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Phenological changes of the most commonly sampled ground beetle (Coleoptera: Carabidae) species in the UK environmental change network

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Abstract

Despite the important roles ground beetles (Coleoptera: Carabidae) play in ecosystems, the highly valued ecosystem services they provide, and ample descriptive documentation of their phenology, the relative impact of various environmental factors on carabid phenology is not well studied. Using the long-term pitfall trap capture data from 12 terrestrial Environmental Change Network (ECN) sites from the UK, we examined how changing climate influenced the phenology of common carabids, and the role particular climate components had on phenological parameters. Of the 28 species included in the analyses, 19 showed earlier start of their activity. This advance was particularly pronounced in the spring, supporting the view that early phenophases have a greater tendency to change and these changes are more directly controlled by temperature than later ones. Autumn activity extended only a few cases, suggesting a photoperiod-driven start of hibernation. No association was found between life-history traits and the ability of species to change their phenology. Air temperatures between April and June were the most important factors determining the start of activity of each species, whilst late season precipitation hastened the cessation of activity. The balance between the advantages and disadvantages of changing phenology on various levels is likely to depend on the species and even on local environmental criteria. The substantially changing phenology of Carabidae may influence their function in ecosystems and the ecosystem services they provide.

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References

  • Ahas R (1999) Long-term phyto-, ornitho- and ichthyophenological time-series analyses in Estonia. Int J Biometeorol 42(3):119–123. https://doi.org/10.1007/s004840050094

    Article  Google Scholar 

  • Altermatt F (2010) Climatic warming increases voltinism in European butterflies and moths. Proc R Soc B Biol Sci 277(1685):1281–1287. https://doi.org/10.1098/rspb.2009.1910

    Article  Google Scholar 

  • Bale JS, Hayward SA (2010) Insect overwintering in a changing climate. J Exp Biol 213(6):980–994. https://doi.org/10.1242/jeb.037911

    Article  CAS  Google Scholar 

  • Bale JS, Masters GJ, Hodkinson ID, Awmack C, Bezemer TM, Brown VK, Butterfield J, Buse A, Coulson JC, Farrar J, Good JEG, Harrington R, Hartley S, Jones TH, Lindroth RL, Press MC, Symrnioudis I, Watt AD, Whittaker JB (2002) Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Glob Chang Biol 8(1):1–16. https://doi.org/10.1046/j.1365-2486.2002.00451.x

    Article  Google Scholar 

  • Bronaugh D, Werner A (2009) zyp: Zhang + Yue-Pilon trends package. http://www.r-project.org

  • Brooks DR, Bater JE, Clark SJ, Monteith DT, Andrews C, Corbett SJ, Beaumont DA, Chapman JW (2012) Large carabid beetle declines in a United Kingdom monitoring network increases evidence for a widespread loss in insect biodiversity. J Appl Ecol 49(5):1009–1019. https://doi.org/10.1111/j.1365-2664.2012.02194.x

    Article  Google Scholar 

  • Carmel Y, Kent R, Bar-Massada A, Blank L, Liberzon J, Nezer O, Sapir G, Federman R (2013) Trends in ecological research during the last three decades—a systematic review. PLoS One 8(4):e59813. https://doi.org/10.1371/journal.pone.0059813

    Article  CAS  Google Scholar 

  • Chapin FS, Zavaleta ES, Eviner VT et al (2000) Consequences of changing biodiversity. Nature 405(6783):234–242. https://doi.org/10.1038/35012241

    Article  CAS  Google Scholar 

  • Cleland EE, Chuine I, Menzel A et al (2007) Shifting plant phenology in response to global change. Trends Ecol Evol 22:357–365

    Article  Google Scholar 

  • Cole LJ, McCracken DI, Dennis P et al (2002) Relationships between agricultural management and ecological groups of ground beetles (Coleoptera: Carabidae) on Scottish farmland. Agric Ecosyst Environ 93(1-3):323–336. https://doi.org/10.1016/S0167-8809(01)00333-4

