Impact of artificial illumination on the development of a leafmining moth in urban trees
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Abstract
Light emission from street lighting or other light sources alters the living conditions for organisms in urban areas. Nowadays, the impact of light at night (ALAN) on urban plants and their trophic environment is not well understood. To gain more insight about herbivore plant’s interaction when exposed to ALAN, outdoor and greenhouse tests were conducted using the horse-chestnut leafminer, Cameraria ohridella, as a test organism due to its adaptive behavior. At the end of the season, the development of chestnut tree leaves and the leafminer were measured at illuminated versus non-illuminated sites in the city of Berlin and the rural area of Brandenburg. Illuminated leaves were larger than those grown in darker rural areas and, extended larval activity was recorded. Additionally, in the greenhouse, infested chestnut seedlings were exposed to two different light regimes; one treatment provided continuous illumination and the other short daylight conditions. After only one week, the mine size was lower on illuminated seedlings, presumably due to reduced leaf senescence. The leafminer developed a lower proportion of diapausing pupae and a higher proportion of free pupae, which leads to a further generation within the season. The results indicate a strong impact of ALAN on plant metabolism, a secondary effect on leafminer development and its larval activity. For urban trees, the consequence might be an increased herbivore / parasite pressure. For herbivores and parasites less adapted to winter damages than the invasive leafminer a reduced dormancy due to direct or indirect effects of ALAN could even threat the population.
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Keywords
Aesculus hippocastanum, artificial light at night, light pollution, horse chestnut leafminer, diapause induction, dormancy
References
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[22.] Valade, R., Kenis, M., Hernandez?Lopez, A., Augustin, S., Mari Mena, N., Magnoux, E., ... & Lopez?Vaamonde, C. (2009). Mitochondrial and microsatellite DNA markers reveal a Balkan origin for the highly invasive horse-chestnut leaf miner Cameraria ohridella (Lepidoptera, Gracillariidae). Molecular Ecology, 18(16), 3458-3470. https://doi.org/10.1111/j.1365-294X.2009.04290.x
[23.] Šefrová, H. & Lašt?vka, Z. (2001). Dispersal of the horse-chestnut leafminer Cameraria ohridella Deschka & Dimic 1986, in Europe: Its course, ways and causes (Lepidoptera?: Gracillariidae). Entomologische Zeitschrift Stuttgart, 111, 194-198.
[24.] Hellrigl, K. (2001). Neue Erkenntnisse und Untersuchungen über die Roßkastanien-Miniermotte Cameraria ohridella Deschka & Dimic, 1986 (Lepidoptera, Gracillariidae). Gredleriana, 1(2001), 9-81. https://www.zobodat.at/stable/pdf/Gredleriana_001_0009-0082.pdf
[25.] Pschorn-Walcher, H. (1994). Freiland-Biologie der eingeschleppten Roßkastanien- Miniermotte Cameraria ohridella DESCHKA et DIMIC (Lep ., Gracillariidae) im Wienerwald. Linzer Biologische Beiträge, 26, 633-642. http://www.zobodat.at/pdf/LBB_0026_2_0633-0642.pdf
[26.] Samek, T. (2003). Diapause of Cameraria ohridella Deschka et Dimic and its impact on the species population dynamics. Journal of Forest Science, 49, 252-258. https://81.0.228.28/publicFiles/55742.pdf
