Lunar illumination shapes small mammal activity in lowland agricultural landscapes

Main Article Content

Carl Soulsbury

Abstract

The behavioural patterns of small mammalian prey species have been shown to be widely impacted by predator avoidance. Cues to avoid predation may come from the predator itself or environmental cues, such as moonlight and available vegetative cover. We investigated how the activity of the bank vole Myodes glareolus, field vole Microtus agrestis, wood mouse Apodemus sylvaticus and the common shrew Sorex araneus were impacted by changes in habitat and lunar light conditions across a range of habitats (mainly grassland protected sites) in Lincolnshire (UK). Microhabitat vegetation density as well as weather conditions were recorded across all trap sites, with Longworth traps set overnight and the successfully captured species recorded the following morning. Overnight temperature was found to positively influence capture rate across all species. The lunar phase was found to significantly impact capture rate, with the gibbous lunar phase providing the highest capture rate across species. The interaction between illumination and vegetation density was also found to impact activity levels in the bank vole and wood mouse, with the bank vole showing higher activity in thick vegetation at low light levels and across habitats at higher light levels, whereas wood mice were more often captured in intermediate cover at low and intermediate illumination but across a range of habitats at brighter illumination. In combination, it suggests that small mammal activity is altered to potentially reduce predation risk. However, in this community at least, brighter lunar illumination leads to increase activity.  

Article Details

How to Cite
Soulsbury, C. (2021). Lunar illumination shapes small mammal activity in lowland agricultural landscapes. European Journal of Ecology, 7(1). https://doi.org/10.17161/eurojecol.v7i1.14753
Section
Articles

References

Bates, D., Maechler, M., Bolker, B. & Walker, S. (2015) Fitting Linear Mixed-Effects Models Using lme4. J. Stat Soft. 67, 1-48.

Beier, P. (2006) Effects of artificial night lighting on terrestrial mammals. In: Ecological Consequences of Artificial Night Lighting. Washington, D.C.: Island Press., pp. 19–42.

Bowers, M.A. (1988) Seed removal experiments on Desert Rodents: The microhabitat by moonlight effect. J. Mammal. 69, 201-204. doi: 10.2307/1381778

Brown, L.E. (1956) Field experiments on the activity of small mammals, Apodemus, Clethrionomys and Microtus. Proc. Zool Soc. Lond. 126, 549-564. doi:10.1111/j.1096-3642.1956.tb00452.x

Caro, T. (2005) Antipredator Defenses in Birds and Mammals. Chicago, Illinois: University of Chicago Press. pp. 1-592.

Churchfield, S. (1982) The influence of temperature on the activity and food consumption of the common shrew. Acta Theriol. 27, 295-304.

Crowcroft, P. (1954) The daily cycle of activity in British shrews. Proc. Zool Soc. Lond. 123, 715-730. doi:/10.1111/j.1096-3642.1954.tb00197.x

Dell’Agnello, F., Martini, M., Mori, E., Mazza, G., Mazza, V. & Zaccaroni, M. (2020) Winter activity rhythms of a rodent pest species in agricultural habitats. Mamm. Res. 65, 69-74. doi:10.1007/s13364-019-00443-4

Díaz, M. (1992) Rodent seed predation in cereal crop areas of central Spain: effects of physiognomy, food availability, and predation risk. Ecog. 15, 77-85. doi:10.1111/j.1600-0587.1992.tb00011.x

Díaz, M., Torre, I., Peris, A. &Tena, L. (2005) Foraging behavior of wood mice as related to presence and activity of genets. J. Mammal. 86, 1178-1185. doi:10.1644/04-MAMM-A-127R1.1

Ferrari, M.C.O., Sih, A. & Chivers, D.P. (2009) The paradox of risk allocation: a review and prospectus. Anim. Behav. 78, 579–585. doi:10.1016/j.anbehav.2009.05.034

Griffin, P.C., Griffin, S.C., Waroquiers, C. & Mills, L.S. (2005) Mortality by moonlight: predation risk and the snowshoe hare. Behav. Ecol. 16, 938-944. doi:10.1093/beheco/ari074

Greenwood, P.J. (1978) Timing of activity of the bank vole Clethrionomys glareolus and the wood mouse Apodemus sylvaticus in a deciduous woodland. Oikos, 31, 123-127.

