Biological Invasions

, Volume 16, Issue 7, pp 1497–1514 | Cite as

Taxon specific response of carabids (Coleoptera, Carabidae) and other soil invertebrate taxa on invasive plant Amorpha fruticosa in wetlands

  • Andreja Brigić
  • Snježana Vujčić-Karlo
  • Renata Matoničkin Kepčija
  • Zvjezdana Stančić
  • Antun Alegro
  • Ivančica Ternjej
Original Paper


False indigo (Amorpha fruticosa L.) is an invasive exotic plant introduced to Europe in the early eighteenth century. Its spread has been rapid, particularly in disturbed wetland habitats, where it forms dense impermeable monospecific stands and modifies habitat conditions. The impact of A. fruticosa on native plant communities has been well analyzed, however knowledge concerning the possible effects on soil invertebrates and particularly carabid beetles is completely lacking. This study analyzed the impact of an A. fruticosa invasion on carabid beetles and other soil invertebrates. Soil fauna was sampled by pitfall traps at natural habitats, initially colonized by A. fruticosa, and habitats largely invaded by A. fruticosa. In total 2,613 carabid beetles belonging to 50 species and 72,166 soil invertebrates were collected. The invasion of A. fruticosa strongly affected the carabid beetle species composition, which clearly differed between all studied sites. Widespread euritopic carabid beetle species showed positive responses to A. fruticosa invasion, while the activity density of open habitat species strongly declined. Mean individual biomass was significantly higher at invaded sites due to increased incidence of large carabids (genus Carabus Linné, 1758). Carabid beetle activity density and abundance of soil invertebrates were considerably higher at invaded sites than in natural sites. Conversely, the impact of A. fruticosa on carabid beetle species richness and diversity was less pronounced, most likely due to immigration from adjacent habitats. Changes in carabid beetle species composition and abundance of soil invertebrates were most likely due to changes in vegetation structure and microclimate. The results suggest that A. fruticosa invasion considerably affected carabid beetles, an insect group that is only indirectly related to plant composition. Therefore, severe future changes can be expected in invertebrate groups that are closely related to plant composition, since A. fruticosa cannot be completely removed from the habitat and covers relatively large areas.


Non-native plants False indigo Diversity Microclimate Mean individual biomass 



First author would like to thank Dario Brigić and Stjepan Križanić for assistance during the field work. We thank anonymous referee for the comments on the paper.


  1. Allen ON, Allen EK (1981) The Leguminosae: a source book of characteristics, uses, and nodulation. WI University of Wisconsin Press, MadisonGoogle Scholar
  2. Anderson R, McFerran D, Cameron A (2000) The ground beetles of Northern Ireland. Ulster Museum, DublinGoogle Scholar
  3. Antolović J, Flajšman E, Frković A, Grgurev M, Grubešić M, Hamidović D, Holcer D, Pavlinić I, Tvrtković N, Vuković M (2006) Red book of mammals of Croatia. Ministry of Culture and State Institute for Nature Protection, ZagrebGoogle Scholar
  4. Braun-Blanquet J (1964) Pflanzensoziologie: Grundzüge der Vegetationskunde. Verlag Eugen Ulmer, WienCrossRefGoogle Scholar
  5. Bryan KM, Wratten SD (1984) The responses of polyphagous predators to spatial heterogeneity: aggregation by carabid and staphylinid beetles to their cereal aphid prey. Ecol Entomol 9:251–259CrossRefGoogle Scholar
  6. Cárdenas AM, Hidalgo JM (2007) Application of the mean individual biomass (MIB) of ground beetles (Coleoptera, Carabidae) to assess the recovery process of the Guadiamar Green Corridor (south Iberian Peninsula). Biodivers Conserv 16:4131–4146CrossRefGoogle Scholar
