Interactions of native and non-native lady beetle species (Coleoptera: Coccinellidae) with aphid-tending ants in laboratory arenas

Environmental Entomology

Volumn 38, Issue 3, 2009, Pages 846-855

  Finlayson, C J ^a   Alyokhin, A V ^a   Porter, E W ^a  

^a UNIVERSITY OF MAINE   (United States)

Author keywords

Ant; Coccinellid; Native; Natural enemies; Non native

Indexed keywords

AGGRESSION; ANT; APHID; BEETLE; INTERSPECIFIC INTERACTION; NATIVE SPECIES; NATURAL ENEMY;

NORTH AMERICA;

APHIDIDAE; COCCINELLA SEPTEMPUNCTATA; COCCINELLA TRIFASCIATA; COCCINELLIDAE; COLEOMEGILLA MACULATA; COLEOPTERA; FORMICIDAE; HARMONIA AXYRIDIS; HEXAPODA; HIPPODAMIA CONVERGENS; HIPPODAMIA VARIEGATA; MACROSIPHUM EUPHORBIAE; MYRMICA RUBRA; PROPYLEA QUATUORDECIMPUNCTATA; SOLANUM TUBEROSUM; SOLENOPSIS GEMINATA;

ANIMAL; ANT; APHID; ARTICLE; BEETLE; COMPARATIVE STUDY; PREDATION; SPECIES DIFFERENCE; SYMBIOSIS;

ANIMALS; ANTS; APHIDS; BEETLES; PREDATORY BEHAVIOR; SPECIES SPECIFICITY; SYMBIOSIS;

EID: 68049083501     PISSN: 0046225X     EISSN: None     Source Type: Journal    
DOI: 10.1603/022.038.0338     Document Type: Article

References (91)

