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Predator and parasitoid insects along elevational gradients: role of temperature and habitat diversity

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Abstract

Elevational gradients are characterized by strong abiotic variation within small geographical distances and provide a powerful tool to evaluate community response to variation in climatic and other environmental factors. We explored how temperature and habitat diversity shape the diversity of holometabolous predator and parasitoid insects along temperate elevational gradients in the European Alps. We surveyed insect communities along 12 elevational transects that were selected to separate effects of temperature from those of habitat diversity. Pitfall traps and pan traps were placed every 100 m of elevation increment along the transects ranging from 120 to 2200 m a.s.l. Sampling took place once a month from June to September 2015. Four groups characterized by having at least one life stage behaving as predator or parasitoid were examined: tachinids (Diptera), hoverflies (Diptera), sphecids (Hymenoptera) and ground beetles (Coleoptera). Species richness and evenness changed with elevation, but the shape and direction of the elevation–diversity patterns varied between groups. The effect of temperature on species richness was positive for all groups except for hoverflies. Habitat diversity did not affect species richness, while it modulated the evenness of most groups. Often, elevational patterns of species richness and evenness were contrasting. Our study indicates that natural enemies characterized by diverse ecological requirements can be differentially affected by temperature and habitat diversity across the same elevational gradients. As climate warming is predicted to increase mean annual temperatures and exacerbate weather variability, it is also expected to strongly influence natural enemies and their ability to regulate herbivore populations.

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References

  • Arroyo MTK, Primack RB, Armesto JJ (1982) Community studies in pollination ecology in the high temperate Andes of Central Chile. I. Pollination mechanisms and altitudinal variation. Am J Bot 69:82–97

    Article  Google Scholar 

  • Ashton S, Gutiérrez D, Wilson RJ (2009) Effects of temperature and elevation on habitat use by a rare mountain butterfly: implications for species responses to climate change. Ecol Entomol 34:437–446

    Article  Google Scholar 

  • Axmacher JC, Fiedler K (2008) Habitat type modifies geometry of elevational diversity gradients in geometrid moths (Lepidoptera Geometridae) on Mt Kilimanjaro, Tanzania. Trop Zool 2:243–251

    Google Scholar 

  • Bar-Massada A, Wood EM (2014) The richness–heterogeneity relationship differs between heterogeneity measures within and among habitats. Ecography 37:528–535

    Article  Google Scholar 

  • Bartsch H, Binkiewicz E, Klintbjer A, RÅden A, Nasibov E (2009a) Blomflugor: Eristalinae Microdontinae. Nationalnyckeln till Sveriges flora och flora, DH 53b. Artdatabanken, SLU, Uppsala, p 478

    Google Scholar 

  • Bartsch H, Binkiewicz E, RÅden A, Nasibov E (2009b) Blomflugor: Syrphidae. Nationalnyckeln till Sveriges flora och flora, DH 53a. Artdatabanken, SLU, Uppsala, p 406

    Google Scholar 

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

    Article  Google Scholar 

  • Bertrand C, Burel F, Baudry J (2016) Spatial and temporal heterogeneity of the crop mosaic influences carabid beetles in agricultural landscapes. Landsc Ecol 31:451–466

    Article  Google Scholar 

  • Bishop TR, Robertson MP, van Rensburg BJ, Parr CL (2014) Elevation–diversity patterns through space and time: ant communities of the Maloti-Drakensberg Mountains of southern Africa. J Biogeogr 41:2256–2268

    Article  Google Scholar 

  • Bitsch J, Leclercq J (1993) Faune de France. France et régions limitrophes. 79. Hyménoptères Sphecidae d’Europe occidentale. Volume 1. Généralités - Crabroninae. Fédération Française des Sociétés de Sciences Naturelles, Paris. 325 pp

  • Bitsch J, Barbier Y, Gayubo SF, Schmidt K, Ohl M (1997) Faune de France. France et régions limitrophes. 82. Hyménoptères Sphecidae d’Europe occidentale. Volume 2 Fédération Française des Sociétés de Sciences Naturelles, Paris. 429 pp

