Hawaiian ant-flower networks: Nectar-thieving ants prefer undefended native over introduced plants with floral defenses

Ecological Monographs

Volumn 81, Issue 2, 2011, Pages 295-311

  Junker, Robert R ^a   Daehler, Curtis C ^b   Stefan, Dötterl ^c   Keller, Alexander ^a   Blëthgen, Nico ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF HAWAII   (United States)

^c UNIVERSITY OF BAYREUTH   (Germany)

Author keywords

Ant flower networks; Biological invasions; Floral antagonists; Hawaii; ITS2; Morphological barriers; Nectar thieves; Olfactometer; Plant defense; Repellent floral scents; Resource quality

Indexed keywords

ANT; ARCHIPELAGO; BIOLOGICAL INVASION; ENDEMIC SPECIES; NECTAR; OLFACTORY CUE; PHYLOGENY; PLANT DEFENSE; PLANT-POLLINATOR INTERACTION; RESOURCE AVAILABILITY;

HAWAII [(ISL) HAWAIIAN ISLANDS]; HAWAII [UNITED STATES]; HAWAIIAN ISLANDS; UNITED STATES;

FORMICIDAE;

EID: 79955518489     PISSN: 00129615     EISSN: 15577015     Source Type: Journal    
DOI: 10.1890/10-1367.1     Document Type: Article

References (109)