1. Alyokhin, A., and G. Sewell. 2004. Changes in lady beetle community following the establishment of three alien species. Biol. Invasions 6: 463-471.
2. Angalet, G. W., and J. R. Jacques. 1975. The establishment of Coccinella septempunctata L. in the continental United States. U. S. Dep. Agric. Co-op. Econ. Insect Rep. 25: 883-884.
3. Angalet, G. W., J. M. Tropp, and A. N. Eggart. 1979. Coccinella septempunctata in the United States: recolonizations and notes on its ecology. Environ. Entomol. 8: 896-901.
4. Attygalle, A. B., M. C. Cammaerts, and E. D. Morgan. 1983a. Dufour gland secretions of Myrmica rugulosa and Myrmica schencki workers. J. Insect. Physiol. 29: 27-32.
5. Attygalle, A. B., R. P. Evershed, E. D. Morgan, and M. C. Cammaerts. 1983b. Dufour gland secretions of workers of the ants Myrmica sulcinodis and Myrmica lobicomis, and comparison with six other species in Myrmica. Insect. Biochem. 13: 507-512.
6. Auclair, J. L. 1963. Aphid feeding and nutrition. Annu. Rev. Entomol. 8: 439-490.
7. Bartlett, B. R. 1961. The influence of ants upon parasites, predators, and scale insects. Ann. Entomol. Soc. Am. 54: 543-551.
8. Bhatkar, A. P. 1982. Orientation and defense of ladybeetles (Coleoptera, Coccinellidae) following ant trails in search of aphids. Folia Entomol. Mex. 53: 75-85.
9. Blackman, R. L., and V. F. Eastop. 1984. Aphids on the world's crops an identification and information guide. Wiley, New York.
10. Bradley, G. A. 1973. Effect of Formica obscuripes (Hymenoptera: Formicidae) on the predator-prey relationship between Hyperaspis congressis (Coleoptera: Coccinellidae) and Toumeyella numismaticum (Homoptera: Coccidae). Can. Entomol. 105:1113-1118.
11. Brown, M. W. 2003. Intraguild responses of aphid predators on apple to the invasion of an exotic species, Harmonia axyridis. BioControl 48: 141-153.
12. Brown, M. W., and S. S. Miller. 1998. Coccinellidae (Coleoptera) in apple orchards of eastern West Virginia and the impact of invasion by Harmonia axyridis. Entomol. News 109:136-142.
13. Buckley, R. 1987. Interactions involving plants, Homoptera and ants. Annu. Rev. Ecol. Syst. 18:111-135.
14. Cammaerts, M. C. 1978. Recruitment to food in Myrmica rubra L. Biol. Behav. 4: 159-172.
15. Cammaerts, M. C. 1984. Probable functions for a previously unrecognized pheromone in ants of the genus Myrmica. Behav. Process. 9:135-145.
16. Cammaerts, M. C. 1992. Anatomical origin and isolation of an ethological factor found on the last sternite of the workers of Myrmica rubra L. (Formicidae, Myrmicinae). J. Insect. Physiol. 38: 101-110.
17. Cammaerts, M. C., R. P. Evershed, and E. D. Morgan. 1981a. Comparative study of pheromones emitted by different species of Myrmica, pp. 185-192. In P. E. Howse and J. L. Clement (eds), Biosystematics of social insects. Academic, London, United Kingdom.
18. Cammaerts, M. C., R. P. Evershed, and E. D. Morgan. 1981b. Comparative study of the Dufour gland secretions of workers of four species of Myrmica ants. J. Insect Physiol. 27: 59-65.
19. Cammaerts-Tricot, M. C., E. D. Morgan, R. C. Tyler, and J. C. Braekman. 1976. Dufour's gland secretion of Myrmica rubra: chemical, electrophysiological, and ethological studies. J. Insect Physiol. 22: 927-932.
20. Carlin, N. F., and B. Holldobler. 1986. The kin recognition system of carpenter ants (Camponotus spp.). I. Hierarchical cues in small colonies. Behav. Ecol. Sociobiol. 19: 123-134.
21. Cavill, G. W. K., and P. L. Robertson. 1965. Ant venoms, attractants, and repellents. Science 149:1337-1345.
22. Chantal, C. 1972. Additions a la faune coleopterique du Quebec. Nat. Can. 99: 243-244.
23. Chapin, E. A. 1966. A new species of Myrmecophilous Coccinellidae, with notes on other Hyperspini (Coleoptera). Psyche 73: 278-283.
24. Chapin, J. B., and V. A. Brou. 1991. Harmonia axyridis (Pallas) the third species of the genus to be found in the United States (Coleoptera: Coccinellidae). Proc. Entomol. Soc. Wash. 93: 630-635.
25. Charles, J. G. 1993. A survey of mealybugs and their natural enemies in horticultural crops in North Island, New Zealand, with implications for biological control. Biocontrol Sci. Technol. 3: 405-418.
26. Collingwood, C. A. 1979. The Formicidae (Hymenoptera) of Fennoscandia and Denmark. Fauna Entomol. Scand. 8: 1-174.
