Eur. J. Entomol. 113: 587-600, 2016 | 10.14411/eje.2016.079

To fly or not to fly: Factors influencing the flight capacity of carabid beetles (Coleoptera: Carabidae)

Stephen VENN
Department of Environmental Sciences, P.O. Box 65 (Viikinkaari 2a), University of Helsinki, FI-00014, Finland; e-mail: stephen.venn@helsinki.fi

This review considers factors affecting the flight capacity of carabid beetles and the implications of flight for carabids. Studies from the Dutch polders in particular show that young populations of carabids consist predominantly of macropterous species and macropterous individuals of wing-dimorphic species. Also populations of wing-dimorphic carabid species at the periphery of their geographical range contain high proportions of macropterous individuals. However, studies from Baltic archipelagos show that older populations of even highly isolated island habitats contain considerable proportions of brachypterous species and individuals. This suggests that macroptery is primarily an adaptation for dispersal and that there exists a mechanism for subsequently reducing the ratio of macropterous to brachypterous species under stable conditions, due to the competitive advantage of brachyptery. Populations in isolated habitats, such as islands and mountains, have high proportions of brachypterous species. Many macropterous species do not possess functional flight muscles. Species of unstable habitats, such as tree canopies and wet habitats, are mostly macropterous. Brachypterous species tend to disappear from disturbed habitats. There is uncertainty regarding the extent to which carabid dispersal is directed and how much passive. Both Den Boer and Lindroth recognized that mostly macropterous individuals of macropterous and wing-dimorphic species disperse and found new populations, after which brachyptery tends to rapidly appear and proliferate in the newly founded population. It is most likely that the allele for brachyptery would arrive via the dispersal of gravid females which had mated with brachypterous males prior to emigration. Whilst many studies consider wing morphology traits of carabid beetles to be species-specific and permanent, a number of studies have shown that the oogenesis flight syndrome, whereby females undertake migration and subsequently lose their flight muscles by histolysis before eventually regenerating them after reproducing, has been reported for a growing number of carabid species. Wing morphology of carabid beetles clearly offers strong potential for the study of population dynamics. This field of study flourished during the 1940's to the late 1980's. Whilst a considerable amount of valuable research has been performed and published, the topic clearly holds considerable potential for future study.

Keywords: Coleoptera, Carabidae, aeroplankton, anemohydrochoric dispersal, autolysis, biogeography, brachyptery, colonization, dispersal, disturbance, flight muscle, flight wing, histolysis, macroptery, migration, oogenesis flight syndrome

Received: March 11, 2015; Accepted: December 2, 2015; Published online: December 30, 2016

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References

  1. Andersen N.M. 1973: Seasonal polymorphism and developmental changes in organs of flight and reproduction in bivoltine pondskaters (Hem. Gerridae). - Entomol. Scand. 4: 1-20. Go to original source...
  2. Andersen N.M. 2000: The evolution of dispersal dimorphism and other life history traits in water striders (Hem. Gerridae). - Entomol. Sci. 3: 187-199.
  3. Atkins M.D. & Harris S.H. 1962: A contribution to the knowledge of flight muscle changes in the Scolytidae (Coleoptera). - Can. Entomol. 94: 25-32. Go to original source...
  4. Aukema B. 1986: Winglength determination in relation to dispersal by flight in two wing dimorphic species of Calathus Bonelli (Coleoptera, Carabidae). In Den Boer P.J., Luff M.L., Mossakowski D. & Weber F. (eds): Carabid Beetles. Gustav Fischer, Stuttgart, pp. 91-99.
  5. Aukema B. 1991: Fecundity in relation to wing-morph of three closely related species of the melanocephalus group of the genus Calathus (Coleoptera: Carabidae). - Oecologia 87: 118-126. Go to original source...
  6. Aukema B. 1995: The evolutionary significance of wing dimorphism in carabid beetles (Coleoptera: Carabidae). - Res. Popul. Ecol. 37: 105-110. Go to original source...
  7. Ås S. 1984: To fly or not to fly? Colonization of Baltic islands by winged and wingless carabid beetles. - J. Biogeogr. 11: 413-426. Go to original source...
  8. Ås S., Bengtsson J. & Ebenhard T. 1997: Archipelagos and theories of insularity. - Ecol. Bull. 46: 88-116.
  9. Bonn A., Hagen K. & Reiche D.W.-v. 2002: The significance of flood regimes for carabid beetle and spider communities in riparian habitats - a comparison of three major rivers in Germany. - River Res. Appl. 18: 43-64. Go to original source...
