Abstract
Changes in large herbivore distribution and abundance can have effects that potentially cascade throughout the trophic structure of an ecosystem. Little is known about these indirect trophic effects of ungulate herbivory, so the aim of this study was to investigate the role of red deer (Cervus elaphus) in determining the distribution and diversity of ground-dwelling beetles. We collected > 9000 beetles belonging to 149 species in a Western Norway boreal forest by pitfall trapping inside and outside red-deer exclosures placed along a gradient in herbivory intensity. Our study showed that red deer herbivory had a significant effect on structuring ground beetle communities in this boreal ecosystem. Key findings were that: (1) out of 17 beetle species represented by more than 100 specimens, four species benefited from red deer herbivory and associated impacts, while two were detrimentally affected; 2) red deer herbivory did not affect beetle abundance or alpha diversity, but increased local variation in beetle community structure (higher beta diversity); and 3) red deer browsing is important for the composition of the ground-beetle fauna. Herbivory improved the explanation of variation in beetle species composition on the forest floor by 40%. Given that herbivory is an indirect but central predictor of ground-dwelling beetle communities, it should be included in future studies or monitoring programs of red listed or keystone ground-dwelling beetles.
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Abbas F, Merlet J, Morellet N, Verheyden H, Hewison AJM, Cargnelutti B, Angibault JM, Picot D, Rames JL, Lourtet B, Aulagnier S, Daufresne T (2012) Roe deer may markedly alter forest nitrogen and phosphorus budgets across Europe. Oikos 121:1271–1278. https://doi.org/10.1111/j.1600-0706.2011.20103.x
Adler PB, Raff DA, Lauenroth WK (2001) The effect of grazing on the spatial heterogeneity of vegetation. Oecologia 128:465–479
Allombert S, Gaston AJ, Martin JL (2005a) A natural experiment on the impact of overabundant deer on songbird populations. Biol Conserv 126:1–13. https://doi.org/10.1016/j.biocon.2005.04.001
Allombert S, Stockton S, Martin JL (2005b) A natural experiment on the impact of overabundant deer on forest invertebrates. Conserv Biol 19:1917–1929. https://doi.org/10.1111/j.1523-1739.2005.00280.x
Andersen J (1995) A comparison of pitfall trapping and quadrat sampling of Carabidae (Coleoptera) on river banks. Entomol Fenn 6:65–77
Anderson MJ, Ellingsen KE, McArdle BH (2006) Multivariate dispersion as a measure of beta diversity. Ecol Lett 9:683–693. https://doi.org/10.1111/j.1461-0248.2006.00926.x
Auestad I, Rydgren K, Økland RH (2008) Scale-dependence of vegetation–environment relationships in semi-natural grasslands. J Veg Sci 19:139–148. https://doi.org/10.3170/2007-8-18344
Augustine DJ, McNaughton SJ (1998) Ungulate effects on the functional species composition of plant communities: herbivore selectivity and plant tolerance. J Wildl Manag 62:1165–1183. https://doi.org/10.2307/3801981
Austrheim G, Solberg EJ, Mysterud A (2011) Spatio-temporal variation in large herbivore pressure in Norway during 1949–1999: has decreased grazing by livestock been countered by increased browsing by cervids? Wildl Biol 17:286–298. https://doi.org/10.2981/10-038
Bachand M, Pellerin S, Cote SD, Moretti M, De Caceres M, Brousseau P-M, Cloutier C, Hebert C, Cardinal E, Martin J-L, Poulin M (2014) Species indicators of ecosystem recovery after reducing large herbivore density: comparing taxa and testing species combinations. Ecol Indic 38:12–19. https://doi.org/10.1016/j.ecolind.2013.10.018