    Article  Google Scholar 

  • den Boer PJ (1985) Fluctuations of density and survival of carabid populations. Oecologia 67(3):322–330. https://doi.org/10.1007/BF00384936

    Article  Google Scholar 

  • Devictor V, Julliard R, Couvet D, Jiguet F (2008) Birds are tracking climate warming, but not fast enough. Proc R Soc B Biol Sci 275(1652):2743–2748. https://doi.org/10.1098/rspb.2008.0878

    Article  Google Scholar 

  • Dixon AFG (2003) Climate change and phenological asynchrony. Ecol Entomol 28(3):380–381. https://doi.org/10.1046/j.1365-2311.2003.00509.x

    Article  Google Scholar 

  • Easterling DR (2000) Climate extremes: observations, modeling, and impacts. Science 289:2068–2074

    Article  CAS  Google Scholar 

  • Ellwood ER, Diez JM, Ibáñez I, Primack RB, Kobori H, Higuchi H, Silander JA (2012) Disentangling the paradox of insect phenology: are temporal trends reflecting the response to warming? Oecologia 168(4):1161–1171. https://doi.org/10.1007/s00442-011-2160-4

    Article  Google Scholar 

  • Encinas-Viso F, Revilla TA, Etienne RS (2012) Phenology drives mutualistic network structure and diversity. Ecol Lett 15(3):198–208. https://doi.org/10.1111/j.1461-0248.2011.01726.x

    Article  Google Scholar 

  • Forrest JRK, Thomson JD (2011) An examination of synchrony between insect emergence and flowering in Rocky Mountain meadows. Ecol Monogr 81(3):469–491. https://doi.org/10.1890/10-1885.1

    Article  Google Scholar 

  • Graham-Taylor LG, Stubbs AE, Brooke MDL (2009) Changes in phenology of hoverflies in a central England garden. Insect Conserv Divers 2(1):29–35. https://doi.org/10.1111/j.1752-4598.2008.00034.x

    Article  Google Scholar 

  • Harada T, Nitta S, Ito K (2005) Photoperiodic changes according to global warming in wing-form determination and diapause induction of a water strider, Aquarius paludum (Heteroptera: Gerridae). Appl Entomol Zool 40(3):461–466. https://doi.org/10.1303/aez.2005.461

    Article  Google Scholar 

  • Hassall C, Thompson DJ, French GC, Harvey IF (2007) Historical changes in the phenology of British Odonata are related to climate. Glob Chang Biol 13(5):933–941. https://doi.org/10.1111/j.1365-2486.2007.01318.x

    Article  Google Scholar 

  • Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Statist 6:65–70

    Google Scholar 

  • Homburg K, Homburg N, Schäfer F, Schuldt A, Assmann T (2014) Carabids.org—a dynamic online database of ground beetle species traits (Coleoptera, Carabidae). Insect Conserv Divers 7(3):195–205. https://doi.org/10.1111/icad.12045

