The long and the short of it: a global analysis of hawkmoth pollination niches and interaction networks

Functional Ecology

Volumn 31, Issue 1, 2017, Pages 101-115

  Johnson, Steven D ^a   Moré, Marcela ^b   Amorim, Felipe W ^c   Haber, William A ^d   Frankie, Gordon W ^e   Stanley, Dara A ^a   Cocucci, Andrea A ^b   Raguso, Robert A ^f  

^a UNIVERSITY OF KWAZULU NATAL   (South Africa)

^b Instituto Multidisciplinario de Biologia Vegetal   (Argentina)

^c SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^d Apartado Postal 50 5655 ^*  (Costa Rica)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f Department of Obstetrics Gynecology   (United States)

Author keywords

adaptive radiation; biogeography; co evolution; community ecology; ecological shifts; floral adaptation; long tongued; nectar; Sphingidae

Indexed keywords

ADAPTIVE RADIATION; BIMODAL ASSOCIATION; BIOGEOGRAPHY; BIRD; COEVOLUTION; COMMUNITY ECOLOGY; DATA SET; LOCAL ADAPTATION; MORPHOLOGY; MOTH; NECTAR; NICHE BREADTH; POLLINATION; SPECIALIZATION;

APOIDEA; HEXAPODA; SPHINGIDAE; TROCHILIDAE;

EID: 84989247309     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/1365-2435.12753     Document Type: Review

References (99)

