Artificial light changes visual perception by pollinators in a hawkmoth-plant interaction system
Springer Science and Business Media LLC - Trang 1-15 - 2024
Tóm tắt
Night-flying pollinators, such as hawkmoths, are particularly vulnerable to the global spread of urban artificial lighting which is changing nighttime environments worldwide, impacting organisms and their interactions. Incident light quality can alter flower and leaf color perception by insects, depending on the emission spectra of light sources and the spectral sensitivity of insects. We asked, using Manduca sexta visual models, whether color contrast against natural backgrounds is altered by artificial lights for flowers and leaves of 16 plant species with an estimated long history of coevolution with hawkmoth pollinators. Specifically, we compared the perception of flowers and leaves by hawkmoths under artificial lights, including light-emitting diodes (5000 K LED), mercury vapor (MV), and high-pressure sodium (HPS) artificial lights, with the perception under natural illuminations. The models we implemented estimate that LED and HPS lighting change hawkmoth perception of flowers and leaves, with color loci appearing nearer to each other in hawkmoths perceptual space than they would be under natural nighttime conditions. Receptor Noise Limited models show that under the different lighting conditions hawkmoths would still discriminate flowers from their leaves in most but not all species. Consequently, artificial lights likely alter perception by hawkmoths of floral and leaf signals possibly affecting interactions and fitness of plants and pollinators. Our results emphasize the intricate and insidious ways in which human-made environments impact species interactions. Further studies should confirm whether light pollution represents a novel selective force to nocturnal interacting partners as emerging evidence suggests. Addressing the effects of artificial lighting is crucial for designing infrastructure development strategies that minimize these far-reaching effects on ecosystem functioning.
Tài liệu tham khảo
Aoki S, Ito M (2000) Molecular phylogeny of Nicotiana (Solanaceae) based on the nucleotide sequence of the matK gene. Plant Biol 2:316–324. https://doi.org/10.1055/s-2000-3710
Balbuena MS, Broadhead GT, Dahake A et al (2022) Mutualism has its limits: consequences of asymmetric interactions between a well-defended plant and its herbivorous pollinator. Philos Trans R Soc B Biol Sci 377:20210166. https://doi.org/10.1098/rstb.2021.0166
Balkenius A, Kelber A, Balkenius C (2004) A model of selection between stimulus and place strategy in a hawkmoth. Adapt Behav 12:21–35. https://doi.org/10.1177/105971230401200101
Bariles JB, Cocucci AA, Soteras F (2021) Pollination and fitness of a hawkmoth-pollinated plant are related to light pollution and tree cover. Biol J Linn Soc 134:815–822. https://doi.org/10.1093/biolinnean/blab114/6377657
Bennett RR, Brown PK (1985) Properties of the visual pigments of the moth Manduca sexta and the effects of two detergents, digitonin and CHAPS. Vis Res 25:1771–1781. https://doi.org/10.1016/0042-6989(85)90002-1
Boyes DH, Evans DM, Fox R et al (2020) Is light pollution driving moth population declines? A review of causal mechanisms across the life cycle. Insect Conserv Divers 14:167–187. https://doi.org/10.1111/icad.12447
Briolat ES, Gaston KJ, Bennie J et al (2021) Artificial nighttime lighting impacts visual ecology links between flowers, pollinators and predators. Nat Commun 12:4163. https://doi.org/10.1038/s41467-021-24394-0
Bukovac Z, Shrestha M, Garcia JE et al (2017) Why background colour matters to bees and flowers. J Comp Physiol A 203:369–380. https://doi.org/10.1007/s00359-017-1175-7
Chittka L, Kevan PG (2005) Flower colors as advertisement. In Practical pollination biology. Enviroquest
