Cascading effects of artificial light at night: Resource-mediated control of herbivores in a grassland ecosystem

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 370, Issue 1667, 2015, Pages

  Bennie, Jonathan ^a   Davies, Thomas W ^a   Cruse, David ^a   Inger, Richard ^a   Gaston, Kevin J ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

Artificial light at night; Biotic interactions; Bottom up effects; Community level; Light pollution; Photopollution

Indexed keywords

BOTTOM-UP APPROACH; COMPETITION (ECOLOGY); GRASSLAND; HERBIVORE; LIGHT EFFECT; LIGHT POLLUTION; PLANT COMMUNITY; PLANT-HERBIVORE INTERACTION; POLLINATION; SEED DISPERSAL; TOP-DOWN CONTROL;

ACYRTHOSIPHON PISUM; ANIMALIA;

ANIMAL; APHID; BEETLE; CIRCADIAN RHYTHM; COLOR; ENVIRONMENTAL MONITORING; FOOD CHAIN; GRASSLAND; HERBIVORY; ILLUMINATION; LOTUS (GENUS); PHYSIOLOGY; POLLUTION; RADIATION RESPONSE; SEA;

ANIMALS; APHIDS; BEETLES; CIRCADIAN RHYTHM; COLOR; ENVIRONMENTAL MONITORING; ENVIRONMENTAL POLLUTION; FOOD CHAIN; GRASSLAND; HERBIVORY; LIGHTING; LOTEAE; OCEANS AND SEAS;

EID: 84924859660     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2014.0131     Document Type: Article

References (87)