1. Adams, R. P. 2007. Identification of essential oil components by gas chromatography/mass spectrometry. Fourth edition.Allured Publishing Corporation, Carol Stream, Illinois, USA.
2. Adler, L. S. 2000. The ecological significance of toxic nectar. Oikos 91:409-420. (Pubitemid 32113777)
3. Allison, S. D., and P. M. Vitousek. 2004. Rapid nutrient cycling in leaf litter from invasive plants in Hawai'i. Oecologia 141:612-619. (Pubitemid 40033028)
4. Amirav, A., and S. Dagan. 1997. A direct sample introduction device for mass spectrometry studies and gas chromatography mass spectrometry analyses. European Mass Spectrometry 3:105-111.
5. Beattie, A. J. 2006. The evolution of ant pollination systems. Botanische Jahrbücher für Systematik 127:43-55.
6. Beattie, A. J., C. Turnbull, T. Hough, S. Jobson, and R. B. Knox. 1985. The vulnerability of pollen and fungal spores to ant secretions: evidence and some evolutionary implications. American Journal of Botany 72:606-614. (Pubitemid 17245667)
7. Beattie, A. J., C. Turnbull, R. B. Knox, and E. G. Williams. 1984. Ant inhibition of pollen function: a possible reason why ant pollination is rare. American Journal of Botany 71:421-426.
8. Benson, D. A., I. Karsch-Mizrachi, D. J. Lipman, J. Ostell, and E. W. Sayers. 2009. GenBank. Nucleic Acids Research 37:D26-D31.
9. Blüthgen, N., and K. Fiedler. 2004. Preferences for sugars and amino acids and their conditionality in a diverse nectarfeeding ant community. Journal of Animal Ecology 73:155-166. (Pubitemid 38106597)
10. Blüthgen, N., and K. Reifenrath. 2003. Extrafloral nectaries in an Australian rainforest: structure and distribution. Australian Journal of Botany 51:515-527. (Pubitemid 37358519)
11. Blüthgen, N., N. E. Stork, and K. Fiedler. 2004. Bottom-up control and co-occurrence in complex communities: honeydew and nectar determine a rainforest ant mosaic. Oikos 106:344-358. (Pubitemid 39059108)
12. Bonser, R., P. J. Wright, S. Bament, and U. O. Chukwu. 1998. Optimal patch use by foraging workers of Lasius fuliginosus, L. niger and Myrmica ruginodis. Ecological Entomology 23:15-21. (Pubitemid 28139870)
13. Cane, J. H. 1986. Predator deterrence by mandibular gland secretions of bees (Hymenoptera, Apoidea). Journal of Chemical Ecology 12:1295-1309.
14. Daly, H. V., and K. N. Magnacca. 2003. Insects of Hawaii. University of Hawaii Press, Honolulu, Hawaii, USA.
15. Denslow, J. S. 2003. Weeds in paradise: thoughts on the invasibility of tropical islands. Annals of the Missouri Botanical Garden 90:119-127. (Pubitemid 36234312)
16. de Vega, C., M. Arista, P. L. Ortiz, C. M. Herrera, and S. Talavera. 2009. The ant-pollination system of Cytinus hypocistis (Cytinaceae), a Mediterranean root holoparasite. Annals of Botany 103:1065-1075.
17. Dö tterl, S., A. Jü rgens, K. Seifert, T. Laube, B. Weisbecker, and S. Schü tz. 2006. Nursery pollination by a moth in Silene latifolia: the role of odours in eliciting antennal and behavioural responses. New Phytologist 169:707-718. (Pubitemid 43980663)
18. Dö tterl, S., A. Jü rgens, L. Wolfe, and A. Biere. 2009. Disease status and population origin effects on floral scent: potential consequences for oviposition and fruit predation in a complex interaction between a plant, fungus, and noctuid moth. Journal of Chemical Ecology 35:307-319.
19. Dötterl, S., L. M. Wolfe, and A. Jurgens. 2005. Qualitative and quantitative analyses of flower scent in Silene latifolia. Phytochemistry 66:203-213. (Pubitemid 40126421)
20. Feinsinger, P., and L. A. Swarm. 1978. How common are antrepellent nectars? Biotropica 10:238-239.
21. Fretwell, S., and H. L. Lucas. 1970. On territorial behavior and other factors influencing habitat distribution in birds. I. Theoretical Development. Acta Biotheoretica 19:16-36.
22. Galen, C. 1983. The effects of nectar thieving ants on seedset in floral scent morphs of Polemonium viscosum. Oikos 41:245-249. (Pubitemid 14275517)
