Parasitoid-induced behavioral alterations of Aedes aegypti mosquito larvae infected with mermithid nematodes (Nematoda: Mermithidae)

Journal of Vector Ecology

Volumn 31, Issue 2, 2006, Pages 344-354

  Wise de Valdez, Megan R ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Aedes aegypti; Behavior; Host parasite interactions; Mermithid nematodes; Mosquito larvae

Indexed keywords

AEDES; ANIMAL; ANIMAL BEHAVIOR; ARTICLE; FOOD DEPRIVATION; GROWTH, DEVELOPMENT AND AGING; HOST PARASITE INTERACTION; LARVA; MERMITHOIDEA; PARASITOLOGY; PHYSIOLOGY;

AEDES; ANIMALS; BEHAVIOR, ANIMAL; FOOD DEPRIVATION; HOST-PARASITE RELATIONS; LARVA; MERMITHOIDEA;

AEDES AEGYPTI; HEXAPODA; MERMITHIDA; MERMITHIDAE; NEMATODA; ROMANOMERMIS CULICIVORAX; STRELKOVIMERMIS SPICULATUS;

EID: 33847035133     PISSN: 10811710     EISSN: None     Source Type: Journal    
DOI: 10.3376/1081-1710(2006)31[344:PBAOAA]2.0.CO;2     Document Type: Article

References (71)

