Pollination by nocturnal Lepidoptera, and the effects of light pollution: A review

Ecological Entomology

Volumn 40, Issue 3, 2015, Pages 187-198

  Macgregor, Callum J ^a,b,c   Pocock, Michael J O ^b   Fox, Richard ^c   Evans, Darren M ^a  

^a UNIVERSITY OF HULL   (United Kingdom)

^b CENTRE FOR ECOLOGY AND HYDROLOGY   (United Kingdom)

^c BUTTERFLY CONSERVATION   (United Kingdom)

Author keywords

Agro ecosystems; Artificial night lighting; Ecological networks; Ecosystem services; Flowering plants; Food webs; Moths; Population declines

Indexed keywords

ECOSYSTEM FUNCTION; LIGHT EFFECT; MOTH; POLLINATION; POLLUTION TOLERANCE; POPULATION DECLINE;

EUROPE;

LEPIDOPTERA; MAGNOLIOPHYTA;

EID: 84927002369     PISSN: 03076946     EISSN: 13652311     Source Type: Journal    
DOI: 10.1111/een.12174     Document Type: Review

References (120)

1. Acharya, L. & Fenton, M.B. (1999) Bat attacks and moth defensive behaviour around street lights. Canadian Journal of Zoology, 77, 27-33.
2. Altermatt, F., Baumeyer, A. & Ebert, D. (2009) Experimental evidence for male biased flight-to-light behaviour in two moth species. Entomologia Experimentalis et Applicata, 130, 259-265.
3. Baker, R.R. & Sadovy, Y. (1978) The distance and nature of the light-trap response of moths. Nature, 276, 818-821.
4. Banza, P. (2011) Investigating the importance of nocturnal Lepidoptera as pollinators: a network approach. MSc thesis, Universidade de Évora, Portugal.
5. Barth, F.G. (1985) Insects and Flowers: The Biology of a Partnership. Princeton University Press, Princeton, New Jersey.
6. Barthelmess, E.L., Richards, C.M. & McCauley, D.E. (2006) Relative effects of nocturnal vs diurnal pollinators and distance on gene flow in small Silene alba populations. New Phytologist, 169, 689-698.
7. Bascompte, J. (2007) Networks in ecology. Basic and Applied Ecology, 8, 485-490.
8. Bascompte, J. (2009) Disentangling the web of life. Science, 325, 416-419.
9. Bascompte, J., Jordano, P., Melián, C.J. & Olesen, J.M. (2003) The nested assembly of plant-animal mutualistic networks. Proceedings of the National Academy of Sciences, 100, 9383-9387.
10. Bawa, K.S., Bullock, S.H., Perry, D.R., Coville, R.E. & Grayum, M.H. (1985) Reproductive biology of tropical lowland rain forest trees. II. Pollination systems. American Journal of Botany, 72, 346-356.
11. Bennie, J., Davies, T.W., Duffy, J.P., Inger, R. & Gaston, K.J. (2014) Contrasting trends in light pollution across Europe based on satellite observed night time lights. Scientific Reports, 4, 3789.
12. Berlinger, M.J. & Ankersmit, G.W. (1976) Manipulation with the photoperiod as a method of control of Adoxophyes orana (Lepidoptera, Torticidae). Entomologia Experimentalis et Applicata, 19, 96-107.
13. Bernhard, C.G. & Ottoson, D. (1960) Studies on the relation between the pigment migration and the sensitivity changes during dark adaptation in diurnal and nocturnal Lepidoptera. Journal of General Physiology, 44, 205-215.
14. Bertin, R.I. & Willson, M.F. (1980) Effectiveness of diurnal and nocturnal pollination of two milkweeds. Canadian Journal of Botany, 58, 1744-1746.
15. Biesmeijer, J.C., Roberts, S.P.M., Reemer, M., Ohlemüller, R., Edwards, M., Peeters, T. et al. (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science, 313, 351-354.
16. Bosch, J., Gonzalez, A.M.M., Rodrigo, A. & Navarro, D. (2009) Plant-pollinator networks: adding the pollinator's perspective. Ecology Letters, 12, 409-419.
17. Brown, L.N. (1984) Population outbreak of Pandora moths (Coloradia pandora Blake) on the Kaibab plateau, Arizona (Saturniidae). Journal of the Lepidopterists' Society, 38, 65.