1. Longcore T, Rich C. 2004 Ecological light pollution. Front. Ecol. Environ. 2, 191–198. (doi:10.1890/1540-9295(2004)002[0191:ELP]2.0.CO;2).
2. Gaston KJ, Bennie J, Davies TW, Hopkins J. 2013 The ecological impacts of nighttime light pollution: a mechanistic appraisal. Biol. Rev. 88, 912–927. (doi:10.1111/brv.12036).
3. Davies TW, Duffy JP, Bennie J, Gaston KJ. 2014 The nature, extent and ecological implications of marine light pollution. Front. Ecol. Env. 12, 347–355. (doi:10.1890/130281).
4. Gaston KJ, Bennie J. 2014 Demographic effects of artificial nighttime lighting on animal populations. Environ. Rev. 22, 1–8. (doi:10.1139/er-2014-0041).
5. Davies TW, Bennie J, Gaston KJ. 2012 Street lighting changes the composition of invertebrate communities. Biol. Lett. 8, 764–767. (doi:10.1098/rsbl.2012.0216).
6. Lewansik D, Voigt CC. 2014 Artificial light puts ecosystem services of frugivorous bats at risk. J. Appl. Ecol. 52, 388–394. (doi:10.1111/1365-2664.12206).
7. Meyer LA, Sullivan SMP. 2013 Bright lights, big city: influences of ecological light pollution on reciprocal stream-riparian invertebrate fluxes. Ecol. Appl. 23, 1322–1330. (doi:10.1890/12-2007.1).
8. Van der Putten WH, Ruiter PC, Bezemer TM, Harvey JA, Wassen M, Wolters V. 2004 Trophic interactions in a changing world. Basic Appl. Ecol. 5, 487–494. (doi:10.1016/j.baae.2004.09.003).
9. Estes JA, Tinker MT, Williams TM, Doak DF. 1998 Killer whale predation on sea otters linking oceanic and nearshore ecosystems. Science 282, 473–476. (doi:10.1126/science.282.5388.473).
10. Byrnes J, Stachowicz JJ, Hultgren KM, Hughes AR, Olyarnik SV, Thornber CS. 2006 Predator diversity strengthens trophic cascades in kelp forests by modifying herbivore behaviour. Ecol. Lett. 9, 61–71. (doi:10.1111/j.1461-0248.2005.00842.x).
11. Otto SB, Berlow EL, Rank NE, Smiley J, Brose U. 2008 Predator diversity and identity drive interaction strength and trophic cascades in a food web. Ecology 89, 134–144. (doi:10.1890/07-0066.1).
12. Baum JK, Worm B. 2009 Cascading top-down effects of changing oceanic predator abundances. J. Anim. Ecol. 78, 699–714. (doi:10.1111/j.1365-2656.2009.01531.x).
13. Ripple WJ, Beschta RL. 2012 Trophic cascades in Yellowstone: the first 15 years after wolf reintroduction. Biol. Conserv. 145, 205–213. (doi:10.1016/j.biocon.2011.11.005).
14. Hairston NG, Smith FE, Slobodkin LB. 1960 Community structure, population control, and competition. Am. Nat. 94, 421–425. (doi:10.1086/282146).
15. Schmitz OJ. 2003 Top predator control of plant biodiversity and productivity in an old-field ecosystem. Ecol. Lett. 6, 156–163. (doi:10.1046/j.1461-0248.2003.00412.x).
16. Rzanny M, Kuu A, Voigt W. 2013 Bottom-up and top-down forces structuring consumer communities in an experimental grassland. Oikos 122, 967–976. (doi:10.1111/j.1600-0706.2012.00114.x).
17. Biesmeijer JC et al. 2006 Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313, 351–354. (doi:10.1126/science.1127863).
18. Francis CD, Kleist NJ, Ortega CP, Cruz A. 2012 Noise pollution alters ecological services: enhanced pollination and disrupted seed dispersal. Proc. R. Soc. B 279, 2727–2735. (doi:10.1098/rspb.2012.0230).
19. Denno RF, McClure MS, Ott JR. 1995 Interspecific interactions in phytophagous insects: competition revisited and resurrected. Annu. Rev. Entomol. 40, 297–331. (doi:10.1146/annurev.en.40.010195.001501).
20. Moran MD, Scheidler AR. 2002 Effects of nutrients and predators on an old-field food-chain: interactions of top-down and bottom-up processes. Oikos 98, 116–124. (doi:10.1034/j.1600-0706.2002.980112.x).
21. Boyer AG, Swearingen RE, Blaha MA, Fortson CT, Gremillion SKG, Osborn KA, Moran MD. 2003 Seasonal variation in top-down and bottom-up processes in a grassland arthropod community. Oecologia 136, 309–316. (doi:10.1007/s00442-003-1272-x).
22. Wardle DA, Barker GM. 1997 Competition and herbivory in establishing grassland communities: implications for plant biomass, species diversity and soil microbial activity. Oikos 80, 470–480. (doi:10.2307/3546620).