1. Achinelly, M.F., M.V. Micieli, G.A. Marti, and J. García. 2004. Susceptibility of neotropical mosquito larvae (Diptera: Culicidae) and non-target aquatic organisms to the entomoparasitic nematodo Strelkovimermis spiculatus Poinar & Camino, 1986 (Nematodo: Mermithidae). Nematology 6: 299-302.
2. Anderson, R.A., J.C. Koella, and H. Hurd. 1999. The effect of Plasmodium yoelii nigeriensis infection on the feeding persistence of Anopheles stephensi Liston throughout the sporogonic cycle. Proc. R. Soc. B 266: 1729-1733.
3. Bailey, C.H. and R. Gordon. 1973. Histopathology of Aedes aegypti (Diptera-Culicidae) larvae parasitized by Reesimermis nielseni (Nematoda-Mermithidae). J. Invertebr. Pathol. 22: 435-441.
4. Ballinger-Crabtree, M.E., W.C. Black IV, and B.R. Miller. 1992. Use of genetic polymorphisms detected by the random-amplified polymorphic DNA polymerase chain reaction (RAPD-PCR) for differentiation and identification of Aedes aegypti subspecies and populations. Am. J. Trop. Med. Hyg. 47: 893-901.
5. Becnel J.J. and M.A. Johnson. 1998. Pathogenicity tests on nine mosquito species and several non-target organisms with Strelkovimermis spiculatus (Nemata Mermithidae). J. Nematol. 30: 411-414.
6. Benton, M.J. and G. Pritchard. 1990. Mayfly locomotory responses to endoparasitic infection and predator presence - the effects on predator encounter rate. Freshwater Biol. 23: 363-371.
7. Bethel, W.M. and J.C. Holmes. 1973. Altered evasive behavior and responses to light in ampipods harboring acanthocephalan cystacanths. J. Parasitol. 59: 945-956.
8. Bethel, W.M. and J.C. Holmes. 1977. Increased vulnerability of amphipods to predation owing to altered behavior induced by larval acanthocephalans. Can. J. Zool. 55: 110-115.
9. Biron, D.G., L. Marché, F. Ponton, H.D. Loxdale, N. Galéotti, L. Renault, C. Joly, and F. Thomas. 2005. Behavioural manipulation in a grasshopper harbouring hairworm: a proteomics approach. Proc. R. Soc. B 272: 2117-2126
10. Blackmore, M.S. 1994. Mermithid parasitism of adult mosquitoes in Sweden. Am. Mid. Nat. 132: 192-198.
11. Blackmore, M.S., R.L. Berry, W.A. Foster, E.D. Walker, T.R. Wilmot, and G.B.Craig. 1993. Records of mosquito-parasitic mermithid nematodes in the North-Central United-States. J. Am. Mosq. Contr. Assoc. 9: 338-343.
12. Brodeur, J. and J.N. McNeil. 1989. Seasonal microhabitat selection by an endoparasitoid through adaptive modification of host behavior. Science 244: 226-228.
13. Campos, R.E. and V.E. Sy. 2003. Mortality in immatures of the floodwater mosquito Ochlerotatus albifasciatus (Diptera: Culicidae) and effects of parasitism by Strelkovimermis spiculatus (Nematoda: Mermithidae) in Buenos Aires Province, Argentina. Mem. Inst. Oswaldo Cruz 98: 199-208.
14. Chow, A. and M. MacKauer. 1999. Altered dispersal behaviour in parasitised aphids: parasitoid-mediated or pathology? Ecol. Entomol. 24: 276-283.
15. Christophers, S.R. 1960. Aedes aegypti (L.) The Yellow Fever Mosquito. Cambridge, Cambridge University Press.
16. Doucet, M.M., C. Laumond, and O. Bain. 1979. Empidomermis riouxi N Sp (Nematoda, Mermithidae). Annal. Parasitol. Hum. Comp. 54: 341-351.
17. Ewing, S.A., J.J. Peterson, and J.S. Afolabi. 1989. Prevalence of parasitism of adult Aedes vexans by a mermithid (Nematoda, Mermithidae) in Oklahoma. J. Am. Mosq. Contr. Assoc. 5: 106-108.
18. Ferguson, H.M. and A.F. Read. 2004. Mosquito appetite for blood is stimulated by Plasmodium chabaudi infections in themselves and their vertebrate hosts. Malaria Journal 3.
19. Fincke, O.M., S.P. Yanoviak, and R.D. Hanschu. 1997. Predation by odonates depresses mosquito abundance in water-filled tree holes in Panama. Oecologia 112: 244-253.
20. Fritz, R.S. 1982. Selection for host modification by insect parasitoids. Evolution 36: 283-288.
21. Galloway, T.D. and R.A. Brust. 1985. The effects of parasitism by Romanomermis-culicivorax (Nematoda, Mermithidae) on growth and development of Aedes vexans (Diptera, Culicidae) in laboratory and field-tests. Can. J. Zool. 63: 2437-2442.