  • Bitsch J, Dollfuss H, Boucek Z, Schmidt K, Schmid-Egger Ch, Gayubo SF, Antropov AV, Barbier Y (2001) Hyménoptères Sphecidae d’Europe Occidentale. Volume 3. Faune de France 86. Fédération française des Sociétés de Sciences Naturelles, Paris. 459 pp

  • Bock CE, Jones ZF, Bock JH (2007) Relationships between species richness, evenness, and abundance in a southwestern savanna. Ecology 88:1322–1327

    Article  PubMed  Google Scholar 

  • Brandmayr P, Zetto T, Pizzolotto R (2005) I Coleotteri Carabidi per la valutazione ambientale e la conservazione della biodiversità. Manuali e linee guida, 34/2005. APAT, Roma

  • Brenner GJ, Oboyski PT, Banko PC (2002) Parasitism of Cydia spp. (Lepidoptera: tortricidae) on Sophora chrysophylla (Fabaceae) along an elevation gradient of dry subalpine forest on Mauna Kea, Hawaii. Pan-Pac Entomol 78:101–109

    Google Scholar 

  • Brown JH (2014) Why are there so many species in the tropics? J Biogeogr 41:8–22

    Article  PubMed  Google Scholar 

  • Cerretti P (2010) I tachinidi della fauna italiana (Diptera Tachinidae), con chiave interattiva dei generi ovest paleartici, Vol. I & II, CD-rom (in Italian with English interactive key). Cierre Edizioni, Verona

    Google Scholar 

  • Cerretti P, Tschorsnig H-P, Lopresti M, Di Giovanni F (2012) MOSCHweb: a matrix-based interactive key to the genera of the Palaearctic Tachinidae (Insecta, Diptera). Zookeys 205:5–18

    Article  Google Scholar 

  • Chamberlain D, Brambilla M, Caprio E, Pedrini P, Rolando A (2016) Alpine bird distributions along elevation gradients: the consistency of climate and habitat effects across geographic regions. Oecologia 181:1139–1150

    Article  PubMed  Google Scholar 

  • Colwell RK, Rahbek C, Gotelli NJ (2004) The Mid-Domain effect and species richness patterns: what have we learned so far? Am Nat 163:E1–E23

    Article  PubMed  Google Scholar 

  • Colwell RK, Brehm G, Cardelús CL, Gilman AC, Longino JT (2008) Global warming, elevational range shifts, and lowland biotic attrition in the wet tropics. Science 322:258–261

    Article  PubMed  CAS  Google Scholar 

  • Corcos D, Inclán DJ, Cerretti P, Mei M, Di Giovanni F, Birtele D, Rosa P, De Biase A, Audisio P, Marini L (2017) Environmental heterogeneity effect on insect natural enemies varies across spatial scales and seasons: a multi-taxon approach. Insect Conserv Divers 10:462–471

    Article  Google Scholar 

  • Dangles O, Carpio C, Barragan A, Zeddam J-L, Silvain J-F (2008) Temperature as a key driver of ecological sorting among invasive pest species in the tropical Andes. Ecol Appl 18:1795–1809

    Article  PubMed  CAS  Google Scholar 

  • De Arce Crespo JA, Gutiérrez D (2011) Altitudinal trends in the phenology of butterflies in a mountainous area in central Spain. Eur J Entomol 108:651–658

    Article  Google Scholar 

  • Dorji T, Moe SR, Klein JA, Totland Ø (2014) Plant species richness, evenness, and composition along environmental gradients in an Alpine meadow grazing ecosystem in Central Tibet, China. Arct Antarct Alp Res 46:308–326

    Article  Google Scholar 

  • Dunn RR, McCain CM, Sanders NJ (2007) When does diversity fit null model predictions? Scale and range size mediate the mid-domain effect. Glob Ecol Biogeogr 16:305–312

    Article  Google Scholar 

  • Durant JM, Hjermann DØ, Ottersen G, Stenseth NC (2007) Climate and the match or mismatch between predator requirements and resource availability. Clim Res 33:271–283

