Journal of Insect Conservation

, Volume 18, Issue 1, pp 85–98 | Cite as

Intra-annual variations in abundance and species composition of carabid beetles in a temperate forest in Northeast China

  • Xiaowei WangEmail author
  • Jörg Müller
  • Linli An
  • Lanzhu Ji
  • Yan Liu
  • Xugao Wang
  • Zhanqing Hao


In most habitats in temperate zones, species show clear intra-annual shifts in abundance and species composition. Here we aimed to present a comprehensive picture of community composition and seasonal dynamics of carabid beetles (Coleoptera: Carabidae) in broad-leaved Korean pine mixed forest in Northeast China, which harbors a large diversity. We sampled 23,336 individuals from 14 genera and 39 species with pitfall traps over more than 1 year in a 25-ha plot. The six most abundant species accounted for 76.65 % of all individuals. Species estimations for the 25 ha plot ranged from 40 to 45 species. Overall abundance, species diversity, community composition, and abundance of individual species varied seasonally. Most of the abundant species showed an activity pattern of single peak, and were most active between July and early September. Few species showed a bimodal seasonal activity pattern. Both temperature and precipitation significantly influenced the carabid community within a year. Hierarchical clustering indicated that carabid communities of ten consecutive sampling periods could be partitioned into three time-windows, respectively, corresponding with warm temperature-high rainfall season, warm temperature-low rainfall season, and cool and cold season. By using the extended method of indicator species analysis, 11 indicator species were identified for the three time-groups and their combinations, suggesting the existence of temporal niche partitioning among carabid species. We suggest that intra-annual patterns of carabid abundance and species composition can be explained by species responses to seasonal changes in hydrothermal conditions. Cost-effective sampling effort to assess native carabid diversity and assemblage was also discussed in this study.


Ground beetles Species richness estimators Sampling intensity Seasonality Population dynamics Surface fitting 



We gratefully acknowledge Prof. Hongbin Liang, Dr. Hongliang Shi and Dr. Yuki Imura for their assistance in carabid identifications. We are grateful to all of those who contributed to this study in the field, especially Mr. Luxin Zhao, Mr. Laibao Song and Mr. Xichang He. We also thank Prof. Shijie Han, the director of Changbai Mountain Forest Ecosystem Research Station, who provides meteorological observation data for this study. The authors would like to thank Dr. Qing-He Zhang for his help and good advices throughout this work. We thank Alison Cassidy at the University of British Columbia for her assistance with English language and grammatical editing of the manuscript. Partial funding support for this research was provided by the National Natural Science Foundation of China (Project Number 30970515), the Ministry of Science and Technology of China (2012BAD22B0401) and the Science and Technology Department of Liaoning Province (2012214001).