    Article  Google Scholar 

  • Hudson LN, Newbold T, Contu S, Hill SLL, Lysenko I, de Palma A, Phillips HRP, Alhusseini TI, Bedford FE, Bennett DJ, Booth H, Burton VJ, Chng CWT, Choimes A, Correia DLP, Day J, Echeverría-Londoño S, Emerson SR, Gao D, Garon M, Harrison MLK, Ingram DJ, Jung M, Kemp V, Kirkpatrick L, Martin CD, Pan Y, Pask-Hale GD, Pynegar EL, Robinson AN, Sanchez-Ortiz K, Senior RA, Simmons BI, White HJ, Zhang H, Aben J, Abrahamczyk S, Adum GB, Aguilar-Barquero V, Aizen MA, Albertos B, Alcala EL, del Mar Alguacil M, Alignier A, Ancrenaz M, Andersen AN, Arbeláez-Cortés E, Armbrecht I, Arroyo-Rodríguez V, Aumann T, Axmacher JC, Azhar B, Azpiroz AB, Baeten L, Bakayoko A, Báldi A, Banks JE, Baral SK, Barlow J, Barratt BIP, Barrico L, Bartolommei P, Barton DM, Basset Y, Batáry P, Bates AJ, Baur B, Bayne EM, Beja P, Benedick S, Berg Å, Bernard H, Berry NJ, Bhatt D, Bicknell JE, Bihn JH, Blake RJ, Bobo KS, Bóçon R, Boekhout T, Böhning-Gaese K, Bonham KJ, Borges PAV, Borges SH, Boutin C, Bouyer J, Bragagnolo C, Brandt JS, Brearley FQ, Brito I, Bros V, Brunet J, Buczkowski G, Buddle CM, Bugter R, Buscardo E, Buse J, Cabra-García J, Cáceres NC, Cagle NL, Calviño-Cancela M, Cameron SA, Cancello EM, Caparrós R, Cardoso P, Carpenter D, Carrijo TF, Carvalho AL, Cassano CR, Castro H, Castro-Luna AA, Rolando CB, Cerezo A, Chapman KA, Chauvat M, Christensen M, Clarke FM, Cleary DFR, Colombo G, Connop SP, Craig MD, Cruz-López L, Cunningham SA, D'Aniello B, D'Cruze N, da Silva PG, Dallimer M, Danquah E, Darvill B, Dauber J, Davis ALV, Dawson J, de Sassi C, de Thoisy B, Deheuvels O, Dejean A, Devineau JL, Diekötter T, Dolia JV, Domínguez E, Dominguez-Haydar Y, Dorn S, Draper I, Dreber N, Dumont B, Dures SG, Dynesius M, Edenius L, Eggleton P, Eigenbrod F, Elek Z, Entling MH, Esler KJ, de Lima RF, Faruk A, Farwig N, Fayle TM, Felicioli A, Felton AM, Fensham RJ, Fernandez IC, Ferreira CC, Ficetola GF, Fiera C, Filgueiras BKC, Fırıncıoğlu HK, Flaspohler D, Floren A, Fonte SJ, Fournier A, Fowler RE, Franzén M, Fraser LH, Fredriksson GM, Freire GB Jr, Frizzo TLM, Fukuda D, Furlani D, Gaigher R, Ganzhorn JU, García KP, Garcia-R JC, Garden JG, Garilleti R, Ge BM, Gendreau-Berthiaume B, Gerard PJ, Gheler-Costa C, Gilbert B, Giordani P, Giordano S, Golodets C, Gomes LGL, Gould RK, Goulson D, Gove AD, Granjon L, Grass I, Gray CL, Grogan J, Gu W, Guardiola M, Gunawardene NR, Gutierrez AG, Gutiérrez-Lamus DL, Haarmeyer DH, Hanley ME, Hanson T, Hashim NR, Hassan SN, Hatfield RG, Hawes JE, Hayward MW, Hébert C, Helden AJ, Henden JA, Henschel P, Hernández L, Herrera JP, Herrmann F, Herzog F, Higuera-Diaz D, Hilje B, Höfer H, Hoffmann A, Horgan FG, Hornung E, Horváth R, Hylander K, Isaacs-Cubides P, Ishida H, Ishitani M, Jacobs CT, Jaramillo VJ, Jauker B, Hernández FJ, Johnson MKF, Jolli V, Jonsell M, Juliani SN, Jung TS, Kapoor V, Kappes H, Kati V, Katovai E, Kellner K, Kessler M, Kirby KR, Kittle AM, Knight ME, Knop E, Kohler F, Koivula M, Kolb A, Kone M, Kőrösi Á, Krauss J, Kumar A, Kumar R, Kurz DJ, Kutt AS, Lachat T, Lantschner V, Lara F, Lasky JR, Latta SC, Laurance WF, Lavelle P, le Féon V, LeBuhn G, Légaré