A review on self-destructive defense behaviors in social insects

Insectes Sociaux

Volumn 59, Issue 1, 2012, Pages 1-10

  Shorter, J R ^a   Rueppell, O ^b  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NORTH CAROLINA AT GREENSBORO   (United States)

Author keywords

Altruism; Autothysis; Defensive behavior; Host suicide; Sting autotomy

Indexed keywords

ALTRUISM; ANTIPARASITE DEFENSE; AUTOTOMY; COLONIAL ORGANISM; EUSOCIALITY; EVOLUTIONARILY STABLE STRATEGY; KIN SELECTION; MORTALITY; NEST GUARDING; PATHOGEN; SOCIAL INCLUSION;

HEXAPODA;

EID: 84855744656     PISSN: 00201812     EISSN: 14209098     Source Type: Journal    
DOI: 10.1007/s00040-011-0210-x     Document Type: Review

References (95)

1. Arechavaleta-Velasco M. E., Hunt G. J. and Emore C. 2003. Quantitative trait loci that influence the expression of guarding and stinging behaviors of individual honey bees. Behav. Genet. 33: 357-364.
2. Batchelor T. P. and Briffa M. 2011. Fight tactics in wood ants: individuals in smaller groups fight harder but die faster. P. Roy. Soc. Lond. B. Biol. 278: 3243-3250.
3. Benton R. 2011. Decision making: singin' in the brain. Neuron. 69: 399-401.
4. Beshers S. N. and Fewell J. H. 2001. Models of division of labor in social insects. Annu. Rev. Entomol. 46: 413-440.
5. Bordereau C., Robert A., VanTuyen V. and Peppuy A. 1997. Suicidal defensive behaviour by frontal gland dehiscence in Globitermes sulphureus Haviland soldiers (Isoptera). Insect. Soc. 44: 289-297.
6. Bourke A. F. G. 2008. Social evolution: daily self-sacrifice by worker ants. Curr. Biol. 18: R1100-R1101.
7. Breed M. D., Guzman-Novoa E. and Hunt G. J. 2004. Defensive behavior of honey bees: organization, genetics, and comparisons with other bees. Annu. Rev. Entomol. 49: 271-298.
8. Buchwald R. and Breed M. D. 2005. Nestmate recognition cues in a stingless bee, Trigona fulviventris. Anim. Behav. 70: 1331-1337.
9. Buschinger A. and Maschwitz U. 1984. Defensive behavior and defensive mechanisms in ants. In: Defensive Mechanisms in Social Insects (Hermann H. R., Ed), Praeger, New York, pp 95-150.
10. Cook S. C. 2008. Functional and nutritional biology of exudate-feeding ants. PhD Thesis, University of Utah Press, UT, USA.
11. Costa-Leonardo A. M. 2004. A new interpretation of the defense glands of neotropical Ruptitermes (Isoptera, Termitidae, Apicotermitinae). Sociobiology 44: 391-402.
12. Costa-Leonardo A. M. and Kitayama K. 1991. Frontal gland dehiscence in the Brazilian termite Serritermes serrifer (Isoptera: Serritermitidae). Sociobiology 19: 333-338.
13. Cremer S. and Sixt M. 2009. Analogies in the evolution of individual and social immunity. Philos. T. Roy. Soc. B. 364: 129-142.
14. Cunard S. J. and Breed M. D. 1998. Post-stinging behavior of worker honey bees (Hymenoptera: Apidae). Ann. Entomol. Soc. Am. 91: 754-757.
15. Davidson D. W., Anderson N. F., Cook S. C., Bernau C. R., Jones T. H., Kamariah A. S., Lim L. B., Chan C. M. and Clark D. A. 2009. An experimental study of microbial nest associates of Borneo's exploding ants (Camponotus [Colobopsis] species). J. Hymenopt. Res. 18: 341-360.
16. Davidson D. W., Kamariah A. S. and Billen J. 2011. Histology of structures used in territorial combat by Borneo's 'exploding ants'. Acta Zool.-Stockholm 00: 1-5.
17. Davidson D. W., Lessard J. P., Bernau C. R. and Cook S. C. 2007. The tropical ant mosaic in a primary Bornean rain forest. Biotropica 39: 468-475.
18. Deligne J. and De Coninck E. 2006. Suicidal defence through a dehiscent frontal weapon in Apilitermes longiceps soldiers (Isoptera: Termitidae). Belg. J. Entomol. 8: 3-10.
19. Edwards J. S. 1966. Defense by smear: supercooling in the cornicle wax of aphids. Nature 211: 73-74.
20. Ellis R. E., Yuan J. Y. and Horvitz H. R. 1991. Mechanisms and functions of cell-death. Annu. Rev. Cell Biol. 7: 663-698.