23. Galen, C. 1999. Flowers and enemies: predation by nectarthieving ants in relation to variation in floral form of an alpine wildflower, Polemonium viscosum. Oikos 85:426-434. (Pubitemid 29300744)
24. Galen, C., and B. Butchart. 2003. Ants in your plants: effects of nectar-thieves and pollen fertility and seed-siring capacity in the alpine wildflower, Polemonium viscosum. Oikos 101:521-528. (Pubitemid 36599472)
25. Galen, C., and J. Cuba. 2001. Down the tube: pollinators, predators, and the evolution of flower shape in the Alpine Skypilot, Polemonium viscosum. Evolution 55:1963-1971. (Pubitemid 34003818)
26. Galen, C., and J. C. Geib. 2007. Density-dependent effects of ants on selection for bumble bee pollination in Polemonium viscosum. Ecology 88:1202-1209. (Pubitemid 351345250)
27. Gardener, M. C., and C. C. Daehler. 2006. Documenting floral visitors to rare Hawaiian plants using automated video recordings. Pacific Conservation Biology 12:189-194. (Pubitemid 44382965)
28. Ghazoul, J. 2001. Can floral repellents pre-empt potential ant-plant conflicts? Ecology Letters 4:295-299. (Pubitemid 32752206)
29. Gomez, J. M. 2000. Effectiveness of ants as pollinators of Lobularia maritima: effects on main sequential fitness components of the host plant. Oecologia 122:90-97. (Pubitemid 30104706)
30. Gomez, J. M., F. Perfecti, J. Bosch, and J. P. M. Camacho. 2009. A geographic selection mosaic in a generalized plant-pollinator-herbivore system. Ecological Monographs 79:245-263.
31. Gomez, J. M., and R. Zamora. 1992. Pollination by ants: consequences of quantitative effects on a mutualistic system. Oecologia 91:410-418.
32. Gomez, J. M., R. Zamora, J. A. Hodar, and D. Garcia. 1996. Experimental study of pollination by ants in Mediterranean high mountain and arid habitats. Oecologia 105:236-242.
33. Guerrant, E. O., Jr., and P. G. Fiedler. 1981. Flower defenses against nectar-pilferage by ants. Biotropica 13:25-33.
34. Haber, W. A., G. W. Frankie, H. G. Baker, I. Baker, and S. Koptur. 1981. Ants like flower nectar. Biotropica 13:211-214.
35. Hanley, M. E., B. B. Lamont, and W. S. Armbruster. 2009. Pollination and plant defence traits co-vary in Western Australian Hakeas. New Phytologist 182:251-260.
36. Harley, R. 1991. The greasy pole syndrome. 430-433 in C. R. Huxley and D. F. Cutler, editors. Ant-plant interactions. Oxford University Press, Oxford, UK.
37. Heil, M., and D. McKey. 2003. Protective ant-plant interactions as model systems in ecological and evolutionary research. Annual Review of Ecology, Evolution, and Systematics 34:425-453. (Pubitemid 38171426)
38. Herrera, C. M., J. Herrera, and X. Espadaler. 1984. Nectar thievery by ants from southern Spanish insect-pollinated flowers. Insectes Sociaux 31:142-154.
39. Holway, D. A., L. Lach, A. V. Suarez, N. D. Tsutsui, and T. J. Case. 2002. The causes and consequences of ant invasions. Annual Review of Ecology and Systematics 33:181-233. (Pubitemid 36035140)
40. Irwin, R. E., L. S. Adler, and A. K. Brody. 2004. The dual role of floral traits: pollinator attraction and plant defense. Ecology 85:1503-1511. (Pubitemid 39188140)
41. Janzen, D. H. 1977. Why don't ants visit flowers? Biotropica 9:252.
42. Johnson, S. D., A. L. Hargreaves, and M. Brown. 2006. Dark, bitter-tasting nectar functions as a filter of flower visitors in a bird-pollinated plant. Ecology 87:2709-2716. (Pubitemid 44904856)
43. Junker, R. R., R. Bleil, C. C. Daehler, and N. Blüthgen. 2010a. Intra-floral resource partitioning between endemic and invasive flower visitors: consequences for pollinator effectiveness. Ecological Entomology 35:760-767.
44. Junker, R. R., and N. Blüthgen. 2008. Floral scents repel potentially nectar-thieving ants. Evolutionary Ecology Research 10:295-308. (Pubitemid 351501883)
