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

Kurze, Susanne; Heinken, Thilo; Fartmann, Thomas

doi:10.1007/s00442-018-4266-4

Global change ecology – original research
Published: 04 October 2018

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

Oecologia volume 188, pages 1227–1237 (2018)Cite this article

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Abstract

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.

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References

Awmack CS, Leather SR (2002) Host plant quality and fecundity in herbivorous insects. Annu Rev Entomol 47:817–844. https://doi.org/10.1146/annurev.ento.47.091201.145300
CAS Article PubMed Google Scholar
Barton K (2016) MuMIn: multi-model inference. R package version 1.15.6. http://CRAN.R-project.org/package=MuMIn. Accessed 29 July 2017
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
Article Google Scholar
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. https://doi.org/10.1127/entom.gen/20/1996/271
Article Google Scholar
Boersma M, Elser JJ (2006) Too much of a good thing: on stoichiometrically balanced diets and maximal growth. Ecology 87:1325–1330. https://doi.org/10.1890/0012-9658(2006)87[1325:tmoagt]2.0.co;2
Article PubMed Google Scholar
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. https://doi.org/10.1016/j.tree.2008.10.008
Article PubMed Google Scholar
Bräu M, Bolz R, Kolbeck H, Nummer A, Voith J, Wolf W (2013) Tagfalter in Bayern. Eugen Ulmer, Stuttgart
Google Scholar
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. https://doi.org/10.4039/ent11723-1
Article Google Scholar
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. https://doi.org/10.1016/j.biocon.2016.02.018
Article Google Scholar
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 43:778–786
Google Scholar
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. https://doi.org/10.1111/j.1570-7458.2007.00662.x
CAS Article Google Scholar
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. https://doi.org/10.1016/j.biocon.2006.04.020
Article Google Scholar
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. https://doi.org/10.1007/s10531-005-4314-3
Article Google Scholar
Dover JW, Settele J (2009) The influences of landscape structure on butterfly distribution and movement: a review. J Insect Conserv 13:3–27. https://doi.org/10.1007/s10841-008-9135-8
Article Google Scholar
Ebert G (ed) (1997) Die Schmetterlinge Baden-Württembergs. Band 5: Nachtfalter III. Eugen Ulmer, Stuttgart
Ebert G (ed) (2001) Die Schmetterlinge Baden-Württembergs. Band 8: Nachtfalter VI. Eugen Ulmer, Stuttgart
Ebert G, Rennwald E (1991) Die Schmetterlinge Baden-Württembergs. Band 1: Tagfalter I. Eugen Ulmer, Stuttgart
Ellenberg H, Leuschner C (2010) Vegetation Mitteleuropas mit den Alpen in ökologischer, dynamischer und historischer Sicht, 6th edn. Eugen Ulmer, Stuttgart
Google Scholar
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. https://doi.org/10.1007/s004420000365
CAS Article PubMed Google Scholar
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 29–42
Google Scholar
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. https://doi.org/10.1046/j.1365-2486.2003.00520.x
Article Google Scholar
Grime JP, Hodgson JG, Hunt R (2007) Comparative plant ecology, 2nd edn. Castlepoint Press, Dalbeattie
Google Scholar
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. https://doi.org/10.1038/srep04455
CAS Article PubMed PubMed Central Google Scholar
Harrison XA (2014) Using observation-level random effects to model overdispersion in count data in ecology and evolution. PeerJ 2:e616. https://doi.org/10.7717/peerj.616
Article PubMed PubMed Central Google Scholar
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. https://doi.org/10.1046/j.1365-2435.1997.00123.x
Article Google Scholar
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. https://doi.org/10.1016/j.eja.2005.07.006
Article Google Scholar
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. https://doi.org/10.1007/s004420050301
Article PubMed Google Scholar
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. https://doi.org/10.1007/bf00194070
CAS Article PubMed Google Scholar
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. https://doi.org/10.1098/rspb.2008.1509
CAS Article PubMed Google Scholar
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. https://doi.org/10.1007/s10841-014-9748-z
Article Google Scholar
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. https://doi.org/10.1016/j.actao.2017.11.005
Article Google Scholar
Lenth RV (2016) Least-squares means: the r package lsmeans. J Stat Softw 69:1–33
Article Google Scholar
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. https://doi.org/10.1007/s13593-014-0259-9
CAS Article Google Scholar
Loader C, Damman H (1991) Nitrogen content of food plants and vulnerability of Pieris rapae to natural enemies. Ecology 72:1586–1590. https://doi.org/10.2307/1940958
Article Google Scholar
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. https://doi.org/10.14411/eje.2013.020
Article Google Scholar
Maes D, van Dyck H (2001) Butterfly diversity loss in Flanders (north Belgium): Europe’s worst case scenario? Biol Conserv 99:263–276. https://doi.org/10.1016/s0006-3207(00)00182-8
Article Google Scholar
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. https://doi.org/10.1890/14-1307.1
Article Google Scholar
Mattson WJ (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Evol Syst 11:119–161. https://doi.org/10.1146/annurev.es.11.110180.001003
Article Google Scholar
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. https://doi.org/10.1007/bf00390669
CAS Article PubMed Google Scholar
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. https://doi.org/10.1007/s00265-003-0601-8