27. Colunga-Garcia, M., and S. H. Gage. 1998. Arrival, establishment, and habitat use of the multicolored Asian lady beetle (Coleoptera: Coccinellidae) in a Michigan landscape. Environ. Entomol. 27:1574-1580.
28. Conover, W. J., and R. L. Iman. 1981. Rank transformations as a bridge between parametric and non-parametric statistics. Am. Stat. 35:124-129.
29. Corbara, B., A. Dejean, and P. Cerdan. 1999. A myrmecophilous ladybird associated with the arboricolous ant Dolichoderus bidens (Dolichoderinae). Actes Colloques Insect Soc. 12: 171-179.
30. Cormier, C. M., T. A. Forbes, T. A. Jones, R. D. Morrison, and D. B. McCorquodale. 2000. Alien invasion: the status of non-native lady beetles (Coleoptera: Coccinellidae) in industrial Cape Breton, Nova Scotia. Northeast. Nat. 7: 241-247.
31. Cottrell, T. E., and K. V. Yeargan. 1998. Intraguild predation between an introduced lady beetle, Harmonia axyridis (Coleoptera: Coccinellidae), and a native lady beetle, Coleomegilla maculata (Coleoptera: Coccinellidae). J. Kans. Entomol. Soc. 71:159-163.
32. Czechowski, W., A. Radchenko, and W. Czechowska. 2002. The ants (Hymenoptera, Formicidae) of Poland. Museum and Institute of Zoology PAS, Warszawa, Poland.
33. Day, W. H., D. R. Prokrym, D. R. Ellis, and R. J. Chianese. 1994. The known distribution of the predator Propylea quatuordecimpunctata (Coleoptera: Coccinellidae) in the United States, and thoughts on the origin of this species and five other exotic lady beetles in Eastern North America. Entomol. News 105: 244-256.
34. De Clercq, P., I. Peeters, G. Vergauwe, and O. Thas. 2003. Interactions between Podisus maculiventris and Harmonia axyridis, two predators used in augmentative biological control in greenhouse crops. BioControl 48: 39-55.
35. Dixon, A.F.G. 2000. Insect predator-prey dynamics: ladybird beetles and biological control. Cambridge University Press, Cambridge, United Kingdom.
36. Dreistadt, S. H., and M. L. Flint. 1996. Melon aphid (Ho-moptera: Aphididae) control by inundative convergent lady beetle (Coleoptera: Coccinellidae) release on chrysanthemum. Environ. Entomol. 25: 688-697.
37. Dutcher, J. D., P. M. Estes, and M. J. Dutcher. 1999. Interaction in entomology: aphids, aphidophaga and ants in pecan orchards. J. Entomol. Sci. 34: 40-56.
38. Elliot, N., R. Kieckhefer, and W. Kauffman. 1996. Effects of an invading coccinellid on native coccinellids in an agricultural landscape. Oecologica 105: 537-544.
39. Ellis, D. R., D. R. Prokrym, and R. G. Adams. 1999. Exotic lady beetle survey in northeastern United States: Hippodamia variegata and Propylea quatuordecimpunctata (Coleoptera: Coccinellidae). Entomol. News 110: 73-84.
40. Elmes, G. W. 1975. Population studies on the genus Myrmica (Hymenoptera, Formicidae), with special reference to southern England. PhD thesis, University of London, London, United Kingdom.
41. Elmes, G. W., J. C. Wardlaw, M. K. Nielsen, V. E. Kipyatkov, E. B. Lopatina, A.G. Radchenko, and B. Barr. 1999. Site latitude influences on the respiration rate, fat content and the ability of worker ants to rear larvae: a comparison of Myrmica rubra (Hymenoptera: Formicidae) populations over their European range. Eur. J. Entomol. 96:117-123.
42. Evershed, R. P., E. D. Morgan, and M. C. Cammaerts. 1981. Identification of the trail pheromone of the ant Myrmica rubra L., and related species, Naturwissenschaften 68: 374-376.
43. Evershed, R. P., E. D. Morgan, and M. C. Cammaerts. 1982. 3-ethyl-2,5-dimethylpyrazine, the trail pheromone from the venom gland of eight species of Myrmica ants. Insect Biochem. 12: 383-391.
44. Finlayson, C. J., K. M. Landry, and A. V. Alyokhin. 2008. Abundance of native and non-native lady beetles (Coleoptera: Coccinellidae) in different habitats in Maine. Ann. Entomol. Soc. Am. 101:1078-1087.
45. Garnas, J. R. 2005. European fire ants on Mount Desert Island, Maine: population structure, mechanisms of competition and community impacts of Myrmica rubra L. (Hymenoptera: Formicidae). PhD thesis, University of Maine, Orono, ME.
46. Garnas, J. R., F. A. Drummond, and E. Groden. 2007. Intercolony aggression within and among local populations of the invasive ant, Myrmica rubra (Hymenoptera: Formicidae), in coastal Maine. Environ. Entomol. 36: 105-113.
