Grooming behaviours in the Hymenoptera (Insecta): Potential phylogenetic significance

Zoological Journal of the Linnean Society

Volumn 125, Issue 3, 1999, Pages 349-382

  Basibuyuk, Hasan H ^a,b,c   Quicke, Donald L J ^a,b  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b DEPARTMENT OF LIFE SCIENCES   (United Kingdom)

^c CUMHURIYET UNIVERSITY   (Turkey)

Author keywords

Phylogenetic relationships evolution

Indexed keywords

APOCRITA; CHALCIDOIDEA; CYNIPOIDEA; HYMENOPTERA; ICHNEUMONOIDEA; INSECTA; MYMARIDAE; PLATYGASTROIDEA;

EID: 0033247144     PISSN: 00244082     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1096-3642.1999.tb00597.x     Document Type: Article

References (103)

1. Alexander RD. 1962. The role of behavioral study in cricket classification. Systematic Zoology 11: 53-72.
2. Assem J van den, Gijswijt MJ, Nübel BK. 1982. Characteristics of courtship and mating behaviour used as classificatory criteria in Eulophidae-Tetrastichinae (Hymenoptera), with special reference to the genus Tetrastichus s.l. Tijdschrift voor Entomologie 125: 205-220.
3. Assem J van den, in den Bosch HAJ, Prooy E. 1982. Melittobia courtship behaviour: a comparative study of the evolution of a display. Netherlands Journal of Zoology 32: 427-471.
4. Barry MW, Nielsen DG. 1984. Behavior of adult peachtree borer (Lepidoptera: Sesiidae). Annals of the Entomological Society of America 77: 246-250.
5. Basibuyuk HH, Quicke DLJ. 1994. Evolution of antennal cleaner structure in the Hymenoptera 'Insecta). Norwegian Journal of Agricultural Sciences Suppl. no. 16: 199-200.
6. Basibuyuk HH, Quicke DLJ. 1995. Morphology of the antenna cleaner in the Hymenoptera with particular reference to non-aculeate families (Insecta). Zoologica Scripta 24: 157-177.
7. Basibuyuk HH, Quicke DLJ. 1997. Hamuli in the Hymenoptera (Insecta) and their phylogenetic implications. Journal of Natural Historyn 31: 1563-1585.
8. Batra SWT. 1964. Behavior of the social bee, Lasioglossum zephyrum, within the nest (Hymenoptera: Halictidae). Insectes Socieaux, Paris 11: 159-186.
9. Bayliss PS, Brothers DJ. 1996. Biology of Tricholabiodes Radoszkowski in Southern Africa, with a new synonymy and review of recent biological literature (Hymenoptera: Mutillidae). Journal of Hymenoptera Research 5: 249-258.
10. Beani L, Calloni C. 1991. Leg tegumental glands and male rubbing behavior at leks in Polistes dominulus (Hymenoptera: Vespidae). Journal of Insect Behavior 4: 449-462.
11. Beeken W. 1934. Über die Putz-und Säuberungshandlungen der Honigbiene (Apis mellifica . Archiv für Bienenkunde 15: 213-275.
12. Blom J van der, Velthuis HHW. 1988. Social behaviour of the carpenter bee Xylocopa pubescens (Spinola). Ethology 79: 281-294.
13. Boecking O, Rath W, Drescher W. 1993. Grooming and removal behaviour-strategies of Apis mellifera and Apis cerana bees against Varroa jacobsoni. American Bee Journal 133: 117-119.
14. Brothers DJ. 1975. Phylogeny and classification of the aculeate Hymenoptera, with special reference to Mutillidae. The University of Kansas Science Bulletin 50: 483-648.
15. Brothers DJ, Carpenter JM. 1993. Phylogeny of Aculeata: Chrysidoidea and Vespoidea. Journal of Hymenoptera Research 2: 227-302.
16. Callahan PS. 1975. Insect antennae with special reference to the mechanism of scent detection and the evolution of sensilla. International Journal of Insect Morphology & Embryology 4: 381-430.