JP, Lehouck V, Lencinas MV, Lentini PE, Letcher SG, Li Q, Litchwark SA, Littlewood NA, Liu Y, Lo-Man-Hung N, López-Quintero CA, Louhaichi M, Lövei GL, Lucas-Borja ME, Luja VH, Luskin MS, MacSwiney G MC, Maeto K, Magura T, Mallari NA, Malone LA, Malonza PK, Malumbres-Olarte J, Mandujano S, Måren IE, Marin-Spiotta E, Marsh CJ, Marshall EJP, Martínez E, Martínez Pastur G, Moreno Mateos D, Mayfield MM, Mazimpaka V, McCarthy JL, McCarthy KP, McFrederick QS, McNamara S, Medina NG, Medina R, Mena JL, Mico E, Mikusinski G, Milder JC, Miller JR, Miranda-Esquivel DR, Moir ML, Morales CL, Muchane MN, Muchane M, Mudri-Stojnic S, Munira AN, Muoñz-Alonso A, Munyekenye BF, Naidoo R, Naithani A, Nakagawa M, Nakamura A, Nakashima Y, Naoe S, Nates-Parra G, Navarrete Gutierrez DA, Navarro-Iriarte L, Ndang'ang'a PK, Neuschulz EL, Ngai JT, Nicolas V, Nilsson SG, Noreika N, Norfolk O, Noriega JA, Norton DA, Nöske NM, Nowakowski AJ, Numa C, O'Dea N, O'Farrell PJ, Oduro W, Oertli S, Ofori-Boateng C, Oke CO, Oostra V, Osgathorpe LM, Otavo SE, Page NV, Paritsis J, Parra-H A, Parry L, Pe'er G, Pearman PB, Pelegrin N, Pélissier R, Peres CA, Peri PL, Persson AS, Petanidou T, Peters MK, Pethiyagoda RS, Phalan B, Philips TK, Pillsbury FC, Pincheira-Ulbrich J, Pineda E, Pino J, Pizarro-Araya J, Plumptre AJ, Poggio SL, Politi N, Pons P, Poveda K, Power EF, Presley SJ, Proença V, Quaranta M, Quintero C, Rader R, Ramesh BR, Ramirez-Pinilla MP, Ranganathan J, Rasmussen C, Redpath-Downing NA, Reid JL, Reis YT, Rey Benayas JM, Rey-Velasco JC, Reynolds C, Ribeiro DB, Richards MH, Richardson BA, Richardson MJ, Ríos RM, Robinson R, Robles CA, Römbke J, Romero-Duque LP, Rös M, Rosselli L, Rossiter SJ, Roth DS, Roulston T'H, Rousseau L, Rubio AV, Ruel JC, Sadler JP, Sáfián S, Saldaña-Vázquez RA, Sam K, Samnegård U, Santana J, Santos X, Savage J, Schellhorn NA, Schilthuizen M, Schmiedel U, Schmitt CB, Schon NL, Schüepp C, Schumann K, Schweiger O, Scott DM, Scott KA, Sedlock JL, Seefeldt SS, Shahabuddin G, Shannon G, Sheil D, Sheldon FH, Shochat E, Siebert SJ, Silva FAB, Simonetti JA, Slade EM, Smith J, Smith-Pardo AH, Sodhi NS, Somarriba EJ, Sosa RA, Soto Quiroga G, St-Laurent MH, Starzomski BM, Stefanescu C, Steffan-Dewenter I, Stouffer PC, Stout JC, Strauch AM, Struebig MJ, Su Z, Suarez-Rubio M, Sugiura S, Summerville KS, Sung YH, Sutrisno H, Svenning JC, Teder T, Threlfall CG, Tiitsaar A, Todd JH, Tonietto RK, Torre I, Tóthmérész B, Tscharntke T, Turner EC, Tylianakis JM, Uehara-Prado M, Urbina-Cardona N, Vallan D, Vanbergen AJ, Vasconcelos HL, Vassilev K, Verboven HAF, Verdasca MJ, Verdú JR, Vergara CH, Vergara PM, Verhulst J, Virgilio M, Vu LV, Waite EM, Walker TR, Wang HF, Wang Y, Watling JI, Weller B, Wells K, Westphal C, Wiafe ED, Williams CD, Willig MR, Woinarski JCZ, Wolf JHD, Wolters V, Woodcock BA, Wu J, Wunderle JM Jr, Yamaura Y, Yoshikura S, Yu DW, Zaitsev AS, Zeidler J, Zou F, Collen B, Ewers RM, Mace GM, Purves DW, Scharlemann JPW, Purvis A (2017) The database of the PREDICTS (projecting responses of ecological diversity in changing terrestrial systems) project. Ecol Evol 7(1):145–188. https://doi.org/10.1002/ece3.2579

