The Science of Nature

, 103:1 | Cite as

Costs and benefits of larval jumping behaviour of Bathyplectes anurus

  • Yoriko SaekiEmail author
  • Soichiro Tani
  • Katsuto Fukuda
  • Shun-ichiro Iwase
  • Yuma Sugawara
  • Midori TudaEmail author
  • Masami Takagi
Original Paper


Bathyplectes anurus, a parasitoid of the alfalfa weevils, forms a cocoon in the late larval stage and exhibits jumping behaviour. Adaptive significance and costs of the cocoon jumping have not been thoroughly studied. We hypothesised that jumping has the fitness benefits of enabling habitat selection by avoiding unfavourable environments. We conducted laboratory experiments, which demonstrated that jumping frequencies increased in the presence of light, with greater magnitudes of temperature increase and at lower relative humidity. In addition, when B. anurus individuals were allowed to freely jump in an arena with a light gradient, more cocoons were found in the shady area, suggesting microhabitat selection. In a field experiment, mortality of cocoons placed in the sun was significantly higher than for cocoons placed in the shade. B. anurus cocoons respond to environmental stress by jumping, resulting in habitat selection. In the presence of potential predators (ants), jumping frequencies were higher than in the control (no ant) arenas, though jumping frequencies decreased after direct contact with the predators. Body mass of B. anurus cocoons induced to jump significantly decreased over time than cocoons that did not jump, suggesting a cost to jumping. We discuss the benefits and costs of jumping behaviour and potential evolutionary advantages of this peculiar trait, which is present in a limited number of species.


Biological control Cocoon Habitat selection Leaping behaviour Locomotory mode Parasitoid 



We are indebted to four anonymous reviewers and M. Hart for their valuable and constructive suggestions. This study was supported by a Grant-in-Aid from JSPS (KAKENHI 22570215, 23405008 and 25430194) and by Kyushu University Interdisciplinary Programs in Education and Projects in Research Development (25412) to M. Tuda.