  1. Ahearn GA (1971) Ecological factors affecting population sampling of desert tenebrionid beetles. Am Midl Nat 86:385–406CrossRefGoogle Scholar
  2. Atlegrim O, Sjöberg K, Ball JP (1997) Forestry effects on a boreal ground beetle community in spring: selective logging and clear-cutting compared. Entomol Fenn 8:19–26Google Scholar
  3. Baars MA (1979) Catches in pitfall traps in relation to mean densities of carabid beetles. Oecologia 41:25–46CrossRefGoogle Scholar
  4. Boivin G, Hance T (2003) Ground beetle assemblages in cultivated organic soil and adjacent habitats: temporal dynamics of microspatial changes. Pedobiologia 47:193–202CrossRefGoogle Scholar
  5. Boonzaaier C, McGeoch MA, Parr CL (2007) Fine-scale temporal and spatial dynamics of epigaeic ants in Fynbos: sampling implications. Afr Entomol 15:1–11CrossRefGoogle Scholar
  6. Brose U, Martinez ND, Williams RJ (2003) Estimating species richness: sensitivity to sample coverage and insensitivity to spatial patterns. Ecology 84:2364–2377CrossRefGoogle Scholar
  7. Butterfield J (1996) Carabid life-cycle strategies and climate change: a study on an altitude transect. Ecol Entomol 21:9–16CrossRefGoogle Scholar
  8. Cartellieri M, Lövei GL (2003) Seasonal dynamics and reproductive phenology of ground beetles (Coleoptera, Carabidae) in fragments of native forest in the Manawatu, North Island, New Zealand. N Z J Zool 30:31–42CrossRefGoogle Scholar
  9. Colwell RK (2009) Biodiversity: concepts, patterns, and measurement. In: Levin SA, Carpenter SR, Godfray HCJ et al (eds) The Princeton guide to ecology. Princeton University Press, Princeton, pp 257–263Google Scholar
  10. Colwell RK, Coddington JA (1994) Estimating terrestrial biodiversity through extrapolation. Philos Trans R Soc Lond B Biol Sci 345:101–118PubMedCrossRefGoogle Scholar
  11. De Cáceres M, Legendre P (2009) Associations between species and groups of sites: indices and statistical inference. Ecology 90:3566–3574PubMedCrossRefGoogle Scholar
  12. De Cáceres M, Legendre P, Moretti M (2010) Improving indicator species analysis by combining groups of sites. Oikos 119:1674–1684CrossRefGoogle Scholar
  13. Dufrêne M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67:345–366Google Scholar
  14. Epstein ME, Kulman HM (1990) Habitat distribution and seasonal occurrence of carabid beetles in east-central Minnesota. Am Midl Nat 123:209–225CrossRefGoogle Scholar
  15. Fadl A, Purvis G (1998) Field observations on the lifecycles and seasonal activity patterns of temperate carabid beetles (Coleoptera: Carabidae) inhabiting arable land. Pedobiologia 42:171–183Google Scholar
  16. Fadl A, Purvis G, Towey K (1996) The effect of time of soil cultivation on the incidence of Pterostichus melanarius (Illig) (Coleoptera: Carabidae) in arable land in Ireland. Ann Zool Fenn 33:207–214Google Scholar
  17. Finch OD (2005) Evaluation of mature conifer plantations as secondary habitat for epigeic forest arthropods (Coleoptera: Carabidae; Araneae). For Ecol Manag 204:21–34CrossRefGoogle Scholar
  18. French BW, Elliott NC (1999) Temporal and spatial distribution of ground beetle (Coleoptera: Carabidae) assemblages in grasslands and adjacent wheat fields. Pedobiologia 43:73–84Google Scholar
  19. Gómez AD (2009) Environmental correlates of life history pattern in ground-beetles on Tenerife (Canary Islands). Acta Oecol 35:355–369CrossRefGoogle Scholar
  20. Guan DX, Wu JB, Yu GR, Sun XM, Zhao XS, Han SJ, Jin CJ (2005) Meteorological control on CO2 flux above broad-leaved Korean pine mixed forest in Changbai Mountains. Sci China D 48:116–122CrossRefGoogle Scholar
  21. Halsall NB, Wratten SD (1988) The efficiency of pitfall trapping for polyphagous predatory Carabidae. Ecol Entomol 13:293–299CrossRefGoogle Scholar