    Article  Google Scholar 

  • Hůrka K (1996) Carabidae of the Czech and Slovak Republics. Kabourek, Zlín

  • Ibáñez I, Primack RB, Miller-Rushing AJ et al (2010) Forecasting phenology under global warming. Philos Trans R Soc Lond Ser B Biol Sci 365(1555):3247–3260. https://doi.org/10.1098/rstb.2010.0120

    Article  Google Scholar 

  • IPCC (2013) IPCC, 2013: climate change 2013: the physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovern-mental Panel on Climate Change. Cambridge University Press, Cambridge, United Kingdom

  • Jones T, Cresswell W (2010) The phenology mismatch hypothesis: are declines of migrant birds linked to uneven global climate change? J Anim Ecol 79(1):98–108. https://doi.org/10.1111/j.1365-2656.2009.01610.x

    Article  Google Scholar 

  • Jönsson AM, Appelberg G, Harding S, Bärring L (2009) Spatio-temporal impact of climate change on the activity and voltinism of the spruce bark beetle, Ips typographus. Glob Chang Biol 15(2):486–499. https://doi.org/10.1111/j.1365-2486.2008.01742.x

    Article  Google Scholar 

  • La Sorte FA, Lee TM, Wilman H, Jetz W (2009) Disparities between observed and predicted impacts of climate change on winter bird assemblages. Proc R Soc B Biol Sci 276(1670):3167–3174. https://doi.org/10.1098/rspb.2009.0162

    Article  Google Scholar 

  • Lindroth CH (1985) The Carabidae (Coleoptera) of Fennoscandia and Denmark. E.J. Brill, Leiden

    Google Scholar 

  • Lindroth CH (1986) The Carabidae (Coleoptera) of Fennoscandia and Denmark. E.J. Brill, Leiden

    Google Scholar 

  • Lövei GL (2008) Ecology and conservation biology of ground beetles (Coleoptera: Carabidae) in an age of increasing human dominance. Hungarian Academy of Sciences, Budapest

    Google Scholar 

  • Lövei GL, Magura T, Tóthmérész B, Ködöböcz V (2006) The influence of matrix and edges on species richness patterns of ground beetles (Coleoptera: Carabidae) in habitat islands. Glob Ecol Biogeogr 15(3):283–289. https://doi.org/10.1111/j.1466-8238.2005.00221.x

    Article  Google Scholar 

  • Lövei GL, Sunderland KD (1996) Ecology and behavior of ground beetles. Annu Rev Entomol 41(1):231–256. https://doi.org/10.1146/annurev.en.41.010196.001311

    Article  Google Scholar 

  • Luff ML, Turner J, Lindroth CH (2007) The Carabidae (ground beetles) of Britain and Ireland. Royal Entomological Society, St. Albans

    Google Scholar 

  • Magurran AE, Baillie SR, Buckland ST et al (2010) Long-term datasets in biodiversity research and monitoring: assessing change in ecological communities through time. Trends Ecol Evol 25:574–582