17. Callow NA. 1993. Antennal cleaning behaviour of Vespula germanica (F.) (Hymenoptera: Vespidae). British Journal of Entomology and Natural History: 6: 89.
18. Cane JH, Eickwort GC, Wesley FR, Spielholz J. 1983. Foraging, grooming, and mate-seeking behaviors of Macropis nuda (Hymenoptera, Melittidae) and use of Lysimachia ciliata (Primulaceae) oils in larval provisions and cell linings. The American Midland Naturalist 110: 257-269.
19. Carpenter JM. 1986. Cladistics of the Chrysidoidea (Hymenoptera). Journal of the New York Entomological Society 94: 303-330.
20. Connolly K. 1968. The social facilitation of preening behaviour in Drosophila melanogaster. Animal Behavior 16: 385-391.
21. Conway JR. 1983. A study of winged queens of the Colorado honey ant, Myrmecocystus mexicanus in captivity. Journal of the New York Entomological Society 91: 252-263.
22. Dawkins R, Dawkins M. 1976. Hierarchical organization and postural facilitation: rules for grooming in flies. Animal Behavior 24: 739-755.
23. de Queiroz A, Wimberger PH. 1993. The usefulness of behavior for phylogeny estimation: levels of homoplasy in behavioral and morphological characters. Evolution 47: 46-60.
24. Dowton M, Austin AD. 1994. Molecular phylogeny of the insect order Hymenoptera: apocritan relationships. Proceedings of the National Academy of Sciences, U.S.A. 91: 9911-9915.
25. Dustmann JH. 1993. Natural defence mechanisms of honey bee colony against diseases and parasites. American Bee Journal 133: 431-434.
26. Farish DJ. 1969. The grooming behavior of Hymenoptera (Insecta). Unpublished Ph.D. Thesis. Harvard University.
27. Farish DJ. 1972. The evolutionary implications of qualitative variation in the grooming behaviour of the Hymenoptera (Insecta). Animal Behavior 20: 662-676.
28. Gangwere SK. 1958. Grooming behavior in Orthoptera. Entomological News 69: 123-128.
29. Gauld ID, Bolton B. 1988. The Hymenoptera. New York: Oxford University Press.
30. Gibson GAP. 1985. Some pro- and mesothoracic structures important for phylogenetic analysis of Hymenoptera, with a review of terms used for the structures. Canadian Entomologist 117: 1395-1443.
31. Gibson GAP. 1986. Evidence for monophyly and relationships of Chalcidoidea, Mymaridae, and Mymarommatidae (Hymenoptera: Terebrantes). Canadian Entomologist 118: 205-240.
32. Gibson GAP. 1993. Groundplan structure and homology of the pleuron in Hymenoptera based on a comparison of the skeletomusculature of Xyelidae (Hymenoptera) and Raphidiidae (Neuroptera). Memoirs of the Entomological Society of Canada 165: 165-187.
33. Goulet H, Huber JT. 1993. Hymenoptera of the world: an identification guide to families. Ottawa: Agriculture Canada.
34. Harvey PH, Pagel MD. 1993. The comparative method in evolutionary biology. Oxford: Oxford University Press.
35. Heatwole H, Davis DM, Wenner AM. 1962. The behaviour of Megarhyssa, a genus of parasitic hymenopterans (Ichneumonidae: Ephialtinae). Zeitschrift für Tierpsychologie 19: 652-664.
36. Heinz HJ. 1949. Beobachtungen über die Patzhandlungen bei Dipteren im allgemeinen und bei Salcophaga carnaria L. im besonderen. Zeitschrift für Tierpsychologie 6: 330-371.
37. Heraty JM, Woolley JB, Darling DC. 1994. Phylogenetic implications of the mesofurca and mesopostnotum in Hymenoptera. Journal of Hymenoptera Research 3: 241-277.