  7. Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-E, PlymouthGoogle Scholar
  8. Comandini F, Taglianti AV (1990) Ground beetle communities in a Mediterranean area (Tolfa Mountains, Central Italy). In: Stork NE (ed) The role of ground beetles in ecological and environmental studies. Intercept Ltd., Andover, pp 171–179Google Scholar
  9. D’Auria G, Zavagno F (1998) Alien plants and protected areas: synecology and dynamics of Amorpha fruticosa L. in the Po Valley (Northern Italy). Arch Geobot 4 (I):131–136Google Scholar
  10. de Groot M, Kleijn D, Jogan N (2007) Species groups occupying different trophic levels respond differently to the invasion of semi-natural vegetation by Solidago canadensis. Biol Conserv 136:612–617CrossRefGoogle Scholar
  11. de Vries HH (1994) Size of habitat and presence of ground beetle species. In: Desender K, Dufrêne M, Maelfait JP (eds) Carabid beetles—ecology and evolution. Kluwer Academic Publishers, Dordrecht, pp 253–259CrossRefGoogle Scholar
  12. DeHaan L, Ehlke N, Sheaffer C, Wyse D, DeHaan R (2006) Evaluation of diversity among North American accessions of false indigo (Amorpha fruticosa L.) for forage and biomass. Genet Resour Crop Evol 53:1463–1476CrossRefGoogle Scholar
  13. Den Boer PJ (1990) Density limits and survival of local populations in 64 carabid species with different powers of dispersal. J Evol Biol 3:19–48CrossRefGoogle Scholar
  14. Digweed SC, Currie CR, Cárcamo HA, Spence JR (1995) Digging out the digging-in effect of pitfall traps: influences of depletion and disturbance on catches of ground beetles (Coleoptera: Carabidae). Pedobiologia 39:561–576Google Scholar
  15. Dumitraşcu M, Grigorescu I, Kucsicsa G, Dragotă C-S, Năstase M (2011) Non-native and native invasive terrestrial plant species in Comana Natural Park. Case-studies: Amorpha fruticosa and Crataegus monogyna. Rom J Geogr 55:81–89Google Scholar
  16. Freude H, Harde K-W, Lohse GA, Klausnitzer B (2006) Die Käfer Mitteleuropas, Band 2 Adephaga 1: Carabidae (Laufkäfer). Spektrum Verlag, HeidelbergGoogle Scholar
  17. Giglio A, Giulianini PG, Zetto T, Talarico F (2011) Effects of the pesticide dimethoate on a non-target generalist carabid, Pterostichus melas italicus (Dejean, 1828) (Coleoptera: Carabidae). Ital J Zool 78(4):471–477CrossRefGoogle Scholar
  18. Greenslade PJM (1963) Further notes on aggregation in Carabidae (Coleoptera), with special references to Nebria brevicollis (F.). Entomol Mon Mag 99:109–114Google Scholar
  19. Herrera AM, Dudley TL (2003) Reduction of riparian arthropod abundance and diversity as a consequence of giant reed (Arundo donax) invasion. Biol Invasions 5:167–177CrossRefGoogle Scholar
  20. Honĕk A (1997) The effect of plant cover and weather on the activity density of ground surface arthropods in a fallow field. Entomol Res Org Agric 3:203–210Google Scholar
  21. Hore U, Uniyal VP (2008) Influence of space, vegetation structure, and microclimate on spider (Araneae) species composition in Terai Conservation Area, India. In: Nentwig W, Entling M, Kropf C (eds) Proceedings of the 24th European Congress of Arachnology, Bern, Natural Museum, pp 71–77Google Scholar
  22. Hornung E (2011) Evolutionary adaptation of oniscidean isopods to terrestrial life: structure, physiology and behaviour. Terr Arthropod Rev 4:95–130CrossRefGoogle Scholar
  23. Horvat I (1949) Nauka o biljnim zajednicama. Nakladni zavod Hrvatske, ZagrebGoogle Scholar
  24. Houlahan JF, Findlay CS (2004) Effect of invasive plant species on temperate wetland plant diversity. Conserv Biol 18:1132–1138CrossRefGoogle Scholar
  25. Hulina N (1998) Rare, endangered or vulnerable plants and neophytes in a drainage system in Croatia. Nat Croat 7:279–289Google Scholar
  26. Hulina N (2010) “Planta Hortifuga” in flora of the continental part of Croatia. Agric Conspec Sci 75:57–65Google Scholar
