant Biology 10: 220-230.
38. Mabberley D. 1997. The plant book, 2nd edn. Cambridge: Cambridge University Press.
39. Martin FW. 1959. Staining and observing pollen tubes in the styles by means of fluorescence. Stain Technology 34: 125-128.
40. Matuda E. 1947. On the genus Mitrastemon. Bulletin of the Torrey Botanical Club 74: 133-141.
41. McDade LA, Kinsman S. 1980. The impact of floral parasitism in two neotropical hummingbird-pollinated plant species. Evolution 34: 944-958.
42. Meijer W. 1993. Rafflesiaceae. In: Kubitzki K, Rohwer JG, Bittrich V eds. The families and genera of vascular plants, vol. II. Berlin: Sringer-Verlag, 557-563.
43. Molau U. 1995. Reproductive ecology and biology. In: Press MC, Graves JD eds. Parasitic plants. London: Chapman and Hall, 141-177.
44. Nickrent DL. 2002a. Plantas parásitas en el mundo. In: López-Sáez JA, Catalán P, Sáez L eds. Plantas Parásitas de la Península Ibérica e Islas Baleares. Madrid: Mundi-Prensa Libros S.A., 7-28.
45. Nickrent DL. 2002b. Origen filogenético de las plantas parásitas. In: López-Sáez JA, Catalán P, Sáez L eds. Plantas Parásitas de la Península Ibérica e Islas Baleares. Madrid: Mundi-Prensa Libros S.A., 29-56.
46. Nickrent DL, Duff RJ, Colwell AE, et al. 1998. Molecular phylogenetic and evolutionary studies of parasitic plants. In: Soltis DE, Soltis PS, Doyle JJ eds. Plant molecular systematics II. Boston, MA: Kluwer, 211-241.
47. Nickrent DL, Blarer A, Qiu YL, Vidal-Russell R, Anderson FE. 2004. Phylogenetic inference in Rafflesiales: the influence of rate heterogeneity and horizontal gene transfer. BMC Evolutionary Biology 4: 40. doi:10.1186/1471-2148-4-40
48. Nybom H. 2004. Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Molecular Ecology 13: 1143-1155.
49. Pannell JR, Barrett SCH. 1998. Baker's law revised: reproductive assurance in a metapopulation. Evolution 52: 657-668.
50. Peakall R. 1989. The unique pollination of Leporellafimbriata (Orchidaceae): Pollination by pseudocopulating male ants (Myrmecia urens, Formicidae). Plant Systematics and Evolution 167: 137-148.
51. Peakall R, Beattie AJ. 1989. Pollination of the orchid Microtis parviflora R. Br. by flightless worker ants. Functional Ecology 3: 515-522.
52. Peakall R, Beattie AJ. 1991. The genetic consequences of worker ant pollination in a self-compatible, clonal orchid. Evolution 45: 1837-1848.
53. Peakall R, Beattie AJ, James SH. 1987. Pseudocopulation of an orchid by male ants: a test of two hypotheses accounting for the rarity of ant pollination. Oecologia 73: 522-524.
54. Peitsch D, Fietz A, Hertel H, Desouza J, Ventura DF, Menzel R. 1992. The spectral input systems of hymenopteran insects and their receptor-based color-vision. Journal of Comparative Physiology A 170: 23-40.
55. Philpott SM, Greenberg R, Bichier P. 2005. The Influence of ants on the foraging behavior of birds in an agroforest. Biotropica 37: 468-471.
56. van der Pijl L. 1961. Ecological aspects of flower evolution. II. Zoophilous flower classes. Evolution 15: 44-59.
57. Puterbaugh MN. 1998. The roles of ants as flowers visitors: experimental analysis in three alpine plant species. Oikos 83: 36-46.
58. Ramsey M. 1995. Ant pollination of the perennial herb Blandfordia grandiflora (Liliaceae). Oikos 74: 265-272.
59. Schürch S, Pfunder M, Roy BA. 2000. Effects of ant on the reproductive success of Euphorbia cyparissias and associated pathogenic rust fungi. Oikos 88: 6-12.
60. Schemske DW, Lande R. 1985. The evolution of self-fertilization and inbreeding depression in plants. II. Empirical observations. Evolution 39:41-52.
61. Shen H, Ye W, Hong L, et al. 2006. Progress in parasitic plant biology: host selection and nutrient transfer. Plant Biology 8: 175-185.
62. Sugiura N, Miyazaki S, Nagaishi S. 2006. A supplementary contribution of ants in the pollination of an orchid, Epipactis thunbergii, usually pollinated by hover flies. Plant Systematics and Evolution 258: 17-26.
63. Smithson A. 2006. Pollinator limitation and inbreeding depression in orchid species with and without nectar rewards. New Phytologist 169: 419-430.
64. StatSoft Inc. 2001. STATISTICA (data analysis software), version 6. http://www.statsoft.com
65. Stebbins GL. 1957. Self-fertilization and population variability in the higher plants. American Naturalist 91: 337-354.
66. Stewart GR, Press MC. 1990. The physiology and biochemistry of parasitic angiosperms. Annual Review of Plant Physiology and Plant Molecular Biology 41: 127-151.
67. Svensson L. 1985. An estimate of pollen carryover by ants in a natural population of Scleranthus perennis L. (Caryophyllaceae). Oecologia 66: 373-377.
68. Thompson JD. 2001. How do visitation patterns vary among pollinators in relation to floral display and floral design in a generalist pollination system? Oecologia 126: 386-394.
69. de Vattimo I. 1971. Contribuição ao conhecimento da tribu Apodantheae R. Br. Parte 1 Conspecto das espécies (Rafflesiaceae). Rodriguésia 26: 37-62.
70. de Vega C. 2007. Reproductive biology of Cytinus hypocistis (L.) L.: host-parasite interactions. Ph.D. Thesis, University of Seville, Spain.
71. de Vega C, de Oliveira RC. 2007. A new procedure for making observations of embryo morphology in dust-like seeds with rigid coats. Seed Science Research 17: 63-67.
72. de Vega C, Ortiz PL, Arista M, Talavera S. 2007. The endophytic system of Mediterranean Cytinus (Cytinaceae) developing on five host Cistaceae species. Annals of Botany 100: 1209-1217.
73. de Vega C, Berjano R, Arista M, Ortiz PL, Talavera S, Stuessy TF. 2008. Genetic races associated with the genera and sections of host species in the holoparasitic plant Cytinus (Cytinaceae) in the Western Mediterranean basin. New Phytologist 178: 875-887.
74. Visser J. 1981. South African parasitic flowering plants. Capetown: Juta & Co.
75. Wallace LE. 2003. The cost of inbreeding in Platanthera leucophaea (Orchidaceae). American Journal of Botany 90: 235-242.
76. Webb DA. 1964. Cytinus. In: Tutin TG, Heywood VH, Burges NA, Valentine DH, Walters SM, Webb DA eds. Flora Europaea. Cambridge: Cambridge University Press, 75.
77. Wyatt R. 1981. Ant-pollination of the granite outcrop endemic Diamorpha smallii (Crassulaceae). American Journal of Botany 68: 1212-1217.