  10. Brandmayr P. 1983: The main axes of the coenoclinal continuum from macroptery to brachyptery in carabid communities of the temperate zone Ecology of carabids: the synthesis of field study and laboratory experiment. The main axes of the coenoclinal continuum from macroptery to brachyptery in carabid communities of the temperate zone. In Brandmayr P., den Boer P.J. & Weber F. (eds): Ecology of Carabids: The Synthesis of Field Study and Laboratory Experiment. Report of the Fourth Meeting of European Carabidologists. PUDOC, Wageningen pp. 147-169.
  11. Carter A. 1976: Wing polymorphism in the insect species Agonum retractum Leconte (Coleoptera, Carabidae). - Can. J. Zool. 54: 1375-1382. Go to original source...
  12. Chapman J.W., Reynolds D.R., Smith A.D., Riley J.R., Telfer M.G. & Woiwood I.P. 2005: Mass aerial migration in the carabid beetle Notiophilus biguttatus. - Ecol. Entomol. 30: 264-272. Go to original source...
  13. Chapman, J., Reynolds, D. & Smith, A. 2010: Migratory and foraging movements in beneficial insects: A review of radar monitoring and tracking methods. - Int. J. Pest Manage. 50: 225-232. Go to original source...
  14. Chernov Y.I. & Makarova O.L. 2008: Beetles (Coleoptera) in High Arctic. In Penev L., Erwin T. & Assmann T. (eds): Back to the Roots and Back to the Future. Towards a Synthesis amongst Taxonomic, Ecological and Biogeographical Approaches in Carabidology. Proc. of the XIII European Carabidologists Meeting, Blagoevgrad, August 20-24, 2007. Pensoft, Sofia, pp. 213-246.
  15. Crespi B.J. 1988: Adaptation, compromise, and constraint: the development, morphometrics, and behavioural basis on a fighter-flier polymorphism in male Hoplothrips karnyi (Insecta: Thysanoptera). - Behav. Ecol. Sociobiol. 23: 93-104. Go to original source...
  16. Dacke M., Byrne M.J., Scholtz C.H. & Warrant E.J. 2004: Lunar orientation in a beetle. - Proc. R. Soc. Lond. (B) 271: 361-365. Go to original source...
  17. Darlington P.J. 1943: Carabidae of mountains and islands: data on the evolution of isolated faunas, and on atrophy of wings. - Ecol. Monogr. 13: 39-61. Go to original source...
  18. Darwin C. 1872: The Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life. 6th London ed. John Murray, London, 504 pp.
  19. De Kort C.A.D. 1969: Hormones and the structural and biochemical properties of the flight muscles in the Colorado beetle. - Med. Landb. Hogeschool 69: 1-63.
  20. Den Boer P.J. 1970: On the significance of dispersal power for populations of carabid beetles (Coleoptera, Carabidae). - Oecologia 4: 1-28. Go to original source...
  21. Den Boer P.J. 1971a: On the dispersal power of carabid beetles and its possible significance. In Den Boer P.J. (ed.): Dispersal and Dispersal Power of Carabid Beetles. - Miscellaneous Papers (Landbouwhogeschool, Wageningen) 8: 119-138.
  22. Den Boer P.J. (ed.) 1971b: Dispersal and Dispersal Power of Carabid Beetles. - Miscellaneous Papers (Landbouwhogeschool, Wageningen) 8: 1-151.
  23. Den Boer P.J. 1977: Dispersal power and survival. Carabids in a cultivated countryside. - Miscellaneous Papers (Landbouwhogeschool, Wageningen) 14: 1-190.
  24. Den Boer P.J., Van Huizen T.H.P., Den Boer-Daanje W., Aukema B. & Den Bieman C.F.M. 1980: Wing polymorphism and dimorphism in ground beetles as stages in an evolutionary process (Coleoptera: Carabidae). - Entomol. Gener. 6: 107-134.
  25. Denno R.F., Olmstead K.L. & McCloud E.S. 1989: Reproductive cost of flight capability: a comparison of life history traits in wing dimorphic planthoppers. - Ecol. Entomol. 14: 31-44. Go to original source...
  26. Denno R.F., Roderick G.K., Olmstead K.L. & Döbel H.G. 1991: Density-related migration in planthoppers (Homoptera: Delphacidae): the role of habitat persistence. - Am. Nat. 138: 1513-1541. Go to original source...