    Article  Google Scholar 

  • Evans EW, Carlile NR, Innes MB, Pitigala N (2013) Warm springs reduce parasitism of the cereal leaf beetle. J Appl Entomol 137:383–391

    Article  Google Scholar 

  • Fauth JE, Crother BI, Slowinski JB (1989) Elevational patterns of species richness, evenness and abundance of the Costa Rican leaf–litter herpetofauna. Biotropica 21:178–185

    Article  Google Scholar 

  • Fleishman E, Fay JP, Murphy DD (2000) Upsides and downsides: contrasting topographic gradients in species richness and associated scenarios for climate change. J Biogeogr 27:1209–1219

    Article  Google Scholar 

  • Hawkins BA, Porter EE, Diniz-Filho JAF (2003) Productivity and history as predictors of the latitudinal diversity gradient for terrestrial birds. Ecology 84:1608–1623

    Article  Google Scholar 

  • Hodkinson ID (2005) Terrestrial insects along elevation gradients: species and community responses to altitude. Biol Rev 80:489–513

    Article  PubMed  Google Scholar 

  • Hutchinson GE (1957) Concluding remarks. Cold Spring Harb Symp Quant Biol 22:415–427

    Article  Google Scholar 

  • Keil P, Dziock F, Storch D (2008) Geographical patterns of hoverfly (Diptera, Syrphidae) functional groups in Europe: inconsistency in environmental correlates and latitudinal trends. Ecol Entomol 33:748–757

    Google Scholar 

  • Körner C (2007) The use of ‘altitude’ in ecological research. Trends Ecol Evol 22:569–574

    Article  PubMed  Google Scholar 

  • Kumar A, Longino JT, Colwell RK, O’Donnell S (2009) Elevational patterns of diversity and abundance of eusocial paper wasps (Vespidae) in Costa Rica. Biotropica 41:338–346

    Article  Google Scholar 

  • Lessard J-P, Sackett TE, Reynolds WN, Fowler DA, Sanders NJ (2011) Determinants of the detrital arthropod community structure: the effects of temperature and resources along an environmental gradient. Oikos 320:333–343

    Article  Google Scholar 

  • Levy RA, Nufio CR (2015) Dispersal potential impacts size clines of grasshoppers across an elevation gradient. Oikos 124:610–619

    Article  Google Scholar 

  • Lövei GL, Sunderland KD (1996) Ecology and behaviour of ground beetles (Coleoptera: Carabidae). Annu Rev Entomol 41:231–256

    Article  PubMed  Google Scholar 

  • Ma M (2005) Species richness vs evenness: independent relationship and different responses to edaphic factors. Oikos 111:192–198

    Article  Google Scholar 

  • Malhi Y, Silman M, Salinas N, Bush M, Meier P, Saatchi S (2010) Introduction: elevation gradients in the tropics: laboratories for ecosystem ecology and global change research. Glob Change Biol 16:3171–3175

    Article  Google Scholar 

  • Marini L, Prosser F, Klimek S, Marrs RH (2008) Water-energy, land-cover, and heterogeneity drivers of the distribution of plant species richness in a mountain region of the European Alps. J Biogeogr 35:1826–1839

    Article  Google Scholar 

  • Marini L, Bommarco R, Fontana P, Battisti A (2010) Disentangling area and habitat diversity effects on orthopteran species with contrasting mobility. Biol Cons 143:2164–2171

    Article  Google Scholar 

  • Marini L, Bona E, Kunin WE, Gaston KJ (2011) Exploring anthropogenic and natural processes shaping fern species richness along elevational gradients. J Biogeogr 38:78–88

    Article  Google Scholar 

  • Marini L, Öckinger E, Bergman K-O, Jauker B, Krauss J, Kuussaari M, Pöyry J, Smith HG, Steffan-Dewenter I, Bommarco R (2014) Contrasting effects of habitat area and connectivity on evenness of pollinator communities. Ecography 37:544–551

    Article  Google Scholar 

  • Maunsell SC, Kitching RL, Burwell CJ, Morris RJ (2015) Changes in host-parasitoid food web structure with elevation. J Anim Ecol 84:353–363