  22. Hao ZQ, Zhang J, Song B, Ye J, Li BH (2007) Vertical structure and spatial associations of dominant tree species in an old-growth temperate forest. For Ecol Manag 252:1–11CrossRefGoogle Scholar
  23. Holland JM, Luff ML (2000) The effects of agricultural practices on Carabidae in temperate agroecosystems. Integr Pest Manag Rev 5:109–129CrossRefGoogle Scholar
  24. Honek A (1997) The effect of temperature on the activity of Carabidae (Coleoptera) in a fallow field. Eur J Entomol 94:97–104Google Scholar
  25. Honek A, Martinkova Z, Jarosik V (2003) Ground beetles (Carabidae) as seed predators. Eur J Entomol 100:531–544CrossRefGoogle Scholar
  26. Huber C, Baumgarten M (2005) Early effects of forest regeneration with selective and small scale clear-cutting on ground beetles (Coleoptera, Carabidae) in a Norway spruce stand in Southern Bavaria (Höglwald). Biodivers Conserv 14:1989–2007CrossRefGoogle Scholar
  27. Hutchison MAS (2007) Seasonality and life histories of two endemic New Zealand carabid beetles (Coleoptera: Carabidae): Mecodema oconnori Broun and Megadromus capito (White). N Z J Zool 34:79–89CrossRefGoogle Scholar
  28. Huusela-Veistola E (1996) Effects of pesticide use and cultivation techniques on ground beetles (Col., Carabidae) in cereal fields. Ann Zool Fenn 33:197–205Google Scholar
  29. Jung J-K, Kim S-T, Lee S-Y, Park C-G, Park J-K, Lee J-H (2012) Community structure of ground beetles (Coleoptera: Carabidae) along an altitudinal gradient on Mt. Sobaeksan, Korea. J Asia Pac Entomol 15:487–494CrossRefGoogle Scholar
  30. Klimaszewski J, Langor DW, Work TT, Pelletier G, Hammond HEJ, Germain C (2005) The effects of patch harvesting and site preparation on ground beetles (Coleoptera, Carabidae) in yellow birch dominated forests of southeastern Quebec. Can J For Res 35:2616–2628CrossRefGoogle Scholar
  31. Koivula MJ (2011) Useful model organisms, indicators, or both? Ground beetles (Coleoptera, Carabidae) reflecting environmental conditions. Zookeys 100:287–317PubMedGoogle Scholar
  32. Kotze DJ, Brandmayr P, Casale A et al (2011) Forty years of carabid beetle research in Europe—from taxonomy, biology, ecology and population studies to bioindication, habitat assessment and conservation. Zookeys 100:55–148PubMedCrossRefGoogle Scholar
  33. Krasnov B, Ayal Y (1995) Seasonal changes in darkling beetle communities (Coleoptera: Tenebrionidae) in the Ramon erosion cirque, Negev Highlands, Israel. J Arid Environ 31:335–347CrossRefGoogle Scholar
  34. Larsson SG (1939) Entwicklungstypen und Entwicklungszeiten der dänischen Carabiden. Entomol Medd 20:277–560Google Scholar
  35. Latty EF, Werner SM, Mladenoff DJ, Raffa KF, Sickley TA (2006) Response of ground beetle (Carabidae) assemblages to logging history in northern hardwood-hemlock forests. For Ecol Manag 222:335–347CrossRefGoogle Scholar
  36. Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280CrossRefGoogle Scholar
  37. Legendre P, Legendre L (2012) Numerical ecology, 3rd edn. Elsevier, AmsterdamGoogle Scholar
  38. Liebherr J, Mahar J (1979) The carabid fauna of the upland oak forest in Michigan: survey and analysis. Coleopt Bull 33:183–197Google Scholar
  39. Lopatina EB, Kipyatkov VE, Balashov SV, Kutcherov DA (2011) Photoperiod–temperature interaction—a new form of seasonal control of growth and development in insects and in particular a carabid beetle, Amara communis (Coleoptera: Carabidae). J Evol Biochem Physiol 47:578–592CrossRefGoogle Scholar
  40. Loreau M (1985) Annual activity and life cycles of carabid beetles in two forest communities. Holarct Ecol 8:228–235Google Scholar
  41. Loreau M (1988) Determinants of the seasonal pattern in the niche structure of a forest carabid community. Pedobiologia 31:75–87Google Scholar