23. Power M. 1992 Top-down and bottom-up forces in food webs: do plants have primacy? Ecology 73, 733–746. (doi:10.2307/1940153).
24. Gripenberg S, Roslin T. 2007 Up or down in space? Uniting the bottom-up versus top-down paradigm and spatial ecology. Oikos 116, 181–188. (doi:10.1111/j.0030-1299.2007.15266.x).
25. Zhang Y, Adams J. 2011 Top-down control of herbivores varies with ecosystem types. J. Ecol. 99, 370–372.
26. Schmitz OJ, Beckerman AP, O’Brien KM. 1997 Behaviourally mediated trophic cascades: effects of predation risk on food web interactions. Ecology 78, 1388–1399. (doi:10.1890/0012-9658(1997)078[1388:BMTCEO]2.0.CO;2).
27. Sarfraz RM, Dosdall LM, Keddie AB. 2009 Bottomup effects of host plant nutritional quality on Plutella xylostella (Lepidoptera: Plutellidae) and top-down effects of herbivore attack on plant compensatory ability. Eur. J. Entomol. 106, 583–594. (doi:10.14411/eje.2009.073).
28. Schereber C et al. 2010 Bottom-up effects of plant diversity on multitrophic interactions in a biodiversity experiment. Nature 468, 553–556. (doi:10.1038/nature09492).
29. Schaffers AP, Raemakers IP, Sykora KV, ter Braak CLF. 2008 Arthropod assemblages are best predicted by plant species composition. Ecology 89, 782–794. (doi:10.1890/07-0361.1).
30. Koricheva J, Mulder CPH, Schmid B, Joshi J, Huss-Danell K. 2000 Numerical responses of different trophic groups of invertebrates to manipulations of plant diversity in grasslands. Oecologia 125, 271–282. (doi:10.1007/s004420000450).
31. Folkard NFG, Smith JNM. 1995 Evidence for bottomup effects in the boreal forest: do passerine birds respond to large-scale experimental fertilization? Can. J. Zool. 73, 2231–2237. (doi:10.1139/z95-264).
32. Hoekman D. 2010 Turning up the heat: temperature influences the relative importance of top-down and bottom-up effects. Ecology 91, 2819–2825. (doi:10.1890/10-0260.1).
33. Van der Putten W, Macel M, Visser ME. 2010 Predicting species distribution and abundance responses to climate change: why it is essential to include biotic interactions across trophic levels. Phil. Trans. R. Soc. B 365, 2025–2034. (doi:10.1098/rstb.2010.0037).
34. Vermeulen HJW. 1994 Corridor function of a road verge for dispersal of stenotopic heathland ground beetles Carabidae. Biol. Conserv. 69, 339–349. (doi:10.1016/0006-3207(94)90433-2).
35. Meunier FD, Verheyden C, Jouventin P. 2000 Use of roadsides by diurnal raptors in agricultural landscapes. Biol. Conserv. 93, 291–298. (doi:10.1016/S0006-3207(99)00094-4).
36. Hopwood JL. 2008 The contribution of roadside grassland restorations to native bee conservation. Biol. Conserv. 141, 2632–2640. (doi:10.1016/j.biocon.2008.07.026).
37. Cousins SAO. 2006 Plant species richness in midfield islets and road verges—the effect of landscape fragmentation. Biol. Conserv. 127, 500–509. (doi:10.1016/j.biocon.2005.09.009).
38. Spellerberg IF. 1998 Ecological effects of roads and traffic: a literature review. Glob. Ecol. Biogeogr. Lett. 7, 317–333. (doi:10.2307/2997681).
39. Moran MD, Rooney TP, Hurd LE. 1996 Top-down cascade from a bitrophic predator in an old-field community. Ecology 77, 2219–2227. (doi:10.2307/2265715).
40. Halaj J, Wise DH. 2001 Terrestrial trophic cascades: how much do they trickle? Am. Nat. 157, 262–281. (doi:10.1086/319190).
41. Myers RA, Baum JK, Shepherd TD, Powers SP, Peterson CH. 2007 Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315, 1846–1850. (doi:10.1126/science.1138657).
42. Schmitz OJ. 2009 Effects of predator functional diversity on grassland ecosystem function. Ecology 90, 2339–2345. (doi:10.1890/08-1919.1).
43. Wolff RJ. 1982 Nocturnal activity under artificial lights by the jumping spider Sitticus faciger. Peckhamia 2, 32.
44. Frank KD. 2006 Effects of artificial night lighting on moths. In Ecological consequences of artificial night lighting (eds C Rich, T Longcore), pp. 305–344. Washington, DC: Island Press.