Article Google Scholar
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. https://doi.org/10.1007/bf00347957
Article PubMed Google Scholar
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. https://doi.org/10.1111/j.2041-210x.2012.00261.x
Article Google Scholar
Nijssen ME, WallisDeVries MF, Siepel H (2017) Pathways for the effects of increased nitrogen deposition on fauna. Biol Conserv 212:423–431. https://doi.org/10.1016/j.biocon.2017.02.022
Article Google Scholar
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. https://doi.org/10.1016/j.biocon.2005.10.024
Article Google Scholar
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. https://doi.org/10.1007/s00442-005-0008-5
Article PubMed Google Scholar
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/. Accessed 29 July 2017
Raubenheimer D, Lee KP, Simpson SJ (2005) Does Bertrand’s rule apply to macronutrients? Proc R Soc B 272:2429–2434. https://doi.org/10.1098/rspb.2005.3271
CAS Article PubMed Google Scholar
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 165–194
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, Germany
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. https://doi.org/10.1016/j.fcr.2009.05.003
Article Google Scholar
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. https://doi.org/10.14411/eje.2009.073
CAS Article Google Scholar
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. https://doi.org/10.1111/j.1365-2486.2007.01319.x
Article Google Scholar
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. https://doi.org/10.2307/1942617
Article Google Scholar
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. https://doi.org/10.1016/j.baae.2012.12.003
Article Google Scholar
Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton
Google Scholar
Stevens CJ, Dise NB, Mountford JO, Gowing DJ (2004) Impact of nitrogen deposition on the species richness of grasslands. Science 303:1876–1879. https://doi.org/10.1126/science.1094678
CAS Article PubMed Google Scholar
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. https://doi.org/10.4141/cjps2011-042
Article Google Scholar
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. https://doi.org/10.1007/bf00376927
Article PubMed Google Scholar
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. https://doi.org/10.1126/science.1095046
CAS Article PubMed Google Scholar
Throop HL, Lerdau MT (2004) Effects of nitrogen deposition on insect herbivory: implications for community and ecosystem processes. Ecosystems 7:109–133. https://doi.org/10.1007/s10021-003-0225-x
CAS Article Google Scholar
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. https://doi.org/10.1126/science.1057544
CAS Article PubMed Google Scholar
Tscharntke T, Greiler H (1995) Insect communities, grasses, and grasslands. Annu Rev Entomol 40:535–558. https://doi.org/10.1146/annurev.en.40.010195.002535
CAS Article Google Scholar
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. https://doi.org/10.1111/j.1461-0248.2005.00782.x
Article Google Scholar
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. https://doi.org/10.1002/ece3.427
Article PubMed Google Scholar
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. https://doi.org/10.1111/j.1523-1739.2009.01175.x
Article PubMed Google Scholar
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, Wageningen
Vick JK, Young DR (2011) Spatial variation in environment and physiological strategies for forb distribution on coastal dunes. J Coastal Res 27:1113–1121. https://doi.org/10.2112/jcoastres-d-10-00156.1
CAS Article Google Scholar
WallisDeVries M, Bobbink R (2017) Nitrogen deposition impacts on biodiversity in terrestrial ecosystems: mechanisms and perspectives for restoration. Biol Conserv 212:387–389. https://doi.org/10.1016/j.biocon.2017.01.017
Article Google Scholar
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. https://doi.org/10.1046/j.1570-7458.1999.00539.x
Article Google Scholar
White TCR (1993) The inadequate environment—nitrogen and the abundance of animal. Springer, Berlin, Heidelberg
Book Google Scholar

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Acknowledgements

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.

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Authors and Affiliations

Institute of Biochemistry and Biology, General Botany, University of Potsdam, Maulbeerallee 3, 14469, Potsdam, Germany
Susanne Kurze & Thilo Heinken
Department of Biodiversity and Landscape Ecology, Faculty of Biology and Chemistry, Osnabrück University, Barbarastraße 11, 49076, Osnabrück, Germany
Thomas Fartmann
Institute of Biodiversity and Landscape Ecology (IBL), An der Kleimannbrücke 98, 48157, Münster, Germany
Thomas Fartmann

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Susanne Kurze
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Thilo Heinken
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Thomas Fartmann
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Contributions

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.

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Correspondence to Thomas Fartmann.

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Communicated by Klaus Fischer.

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Kurze, S., Heinken, T. & Fartmann, T. Nitrogen enrichment in host plants increases the mortality of common Lepidoptera species. Oecologia 188, 1227–1237 (2018). https://doi.org/10.1007/s00442-018-4266-4

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Received: 24 May 2018
Accepted: 26 September 2018
Published: 04 October 2018
Issue Date: December 2018
DOI: https://doi.org/10.1007/s00442-018-4266-4

Keywords

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