    Article  Google Scholar 

  • Matalin A V (2008) Evolution of biennial life cycles in ground beetles (Coleoptera, Carabidae) of the Western Palaearctic. In: Penev L, Erwin TL, Assmann T (eds) Back to the roots and back to the future. Towards a new synthesis amongst taxonomic, ecological and biogeographical approaches in Carabidology Proceedings of the XIII European Carabidologists Meeting, Blagoevgrad, August 20–24, 2007. Pensoft Publishers, Sofia–Moscow, pp 259–284

  • McKenzie SW, Hentley WT, Hails RS et al (2013) Global climate change and above- belowground insect herbivore interactions. Front Plant Sci 4:412

    Article  Google Scholar 

  • McLeod AI (2009) Kendall: Kendall rank correlation and Mann-Kendall trend test. http://cran.r-project.org/package=Kendall

  • Menéndez R (2007) How are insects responding to global warming? Tijdschr voor Entomol 150:355–365

    Google Scholar 

  • Moore JW, Schindler DE (2010) Spawning salmon and the phenology of emergence in stream insects. Proc R Soc B Biol Sci 277(1688):1695–1703. https://doi.org/10.1098/rspb.2009.2342

    Article  Google Scholar 

  • Musolin DL, Saulich a K (2012) Responses of insects to the current climate changes: from physiology and behavior to range shifts. Entomol Rev 92(7):715–740. https://doi.org/10.1134/S0013873812070019

    Article  Google Scholar 

  • Nakazawa T, Doi H (2012) A perspective on match/mismatch of phenology in community contexts. Oikos 121(4):489–495. https://doi.org/10.1111/j.1600-0706.2011.20171.x

    Article  Google Scholar 

  • Norling U (1984) Photoperiodic control of larval development in Leucorrhinia dubia (Vander Linden): a comparison between populations from northern and southern Sweden (Anisoptera: Libellulidae). Odonatologica 13:529–550

    Google Scholar 

  • Nylin S, Gotthard K (1998) Plasticity in life-history traits. Annu Rev Entomol 43(1):63–83. https://doi.org/10.1146/annurev.ento.43.1.63

    Article  CAS  Google Scholar 

  • Pakeman RJ, Stockan JA (2014) Drivers of carabid functional diversity: abiotic environment, plant functional traits, or plant functional diversity? Ecology 95(5):1213–1224. https://doi.org/10.1890/13-1059.1

    Article  Google Scholar 

  • Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37(1):637–669. https://doi.org/10.1146/annurev.ecolsys.37.091305.110100

    Article  Google Scholar 

  • Parmesan C, Ryrholm N, Stefanescu C, Hill JK, Thomas CD, Descimon H, Huntley B, Kaila L, Kullberg J, Tammaru T, Tennent WJ, Thomas JA, Warren M (1999) Poleward shifts in geographical ranges of butterfly species associated with regional warming. Nature 399(6736):579–583. https://doi.org/10.1038/21181

    Article  CAS  Google Scholar 

  • Pau S, Wolkovich EM, Cook BI, Davies TJ, Kraft NJB, Bolmgren K, Betancourt JL, Cleland EE (2011) Predicting phenology by integrating ecology, evolution and climate science. Glob Chang Biol 17(12):3633–3643. https://doi.org/10.1111/j.1365-2486.2011.02515.x

    Article  Google Scholar 

  • Paull SH, Johnson PTJ (2014) Experimental warming drives a seasonal shift in the timing of host-parasite dynamics with consequences for disease risk. Ecol Lett 17(4):445–453. https://doi.org/10.1111/ele.12244

    Article  Google Scholar 

  • Pearce-Higgins JW, Yalden DW, Whittingham MJ (2005) Warmer springs advance the breeding phenology of golden plovers Pluvialis apricaria and their prey (Tipulidae). Oecologia 143(3):470–476. https://doi.org/10.1007/s00442-004-1820-z

    Article  CAS  Google Scholar 

  • Petersen MK, Ekbom B, Ravn HP (1996) Temperature dependent winter survival of Bembidion lampros and Tachyporus hypnorum. J Insect Physiol 42(11-12):997–1005. https://doi.org/10.1016/S0022-1910(96)00072-8