38. Hlavac TF. 1975. Grooming system of insects: structure, mechanics. Annals of the Entomological Society of America 68: 823-826.
39. Honegger HW, Reif H, Müller W. 1979. Sensory mechanisms of eye cleaning behavior in the cricket Gryllus campestris. Journal of Comparative Physiology 129: 247-256.
40. Jander U. 1966. Untersuchen zur Stammesgeschichte von Putzbewegungen von Tracheaten. Zeitschrift für Tierpsychologie 23: 799-844.
41. Jander R. 1976. Grooming and pollen manipulation in bees Apoidea: the nature and evolution of movements involving the fore leg. Physiological Entomology 1: 179-184.
42. Jander R, Jander U. 1978. Wing grooming in bees Apoidea and the evolution of wing grooming in insects. Journal of the Kansas Entomological Society 51: 653-665.
43. Johnson NF. 1988. Mideoxal articulations and the phylogeny of the order Hymenoptera. Annals of the Entomological Society of America 81: 870-881.
44. Jung K. 1937. Die Sauberungshandlungen der Ameisen, zugleich ein Beitrag zur Plastizital des Nervensystems. Zoologische Jahrbücher (Abteilung für Systematik) 69: 373-416.
45. Kimsey LS. 1984. The behavioural and structural aspects of grooming and related activities in euglossine bees (Hymenoptera: Apidae). Journal of Zoology, London 204: 541-550.
46. Kitano H. 1976. Studies on the courtship behavior of Apanteles glomeratus L. 3. On the behavior of males and females after their emergence from cocoons. Physiology and Ecology, Japan 17: 383-393.
47. Königsmann E. 1976. Das phylogenetische System der Hymenoptera. Teil 1: Einfuhrung. Grundplanmerkmaie, Schwestergruppe und Fossilfunde. Deutsche Entomologische Zeitschrift 23: 253-279.
48. Königsmann E. 1977. Das phylogenetische System der Hymenoptera. Teil 2: Symphyta. Deutsche Entomologische Zeitschrift 24: 1-40.
49. Königsmann E. 1978a. Das phylogenetische System der Hymenoptera. Teil 3: Terebrantes Underordnung Apocrita). Deutsche Entomologische Zeitschrift 25: 1-55.
50. Königsmann E. 1978b. Das phylogenetische System der Hymenoptera. Teil 4: Aculeata Underordnung Apocrita. Deutsche Entolologische Zeitschrift 25: 365-435.
51. Kovac D, Maschwitz U. 1989. Secretion-grooming in the water bug Plea minutissima: a chemical defence against microorganisms interfering with the hydrofuge properties of the respiratory region. Ecological Entomology 14: 403-411.
52. Kovarik PW, Burke HR, Agnew CW. 1991. Development and behavior of snakefly. Raphidia bicolor Albarda (Neuroptera: Raphidiidae). South Western Entomologist 16: 353-364.
53. Kurt F, Hartl GB. 1995. Socio-ethogram of adult males versus biochemical-genetic variation in assessing phylogenetic relationships of the Caprinae. Acta Theriologica. Suppl. no. 3: 183-197.
54. Lee HP, Lee JH. 1989. Oviposition behavior of Ooencyrtus kuvanae (Howard) (Hymenoptera: Encyrtidae), egg parasitoid of Lymantria dispar L. (Lepidoptera: Lymantriidae). Korean Journal of Applied Entomology 28: 221-228.
55. Lefebvre L. 1981. Grooming in crickets: timing and hierarchical organization. Animal Behavior 29: 973-984.
56. Maddison WP. 1990. A method for testing the correlated evolution of two binary characters: are gains or losses concentrated on certain branches of a phylogenetic tree. Evolution 44: 539-557.