  27. Desender K. 1984: Evolutionary ecology of carabids in Galapagos. In Stork N. (ed.): The Role of Ground Beetles in Ecological and Environmental Studies. Intercept, Andover, pp. 13-20.
  28. Desender K. 1989a: [Dispersal forms in the ecology of carabid beetles (Coleoptera, Carabidae).] Doc. Trav. Inst. R. Sci. Nat. Belge (Gent) 54: 1-136 [in Dutch].
  29. Desender K. 1989b: Heritability of wing development and body size in a carabid beetle, Pogonus chalceus Marsham, and its evolutionary significance. - Oecologia 78: 513-520. Go to original source...
  30. Desender K. 2000: Flight muscle development and dispersal in the life history of carabid beetles: patterns and processes. - Bull. Inst. R. Sci. Nat. Belg. (Entomologie) 70: 13-31.
  31. Dingle H. 1974: The experimental analysis of migration and life-history strategies in insects. In Browne L.B. (ed.): Experimental Analysis of Insect Behaviour. Springer, Berlin, Heidelberg, New York, pp. 329-342.
  32. Feng H.Q., Zhang Y.H., Wu K.M., Cheng D.F. & Gou Y.-Y. 2007: Nocturnal windborne migration of ground beetles, particularly Pseudoophonus griseus (Coleoptera: Carabidae), in China. - Agric. Forest Entomol. 9: 103-113. Go to original source...
  33. Fujisaki K. 1992: A male fitness advantage to wing reduction in the oriental chinch bug, Calvelerius saccharivorus Okajima (Heteroptera: Lygaeidae). - Res. Popul. Ecol. 34: 173-183. Go to original source...
  34. Glick P.A. 1939: The Distribution of Insects, Spiders and Mites in the Air. U.S. Department of Agriculture, Technical Bulletins 673, Washington, 150 pp.
  35. Gobbi M., Caccianiga M., Cerabolini B., De Bernardi F., Luzzaro A. & Pierce S. 2010: Plant adaptive responses during primary succession are associated with functional adaptations in ground beetles on deglaciated terrain. - Commun. Ecol. 11: 223-231. Go to original source...
  36. Goodwyn P.P. & Fujisaki K. 2007: Sexual conflicts, loss of flight, and fitness gains in locomotion of polymorphic water striders. - Entomol. Exp. Appl. 124: 249-259. Go to original source...
  37. Gray J.S. 1989: Effects of environmental stress on species rich assemblages. - Biol. J. Linn. Soc. 37: 19-32. Go to original source...
  38. Haeck J. 1971: The immigration and settlement of carabids in the new Ijsselmeer-polders. In Den Boer P.J. (ed.): Dispersal and Dispersal Power of Carabid Beetles. - Miscellaneous Papers (Landbouwhogeschool, Wageningen) 8: 33-51.
  39. Homburg K., Homburg N., Schäfer F., Schuldt A. & Assmann T. 2013: Carabids.org - a dynamic online database of ground beetle species traits (Coleoptera, Carabidae). - Insect Conserv. Diver. 7: 195-205. Go to original source...
  40. Honek A. 1981: Wing polymorphism in Notiophilus biguttatus in Bohemia. - Vest. Cs. Spol. Zool. 45: 81-86.
  41. Ichikawa T. 1982: Density related changes in male-male competitive behavior in the rice brown planthopper, Nilarparvata lugens (Stal) (Homoptera: Delphacidae). - Appl. Entomol. Zool. 17: 439-452.
  42. Jackson D.J. 1928: The inheritance of long and short wings in the weevil, Sitona hispidula, with a discussion of wing reduction among beetles. - Trans. R. Soc. Edinburgh 55: 665-735. Go to original source...
  43. Jackson D.J. 1933: Observations on the flight muscles of Sitona weevils. - Ann. Appl. Biol. 20: 731-770. Go to original source...
  44. Johnson B. 1953: Flight muscle autolysis and reproduction in aphids. - Nature 4383: 813. Go to original source...
  45. Johnson C.G. 1969: Migration and Dispersal of Insects by Flight. Methuen, London 763 pp.
  46. Järvinen O. & Vepsälainen K. 1976: Wing dimorphism as an adaptive strategy in water-striders (Gerris). - Hereditas 84: 61-68. Go to original source...
  47. Kadar F. & Szentkiralyi F. 1997: Effects of climatic variations on long-term fluctuation patterns of ground beetles (Coleoptera, Carabidae) collected by light trapping in Hungary. - Acta Phytopathol. Entomol. Hungar. 32: 185-203.