45. Junker, R. R., and N. Blüthgen. 2010a. Dependency on floral resources determines the animals' responses to floral scents. Plant Signaling and Behavior 5:1014-1016.
46. Junker, R. R., and N. Blüthgen. 2010b. Floral scents repel facultative flower visitors, but attract obligate ones. Annals of Botany 105:777-782.
47. Junker, R., A. Y. C. Chung, and N. Blüthgen. 2007. Interaction between flowers, ants and pollinators: additional evidence for floral repellence against ants. Ecological Research 22:665-670. (Pubitemid 46998918)
48. Junker, R. R., N. Hö cherl, and N. Blüthgen. 2010b. Responses to olfactory signals reflect network structure of flower-visitor interactions. Journal of Animal Ecology 79:818-823.
49. Kato, M., A. Shibata, T. Yasui, and H. Nagamasu. 1999. Impact of introduced honeybees, Apis mellifera, upon native bee communities in the Bonin (Ogasawara) Islands. Researches on Population Ecology 41:217-228. (Pubitemid 129493621)
50. Keeler, K. H. 1985. Extrafloral nectaries on plants in communities without ants: Hawaii. Oikos 44:407-414. (Pubitemid 16279716)
51. Keller, A., F. Fö rster, T. Muller, T. Dandekar, J. Schultz, and M. Wolf. 2010. Including RNA secondary structures improves accuracy and robustness in reconstruction of phylogenetic trees. Biology Direct 5:4.
52. Keller, A., T. Schleicher, F. Fö rster, B. Ruderisch, T. Dandekar, T. Muller, and M. Wolf. 2008. ITS2 data corroborate a monophyletic chlorophycean DO-group (Sphaeropleales). BMC Evolutionary Biology 8:218.
53. Keller, A., T. Schleicher, J. Schultz, T. Muller, T. Dandekar, and M. Wolf. 2009. 5.8S-28S rRNA interaction and HMMbased ITS2 annotation. Gene 430:50-57.
54. Kerner, A. 1879. Die Schutzmittel der Blü then gegen unberufene Gä ste. Verlag der Wagner'schen Universitä ts-Buchhandlung, Innsbruck, Austria.
55. Kessler, D., and I. T. Baldwin. 2006. Making sense of nectar scents: the effects of nectar secondary metabolites on floral visitors of Nicotiana attenuata. Plant Journal 49:840-854. (Pubitemid 46279267)
56. Koetschan, C., F. Fö rster, A. Keller, T. Schleicher, B. Ruderisch, R. Schwarz, T. Mü ller, M. Wolf, and J. Schultz. 2009. The ITS2 Database III-sequences and structures for phylogeny. Nucleic Acids Research 38:D275-9.
57. Krushelnycky, P. D., and R. G. Gillespie. 2008. Compositional and functional stability of arthropod communities in the face of ant invasions. Ecological Applications 18:1547-1562.
58. Krushelnycky, P. D., L. L. Loope, and N. J. Reimer. 2005. The ecology, policy, and management of ants in Hawaii. Proceedings of the Hawaiian Entomological Society 37:1-25.
59. Lach, L. 2005. Interference and exploitation competition of three nectar-thieving invasive ant species. Insectes Sociaux 52:257-262. (Pubitemid 41187588)
60. Lach, L. 2007. A mutualism with a native membracid facilitates pollinator displacement by Argentine ants. Ecology 88:1994-2004. (Pubitemid 351345166)
61. Lach, L. 2008a. Argentine ants displace floral arthropods in a biodiversity hotspot. Diversity and Distributions 14:281-290. (Pubitemid 351208152)
62. Lach, L. 2008b. Floral visitation patterns of two invasive ant species and their effects on other hymenopteran visitors. Ecological Entomology 33:155-160.
63. Lach, L., C. Parr, and K. Abbott, editors. 2010. Ant ecology. Oxford University Press, Oxford, UK.
64. Laloi, D., O. Bailez, M. M. Blight, B. Roger, M.-H. Pham- Delegue, and L. J. Wadhams. 2000. Recognition of complex odors by restrained and free-flying honeybees, Apis mellifera. Journal of Chemical Ecology 26:2307-2319.
65. Lammers, T. G., and C. E. Freeman. 1986. Ornithophily among the Hawaiian Lobelioideae (Campanulaceae): evidence from floral nectar sugar compositions. American Journal of Botany 73:1613-1619.
66. Lonsdale, W. M. 1999. Global patterns of plant invasions and the concept of invasibility. Ecology 80:1522-1536. (Pubitemid 29355291)