Clarkson JJ, Dodsworth S, Chase MW (2017) Time-calibrated phylogenetic trees establish a lag between polyploidisation and diversification in Nicotiana (Solanaceae). Plant Syst Evol 303:1001–1012. https://doi.org/10.1007/s00606-017-1416-9
R Core Team (2022) R: A language and environment for statistical computing
Cutler D, Bennett R, Stevenson R, White R (1995) Feeding behavior in the nocturnal moth Manduca sexta is mediated mainly by blue receptors, but where are they located in the retina? J Exp Biol 198:1909–1917. https://doi.org/10.1242/jeb.198.9.1909
Davies TW, Bennie J, Inger R, Gaston KJ (2013) Artificial light alters natural regimes of night-time sky brightness. Sci Rep 3:1–6. https://doi.org/10.1038/srep01722
Deichmann JL, Ampudia Gatty C, Andía Navarro JM et al (2021) Reducing the blue spectrum of artificial light at night minimises insect attraction in a tropical lowland forest. Insect Conserv Divers 14:247–259. https://doi.org/10.1111/icad.12479
Deora T, Ahmed MA, Brunton BW, Daniel TL (2021) Learning to feed in the dark: how light level influences feeding in the Hawkmoth Manduca sexta. Biol Lett 17:20210320. https://doi.org/10.1098/rsbl.2021.0320
Dimovski AM, Robert KA (2018) Artificial light pollution: shifting spectral wavelengths to mitigate physiological and health consequences in a nocturnal marsupial mammal. J Exp Zool Part Ecol Integr Physiol 329:497–505. https://doi.org/10.1002/jez.2163
Fenske MP, Nguyen LAP, Horn EK et al (2018) Circadian clocks of both plants and pollinators influence flower seeking behavior of the pollinator hawkmoth Manduca sexta. Sci Rep 8:1–13. https://doi.org/10.1038/s41598-018-21251-x
Gagnon E, Ringelberg JJ, Bruneau A et al (2019) Global succulent biome phylogenetic conservatism across the pantropical Caesalpinia Group (Leguminosae). New Phytol 222:1994–2008. https://doi.org/10.1111/nph.15633
Galfrascoli GM, Calviño A, Chiapero AL, Fenoglio MS (2023) Living in an urban pod: seed predation and parasitism of bruchid beetles in a native tree species. Ecol Entomol 48:31–39. https://doi.org/10.1111/een.13199
Gaston KJ, Bennie J, Davies TW, Hopkins J (2013) The ecological impacts of nighttime light pollution: a mechanistic appraisal. Biol Rev 88:912–927. https://doi.org/10.1111/brv.12036
Giavi S, Fontaine C, Knop E (2021) Impact of artificial light at night on diurnal plant-pollinator interactions. Nat Commun 12:8–13. https://doi.org/10.1038/s41467-021-22011-8
Goyret J, Raguso RA (2006) The role of mechanosensory input in flower handling efficiency and learning by Manduca sexta. J Exp Biol 209:1585–1593. https://doi.org/10.1242/jeb.02169
Goyret J, Markwell PM, Raguso RA (2007) The effect of decoupling olfactory and visual stimuli on the foraging behavior of Manduca sexta. J Exp Biol 210:1398–1405. https://doi.org/10.1242/jeb.02752
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. Naturwissenschaften 95:569–576. https://doi.org/10.1007/s00114-008-0350-7
Haxaire J (2019) A revised and annotated checklist of the Brazilian Sphingidae with new records, taxonomical notes, and description of one new species (Lepidoptera Sphingidae). Eur Entomol 11:101–187
Henze MJ, Lind O, Mappes J et al (2018) An aposematic colour-polymorphic moth seen through the eyes of conspecifics and predators – sensitivity and colour discrimination in a tiger moth. Funct Ecol 32:1797–1809. https://doi.org/10.1111/1365-2435.13100
Johnsen S, Kelber A, Eric Warrant et al (2006) Crepuscular and nocturnal illumination and its effects on color perception by the nocturnal hawkmoth Deilephila elpenor. J Exp Biol 209:789–800
Kariñho-Betancourt E, Carlson D, Hollister J et al (2022) The evolution of multi-gene families and metabolic pathways in the evening primroses (Oenothera: Onagraceae): a comparative transcriptomics approach. PLoS ONE 17:e0269307. https://doi.org/10.1371/journal.pone.0269307
Kessler D, Diezel C, Baldwin IT (2010) Changing pollinators as a means of escaping herbivores. Curr Biol 20:237–242. https://doi.org/10.1016/j.cub.2009.11.071