  27. Hůrka K (1996) Carabidae of the Czech and Slovak Republics. Kabourek, ZlínGoogle Scholar
  28. Huxley A (1992) The new RHS dictionary of gardening. MacMillian Press, New YorkGoogle Scholar
  29. Idžojtić M, Poljak I, Zebec M, Perić S (2009) Biological, morphological and ecological characteristics of indigobush (Amorpha fruticosa L.). In: Krpan APB (ed) Biological-ecological and energetic characteristics of indigobush (Amorpha fruticosa L.) in Croatia. Book of abstracts, Forest Research Institute, Croatian Forests, Croatian Chamber of Forestry and Wood Technology Engineers, Zagreb pp 39Google Scholar
  30. Jaenike J (1990) Host specialization in phytophagous insects. Annu Rev Ecol Syst 21:243–273CrossRefGoogle Scholar
  31. Kegel B (1990) Diurnal activity of carabid beetles living on arable land. In: Stork NE (ed) The role of ground beetles in ecological and environmental studies. Intercept Ltd., Andover, pp 66–76Google Scholar
  32. Koivula M, Kukkonen J, Niemelä J (2002) Boreal carabid-beetle (Coleoptera, Carabidae) assemblages along the clear-cut originated succession gradient. Biodivers Conserv 11:1269–1288CrossRefGoogle Scholar
  33. Kovačić D (1999) Spoonbill Colony Krapje Đol; JUPP. Lonjsko Polje report, JasenovacGoogle Scholar
  34. Križanić A (2002) The ground beetles (Coleoptera, Carabidae) of the Krapje Đol Ornithological Reserve. Diploma thesis, University of ZagrebGoogle Scholar
  35. Krpan APB (ed) (2009) Biological-ecological and energetic characteristics of indigobush (Amorpha fruticosa L.) in Croatia. Book of abstracts, Forest Research Institute, Croatian Forests, Croatian Chamber of Forestry and Wood Technology Engineers, ZagrebGoogle Scholar
  36. Krpan APB, Tomašić Ž, Bašić Palković P (2011) Biopotencijal amorfe (Amorpha fruticosa L.)—druga godina istraživanja. Šumarski List 135:103–113Google Scholar
  37. Lindroth CH (1992) Ground beetles (Carabidae) of Fennoscandia: a zoogeographic study. Specific knowledge regarding the species. Part 1. Smithsonian Institution Libraries and the National Science Foundation, Washington DCGoogle Scholar
  38. Liović B, Halambek M (1988) Weed control of indigobush (Amorpha fruticosa L.). Radovi 75:141–145Google Scholar
  39. Litt AR, Steidl RJ (2010) Insect assemblages change along a gradient of invasion by a non-native grass. Biol Invasions 12:3449–3463CrossRefGoogle Scholar
  40. Löbl I, Smetana A (eds) (2003) Catalogue of Palaearctic Coleoptera, vol 1. Apollo Books, StenstrupGoogle Scholar
  41. Lövei GL, Sunderland KD (1996) Ecology and behavior of ground beetles (Coleoptera: Carabidae). Annu Rev Entomol 41:231–256PubMedCrossRefGoogle Scholar
  42. Maelfait JP, Desender K (1990) Possibilities of short-term carabid sampling for site assessment studies. In: Stork NE (ed) The role of ground beetles in ecological and environmental studies. Intercept Ltd., Andower, pp 217–225Google Scholar
  43. Magura T, Elek Z, Tóthmérész B (2002) Impacts of non-native spruce reforestation on ground beetles. Eur J Soil Biol 38:291–295CrossRefGoogle Scholar
  44. McGeoch MA, Chown SL (1998) Scaling up the value of bioindicators. Trends Ecol Evol 13:46–47PubMedCrossRefGoogle Scholar
  45. Morecroft MD, Taylor ME, Oliver HR (1998) Air and soil microclimates of deciduous woodland compared to an open site. Agric For Meteorol 90:141–156CrossRefGoogle Scholar
  46. Mršić N (1997) Živali naših tal, Uvod v pedozoologijo—sistematika in ekologija s splošnim pregledom talnih živali. Tehnička založba Slovenije, LjubljanaGoogle Scholar
  47. Niemelä J, Haila Y, Punttila P (1996) The importance of small-scale heterogeneity in boreal forests: variation in diversity in forest-floor invertebrates across the succession gradient. Ecography 19:352–368CrossRefGoogle Scholar