  48. Kaitala A. & Dingle H. 1993: Wing dimorphism, territoriality and mating frequency of the water strider Aquarius remigis (Say). - Ann. Zool. Fenn. 30: 163-168.
  49. Kataev B.M. 2001: On some, mostly East European and Asian species of the genus Ophonus (Coleoptera: Carabidae). - Zoosyst. Rossica 99[2000]: 161-187.
  50. Kavanaugh D.H. 1985: On wing atrophy in carabid beetles (Coleoptera: Carabidae), with special reference to Nearctic Nebria. In Ball G.E. (ed.): Taxonomy, Phylogeny and Zoogeography of Beetles and Ants. A Volume Dedicated to the Memory of Philip Jackson Darlington, Jr. (1904-1983). Series Entomologica 33. Dr. W. Junk, Dordrecht, Boston, Lancaster, pp. 408-431.
  51. Kirschfeld K. 1988: Navigation and compass orientation by insects according to the polarization pattern of the sky. - Z. Naturforsch. (C) 43: 467-469.
  52. Kotze D.J. 2008: The occurrence and distribution of carabid beetles (Carabidae) on islands in the Baltic Sea: a review. - J. Insect Conserv. 12: 265-276. Go to original source...
  53. Kotze D.J. & O'Hara R.B. 2003: Species decline - but why? Explanations of carabid beetle (Coleoptera, Carabidae) declines in Europe. - Oecologia 135: 138-148. Go to original source...
  54. Langellotto G.A., Denno R.F. & Ott J.R. 2000: A trade-off between flight capability and reproduction in males of a wing-dimorphic insect. - Ecology 81: 865-875. Go to original source...
  55. Lindroth C.H. 1945: Die Fennoskandischen Carabidae. Eine tiergeographische Studie. I. Spezieller Teil. - Göteborgs Kungliga Vetenskaps- och Vitterhets-Samhälles Handlingar (B. 4): 1-709.
  56. Lindroth C.H. 1946: Inheritance of wing dimorphism in Pterostichus anthracinus Ill. - Hereditas 32: 37-40. Go to original source...
  57. Lindroth C.H. 1949: Die Fennoskandischen Carabidae. III. Allgemeiner Teil. - Göteborgs Kungliga Vetenskaps- och Vitterhets-Samhälles Handlingar (B. 4): 1-911.
  58. Lindroth C.H. 1953: Some attempts towards experimental zoogeography. - Ecology 34: 657-666. Go to original source...
  59. Lindroth C.H. 1969: The theory of glacial refugia in Scandinavia - comments on present opinions. - Notul. Entomol. 39: 178-192.
  60. Lindroth C.H. 1974: Handbooks for the Identification of British Insects. Vol. IV, Part 2. Royal Entomological Society, London, 148 pp.
  61. Lindroth C.H. 1985: The Carabidae (Coleoptera) of Fennoscandia and Denmark. Vol. 15, Part 1. Scandinavian Press, Leiden, 225 pp.
  62. Lindroth C.H. 1986: The Carabidae (Coleoptera) of Fennoscandia and Denmark. Vol. 15, Part 2. Scandinavian Press, Leiden, 497 pp.
  63. Lindroth C.H. 1992: Ground Beetles (Carabidae) of Fennoscandia - A Zoogeographic Study. Part III, General Analysis With a Discussion on Biogeographic Principles. Smithsonian Institute Libraries and The National Science Foundation, Washington D.C., 814 pp.
  64. MacArthur R.H. & Wilson E.O. 1967: The Theory of Island Biogeography. Princeton University Press, Princeton, 205 pp.
  65. Magura T., Lövei G. & Tóthmérész B. 2010: Does urbanization decrease diversity in ground beetle (Carabidae) assemblages? - Global Ecol. Biogeogr. 19: 16-26. Go to original source...
  66. Matalin A.V. 1994: The strategy of dispersal behaviour in some Carabidae species of southeastern Europe. In Desender K., Dufrêne M., Loreau M., Luff M.L. & Maelfait J.-P. (eds): Carabid Beetles - Ecology and Evolution. Kluwer Academic Publishers, Dordrecht, pp. 183-188.
  67. Matalin A.V. 1998: Influence of weather conditions on migratory activity of ground beetles (Coleoptera, Carabidae) in the steppe zone. - Biol. Bull. 25: 485-494.