1. Ackerman, J.D. (1985) Euglossine bees and their nectar hosts. The Botany and Natural History of Panama (eds W.G. D'Arcy & M.D. Correa), pp. 225–233. Missouri Botanical Garden, St. Louis, MO, USA.
2. Agosta, S.J. & Janzen, D.H. (2005) Body size distributions of large Costa Rican dry forest moths and the underlying relationship between plant and pollinator morphology. Oikos, 108, 183–193.
3. Alarcón, R. (2010) Congruence between visitation and pollen-transport networks in a California plant–pollinator community. Oikos, 119, 35–44.
4. Alarcón, R., Davidowitz, G. & Bronstein, J.L. (2008) Nectar usage in a southern Arizona hawkmoth community. Ecological Entomology, 33, 503–509.
5. Alexandersson, R. & Johnson, S.D. (2002) Pollinator mediated selection on flower-tube length in a hawkmoth-pollinated Gladiolus (Iridaceae). Proceedings of the Royal Society of London. Series B: Biological Sciences, 269, 631–636.
6. Amorim, F.W., Wyatt, G.E. & Sazima, M. (2014) Low abundance of long-tongued pollinators leads to pollen limitation in four specialized hawkmoth-pollinated plants in the Atlantic Rain forest, Brazil. Naturwissenschaften, 101, 893–905.
7. Amorim, F.W., de Avila, R.S., de Camargo, A.J.A., Vieira, A.L. & Oliveira, P.E. (2009) A hawkmoth crossroads? Species richness, seasonality and biogeographical affinities of Sphingidae in a Brazilian Cerrado. Journal of Biogeography, 36, 662–674.
8. Anderson, B., Alexandersson, R. & Johnson, S.D. (2010) Evolution and coexistence of pollination ecotypes in an African Gladiolus (Iridaceae). Evolution, 64, 960–972.
9. Anderson, B. & Johnson, S.D. (2008) The geographical mosaic of coevolution in a plant-pollinator mutualism. Evolution, 62, 220–225.
10. Arditti, J., Elliott, J., Kitching, I.J. & Wasserthal, L.T. (2012) ‘Good Heavens what insect can suck it’- Charles Darwin, Angraecum sesquipedale and Xanthopan morganii praedicta. Botanical Journal of the Linnean Society, 169, 403–432.
11. Armstrong, J.A. (1979) Biotic pollination mechanisms in the Australian flora - a review. New Zealand Journal of Botany, 17, 467–508.
12. Balkenius, A., Kelber, A. & Balkenius, C. (2004) A model of selection between stimulus and place strategy in a hawkmoth. Adaptive Behavior, 12, 21–35.
13. Baum, D.A. (1995) The comparative pollination and floral biology of baobabs (Adansonia Bombacaceae). Annals of the Missouri Botanical Garden, 82, 322–348.
14. Beck, J., Kitching, I.J. & Eduard Linsenmair, K. (2006) Wallace's line revisited: has vicariance or dispersal shaped the distribution of Malesian hawkmoths (Lepidoptera : Sphingidae)? Biological Journal of the Linnean Society, 89, 455–468.
15. Beck, J. & Linsenmair, K.E. (2006) Feasibility of light-trapping in community research on moths: attraction radius of light, completeness of samples, nightly flight times and seasonality of Southeast-Asian hawkmoths (Lepidoptera: Sphingidae). The Journal of Research on the Lepidoptera, 39, 18–37.
16. Blüthgen, N., Menzel, F. & Blüthgen, N. (2006) Measuring specialization in species interaction networks. BMC Ecology, 6, 9.
17. Borrell, B.J. (2005) Long tongues and loose niches: evolution of euglossine bees and their nectar flowers. Biotropica, 37, 664–669.
18. Burnham, K.P. & Anderson, D.R. (2004) Multimodel inference - understanding AIC and BIC in model selection. Sociological Methods & Research, 33, 261–304.
19. Butler, L., Kondo, V., Barrows, E.M. & Townsend, E.C. (1999) Effects of weather conditions and trap types on sampling for richness and abundance of forest Lepidoptera. Environmental Entomology, 28, 795–811.
20. Chase, J.M. & Leibold, M.A. (2003) Ecological Niches: Linking Classical and Contemporary Approaches. The University of Chicago Press, Chicago, IL, USA.
21. Coombs, G. & Peter, C.I. (2010) The invasive ‘mothcatcher’ (Araujia sericifera Brot.; Asclepiadoideae) co-opts native honeybees as its primary pollinator in South Africa. AoB Plants, 2010, plq021.
22. Cruden, R.W. & Hermann, S.M. (1983) Studying nectar? some observations on the art. The Biology of Nectaries (eds B. Bentley & T.S. Elias), pp. 223–242. Columbia University Press, New York, NY, USA.
23. Darwin, C.R. (1862) On the Various Contrivances by Which British and Foreign Orchids Are Fertilized by Insects. John Murray, London, UK.
24. Devictor, V., Clavel, J., Julliard, R., Lavergne, S., Mouillot, D., Thuiller, W. et al. (2010) Defining and measuring ecological specialization. Journal of Applied Ecology, 47, 15–25.