18. Bruce-White, C. & Shardlow, M. (2011) A Review of the Impact of Artificial Light on Invertebrates. Buglife, U.K.
19. Callahan, P.S. (1965) Intermediate and far infrared sensing of nocturnal insects. Part I. Evidences for a far infrared (FIR) electromagnetic theory of communication and sensing in moths and its relationship to the limiting biosphere of the corn earworm. Annals of the Entomological Society of America, 58, 727-745.
20. Carvalheiro, L.G., Kunin, W.E., Keil, P., Aguirre-Gutiérrez, J., Ellis, W.N., Fox, R. et al. (2013) Species richness declines and biotic homogenisation have slowed down for NW-European pollinators and plants. Ecology Letters, 16, 870-878.
21. Chamorro, S., Heleno, R., Olesen, J.M., McMullen, C.K. & Traveset, A. (2012) Pollination patterns and plant breeding systems in the Galápagos: a review. Annals of Botany, 110, 1489-1501.
22. Cinzano, P., Falchi, F. & Elvidge, C.D. (2001) The first World Atlas of the artificial night sky brightness. Monthly Notices of the Royal Astronomical Society, 328, 689-707.
23. Conrad, K.F., Woiwod, I.P., Parsons, M., Fox, R. & Warren, M.S. (2004) Long-term population trends in widespread British moths. Journal of Insect Conservation, 8, 119-136.
24. Conrad, K.F., Warren, M.S., Fox, R., Parsons, M.S. & Woiwod, I.P. (2006) Rapid declines of common, widespread British moths provide evidence of an insect biodiversity crisis. Biological Conservation, 132, 279-291.
25. Costanza, R., d'Arge, R., de Groot, R., Farber, S., Grasso, M., Hannon, B. etal. (1997) The value of the world's ecosystem services and natural capital. Nature, 387, 253-260.
26. Cowan, T. & Gries, G. (2009) Ultraviolet and violet light: attractive orientation cues for the Indian meal moth, Plodia interpunctella. Entomologia Experimentalis et Applicata, 131, 148-158.
27. Cruden, R.W. (1973) Reproductive biology of weedy and cultivated Mirabilis (Nyctaginaceae). American Journal of Botany, 60, 802-809.
28. Davies, T.W., Bennie, J. & Gaston, K.J. (2012) Street lighting changes the composition of invertebrate communities. Biology Letters, 8, 764-767.
29. Davies, T.W., Bennie, J., Inger, R., de Ibarra, N.H. & Gaston, K.J. (2013) Artificial light pollution: are shifting spectral signatures changing the balance of species interactions? Global Change Biology, 19, 1417-1423.
30. Delisle, J., West, R.J. & Bowers, W.W. (1998) The relative performance of pheromone and light traps in monitoring the seasonal activity of both sexes of the eastern hemlock looper, Lambdina fiscellaria fiscellaria. Entomologia Experimentalis et Applicata, 89, 87-98.
31. Devoto, M., Bailey, S. & Memmott, J. (2011) The 'night shift': nocturnal pollen-transport networks in a boreal pine forest. Ecological Entomology, 36, 25-35.
32. Dicks, L.V., Corbet, S.A. & Pywell, R.F. (2002) Compartmentalization in plant-insect flower visitor webs. Journal of Animal Ecology, 71, 32-43.
33. Eaton, J.L., Tignor, K.R. & Holtzman, G.I. (1983) Role of moth ocelli in timing flight initiation at dusk. Physiological Entomology, 8, 371-375.
34. Eguchi, E., Watanabe, K., Hariyama, T. & Yamamoto, K. (1982) A comparison of electrophysiologically determined spectral responses in 35 species of Lepidoptera. Journal of Insect Physiology, 28, 675-682.
35. Eisenbeis, G. (2006) Artificial night lighting and insects: attraction of insects to streetlamps in a rural setting in Germany. Ecological Consequences of Artificial Night Lighting (ed. by C. Rich and T. Longcore ), pp. 281-304. Island Press, Washington, District of Columbia.
