Skip to main content
Log in

Light at night disrupts trophic interactions and population growth of lady beetles and pea aphids

  • Highlighted Student Research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Natural variation in light has historically correlated with seasonality, providing an honest cue to organisms with seasonal life history cycles. However, with the onset of widespread light at night (LAN), the reliability of light as a cue has decreased in polluted areas, making its timing or intensity potentially clash with temperature trends. These clashing cues may influence biological systems on multiple levels. Yet, a few studies have connected behavioral underpinnings and larger community-level processes, resulting in a knowledge gap bridging individual-, population-, and community-level responses to mismatched cues. We experimentally investigated impacts of cool temperature and LAN on a lady beetle–aphid–fava system to test how light and temperature influenced aphid population growth and their underlying behavioral drivers. We used Coccinella septempunctata and Coleomegilla maculata beetles to understand the interaction of the environment and predation on pea aphid (Acyrthosiphon pisum) population growth. Aphids and their predators reacted differently to variation in light and temperature, influencing the strength of aphid-driven and predator-driven dynamics in the different conditions. We observed evidence of aphid-driven dynamics in the cool, light conditions where aphids excel and exhibited strong anti-predator behavior. In contrast, we found stronger predator-driven dynamics in warm conditions where lady beetle predatory success was higher. Overall, we found that LAN has context-dependent effects on insect communities due to the varied responses each player has to its environment.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Availability of data and code

Data and code from the study are available on GitHub: https://github.com/ccm246/aphid_lb_community.

References

  • Agabiti B, Wassenaar RJ, Winder L (2016) Dropping behaviour of pea aphid nymphs increases their development time and reduces their reproductive capacity as adults. PeerJ 4:e2236

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Bennie J, Davies TW, Cruse D, Inger R, Gaston KJ (2015) Cascading effects of artificial light at night: resource-mediated control of herbivores in a grassland ecosystem. Philos Trans R Soc B Biol Sci 370:20140131

    Article  Google Scholar 

  • Bolton D, Mayer-Pinnto M, Clark GF, Dafforn KA, Brassil WA, Becker A, Johnston EL (2017) Coastal urban lighting has ecological consequences for multiple trophic levels under the sea. Sci Total Environ 576:1–9

    Article  CAS  Google Scholar 

  • Boyes DH, Evans DM, Fox R, Parsons MS, Pocock MJO (2020) Is light pollution driving moth population declines? A review of causal mechanisms across the life cycle. Insect Conserv Divers 14(2):167–187

    Article  Google Scholar 

  • Bradshaw WE, Holzapfel CM (2009) Light, time, and the physiology of biotic response to rapid climate change in animals. Annu Rev Physiol 72:147–166

    Article  Google Scholar 

  • Clegg JM, Barlow CA (1982) Escape behaviour of the pea aphid Acyrthosiphon pisum (Harris) in response to alarm pheromone and vibration. Can J Zool 60:2245–2252

    Article  Google Scholar 

  • Davies TW, Bennie J, Inger R, Gaston KJ (2013) Artificial light alters natural regimes of night-time sky brightness. Sci Rep 3:1722

    Article  CAS  Google Scholar 

  • Davies TW, Bennie J, Cruse D, Blumgart D, Inger R, Gaston KJ (2017) Multiple night-time light-emitting diode lighting strategies impact grassland invertebrate assemblages. Glob Change Biol 23:2641–2648

    Article  Google Scholar 

  • Denno RF, Dingle H (1981) Insect life history patterns: habitat and geographic variation. Springer, New York

    Book  Google Scholar 

  • Desouhant E, Gomes E, Mondy N, Amat I (2019) Mechanistic, ecological, and evolutionary consequences of artificial light at night for insects: review and prospective. Entomol Exp Appl 167(1):37–58

    Article  Google Scholar 

  • Dominoni DM (2015) The effects of light pollution on biological rhythms of birds: an integrated, mechanistic perspective. J Ornithol 156(S1):409–418

    Article  Google Scholar 

  • Dominoni DM, Goymann W, Helm B, Partecke J (2013) Urban-like night illumination reduces melatonin release in European blackbirds (Turdus merula): implications of city life for biological time-keeping of songbirds. Front Zool 10(60):1–10

    Google Scholar 

  • Fonken LK, Workman JL, Walton JC, Weil ZM, Morris JS, Haim A, Nelson RJ (2010) Light at nightincreases body mass by shifting the time of food intake. Proc Natl Acad Sci USA 107(43):1008734107

    Article  Google Scholar 

  • Gaston KJ, Bennie J, Davies TW, Hopkins J (2013) The ecological impacts of night-time light pollution: a mechanistic appraisal. Biol Rev 88:912–917

    Article  Google Scholar 

  • Gaston KJ, Duffy JP, Gaston S, Bennie J, Davies TW (2014) Human alteration of natural light cycles: causes and ecological consequences. Oecologia 176:917–931

    Article  Google Scholar 

  • Gaston K, Ackermann S, Bennie J, Cox DTC, Phillips BB, de Miguel AS, Sanders D (2021) Pervasiveness of biological impacts of artificial light at night. Integr Comp Biol 61(3):1098–1110

    Article  Google Scholar 

  • Grenis K, Murphy SM (2019) Direct and indirect effects of light pollution on the performance of an herbivorous insect. Insect Sci 26:770–776

    Article  Google Scholar 

  • Grubisic M, van Grunsven RHA (2021) Artifical light at night disrupts species interactions and changes insect communities. Curr Opin Insect Sci 47:136–141