57. Maddison WP, Maddison DR. 1992. Mac Clade: Analysis of phylogeny and character evolution (Version 3.04, 1993). Sunderland, Massachusetts: Sinauer Associates.
58. Mason WRM. 1976. The identity of Macrocentrus uniformis Provancher (Nec Cresson), description of a sibling species and a possible grooming organ (Hym.: Braconidae). Le Naturaliste Canadian 103: 513-515.
59. Matthewes RW, Matthewes JR. 1978. Insect behavior. New York: John Wiley & Sons.
60. McCook HC. 1879. The natural history of the agricultural ant of Texas. Philadelphia: Lippincott's Press.
61. Michener CD, Winston ML, Jander R. 1978. Pollen manipulation and related activities and structures in bees of the family Apidae. The University of Kansas Science Bulletin 51: 575-601.
62. Naumann K. 1991. Grooming behaviors and the translocation of queen mandibular gland pheromone on worker honey bee (Apis mellifera L.). Apidologie 22: 523-531.
63. Oi DH, Pereira RM. 1993. Ant behavior and microbial pathogens (Hymenoptera: Formicidae). Florida Entomologist (Symposium: Insect Behavioral Ecology) 76: 63-74.
64. Olberg G. 1959. Das Verhalten der Solitaren Waspen Mitteleuropas. Berlin: Deutscher Verlag Wissenschaften.
65. Pagel MD, Harvey PH. 1989. Comparative methods for examining adaptation depend on evolutionary models. Folia Primatologica 53: 203-220.
66. Prum RO. 1990. Phylogenetic analysis of the evolution of display behavior in the neotropical manakins (Aves: Pipridae). Ethology 84: 202-231.
67. Quicke DLJ, Fitton MG, Ingram S. 1992. Phylogenetic implication of the structure and distribution of ovipositor valvilli in the Hymenoptera. Journal of Natural History 26: 587-608.
68. Rakitov RA. 1992. The leafhopper Vilbasteana oculata (Lindb.) coats its cuticle with a secretion of the Malpighian tubules. Zoologicheskii Zhurnal 71: 49-57. (In Russian).
69. Rasnitsyn AP. 1969. Origin and evolution of lower Hymenoptera. Trudy Paleontologicheskogo Instituta. Academiya Nauk SSSR No. 123: 1-195. (In Russian).
70. Rasnitsyn AP. 1980. Origin and evolution of Hymenoptera. Trudy Paleontologicheskogo Instituta. Academiya Nauk SSSR No. 174: 1-191. (In Russian).
71. Rasnitsyn AP. 1988. An outline of evolution of the hymenopterous insects (Order Vespida). Oriental Insects 22: 115-145.
72. Ridley M. 1983. The explanation of organic diversity: the comparative method and adaptations for mating. Oxford: Oxford University Press.
73. Rita C, Ananthasubramanian KS. 1991. Grooming pattern in Oligotoma saundersii and Pseudembia flava (Embiidina: Insecta). The Indian Zoologist. 15: 55-57.
74. Schönitzer K, Lawitzky G. 1987. A phylogenetic study of the antenna cleaner in Formicidae, Mutillidae, and Tiphiidae (Insecta, Hymenoptera). Zoomorphology 107: 273-285.
75. Schönitzer K, Renner M. 1984. The function of the antenna cleaner of the honeybee Apis mellifica. Apidologie 15: 23-32.
76. Schönitzer K, Dott H, Melzer RR. 1996. The antenna cleaner gland in Messor rufitarsis (Hymenoptera, Formicidae). Tissue & Cell 28: 107-113.
77. Schulze Von H. 1924. Über die Putztatigkeit von Habrobracon: zugleich ein Beitrag zur Sinnes-physiologie und Psychologie dieser Schlupfwespe. Zoologischer Anzeiger 59: 313-323.
78. Sharkey MJ, Wahl DB. 1992. Cladistics of the Ichneumonoidea (Hymenoptera). Journal of Hymenoptera Research 1: 15-24.
79. Shuckard WE. 1866. British bees: an introduction to the study of the natural history and economy of the bees. London: Lovell Reeve & Co.