36. Evans, D.M., Pocock, M.J.O. & Memmott, J. (2013) The robustness of a network of ecological networks to habitat loss. Ecology Letters, 16, 844-852.
37. Fatzinger, C.W. (1973) Circadian rhythmicity of sex pheromone release by Dioryctria abietella (Lepidoptera: Pyralidae (Phycitinae)) and the effect of a diel light cycle on its precopulatory behaviour. Annals of the Entomological Society of America, 66, 1147-1153.
38. Fontaine, C., Dajoz, I., Meriguet, J. & Loreau, M. (2006) Functional diversity of plant-pollinator interaction webs enhances the persistence of plant communities. PLoS Biology, 4, e1.
39. Forup, M.L., Henson, K.S.E., Craze, P.G. & Memmott, J. (2008) The restoration of ecological interactions: plant-pollinator networks on ancient and restored heathlands. Journal of Applied Ecology, 45, 742-752.
40. Fox, R. (2013) The decline of moths in Great Britain: a review of possible causes. Insect Conservation and Diversity, 6, 5-19.
41. Fox, R., Randle, Z., Hill, L., Anders, S., Wiffen, L. & Parsons, M.S. (2011) Moths count: recording moths for conservation in the UK. Journal of Insect Conservation, 15, 55-68.
42. Fox, R., Parsons, M.S., Chapman, J.W., Woiwod, I.P., Warren, M.S. & Brooks, D.R. (2013) The State of Britain's Larger Moths 2013. Butterfly Conservation and Rothamsted Research, U.K.
43. Fox, R., Oliver, T.H., Harrower, C., Parsons, M.S., Thomas, C.D. & Roy, D.B. (2014) Long-term changes to the frequency of occurrence of British moths are consistent with opposing and synergistic effects of climate and land-use changes. Journal of Applied Ecology, 51, 949-957.
44. Frank, K.D. (2006) Effects of artificial night lighting on moths. Ecological Consequences of Artificial Night Lighting (ed. by C. Rich and T. Longcore ), pp. 305-344. Island Press, Washington, District of Columbia.
45. Frick, T.B. & Tallamy, D.W. (1996) Density and diversity of nontarget insects killed by suburban electric insect traps. Entomological News, 107, 77-82.
46. Garibaldi, L.A., Steffan-Dewenter, I., Winfree, R., Aizen, M.A., Bommarco, R., Cunningham, S.A. et al. (2013) Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science, 339, 1608-1611.
47. Garris, H.W. & Snyder, J.A. (2010) Sex-specific attraction of moth species to ultraviolet light traps. Southeastern Naturalist, 9, 427-434.
48. Gaston, K.J., Davies, T.W., Bennie, J. & Hopkins, J. (2012) Reducing the ecological consequences of night-time light pollution: options and developments. Journal of Applied Ecology, 49, 1256-1266.
49. Gaston, K.J., Bennie, J., Davies, T.W. & Hopkins, J. (2013) The ecological impacts of nighttime light pollution: a mechanistic appraisal. Biological Reviews, 88, 912-927.
50. van Geffen, K.G., van Grunsven, R.H.A., van Ruijven, J., Berendse, F. & Veenendaal, E.M. (2014) Artificial light at night causes diapause inhibition and sex-specific life history changes in a moth. Ecology and Evolution, 4, 2082-2089.
51. Gillett, M.P.T. & Gardner, A.S. (2009) An unusual observation - attraction of caterpillars to mercury vapour light in the Abu Dhabi desert (Lepidoptera: Pyralidae). Tribulus, 18, 56-59.
52. Groenendijk, D. & Ellis, W.N. (2011) The state of the Dutch larger moth fauna. Journal of Insect Conservation, 15, 95-101.
53. van Grunsven, R.H.A., Lham, D., van Geffen, K.G. & Veenendaal, E.M. (2014) Range of attraction of a 6-W moth light trap. Entomologia Experimentalis et Applicata, 152, 87-90.
54. Hamdorf, K. & Höglund, G. (1981) Light induced retinal screening pigment migration independent of visual cell activity. Journal of Comparative Physiology, 143, 305-309.
