Interactions between hawkmoths and flowering plants in east africa: Polyphagy and evolutionary specialization in an ecological context

Biological Journal of the Linnean Society

Volumn 110, Issue 1, 2013, Pages 199-213

  Martins, Dino J ^a,b   Johnson, Steven D ^a  

^a UNIVERSITY OF KWAZULU NATAL   (South Africa)

^b Turkana Basin Institute   (Kenya)

Author keywords

Agrius; Coevolution; Generalization; Insect; Kenya; Nephele; Plant interactions; Pollination

Indexed keywords

COEVOLUTION; EVOLUTIONARY BIOLOGY; GUILD; MOTH; NATURAL SELECTION; NECTAR; PHYLOGENETICS; PLANT-POLLINATOR INTERACTION; POLLINATION; SPECIALIZATION;

KENYA;

AGRIUS; HEXAPODA; LEPIDOPTERA; MAGNOLIOPHYTA; NEPHELE; SPHINGIDAE;

EID: 84881614659     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/bij.12107     Document Type: Article

References (73)

1. Acharya L, McNeil JN. 1998. Predation risk and mating behavior: the responses of moths to bat-like ultrasound. Behavioral Ecology 9: 552-558.
2. Agnew ADQ, Agnew S. 1994. Upland Kenya wild flowers: a flora of the ferns and herbaceous flowering plants of Upland Kenya. Nairobi: East Africa Natural History Society.
3. Agosta SJ, Janzen DH. 2005. Body size distributions of large Costa Rican dry forest moths and the underlying relationship between plant and pollinator morphology. Oikos 108: 183-193.
4. Alarcon R, Davidowitz G, Bronstein JL. 2008. Nectar usage in a southern Arizona hawkmoth community. Ecological Entomology 33: 503-509.
5. Alexandersson R, Johnson SD. 2002. Pollinator-mediated selection on flower-tube length in a hawkmoth-pollinated Gladiolus (Iridaceae). Proceedings of the Royal Society London B 269: 631-636.
6. Anderson B, Alexandersson R, Johnson SD. 2010. Evolution and coexistence of pollination ecotypes in an African Gladiolus (Iridaceae). Evolution 64: 960-972.
7. Baker HG. 1961. The adaptation of flowering plants to nocturnal and crepuscular pollinators. Quarterly Review of Biology 36: 64-73.
8. Baker HG. 1963. Evolutionary mechanisms in pollination biology. Science 139: 877-883.
9. Baker HG. 1970. Two cases of bat pollination in Central America. Revista de Biologia Tropical 17: 187-197.
10. Baum DA. 1995. The comparative pollination and floral biology of baobabs (Adansonia - Bombacaceae). Annals of the Missouri Botanical Garden 82: 322-348.
11. Beentje H. 1994. Kenya trees, shrubs and lianas. Nairobi: National Museums of Kenya.
12. Bennun L, Njoroge P. 1999. Important bird areas in Kenya. Nairobi: The East Africa Natural History Society.
13. Blundell M. 1987. Wildflowers of East Africa. London: William Collins Sons & Co. Ltd.
14. Carcasson RH. 1976. Revised catalogue of the African Sphingidae (Lepidoptera) with descriptions of the East African species. Faringdon, UK: E. W. Classey Ltd.
15. Cribb P. 1984. Flora of tropical East Africa: Orchidaceae 271. Kew: Royal Botanic Gardens.
16. Cruz-Neto O, Machado IC, Duarte Jr. JA, Lopes AV. 2011. Synchronous phenology of hawkmoths (Sphingidae)? and Inga species (Fabaceae-Mimosoideae): implications for the restoration of the Atlantic forest of northeastern Brazil. Biodiversity & Conservation 20: 751-765.
17. Daly KC, Durtschi ML, Smith BH. 2001. Olfactory-based discrimination learning in the moth, Manduca sexta. Journal of Insect Physiology 47: 375-384.
18. Darwin C. 1877. The various contrivances by which orchids are fertilized by insects, 2nd edn. London: John Murray.
19. Dressler RL. 1981. The orchids: natural history and classification. Cambridge, MA: Harvard University Press.
20. Feldman TS, Morris WF, Wilson WG. 2004. When can two plant species facilitate each other's pollination? Oikos 105: 197-207.
21. Fenton MB, Fullard JH. 1981. Moth hearing and the feeding strategies of bats: variations in the hunting and echolocation behavior of bats may reflect a response to hearing-based defenses evolved by their insect prey. American Scientist 69: 266-275.
22. Garland T, Harvey PH, Ives AR. 1992. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Systematic Biology 41: 18-32.