  48. Novak N, Kravarščan M (2011) Invazivne strane korovne vrste u Republici Hrvatskoj. Hrvatski centar za poljoprivredu, hranu i selo, ZagrebGoogle Scholar
  49. Pedaschenko HP, Apostolova II, Vassilev KV (2012) Amorpha fruticosa invasibility of different habitats in lower Danube. Phytol Balcan 18:285–291Google Scholar
  50. Pétillon J, Ysnel F, Canard A, Lefeuvre J-C (2005) Impact of an invasive plant (Elymus athericus) on the conservation value of tidal salt marshes in western France and implications for management: response of spider populations. Biol Consev 126:103–117CrossRefGoogle Scholar
  51. Radović D, Kralj J, Tutiš V, Ćiković D (2003) Red data book of birds of Croatia. Ministry of Environmental and Physical Planning, ZagrebGoogle Scholar
  52. Radović A, Mikulić K, Vasilik Ž, Budinski I, Jelaska SD (2012) The impact of invasive species Amorpha fruticosa on the structure of bird communities in agricultural areas in the “Lonjsko polje” Nature Park. In: Jelaska SD, Klobučar GIV, Šerić Jelaska L, Leljak Levanić D, Lukša Ž (eds) 11th Croatian biological congress with international participation. Book of abstracts, Croatian biological society, Zagreb, pp 224–225Google Scholar
  53. Rainio J, Niemelä J (2003) Ground beetles (Coleoptera: Carabidae) as bioindicators. Biodivers Conserv 12:487–506CrossRefGoogle Scholar
  54. Ravenga C, Brunner J, Henninger N, Kassem K, Payne R (2000) Pilot analysis of global ecosystems: wetland ecosystems. World Resources Institute, Washington, DCGoogle Scholar
  55. Samways MJ, Caldwell PM, Osborn R (1996) Ground-living invertebrate assemblages in native, planted and invasive vegetation in South Africa. Agric Ecosyst Environ 59:19–32CrossRefGoogle Scholar
  56. Sărăţeanu V (2010) Assessing the influence of Amorpha fruticosa L. invasive shrub species on some grassland vegetation types from Western Romania. Res J Agric Sci 42:536–540Google Scholar
  57. Schirmel J, Timler L, Buchholz S (2010) Impact of the invasive moss Campylopus introflexus on carabid beetles (Coleoptera: Carabidae) and spiders (Araneae) in acidic coastal dunes at the southern Baltic Sea. Biol Invasions 13:605–620CrossRefGoogle Scholar
  58. Schmidt L (1970) Tablice za determinaciju Insekata, Priručnik za agronome, šumare i biologe. Sveučilište u Zagrebu, ZagrebGoogle Scholar
  59. Schneider-Jacoby M (2005) The Sava and Drava floodplains: threatened ecosystems of international importance. Arch Hydrobiol (Supplement band: Large rivers) 16:249–288Google Scholar
  60. Schneider-Jacoby M, Ern H (1993) The Lonjsko Polje Nature Park—diversity caused by floods. Croatian Ecological Society, ZagrebGoogle Scholar
  61. Schnitzler A, Hale BW, Alsum EM (2007) Examining native and exotic species diversity in European riparian forests. Biol Conserv 138:146–156CrossRefGoogle Scholar
  62. Schwerk A, Szyszko J (2007) Increase of Mean Individual Biomass (MIB) of Carabidae (Coleoptera) in relation to succession in forest habitats. Wiad Entomol 26:195–206Google Scholar
  63. Schwerk A, Szyszko J (2008) Patterns of succession and conservation value of post-industrial areas in central Poland based on carabid fauna (Coleoptera, Carabidae). In: Penev L, Erwin T, Assmann T (eds) Back to the roots and back to the future. Towards a new synthesis between taxonomic, ecological and biogeographical approaches in carabidology. Proceedings of the XIII European Carabidologist Meeting, Pensoft Publishers, Blagoevgrad, pp 469–482Google Scholar
  64. Seibold S, Fischer A (2013) Suppression of alien invasive species by traditional land use forms: Amorpha fruticosa L. in the Croatian nature park Lonjsko Polje. Sauteria 20:265–276Google Scholar
  65. Stančić Z (2007) Final report of the projects ‘Neophytic species of vascular flora in Croatia’ and ‘Habitats of neophytic species of vascular flora in Croatia’. State Institute for Nature Protection, ZagrebGoogle Scholar