Baines D, Sage RB, Baines MM (1994) The implications of red deer grazing to ground vegetation and invertebrate communities of Scottich native pinewoods. J Appl Ecol 31:776–783. https://doi.org/10.2307/2404167
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Ben-Ari M, Inbar M (2013) When herbivores eat predators: predatory insects effectively avoid incidental ingestion by mammalian herbivores. PLoS ONE 8:e56748. https://doi.org/10.1371/journal.pone.0056748
Beschta RL, Ripple WJ (2016) Riparian vegetation recovery in Yellowstone: the first two decades after wolf reintroduction. Biol Conserv 198:93–103. https://doi.org/10.1016/j.biocon.2016.03.031
Birkemoe T (1993) Distribution of ground dwelling beetles along the main vegetation gradient in an old growth boreal forest. Cand. Scient., University of Oslo
Bonan GB, Shugart HH (1989) Environmental-factors and ecological processes in boreal forests. Annu Rev Ecol Syst 20:1–28. https://doi.org/10.1146/annurev.es.20.110189.000245
Borcard D, Legendre P, Drapeau P (1992) Partialling out the spatial component of ecological variation. Ecology 73:1045–1055. https://doi.org/10.2307/1940179
Bremmer JM, Mulvaney CS (1982) Nitrogen-total, kap. 31. In: Page AL, Keeney DR (eds) Methods of soil analysis, Part 2, Agronomy 9, 2nd edn. American Society of Agronomy, Madison, pp 595–624
Brousseau PM, Hebert C, Cloutier C, Cote SD (2013) Short-term effects of reduced white-tailed deer density on insect communities in a strongly overbrowsed boreal forest ecosystem. Biodivers Conserv 22:77–92. https://doi.org/10.1007/s10531-012-0400-5
Chollet S, Padie S, Stockton S, Allombert S, Gaston AJ, Martin JL (2016) Positive plant and bird diversity response to experimental deer population reduction after decades of uncontrolled browsing. Divers Distrib 22:274–287. https://doi.org/10.1111/ddi.12393
Côté SD, Rooney TP, Tremblay J-P, Dussault C, Waller DM (2004) Ecological impacts of deer overabundance. Annu Rev Ecol Evol Syst 35:113–147. https://doi.org/10.1146/annurev.ecolsys.35.021103.105725
deCalesta DS (1994) Effect of white-tailed deer on songbirds within managed forests in Pennsylvania. J Wildl Manag 58:711–718. https://doi.org/10.2307/3809685
Dornelas M, Soykan CU, Ugland KI (2011) Biodiversity and disturbance. In: Magurran AE, McGill BJ (eds) Biological Diversity frontiers in measurements and assessment. Oxford University Press, Oxford, pp 237–251
Elek Z, Howe AG, Enggaard MK, Lovei GL (2017) Seasonal dynamics of common ground beetles (Coleoptera: Carabidae) along an urbanisation gradient near Soro, Zealand, Denmark. Entomol Fenn 28:27–40
Foster CN, Barton PS, Lindenmayer DB (2014) Effects of large native herbivores on other animals. J Appl Ecol 51:929–938. https://doi.org/10.1111/1365-2664.12268
Fuller RJ, Gill RMA (2001) Ecological impacts of increasing numbers of deer in British woodland. Forestry 74:193–199. https://doi.org/10.1093/forestry/74.3.193
Gish M, Ben-Ari M, Inbar M (2017) Direct consumptive interactions between mammalian herbivores and plant-dwelling invertebrates: prevalence, significance, and prospectus. Oecologia 183:347–352. https://doi.org/10.1007/s00442-016-3775-2
Gonzalez-Megias A, Gomez JM, Sanchez-Pinero F (2004) Effects of ungulates on epigeal arthropods in Sierra Nevada National Park (southeast Spain). Biodivers Conserv 13:733–752. https://doi.org/10.1023/b:bioc.0000011723.82351.82
Gullan PJ, Cranston PS (2005) The insects: an ouline of entomology, 3rd edn. Blackwell, Malden
Hegland SJ, Rydgren K (2016) Eaten but not always beaten: winners and losers along a red deer herbivory gradient in boreal forest. J Veg Sci 27:111–122. https://doi.org/10.1111/jvs.12339