  68. Matalin A.V. 2003: Variations in flight ability with sex and age in ground beetles (Coleoptera, Carabidae) of south-western Moldova. - Pedobiologia 47: 311-319. Go to original source...
  69. Matalin A.V. & Makarov K.V. 2008: Life cycles in the ground beetle tribe Pogonini (Coleoptera, Carabidae) from the Lake Elton region, Russia. In Penev L., Erwin T. & Assmann T. (eds): Back to the Roots and Back to the Future. Towards a Synthesis amongst Taxonomic, Ecological and Biogeographical Approaches in Carabidology. Proc. of the XIII European Carabidologists Meeting, Blagoevgrad, August 20-24, 2007. Pensoft, Sofia, pp. 305-338.
  70. Meijer J. 1974: A comparative study of the immigration of carabids (Coleoptera, Carabidae) into a new polder. - Oecologia 16: 185-208. Go to original source...
  71. Midtgaard F. 1999: Is dispersal density-dependent in carabid beetles? A field experiment with Harpalus rufipes (Degeer) and Pterostichus niger (Schaller) (Col., Carabidae). - J. Appl. Entomol. 123: 9-12. Go to original source...
  72. Nilsson A.N., Pettersson R.B. & Lemdahl G. 1993: Macroptery in altitudinal specialists versus brachyptery in generalists - a paradox of alpine Scandinavian carabid beetles (Coleoptera: Carabidae). - J. Biogeogr. 20: 227-234. Go to original source...
  73. Novotny V. 1995: Adaptive significance of wing dimorphism in males of Nilaparvata lugens. - Entomol. Exp. Appl. 76: 233-239. Go to original source...
  74. Ott J.R. 1994: An ecological framework for the study of planthopper mating systems. In Denno R.F. & Perfect T.J. (eds): Planthoppers: Their Ecology and Management. Chapman and Hall, New York, pp. 234-254.
  75. Paarmann W. 1966: Vergleichende Untersuchungen über die Bindung zweier Carabidenarten (Pterostichus angustatus Dft. und P. oblongopunctatus F.) an ihre verschiedenen Lebensträume. - Z. Wiss. Zool. 174: 83-176.
  76. Palmén E. 1944: Die anemohydrochore Ausbreitung der insekten als zoogeographischer Faktor. - Ann. Zool. Soc. Zool. Bot. Fenn. Vanamo 10: 1-262.
  77. Pulliam H.R. 1988: Sources, sinks, and population regulation. - Am. Nat. 132: 652-661. Go to original source...
  78. Ranta E. & Ås S. 1982: Non-random colonization of habitat islands by carabid beetles. - Ann. Zool. Fenn. 19: 175-181.
  79. Roderick G.K. 1987: Ecology and Evolution of Dispersal in California Populations of a Salt Marsh Insect, Prokelisia marginata. PhD Thesis, University of California, Berkeley, CA.
  80. Roff D.A. 1986: The evolution of wing dimorphism in insects. - Evolution 40: 1009-1020. Go to original source...
  81. Roff D.A. 1990: The evolution of flightlessness in insects. - Ecol. Monogr. 60: 389-421. Go to original source...
  82. Roff D.A. & Fairbairn D.J. 1991: Wing dimorphisms and the evolution of migratory polymorphisms among the Insecta. - Am. Zool. 31: 243-251. Go to original source...
  83. Ryan R.B. 1959: Termination of diapause in the Douglas fir beetle, Dendroctonus pseudotsugae Hopkins, as an aid to continuous laboratory rearing. - Can. Entomol. 91: 520-525. Go to original source...
  84. Sahlberg J. 1868: Bidrag till kännedomen om Finlands Dimorpha Insekt-arter (Contribution to the knowledge of Finland's Dimorpha insect species). - Notiser ur Säällskapets pro Fauna et Flora Fennica 9 (1867), Helsinki [quoted in Lindroth, C.H. 1992].
  85. Solbreck C. 1978: Migration, diapause, and direct development as alternative life histories in a seed bug, Neacoryphus bicrucis. In Dingle H. (ed.): Evolution of Insect Migration and Diapause. Springer, New York, pp. 195-217.
  86. Spence J.R. 2000: Seasonal aspects of flight in water striders (Hemiptera: Gerridae). - Entomol. Sci. 3: 399-417.
  87. Stegwee D., Kimmel E.C., Den Boer J.A. & Henstra S. 1963: Hormonal control of reversible degeneration of flight muscle in the Colorado potato beetle, Leptinotarsa decemlineata Say (Coleoptera). - J. Cell Biol. 19: 519-527. Go to original source...
