, Volume 188, Issue 4, pp 1227–1237 | Cite as

Nitrogen enrichment in host plants increases the mortality of common Lepidoptera species

  • Susanne Kurze
  • Thilo Heinken
  • Thomas FartmannEmail author
Global change ecology – original research


The recent decline of Lepidoptera species strongly correlates with the increasing intensification of agriculture in Western and Central Europe. However, the effects of changed host-plant quality through agricultural fertilization on this insect group remain largely unexplored. For this reason, we tested the response of six common butterfly and moth species to host-plant fertilization using fertilizer quantities usually applied in agriculture. The larvae of the study species Coenonympha pamphilus, Lycaena phlaeas, Lycaena tityrus, Pararge aegeria, Rivula sericealis and Timandra comae were distributed according to a split-brood design to three host-plant treatments comprising one control treatment without fertilization and two fertilization treatments with an input of 150 and 300 kg N ha−1 year−1, respectively. In L. tityrus, we used two additional fertilization treatments with an input of 30 and 90 kg N ha−1 year−1, respectively. Fertilization increased the nitrogen concentration of both host-plant species, Rumex acetosella and Poa pratensis, and decreased the survival of larvae in all six Lepidoptera species by at least one-third, without clear differences between sorrel- and grass-feeding species. The declining survival rate in all species contradicts the well-accepted nitrogen-limitation hypothesis, which predicts a positive response in species performance to dietary nitrogen content. In contrast, this study presents the first evidence that current fertilization quantities in agriculture exceed the physiological tolerance of common Lepidoptera species. Our results suggest that (1) the negative effect of plant fertilization on Lepidoptera has previously been underestimated and (2) that it contributes to the range-wide decline of Lepidoptera.


Agricultural fertilization Global change Host-plant quality Nitrogen-limitation hypothesis Rearing experiment 



We are grateful to the Kurze family (Dresden) and Tommy Kästner (Dresden) for contributing to the capture of females of different species for the experiments. C:N analyses were carried out by Antje Möhlmeyer (Osnabrück). Moreover, we would like to thank two anonymous reviewers for helpful comments on an earlier version of the manuscript.

Author contribution statement

SK, TF and TH designed the experiments. SK conducted the experiments, analysed the data and wrote the article. TF and TH made substantial contributions to the manuscript, revising and commenting on subsequent drafts.