Hegland SJ, Lilleeng MS, Moe SR (2013) Old-growth forest floor richness increases with red deer herbivory intensity. For Ecol Manag 310:267–274. https://doi.org/10.1016/j.foreco.2013.08.031
Henriksen S, Hilmo O (eds) (2015) Norsk rødliste for arter 2015. Artsdatabanken, Norge
Hill MO, Gauch HG (1980) Detrended correspondence-analysis—an improved ordination technique. Vegetatio 42:47–58. https://doi.org/10.1007/bf00048870
Hofmann RR (1989) Evolutionanry steps of ecophysiological adaptation and diversification of ruminants: a comparative view of their digestive-system. Oecologia 78:443–457. https://doi.org/10.1007/bf00378733
Iida T, Soga M, Hiura T, Koike S (2016) Life history traits predict insect species responses to large herbivore overabundance: a multitaxonomic approach. J Insect Conserv 20:295–304. https://doi.org/10.1007/s10841-016-9866-x
Ikeda H, Kubota K, Kagaya T, Abe T (2007) Flight capabilities and feeding habits of silphine beetles: are flightless species really “carrion beetles”? Ecol Res 22:237–241. https://doi.org/10.1007/s11284-006-0012-1
Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386. https://doi.org/10.2307/3545850
Kindt R, Coe R (2005) Tree diversity analysis: a manual and software for common statistical methods for ecological and biodiversity studies. World Agroforestry Centre (ICRAF), Nairobi
Koivula MJ (2011) Useful model organisms, indicators, or both? Ground beetles (Coleoptera, Carabidae) reflecting environmental conditions. ZooKeys 100:287–317. https://doi.org/10.3897/zookeys.100.1533
Koivula M, Kukkonen J, Niemela J (2002) Boreal carabid-beetle (Coleoptera, Carabidae) assemblages along the clear-cut originated succession gradient. Biodiver Conserv 11:1269–1288. https://doi.org/10.1023/a:1016018702894
Koleff P, Gaston KJ, Lennon JJ (2003) Measuring beta diversity for presence-absence data. J Anim Ecol 72:367–382. https://doi.org/10.1046/j.1365-2656.2003.00710.x
Kotze DJ, Brandmayr P, Casale A, Dauffy-Richard E, Dekoninck W, Koivula MJ, Lovei GL, Mossakowski D, Noordijk J, Paarmann W, Pizzolotto R, Saska P, Schwerk A, Serrano J, Szyszko J, Taboada A, Turin H, Venn S, Vermeulen R, Zetto T (2011) Forty years of carabid beetle research in Europe—from taxonomy, biology, ecology and population studies to bioindication, habitat assessment and conservation. ZooKeys 100:55–148. https://doi.org/10.3897/zookeys.100.1523
Kuznetsova A, Brockhoff PB, Christensen RHB (2016) lmerTest: tests in linear mixed effects models. R package version 2.0-30. http://CRAN.R-project.org/package=lmerTest
Lilleeng MS, Hegland SJ, Rydgren K, Moe SR (2016) Red deer mediate spatial and temporal plant heterogeneity in boreal forests. Ecol Res 31:777–784. https://doi.org/10.1007/s11284-016-1391-6
Liu HY, Økland T, Halvorsen R, Gao JX, Liu QR, Eilertsen O, Bratli H (2008) Gradient analyses of forests ground vegetation and its relationships to environmental variables in five subtropical forest areas, S and SW China. Sommerfeltia 32:1–196
Martin JL, Stockton SA, Allombert S, Gaston AJ (2010) Top-down and bottom-up consequences of unchecked ungulate browsing on plant and animal diversity in temperate forests: lessons from a deer introduction. Biol Invasions 12:353–371. https://doi.org/10.1007/s10530-009-9628-8
McCullagh P, Nelder J (1989) Generalized linear models. Chapman & Hall, New York
Melis C, Buset A, Aarrestad PA, Hanssen O, Meisingset EL, Andersen R, Moksnes A, Røskaft E (2006) Impact of red deer Cervus elaphus grazing on bilberry Vaccinium myrtillus and composition of ground beetle (Coleoptera, Carabidae) assemblage. Biodivers Conserv 15:2049–2059. https://doi.org/10.1007/s10531-005-2005-8