22. García, J.J., R.E. Campos, and A. Maciá. 1994. Prospección de enemigos naturales de Culicidae (Diptera) de la Selva Marginal de Punta Lara (Prov. de Buenos Aires), República Argentina). Rev. Acad. Colomb. Ciencias Exact. Físicas Nat. 19: 209-215.
23. Gaugler, R., S. Wraight, and D. Molloy. 1984. Bionomics of a mermithid parasitizing snow-pool Aedes spp mosquitos. Can. J. Zool. 62: 670-674.
24. Giblin, R.M. and E.G. Platzer. 1985. Romanomermis culicivorax parasitism and the development, growth, and feeding rates of two mosquito species. J. Invert. Zoo. 46: 11-19.
25. Gordon, R. 1981. Mermithid nematodes - Physiological relationships with their insect hosts. J. Nematol. 13: 266-274.
26. Gordon, R., C.H. Bailey, and J.M. Barber. 1974. Parasitic development of mermithid nematode Reesimermis nielseni in larval mosquito Aedes aegypti. Can. J. Zool. 52: 1293-1302.
27. Gordon, R., J.M. Squires, S.J. Babie, and I.R. Burford. 1981. Effects of host diet on Romanomermis culicivorax, a mermithid parasite of mosquitos. J. Nematol. 13: 285-290.
28. Grill, C.P. and S.A. Juliano. 1996. Predicting species interactions based on behaviour: Predation and competition in container-dwelling mosquitoes. J. Anim. Ecol. 65: 63-76.
29. Harlos, J., R.A. Brust, and T.D. Galloway. 1980. Observations on a nematode parasite of Aedes vexans (Diptera, Culicidae) in Manitoba. Can. J. Zool. 58: 215-220.
30. Holmes, J.C. and S. Zohar. 1990. Pathology and host behaviour. In: C.J. Barnard and J.M. Behnke (eds.) Parasitism and Host Behaviour. pp. 35-63. Taylor & Francis Ltd., London.
31. Hurd, H. 2003. Manipulation of medically important insect vectors by their parasites. Annu. Rev. Entomol. 48:141-161.
32. Juliano, S.A. and L. Reminger. 1992. The relationship between vulnerability to predation and behavior of larval treehole mosquitoes: geographic and ontogenetic differences. Oikos 63: 465-476.
33. Juliano, S.A. and M.E. Gravel. 2002. Predation and the evolution of prey behavior: an experiment with tree hole mosquitoes. Behav. Ecol. 13: 301-311.
34. Karban, R. and G. English-Loeb. 1997. Tachinid parasitoids affect host plant choice by caterpillars to increase caterpillar survival. Ecology 78: 603-611
35. Kesavaraju, B. and S.A. Juliano. 2004. Differential behavioral responses to water-borne cues to predation in two container-dwelling mosquitoes. Ann. Entomol. Soc. Am. 97: 194-201.
36. Koella, J.C. and M.J. Packer. 1996. Malaria parasites enhance blood-feeding of their naturally infected vector Anopheles punctulatus. Parasitology 113: 105-109.
37. Koella, J.C., F.L. Sorensen, and R.A. Anderson. 1998. The malaria parasite, Plasmodium falciparum, increases the frequency of multiple feeding of its mosquito vector, Anopheles gambiae. Proc. R. Soc. B 265: 763-768.
38. Koella, J.C., L. Rieu, and R.E.L. Paul. 2002. Stage-specific manipulation of a mosquito's host-seeking behavior by the malaria parasite Plasmodium gallinaceum. Behav. Ecol. 13: 816-820.
39. Maciá, A., J.J. García, and R.E. Campos. 1995. Bionomía de Aedes albifasciatus y Ae. crinifer (Diptera: Culicidae) y sus enemigos naturales en Punta Lara, Buenos Aires. Neotrópica 41: 43-50.
40. Maeyama, T., M. Terayama, and T. Matsumoto. 1994. The abnormal behavior of Colobopsis sp. (Hymenoptera: Formicidae) parasitized by Mermis (Nematoda) in Papua New Guinea. Sociobiology 24: 115-119.
41. Moore, J. 1983. Responses of an avian predator and its isopod prey to an acanthocephalan parasite. Ecology 64: 1000-1015.
42. Moore, J. 1984. Altered behavioral responses in intermediate hosts - an acanthocephalan parasite strategy. Am. Nat. 123: 572-577.
43. Moore, J. 2002. Parasites and the behavior of animals: ecology and evolution. Oxford Univ. Press. New York.
44. Müller, C.B. 1994. Parasitoid induced digging behavior in bumblebee workers. Anim. Behav. 48: 961-966.
45. Nguyen, D., P. Dutilleul, and M.E. Rau. 2002. Impact of nutrition and exposure to the parasite Plagiorchis elegans (Trematoda:Plagiorchiidae) on the development of Aedes aegypti (Diptera : Culicidae): Analysis by time-dependent transition probabilities. Environ. Entomol. 31: 54-64.
46. Petersen, J. J. 1984. Nematode parasites of mosquitoes, In: W.R. Nickle (ed.) Plant and Insect Nematodes. pp. 797-820. Marcel Dekker Inc., New York.