25. Devy, M.S. & Davidar, P. (2003) Pollination systems of trees in Kakachi, a mid-elevation wet evergreen forest in Western Ghats, India. American Journal of Botany, 90, 650–657.
26. Devy, M.S. & Davidar, P. (2006) Breeding systems and pollination modes of understorey shrubs in a medium elevation wet evergreen forest, southern Western Ghats, India. Current Science, 90, 838–842.
27. Dormann, C.F. (2011) How to be a specialist? Quantifying specialisation in pollination networks. Network Biology, 1, 1–20.
28. Dormann, C.F., Gruber, B. & Fruend, J. (2008) Introducing the bipartite package: analysing ecological networks. R News, 8, 8–11.
29. Dormann, C.F., Fruend, J., Bluethgen, N. & Gruber, B. (2009) Indices, graphs and null models: analyzing bipartite ecological networks. The Open Ecology Journal, 2, 7–24.
30. Fenster, C.B., Armbruster, W.S., Wilson, P., Dudash, M.R. & Thomson, J.D. (2004) Pollination syndromes and floral specialization. Annual Review of Ecology Evolution and Systematics, 35, 375–403.
31. Gemmill, C.E.C., Ranker, T.A., Ragone, D., Perlman, S.P. & Wood, K.R. (1998) Conservation genetics of the endangered endemic Hawaiian genus Brighamia (Campanulaceae). American Journal of Botany, 85, 528–539.
32. Gowell, C.P., Quinn, T.P. & Taylor, E.B. (2012) Coexistence and origin of trophic ecotypes of pygmy whitefish, Prosopium coulterii, in a south-western Alaskan lake. Journal of Evolutionary Biology, 25, 2432–2448.
33. Grant, V. (1983) The systematic and geographical distribution of hawkmoth flowers in the temperate North American flora. Botanical Gazette, 144, 439–449.
34. Grant, B.R. & Grant, P.R. (1982) Niche shifts and competition in Darwin's finches: Geospiza conirostris and congeners. Evolution, 36, 637–657.
35. Haber, W.A. & Frankie, G.W. (1989) A tropical hawkmoth community: Costa Rican dry forest Sphingidae. Biotropica, 21, 155–172.
36. Hammer, Ø., Harper, D.A.T. & Ryan, P.D. (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4, 9.
37. Hansman, D.J. (2001) Floral biology of dry rainforest in north Queensland and a comparison with adjacent savanna woodland. Australian Journal of Botany, 49, 137–153.
38. Harder, L.D. (1985) Morphology as a predictor of flower choice by bumble bees. Ecology, 66, 198–210.
39. Hartigan, J.A. & Hartigan, P.M. (1985) The dip test of unimodality. Annals of Statistics, 13, 70–84.
40. Hirota, S.K., Nitta, K., Kim, Y., Kato, A., Kawakubo, N., Yasumoto, A.A. et al. (2012) Relative role of flower color and scent on pollinator attraction: experimental tests using F1 and F2 hybrids of daylily and nightlily. PLoS ONE, 7, e39010.
41. Hirota, S.K., Nitta, K., Suyama, Y., Kawakubo, N., Yasumoto, A.A. & Yahara, T. (2013) Pollinator-mediated selection on flower color, flower scent and flower morphology of hemerocallis: evidence from genotyping individual pollen grains on the stigma. PLoS ONE, 8, e85601.
42. Hopper, S.D. (1980) Pollination of the rain-forest tree Syzygium tierneyanum (Myrtaceae) at Kuranda, Northern Queensland. Australian Journal of Botany, 28, 223–237.
43. Howell, G. & Prakash, N. (1990) Embryology and reproductive ecology of the Darling Lily, Crinum flaccidum Herbert. Australian Journal of Botany, 38, 433–444.
44. Inoue, K. (1986) Different effects of sphingid and noctuid moths on the fecundity of Platanthera metabifolia (Orchidaceae) in Hokkaido. Ecological Research, 1, 25–36.
45. Johnson, S.D. (2010) The pollination niche and its role in the diversification and maintenance of the southern African flora. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 365, 499–516.
46. Johnson, S.D. & Raguso, R. (2016) The long-tongued hawkmoth pollinator niche for native and invasive plants in Africa. Annals of Botany, 117, 25–36.
47. Johnson, S.D., Neal, P.R., Peter, C.I. & Edwards, T.J. (2004) Fruiting failure and limited recruitment in remnant populations of the hawkmoth-pollinated tree Oxyanthus pyriformis subsp pyriformis (Rubiaceae). Biological Conservation, 120, 31–39.
48. Kaczorowski, R.L., Seliger, A.R., Gaskett, A.C., Wigsten, S.K. & Raguso, R.A. (2012) Corolla shape vs. size in flower choice by a nocturnal hawkmoth pollinator. Functional Ecology, 26, 577–587.
49. Kawahara, A.Y., Mignault, A.A., Regier, J.C., Kitching, I.J. & Mitter, C. (2009) Phylogeny and biogeography of hawkmoths (Lepidoptera: Sphingidae): evidence from five nuclear genes. PLoS ONE, 4, e5719.