    Article  Google Scholar 

  • Grubisic M, van Grunsven RHA, Kyba CCM, Manfrin A, Hölker F (2018) Insect declines and agroecosystems: does light pollution matter? Ann Appl Biol 173(2):180–189

    Article  Google Scholar 

  • Grubisic M, Haim A, Bhusal P, Dominoni DM, Gabriel KMA, Jechow A, Kupprat F, Lerner A, Marchant P, Riley W, Stebelova K, van Grunscen RHA, Zeman M, Zubidat AE, Hölker F (2019) Light pollution, circadian photoreception, and melatonin in vertebrates. Sustainability 11:6400

    Article  CAS  Google Scholar 

  • Hagen KS (1962) Biology and ecology of predaceous coccinellidae. Annu Rev Entomol 7:289–326

    Article  Google Scholar 

  • Kehoe R, Sanders D, Cruse D, Silk M, Gaston KJ, Bridle JR, van Veen F (2020) Longer photoperiods through range shifts and artificial light lead to a destabilizing increase in host-parasitoid interaction strengths. J Anim Ecol 89(11):2508–2516

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Lavy O, Sher N, Malik A, Chiel E (2015) Do Bacterial symbionts Govern aphid’s dropping behavior? Environ Entomol 44:588–592

    Article  CAS  Google Scholar 

  • Lenth R, Singmann H, Love J, Buerkner P, Herve M (2020) emmeans: estimated marginal means, aka least-squares means. R package version 1.4.5

  • McMahon TA, Rohr JR, Bernal XE (2017) Light and noise pollution interact to disrupt interspecific interactions. Ecology 98(5):1290–1299

    Article  Google Scholar 

  • Mellanby K (1935) Low temperature and insect activity. Proc R Soc B 127:473–487

    Google Scholar 

  • Miller CR, Barton BT, Zhu L, Radeloff VC, Oliver KM, Harmon JP, Ives AR (2017) Combined effects of night warming and light pollution on predator–prey interactions. Proc R Soc B 284:20171195

    Article  Google Scholar 

  • Navara KJ, Nelson RJ (2007) The dark side of light at night: physiological, epidemiological, and ecological consequences. J Pineal Res 43:215–224

    Article  CAS  Google Scholar 

  • Ouyang JQ, de Jong M, van Grunsven RHA, Matson KD, Haussmann MF, Meerlo P, Visser ME, Spoelstra K (2017) Restless roosts: light pollution affects behavior, sleep, and physiology in a free-living songbird. Glob Change Biol 23:4987–4994

    Article  Google Scholar 

  • Owens ACS, Lewis SM (2018) The impact of artificial light at night on nocturnal insects: a review and synthesis. Ecol Evol 8(22):11337–11358

    Article  Google Scholar 

  • Perkin EK, Hölker F, Richardson JS, Sadler JP, Wolter C, Tockner K (2011) The influence of artificial light on stream and riparian ecosystems: questions, challenges, and perspectives. Ecosphere 2(11):1–16

    Article  Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  • Sanders D, Frago E, Kehoe R, Patterson C, Gaston KJ (2021) A meta-analysis of biological impacts of artificial light at night. Nat Ecol Evol 5(1):74–81

    Article  Google Scholar 

  • Shipley JR, Twining CW, Taff CC, Vitousek MN, Flack A, Winkler DW (2020) Birds advancing lay dates with warming springs face greater risk of chick mortality. Proc Natl Acad Sci 117:25590–25594

    Article  CAS  Google Scholar 

  • Swaddle JP, Francis CD, Barber JR, Cooper CB, Kyba CCM, Dominoni DM, Shannon G, Ashehoug E, Goodwin SE, Kawahara AY, Luther D, Spoelstra K, Voss M, Longcore T (2015) A framework to assess evolutionary responses to anthropogenic light and sound. Trends Ecol Evol 30(9):550–560

    Article  Google Scholar 

  • Taylor LR (1963) Analysis of the effect of temperature on insects in flight. J Anim Ecol 32:99–117

    Article  Google Scholar 

  • Tomioka K, Matsumoto A (2010) A comparative view of insect circadian clock systems. Cell Mol Life Sci 67:1397–1406

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to T. Ugine and J. Losey for space support and to A. Injaian, K. Sparks, J. Peters, and N. van Eck for technical assistance as well as the Sparks and Powers Labs for space. We are also grateful to the Guterman Bioclimatic Laboratory for space. We appreciate the husbandry assistance of T. Ugine, J. Davis, J. Houtz, T. Ryan, and J. Uehling. We thank J. Davis, Z. Getman-Pickering, S. Kariuki, and T. Lambert for manuscript feedback. We thank J. Houtz and M. Barkdull for figure assistance. We are grateful for the Cornell Statistical Consulting Unit’s assistance with statistics. We appreciate the contribution of C. septempunctata adults by Y. Yang and C. maculata eggs from E. Riddick.

Funding

Funding from Cornell University to MNV.

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to study conception and design. CRM and JST composed methods; CRM executed rearing, experiments, and analysis. CRM drafted the manuscript, and JST and MNV provided feedback.

Corresponding author

Correspondence to Colleen R. Miller.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethics approval

All experiments were conducted within institutional guidelines.

Additional information

Communicated by Sylvain Pincebourde.

Our research discovered that predator–prey interactions are context-dependent, and that novel circumstances, such as light at night, may lead to prey-driven patterns.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Miller, C.R., Vitousek, M.N. & Thaler, J.S. Light at night disrupts trophic interactions and population growth of lady beetles and pea aphids. Oecologia 199, 527–535 (2022). https://doi.org/10.1007/s00442-022-05146-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-022-05146-3

Keywords

Navigation