Melis C, Sundby M, Andersen R, Moksnes A, Pedersen B, Røskaft E (2007) The role of moose Alces alces L. in boreal forest—the effect on ground beetles (Coleoptera, Carabidae) abundance and diversity. Biodivers Conserv 16:1321–1335. https://doi.org/10.1007/s10531-005-6230-y
Minchin PR (1987) An evaluation of the relative robustness of techniques for ecological ordination. Vegetatio 69:89–107. https://doi.org/10.1007/bf00038690
Moe SR, Wegge P (2008) Effects of deposition of deer dung on nutrient redistribution and on soil and plant nutrients on intensively grazed grasslands in lowland Nepal. Ecol Res 23:227–234. https://doi.org/10.1007/s11284-007-0367-y
Moen A (1999) National atlas of Norway: vegetation. Norwegian Mapping Authority, Hønefoss
Mysterud A, Askilsrud H, Loe LE, Veiberg V (2010) Spatial patterns of accumulated browsing and its relevance for management of red deer Cervus elaphus. Wildl Biol 16:162–172. https://doi.org/10.2981/09-043
Niemelä J, Koivula M, Kotze DJ (2007) The effects of forestry on carabid beetles (Coleoptera: Carabidae) in boreal forests. J Insect Conserv 11:5–18. https://doi.org/10.1007/s10841-006-9014-0
Økland RH (1990) Vegetation ecology: theory, methods and applications with reference to Fennoscandia. Sommerfeltia Suppl 1:1–233
Økland RH (1996) Are ordination and constrained ordination alternative or complementary strategies in general ecological studies? J Veg Sci 7(2):289–292
Økland RH (1999) On the variation explained by ordination and constrained ordination axes. J Veg Sci 10:131–136
Økland RH (2003) Partitioning the variation in a plot-by-species data matrix that is related to n sets of explanatory variables. J Veg Sci 14:693–700. https://doi.org/10.1111/j.1654-1103.2003.tb02201.x
Økland RH, Økland T, Rydgren K (2001) Vegetation–environment relationships of boreal spruce swamp forests in Østmarka Nature Reserve, SE Norway. Sommerfeltia 29:1–190
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2016) vegan: Community Ecology Package. R Package version 2.3-3. http://CRAN.R-project.org/package=vegan
Paje F, Mossakowski D (1984) pH-preferences and habitat selection in carabid beetles. Oecologia 64:41–46. https://doi.org/10.1007/bf00377541
Pedersen S, Andreassen HP, Persson IL, Julkunen-Tiitto R, Danell K, Skarpe C (2011) Vole preference of bilberry along gradients of simulated moose density and site productivity. Integr Zool 6:341–351. https://doi.org/10.1111/j.1749-4877.2011.00260.x
Polis GA (1999) Why Are parts of the world green? Multiple factors control productivity and the distribution of biomass. Oikos 86:3–15. https://doi.org/10.2307/3546565
Prather CM, Pelini SL, Laws A, Rivest E, Woltz M, Bloch CP, Del Toro I, Ho CK, Kominoski J, ScottNewbold TA, Parsons S, Joern A (2013) Invertebrates, ecosystem services and climate change. Biol Rev 88:327–348. https://doi.org/10.1111/brv.12002
R Core Team (2015) R: a language and environment for statistical computing, 3.1.3 edn. R Foundation for Statistical Computing, Vienna
R Core Team (2017) R: a language and environment for statistical computing, vol 3.4.2. R Foundation for Statistical Computing, Vienna
Ripple WJ, Beschta RL, Fortin JK, Robbins CT (2014) Trophic cascades from wolves to grizzly bears in Yellowstone. J Anim Ecol 83:223–233. https://doi.org/10.1111/1365-2656.12123
Rooney TP, Waller DM (2003) Direct and indirect effects of white-tailed deer in forest ecosystems. For Ecol Manag 181:165–176. https://doi.org/10.1016/s0378-1127(03)00130-0