55. Hartstack, A.W. Jr., Hollingsworth, J.P. & Lindquist, D.A. (1968) A technique for measuring trapping efficiency of electric insect traps. Journal of Economic Entomology, 61, 546-552.
56. Heiling, A.M. (1999) Why do nocturnal orb-web spiders (Araneidae) search for light? Behavioral Ecology and Sociobiology, 46, 43-49.
57. Henderson, R.W. & Powell, R. (2001) Responses by the West Indian herpetofauna to human-influenced resources. Caribbean Journal of Science, 37, 41-54.
58. Hölker, F., Moss, T., Griefahn, B., Kloas, W., Voigt, C.C., Henckel, D. et al. (2010a) The dark side of light: a transdisciplinary research agenda for light pollution policy. Ecology and Society, 15, 13.
59. Hölker, F., Wolter, C., Perkin, E.K. & Tockner, K. (2010b) Light pollution as a biodiversity threat. Trends in Ecology & Evolution, 25, 681-682.
60. Howe, W.H. (1959) A swarm of noctuid moths in southeastern Kansas. Journal of the Lepidopterists' Society, 13, 26.
61. Hsiao, H.S. (1973) Flight paths of night-flying moths to light. Journal of Insect Physiology, 19, 1971-1976.
62. Ingalls, V. (1993) Startle and habituation responses of Blue Jays (Cyanocitta cristata) in a laboratory simulation of anti-predator defenses of Catocala moths (Lepidoptera: Noctuidae). Behaviour, 126, 77-96.
63. Ings, T.C., Montoya, J.M., Bascompte, J., Blüthgen, N., Brown, L., Dormann, C.F. et al. (2009) Ecological networks - beyond food webs. Journal of Animal Ecology, 78, 253-269.
64. Jennersten, O. & Morse, D.H. (1991) The quality of pollination by diurnal and nocturnal insects visiting Common Milkweed, Asclepias syriaca. American Midland Naturalist, 125, 18-28.
65. 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.
66. Jürgens, A., Witt, T. & Gottsberger, G. (2002) Pollen grain numbers, ovule numbers and pollen-ovule ratios in Caryophylloideae: correlation with breeding system, pollination, life form, style number, and sexual system. Sexual Plant Reproduction, 14, 279-289.
67. Kato, M. & Kawakita, A. (2004) Plant-pollinator interactions in New Caledonia influenced by introduced honey bees. American Journal of Botany, 91, 1814-1827.
68. Kato, M., Inoue, T. & Nagamitsu, T. (1995) Pollination biology of Gnetum (Gnetaceae) in a lowland mixed dipterocarp forest in Sarawak. American Journal of Botany, 82, 862-868.
69. King, C., Ballantyne, G. & Willmer, P.G. (2013) Why flower visitation is a poor proxy for pollination: measuring single-visit pollen deposition, with implications for pollination networks and conservation. Methods in Ecology and Evolution, 4, 811-818.
70. van Langevelde, F., Ettema, J.A., Donners, M., Wallis De Vries, M.F. & Groenendijk, D. (2011) Effect of spectral composition of artificial light on the attraction of moths. Biological Conservation, 144, 2274-2281.
71. LeCroy, K.A., Shew, H.W. & van Zandt, P.A. (2013) Pollen presence on nocturnal moths in the Ketona Dolomite glades of Bibb County, Alabama. Southern Lepidopterists' News, 35, 136-142.
72. Lewanzik, D. & Voigt, C.C. (2014) Artificial light puts ecosystem services of frugivorous bats at risk. Journal of Applied Ecology, 51, 388-394.
73. Longcore, T. & Rich, C. (2004) Ecological light pollution. Frontiers in Ecology and the Environment, 2, 191-198.
74. Lyytimäki, J. (2013) Nature's nocturnal services: light pollution as a non-recognised challenge for ecosystem services research and management. Ecosystem Services, 3, e44-e48.
75. Martinell, M.C., Dötterl, S., Blanché, C., Rovira, A., Massó, S. & Bosch, M. (2010) Nocturnal pollination of the endemic Silene sennenii (Caryophyllaceae): an endangered mutualism? Plant Ecology, 211, 203-218.