  1. Awmack CS, Leather SR (2002) Host plant quality and fecundity in herbivorous insects. Annu Rev Entomol 47:817–844. CrossRefPubMedGoogle Scholar
  2. Barton K (2016) MuMIn: multi-model inference. R package version 1.15.6. Accessed 29 July 2017
  3. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. CrossRefGoogle Scholar
  4. Bink FA, Siepel H (1996) Nitrogen and phosphorus in Molinia caerulea (Gramineae) and its impact on the larval development in the butterfly-species Lasiommata megera (Lepidoptera: Satyridae). Entomol Gen. 20:271–280. CrossRefGoogle Scholar
  5. Boersma M, Elser JJ (2006) Too much of a good thing: on stoichiometrically balanced diets and maximal growth. Ecology 87:1325–1330.[1325:tmoagt];2 CrossRefPubMedGoogle Scholar
  6. Bolker BM, Brooks ME, Clark CJ, Gaenge SW, Poulsen JR, Stevens MHH, White JS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135. CrossRefPubMedGoogle Scholar
  7. Bräu M, Bolz R, Kolbeck H, Nummer A, Voith J, Wolf W (2013) Tagfalter in Bayern. Eugen Ulmer, StuttgartGoogle Scholar
  8. Brewer JW, Capinera JL, Deshon RE, Walmsley ML (1985) Influence of foliar nitrogen levels on survival, development, and reproduction of western spruce budworm, Choristoneura occidentals (Lepidoptera: Tortricidae). Can Entomol 117:23–32. CrossRefGoogle Scholar
  9. Bruppacher L, Pellet J, Arlettaz R, Humbert J (2016) Simple modifications of mowing regime promote butterflies in extensively managed meadows: evidence from field-scale experiments. Biol Conserv 196:196–202. CrossRefGoogle Scholar
  10. Chen Y, Lin L, Wang C, Yeh C, Hwang S (2004) Response of two Pieris (Lepidoptera: Pieridae) species to fertilization of a host plant. Zool Stud 43:778–786Google Scholar
  11. Chen Y, Ruberson JR, Olson DM (2008) Nitrogen fertilization rate affects feeding, larval performance, and oviposition preference of the beet armyworm, Spodoptera exigua, on cotton. Entomol Exp Appl 126:244–255. CrossRefGoogle Scholar
  12. Conrad KF, Warren MS, Fox R, Parsons MS, Woiwod IP (2006) Rapid declines of common, widespread British moths provide evidence of an insect biodiversity crisis. Biol Conserv 132:279–291. CrossRefGoogle Scholar
  13. Dennis RLH, Shreeve TG, van Dyck H (2006) Habitats and resources: the need for a resource-based definition to conserve butterflies. Biodivers Conserv 15:1943–1966. CrossRefGoogle Scholar
  14. Dover JW, Settele J (2009) The influences of landscape structure on butterfly distribution and movement: a review. J Insect Conserv 13:3–27. CrossRefGoogle Scholar
  15. Ebert G (ed) (1997) Die Schmetterlinge Baden-Württembergs. Band 5: Nachtfalter III. Eugen Ulmer, StuttgartGoogle Scholar
  16. Ebert G (ed) (2001) Die Schmetterlinge Baden-Württembergs. Band 8: Nachtfalter VI. Eugen Ulmer, StuttgartGoogle Scholar
  17. Ebert G, Rennwald E (1991) Die Schmetterlinge Baden-Württembergs. Band 1: Tagfalter I. Eugen Ulmer, StuttgartGoogle Scholar
  18. Ellenberg H, Leuschner C (2010) Vegetation Mitteleuropas mit den Alpen in ökologischer, dynamischer und historischer Sicht, 6th edn. Eugen Ulmer, StuttgartGoogle Scholar
  19. Fischer K, Fiedler K (2000) Response of the copper butterfly Lycaena tityrus to increased leaf nitrogen in natural food plants: evidence against the nitrogen limitation hypothesis. Oecologia 124:235–241. CrossRefPubMedGoogle Scholar
  20. García-Barros E, Fartmann T (2009) Butterfly oviposition: sites, behaviour and modes. In: Settele J, Shreeve TG, Konvička M, van Dyck H (eds) Ecology of butterflies in Europe. Cambridge University Press, Cambridge, pp 29–42Google Scholar
  21. Goverde M, Erhardt A (2003) Effects of elevated CO2 on development and larval food-plant preference in the butterfly Coenonympha pamphilus (Lepidoptera, Satyridae). Glob Change Biol 9:74–83. CrossRefGoogle Scholar