45. Polak T, Korine C, Yair S, Holderied MW. 2011 Differential effects of artificial lighting on flight and foraging behaviour of two sympatric bat species in a desert. J. Zool. 285, 21–27. (doi:10.1111/j.1469-7998.2011.00808.x).
46. Garber SD. 1978 Opportunistic feeding behaviour of Anolis cristatellus (Iguanidae: Reptilia) in Puerto Rico. Trans. Kansas Acad. Sci. 81, 19–80. (doi:10.2307/3627360).
47. Negro JJ, Bustamante J, Melguizo C, Ruiz JL, Grande JM. 2000 Nocturnal activity of lesser kestrels under artificial lighting conditions in Seville, Spain. J. Raptor Res. 34, 327–329.
48. Dwyer RG, Bearhop S, Campbell HA, Bryant DM. 2012 Shedding light on light: benefits of anthropogenic illumination to a nocturnally foraging shorebird. J. Anim. Ecol. 82, 478–485. (doi:10.1111/1365-2656.12012).
49. Santos CD, Miranda AC, Granadeiro JP, Lourenco PM, Saraiva S, Palmeirim JM. 2010 Effects of artificial illumination on the nocturnal foraging of waders. Acta Oecol. 36, 166–172. (doi:10.1016/j.actao.2009.11.008).
50. Dice LD. 1945 Minimum intensities of illumination under which owls can find dead prey by sight. Am. Nat. 79, 385–416. (doi:10.1086/281276).
51. Larsen LO, Pedersen JN. 1982 The snapping response of the toad Bufo bufo towards prey dummies at very low light intensities. Amphibia-Reptilia 2, 321–327. (doi:10.1163/156853882X00248).
52. Kotler BP. 1984 Effects of illumination on the rate of resource harvesting in a community of desert rodents. Am. Midl. Nat. 111, 383–389. (doi:10.2307/2425333).
53. Cathay AR, Campbell LE. 1975 Effectiveness of five vision-lighting sources on photo-regulation of 22 species of ornamental plants. J. Am. Soc. Hort. Sci. 100, 65–71.
54. Briggs WR. 2006 Physiology of plant responses to artificial lighting. In Ecological consequences of artificial night lighting (eds C Rich, T Longcore), pp. 281–304. Washington, DC: Island Press.
55. Smith H. 1995 Physiological and ecological function within the phytochrome family. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46, 289–315. (doi:10.1146/annurev.pp.46.060195.001445).
56. Weller JL, Reid JB, Taylor SA, Murfet IC. 1997 The genetic control of flowering in pea. Trends Plant Sci. 2, 412–418. (doi:10.1016/S1360-1385(97) 85580-X).
57. Franklin KA, Whitelam GC. 2005 Phytochromes and shade-avoidance responses in plants. Ann. Bot. 96, 169–175. (doi:10.1093/aob/mci165).
58. Takeda F, Glenn DM, Stutte GW. 2008 Red light affects flowering under long days in a short-day strawberry cultivar. HortScience 43, 2245–2247.
59. Ito A, Saito T, Nishijima T, Moriguchi T. 2014 Effect of extending the photoperiod with lowintensity red or far-red light on the timing of shoot elongation and flower-bud formation of 1-year-old Japanese pear (Pyrus pyrifolia). Tree Physiol. 34, 534–546. (doi:10.1093/treephys/tpu033).
60. Matzke EB. 1936 The effect of street lights in delaying leaf-fall in certain trees. Am. J. Bot. 23, 446–452. (doi:10.2307/2436035).
61. Sinnadurai S. 1981 High pressure sodium lights affect crops in Ghana. World Crops 33, 120–122.
62. Gruner DS. 2004 Attenuation of top-down and bottom-up forces in a complex terrestrial community. Ecology 85, 3010–3022. (doi:10.1890/04-0020).
63. Schuldt A, Baruffol M, Bruelheide H, Chen S, Chi X, Wall M, Assman T. 2014 Woody plant phylogenetic diversity mediates bottom-up control of arthropod biomass in species-rich forests. Oecologia 176, 171–182. (doi:10.1007/s00442-014-3006-7).
64. Haddad NM, Tilman D, Haarstad J, Ritche M, Knops JMH. 2001 Contrasting effects of plant diversity and composition on insect communities: a field experiment. Am. Nat. 158, 17–35. (doi:10.1086/320866).
65. Frank KD. 1988 Impact of outdoor lighting on moths: an assessment. J. Lepid. Soc. 42, 63–93.
66. Eisenbeis G, Hassel F. 2000 Zur Anziehung nachtaktiver Insekten durch Strabenlaternen: eine Studie kommunaler Beleuchtungseinrichtungen in der Agrarlandschaft Rheinhessens [Attraction of nocturnal insects to street lights: a study of municipal lighting systems in a rural area of Rheinhessen (Germany)]. Nat. Landschaft 75, 145–156.