    Article  CAS  Google Scholar 

  • Pozsgai G, Littlewood NA (2014) Ground beetle (Coleoptera: Carabidae) population declines and phenological changes: is there a connection? Ecol Indic 41:15–24. https://doi.org/10.1016/j.ecolind.2014.01.029

    Article  Google Scholar 

  • Pozsgai G, Littlewood NA (2011) Changes in the phenology of the ground beetle Pterostichus madidus (Fabricius, 1775). Insect Sci 18(4):462–472. https://doi.org/10.1111/j.1744-7917.2011.01416.x

    Article  Google Scholar 

  • R Core Team (2012) R: a language and environment for statistical computing. http://www.r-project.org/

  • Radchuk V, Turlure C, Schtickzelle N (2013) Each life stage matters: the importance of assessing the response to climate change over the complete life cycle in butterflies. J Anim Ecol 82(1):275–285. https://doi.org/10.1111/j.1365-2656.2012.02029.x

    Article  Google Scholar 

  • Rennie S, Adamson J, Anderson R, et al (2015a) UK environmental change network (ECN) carabid beetle data: 1992-2012. https://doi.org/10.5285/4c9613ce-de52-41b1-9fde-7c41f9199686

  • Rennie S, Adamson J, Anderson R, et al (2015b) UK Environmental Change Network (ECN) meteorology data: 1992-2012. https://doi.org/10.5285/e1d33b37-f1d4-4234-a0d5-8bf4e657f653

  • Ribera I, Foster GN, Downie ISIS et al (1999) A comparative study of the morphology and life traits of Scottish ground beetles (Coleoptera, Carabidae). Ann Zool Fennici 36:21–37

    Google Scholar 

  • Schaber J (2012) Pheno: auxiliary functions for phenological data analysis. https://cran.r-project.org/package=pheno

  • Searle KR, Blackwell A, Falconer D, Sullivan M, Butler A, Purse BV (2013) Identifying environmental drivers of insect phenology across space and time: Culicoides in Scotland as a case study. Bull Entomol Res 103(02):155–170. https://doi.org/10.1017/S0007485312000466

    Article  CAS  Google Scholar 

  • Sheridan JA, Bickford D (2011) Shrinking body size as an ecological response to climate change. Nat Clim Chang 1(8):401–406. https://doi.org/10.1038/nclimate1259

    Article  Google Scholar 

  • Singer MC, Parmesan C (2010) Phenological asynchrony between herbivorous insects and their hosts: signal of climate change or pre-existing adaptive strategy? Philos Trans R Soc Lond Ser B Biol Sci 365(1555):3161–3176. https://doi.org/10.1098/rstb.2010.0144

    Article  Google Scholar 

  • Skaug H, Fournier D, Bolker B, et al (2016) Generalized linear mixed models using “AD model builder.” https://cran.r-project.org/package=glmmADMB

  • Sokal RR, Rohlf FJ (1981) Biometry. W. H, Freeman, San Francisco

    Google Scholar 

  • Sota T (1994) Variation of carabid life cycles along climatic gradients: an adaptive perspective for life-history evolution under adverse conditions. In: Danks HV (ed) Insect life-cycle polymorphism. Springer Netherlands, Dordrecht, pp 91–112. https://doi.org/10.1007/978-94-017-1888-2_5

    Chapter  Google Scholar 

  • Sparks TH, Langowska A, Głazaczow A et al (2010) Advances in the timing of spring cleaning by the honeybee Apis mellifera in Poland. Ecol Entomol 35(6):788–791. https://doi.org/10.1111/j.1365-2311.2010.01226.x

    Article  Google Scholar 

  • Stefanescu C, Penuelas J, Filella I (2003) Effects of climatic change on the phenology of butterflies in the northwest Mediterranean Basin. Glob Chang Biol 9(10):1494–1506. https://doi.org/10.1046/j.1365-2486.2003.00682.x