Halle, S. & Lehmann, U. (1992) Cycle-correlated changes in the activity behaviour of field voles, Microtus agrestis. Oikos. 64, 489-497. doi:10.2307/3543393

Jacob, S.A., Matter, S.F. & Cameron, G.N. (2017) Interactive effects of vegetation and illumination on foraging behavior of white-footed mice (Peromyscus leucopus). J. Mammal. 98, 804-814. doi:10.1093/jmammal/gyx012

Kaufman, D.W. & Kaufman, G.A. (1982) Effect of moonlight on activity and microhabitat use by Ord's kangaroo rat (Dipodomys ordit). J. Mammal. 63, 309-312. doi: 10.2307/1380644

Kuznetsova, A., Brockhoff, P.B. & Christensen, R.H.B. (2017) lmerTest Package: Tests in Linear Mixed Effects Models. J. Stat. Soft. 82, 1-26.

Lenth, R. (2020) emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.4.5. https://CRAN.R-project.org/package=emmeans

Lima, S. & Dill, L. (1990) Behavioural decisions made under the risk of predation: a review and prospectus. Can. J. Zool. 68, 619-640.

Lockard, R.B. & Owings, D.H. (1974) Seasonal variation in moonlight avoidance by bannertail kangaroo rats. J. Mammal. 55, 189-193. doi:10.1139/z90-092

Longland, W.S. & Price, M.V. (1991) Direct observations of Owls and Heteromyid Rodents: Can predation risk explain microhabitat use? Ecol. 72, 2261-2273. doi: 10.2307/1379266

Mazurkiewicz, M. (1994) Factors influencing the distribution of the bank vole in forest habitats. Acta Theriol. 39, 113-126.

Miller, R.S. & Elton, C. (1955) Activity rhythms in the Wood Mouse, Apodemus sylvaticus and the Bank Vole, Clethrionomys glareolus. Proc. Zool Soc. Lond. 12, 505-519. doi:10.1111/j.1096-3642.1955.tb00613.x

Minitab, LLC (2010) Minitab 17 [Statistical software]. State College, Pennsylvania: Minitab, LLC. Available from https://minitab.com/en-us/

Monamy, V. & Fox, B.J. (2000) Small mammal succession is determined by vegetation density rather than time elapsed since disturbance. Austral Ecol. 25, 580-587. doi:10.1111/j.1442-9993.2000.tb00063.x

Monarca, R.I., Mathias, M.D.L. & Speakman, J.R. (2015) Behavioural and physiological responses of wood mice (Apodemus sylvaticus) to experimental manipulations of predation and starvation risk. Phys & Behav. 149, 331-339. doi:10.1016/j.physbeh.2015.06.037

Mori, E., Sangiovanni, G. & Corlatti, L. (2020) Gimme shelter: The effect of rocks and moonlight on occupancy and activity pattern of an endangered rodent, the garden dormouse Eliomys quercinus. Behav. Proc. 170, 103999. doi:10.1016/j.beproc.2019.103999

Mougeot, F. & Bretagnolle, V. (2000) Predation risk and moonlight avoidance in nocturnal seabirds. J Avian Biol. 31, 376-386. doi: 10.1034/j.1600-048X.2000.310314.x

Navarro-Castilla, Á. & Barja, I. (2014) Does predation risk, through moon phase and predator cues, modulate food intake, antipredatory and physiological responses in wood mice (Apodemus sylvaticus)? Behav. Ecol. Sociobiol. 68, 1505-1512. doi:10.1007/s00265-014-1759-y

Packer, C., Swanson, A., Ikanda, D. & Kushnir, H. (2011) Fear of darkness, the full moon and the nocturnal ecology of African lions. PloS One. 6, e22285. doi 10.1371/journal.pone.0022285

Pearson, D.E. & Ruggiero, L.F. (2003) Transect versus grid trapping arrangements for sampling small-mammal communities. Wild. Soc. Bull., 454-459.