  66. StatSoft Inc. (2010) Statistica (Date Analysis Software System), Version 10.
  67. Škorić A (1982) Manual for pedological investigations. Faculty of Agriculture, ZagrebGoogle Scholar
  68. Szentesi A (1999) Predispersal seed predation of the introduced false indigo, Amorpha fruticosa L. in Hungary. Acta Zool Acad Sci Hung 45:125–141Google Scholar
  69. Szigetvári CS (2002) Initial steps in the regeneration of a floodplain meadow after a decade of dominance of an invasive transformer shrub, Amorpha fruticosa L. Tiscia 33:67–77Google Scholar
  70. Szyszko J (1983) Methods of macrofauna investigations. In: Szujecki A, Szyzsko J, Mazurs S, Perliñski S (eds) The process of forest soil macrofauna formation after afforestation of farmland. Warsaw Agricultural University Press, Warsaw, pp 10–16Google Scholar
  71. Szyszko J (1990) Planning of prophylaxis in threatened pine forest biocenoses based on an analysis of the fauna of epigeic Carabidae. Warsaw Agricultural University Press, WarsawGoogle Scholar
  72. Szyszko J, Vermeulen HJW, Klimaszewski K, Abs M, Schwerk A (2000) Mean individual biomass (MIB) of ground beetles (Carabidae) as an indicator of the state of the environment. In: Brandmayr P, Lövei G, Zetto Brandmayr T, Casale A, Vigna Taglianti A (eds) Natural history and applied ecology of carabid beetles. Pensoft Publishers, Sofia, Moscow, pp 289–294Google Scholar
  73. Takagi K, Hioki Y (2012) Autoecology, distributional expansion and negative effects of Amorpha fruticosa L. on a river ecosystem: a case study in the Sendaigawa River, Tottori Prefecture. Landscape Ecol Eng 9:175–188CrossRefGoogle Scholar
  74. Tallamy DW (2004) Do alien plants reduce insect biomass? Conserv Biol 18:1689–1692CrossRefGoogle Scholar
  75. Thiele HU (1977) Carabid beetles in their environments. A study on habitat selection by adaptation in physiology and behaviour, Zoophysiology and Ecology 10. Springer, BerlinGoogle Scholar
  76. Thomas CFG, Parkinson L, Marshall EJP (1998) Isolating the components of activity-density for the carabid beetle Pterostichus melanarius in farmland. Oecologia 116:103–112CrossRefGoogle Scholar
  77. Tockner K, Uehlinger U, Robinson CT (eds) (2009) Rivers of Europe. Academic Press, LondonGoogle Scholar
  78. Toft S, Bilde T (2002) Carabid diets and food value. In: Holland JM (ed) The agroecology of carabid beetles. Intercept Ltd., Andover, pp 81–110Google Scholar
  79. Topić J, Vuković N, Nikolić T (2010) Lonjsko Polje. In: Alegro A, Bogdanović S, Brana S, Jasprica N, Katalinić A, Kovačić S, Nikolić T, Milović M, Pandža M, Posavec-Vukelić V, Randić M, Ruščić M, Šegota V, Šincek D, Topić J, Vrbek M, Vuković N (eds) Botanically important areas in Croatia. Školska knjiga, Zagreb, pp 255–262Google Scholar
  80. Topp W, Kappes H, Rogers F (2008) Response of ground dwelling beetle (Coleoptera) assemblages to giant knotweed (Reynouria spp.) invasion. Biol Invasions 10:381–390CrossRefGoogle Scholar