  22. Grime JP, Hodgson JG, Hunt R (2007) Comparative plant ecology, 2nd edn. Castlepoint Press, DalbeattieGoogle Scholar
  23. Han P, Lavoir A, Le Bot J, Amiens-Desneux E, Desneux N (2014) Nitrogen and water availability to tomato plants triggers bottom-up effects on the leafminer Tuta absoluta. Sci. Rep. 4:4455. CrossRefPubMedPubMedCentralGoogle Scholar
  24. Harrison XA (2014) Using observation-level random effects to model overdispersion in count data in ecology and evolution. PeerJ 2:e616. CrossRefPubMedPubMedCentralGoogle Scholar
  25. Hatcher PE, Paul ND, Ayres PG, Whittaker JB (1997) The effect of nitrogen fertilization and rust fungus infection, singly and combined, on the leaf chemical composition of Rumex obtusifolius. Funct Ecol 11:545–553. CrossRefGoogle Scholar
  26. Herzog F, Steiner B, Bailey D, Baudry J, Billeter R, Bukacek R, De Blust G, De Cock R, Dirksen J, Dormann CF, De Filippi R, Frossard E, Liira J, Schmidt T, Stöckli R, Thenail C, van Wingerden W, Bugter R (2006) Assessing the intensity of temperate European agriculture at the landscape scale. Eur J Agron 24:165–181. CrossRefGoogle Scholar
  27. Joern A, Behmer ST (1997) Importance of dietary nitrogen and carbohydrates to survival, growth, and reproduction in adults of the grasshopper Ageneotettix deorum (Orthoptera: Acrididae). Oecologia 112:201–208. CrossRefPubMedGoogle Scholar
  28. Karmoker JL, Clarkson DT, Saker LR, Rooney JM, Purves JV (1991) Sulphate deprivation depresses the transport of nitrogen to the xylem and the hydraulic conductivity of barley (Hordeum vulgare L.) roots. Planta 185:269–278. CrossRefPubMedGoogle Scholar
  29. Kleijn D, Kohler F, Báldi A, Batáry P, Concepción ED, Clough Y, Díaz M, Gabriel D, Holzschuh A, Knop E, Kovács A, Marshall EJP, Tscharntke T, Verhulst J (2009) On the relationship between farmland biodiversity and land-use intensity in Europe. Proc R Soc B 276:903–909. CrossRefPubMedGoogle Scholar
  30. Klop E, Omon B, WallisDeVries MF (2015) Impact of nitrogen deposition on larval habitats: the case of the Wall Brown butterfly Lasiommata megera. J Insect Conserv 19:393–402. CrossRefGoogle Scholar
  31. Kurze S, Heinken T, Fartmann T (2017) Nitrogen enrichment of host plants has mostly beneficial effects on the life history traits of nettle-feeding butterflies. Acta Oecol 85:157–164. CrossRefGoogle Scholar
  32. Lenth RV (2016) Least-squares means: the r package lsmeans. J Stat Softw 69:1–33CrossRefGoogle Scholar
  33. Liu Y, Pan X, Li J (2015) A 1961–2010 record of fertilizer use, pesticide application and cereal yields: a review. Agron Sustain Dev 35:83–93. CrossRefGoogle Scholar
  34. Loader C, Damman H (1991) Nitrogen content of food plants and vulnerability of Pieris rapae to natural enemies. Ecology 72:1586–1590. CrossRefGoogle Scholar
  35. Löffler F, Stuhldreher G, Fartmann T (2013) How much care does a shrub-feeding hairstreak butterfly, Satyrium spini (Lepidoptera: Lycaenidae), need in calcareous grasslands? Eur J Entomol 110:145–152. CrossRefGoogle Scholar
  36. Maes D, van Dyck H (2001) Butterfly diversity loss in Flanders (north Belgium): Europe’s worst case scenario? Biol Conserv 99:263–276. CrossRefGoogle Scholar
  37. Manning P, Gossner MM, Bossdorf O, Allan E, Zhang Y, Prati D, Blüthgen N, Boch S, Böhm S, Börschig C, Hölzel N, Jung K, Klaus VH, Klein AM, Kleinebecker T, Krauss J, Lange M, Müller J, Pašalić E, Socher SA, Tschapka M, Türke M, Weiner C, Werner M, Gockel S, Hemp A, Renner SC, Wells K, Buscot F, Kalko EKV, Linsenmair KE, Weisser WW, Fischer M (2015) Grassland management intensification weakens the associations among the diversities of multiple plant and animal taxa. Ecology 96:1492–1501. CrossRefGoogle Scholar