    Article  PubMed  Google Scholar 

  • McCain CM (2009) Global analysis of bird elevational diversity. Glob Ecol Biogeogr 18:346–360

    Article  Google Scholar 

  • McCain CM, Grytnes J-A (2010) Elevational gradients in species richness. In: encyclopedia of life sciences (ELS). Wiley, Chichester

  • Merrill RM, Gutiérrez D, Lewis OT, Gutiérrez J, Díez SB, Wilson RJ (2008) Combined effects of climate and biotic interactions on the elevational range of a phytophagous insect. J Anim Ecol 77:145–155

    Article  PubMed  Google Scholar 

  • Mittelbach GG, Schemske DW, Cornell HV, Allen AP, Brown JM, Bush MB, Harrison SP, Hurlbert AH, Knowlton N, Lessios HA, McCain CM, McCune AR, McDade LA, McPeek MA, Near TJ, Price TD, Ricklefs RE, Roy K, Sax DF, Schluter D, Sobel JM, Turelli M (2007) Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. Ecol Lett 10(4):315–331

    Article  PubMed  Google Scholar 

  • Morris RJ, Sinclair F, Burwell CJ (2015) Food web structure changes with elevation but not rainforest strata. Ecography 38:792–802

    Article  Google Scholar 

  • Nieto-Sanchez S, Gutierrez D, Wilson RJ (2015) Long-term change and spatial variation in butterfly communities over an elevational gradient: driven by climate, buffered by habitat. Divers Distrib 21:950–961

    Article  Google Scholar 

  • O’Brien EM (2006) Biological relativity to water–energy dynamics. J Biogeogr 33:1868–1888

    Article  Google Scholar 

  • Pagliano G, Negrisolo E (2005) Fauna d’Italia. Hymenoptera Sphecidae. Edizioni Calderini, Bologna

    Google Scholar 

  • Pellissier L, Fiedler K, Ndribe C, Dubuis A, Pradervand J-N, Guisan A, Rasmann S (2012) Shifts in species richness, herbivore specialization, and plant resistance along elevation gradients. Ecol Evol 2:1818–1825

    Article  PubMed  PubMed Central  Google Scholar 

  • Péré C, Jactel H, Kenis M (2013) Response of insect parasitism to elevation depends on host and parasitoid life-history strategies. Biol Let 9:20130028

    Article  Google Scholar 

  • Peters MK, Hemp A, Appelhans T, Behler C, Classen A, Detsch F, Ensslin A, Ferger SW, Frederiksen SB, Gebert F, Haas M, Helbig-Bonitz M, Hemp C, Kindeketa WJ, Mwangomo E, Ngereza C, Otte I, Röder J, Rutten G, Schellenberger Costa D, Tardanico J, Zancolli G, Deckert J, Eardley CD, Peters RS, Rödel M-O, Schleuning M, Ssymank A, Kakengi V, Zhang J, Böhning-Gaese K, Brandl R, Kalko EKV, Kleyer M, Nauss T, Tschapka M, Fischer M, Steffan-Dewenter I (2016) Predictors of elevational biodiversity gradients change from single taxa to the multi-taxa community level. Nat Commun 7:13736

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, the R Development Core Team (2013) nlme: linear and nonlinear mixed effects models. R package version 3.1–111

  • Randall MGM (1982) The ectoparasitization of Coleophora alticolella (Lepidoptera) in relation to its altitudinal distribution. Ecol Entomol 7:117–185

    Article  Google Scholar 

  • Rényi A (1970) Probability theory. Akadémiai Kiadó, Budapest

    Google Scholar 

  • Romdal TS, Grytnes JA (2007) An indirect area effect on elevational species richness patterns. Ecography 30:440–448

    Article  Google Scholar 

  • Rotheray GE (1993) Colour guide to hoverfly larvae (Diptera, Syrphidae) in Britain and Europe. Dipterist Digest 9:156

    Google Scholar 

  • Sanders NJ, Lessard J-P, Fitzpatrick MC, Dunn RR (2007) Temperature, but not productivity or geometry, predicts elevational diversity gradients in ants across spatial grains. Glob Ecol Biogeogr 16:640–649