[27.] Pretzsch, H., Biber, P., Uhl, E., Dahlhausen, J., Schütze, G., Perkins, D., ... & Chavanne, A. (2017). Climate change accelerates growth of urban trees in metropolises worldwide. Scientific Reports, 7(1), 15403. https://www.nature.com/articles/s41598-017-14831-w
[28.] Vollsnes, A. V., Eriksen, A. B., Otterholt, E., Kvaal, K., Oxaal, U., & Futsaether, C. M. (2009). Visible foliar injury and infrared imaging show that daylength affects short-term recovery after ozone stress in Trifolium subterraneum. Journal of Experimental Botany, 60(13), 3677-86. https://doi.org/10.1093/jxb/erp213
[29.] Kwak, M. J., Lee, S. H., Khaine, I., Je, S. M., Lee, T. Y., You, H. N., ... & Woo, S. Y. (2017). Stomatal movements depend on interactions between external night light cue and internal signals activated by rhythmic starch turnover and abscisic acid (ABA) levels at dawn and dusk. Acta Physiologae Plantarum, 39(8), 162. https://link.springer.com/article/10.1007/s11738-017-2465-y
[30.] Vogel, G. (2017). Where have all the insects gone? Science, 356(6338), 576-579. http://science.sciencemag.org/content/356/6338/576.summary
[31.] Hallmann, C. A., Sorg, M., Jongejans, E., Siepel, H., Hofland, N., Schwan, H., ... & Goulson, D. (2017). More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS One, 12(10), e0185809. https://doi.org/10.1371/journal.pone.0185809
[32.] Grubisic, M., van Grunsven, R. H. A., Kyba, C. C. M., Manfrin, A. & Hölker, F. (2018). Insect declines and agroecosystems: does light pollution matter? Annals of Applied Biology, 173(2), 180-189. https://doi.org/10.1111/aab.12440
[33.] van Langevelde, F., Braamburg?Annegarn, M., Huigens, M. E., Groendijk, R., Poitevin, O., van Deijk, J. R., ... & Franzén, M. (2018). Declines in moth populations stress the need for conserving dark nights. Global Change Biology, 24(3), 925-932. https://doi.org/10.1111/gcb.14008
[34.] Augustin, S., Guichard, S., Heitland, W., Freise, J., Svatoš, A., & Gilbert, M. (2009). Monitoring and dispersal of the invading Gracillariidae Cameraria ohridella. Journal of Applied Entomology, 133(1), 58-66. https://doi.org/10.1111/j.1439-0418.2008.01333.x
[35.] Kuechly, H. U., Kyba, C. C., Ruhtz, T., Lindemann, C., Wolter, C., Fischer, J., & Hölker, F. (2012). Arial survey and spatial analysis of sources of light pollution in Berlin, Germany. Remote Sensing of Environment, 126, 39-50. https://doi.org/10.1016/j.rse.2012.08.008
[36.] Davies, T. W., Bennie, J., & Gaston, K. J. (2012). Street lighting changes the composition of invertebrate communities. Biology letters, 8, 764-767, rsbl20120216. http://rsbl.royalsocietypublishing.org/content/early/2012/05/15/rsbl.2012.0216.short
[37.] Manfrin, A., Singer, G., Larsen, S., Weiß, N., van Grunsven, R. H., et al. (2017). Artificial light at night affects organism flux across ecosystem boundaries and drives community structure in the recipient ecosystem. Frontiers in Environmental Science, 5, 61. https://doi.org/10.3389/fenvs.2017.00061
[38.] Girardoz, S., Quicke, D. L. J. & Kenis, M. (2007). Factors favouring the development and maintenance of outbreaks in an invasive leaf miner Cameraria ohridella (Lepidoptera: Gracillariidae): A life table study. Agricultureal and Forest Entomology, 9(2), 141-158. https://doi.org/10.1111/j.1461-9563.2007.00327.x
[39.] Balder, H. & Jäckel, B. (2003). Die Kastanienminiermotte und mögliche Gegenmassnahmen. Stadt Grün, 5, 44-49.