50. Kay, K.M. & Schemske, D.W. (2004) Geographic patterns in plant-pollinator mutualistic networks: comment. Ecology, 85, 875–878.
51. Kearns, C.A. & Inouye, D.W. (1993) Techniques for Pollination Biologists. University Press of Colorado, Niwot, CO, USA.
52. Kislev, M.E., Kraviz, Z. & Lorch, J. (1972) A study of hawkmoth pollination by a palynological analysis of the proboscis. Israel Journal of Botany, 21, 57–75.
53. Kitching, I.J. (2002) The phylogenetic relationships of Morgan's Sphinx, Xanthopan morganii (Walker), the tribe Acherontiini, and allied long- tongued hawkmoths (Lepidoptera: Sphingidae, Sphinginae). Zoological Journal of the Linnean Society, 135, 471–527.
54. Kitching, I.J. (2016) Sphingidae taxonomic inventory. Available at: http://sphingidae.myspecies.info/ (accessed 02 September 2016).
55. Kitching, I.J. & Cadiou, J.-M. (2000) Hawkmoths of the World. An Annotated and Illustrated Revisionary Checklist (Lepidoptera: Sphingidae). Cornell University Press, New York, NY, USA.
56. Losos, J.B. (2010) Adaptive radiation, ecological opportunity, and evolutionary determinism. The American Naturalist, 175, 623–639.
57. Losos, J.B. & Mahler, D.L.(2010) Adaptive radiation: the interaction of ecological opportunity, adaptation, and speciation. Evolution since Darwin: The First 150 Years (eds M.A. Bell, D.J. Futuyma, W.F. Eanes & J.S. Levinton), pp. 381–420. Sinauer Associates, Sunderland, MA, USA.
58. Maechler, M. & Ringach, D. (2015) Diptest: Hartigan's dip test statistic for unimodality-corrected code. R package version 0.75-7. Available at: http://CRAN.R-project.org/package=diptest/ (accessed 26 June 2016).
59. Maglianesi, A.M., Bluethgen, N., Boehning-Gaese, K. & Schleuning, M. (2014) Morphological traits determine specialization and resource use in plant-hummingbird networks in the neotropics. Ecology, 95, 3325–3334.
60. Markgraf, V. & D'Antoni, H.L. (1978) Pollen Flora of Argentina. Modern Spore and Pollen Types of Pteridophyta, Gymnospermae, and Angiospermae. University of Arizona Press, Tucson, AZ, USA.
61. Martins, D.J. & Johnson, S.D. (2013) Interactions between hawkmoths and flowering plants in East Africa: polyphagy and evolutionary specialization in an ecological context. Biological Journal of the Linnean Society, 110, 199–213.
62. Miller, W.E. (1997) Diversity and evolution of tongue length in hawkmoths (Sphingidae). Journal of the Lepidopterists' Society, 51, 9–31.
63. Miyake, T. & Yahara, T. (1998) Why does the flower of Lonicera japonica open at dusk? Canadian Journal of Botany, 76, 1806–1811.
64. Momose, K., Yumoto, T., Nagamitsu, T., Kato, M., Nagamasu, H., Sakai, S. et al. (1998) Pollination biology in a lowland dipterocarp forest in Sarawak, Malaysia. I. Characteristics of the plant-pollinator community in a lowland dipterocarp forest. American Journal of Botany, 85, 1477–1501.
65. Moré, M. (2008) Estudios sobre esfingofilia en plantas con longitudes florales extremas de Argentina Subtropical. Doctoral Dissertation, Universidad Nacional de Córdoba, Córdoba, Argentina.
66. Moré, M., Kitching, I.J. & Cocucci, A.A. (2005) Sphingidae: Esfíngidos de Argentina. Hawkmoths of Argentina, 1 edn. L.O.L.A. (Literature of Latin America), Buenos Aires.
67. Moré, M., Sérsic, A.N. & Cocucci, A.A. (2007) Restriction of pollinator assemblage through flower length and width in three long-tongued hawkmoth-pollinated species of Mandevilla (Apocynaceae, Apocynoideae). Annals of the Missouri Botanical Garden, 94, 485–504.
68. Moré, M., Amorim, F.W., Benitez-Vieyra, S., Martin Medina, A., Sazima, M. & Cocucci, A.A. (2012) Armament imbalances: match and mismatch in plant-pollinator traits of highly specialized long-spurred orchids. PLoS ONE, 7, e41878.
69. Müller, H. (1873) Probosces capable of sucking the nectar of Angraecum sesquipedale. Nature, 8, 223.
70. Nilsson, L.A. (1988) The evolution of flowers with deep corolla tubes. Nature, 334, 147–149.
71. Nilsson, L.A. (1998) Deep flowers for long tongues. Trends in Ecology & Evolution, 13, 259–260.
72. Nilsson, L.A., Jonsson, L., Rason, L. & Randrianjohany, E. (1985) Monophily and pollination in Angaecum arachnites Schlrt. (Orchidaceae) in a guild of long-tongued hawk-moths (Sphingidae) in Madagascar. Biological Journal of the Linnean Society, 26, 1–19.
73. Nilsson, L.A., Jonsson, L., Rolison, L. & Randrianjohany, E. (1987) Angraecoid orchids and hawkmoths in central Madagascar: specialized pollination systems and generalist foragers. Biotropica, 19, 310–318.