47. Gonzalez Hernandez, H., M. W. Johnson, and N. J. Reimer. 1999. Impact of Pheidole megacephala (F.) (Hymenoptera: Formicidae) on the biological control of Dysmicoc-cusbreoipes (Cockerell) (Homoptera: Pseudococcidae). Biol. Control 15: 145-152.
48. Gordon, R. D. 1985. The Coccinellidae (Coleoptera) of America north of Mexico. J.N.Y. Entomol. Soc. 93:1-912.
49. Gordon, R. D., and N. J. Vandenberg. 1991. Field guide to recently introduced species of Coccinellidae (Coleoptera) in North America, with a revised key to North American genera of Coccinellini. Proc. Entomol. Soc. Wash. 93: 845-864.
50. Groden, E., F. A. Drummond, J. Garnas, and A. Franceour. 2005. Distribution of an Invasive Ant, Myrmica rubra (Hymenoptera: Formicidae), in Maine. J. Econ. Entomol. 98:1774-1784.
51. Hanks, L. M., and C. S. Sadof. 1990. The effect of ants on nymphal survivorship of Coccus viridis (Homoptera: Coccidae). Biotropica 22: 210-213.
52. Hironori, Y., and S. Katsuhiro. 1997. Cannibalism and interspecific predation in two predatory ladybirds in relation to prey abundance in the field. Entomophaga 42: 53-163.
53. Hodek, I. 1973. Biology of Coccinellidae. Dr. W. Junk N.V., Publisher, The Hague, The Netherlands.
54. Hodek, I., and A. Honěk. 1996. Ecology of Coccinellidae. Kluwer Academic, Boston, MA.
55. Hoebeke, E. R., and A. G. Wheeler. 1996. Adventive lady beetles (Coleoptera: Coccinellidae) in the Canadian Maritime Provinces, with new eastern U.S. records of Harmonia quadripunctata. Entomol. News 107: 281-290.
56. Holldobler, B., and E. O. Wilson. 1990. The ants. Belknap Press of the Harvard University, Cambridge, MA.
57. Holway, D. A., A. V. Suarez, and T. J. Case. 1998. Loss if intraspecific aggression in the success of a widespread invasive social insect. Science 282: 949-952.
58. Hough-Goldstein, J., J. Cox, and A. Armstrong. 1996. Podisus maculiventris (Hemiptera: Pentatomidae) predation on ladybird beetles (Coleoptera: Coccinellidae). Fla. Entomol. 79:64-68.
59. Jahn, G. C., and J. W. Beardsley. 1994. Big-headed ants, Pheidole megacephala: interference with the biological control of mealybugs, pp. 199-205. In D. F. Williams (ed.), Exotic ants: biology, impact, and control of introduced species. Westview Press, Boulder, CO.
60. Jiggins, C., M. Majerus, and U. Gough. 1993. Ant defence of colonies of Aphis fabae Scopoli (Hemiptera: Aphidadae), against predation by ladybirds. Br. J. Entomol. Nat. Hist. 6: 129-137.
61. Kajita, Y., F. Takano, H. Yasuda, and B. K. Agarwala. 2000. Effects of indigenous ladybird species (Coleoptera: Coccinellidae) on the survival of an species in relation to prey abundance. Appl. Entomol. Zool. 35: 473-479.
62. Kaplan, I., and M. D. Eubanks. 2002. Disruption of cotton aphid (Homoptera: Aphididae): natural enemy dynamics by red imported fire ants (Hymenoptera: Formicidae). Environ. Entomol. 31: 1175-1183.
63. Koch, R. L. 2003. The multicolored Asian lady beetle, Harmonia axyridis: a review of its biology, uses in biological control, and non-target impacts. J. Insect Sci. 3: 32.
64. Lynch, L. D., H.M.T. Hokkanen, D. Babendreier, F. Bigler, G. Burgio, Z. H. Gao, S. Kuske, A. Loomans, I. Menzler-Hokkanen, M. B. Thomas, et al. 2001. Insect biological control and non-target effects: a European perspective, pp. 99-125. In E. Wajnberg, J. K. Scott, and P. C. Quinby (eds.), Evaluating indirect ecological effects of biological control. CABI Publishing, Wallingford, United Kingdom.
65. Michaud J.P. 2002. Invasion of the Florida citrus ecosystem by Harmonia axyridis (Coleoptera: Coccinellidae) and asymmetric competition with a native species, Cycloneda sanguinea. Environ. Entomol. 31: 827-835.
66. Morgan, E. D., R. C. Tyler, and M. C. Cammaerts. 1977. Identification of the components of Dufour gland secretion of the ant Myrmica rubra and responses to them. J. Insect Physiol. 23: 511-515.
67. Reimer, N.J., M.L. Cope, and G. Yasuda. 1993. Interference of Pheidole megacephala (Hymenoptera: Formicidae) with biological control of Coccus viridis (Homoptera: Coccidae) in coffee. Environ. Entomol. 22: 483-488.
68. Saito, T., and S. Bjørnson. 2006. Horizontal transmission of a microsporidium from the convergent lady beetle, Hip-podamia convergens Guérin-Méneville (Coleoptera: Coccinellidae), to three coccinellid species of Nova Scotia. Biol. Control 39: 427-433.