80. Siegel S. 1956. Nonparametric statistics for the behavioral sciences. Tokyo: McGraw-Hill Kogakusha Ltd.
81. Smith BJB, Valentine BD. 1985. Phylogenetic implications of grooming behavior of cockroaches (Insecta: Blattaria). Psyche 92: 369-385.
82. Sudd JH. 1967. An introduction to the behaviour of ants. London: Edward Arnold Ltd.
83. Sutcliffe JF, McIver SB. 1974. Head, appendage and wing cleaning in blackflies (Diptera: Simuliidae). Annals of the Entomological Society of America 67: 450-452.
84. Szebenyi AL. 1969. Cleaning behaviour in Drosophila melanogaster. Animal Behavior 17: 641-651.
85. Szymanski JS. 1918. Abhandlungen zum Aufbau der Lehre von den Handlungen der Tiere. Pflüger's Archiv fur die Gesamte Physiologie 170: 1-224.
86. Thelen R, Farish DJ. 1977. An analysis of the grooming behavior of wild and mutant strains of Bracon hebetor (Braconidae: Hymenoptera). Behaviour 62: 70-102.
87. Turillazzi PG, Zapponi GA. 1982. Analysis of relationship between locomotion and grooming activity in cockroach (Periplaneta americana). Fragmenta Entomologica, Roma 16: 133-141.
88. Utzeri C, Falchetti E, Raffi R. 1987. Adult behaviour of Lestes barbarus (Fabricus) and L. virens Charpentier) (Zygoptera, Lestidae). Fragmenta Entomologica, Roma 20: 1-22.
89. Valentine BD. 1973. Grooming behaviour in Coleoptera. The Coleopterists Bulletin 27: 63-73.
90. Valentine BD. 1986. Grooming behavior in Embioptera and Zoroptera (Insecta). Ohio Journal of Science 86: 150-152.
91. Valentine BD, Glorioso MJ. 1978. Grooming behaviour in Diplura (Insecta: Apterygota). Psyche 85: 191-200.
92. Vilhelmsen L. 1996. The preoral cavity of lower Hymenoptera (Insecta). Zoologica Scripta 25: 143-170.
93. Waldorf ES. 1978. Variation in self-grooming in male Sinella coeca (Collembola: Entomobryidae). Transactions of the American Microscoptical Society 97: 111-116.
94. Walker ED, Archer WE. 1988. Sequential organization of grooming behaviors of the mosquito, Aedes triseriatus. Journal of Insect Behavior 1: 97-109.
95. Wallis DI. 1962. Behaviour patterns of the ant, Formica fusca. Animal Behaviour 10: 105-111.
96. Weber NA. 1958. Evolution in fungus-growing ants. Proceedings of the Tenth International Congress of Entomology, vol. 2, 459-473.
97. Wenzel JW. 1991. Evolution of nest architecture. In: Ross KG, Matthews RW, eds. The social biology of trasps. Ithaca: Cornell University Press, 480-519.
98. Whitfield JB, Johnson NF, Hamerski MR. 1989. Identity and phylogenetic significance of the metapostnotum in nonaculeate Hymenoptera. Annals of the Entomological Society of America 82: 663-673.
99. Wilson EO. 1962. Behavior of Daceton armigerum (Latreille), with a classification of self-grooming movements in ants. Bulletin of the Museum of Comparative Zoology 127: 401-422.
100. Wilson EO. 1979. The insect societies. Cambridge, Massachusetts: Belknap Press.
101. Zack S. 1978a. The effects of fore leg amputation on head grooming behaviour in the praying mantis, Sphodromantis tineola. Journal of Comparative Physiology 125: 253-258.
102. Zack S. 1978b. Head grooming behaviour in the praying mantis. Animal Behavior 26: 1107-1119.
103. Zack S. 1978c. Description of the behavior of praying mantis with particular reference to grooming. Behavioural Processes 3: 97-105.