76. Mattila, N., Kaitala, V., Komonen, A., Kotiaho, J.S. & Päivinen, J. (2006) Ecological determinants of distribution decline and risk of extinction in moths. Conservation Biology, 20, 1161-1168.
77. Mattila, N., Kotiaho, J.S., Kaitala, V. & Komonen, A. (2008) The use of ecological traits in extinction risk assessments: a case study on geometrid moths. Biological Conservation, 141, 2322-2328.
78. Mazokhin-Porshnyakov, G.A. (1961) Why insects fly to light by night. Anzeiger für Schädlingskunde, 34, 47.
79. Memmott, J., Waser, N.M. & Price, M.V. (2004) Tolerance of pollination networks to species extinctions. Proceedings of the Royal Society B, 271, 2605-2611.
80. Memmott, J., Craze, P.G., Waser, N.M. & Price, M.V. (2007) Global warming and the disruption of plant-pollinator interactions. Ecology Letters, 10, 710-717.
81. Merckx, T. & Slade, E.M. (2014) Macro-moth families differ in their attraction to light: implications for light-trap monitoring programmes. Insect Conservation and Diversity, 7, 453-461. DOI: 10.1111/icad.12068.
82. Miyake, T. & Yahara, T. (1998) Why does the flower of Lonicera japonica open at dusk? Canadian Journal of Botany, 76, 1806-1811.
83. Miyake, T. & Yahara, T. (1999) Theoretical evaluation of pollen transfer by nocturnal and diurnal pollinators: when should a flower open? Oikos, 86, 233-240.
84. Mizunami, M. (1995) Functional diversity of neural organization in insect ocellar systems. Vision Research, 35, 443-452.
85. Montoya, J.M., Pimm, S.L. & Solé, R.V. (2006) Ecological networks and their fragility. Nature, 442, 259-264.
86. Morse, D.H. & Fritz, R.S. (1983) Contributions of diurnal and nocturnal insects to the pollination of common milkweed (Asclepias syriaca L.) in a pollen-limited system. Oecologia, 60, 190-197.
87. Navara, K.J. & Nelson, R.J. (2007) The dark side of light at night: physiological, epidemiological and ecological consequences. Journal of Pineal Research, 43, 215-224.
88. Nemec, S.J. (1969) Use of artificial lighting to reduce Heliothis spp. populations in cotton fields. Journal of Economic Entomology, 62, 1138-1140.
89. Olesen, J.M., Bascompte, J., Dupont, Y.L. & Jordano, P. (2007) The modularity of pollination networks. Proceedings of the National Academy of Sciences, 104, 19891-19896.
90. Ollerton, J., Winfree, R. & Tarrant, S. (2011) How many flowering plants are pollinated by animals? Oikos, 120, 321-326.
91. Pauw, A. (2007) Collapse of a pollination web in small conservation areas. Ecology, 88, 1759-1769.
92. Pfrimmer, T.R., Lukefahr, M.J. & Hollingsworth, J.P. (1955) Experiments with Light Traps for Control of the Pink Bollworm. ARS-33-6. U.S. Department of Agriculture, Agricultural Research Service, Washington, District of Columbia.
93. Philipp, M., Böcher, J., Siegismund, H.R. & Nielsen, L.R. (2006) Structure of a plant-pollinator network on a pahoehoe lava desert of the Galápagos Islands. Ecography, 29, 531-540.
94. Pocock, M.J.O., Evans, D.M. & Memmott, J. (2012) The robustness and restoration of a network of ecological networks. Science, 335, 973-977.
95. 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.
96. Potts, S.G., Biesmeijer, J.C., Kremen, C., Neumann, P., Schweiger, O. & Kunin, W.E. (2010) Global pollinator declines: trends, impacts and drivers. Trends in Ecology & Evolution, 25, 345-353.
97. Raguso, R.A. & Willis, M.A. (2005) Synergy between visual and olfactory cues in nectar feeding by wild hawkmoths, Manduca sexta. Animal Behaviour, 69, 407-418.