67. Lopezaraiza-Mikel, M. E., R. B. Hayes, M. R. Whalley, and J. Memmott. 2007. The impact of an alien plant on a native plant-pollinator network: an experimental approach. Ecology Letters 10:539-550. (Pubitemid 46850120)
68. Magnacca, K. N., and B. N. Danforth. 2007. Low nuclear DNA variation supports a recent origin of Hawaiian Hylaeus bees (Hymenoptera: Colletidae). Molecular Phylogenetics and Evolution 43:908-915. (Pubitemid 46777377)
69. Mathews, D. H., M. D. Disney, J. L. Childs, S. J. Schroeder, M. Zuker, and D. H. Turner. 2004. Incorporating chemical modification constraints into a dynamic programming algorithm for prediction of RNA secondary structure. Proceedings of the National Academy of Sciences USA 101:7287-7292. (Pubitemid 38638025)
70. Medeiros, A. C., L. L. Loope, and F. R. Cole. 1986. Distribution of ants and their effects on endemic biota of Haleakala and Hawaii Volcanoes National Park: a preliminary assessment. 39-52 in C. W. Smith and C. P. Stone, editors. Proceedings of the Sixth Conference in Natural Sciences, Hawaii Volcanoes National Park, Hawaii. University of Hawaii at Manoa, Honolulu, Hawaii, USA.
71. Memmott, J., and N. M. Waser. 2002. Integration of alien plants into a native flower-pollinator visitation web. Proceedings of the Royal Society of London B 269:2395-2399. (Pubitemid 36005691)
72. Mooney, H. A. 2005. Invasive alien species: the nature of the problem. 1-15 in H. A. Mooney, R. N. Mack, J. A. McNeely, L. E. Neville, P. J. Schei, and J. K. Waage, editors. Invasive alien species. Island Press, Washington, D.C., USA.
73. Mooney, H. A., R. N. Mack, J. A. McNeely, L. E. Neville, P. J. Schei, and J. K. Waage, editors. 2005. Invasive alien species. Island Press, Washington, D.C., USA.
74. Morales, C. L., and M. A. Aizen. 2006. Invasive mutualisms and the structure of plant-pollinator interactions in the temperate forests of north-west Patagonia, Argentina. Journal of Ecology 94:171-180.
75. Pettersson, J. 1970. An aphid sex attractant. I. Biological studies. Entomologica Scandinavica 1:63-73.
76. Raguso, R. A. 2004. Why are some floral nectars scented? Ecology 85:1486-1494. (Pubitemid 39188138)
77. Raguso, R. A. 2008a. Start making scents: the challenge of integrating chemistry into pollination ecology. Entomologia Experimentalis et Applicata 128:196-207. (Pubitemid 351913443)
78. Raguso, R. A. 2008b. Wake up and smell the roses: the ecology and evolution of floral scent. Annual Review of Ecology, Evolution, and Systematics 39:549-569.
79. Raguso, R. A., and E. Pichersky. 1995. Floral volatiles from Clarkia breweri and C. concinna (Onagraceae): recent evolution of floral scent and moth pollination. Plant Systematics and Evolution 194:55-67.
80. Reimer, N. J. 2006. Key to the ants of Hawaii. Plant Pest Control Branch, Hawaii Department of Agriculture, University of Hawaii at Manoa, Honolulu, Hawaii, USA.
81. Reinhard, J., M. Sinclair, M. V. Srinivasan, and C. Claudianos. 2010. Honeybees learn odour mixtures via a selection of key odorants. PLoS ONE 5:e9110.
82. Ricciardi, A. 2005. Facilitation and synergistic interactions between introduced aquatic species. 162-178 in
83. H. A. Mooney, R. N. Mack, J. A. McNeely, L. E. Neville, P. J. Schei, and J. K. Waage, editors. Invasive alien species. Island Press, Washington, D.C., USA.
84. Richardson, D. M., N. Allsopp, C. M. D'Antonio, S. J. Milton, and M. Rejmanek. 2000. Plant invasions: the role of mutualisms. Biological Reviews 75:65-93.
85. Rico-Gray, V., and P. S. Oliveira. 2007. The ecology and evolution of ant-plant interactions. University of Chicago Press, Chicago, Illinois, USA.
86. Riffell, J. A., H. Lei, T. A. Christensen, and J. G. Hildebrand. 2009. Characterization and coding of behaviorally significant odor mixtures. Current Biology 19:335-340.
87. Sayers, E. W., et al. 2009. Database resources of the National Center for Biotechnology Information. Nucleic Acids Research 37:D5-D15.