Simila M, Kouki J, Monkkonen M, Sippola AL (2002) Beetle species richness along the forest productivity gradient in northern Finland. Ecography 25:42–52. https://doi.org/10.1034/j.1600-0587.2002.250106.x
Similä M, Kouki J, Monkkonen M, Sippola AL, Huhta E (2006) Co-variation and indicators, of species diversity: can richness of forest-dwelling species be predicted in northern boreal forests? Ecol Indic 6:686–700. https://doi.org/10.1016/j.ecolind.2005.08.028
Skaug H, Fournier D, Bolker B, Magnusson A, Nielsen A (2016) Generalized linear mixed models using ‘AD Model Builder’. R package version 0.8.3.3
Skogen A, Lunde BN (1997) Flora og vegetasjon på Svanøy i Sunnfjord, med vegetasjonskart. Botanical Institute, University of Bergen, Bergen
Stewart AJA (2001) The impact of deer on lowland woodland invertebrates: a review of the evidence and priorities for future research. Forestry 74:259–270. https://doi.org/10.1093/forestry/74.3.259
Suominen O, Danell K (2006) Effects of large herbivores on other fauna. In: Danell K, Bergstrom R, Duncan P, Pastor J (eds) Large herbivore ecology, ecosystem dynamics and conservation. Cambridge University Press, Cambridge, pp 383–412
Suominen O, Niemela J, Martikainen P, Niemela P, Kojola I (2003) Impact of reindeer grazing on ground-dwelling Carabidae and Curculionidae assemblages in Lapland. Ecography 26:503–513. https://doi.org/10.1034/j.1600-0587.2003.03445.x
ter Braak CJF (1986) Canonical correspondence analysis: a new eigenvector technique for multivariate direct gradient analysis. Ecology 67:1167–1179
Terborgh J, Lopez L, Nunez P, Rao M, Shahabuddin G, Orihuela G, Riveros M, Ascanio R, Adler GH, Lambert TD, Balbas L (2001) Ecological meltdown in predator-free forest fragments. Science 294:1923–1926. https://doi.org/10.1126/science.1064397
Toivanen T, Heikkila T, Koivula MJ (2014) Emulating natural disturbances in boreal Norway spruce forests: effects on ground beetles (Coleoptera, Carabidae). For Ecol Manag 314:64–74. https://doi.org/10.1016/j.foreco.2013.11.028
Tremblay JP, Huot J, Potvin F (2006) Divergent nonlinear responses of the boreal forest field layer along an experimental gradient of deer densities. Oecologia 150:78–88. https://doi.org/10.1007/s00442-006-0504-2
van Klink R, van der Plas F, van Noordwijk CGE, WallisDeVries MF, Olff H (2015) Effects of large herbivores on grassland arthropod diversity. Biol Rev 90:347–366. https://doi.org/10.1111/brv.12113
van Son TC, Halvorsen R (2014) Multiple parallel ordination and data manipulation: the importance of weighting species abundance data. Sommerfeltia 37:1–37
Zuur AF, Saveliev AA, Ieno EN (2012) Zero inflated models and generalized linear mixed models with R. Highland Statistics, Newsburg
Acknowledgements
Sindre Ligaard did the taxonomic determination of the beetles and scored the species to ecological niches. Annie Aasen and Irene Dahl, MINA, NMBU, did the soil analyses. Katrine Eldegard gave early comments on the study design, and Sam Steyaert commented on earlier versions of this manuscript. Peter Frost did copy editing. Two anonymous referees provided constructive comments to earlier drafts. The study was supported by the Norwegian Research Council under the Miljø 2015 programme (project number 204403/E40) and the Norwegian Environment Agency. We thank the Norwegian Red Deer Centre for support during field work.
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Lilleeng, M.S., Rydgren, K., Halvorsen, R. et al. Red deer structure the ground-dwelling beetle community in boreal forest. Biodivers Conserv 27, 2507–2525 (2018). https://doi.org/10.1007/s10531-018-1550-x
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DOI: https://doi.org/10.1007/s10531-018-1550-x