Kitching IJ (2022) Sphingidae Taxonomic Inventory. Accessed 9 Mar 2023
Kuenzinger W, Kelber A, Weesner J et al (2019) Innate colour preferences of a hawkmoth depend on visual context. Biol Lett 15:20180886. https://doi.org/10.1098/rsbl.2018.0886
Lind O (2016) Colour vision and background adaptation in a passerine bird, the zebra finch (Taeniopygia guttata). R Soc Open Sci 3:160383. https://doi.org/10.1098/rsos.160383
Longcore T (2023) A compendium of photopigment peak sensitivities and visual spectral response curves of terrestrial wildlife to guide design of outdoor nighttime lighting. Basic Appl Ecol 73:40–50. https://doi.org/10.1016/j.baae.2023.09.002
Longcore T, Aldern HL, Eggers JF et al (2015) Tuning the white light spectrum of light emitting diode lamps to reduce attraction of nocturnal arthropods. Philos Trans R Soc B Biol Sci 370:20140125. https://doi.org/10.1098/rstb.2014.0125
Longcore T, Rodríguez A, Witherington B et al (2018) Rapid assessment of lamp spectrum to quantify ecological effects of light at night. J Exp Zool Part Ecol Integr Physiol 329:511–521. https://doi.org/10.1002/jez.2184
Macgregor CJ, Evans DM, Fox R, Pocock MJOO (2017) The dark side of street lighting: impacts on moths and evidence for the disruption of nocturnal pollen transport. Glob Change Biol 23:697–707. https://doi.org/10.1111/gcb.13371
Maia R, White TE (2018) Comparing colors using visual models. Behav Ecol 29:649–659. https://doi.org/10.1093/beheco/ary017
Maia R, Gruson H, Endler JA, White TE (2019) pavo 2: New tools for the spectral and spatial analysis of colour in r. Methods Ecol Evol 10:1097–1107. https://doi.org/10.1111/2041-210X.13174
Martins DJ, Johnson SD (2009) Distance and quality of natural habitat influence hawkmoth pollination of cultivated papaya. Int J Trop Insect Sci 29:114–123. https://doi.org/10.1017/S1742758409990208
Moré M, Benitez-vieyra S, Sérsic AN, Cocucci AA (2014) Patrones De depósito De Polen Sobre El Cuerpo De Los polinizadores en comunidades esfingófilas de Argentina subtropical. Darwiniana 2:174–196. https://doi.org/10.14522/darwiniana.2014.21.568
Moré M, Cocucci AA, Sérsic AN, Barboza GE (2015) Phylogeny and floral trait evolution in Jaborosa (Solanaceae). Taxon 64:523–534. https://doi.org/10.12705/643.8
Moré M, Ibañez AC, Drewniak ME et al (2020) Flower diversification across pollinator climates: sensory aspects of corolla color evolution in the florally diverse south American genus Jaborosa (Solanaceae). Front Plant Sci 11:601975. https://doi.org/10.3389/fpls.2020.601975
Moyse E, Firth LB, Smyth T et al (2023) Artificial light at night alters predation on colour-polymorphic camouflaged prey. Basic Appl Ecol 73:88–93. https://doi.org/10.1016/j.baae.2023.11.002
Oksanen J, Simpson G, Blanchet F et al (2022) _vegan: Community Ecology Package_. R package version 2.6–4, https://CRAN.R-project.org/package=vegan
Olsson P, Lind O, Kelber A (2018) Chromatic and achromatic vision: parameter choice and limitations for reliable model predictions. Behav Ecol 29:273–282. https://doi.org/10.1093/beheco/arx133
Owens ACS, Lewis SM (2018) The impact of artificial light at night on nocturnal insects: a review and synthesis. Ecol Evol 8:11337–11358. https://doi.org/10.1002/ece3.4557
Pawson SM, Bader MK-F (2014) LED lighting increases the ecological impact of light pollution irrespective of color temperature. Ecol Appl 24:1561–1568. https://doi.org/10.1890/14-0468.1
Peres-Neto P, Jackson D (2001) How well do multivariate data sets match? The advantages of a procrustean superimposition approach over the Mantel test. Oecologia 129:169–178. https://doi.org/10.1007/s004420100720
Pimputkar S, Speck JS, Denbaars SP, Nakamura S (2009) Prospects for LED lighting. Nat Photonics 3:180–182. https://doi.org/10.1038/nphoton.2009.32
