Abstract
Plant colouration is known to be used by some nocturnal flower-visiting insects to foraging among colourful flowers in dim light. However, it remains unknown whether crepuscular species possibly reliably discriminate plant colouration (i.e. colour and/or brightness) for oviposition even driven by challenges of variably light conditions and similar leaf colouration. Here, we explored this question in the oriental fruit moth Grapholita molesta, a major pest of stone fruits worldwide, using coloured squares under changing illuminants (1000, 100, 1 and 0.01 mW/m2). G. molesta female preferred to oviposit on green and orange over yellow, red, blue and purple with a lower discrimination at starlight (0.01 mW/m2), whereas the preferential brighter white can be discriminated clearly from those achromatic grey and black at all tested light intensities. When both cues were presented in conflicting for oviposition, the moths were more attracted to brightness than colour cues irrespective of light intensity they are exposed to. Interestingly, there was a decrease in the reflectance between young and old leaves of P. persica at similar wavelengths between 500 and 550 nm, providing an apparent brightness. Ovipositing females preferred the brighter light green over the dark green. Our results indicate that as a more reliable cue, brightness of leaves rather than colour plays a more important role for mediating crepuscular moth G. molesta to lay eggs on young leaves in microhabitats in changing light environments. We discuss that the brightness oriented in oviposition task in complex orchards is relevant to leaf apparency.
Similar content being viewed by others
References
Balkenius A, Kelber A (2004) Colour constancy in diurnal and nocturnal hawkmoths. J Exp Biol 207:3307–3316. https://doi.org/10.1242/jeb.01158
Balkenius A, Rosén W, Kelber A (2006) The relative importance of olfaction and vision in a diurnal and a nocturnal hawkmoth. J Comp Physiol A 192:431–437. https://doi.org/10.1007/s00359-005-0081-6
Brito VCLG, Weynans K, Sazima M, Lunau K (2015) Trees as huge flowers and flowers as oversized floral guides: the role of floral colour change and retention of old flowers in Tibouchina pulchra. Front Plant Sci 6:1–10. https://doi.org/10.3389/fpls.2015.00362
Chittka L, Döring TF (2007) Are autumn foliage colours red signals to aphids? PLoS Biol 5:e187. https://doi.org/10.1371/journal.pbio.0050187
Desouhant E, Navel S, Foubert E, Fischbein D, Théry M, Bernstein C (2010) What matters in the associative learning of visual cues in foraging parasitoid wasps: colour or brightness? Anim Cogn 3:535–543. https://doi.org/10.1007/s10071-009-0304-2
Döring TF, Archetti M, Hardie J (2009) Autumn leaves seen through herbivore eyes. Proc Biol Sci 276:121–127. https://doi.org/10.1098/rspb.2008.0858
Endler JL (1993) The colour of light in forests and its implications. Ecol Monogr 63:1–27. https://doi.org/10.2307/2937121
Farnier K, Dyer AG, Steinbauer MJ (2014) Related but not alike: not all Hemiptera are attracted to yellow. Front Ecol Evol 2:1–12. https://doi.org/10.3389/fevo.2014.00067
Farnier K, Dyer AG, Taylor GS, Peters RA, Steinbauer MJ (2015) Visual acuity trade-offs and microhabitat-driven adaptation of searching behaviour in psyllids (Hemiptera: Psylloidea: Aphalaridae). J Exp Biol 218(10):1564–1571. https://doi.org/10.1242/jeb.120808
Frederiksen R, Wcislo WT, Warrant E (2008) Visual reliability and information rate in the retina of a nocturnal bee. Curr Biol 18:349–353. https://doi.org/10.1016/j.cub.2008.01.057
Hempel de Ibarra N, Giurfa M, Vorobyev M (2001) Detection of coloured patterns by honeybees through chromatic and achromatic cues. J Comp Physiol A 187:215–224. https://doi.org/10.1007/s003590100192
Hempel de Ibarra N, Langridge KV, Vorobyev M (2015) More than colour attraction: behavioural functions of flower patterns. Curr Opin Insect Sci 12:64–70. https://doi.org/10.1016/j.cois.2015.09.005