74. Nilsson, L.A., Rabakonandrianina, E., Razananaivo, R. & Randriamanindry, J.-J. (1992) Long pollinia on eyes: hawk-moth pollination of Cynorkis uniflora Lindley (Orchidaceae) in Madagascar. Botanical Journal of the Linnean Society, 109, 145–160.
75. O'Brien, D.M. (1999) Fuel use in flight and its dependence on nectar feeding in the hawkmoth Amphion floridensis. The Journal of Experimental Biology, 202, 441–451.
76. Olesen, J.M., Bascompte, J., Dupont, Y.L. & Jordano, P. (2007) The modularity of pollination networks. Proceedings of the National Academy of Sciences of the United States of America, 104, 19891–19896.
77. Pauw, A., Stofberg, J. & Waterman, R.J. (2009) Flies and flowers in Darwin's race. Evolution, 63, 268–279.
78. Popic, T.J., Wardle, G.M. & Davila, Y.C. (2013) Flower-visitor networks only partially predict the function of pollen transport by bees. Austral Ecology, 38, 76–86.
79. R Core Team (2014) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: http://www.R-project.org.
80. Riffell, J.A., Alarcon, R., Abrell, L., Davidowitz, G., Bronstein, J.L. & Hildebrand, J.G. (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.
81. Riffell, J.A., Lei, H., Abrell, L. & Hildebrand, J.G. (2013) Neural basis of a pollinator's buffet: olfactory specialization and learning in Manduca sexta. Science, 339, 200–204.
82. Robertson, I.A.D. (1977) Records of insects taken at light traps in Tanzania. V. Centre for Overseas Pest Research, London. Miscellaneous Report 31: 1–14.
83. Rodríguez-Gironés, M.A. & Llandres, A.L. (2008) Resource competition triggers the co-evolution of long tongues and deep corolla tubes. PLoS ONE, 3, e2992.
84. Rougerie, R., Kitching, I.J., Haxaire, J., Miller, S.E., Hausmann, A. & Hebert, P.D. (2014) Australian Sphingidae–DNA barcodes challenge current species boundaries and distributions. PLoS ONE, 9, e101108.
85. Sazatornil, F., Moré, M., Benitez-Vieyra, S., Kitching, I., Schlumpberger, B., Oliveira, P. et al. (2016) Beyond neutral and forbidden links: morphological matches and the assembly of mutualistic hawkmoth–plant networks. Journal of Animal Ecology, 85, 1586–1594.
86. Schleuning, M., Fruend, J., Klein, A.-M., Abrahamczyk, S., Alarcon, R., Albrecht, M. et al. (2012) Specialization of mutualistic interaction networks decreases toward tropical latitudes. Current Biology, 22, 1925–1931.
87. Schluter, D. (2000) The Ecology of Adaptive Radiation. Oxford University Press, Oxford, UK.
88. Schreiber, H. (1978) Dispersal centres of Sphingidae (Lepidoptera) in the neotropical region. Biogeographica, 10, 1–195.
89. Schulze, C.H., Hauser, C.L. & Maryati, M. (2000) A checklist of the hawkmoths (Lepidoptera: Sphingidae) of Kinabalu Park, Sabah, Borneo. Malayan Nature Journal, 54, 1–20.
90. Silberbauer-Gottsberger, I.S. & Gottsberger, G. (1975) Über sphingophile Angiospermen Brasiliens. Plant Systematics and Evolution, 123, 157–184.
91. Silvertown, J. (2004) Plant coexistence and the niche. Trends in Ecology & Evolution, 19, 605–611.
92. Suzán, H., Nabhan, G.P. & Patten, D.T. (1994) Nurse plant and floral biology of a rare night-blooming cereus, Peniocereus striatus (Brandegee) F. Buxbaum. Conservation Biology, 8, 461–470.
93. Toju, H. (2008) Fine-scale local adaptation of weevil mouthpart length and camellia pericarp thickness: altitudinal gradient of a putative arms race. Evolution, 62, 1086–1102.
94. Vázquez, D.P. & Aizen, M.A. (2004) Asymmetric specialization: a pervasive feature of plant–pollinator interactions. Ecology, 85, 1251–1257.
95. Vizentin-Bugoni, J., Maruyama, P.K. & Sazima, M. (2014) Processes entangling interactions in communities: forbidden links are more important than abundance in a hummingbird-plant network. Proceedings of the Royal Society of London. Series B: Biological Sciences, 281, 20132397.
96. Wasserthal, L.T. (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.
97. Whittall, J.B. & Hodges, S.A. (2007) Pollinator shifts drive increasingly long nectar spurs in columbine flowers. Nature, 447, 706–709.
98. Williams, G. & Adam, P. (1994) A review of rainforest pollination and plant–pollinator interactions with particular reference to Australian subtropical rainforests. The Australian Zoologist, 29, 177–212.
99. Xu, L., Bedrick, E.J., Hanson, T. & Restrepo, C. (2014) A comparison of statistical tools for identifying modality in body mass distributions. Journal of Data Science, 12, 175–196.