69. Sakuratani, Y., Y. Marsumoto, M. Oka, T. Kubo, A. Fuji, M. Uotani, and T. Teraguchi. 2000. Life history of Adalia bipunctata (Coleoptera: Coccinellidae) in Japan. Eur. J. Entomol. 97: 555-558.
70. Seifert, B. 1996. Ameisen beobachten, bestimmen. Natur-buch-Verlag, Augsburg, Germany.
71. Schaefer, P. W., R. J. Dysart, and H. B. Specht. 1987. North American distribution of Coccinella septempunctata (Coleoptera: Coccinellidae) and its mass appearance in coastal Delaware. Environ. Entomol. 16: 368-373.
72. Shands, W. A., G. W. Simpson, H. E. Wave, and C. C. Gordon. 1972. Importance of arthropod predators in controlling aphids on potatoes in northeastern Maine. University of Maine, Orono, ME.
73. Sloggett, J. J., and M.E.N. Majerus. 2000. Aphid-mediated coexistence of ladybirds (Coleoptera: Coccinellidae) and the wood ant Formica rufa: seasonal effects, interspecific variability and the evolution of a coccinellid myrmeco-phile. Oikos 89: 345-359.
74. Sloggett, J. J., R. A. Wood, and M.E.N. Majerus. 1998. Adaptations of Coccinella magnifica Redtenbacher, a myrmecophilous Coccinellid, to aggression by wood ants (Formiia rufa Group). I. Adult behavioral adaptation, its ecological context and evolution. J. Insect Behav. 11: 889-904.
75. Sloggett, J. J., A. Manica, M. J. Day, and M.E.N. Majerus. 1999. Predation of ladybirds (Coleoptera: Coccinellidae) by wood ants, Formica rufa L. (Hymenoptera: Formicidae). Entomol. Gaz. 50: 217-221.
76. Suarez, A. V., N. D. Tsutsui, D. A. Holway, and T. J. Case. 1999. Behavioral and genetic differentiation between native and introduced populations of the Argentine ant. Biol. Invasions 1: 43-53.
77. Takahashi, K. 1989. Intra- and interspecific predations of lady beetles in spring alfalfa fields. Jpn. J. Entomol. 57: 199-203.
78. Tedders, W. L., and P. W. Schaefer. 1994. Release and establishment of Harmonia axyridis (Coleoptera: Coccinellidae) in the southeastern United States. Entomol. News 105: 228-243.
79. Turnock, W. J., I. L. Wise, and F. O. Matheson. 2003. Abundance of some native coccinellids (Coleoptera: Coccinellidae) before and after the appearance of Coccinella septempunctata. Can. Entomol. 135: 391-404.
80. Tursch, B., D. Daloze, M. Dupont, J. M. Pasteels, and M. C. Tricot. 1971. A defensive alkaloid in a carnivorous beetle. Experientia 27: 1380-1381.
81. Vinson, S. B., and T. A. Scarborough. 1989. Impact of the imported fire ant on laboratory populations of cotton aphid (Aphis gossypii) predators. Fla. Entomol. 72:107-111.
82. Volkl, W., J. Woodring, M. K. Fisher, M. W. Lorenz, and K. H. Hoffmann. 1999. Ant-aphid mutualism: the impact of honeydew production and honeydew sugar composition on ant preferences. Oecologia (Berl.) 118: 483-491.
83. Way, M. S. 1963. Mutualism between ants and honeydew producing homoptera. Annu. Rev. Entomol. 8: 307-344.
84. Wheeler, A. G. 1990. Propylea quatuordecimpunctata: additional records of an adventive lady beetle (Coleoptera: Coccinellidae). Entomol. News 101:164-166.
85. Wheeler, A. G. 1993. Establishment of Hippodamia variegata and new records of Propylea quaruordecimpunctata in the eastern United States. Entomol. News 104:102-110.
86. Wheeler, A. G., and C. A. Stoops. 1996. Status and spread of Palearctic lady beetles Hippodanria variegata and Propylea quatuordecimpunctata (Coleoptera: Coccinellidae) in PA, 1993-1995. Entomol. News 107: 291-298.
87. Wheeler, W. M. 1908. A European ant (Myrmica laevinodis) introduced into Massachusetts. J. Econ. Entomol. 1: 336-339.
88. Yasuda, H., and N. Ohnuma. 1999. Effect of cannibalism and predation on the larval performance of two ladybird beetles. Entomol. Exp. Appl. 93: 63-67.
89. Yasuda, H., T. Kikuchi, P. Kindlmann, and S. Sato. 2001. Relationships between attack and escape rates, cannibalism, and intraguild predation in larvae of two predatory ladybirds. J. Insect Behav. 14: 373-384.
90. Yasuda, H., E. W. Evans, Y. Kajita, K. Urakawa, and T. Takizawa. 2004. Asymmetric larval interactions between introduced and indigenous ladybirds in North America. Oecologia (Berl.) 141:1432-1939.
91. Zar, J. H. 1999. Biostatistical analysis, 4th ed. Prentice Hall, Upper Saddle River, NJ.