Hughes J, Dorn S (2002) Sexual differences in the flight performance of the oriental fruit moth, Cydia molesta. Entomol Exp Appl 103:171–182. https://doi.org/10.1046/j.1570-7458.2002.00967.x
Il’Ichev AL, Kugimiya S (2009) Volatile compounds from young peach shoots attract males of oriental fruit moth in the field. J Plant Interact 4:289–294. https://doi.org/10.1080/17429140903267814
Ilse D (1937) New observations on responses to colours in egg-laying butterflies. Nature 140:544–545. https://doi.org/10.1038/140544a0
Jakobsson J, Henze MJ, Svensson GP, Lind O, Anderbrant O (2017) Visual cues of oviposition sites and spectral sensitivity of Cydia strobilella L. J Insect Physiol 101:161–168. https://doi.org/10.1016/j.jinsphys.2017.06.006
Katsoyannos BI, Patsouras G, Vrekoussi M (1985) Effect of colour hue and brightness of artificial oviposition substrates on the selection of oviposition site by Dacus oleae. Entomol Exp Appl 38:205–214. https://doi.org/10.1111/j.1570-7458.1985.tb03520.x
Kelber A (1999) Ovipositing butterflies use a red receptor to see green. J Exp Biol 202:2619–2630. https://doi.org/10.1038/46204
Kelber A (2005) Alternative use of chromatic and achromatic cues in a hawkmoth. Proc Biol Sci 272:2143–2147. https://doi.org/10.1098/rspb.2005.3207
Kelber A, Balkenius A, Warrant EJ (2002) Scotopic colour vision in nocturnal hawkmoths. Nature 419:922–925. https://doi.org/10.1038/nature01065
Kinoshita M, Takahashi Y, Arikawa K (2012) Simultaneous brightness contrast of foraging Papilio butterflies. Proc Biol Sci 279:1911–1918. https://doi.org/10.1098/rspb.2011.2396
Knight AL, Pickel C, Hawkins L, Abbott C, Hansen R, Hull L (2011) Monitoring oriental fruit moth (Lepidoptera: Tortricidae) and peach twig borer (Lepidoptera: Gelechiidae) with clear delta-shaped traps. J Appl Entomol 135:106–114. https://doi.org/10.1111/j.1439-0418.2010.01538.x
Koethe S, Bossems J, Dyer AG, Lunau K (2016) Colour is more than hue: preferences for compiled colour traits in the stingless bees Melipona mondury and M. quadrifasciata. J Comp Physiol A 202:615–627. https://doi.org/10.1007/s00359-016-1115-y
Lev-Yadun S, Dafni A, Flaishman MA, Inbar M, Izhaki I, Katzir G, Ne’eman G (2004) Plant colouration undermines herbivorous insect camouflage. BioEssays 26:1126–1130. https://doi.org/10.1002/bies.20112
Myers CT, Hull LA, Krawczyk G (2007) Effects of orchard host plants (apple and peach) on development of oriental fruit moth (Lepidoptera: Tortricidae). J Econ Entomol 100:421–430. https://doi.org/10.1603/0022-0493(2007)100%5b421:eoohpa%5d2.0.co;2
Najar-Rodriguez A, Orschel B, Dorn S (2013) Season-long volatile emissions from peach and pear trees in situ, overlapping profiles, and olfactory attraction of an oligophagous fruit moth in the laboratory. J Chem Ecol 39:418–429. https://doi.org/10.1007/s10886-013-0262-7
Natale D, Mattiacci L, Hern A, Pasqualini E, Dorn S (2003) Response of female Cydia molesta (Lepidoptera: Tortricidae) to plant derived volatiles. Bull Entomol Res 93:335–342. https://doi.org/10.1079/ber2003250
Natale D, Mattiacci L, Hern A, Pasqualini E, Dorn S (2004) Apple and peach fruit volatiles and the apple constituent butylhexanoate attract female oriental fruit moth, Cydia molesta, in the laboratory. J Appl Entomol 128:22–27. https://doi.org/10.1046/j.1439-0418.2003.00802.x
Notter-Hausmann C, Dorn S (2010) Relationship between behavior and physiology in an invasive pest species: oviposition site selection and temperature dependent development of the oriental fruit moth (Lepidoptera: Tortricidae). Environ Entomol 39:561–569. https://doi.org/10.1603/EN09231
Piñero JC, Dorn S (2009) Response of female oriental fruit moth to volatiles from apple and peach trees at three phenological stages. Entomol Exp Appl 131:67–74. https://doi.org/10.1111/j.1570-7458.2009.00832.x
Prokopy RJ, Collier RH, Finch S (1983) Leaf colour used by cabbage root flies to distinguish among host plants. Science 221:190–192. https://doi.org/10.1126/science.221.4606.190