    Article  Google Scholar 

  • Smith B, Wilson JB (1996) A consumer’s guide to evenness indices. Oikos 76:70–82

    Article  Google Scholar 

  • Speight MCD (2014) Species accounts of European Syrphidae (Diptera). Syrph the Net, the database of European Syrphidae, vol 78. Syrph the Net publications, Dublin

    Google Scholar 

  • Steffan-Dewenter I, Tscharntke T (2002) Insect communities and biotic interactions on fragmented calcareous grasslands-a mini review. Biol Cons 104:275–284

    Article  Google Scholar 

  • Stein A, Gerstner K, Kreft H (2014) Environmental heterogeneity as a universal driver of species richness across taxa, biomes and spatial scales. Ecol Lett 17:866–880

    Article  PubMed  Google Scholar 

  • Stireman JO III, Dyer LA, Janzen DH, Singer MS, Lill JT, Marquis RJ, Ricklefs RE, Gentry G, Hallwachs W, Coley PD, Barone JA, Greemey HF, Connahs H, Barbosa P, Morais HC, Diniz IR (2005) Climatic unpredictability and parasitism of caterpillars: implications of global warming. Proc Natl Acad Sci 102:17384–17386

    Article  PubMed  CAS  Google Scholar 

  • Stireman JO III, O’Hara JE, Wood DM (2006) Behavior, ecology and evolution of tachinid parasitoids. Annu Rev Entomol 51:525–555

    Article  PubMed  CAS  Google Scholar 

  • Sundqvist MK, Sanders NJ, Wardle DA (2013) Community and ecosystem responses to elevational gradients: processes, mechanisms, and insights for global change. Annu Rev Ecol Evol Syst 44:261–280

    Article  Google Scholar 

  • R Development Core Team (2015) The R foundation for statistical computing, ver 3.0.2 Vienna University of Technology, Vienna. http://www.r-project.org

  • QGIS Development Team (2015) Quantum GIS geographic information system. Open Source Geospatial Foundation Project. http://qgis.osgeo.org

  • Tews J, Brose U, Grimm V, Tielbörger K, Wichmann MC, Schwager M, Jeltsch F (2004) Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. J Biogeogr 31:79–92

    Article  Google Scholar 

  • Thomson LJ, Macfadyen S, Hoffman AA (2010) Predicting the effects of climate change on natural enemies of agricultural pests. Biol Control 52:296–306

    Article  Google Scholar 

  • Tschorsnig HP (2017) Preliminary host catalogue of Palaearctic Tachinidae (Diptera). State Museum of Natural Science, Stuttgart. http://www.nadsdiptera.org/Tach/WorldTachs/CatPalHosts/Home.html. Accessed 16 May 2017

  • van Veen MP (2010) Hoverflies of Northwest Europe: identification keys to the Syrphidae. KNNV Publishing, Utrecht, p 254

    Book  Google Scholar 

  • Yang Z, Liu X, Zhou M, Ai D, Wang G, Wang Y, Chu C, Lundholm JT (2015) The effect of environmental heterogeneity on species richness depends on community position along the environmental gradient. Sci Rep 5:15723

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

We thank Dr. John O. Stireman (Wright State University, Dayton, OH) for his insightful comments and suggestions and for having linguistically revised the manuscript.

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DC, LM and PC designed the study. DC and LM performed the analyses. DC and GS performed the insect sampling. Species identifications were performed by PC (tachinids), MM (sphecids), DP (hoverflies), and AVT (ground beetles). DC drafted the manuscript, with contributions of LM and PC. All authors contributed to interpret the results and to finalize the manuscript. The final draft was approved by all authors.

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Correspondence to Daria Corcos.

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Communicated by Ingolf Steffan-Dewenter.

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Corcos, D., Cerretti, P., Mei, M. et al. Predator and parasitoid insects along elevational gradients: role of temperature and habitat diversity. Oecologia 188, 193–202 (2018). https://doi.org/10.1007/s00442-018-4169-4

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