  88. ©ustek, Z. 1999: Light attraction of carabid beetles and their survival in the city centre. - Biologia (Bratislava) 54: 539-551.
  89. Thiele H.-U. 1977: Carabid Beetles in their Environments - A study on Habitat Selection by Adaptations in Physiology and Behaviour. Springer, Berlin, 369 pp.
  90. Tietze F. 1963: Untersuchungen über die Beziehungen zwischen Flügelreduktion und Ausbildung des Metathorax bei Carabiden. - Beitr. Entomol. 13: 88-167.
  91. Trivers R.L. 1972: Parental investment and sexual selection In Campbell B. (ed.): Sexual Selection and the Descent of Man. Aldine, Chicago, pp. 136-179.
  92. Unnithan G.C. & Nair K.K. 1977: Ultrastructure of juvenile hormone-induced degenerating flight muscles in a bark beetle, Ips paraconfusus. - Cell Tissue Res. 185: 481-490. Go to original source...
  93. Utida S. 1972: Density dependent polymorphism in the adult of Callosobracchus maculatus (Coleoptera: Bruchidae). - J. Stor. Prod. Res. 9: 111-126. Go to original source...
  94. Van Belleghem S.M., Roelofs D. & Hendrickx F. 2015: Evolutionary history of a dispersal associated locus across sympatric and allopatric divergent populations of a wing polymorphic beetle across Atlantic Europe. - Mol. Ecol. 24: 890-908. Go to original source...
  95. Van Huizen T.H.P. 1977: The significance of flight activity in the life cycle of Amara plebeja Gyll. (Coleoptera, Carabidae). - Oecologia (Berlin) 29: 27-41. Go to original source...
  96. Van Huizen T.H.P. 1979: Individual and environmental factors determining flight in carabid beetles. - Miscellaneous Papers (Landbouwhogeschool, Wageningen) 8: 71-74.
  97. Van Huizen T.H.P. 1984: 'Gone with the wind': Flight activity of carabid beetles in relation to wind direction and to the reproductive state of females in flight. In Stork N. (ed.): The Role of Ground Beetles in Ecological and Environmental Studies. Intercept, Andover, pp. 289-293.
  98. Van Schaick Zillesen P.G. & Brunsting A.M.H. 1984: The influence of food quantity and photoperiod during the pre-adult stages on flight muscle development in adult Philonthus decorus (Coleoptera: Staphylinidae) and Pterostichus oblongopunctatus (Coleoptera: Carabidae). - Entomol. Gener. 9: 143-147.
  99. Venn S. & Rokala K. 2005: Effects of grassland management strategy on the carabid fauna of urban parks. In Sk³odowski J., Huruk S., Barsevskis A. & Tarasiuk S. (eds): Protection of Coleoptera in the Baltic Sea Region. Warsaw Agricultural University Press, Warsaw, pp. 65-75.
  100. Venn S.J., Kotze D.J., Lassila T. & Niemelä J. 2013: Urban dry meadows provide valuable habitat for granivorous and xerophylic carabid beetles. - J. Insect Conserv. 17: 747-764. Go to original source...
  101. Venn S. 2007: Morphological responses to disturbance in wing-polymorphic carabid species (Coleoptera, Carabidae) of managed urban grasslands. - Baltic J. Coleopterol. 7: 51-60.
  102. Vepsälainen K. 1978: Wing dimorphism and diapause in Gerris: determination and adaptive significance. In Dingle H. (ed.): Evolution of Insect Migration and Diapause. Springer, New York, pp. 218-253.
  103. Wollaston T.V. 1854: Insecta Maderensia, Being an Account of the Insects of the Islands of the Madeiran Group. J. Van Voorst, London, 634 pp.
  104. Zera A.J. & Brink T. 2000: Nutrient absorption and utilization by wing and flight muscle morphs of the cricket Gryllus firmus: implications for the trade-off between flight capability and early reproduction. - J. Insect Behav. 46: 1207-1218. Go to original source...
  105. Zera A.J. Denno R.F. 1997: Physiology and ecology of dispersal polymorphism in insects. - Annu. Rev. Entomol. 42: 207-230. Go to original source...
  106. Zera A.J., Sall J. & Otto K. 1999: Biochemical aspects of flight and flightlessness in Gryllus: flight fuels, enzyme activities and electrophoretic profiles of flight muscles from flight-capable and flightless morphs. - J. Insect Physiol. 45: 275-285. Go to original source...