23. Goyret J, Markwell PM, Raguso RA. 2007. The effect of decoupling olfactory and visual stimuli on the foraging behavior of Manduca sexta. Journal of Experimental Biology 210: 1398-1405.
24. Goyret J, Pfaff M, Raguso RA, Kelber A. 2008. Why do Manduca sexta feed from white flowers? Innate and learnt colour preferences in a hawkmoth. Die Naturwissenschaften 95: 569-576.
25. Goyret J, Raguso RA. 2006. The role of mechanosensory input in flower handling efficiency and learning by Manduca sexta. Journal of Experimental Biology 209: 1585-1593.
26. Grant V. 1985. Additional observations on temperate North American hawkmoth flowers. Botanical Gazette 146: 517-520.
27. Grant V. 1992. Floral isolation between ornithophilous and sphingophilous species of Ipomopsis and Aquilegia. Proceedings of the National Academy of Sciences of the United States of America 89: 11828-11831.
28. Haber WA, Frankie GW. 1989. A tropical hawkmoth community: Costa Rican dry forest Sphingidae. Biotropica 21: 155-172.
29. Heinrich B. 1976. Resource partitioning among some eusocial insects: bumblebees. Ecology 57: 874-889.
30. Janzen DH. 1980. When is it coevolution? Evolution 34: 611-612.
31. Johnson SD. 1995. Observations of hawkmoth pollination in the South African orchid Disa cooperi. Nordic Journal of Botany 15: 121-125.
32. Johnson SD, Neal PR, Peter CI, Edwards TJ. 2004. Fruiting failure and limited recruitment in remnant populations of the hawkmoth-pollinated tree Oxyanthus pyriformis subsp pyriformis (Rubiaceae). Biological Conservation 120: 31-39.
33. Johnson SD, Nilsson LA. 1999. Pollen carryover, geitonogamy, and the evolution of deceptive pollination systems in orchids. Ecology 80: 2607-2619.
34. Johnson SD, Peter CI, Ågren J, Nilsson LA. 2003. Pollination success in a deceptive orchid is enhanced by co-occurring rewarding 'magnet' plants. Ecology 84: 2919-2927.
35. Kawahara AY, Mignault AA, Regier JC, Kitching IJ, Mitter C. 2009. Phylogeny and biogeography of hawkmoths (Lepidoptera: Sphingidae): evidence from five nuclear genes. PLoS ONE 4: e5719.
36. Kelber A. 1996. Colour learning in the hawkmoth Macroglossum stellatarum. Journal of Experimental Biology 199: 1127-1131.
37. Kelber A. 1997. Innate preferences for flower features in the hawkmoth Macroglossum stellatarum. Journal of Experimental Biology 200: 827-836.
38. Kelber A, Balkenius A, Warrant EJ. 2002. Scotopic colour vision in nocturnal hawkmoths. Nature 419: 922-925.
39. Kelber A, Pfaff M. 1997. Spontaneous and learned preferences for visual flower features in a diurnal hawkmoth. Israel Journal of Plant Sciences 45: 235-245.
40. Kingsolver JG, Daniel TL. 1979. On the mechanics and energetics of nectar feeding butterflies. Journal of Theoretical Biology. 76: 167-179.
41. Kingston AJ, Nummelin M. 1998. Seasonality and abundance of Sphingids in a garden on the lower slopes of the Uluguru Mountains in Morogoro Township in Tanzania. Journal of East African Natural History 87 (1 & 2): 213-220.
42. Kitching IJ, Cadiou JM. 2000. Hawkmoths of the world: an annotated and illustrated revisionary checklist. Ithaca and London: The Natural History Museum - Cornell University Press.
43. Lack A. 1978. The ecology of the flowers of the savanna tree Maranthes polyandra and their visitors, with particular reference to bats. Journal of Ecology 66: 287-295.
44. Luyt R, Johnson SD. 2001. Hawkmoth pollination of the African epiphytic orchid Mystacidium venosum, with special reference to flower and pollen longevity. Plant Systematics and Evolution 228: 49-62.
45. Maddison WP, Maddison DR. 2006. Mesquite: a modular system for evolutionary analysis. Version 1.12. Available at: http://mesquiteproject.org
46. Martins DJ, Johnson SD. 2007. Hawkmoth pollination of aerangoid orchids in Kenya, with special reference to nectar sugar gradients in the floral spurs. American Journal of Botany 94: 650-659.
47. Martins DJ, Johnson SD. 2009. Distance and quality of natural habitat influence hawkmoth pollination of cultivated papaya. International Journal of Tropical Insect Science 29: 114-123.