21. Fewell J. H. 2003. Social insect networks. Science 301: 1867-1870.
22. Foster K. R., Wenseleers T. and Ratnieks F. L. W. 2006. Kin selection is the key to altruism. Trends Ecol. Evol. 21: 57-60.
23. Foster W. A. 2010. Behavioural ecology: the menopausal aphid glue-bomb. Curr. Biol. 20: R559-R560.
24. Fraser C., Riley S., Anderson R. M. and Ferguson N. M. 2004. Factors that make an infectious disease outbreak controllable. P. Natl. Acad. Sci. U. S. A. 101: 6146-6151.
25. Greene A., Breisch N. L., Golden D. B. K., Kwiterovich K. A., Addison B. I. and Schuberth K. C. 1989. The sting that stays: autotomy in 2 common yellowjacket species. J. Allergy Clin. Immun. 83: 229-229.
26. Hamilton W. D. 1964. Genetical evolution of social behaviour. J. Theor. Biol. 7: 1-16.
27. Hart A. G. and Ratnieks F. L. W. 2002. Waste management in the leaf-cutting ant Atta colombica. Behav. Ecol. 13: 224-231.
28. Heinze J. and Walter B. 2010. Moribund ants leave their nests to die in social isolation. Curr. Biol. 20: 249-252.
29. Hermann H. R. 1971. Sting autotomy-defensive mechanism in certain social Hymenoptera. Insect. Soc. 18(2): 111-120.
30. Hermann H. R. 1984a. Defensive mechanisms: general considerations. In: Defensive Mechanisms in Social Insects (Hermann H. R., Ed), Praeger, New York, pp 1-31.
31. Hermann H. R. 1984b. Elaboration and reduction of the venom apparatus in aculeate Hymenoptera. In: Defensive Mechanisms in Social Insects (Hermann H. R., Ed), Praeger, New York, pp 201-238.
32. Herrmann M., Trenzcek T., Fahrenhorst H. and Engels W. 2005. Characters that differ between diploid and haploid honey bee (Apis mellifera) drones. Genet. Molec. Res. 4: 624-641.
33. Higes M., Martin-Hernandez R., Botias C., Bailon E. G., Gonzalez-Porto A. V., Barrios L., del Nozal M. J., Bernal J. L., Jimenez J. J., Palencia P. G. and Meana A. 2008. How natural infection by Nosema ceranae causes honeybee colony collapse. Environ. Microbiol. 10: 2659-2669.
34. Hohorst W. and Graefe G. 1961. Ameisen - obligatorische Zwischenwirte des Lanzettegels (Dicrocoelium dendriticum). Naturwissenschaften 48: 229-230.
35. Hölldobler B. and Wilson E. O. 1990. The Ants. Harvard University Press: Cambridge, Massachusetts, USA.
36. Hughes D. P., Pierce N. E. and Boomsma J. J. 2008. Social insect symbionts: evolution in homeostatic fortresses. Trends Ecol. Evol. 23: 672-677.
37. Human K. G. and Gordon D. M. 1999. Behavioral interactions of the invasive Argentine ant with native ant species. Insect. Soc. 46: 159-163.
38. Hunt G. J. 2007. Flight and fight: A comparative view of the neurophysiology and genetics of honey bee defensive behavior. J. Insect Physiol. 53: 399-410.
39. Hunt G. J., Guzman-Novoa E., Fondrk M. K. and Page R. E. 1998. Quantitative trait loci for honey bee stinging behavior and body size. Genetics 148: 1203-1213.
40. Hydak M. H. 1951. How long does a bee live after losing its sting. Gleanings Bee Cult. 79: 85-86.
41. Jeanne R. L. 1986. The evolution of the organization of work in social insects. Ital. J. Zool. 20: 119-133.
42. Jones T. H., Clark D. A., Edwards A. A., Davidson D. W., Spande T. F. and Snelling R. R. 2004. The chemistry of exploding ants, Camponotus spp. (cylindricus complex). J. Chem. Ecol. 30: 1479-1492.
43. Khoury D. S., Myerscough M. R. and Barron A. B. 2011. A quantitative model of honey bee colony population dynamics. PLoS One 6: e18491.
44. Kohatsu S., Koganezawa M. and Yamamoto D. 2011. Female contact activates male-specific interneurons that trigger stereotypic courtship behavior in Drosophila. Neuron 69: 498-508.
45. Kolmes S. A. and Fergusson-Kolmes L. A. 1989. Stinging behavior and residual value of worker honey bees (Apis-mellifera). J. N. Y. Entomol. Soc. 97: 218-231.
46. Kralj J. and Fuchs S. 2006. Parasitic Varroa destructor mites influence flight duration and homing ability of infested Apis mellifera foragers. Apidologie 37: 577-587.