[40.] Hogewoning, S. W., Trouwborst, G., Maljaars, H., Poorter, H., van Ieperen, W., & Harbinson, J. (2010). Blue light dose-responses of leaf photosynthesis, morphology, and chemical composition of Cucumis sativus grown under different combinations of red and blue light. Journal of Experimental Botany, 61(11), 3107-3117. https://doi.org/10.1093/jxb/erq132
[41.] Longcore, T., Rodríguez, A., Witherington, B., Penniman, J. F., Herf, L., & Herf, M. (2018). Rapid assessment of lamp spectrum to quantify ecological effects of light at night. Journal of Experimental Zoology Part A: Ecological and Integrative Physiology. 1-11. https://doi.org/10.1002/jez.2184
[42.] van Langevelde, F., Ettema, J. A., Donners, M., WallisDeVries, M. F. & Groenendijk, D. (2011). Effect of spectral composition of artificial light on the attraction of moths. Biological Conservation 144(9), 2274-2281. https://doi.org/10.1016/j.biocon.2011.06.004
[43.] Schroer, S. & Hölker, F. (2017) Light pollution reduction. Handbook of Advanced Lighting Technology (eds. Karlicek, R., Sun, C.-C., Zissis, G. & Ma, R.) Springer, Cham, 991-1010. https://link.springer.com/referenceworkentry/10.1007%2F978-3-319-00295-8_43-1
[2.] Kyba, C. C., Kuester, T., de Miguel, A. S., Baugh, K., Jechow, A., Hölker, F., ... & Guanter, L.. et al. (2017). Artificially lit surface of Earth at night increasing in radiance and extent. cience Advances, 3(11), 1-9. http://advances.sciencemag.org/content/3/11/e1701528
[3.] Hölker, F., Moss, T., Griefahn, B., Kloas, W. & Voigt, C. C. (2010). The dark side of light: a transdisciplinary research agenda for light. Ecolology and Society, 15(4), 13. https://www.jstor.org/stable/26268230
[4.] Kyba, C. C., Tong, K. P., Bennie, J., Birriel, I., Birriel, J. J., Cool, A., ... & Ehlert, R. (2015). Worldwide variations in artificial skyglow. Scientific Reports, 5, 8409. https://www.nature.com/articles/srep08409
[5.] Kyba, C. C. M., Ruhtz, T., Fischer, J. & Hölker, F. (2011). Cloud coverage acts as an amplifier for ecological light pollution in urban ecosystems. PLoS One, 6, e17307. https://doi.org/10.1371/journal.pone.0017307
[6.] Matzke, E. B. (1936) The effect of street lights in delaying leaf-fall in certain trees. American Journal of Botany, 23, 446-452. https://onlinelibrary.wiley.com/doi/abs/10.1002/j.1537-2197.1936.tb09009.x
[7.] Cathey, H. M. & Campbell, L. E. (1975). Security lighting and its impact on the landscape. Journal of Arboriculture, 1, 181-187.
[8.] Keller, M. M., Jaillais, Y., Pedmale, U. V., Moreno, J. E., Chory, J., & Ballaré, C. L. (2011). Cryptochrome 1 and phytochrome B control shade-avoidance responses in Arabidopsis via partially independent hormonal cascades. Plant Journal, 67(2), 195-207. https://doi.org/10.1111/j.1365-313X.2011.04598.x
[9.] Briggs, W. R. & Christie, J. M. (2002). Phototropins 1 and 2: versatile plant blue-light receptors. Trends in Plant Science, 7, 204-10. https://doi.org/10.1016/S1360-1385(02)02245-8
[10.] Schroer, S. & Hölker, F. (2017). Impact of lighting on flora and fauna. Handbook of Advanced Lighting Technology (eds. Karlicek, R., Sun, C.-C., Zissis, G. & Ma, R.) Springer, Cham, 957-989. https://link.springer.com/referenceworkentry/10.1007%2F978-3-319-00176-0_42
[11.] Sinnadurai, S. (1981) High pressure sodium street lights affect crops in Ghana. World Crops, 33, 120-122.
[12.] Palmer, M., Gibbons, R., Bhagavathula, R., Holshouser, D. & Davidson, D. (2017) Roadway Lighting’S Impact on Altering Soybean Growth. (No. FHWA-ICT-17-010). https://trid.trb.org/view/1471129
[13]. Somers-Yeates, R., Bennie, J., Economou, T., Hodgson, D., Spalding, A., & McGregor, P. K. (2016). Light pollution is associated with earlier tree budburst across the United Kingdom. Proceedings of the Royal Society B, 283(1833), 20160813. http://rspb.royalsocietypublishing.org/content/283/1833/20160813
[14.] Massetti, L. (2018). Assessing the impact of street lighting on Platanus x acerifolia phenology. Urban Forestry and Urban Greening, 34, 71-77. https://doi.org/10.1016/j.ufug.2018.05.015