  38. Mattson WJ (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Evol Syst 11:119–161. CrossRefGoogle Scholar
  39. Melzer A, Gebauer G, Rehder H (1984) Nitrate content and nitrate reductase activity in Rumex obtusifolius L. II. Responses to nitrate starvation and nitrogen fertilization. Oecologia 63:380–385. CrossRefPubMedGoogle Scholar
  40. Mevi-Schütz J, Goverde M, Erhardt A (2003) Effects of fertilization and elevated CO2 on larval food and butterfly nectar amino acid preference in Coenonympha pamphilus. Behav Ecol Sociobiol 54:36–43. CrossRefGoogle Scholar
  41. Myers JH, Post BJ (1981) Plant nitrogen and fluctuations of insect populations: a test with the cinnabar moth-tansy ragwort system. Oecologia 48:151–156. CrossRefPubMedGoogle Scholar
  42. Nakagawa S, Schielzeth H (2012) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142. CrossRefGoogle Scholar
  43. Nijssen ME, WallisDeVries MF, Siepel H (2017) Pathways for the effects of increased nitrogen deposition on fauna. Biol Conserv 212:423–431. CrossRefGoogle Scholar
  44. Öckinger E, Hammarstedt O, Nilsson SG, Smith HG (2006) The relationship between local extinctions of grassland butterflies and increased soil nitrogen levels. Biol Conserv 128:564–573. CrossRefGoogle Scholar
  45. Prudic KL, Oliver JC, Bowers MD (2005) Soil nutrient effects on oviposition preference, larval performance, and chemical defense of a specialist insect herbivore. Oecologia 143:578–587. CrossRefPubMedGoogle Scholar
  46. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Accessed 29 July 2017
  47. Raubenheimer D, Lee KP, Simpson SJ (2005) Does Bertrand’s rule apply to macronutrients? Proc R Soc B 272:2429–2434. CrossRefPubMedGoogle Scholar
  48. Reinhardt R, Bolz R (2011) Rote Liste und Gesamtartenliste der Tagfalter (Rhopalocera) (Lepidoptera: Papilionoidea et Hesperioidea) Deutschlands. In: Binot-Hafke M, Balzer S, Becker N, Gruttke H, Haupt H, Hofbauer N, Ludwig G, Matzke-Hajek G, Strauch M (eds) Rote Liste gefährdeter Tiere, Pflanzen und Pilze Deutschlands. Band 3: Wirbellose Tiere (Teil 1). Naturschutz und Biologische Vielfalt 70. Bonn, Bad Godesberg, pp 165–194Google Scholar
  49. Rose S (2010) Generalist vs. Specialist? Egg laying and food plant preferences in two related lycaenid butterflies. Diploma Thesis. Institute of Landscape Ecology, Westphalian Wilhelms-University, Münster, GermanyGoogle Scholar
  50. Salvagiotti F, Castellarín JM, Miralles DJ, Pedrol HM (2009) Sulfur fertilization improves nitrogen use efficiency in wheat by increasing nitrogen uptake. Field Crop Res 113:170–177. CrossRefGoogle Scholar
  51. Sarfraz RM, Dosdall LM, Keddie AB (2009) Bottom-up 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. CrossRefGoogle Scholar
  52. Schädler M, Roeder M, Brandl R, Matthies D (2007) Interacting effects of elevated CO2, nutrient availability and plant species on a generalist invertebrate herbivore. Glob Change Biol 13:1005–1015. CrossRefGoogle Scholar
  53. Slansky F, Feeny P (1977) Stabilization of the rate of nitrogen accumulation by larvae of the cabbage butterfly on wild and cultivated food plants. Ecol Monogr 47:209–228. CrossRefGoogle Scholar
  54. Socher SA, Prati D, Boch S, Müller J, Baumbach H, Gockel S, Hemp A, Schöning I, Wells K, Buscot F, Kalko EKV, Linsenmair KE, Schulze E, Weisser WW, Fischer M (2013) Interacting effects of fertilization, mowing and grazing on plant species diversity of 1500 grasslands in Germany differ between regions. Basic Appl Ecol 14:126–136. CrossRefGoogle Scholar
  55. Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, PrincetonGoogle Scholar