Raguso RA, Willis MA (2002) Synergy between visual and olfactory cues in nectar feeding by naïve hawkmoths, Manduca sexta. Anim Behav 64:685–695. https://doi.org/10.1006/anbe.2002.4010
Reck-Kortmann M, Silva-Arias GA, Segatto ALA et al (2014) Multilocus phylogeny reconstruction: new insights into the evolutionary history of the genus Petunia. Mol Phylogenet Evol 81:19–28. https://doi.org/10.1016/j.ympev.2014.08.022
Renoult JP, Kelber A, Schaefer HM (2017) Colour spaces in ecology and evolutionary biology. Biol Rev Camb Philos Soc 92:292–315. https://doi.org/10.1111/brv.12230
Sazatornil FD, Moré M, Benitez-Vieyra S et al (2016) Beyond neutral and forbidden links: morphological matches and the assembly of mutualistic hawkmoth–plant networks. J Anim Ecol 85:1586–1594. https://doi.org/10.1111/1365-2656.12509
Silberbauer-Gottsberger I, Gottsberger G (1975) Über Sphingophile Angiospermen Brasiliens. Plant Syst Evol 123:157–184. https://doi.org/10.1007/BF00989402
Soteras F, Rubini Pisano MA, Bariles JB et al (2020) Phenotypic selection mosaic for flower length influenced by geographically varying hawkmoth pollinator proboscis length and abiotic environment. New Phytol 225:985–998. https://doi.org/10.1111/nph.16192
Stöckl AL, Kelber A (2019) Fuelling on the wing: sensory ecology of hawkmoth foraging. J Comp Physiol A 205:399–413. https://doi.org/10.1007/s00359-019-01328-2
Stöckl A, Heinze S, Charalabidis A et al (2016) Differential investment in visual and olfactory brain areas reflects behavioural choices in hawk moths. Sci Rep 6:26041. https://doi.org/10.1038/srep26041
Storms M, Mitesser O, Degen T et al (2022) The rising moon promotes mate finding in moths. Commun Biol 5:393. https://doi.org/10.1038/s42003-022-03331-x
Straka TM, von der Lippe M, Voigt CC et al (2021) Light pollution impairs urban nocturnal pollinators but less so in areas with high tree cover. Sci Total Environ 778:146244. https://doi.org/10.1016/j.scitotenv.2021.146244
Telles FJ, Lind O, Henze MJ et al (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
van der Kooi CJ, Kelber A (2022) Achromatic cues are important for flower visibility to hawkmoths and other insects. Front Ecol Evol 10:819436. https://doi.org/10.3389/fevo.2022.819436
van Grunsven RHA, Lham D, Van Geffen KG, Veenendaa EM (2014) Range of attraction of a 6-W moth light trap. Entomol Exp Appl 152:87–90. https://doi.org/10.1111/eea.12196
van Langevelde F, Ettema JA, Donners M et al (2011) Effect of spectral composition of artificial light on the attraction of moths. Biol Conserv 144:2274–2281. https://doi.org/10.1016/j.biocon.2011.06.004
Vorobyev M, Osorio D (1998) Receptor noise as a determinant of colour thresholds. Proc R Soc Lond B Biol Sci 265:351–358. https://doi.org/10.1098/rspb.1998.0302
Walton RE, Sayer CD, Bennion H, Axmacher JC (2020) Nocturnal pollinators strongly contribute to pollen transport of wild flowers in an agricultural landscape. Biol Lett 16:20190877. https://doi.org/10.1098/rsbl.2019.0877
Warrant EJ (2017) The remarkable visual capacities of nocturnal insects: vision at the limits with small eyes and tiny brains. Philos Trans R Soc B Biol Sci 372:20160063. https://doi.org/10.1098/rstb.2016.0063
Warrant E, Dacke M (2011) Vision and visual navigation in nocturnal insects. Annu Rev Entomol 56:239–254. https://doi.org/10.1146/annurev-ento-120709-144852
Warrant E, Somanathan H (2022) Colour vision in nocturnal insects. Philos Trans R Soc B Biol Sci 377:20210285. https://doi.org/10.1098/rstb.2021.0285
White RH, Stevenson RD, Bennett RR et al (1994) Wavelength discrimination and the role of ultraviolet vision in the feeding behavior of Hawkmoths. Biotropica 26:427. https://doi.org/10.2307/2389237
White RH, Xu H, Münch TA et al (2003) The retina of Manduca sexta: rhodopsin expression, the mosaic of green-, blue- and UV-sensitive photoreceptors, and regional specialization. J Exp Biol 206:3337–3348. https://doi.org/10.1242/jeb.00571