[15.] Bennie, J., Davies, T. W., Cruse, D., Bell, F. & Gaston, K. J. (2018). Artificial light at night alters grassland vegetation species composition and phenology. Journal of Applied Ecology, 55(1), 442-450. https://doi.org/10.1111/1365-2664.12927
[16.] Futsaether, C. M., Vollsnes, A. V., Kruse, O. M. O., Otterholt, E., Kvaal, K., & Eriksen, A. B. (2009). Effects of the Nordic photoperiod on ozone sensitivity and repair in different clover species studied using infrared imaging. Ambio, 38, 437-42. https://www.jstor.org/stable/40390422
[17.] Knop, E., Zoller, L., Ryser, R., Gerpe, C., Hörler, M., & Fontaine, C. (2017). Artificial light at night as a new threat to pollination. Nature, 548(7666), 206–209. https://www.nature.com/articles/nature23288
[18.] MacGregor, C. J., Evans, D. M., Fox, R. & Pocock, M. J. O. (2017). The dark side of street lighting: Impacts on moths and evidence for the disruption of nocturnal pollen transport. Global Change Biology, 23(2), 697-707. https://doi.org/10.1111/gcb.13371
[19.] van Geffen, K. G., van Eck, E., de Boer, R. A., van Grunsven, R. H., Salis, L., Berendse, F., & Veenendaal, E. M. (2015). Artificial light at night inhibits mating in a Geometrid moth. Insect Conservervation and Diversity, 8(3), 282-287. https://doi.org/10.1111/icad.12116
[20.] van Geffen, K. G., van Grunsven, R. H., 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. Ecolology and Evolution, 4(11), 2082-2089. https://doi.org/10.1002/ece3.1090
[21.] Vänninen, I., Pinto, D. M., Nissinen, A. I., Johansen, N. S. & Shipp, L. (2010). In the light of new greenhouse technologies: 1. Plant-mediated effects of artificial lighting on arthropods and tritrophic interactions. Annals of Applied Biology, 157(3), 393-414. https://doi.org/10.1111/j.1744-7348.2010.00438.x
[22.] Valade, R., Kenis, M., Hernandez?Lopez, A., Augustin, S., Mari Mena, N., Magnoux, E., ... & Lopez?Vaamonde, C. (2009). Mitochondrial and microsatellite DNA markers reveal a Balkan origin for the highly invasive horse-chestnut leaf miner Cameraria ohridella (Lepidoptera, Gracillariidae). Molecular Ecology, 18(16), 3458-3470. https://doi.org/10.1111/j.1365-294X.2009.04290.x
[23.] Šefrová, H. & Lašt?vka, Z. (2001). Dispersal of the horse-chestnut leafminer Cameraria ohridella Deschka & Dimic 1986, in Europe: Its course, ways and causes (Lepidoptera?: Gracillariidae). Entomologische Zeitschrift Stuttgart, 111, 194-198.
[24.] Hellrigl, K. (2001). Neue Erkenntnisse und Untersuchungen über die Roßkastanien-Miniermotte Cameraria ohridella Deschka & Dimic, 1986 (Lepidoptera, Gracillariidae). Gredleriana, 1(2001), 9-81. https://www.zobodat.at/stable/pdf/Gredleriana_001_0009-0082.pdf
[25.] Pschorn-Walcher, H. (1994). Freiland-Biologie der eingeschleppten Roßkastanien- Miniermotte Cameraria ohridella DESCHKA et DIMIC (Lep ., Gracillariidae) im Wienerwald. Linzer Biologische Beiträge, 26, 633-642. http://www.zobodat.at/pdf/LBB_0026_2_0633-0642.pdf
[26.] Samek, T. (2003). Diapause of Cameraria ohridella Deschka et Dimic and its impact on the species population dynamics. Journal of Forest Science, 49, 252-258. https://81.0.228.28/publicFiles/55742.pdf
[27.] Pretzsch, H., Biber, P., Uhl, E., Dahlhausen, J., Schütze, G., Perkins, D., ... & Chavanne, A. (2017). Climate change accelerates growth of urban trees in metropolises worldwide. Scientific Reports, 7(1), 15403. https://www.nature.com/articles/s41598-017-14831-w
[28.] Vollsnes, A. V., Eriksen, A. B., Otterholt, E., Kvaal, K., Oxaal, U., & Futsaether, C. M. (2009). Visible foliar injury and infrared imaging show that daylength affects short-term recovery after ozone stress in Trifolium subterraneum. Journal of Experimental Botany, 60(13), 3677-86. https://doi.org/10.1093/jxb/erp213