Penteriani, V., Kuparinen, A., del Mar Delgado, M., Palomares, F., López-Bao, J.V., Fedriani, J.M., Calzada, J., Moreno, S., Villafuerte, R., Campioni, L. & Lourenço, R. (2013) Responses of a top and a meso predator and their prey to moon phases. Oecol. 173, 753-766. doi: 10.1007/s00442-013-2651-6

Plesner Jensen, S. & Honess, P. (1995) The influence of moonlight on vegetation height preference and trappability of small mammals. Mammal. 59, 35-42.

Price, M.V., Waser, N.M. & Bass, T.A. (1984) Effects of moonlight on microhabitat use by desert rodents. J. Mammal. 65, 353-356. doi: 10.2307/1381183

Prochaska, M.L. & Slade, N.A. (1981) The effect of Sigmodon hispidus on summer diel activity patterns of Microtus ochrogaster .Kansas. Trans. Kans. Acad. Sci. 84, 134–138. doi: 10.2307/3628304

Prugh, L.R.& Brashares, J. (2010) Basking in the moonlight? Effect of illumination on capture success of the endangered giant kangaroo rat. J. Mammal. 91, 1205-1212. doi:10.1644/10-MAMM-A-011.1

Prugh, L.R. & Golden, C.D. (2014) Does moonlight increase predation risk? Meta-analysis reveals divergent responses of nocturnal mammals to lunar cycles. J Anim. Ecol. 83, 504-514. doi:10.1111/1365-2656.12148

R Core Team. (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/.

San-Jose, L., Séchaud, R., Schalcher, K., Judes, C., Questiaux, A., Oliveira-Xavier, A., Gémard, C., Almasi, B,. Béziers, P., Kelber, A., Amar, A. & Roulin, A. (2019) Differential fitness effect of moonlight on plumage colour morphs in barn owls. Nature Ecol Evol. 3, 1331-1340. doi:10.1038/s41559-019-0967-2

Shrubb, M. (1980) Farming influences on the food and hunting of kestrels. Bird Study 27, 109-115. doi: 10.1080/00063658009476666

Soulsbury, C.D., Gray, H.E., Smith, L.M., Braithwaite, V., Cotter, S.C., Elwood, R.W., Wilkinson, A. & Collins, L.M. (2020) The welfare and ethics of research involving wild animals: A primer. Methods in Ecology and Evolution, 11, 1164-1181. doi: 10.1111/2041-210X.13435

Spitschan, M., Aguirre, G.K., Brainard, D.H. & Sweeney, A.M. (2016) Variation of outdoor illumination as a function of solar elevation and light pollution. Sci Reports. 6, e26756. doi: 10.1038/srep26756

Upham, N. & Hafner, J. (2013) Do nocturnal rodents in the Great Basin Desert avoid moonlight? J. Mammal. 94, 59-72. doi: 10.1644/12-MAMM-A-076.1

Vickery, W.L. & Bider, J.R. (1981) The influence of weather on rodent activity. J. Mammal. 62, 140-145. doi: 10.2307/1380484

Wilson, W.L. (1992) Behavioral ecology and population regulation of the wood mouse (Apodemus sylvaticus). PhD thesis. Queen’s University: Belfast.

Wolfe, J.H. & Summerlin, C.T. (1989) The influence of lunar light on nocturnal activity of the old-field mouse. Anim. Behav. 37, 410-414. doi: 10.1016/0003-3472(89)90088-2

Wolton, R. (1983) The activity of free-ranging wood mice Apodemus sylvaticus. J. Anim. Ecol. 52, 781-794. doi: 10.2307/4453

World weather online (2019) World weather. Available from https://www.worldweatheronline.com [accessed 21 July 2019].

Wróbel, A., Bogdziewicz, M. (2015) It is raining mice and voles: which weather conditions influence the activity of Apodemus flavicollis and Myodes glareolus? Euro. J. Wild. Res. 61, 475-478. doi: 10.1007/s10344-014-0892-2