98. Ramirez, N. (2004) Pollination specialization and time of pollination on a tropical Venezuelan plain: variation in time and space. Botanical Journal of the Linnean Society, 145, 1-16.
99. Rathke, B.J. & Jules, E.S. (1993) Habitat fragmentation and plant-pollinator interactions. Current Science, 65, 273-277.
100. Riordan, D.F. (1964) High-intensity flash discharge as a source of radiant energy for sterilizing insects. Nature, 204, 1332.
101. Robinson, H.S. & Robinson, P.J.M. (1950) Some notes on the observed behavior of Lepidoptera in flight in the vicinity of light sources. Entomologist's Gazette, 1, 3-20.
102. Rydell, J. (1992) Exploitation of insects around streetlamps by bats in Sweden. Functional Ecology, 6, 744-750.
103. Schlenoff, D.H. (1985) The startle responses of blue jays to Catocala (Lepidoptera: Noctuidae) prey models. Animal Behaviour, 33, 1057-1067.
104. Solé, R.C. & Montoya, M. (2001) Complexity and fragility in ecological networks. Proceedings of the Royal Society B, 268, 2039-2045.
105. Somers-Yeates, R., Hodgson, D., McGregor, P.K., Spalding, A. & ffrench-Constant, R.H. (2013) Shedding light on moths: shorter wavelengths attract noctuids more than geometrids. Biology Letters, 9, 20130376.
106. Sotthibandhu, S. & Baker, R.R. (1979) Celestial orientation by the large yellow underwing moth, Noctua pronuba L. Animal Behaviour, 27, 786-800.
107. Sower, L.L., Shorey, H.H. & Gaston, L.K. (1970) Sex pheromones of noctuid moths. XXI. Light: dark cycle regulation and light inhibition of sex pheromone release by females of Trichoplusia ni. Annals of the Entomological Society of America, 63, 1090-1092.
108. Sutherland, W.J., Armstrong-Brown, S., Armsworth, P.R., Brereton, T., Brickland, J., Campbell, C.D. et al. (2006) The identification of 100 ecological questions of high policy relevance in the UK. Journal of Applied Ecology, 43, 617-627.
109. Svensson, A.M. & Rydell, J. (1998) Mercury vapour lamps interfere with the bat defence of tympanate moths (Operophtera spp.; Geometridae). Animal Behaviour, 55, 223-226.
110. Syed, R.A. (1979) Studies on oil palm pollination by insects. Bulletin of Entomological Research, 69, 213-224.
111. Truxa, C. & Fiedler, K. (2012) Attraction to light - from how far do moths (Lepidoptera) return to weak artificial sources of light? European Journal of Entomology, 109, 77-84.
112. Tylianakis, J.M., Didham, R.K., Bascompte, J. & Wardle, D.A. (2008) Global change and species interactions in terrestrial ecosystems. Ecology Letters, 11, 1351-1363.
113. Tylianakis, J.M., Laliberté, E., Nielsen, A. & Bascompte, J. (2010) Conservation of species interaction networks. Biological Conservation, 143, 2270-2279.
114. Wallis De Vries, M.F., Van Swaay, C.A.M. & Plate, C.L. (2012) Changes in nectar supply: a possible cause of widespread butterfly decline. Current Zoology, 58, 384-391.
115. Warren, A.D. (1990) Predation of five species of Noctuidae at ultraviolet light by the western yellowjacket (Hymenoptera: Vespidae). Journal of the Lepidopterists' Society, 44, 32.
116. 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.
117. Williams, P.H. (1982) The distribution and decline of British bumble bees (Bombus Latr.). Journal of Apicultural Research, 21, 236-245.
118. Willmer, P. (2011) Pollination and Floral Ecology. Princeton University Press, Princeton, New Jersey.
119. Winfree, R., Bartomeus, I. & Cariveau, D.P. (2011) Native pollinators in anthropogenic habitats. Annual Review of Ecology, Evolution, and Systematics, 42, 1-22.
120. Young, H.J. (2002) Diurnal and nocturnal pollination of Silene alba (Caryophyllaceae). American Journal of Botany, 89, 433-440.