47. Kralj J. and Fuchs S. 2010. Nosema sp. influences flight behavior of infected honey bee (Apis mellifera) foragers. Apidologie 41: 21-28.
48. Kurosu U., Aoki S. and Fukatsu T. 2003. Self-sacrificing gall repair by aphid nymphs. P. Roy. Soc. Lond. B. Biol. 270: S12-S14.
49. Kurzfeld-Zexer L., Wool D. and Inbar M. 2010. Modification of tree architecture by a gall-forming aphid. Trees-Struct. Funct. 24: 13-18.
50. Kutsukake M., Shibao H., Uematsu K. and Fukatsu T. 2009. Scab formation and wound healing of plant tissue by soldier aphid. P. Roy. Soc. Lond. B. Biol. 276: 1555-1563.
51. Libersat F., Delago A. and Gal R. 2009. Manipulation of host behavior by parasitic insects and insect parasites. Annu. Rev. Entomol. 54: 189-207.
52. Manzoli-Palma M. D., daCunha M. S. and Gobbi N. 1997. Muscles-bearing of sting apparatus in social wasps and their relationship with the autotomy (Hymenoptera: Vespidae: Polistinae). J. Adv. Zool. 18: 1-6.
53. Maschwitz U. and Maschwitz E. 1974. Platzende Arbeiterinnen: Eine neue Art der Feindabwehr bei sozialen Hautflüglern. Oecologia 14: 289-294.
54. McAllister M. K. and Roitberg B. D. 1987. Adaptive suicidal-behavior in pea aphids. Nature 328: 797-799.
55. Millor J., Pham-Delegue M., Deneubourg J. L. and Camazine S. 1999. Self-organized defensive behavior in honeybees. P. Natl. Acad. Sci. U. S. A. 96: 12611-12615.
56. Moron D., Witek M. and Woyciechowski M. 2008. Division of labour among workers with different life expectancy in the ant Myrmica scabrinodis. Anim. Behav. 75: 345-350.
57. Moura F. M. S., Vasconcellos A., Silva N. B. and Bandeira A. G. 2011. Caste development systems of the neotropical termite Constrictotermes cyphergaster (Isoptera, Termitidae). Insect. Soc. 58: 169-175.
58. Mulfinger L., Yunginger J., Styer W., Guralnick M. and Lintner T. 1992. Sting morphology and frequency of sting autotomy among medically important vespids (Hymenoptera, Vespidae) and the honey bee (Hymenoptera, Apidae). J. Med. Entomol. 29: 325-328.
59. Muller C. B. and Schmid-Hempel P. 1993. Exploitation of cold temperature as defense against parasitoids in bumblebees. Nature 363: 65-67.
60. Naug D. and Camazine S. 2002. The role of colony organization on pathogen transmission in social insects. J. Theor. Biol. 215: 427-439.
61. Nogueira-Neto P. 1964. The spread of a fierce African bee in Brazil. Bee World 45: 119-121.
62. O'Gorman R., Wilson D. S. and Miller R. R. 2005. Altruistic punishing and helping differ in sensitivity to relatedness, friendship, and future interactions. Evol. Hum. Behav. 26: 375-387.
63. Oster G. F. and Wilson E. O. 1978. Caste and Ecology in the Social Insects. Princeton University Press, Princeton. NJ.
64. Pike N. 2007. Specialised placement of morphs within the gall of the social aphid Pemphigus spyrothecae. BMCEvol. Biol. 7: 18.
65. Pike N. and Foster W. 2004. Fortress repair in the social aphid species Pemphigus spyrothecae. Anim. Behav. 67: 909-914.
66. Poulin R. 1992. Altered behavior in parasitized bumblebees - parasite manipulation or adaptive suicide. Anim. Behav. 44: 174-176.
67. Poulin R., Brodeur J. and Moore J. 1994. Parasite manipulation of host behaviour: should hosts always lose? Oikos 70: 479-484.
68. Quenette P. Y. 1990. Functions of vigilance behavior in mammals - a review. Acta Oecol. 11: 801-818.
69. Ratnieks F. L. W. and Wenseleers T. 2008. Altruism in insect societies and beyond: voluntary or enforced? Trends Ecol. Evol. 23: 45-52.
70. Rueppell O., Bachelier C., Fondrk M. K. and Page R. E. 2007. Regulation of life history determines lifespan of worker honey bees (Apis mellifera L.). Exp. Gerontol. 42: 1020-1032.
71. Rueppell O., Hayworth M. K. and Ross N. P. 2010. Altruistic self-removal of health-compromised honey bee workers from their hive. J. Evol. Biol. 23: 1538-1546.