  42. Lövei GL, Magura T (2011) Can carabidologists spot a pitfall? The non-equivalence of two components of sampling effort in pitfall-trapped ground beetles (Carabidae). Community Ecol 12:18–22CrossRefGoogle Scholar
  43. Lövei GL, Sunderland KD (1996) Ecology and behavior of ground beetles (Coleoptera: Carabidae). Annu Rev Entomol 41:231–256PubMedCrossRefGoogle Scholar
  44. Lundgren JG, Nichols S, Prischmann DA, Ellsbury MM (2009) Seasonal and diel activity patterns of generalist predators associated with Diabrotica virgifera immatures (Coleoptera: Chrysomelidae). Biocontrol Sci Technol 19:327–333CrossRefGoogle Scholar
  45. Lys JA, Nentwig W (1991) Surface activity of carabid beetles inhabiting cereal fields: seasonal phenology and the influence of farming operations on five abundant species. Pedobiologia 35:129–138Google Scholar
  46. Müller J, Goßner MM (2010) Three-dimensional partitioning of diversity informs state-wide strategies for the conservation of saproxylic beetles. Biol Conserv 143:625–633CrossRefGoogle Scholar
  47. Niemelä J, Haila Y, Halme E, Lahti T, Pajunen T, Punttila P (1988) The distribution of carabid beetles in fragments of old coniferous taiga and adjacent managed forest. Ann Zool Fenn 25:107–119Google Scholar
  48. Niemelä J, Haila Y, Halme E, Pajunen T, Punttila P (1989) The annual activity cycle of carabid beetles in the southern Finnish taiga. Ann Zool Fenn 26:35–41Google Scholar
  49. Niemelä J, Spence JR, Spence DH (1992) Habitat associations and seasonal activity of ground-beetles (Coleoptera, Carabidae) in central Alberta. Can Entomol 124:521–540CrossRefGoogle Scholar
  50. Niemelä J, Spence JR, Carcamo H (1997) Establishment and interactions of carabid populations: an experiment with native and introduced species. Ecography 20:643–652CrossRefGoogle Scholar
  51. Obrtel R (1971) Number of pitfall traps in relation to the structure of the catch of soil surface Coleoptera. Acta Entomol Bohemoslov 68:300–309Google Scholar
  52. Oksanen J, Blanchet FG, Kindt R et al (2011) Vegan: community ecology package. R package version 2.0-2Google Scholar
  53. Paarmann W (1990) Poecilus lepidus Leske (Carabidae, Coleoptera), a species with the ability to be a spring and autumn breeder. In: Stork NE (ed) The role of ground beetles in ecological and environmental studies. Intercept Publishers, Andover, pp 259–267Google Scholar
  54. Paarmann W, Stork NE (1987) Seasonality of ground beetles (Coleoptera: Carabidae) in the rain forests on N. Sulawesi (Indonesia). Int J Trop Insect Sci 8:483–487CrossRefGoogle Scholar
  55. Paill W (2004) Slug feeding in the carabid beetle Pterostichus melanarius: seasonality and dependence on prey size. J Molluscan Stud 70:203–205CrossRefGoogle Scholar
  56. Pullen AJ, Jepson PC, Sotherton NW (1992) Terrestrial non-target invertebrates and the autumn application of synthetic pyrethroids: experimental methodology and the trade-off between replication and plot size. Arch Environ Contam Toxicol 23:246–258CrossRefGoogle Scholar
  57. R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0.
  58. Rainio J, Niemelä J (2003) Ground beetles (Coleoptera: Carabidae) as bioindicators. Biodivers Conserv 12:487–506CrossRefGoogle Scholar
  59. Refseth D (1980) Differences in seasonal activity pattern and breeding time of Patrobus atrorufus (Carabidae) in central Norway. Holarct Ecol 3:87–90Google Scholar
  60. Riley KN, Browne RA (2011) Changes in ground beetle diversity and community composition in age structured forests (Coleoptera, Carabidae). Zookeys 147:601–621PubMedCrossRefGoogle Scholar
  61. Saska P, Martinkova Z, Honek A (2010) Temperature and rate of seed consumption by ground beetles (Carabidae). Biol Control 52:91–95CrossRefGoogle Scholar