48. Midford PE, Garland JT, Maddison WP. 2005. PDAP package of mesquite. Version 1.07.
49. Miller RB. 1981. Hawkmoths and the geographic patterns of floral variation in Aquilegia caerulea. Evolution 35: 763-774.
50. Miller RB. 1985. Hawkmoth pollination of Aquilegia chrysantha (Ranunculaceae) in Southern Arizona, USA. Southwestern Naturalist 30: 69-76.
51. Miller WE. 1997. Diversity and evolution of tongue length in hawkmoths (Sphingidae). Journal of the Lepidopterists' Society 51: 9-31.
52. Murcia C. 1990. Effect of floral morphology and temperature on pollen receipt and removal in Ipomoea trichocarpa. Ecology 71: 1098-1109.
53. National Atlas of Kenya. 1969. Kenya Government: survey of Kenya, Nairobi.
54. Ng'weno F. 1981. Hawkmoths in my garden. Bulletin of the East Africa Natural History Society. September - October.
55. Nilsson LA. 1992. Orchid pollination biology. Trends in Ecology and Evolution 7: 255-259.
56. Nilsson LA. 1998. Deep flowers for long tongues. Trends in Ecology and Evolution 13: 259-260.
57. Nilsson LA, Jonsson L, Ralison L, Randrianjohany E. 1987. Angraecoid orchids and hawkmoths in central Madagascar: specialized pollination systems and generalist foragers. Biotropica 19: 310-318.
58. Nilsson LA, Jonsson L, Rason L, Randrianjohany E. 1985. Monophily and pollination mechanisms in Angraecum arachnites Schltr. (Orchidaceae) in a guild of long-tongued hawkmoths (Sphingidae) in Madagascar. Biological Journal of the Linnean Society 26: 1-19.
59. Nilsson LA, Rabakonandrianina E, Pettersson B. 1992. Exact tracking of pollen transfer and mating in plants. Nature 360: 666-667.
60. Oliveira PE, Gibbs PE, Barbosa AA. 2004. Moth pollination of woody species in the cerrados of Central Brazil: a case of so much owed to so few? Plant Systematics & Evolution 245: 41-54.
61. Owen DF. 1969. Species diversity and seasonal abundance in tropical Sphingidae (Lepidoptera). Proceedings of the Royal Entomological Society London A 44: 162-168.
62. Pagel MD. 1992. A method for the analysis of comparative data. Journal of Theoretical Biology 156: 431-442.
63. Papaj DR, Prokopy RJ. 1989. Ecological and evolutionary aspects of learning in phytophagous insects. Annual Review of Entomology 34: 315-350.
64. Pinhey E. 1962. Hawk moths of Central and Southern Africa. South Africa: Longmans, National Museums of Southern Rhodesia.
65. Riffell JA, Alarcon R, Abrell L, Davidowitz G, Bronstein JL, Hildebrand JG. 2008. Behavioral consequences of innate preferences and olfactory learning in hawkmoth-flower interactions. Proceedings of the National Academy of Sciences of the United States of America 105: 3404-3409.
66. Robertson IAD. 1977. Records of insects taken at light traps in Tanzania. V - Seasonal changes in catches and effect of the lunar cycle on hawkmoths of subfamily Asemanophorinae (Lepidoptera: Sphingidae). Centre for Overseas Pest Research, Miscellaneous Report No. 31. College House, London.
67. Sargent RD, Goodwillie C, Kalisz S, Rees RH. 2007. Phylogenetic evidence for a flower size and number trade-off. American Journal of Botany 94: 2059-2062.
68. Stewart J. 1996. Orchids of Kenya. Portland, OR: Timber Press.
69. Taylor LR, Brown ES. 1972. Effects of light-trap design and illumination on samples of moths in the Kenya highlands. Bulletin of Entomological Research 62: 91-112.
70. Wasserthal LT. 1997. The pollinators of the Malagasy star orchids Angraecum sesquipedale, A. sororium and A. compactum and the evolution of extremely long spurs by pollinator shift. Botanica Acta 110: 343-359.
71. Webb CO, Donoghue MJ. 2005. Phylomatic: tree retrieval for applied phylogenetics. Molecular Ecology Notes 5: 181-183.
72. White RH, Stevenson RD, Bennet RR, Cultler DE, Haber WA. 1994. Wavelength discrimination and the role of ultraviolet vision in the feeding behavior of hawkmoths. Biotropica 26: 427-435.
73. Whittall JB, Hodges SA. 2007. Pollinator shifts drive increasingly long nectar spurs in columbine flowers. Nature 447: 706-709.