  1. Alcock J (1998) Animal behaviour: an evolutionary approach, 6th edn. Sinauer Associates, Inc, MassachusettsGoogle Scholar
  2. Alexander RM (2000) Hovering and jumping: contrasting problems in scaling. In: Brown JH, West GB (eds) Scaling in Biology. Oxford University Press, Oxford, pp 37–50Google Scholar
  3. Alyokhin AV, Mille C, Messing RH, Duan JJ (2001) Selection of pupation habitats by oriental fruit fly larvae in the laboratory. J Insect Behav 14:57–67. doi: 10.1023/A:1007849629409 CrossRefGoogle Scholar
  4. Amat I, Castelo M, Desouhant E, Bernstein C (2006) The influence of temperature and host availability on the host exploitation strategies of sexual and asexual parasitic wasps of the same species. Oecologia 148:153–161. doi: 10.1007/s00442-005-0332-9 CrossRefPubMedGoogle Scholar
  5. Angilletta MJ Jr (2009) Thermal adaptation: a theoretical and empirical synthesis. Oxford University Press, OxfordCrossRefGoogle Scholar
  6. Bartell DP, Pass BC (1978) Effects of Bathyplectes curculionis and Bathyplectes anurus [Hym.: Ichneumonidae] on the growth and development of Hypera postica [Col.: Curculionidae]. Entomophaga 23:281–291. doi: 10.1007/BF02373103 CrossRefGoogle Scholar
  7. Battisti A, Marini L, Pitacco A, Larsson S (2013) Solar radiation directly affects larval performance of a forest insect. Ecol Entomol 38:553–559. doi: 10.1111/een.12047 CrossRefGoogle Scholar
  8. Bazzaz FA (1991) Habitat selection in plants. Am Nat 137:S116–S130. doi: 10.1086/285142 CrossRefGoogle Scholar
  9. Berberet RC, Bisges AD, Zarrabi AA (2002) Role of cold tolerance in the seasonal life history of Bathyplectes curculionis (Hymenoptera: Ichneumonidae) in the Southern Great Plains. Environ Entomol 31:739–745. doi: 10.1603/0046-225X-31.4.739 CrossRefGoogle Scholar
  10. Berrigan D, Lighton JRB (1993) Bioenergetic and kinematic consequences of limblessness in larval Diptera. J Exp Biol 179:245–259PubMedGoogle Scholar
  11. Berrigan D, Pepin DJ (1995) How maggots move: allometry and kinematics of crawling in larval Diptera. J Insect Physiol 41:329–337. doi: 10.1016/0022-1910(94)00113-U CrossRefGoogle Scholar
  12. Binz H, Bucher R, Entling MH, Menzel F (2014) Knowing the risk: crickets distinguish between spider predators of different size and commonness. Ethology 120:99–110. doi: 10.1111/eth.12183 CrossRefGoogle Scholar
  13. Bonduriansky R (2002) Leaping behaviour and responses to moisture and sound in larvae of piophilid carrion flies. Can Entomol 134:647–656CrossRefGoogle Scholar
  14. Brackenbury J (2000) Locomotory modes in the larva and pupa of Chironomus plumosus (Diptera, Chironomidae). J Insect Physiol 46:1517–1527. doi: 10.1016/S0022-1910(00)00079-2 CrossRefPubMedGoogle Scholar
  15. Bucher R, Binz H, Menzel F, Entling MH (2014) Effects of spider chemotactile cues on arthropod behavior. J Insect Behav 27:567–580. doi: 10.1007/s10905-014-9449-1 CrossRefGoogle Scholar
  16. Casey TM (1991) Energetics of caterpillar locomotion: biomechanical constraints of a hydraulic skeleton. Science 252:112–114. doi: 10.1126/science.252.5002.112 CrossRefPubMedGoogle Scholar
  17. Chen F, Hesselberg T, Porter D, Vollrath F (2013) The impact behaviour of silk cocoons. J Exp Biol 216:2648–2657. doi: 10.1242/jeb.082545 CrossRefPubMedGoogle Scholar
  18. Cherry RH, Armbrust EJ (1977) Predators of Bathyplectes curculionis [Hym.: Ichneumonidae], a parasite of Hypera postica [Col.: Curculionidae]. Entomophaga 22:323–329. doi: 10.1007/BF02372155 CrossRefGoogle Scholar
  19. Cherry RH, Armbrust EJ, Ruesink WG (1976) Lethal temperatures of diapausing Bathyplectes curculionis (Hymenoptera: Ichneumonidae) a parasite of the alfalfa weevil (Coleoptera: Curculionidae). Great Lakes Entomol 9:189–193Google Scholar
  20. Danks HV (2004) The roles of insect cocoons in cold conditions. Eur J Entomol 101:433–437CrossRefGoogle Scholar
  21. Day WH (1970) The survival value of its jumping cocoons to Bathyplectes anurus, a parasite of the alfalfa weevil. J Econ Entomol 63:586–589CrossRefGoogle Scholar
  22. Eilers S, Pettersson L, Ockinger E (2013) Micro-climate determines oviposition site selection and abundance in the butterfly Pyrgus armoricanus at its northern range margin. Ecol Entomol 38:183–192. doi: 10.1111/een.12008 CrossRefGoogle Scholar
  23. Fonken LK, Nelson RJ (2013) The effect of light at night on circadian clocks and metabolism. Endocr Rev 35:648–670. doi: 10.1210/er.2013-1051 CrossRefGoogle Scholar
  24. Frouz J, Matĕna J, Ali A (2003) Survival strategies of chironomids (Diptera: Chironomidae) living in temporary habitats: a review. Eur J Entomol 100:459–465. doi: 10.14411/eje.2003.069 CrossRefGoogle Scholar
  25. Gauld ID, Bolton B (1988) The Hymenoptera. British Museum (Natural History) and Oxford University Press, OxfordGoogle Scholar
  26. Gonzalez D, Etzel L, Esmaili M, El-Heneidy AH, Kaddou I (1980) Distribution of Bathyplectes curculionis and Bathyplectes anurus [Hym.: Ichneumonidae] from Hypera [Col.: Curculionidae] on alfalfa in Egypt, Iraq, and Iran. Entomophaga 25:111–121. doi: 10.1007/BF02374313 CrossRefGoogle Scholar
  27. Hagstrum DW, Subramanyam B (2010) Immature insects: ecological roles of mobility. Am Entomol 56:230–241,  10.1093/ae/56.4.230 CrossRefGoogle Scholar
  28. Hamm CE, Merkel R, Springer O, Jurkojc P, Maier C, Prechtel K, Smetacek V (2003) Architecture and material properties of diatom shells provide effective mechanical protection. Nature 421:841–843. doi: 10.1038/nature01416 CrossRefPubMedGoogle Scholar