72. Sands W. A. 1982. Agonistic behavior of African soldierless Apicotermitinae (Isoptera, Termitidae). Sociobiology 7: 61-72.
73. Santomauro G., Oldham N. J., Boland W. and Engels W. 2004. Cannibalism of diploid drone larvae in the honey bee (Apis mellifera) is released by odd pattern of cuticular substances. J. Apicult. Res. 43: 69-74.
74. Schmid-Hempel P. 1998. Parasites in Social Insects. Princeton University Press, Princeton, NJ.
75. Schmidt J. O., Blum M. S. and Overal W. L. 1980. Comparative lethality of venoms from stinging Hymenoptera. Toxicon 18: 469-474.
76. Schumacher M. J. and Egen N. B. 1995. Significance of Africanized bees for public-health - a review. Arch. Intern. Med. 155: 2038-2043.
77. Shapiro A. M. 1976. Beau Geste? Am. Nat. 110: 900-902.
78. Sledge M. F., Dani F. R., Fortunato A., Maschwitz U., Clarke S. R., Francescato E., Hashim R., Morgan E. D., Jones G. R. and Turillazzi S. 1999. Venom induces alarm behaviour in the social wasp Polybioides raphigastra (Hymenoptera: Vespidae): an investigation of alarm behaviour, venom volatiles and sting autotomy. Physiol. Entomol. 24(3): 234-239.
79. Smith-Trail D. R. 1980. Behavioral interactions between parasites and hosts: host suicide and the evolution of complex life cycles. Am. Nat. 116: 77-91.
80. Sobotnik J., Bourguignon T., Hanus R., Weyda F. and Roisin Y. 2010a. Structure and function of defensive glands in soldiers of Glossotermes oculatus (Isoptera: Serritermitidae). Biol. J. Linn. Soc. 99: 839-848.
81. Sobotnik J., Sillam-Dusses D., Weyda F., Dejean A., Roisin Y., Hanus R. and Bourguignon T. 2010b. The frontal gland in workers of neotropical soldierless termites. Naturwissenschaften 97: 495-503.
82. Thorne B. L. 1997. Evolution of eusociality in termites. Annu. Rev. Ecol. Syst. 28: 27-54.
83. Tofilski A. 2002. Influence of age polyethism on longevity of workers in social insects. Behav. Ecol. Sociobiol. 51: 234-237.
84. Tofilski A. 2006. Influence of caste polyethism on longevity social insect colonies. J. Theor. Biol. 238: 527-531.
85. Tofilski A. 2009. Shorter-lived workers start foraging earlier. Insect. Soc. 56: 359-366.
86. Tofilski A., CouvillonM. J., Evison S. E. F., Helanterä H., Robinson E. J. H. and Ratnieks F. L. W. 2008. Preemptive defensive self-sacrifice by ant workers. Am. Nat. 172: E239-E243.
87. Uematsu K., Kutsukake M., Fukatsu T., Shimada M. and Shibao H. 2007. Altruistic defenders in a Japanese gall-forming aphid, Quadrartus yoshinomiyai (Homoptera: Aphididae: Hormaphidinae). Sociobiology 50: 711-724.
88. Uematsu K., Kutsukake M., Fukatsu T., Shimada M. and Shibao H. 2010. Altruistic colony defense by menopausal female insects. Curr. Biol. 20: 1182-1186.
89. van Zweden J. S., Gruter C., Jones S. M. and Ratnieks F. L. W. 2011. Hovering guards of the stingless bee Tetragonisca angustula increase colony defensive perimeter as shown by intra- and inter-specific comparisons. Behav. Ecol. Sociobiol. 65: 1277-1282.
90. vanEngelsdorp D., Evans J. D., Saegerman C., Mullin C., Haubruge E., Nguyen B. K., Frazier M., Frazier J., Cox-Foster D., Chen Y. P., Underwood R., Tarpy D. R. and Pettis J. S. 2009. Colony collapse disorder: a descriptive study. PLoS One 4: e6481.
91. von Philipsborn A. C., Liu T. X., Yu J. Y., Masser C., Bidaye S. S. and Dickson B. J. 2011. Neuronal control of Drosophila courtship song. Neuron 69: 509-522.
92. Williams M. W. and Williams C. S. 1965. Toxicity of ant venom further studies of venom from Pogonomyrmex barbatus. P. Soc. Exp. Biol. Med. 119: 344-346.
93. Wilson E. O. 1975. Sociobiology. Belknap Press, Cambridge, MA.
94. Woyciechowski M. and Kozlowski J. 1998. Division of labor by division of risk according to worker life expectancy in the honey bee (Apis mellifera L.). Apidologie 29: 191-205.
95. Woyciechowski M. and Moron D. 2009. Life expectancy and onset of foraging in the honeybee (Apis mellifera). Insect. Soc. 56: 193-201.