  62. Schuldt A, Wang ZH, Zhou HZ, Assmann T (2009) Integrating highly diverse invertebrates into broad-scale analyses of cross-taxon congruence across the Palaearctic. Ecography 32:1019–1030CrossRefGoogle Scholar
  63. Schultz TD (1989) Habitat preferences and seasonal abundances of eight sympatric species of tiger beetle, Genus Cicindela (Coleoptera: Cicindelidae), in Bastrop State Park, Texas. Southwest Nat 34:468–477CrossRefGoogle Scholar
  64. Sota T (1996) Altitudinal variation in life cycles of carabid beetles: life-cycle strategy and colonization in alpine zones. Arct Antarct Alp Res 28:441–447CrossRefGoogle Scholar
  65. Suenaga H, Hamamura T (2001) Occurrence of carabid beetles (Coleoptera: Carabidae) in cabbage fields and their possible impact on lepidopteran pests. Appl Entomol Zool 36:151–160CrossRefGoogle Scholar
  66. Tauber CA, Tauber MJ (1981) Insect seasonal cycles: genetics and evolution. Annu Rev Ecol Syst 12:281–308CrossRefGoogle Scholar
  67. Tauber MJ, Tauber CA, Masaki S (1986) Seasonal adaptations of insects. Oxford University Press, OxfordGoogle Scholar
  68. Tauber MJ, Tauber CA, Nyrop JP, Villani MG (1998) Moisture, a vital but neglected factor in the seasonal ecology of insects: hypotheses and tests of mechanisms. Environ Entomol 27:523–530Google Scholar
  69. Thiele HU (1969) The control of larval hibernation and of adult aestivation in the carabid beetles Nebria brevicollis F. and Patrobus atrorufus stroem. Oecologia 2:347–361CrossRefGoogle Scholar
  70. Thiele HU (1977) Carabid beetles in their environments—a study on habitat selection by adaptations in physiology and behaviour. Springer, BerlinCrossRefGoogle Scholar
  71. Traugott M (1998) Larval and adult species composition, phenology and life cycles of carabid beetles (Coleoptera: Carabidae) in an organic potato field. Eur J Soil Biol 34:189–197CrossRefGoogle Scholar
  72. Wallin H (1989) The influence of different age classes on the seasonal activity and reproduction of four medium-sized carabid species inhabiting cereal fields. Holarct Ecol 12:201–212Google Scholar
  73. Werner SM, Raffa KF (2003) Seasonal activity of adult, ground-occurring beetles (Coleoptera) in forests of northeastern Wisconsin and the Upper Peninsula of Michigan. Am Midl Nat 149:121–133CrossRefGoogle Scholar
  74. Whicker AD, Tracy CR (1987) Tenebrionid beetles in the shortgrass prairie: daily and seasonal patterns of activity and temperature. Ecol Entomol 12:97–108CrossRefGoogle Scholar
  75. Wolda H (1988) Insect seasonality: why? Annu Rev Ecol Syst 19:1–18Google Scholar
  76. Woodcock BA (2005) Pitfall trapping in ecological studies. In: Leather SR (ed) Insect sampling in forest ecosystems. Blackwell, Oxford, pp 37–57CrossRefGoogle Scholar
  77. Yu X, Luo T, Zhou H (2006) Habitat associations and seasonal activity of carabid beetles (Coleoptera: Carabidae) in Dongling Mountain, North China. Entomol Fenn 17:174–183Google Scholar
  78. Zou Y, Sang W, Zhou H, Huang L, Axmacher JC (2013) Altitudinal diversity patterns of ground beetles (Coleoptera: Carabidae) in the forests of Changbai Mountain, Northeast China. Insect Conserv Divers. doi: 10.1111/icad.12039

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Xiaowei Wang
    • 1
    Email author
  • Jörg Müller
    • 2
    • 3
  • Linli An
    • 1
    • 4
  • Lanzhu Ji
    • 1
  • Yan Liu
    • 1
  • Xugao Wang
    • 1
  • Zhanqing Hao
    • 1
  1. 1.Institute of Applied EcologyChinese Academy of SciencesShenyangChina
  2. 2.Bavarian Forest National ParkGrafenauGermany
  3. 3.Chair for Terrestrial Ecology, Department of Ecology and Ecosystem Management, Center for Life and Food Sciences WeihenstephanTechnische Universität München FreisingFreisingGermany
  4. 4.Shenyang Institute of TechnologyFushunChina

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