67. Eisenbeis G. 2006 Artificial night lighting and insects: attraction of insects to streetlamps in a rural setting in Germany. In Ecological consequences of artificial night lighting (eds C Rich, T Longcore), pp. 281–304. Washington, DC: Island Press.
68. van Langevelde F, Ettema JA, Donners M, WallisDeVries MF, Groenendijk D. 2011 Effect of spectral composition of artificial light on the attraction of moths. Biol. Conserv. 144, 2274–2281. (doi:10.1016/j.biocon.2011.06.004).
69. Somers-Yeates R, Hodgson D, McGregor PK, Spalding A. 2013 Shedding light on moths: shorter wavelengths attract noctuids more than geometrids. Biol. Lett. 9, 20130376. (doi:10.1098/rsbl.2013.0376).
70. Rydell J. 1991 Seasonal use of illuminated areas by foraging northern bats Eptesicus nilssoni. Holarctic Ecol. 14, 203–207.
71. Rydell J. 1992 Exploitation of insects around streetlamps by bats in Sweden. Funct. Ecol. 6, 744–750. (doi:10.2307/2389972).
72. Blake D, Racey PA, Rydell J, Speakman JR. 1994 Use of lamplit roads by foraging bats in southern England. J. Zool. 234, 453–462. (doi:10.1111/j.1469-7998.1994.tb04859.x).
73. Stone EL, Jones G, Harris S. 2009 Street lighting disturbs commuting bats. Curr. Biol. 19, 1123–1127. (doi:10.1016/j.cub.2009.05.058).
74. Jung K, Kalko EKV. 2010 Where forest meets urbanization: foraging plasticity of aerial insectivorous bats in an anthropogenically altered environment. J. Mammal. 91, 144–153. (doi:10.1644/08-MAMM-A-313R.1.).
75. Martinell MC, Dotterl S, Blanche C, Rovira A, Masso S, Bosch M. 2010 Nocturnal pollination of the endemic Silene sennesii (Caryophyllaceae): an endangered mutualism? Plant Ecol. Evol. 143, 203–208. (doi:10.1007/s11258-010-9785-y).
76. Kronfeld-Schor N, Dayan T. 2003 Partitioning of time as an ecological resource. Annu. Rev. Ecol. Evol. Syst. 34, 153–181. (doi:10.1146/annurev.ecolsys.34.011802.132435).
77. Gerrish GA, Morin JG, Rivers TJ, Patrawala Z. 2009 Darkness as an ecological resource: the role of light in partitioning the nocturnal niche. Oecologia 160, 525–536. (doi:10.1007/s00442-009-1327-8).
78. Forde DJ, Thomas RG. 1966 Flowering in Lotus pedunculatus cav. NZ J. Bot. 4, 147–152. (doi:10.1080/0028825X.1966.10429036).
79. Omkar, Pervez A. 2005 Ecology of two-spotted ladybird Adalia punctata: a review. J. Appl. Entomol. 129, 465–474. (doi:10.1111/j.1439-0418.2005.00998.x).
80. Allema AB, Rossing WAH, van der Werf W, Heusinkveld BG, Bukovinszky T, Steingrover E, van Lenteren JC. 2012 Effect of light quality on movement of Pterostichus melanarius (Coleoptera: Carabidae). J. Appl. Entomol. 136, 793–800. (doi:10.1111/j.1439-0418.2012.01728.x).
81. Omkar Pathak S. 2006 Effects of different photoperiods and wavelengths of light on the lifehistory traits of an aphidophagous ladybird, Coelophora saucia (Mulsant). J. Appl. Entomol. 130, 45–50. (doi:10.1111/j.1439-0418.2005.01016.x).
82. Erlykova N. 2003 Inter- and intraclonal variability in the photoperiodic response and fecundity in the pea aphid Acyrthosiphon pisum (Hemiptera: Aphididae). Eur. J. Entomol. 100, 31–37. (doi:10.14411/eje.2003.006).
83. Pawson SM, Bader MKF. 2014 LED lighting increases the ecological impact of light pollution irrespective of color temperature. Ecol. Appl. 24, 1561–1568. (doi:10.1890/14-0468.1).
84. Gaston KJ, Davies TW, Bennie J, Hopkins J. 2012 Reducing the ecological consequences of night-time light pollution: options and developments. J. Appl. Ecol. 49 1256–1266. (doi:10.1111/j.1365-2664.2012.02212.x).
85. European Committee for Standardization. 2014 Road lighting—part 1: selection of lighting classes. Technical Report CEN/TR 13201–1. CEN, Brussels, Belgium.
86. Skaug H, Fournier D, Bolker B, Magnusson A, Nielsen A. 2014 Generalized Linear Mixed Models using AD Model Builder. R package v. 0.8.0. See http://r-forge.r-project.org/projects/glmmadmb/.
87. Thapan K, Arendt J, Skene DJ. 2001 An action spectrum for melatonin suppression: evidence for a novel non-rod, non-cone photoreceptor system in humans. J. Physiol. 535, 261–267. (doi:10.1111/j.1469-7793.2001.t01-1-00261.x).