88. Schultz, J., and M. Wolf. 2009. ITS2 sequence-structure analysis in phylogenetics: a how-to manual for molecular systematics. Molecular Phylogenetics and Evolution 52:520-523.
89. Seibel, P., T. Mü ller, T. Dandekar, and M. Wolf. 2008. Synchronous visual analysis and editing of RNA sequence and secondary structure alignments using 4SALE. BMC Research Notes 1:91.
90. Simberloff, D., and B. Von Holle. 1999. Positive interactions of nonindigenous species: invasional meltdown? Biological Invasions 1:21-32. (Pubitemid 129644797)
91. Stang, M., P. G. L. Klinkhamer, and E. van der Meijden. 2006. Size constraints and flower abundance determine the number of interactions in a plant-flower visitor web. Oikos 112:111-121.
92. Stang, M., P. G. L. Klinkhamer, and E. van der Meijden. 2007. Asymmetric specialization and extinction risk in plant-flower visitor webs: a matter of morphology or abundance? Oecologia 151:442-453. (Pubitemid 46363427)
93. Stone, C. P., and J. M. Scott, editors. 1985. Hawaii's terrestrial ecosystems: preservation and management. University of Hawaii, Honolulu, Hawaii, USA.
94. Stone, C. P., C. W. Smith, and J. T. Tunison, editors. 1992. Alien plant invasions in native ecosystems of Hawaii: management and research. University of Hawaii Press, Honolulu, Hawaii, USA.
95. Stringer, L. D., A. M. El-Sayed, L. M. Cole, L. A. M. Manning, and D. M. Suckling. 2008. Floral attractants for the female soybean looper, Thysanoplusia orichalcea (Lepidoptera: Noctuidae). Pest Management Science 64:1218-1221.
96. Symstad, A. J. 2000. A test of the effects of functional group richness and composition on grassland invasibility. Ecology 81:99-109. (Pubitemid 30086576)
97. Taylor, F. 1977. Foraging behavior of ants: experiments with two species of Myrmecine ants. Behavioral Ecology and Sociobiology 2:147-167.
98. Tilman, D. 1997. Community invasibility, recruitment limitation, and grassland biodiversity. Ecology 78:81-92.
99. Tsuji, K., A. Hasyim, H. Nakamura, and K. Nakamura. 2004. Asian weaver ants, Oecophylla smaragdina, and their repelling of pollinators. Ecological Research 19:669-673. (Pubitemid 39623332)
100. van der Pijl, L. 1955. Some remarks on myrmecophytes. Phytomorphology 5:190-200.
101. Vet, L. E. M., J. C. Van Lenteren, M. Heymans, and E. Meelis. 1983. An airflow olfactometer for measuring olfactory responses of hymenopterous parasitoids and other small insects. Physiological Entomology 8:97-106.
102. Vila, M., I. Bartomeus, A. C. Dietzsch, T. Petanidou, I. Steffan-Dewenter, J. C. Stout, and T. Tscheulin. 2009. Invasive plant integration into native plant-pollinator networks across Europe. Proceedings of the Royal Society B 276:3887-3893.
103. Wagner, W. L., D. R. Herbst, and S. H. Sohmer. 1990. Manual of the flowering plants of Hawai'i. Bishop Museum, Honolulu, Hawaii, USA.
104. Wetterer, J. K. 1998. Nonindigenous ants associated with geothermal and human disturbance in Hawai'i Volcanoes National Park. Pacific Science 52:40-50.
105. Wheeler, W. M. 1934. Revised list of Hawaiian ants. Bishop Museum Occasional Papers 10:1-21.
106. Willmer, P. G., C. V. Nuttman, N. E. Raine, G. N. Stone, J. G. Pattrick, K. Henson, P. Stillman, L. McIlroy, S. G. Potts, and J. T. Knudsen. 2009. Floral volatiles controlling ant behaviour. Functional Ecology 23:888-900.
107. Willmer, P. G., and G. N. Stone. 1997. How aggressive antguards assist seed-set in Acacia flowers. Nature 388:165-167. (Pubitemid 27297450)
108. Wilson, P., M. C. Castellanos, J. N. Hogue, J. D. Thomson, and W. S. Armbruster. 2004. A multivariate search for pollination syndromes among penstemons. Oikos 104:345-361. (Pubitemid 38143441)
109. Wolf, M., B. Ruderisch, T. Dandekar, J. Schultz, and T. Muller. 2008. ProfDistS: (profile-) distance based phylogeny on sequence-structure alignments. Bioinformatics 24:2401-2402.