  29. Heckrotte C (1983) The influence of temperature on the behavior of the Mexican jumping bean. J Therm Biol 8:333–335. doi: 10.1016/0306-4565(83)90018-9 CrossRefGoogle Scholar
  30. Heinrich B (1981) Insect thermoregulation. John Wiley & Sons, New YorkGoogle Scholar
  31. Helfman GS (1989) Threat-sensitive predator avoidance in damselfish-trumpetfish interactions. Behav Ecol Sociobiol 24:47–58. doi: 10.1007/BF00300117 CrossRefGoogle Scholar
  32. Horn DJ (1976) Brief note behavior of Gelis species’ parasitizing Bathyplectes, parasitoids of the alfalfa weevil. Ohio J Sci 76:279–280Google Scholar
  33. Hulthen AD, Clarke AR (2006) The influence of soil type and moisture on pupal survival of Bactrocera tryoni (Froggatt) (Diptera: Tephritidae). Aust J Entomol 45:16–19. doi: 10.1111/j.1440-6055.2006.00518.x CrossRefGoogle Scholar
  34. Humphreys K, Darling DC (2013) Not looking where you are leaping: a novel method of oriented travel in the caterpillar Calindoea trifascialis (Moore) (Lepidoptera: Thyrididae). Biol Lett 9:20130397. doi: 10.1098/rsbl.2013.0397 PubMedCentralCrossRefPubMedGoogle Scholar
  35. Ito T (2012) Jumping cocoons of Orchestes jozanus (Kono). Monthly J Entomol 499:22–24 (In Japanese)Google Scholar
  36. Iwase S, Nakahira K, Tuda M, Kagoshima K, Takagi M (2015) Host-plant dependent population genetics of the invading weevil Hypera postica. B Entomol Res 105:92–100. doi: 10.1017/S0007485314000728 CrossRefGoogle Scholar
  37. Josso C, Moiroux J, Vernon P, Van Baaren J, Van Alphen JJM (2011) Temperature and parasitism by Asobara tabida (Hymenoptera: Braconidae) influence larval pupation behaviour in two Drosophila species. Naturwissenschaften 98:705–709. doi: 10.1007/s00114-011-0813-0 CrossRefPubMedGoogle Scholar
  38. Juliano SA, Gravel ME (2002) Predation and the evolution of prey behavior: an experiment with tree hole mosquitoes. Behav Ecol 13:301–311. doi: 10.1093/beheco/13.3.301 CrossRefGoogle Scholar
  39. Kats L, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361–394Google Scholar
  40. Kingsolver JG, Huey RB (2008) Size, temperature, and fitness: three rules. Evol Ecol Res 10:251–268Google Scholar
  41. Krämer B, Kämpf I, Enderle J, Poniatowski D, Fartmann T (2012) Microhabitat selection in a grassland butterfly: a trade-off between microclimate and food availability. J Insect Conserv 16:857–865. doi: 10.1007/s10841-012-9473-4 CrossRefGoogle Scholar
  42. Krasnov BR (2008) Functional and evolutionary ecology of fleas: a model for ecological parasitology. Cambridge University Press, New YorkCrossRefGoogle Scholar
  43. Kuusik A, Tartes U, Vanatoa A, Hiiesaar K, Metspalu L (2001) Body movements and their role as triggers of heartbeats in pupae of the Colorado potato beetles Leptinotarsa decemlineata. Physiol Entomol 26:158–164. doi: 10.1046/j.1365-3032.2001.00229.x CrossRefGoogle Scholar
  44. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640. doi: 10.1139/z90-092 CrossRefGoogle Scholar
  45. Lyon BE, Cartar RV (1996) Functional significance of the cocoon in two arctic Gynaephora moth species. P Roy Soc Lond B Biol Sci 263:1159–1163. doi: 10.1098/rspb.1996.0169 CrossRefGoogle Scholar
  46. Maitland DP (1992) Locomotion by jumping in the Mediterranean fruit-fly larva Ceratitis capitata. Nature 355:159–161. doi: 10.1038/355159a0 CrossRefGoogle Scholar
  47. McClure M, Cannell E, Despland E (2011) Thermal ecology and behaviour of the nomadic social forager Malacosoma disstria. Physiol Entomol 36:120–127. doi: 10.1111/j.1365-3032.2010.00770.x CrossRefGoogle Scholar
  48. McPheron LJ, Broce AB (1996) Environmental components of pupariation-site selection by the stable fly (Diptera: Muscidae). Environ Entomol 25:665–671CrossRefGoogle Scholar
  49. Miyatake T, Tabuchi K, Sasaki K, Okada K, Katayama K, Moriya S (2008) Pleiotropic antipredator strategies, fleeing and feigning death, correlated with dopamine levels in Tribolium castaneum. Anim Behav 75:113–121. doi: 10.1016/j.anbehav.2007.04.019 CrossRefGoogle Scholar
  50. Morris DW (2003) Toward an ecological synthesis: a case for habitat selection. Oecologia 136:1–13. doi: 10.1007/s00442-003-1241-4 CrossRefPubMedGoogle Scholar
  51. Orians GH, Wittenberger JF (1991) Spatial and temporal scales in habitat selection. Am Nat 137:S29–S49. doi: 10.1086/285138 CrossRefGoogle Scholar
  52. Radcliffe EB, Flanders KL (1998) Biological control of alfalfa weevil in North America. Integrated Pest Manag Rev 3:225–242CrossRefGoogle Scholar
  53. Reynolds DR, Reynolds AM, Chapman JW (2014) Non-volant modes of migration in terrestrial arthropods. Animal Migration 2:8–28. doi: 10.2478/ami-2014-0002 CrossRefGoogle Scholar
  54. Roy M, Meena SK, Kusurkar TS, Singh SK, Sethy NK, Bhargava K, Sarkar S, Das M (2012) Carbon dioxide gating in silk cocoon. Biointerphases 7:45. doi: 10.1007/s13758-012-0045-7 CrossRefPubMedGoogle Scholar
  55. Tagawa J (1996) Function of the cocoon of the parasitoid wasp, Cotesia glomerata L. (Hymenoptera: Braconidae): protection against desiccation. Appl Entomol Zool 31:99–103Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Institute of Biological Control, Faculty of AgricultureKyushu UniversityFukuokaJapan
  2. 2.Laboratory of Insect Natural Enemies, Division of Agricultural Bioresource Sciences, Department of Bioresource Sciences, Faculty of AgricultureKyushu UniversityFukuokaJapan

Personalised recommendations