47. Petersen, J.J., H.C. Chapman, and D.B. Woodard. 1967. Preliminary observations on the incidence and biology of a mermithid nematode of Aedes sollicitans (Walker) in Louisiana. Mosq. News 27: 493-498.
48. Poinar, G.O. 1983. Nematode parasites of invertebrates, In: G.O. Poinar (ed.) The Natural History of Nematodes. pp. 161-202. Prentice-Hall Inc., Englewood Cliffs, NJ.
49. Poinar, G.O. Jr. and N.B. Camino. 1986. Strelkovimermis spiculatus n. sp. (Mermithidae: Nematoda) parasitizing Aedes albifasciatus Mac. (Culicidae: Diptera) in Argentina. J. Nematol. 18: 317-319.
50. Poulin, R. 1992. Altered behavior in parasitized bumblebees - Parasite manipulation or adaptive suicide. Anim. Behav. 44: 174-176.
51. Poulin, R. J. Brodeur, and J. Moore. 1994. Parasite manipulation of host behavior - Should hosts always lose? Oikos 70: 479-484.
52. Poulin, R., and D.M. Latham. 2002. Parasitism and the burrowing depth of the beach hopper Talorchestia quoyana (Amphipoda : Talitridae). Anim. Behav. 63: 269-275.
53. Reardon, T.P. and S.R. Lunt. 1989. Parasitism of Adult Aedes vexans by a mermithid (Nematoda, Mermithidae) in Iowa. J. Am. Mosq. Contr. Assoc. 5: 446-447.
54. Schmid-Hempel, R. and C.B. Müller. 1991. Do parasitized bumblebees forage for their colony? Anim. Behav. 41: 910-912.
55. Shamseldean, M.M. and E.G. Platzer. 1989. Romanomermis culicivorax - penetration of larval mosquitoes. J. Invertebr. Pathol. 54: 191-199.
56. Sih, A. 1986. Antipredator responses and the perception of danger by mosquito larvae. Ecology 67: 434-441.
57. Slansky, F.J. 1986. Nutritional ecology of endoparasitic insects and their hosts: An overview. J. Insect Physiol. 32: 255-261.
58. Stamp, N.E. 1981. Behavior of parasitized aposematic caterpillars: advantageous to the parasitoid or host? Am. Nat. 118: 715-725.
59. Steiner, G. 1924. Remarks on a mermithid found parasitic in the adult mosquito (Aedes vexans Meigen) in B.C. Can. Entomol. 56:161-164.
60. Thomas, F.A. Schmidt-Rhaesa, G. Martin, C. Manu, P. Durand, and F. Renaud. 2002. Do hairworms (Nematomorpha) manipulate the water seeking behaviour of their terrestrial hosts? J. Evol. Biol. 15: 356-361.
61. Thompson, S.N. 1990. Physiological alterations during parasitism and their effects on host behaviour, In: C.J. Barnard, and J.M. Behnke, (eds.) Parasitism and Host Behaviour. pp. 64-94. Taylor & Francis Ltd., London.
62. Trpiš, M., W.O. Haufe, and J.A. Shemanchuck. 1968. Mermithid parasites of the mosquito Aedes vexans Meigen in British Columbia. Can. J. Zool. 46: 1077.
63. Vance, S.A. 1996. Morphological and behavioural sex reversal in mermithid-infected mayflies. Proc. R. Soc. B 263: 907-912.
64. Vance, S.A. and B.L. Peckarsky. 1997. The effect of mermithid parasitism on predation of nymphal Baetis bicaudatus (Ephemeroptera) by invertebrates. Oecologia 110: 147-152.
65. Vinson, S.B. and G.F. Iwantsch. 1980. Host regulation by insect parasitoids. Q. Rev. Biol. 55: 143-165.
66. Walker, E.D. and R.W. Merritt. 1991. Behavior of larval Aedes triseriatus (Diptera, Culicidae). J. Med. Entomol. 28: 581-589.
67. Webber, R.A., M.E. Rau, and D.J. Lewis. 1987a. The effects of Plagiorchis noblei (Trematoda, Plagiorchiidae) metacercariae on the susceptibility of Aedes aegypti larvae to predation by guppies (Poecilia reticulata) and meadow voles (Microtus pennsylvanicus). Can. J. Zool. 65: 2346-2348.
68. Webber, R.A., M.E. Rau, and D.J. Lewis. 1987b. The effects of Plagiorchis noblei (Trematoda, Plagiorchiidae) metacercariae on the behavior of Aedes aegypti larvae. Can. J. Zool. 65: 1340-1342.
69. Welch, H.E. 1960. Hydromermis churchillensis n. sp. (Nematoda: Mermithidae) a parasite of Aedes communis (DeG.) from Churchill, Manitoba with observation of its incidence and bionomics. Can. J. Zool. 38: 466-474.
70. Williams, J.K., C.R. Townsend, and R. Poulin. 2001. Mermithid nematode infections and drift in the mayfly Deleatidium spp. (Ephemeroptera). J. Parasitol. 87: 1225-1227.
71. Yasuda, H. and T. Mitsui. 1992. Laboratory observations of prey behavior for prey acquisition by a predator among 3 larval mosquitoes. Ecol. Res. 7: 179-182.