  56. Stevens CJ, Dise NB, Mountford JO, Gowing DJ (2004) Impact of nitrogen deposition on the species richness of grasslands. Science 303:1876–1879. CrossRefPubMedGoogle Scholar
  57. Stopps GJ, White SN, Clements DR, Upadhyaya MK (2011) The biology of Canadian weeds. 149. Rumex acetosella L. Can J Plant Sci 91:1037–1052. CrossRefGoogle Scholar
  58. Tabashnik BE (1982) Responses of pest and non-pest Colias butterfly larvae to intraspecific variation in leaf nitrogen and water content. Oecologia 55:389–394. CrossRefPubMedGoogle Scholar
  59. Thomas JA, Telfer MG, Roy DB, Preston CD, Greenwood JJD, Asher J, Fox R, Clarke RT, Lawton JH (2004) Comparative losses of British butterflies, birds, and plants and global extinction crisis. Science 303:1879–1881. CrossRefPubMedGoogle Scholar
  60. Throop HL, Lerdau MT (2004) Effects of nitrogen deposition on insect herbivory: implications for community and ecosystem processes. Ecosystems 7:109–133. CrossRefGoogle Scholar
  61. Tilman D, Fargione J, Wolff B, Ḋ’Antonio C, Dobson A, Howarth R, Schindler D, Schlesinger WH, Simberloff D, Swackhamer D (2001) Forecasting agriculturally driven global environmental change. Science 292:281–284. CrossRefPubMedGoogle Scholar
  62. Tscharntke T, Greiler H (1995) Insect communities, grasses, and grasslands. Annu Rev Entomol 40:535–558. CrossRefGoogle Scholar
  63. Tscharntke T, Klein AM, Kruess A, Steffan-Dewenter I, Thies C (2005) Landscape perspectives on agricultural intensification and biodiversity—ecosystem service management. Ecol Lett 8:857–874. CrossRefGoogle Scholar
  64. Turlure C, Radchuk V, Baguette M, Meijrink M, van den Burg A, WallisDeVries M, van Duinen G (2013) Plant quality and local adaptation undermine relocation in a bog specialist butterfly. Ecol Evol 3:244–254. CrossRefPubMedGoogle Scholar
  65. van Dyck H, van Strien AJ, Maes D, van Swaay CAM (2009) Declines in common, widespread butterflies in a landscape under intense human use. Conserv Biol 23:957–965. CrossRefPubMedGoogle Scholar
  66. van Swaay CAM, van Strien AJ, Aghababyan K, Åström S, Botham M, Brereton T, Chambers P, Collins S, Domènech Ferrés M, Escobés R, Feldmann R, Fernández-García JM, Fontaine B, Goloshchapova S, Gracianteparaluceta A, Harpke A, Heliölä J, Khanamirian G, Julliard R, Kühn E, Lang A, Leopold P, Loos J, Maes D, Mestdagh X, Monasterio Y, Munguira ML, Murray T, Musche M, Õunap E, Pettersson LB, Popoff S, Prokofev I, Roth T, Roy D, Settele J, Stefanescu C, Švitra G, Teixeira SM, Tiitsaar A, Verovnik R, Warren MS (2015) The European Butterfly Indicator for Grassland species 1990–2013. Report VS2015.009, De Vlinderstichting, WageningenGoogle Scholar
  67. Vick JK, Young DR (2011) Spatial variation in environment and physiological strategies for forb distribution on coastal dunes. J Coastal Res 27:1113–1121. CrossRefGoogle Scholar
  68. WallisDeVries M, Bobbink R (2017) Nitrogen deposition impacts on biodiversity in terrestrial ecosystems: mechanisms and perspectives for restoration. Biol Conserv 212:387–389. CrossRefGoogle Scholar
  69. Wheeler GS, Halpern MD (1999) Compensatory responses of Samea multiplicalis larvae when fed leaves of different fertilization levels of the aquatic weed Pistia stratiotes. Entomol Exp Appl 92:205–216. CrossRefGoogle Scholar
  70. White TCR (1993) The inadequate environment—nitrogen and the abundance of animal. Springer, Berlin, HeidelbergCrossRefGoogle Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Institute of Biochemistry and Biology, General BotanyUniversity of PotsdamPotsdamGermany
  2. 2.Department of Biodiversity and Landscape Ecology, Faculty of Biology and ChemistryOsnabrück UniversityOsnabrückGermany
  3. 3.Institute of Biodiversity and Landscape Ecology (IBL)MünsterGermany

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