[29.] Kwak, M. J., Lee, S. H., Khaine, I., Je, S. M., Lee, T. Y., You, H. N., ... & Woo, S. Y. (2017). Stomatal movements depend on interactions between external night light cue and internal signals activated by rhythmic starch turnover and abscisic acid (ABA) levels at dawn and dusk. Acta Physiologae Plantarum, 39(8), 162. https://link.springer.com/article/10.1007/s11738-017-2465-y
[30.] Vogel, G. (2017). Where have all the insects gone? Science, 356(6338), 576-579. http://science.sciencemag.org/content/356/6338/576.summary
[31.] Hallmann, C. A., Sorg, M., Jongejans, E., Siepel, H., Hofland, N., Schwan, H., ... & Goulson, D. (2017). More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS One, 12(10), e0185809. https://doi.org/10.1371/journal.pone.0185809
[32.] Grubisic, M., van Grunsven, R. H. A., Kyba, C. C. M., Manfrin, A. & Hölker, F. (2018). Insect declines and agroecosystems: does light pollution matter? Annals of Applied Biology, 173(2), 180-189. https://doi.org/10.1111/aab.12440
[33.] van Langevelde, F., Braamburg?Annegarn, M., Huigens, M. E., Groendijk, R., Poitevin, O., van Deijk, J. R., ... & Franzén, M. (2018). Declines in moth populations stress the need for conserving dark nights. Global Change Biology, 24(3), 925-932. https://doi.org/10.1111/gcb.14008
[34.] Augustin, S., Guichard, S., Heitland, W., Freise, J., Svatoš, A., & Gilbert, M. (2009). Monitoring and dispersal of the invading Gracillariidae Cameraria ohridella. Journal of Applied Entomology, 133(1), 58-66. https://doi.org/10.1111/j.1439-0418.2008.01333.x
[35.] Kuechly, H. U., Kyba, C. C., Ruhtz, T., Lindemann, C., Wolter, C., Fischer, J., & Hölker, F. (2012). Arial survey and spatial analysis of sources of light pollution in Berlin, Germany. Remote Sensing of Environment, 126, 39-50. https://doi.org/10.1016/j.rse.2012.08.008
[36.] Davies, T. W., Bennie, J., & Gaston, K. J. (2012). Street lighting changes the composition of invertebrate communities. Biology letters, 8, 764-767, rsbl20120216. http://rsbl.royalsocietypublishing.org/content/early/2012/05/15/rsbl.2012.0216.short
[37.] Manfrin, A., Singer, G., Larsen, S., Weiß, N., van Grunsven, R. H., et al. (2017). Artificial light at night affects organism flux across ecosystem boundaries and drives community structure in the recipient ecosystem. Frontiers in Environmental Science, 5, 61. https://doi.org/10.3389/fenvs.2017.00061
[38.] Girardoz, S., Quicke, D. L. J. & Kenis, M. (2007). Factors favouring the development and maintenance of outbreaks in an invasive leaf miner Cameraria ohridella (Lepidoptera: Gracillariidae): A life table study. Agricultureal and Forest Entomology, 9(2), 141-158. https://doi.org/10.1111/j.1461-9563.2007.00327.x
[39.] Balder, H. & Jäckel, B. (2003). Die Kastanienminiermotte und mögliche Gegenmassnahmen. Stadt Grün, 5, 44-49.
[40.] Hogewoning, S. W., Trouwborst, G., Maljaars, H., Poorter, H., van Ieperen, W., & Harbinson, J. (2010). Blue light dose-responses of leaf photosynthesis, morphology, and chemical composition of Cucumis sativus grown under different combinations of red and blue light. Journal of Experimental Botany, 61(11), 3107-3117. https://doi.org/10.1093/jxb/erq132
[41.] Longcore, T., Rodríguez, A., Witherington, B., Penniman, J. F., Herf, L., & Herf, M. (2018). Rapid assessment of lamp spectrum to quantify ecological effects of light at night. Journal of Experimental Zoology Part A: Ecological and Integrative Physiology. 1-11. https://doi.org/10.1002/jez.2184
[42.] van Langevelde, F., Ettema, J. A., Donners, M., WallisDeVries, M. F. & Groenendijk, D. (2011). Effect of spectral composition of artificial light on the attraction of moths. Biological Conservation 144(9), 2274-2281. https://doi.org/10.1016/j.biocon.2011.06.004
[43.] Schroer, S. & Hölker, F. (2017) Light pollution reduction. Handbook of Advanced Lighting Technology (eds. Karlicek, R., Sun, C.-C., Zissis, G. & Ma, R.) Springer, Cham, 991-1010. https://link.springer.com/referenceworkentry/10.1007%2F978-3-319-00295-8_43-1
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