    Article  Google Scholar 

  • Sykes JM, Lane AMJ (eds) (1996) The United Kingdom environmental change network: protocols for standard measurements at terrestrial sites. The Stationery Office, London

    Google Scholar 

  • Thiele H-U (1969) The control of larval hibernation and of adult aestivation in the Carabid beetles Nebria brevicollis F. and Patrobus atrorufus Stroem. Oecologia 2(4):347–361. https://doi.org/10.1007/BF00778991

    Article  Google Scholar 

  • Thiele HU (1977) Carabid beetles in their environments: a study on habitat selection by adaptations in physiology and behaviour. Springer, Berlin. https://doi.org/10.1007/978-3-642-81154-8

    Book  Google Scholar 

  • van Asch M, van Tienderen PH, Holleman LJM, Visser ME (2007) Predicting adaptation of phenology in response to climate change, an insect herbivore example. Glob Chang Biol 13(8):1596–1604. https://doi.org/10.1111/j.1365-2486.2007.01400.x

    Article  Google Scholar 

  • Visser ME (2008) Keeping up with a warming world; assessing the rate of adaptation to climate change. Proc R Soc B Biol Sci 275(1635):649–659. https://doi.org/10.1098/rspb.2007.0997

    Article  Google Scholar 

  • Walther G-R, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin JM, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416(6879):389–395. https://doi.org/10.1038/416389a

    Article  CAS  Google Scholar 

  • Zeigler S (2013) Predicting responses to climate change requires all life-history stages. J Anim Ecol 82(1):3–5. https://doi.org/10.1111/1365-2656.12032

    Article  Google Scholar 

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Acknowledgements

We thank the ECN Central Co-ordination Unit (CCU) at CEH Lancaster for providing the carabid and weather data, and the Scottish Government’s Rural and Environment Science and Analytical Services Division for funding. We are also grateful for Jenni Stockan and Gabor Lövei for their valuable comments and suggestions on the manuscript.

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  1. Gabor Pozsgai

    Present address: , Nagycsarit utca 36., Zalaegerszeg, 8900, Hungary

Authors and Affiliations

  1. The James Hutton Institute, Craigiebuckler, Aberdeen, AB15 8QH, UK

    Gabor Pozsgai, Nick A. Littlewood & Robin J. Pakeman

  2. The School of Biological Sciences, Zoology Building, University of Aberdeen, Tillydrone Avenue, Aberdeen, AB24 2TZ, UK

    Gabor Pozsgai, John Baird & Mark R. Young

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  1. Gabor Pozsgai
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  2. John Baird
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  3. Nick A. Littlewood
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Corresponding author

Correspondence to Gabor Pozsgai.

Electronic supplementary material

Supplementary Material 1

The complete list of assessed life-trait variables of all species included in the analysis. (PDF 97 kb)

Supplementary Material 2

Results of the phenological trend analysis for all species at all sites. Kendal’s taus, p-values and Sen’s slopes are listed, site abbreviations follow those in Table 1. and species abbreviations of those in Table 3. Phenological measures are abbreviated as Table 2. (PDF 378 kb)

Supplementary Material 3

Mean Sen’s slope and standard errors of changes in trait groups for each calculated phenological measures. Significant differences at a P < 0.05 and a P < 0.1 threshold are indicated with asterisks and crosses, respectively. Phenological measures are abbreviated as Table 2. (PDF 327 kb)

Supplementary Material 4

Results of the stepwise GLMM model. Intercept of the final model and most important variables included in the final model are listed. Abbreviated species names as in Table 3. (PDF 523 kb)

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Pozsgai, G., Baird, J., Littlewood, N.A. et al. Phenological changes of the most commonly sampled ground beetle (Coleoptera: Carabidae) species in the UK environmental change network. Int J Biometeorol 62, 1063–1074 (2018). https://doi.org/10.1007/s00484-018-1509-3

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  • DOI: https://doi.org/10.1007/s00484-018-1509-3

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