  81. Trautner J, Geigenmüller K (1987) Tiger beetles and ground beetles, illustrated key to the Cicindelidae and Carabidae of Europe. Josef Margraf, AichtalGoogle Scholar
  82. Tucović A, Isajev V, Šijačić-Nikolić (2004) Secondary range and ecophysio-logical characteristics of Amorpha fruticosa L. in Serbia. B Fac Fore 89:223–230CrossRefGoogle Scholar
  83. Turin H, Penev I, Casale A (eds) (2003) The genus Carabus in Europe. Pensoft Publishers, Sofia, MoscowGoogle Scholar
  84. Tutin TG, Heywood VH, Burges NA, Moore DM, Valentine DH, Walters SM, Webb DA (eds) (1964–1980) Flora Europaea 1–5. Cambridge University Press, CambridgeGoogle Scholar
  85. Tutin TG, Burges NA, Chater AO, Edmondson JR, Heywood VH, Moore DM, Valentine DH, Walters SM, Webb DA (eds) (1993) Flora Europaea 1. Cambridge University Press, CambridgeGoogle Scholar
  86. Vujčić-Karlo S, Brigić A, Šerić-Jelaska L, Kokan B, Hrašovec B (2007) Red List of threatened carabid beetles of Croatia.
  87. Wachmann E, Platen R, Brandt D (1995) Laufkäfer—Beobachtung, Lebenweise. Naturbuch Verlag, AugsburgGoogle Scholar
  88. Wang ET, van Berkum P, Sui XH, Beyene D, Chen WX, Martinéz-Romero E (1999) Diversity of rhizobia associated with Amorpha fruticosa isolated from Chinese soils and description of Mesorhizobium amorphae sp. nov. Inter J Syst Bacteriol 49:51–65CrossRefGoogle Scholar
  89. Wardle DA (2002) Communities and ecosystems, linking the aboveground and belowground components. Princeton University Press, New JerseyGoogle Scholar
  90. Wolters V, Ekschmitt K (1997) Gastropods, isopods, diplopods, and chilopods: neglected groups of decomposer food web. In: Benckiser G (ed) Fauna in soil ecosystems: recycling processes, nutrient fluxes and agriculture production. Marcel Dekker Inc., New York, pp 279–281Google Scholar
  91. Zaninović K, Gajić-Čapka M, Perčec Tadić M, Vučetić M, Milković J, Bajić A, Cindrić K, Cvitan L, Katušin Z, Kaučić D, Likso T, Lončar E, Lončar Ž, Mihajlović D, Pandžić K, Patarčić M, Srnec L, Vučetić V (2008) Climate Atlas of Croatia: 1961–1990, 1971–2000. Meteorological and Hydrological Service of Croatia, ZagrebGoogle Scholar
  92. Zavagno F, D’Auria G (2001) Synecology and dynamics of Amorpha fruticosa communities in the Po plain (Italy). In: Brundu G, Brock J, Camarda I, Child L, Wade M (eds) Plant invasions: species ecology and ecosystem management. Backhuys, Leiden, pp 175–182Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Andreja Brigić
    • 1
  • Snježana Vujčić-Karlo
    • 2
  • Renata Matoničkin Kepčija
    • 1
  • Zvjezdana Stančić
    • 3
  • Antun Alegro
    • 4
  • Ivančica Ternjej
    • 1
  1. 1.Department of Zoology, Faculty of ScienceUniversity of ZagrebZagrebCroatia
  2. 2.Natural History DepartmentNational Museum ZadarZadarCroatia
  3. 3.Geotechnical FacultyUniversity of ZagrebVaraždinCroatia
  4. 4.Department of Botany, Faculty of ScienceUniversity of ZagrebZagrebCroatia

Personalised recommendations