Raguso RA, Willis MA (2005) Synergy between visual and olfactory cues in nectar feeding by wild hawkmoths, Manduca sexta. Anim Behav 69:407–418. https://doi.org/10.1016/j.anbehav.2004.04.015
Régolini M, Castagneyrol B, Dulaurent-Mercadal AM, Piou D, Samalens JC, Jactel H (2014) Effect of host tree density and apparency on the probability of attack by the pine processionary moth. Forest Ecol Manag 334:185–192. https://doi.org/10.1016/j.foreco.2014.08.038
Rohde K, Papiorek S, Lunau K (2013) Bumblebees (Bombus terrestris) and honeybees (Apis mellifera) prefer similar colours of higher spectral purity over trained colours. J Comp Physiol A 199:197–210. https://doi.org/10.1007/s00359-012-0783-5
Somanathan H, Borges RM, Warrant EJ, Kelber A (2008) Nocturnal bees can learn the colours of landmarks in starlight. Curr Biol 18:349–353. https://doi.org/10.1016/j.cub.2008.08.023
Sponberg S, Dyhr JP, Hall RW, Daniel TL (2015) Luminance-dependent visual processing enables moth flight in low light. Science 348:1245–1248. https://doi.org/10.1126/science.aaa3042
Sun YX, Tian A, Zhang XB, Zhao ZG, Zhang ZW, Ma RY (2014) Phototaxis of Grapholitha molesta (Lepidoptera: Olethreutidae) to different light sources. J Econ Entomol 107:1792–1799. https://doi.org/10.1603/EC14155
Talsma JHR, Biere A, Harvey JA, Nouhuys SV (2008) Oviposition cues for a specialist butterfly–plant chemistry and size. J Chem Ecol 34:1202–1212. https://doi.org/10.1007/s10886-008-9519-y
Tasin M, Lucchi A, Ioriatti C, Mraihi M, De CA, Boger Z, Anfora G (2011) Oviposition response of the moth Lobesia botrana to sensory cues from a host plant. Chem Senses 36:633–639. https://doi.org/10.1093/chemse/bjr027
Telles FJ, Lind O, Henze MJ, Rodríguez-Gironés MA, Goyret J, Kelber A (2014) Out of the blue: the spectral sensitivity of hummingbird hawkmoths. J Comp Physiol A 200:537–546. https://doi.org/10.1007/s00359-014-0888-0
Tsuji J, Coe L (2014) Effects of Foliage Colour on the Landing Response of Pieris rapae (Lepidoptera: Pieridae). Environ Entomol 43:989–994. https://doi.org/10.1603/EN14084
Veilleux CC, Cummings ME (2012) Nocturnal light environments and species ecology: implications for nocturnal colour vision in forests. J Exp Biol 215:4085–4096. https://doi.org/10.1242/jeb.071415
Warrant E (2008) Seeing in the dark: vision and visual behaviour in nocturnal bees and wasps. J Exp Biol 211:1737–1746. https://doi.org/10.1242/jeb.015396
Warrant E, Dacke M (2016) Visual navigation in nocturnal insects. Physiology 31:182–192. https://doi.org/10.1152/physiol.00046.2015
Wiklund C (1984) Egg-laying patterns in butterflies in relation to their phenology and the visual apparency and abundance of their host plants. Oecologia 63:23–29. https://doi.org/10.1007/BF00379780
Yang XF, Ma CS, Fan F, Liu YF, Feng N, Li Q, Wei GS (2014) Effect of colours on oviposition preference of the oriental fruit moth, Grapholita molesta Busck. Acta Ecol Sin 34:2971–2977. https://doi.org/10.5846/stxb201211101575
Yang XF, Fan F, Wang C, Wei GS (2016) Effect of host plants on the development, survivorship and reproduction of Grapholita molesta (Lepidoptera: Tortricidae) under laboratory conditions. Aust Entomol 55:433–438. https://doi.org/10.1111/aen.12204
Zhang PJ, Lu YB, Zalucki MP, Liu SS (2012) Relationship between adult oviposition preference and larval performance of the diamondback moth, Plutella xylostella. J Pest Sci 85:247–252. https://doi.org/10.1007/s10340-012-0425-2
Acknowledgements
We thank Zhikui Gao for use of his spectrometer and Yanhong Bian for rearing the insects. This study was supported by the National Key Research and Development Program of China (No. 2017YFD0200906) and the Key Research and Development Program of Hebei (19226511D).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by J. Gross.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Yang, X., Li, M., Fan, F. et al. Brightness mediates oviposition in crepuscular moth, Grapholita molesta. J Pest Sci 93, 1311–1319 (2020). https://doi.org/10.1007/s10340-020-01255-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-020-01255-1