Oviposition preference of aphidophagous hoverflies toward oviposition site quality: The presence of intra- and interspecific competitor, glucosinolate content, and prey species

다국어 초록 (Multilingual Abstract)

The selection of oviposition sites by aphidophagous insects is complex because of tritrophic interactions among host plant, aphid, and natural enemies. Several factors are known to affect the choice of oviposition site by aphidophagous hoverflies. The decisions of ovipositing females about where to lay their eggs are even more important in insects whose newly hatched offspring have limited dispersal ability, such as most aphidophages. In this study, we focused on the oviposition responses of two generalist aphidophagous syrphids (Eupeodes luniger and Episyrphus balteatus) toward host plant–aphid combinations differing in sinigrin content and the presence of intra- and interspecific competitors. The oviposition preference of Eupeodes luniger was significantly influenced in a reverse manner by the presence of intraguild competitors and also by the sinigrin content of host plants (P b 0.0001 for both factors). Likewise, the overall proportion of eggs laid by female Episyrphus balteatus was greater on aphids with relatively low levels of sinigrin. Our findings help in understanding the factors governing the oviposition responses of aphidophagous predators.

참고문헌 (Reference)

1 Chambers, R. J., "World Crop Pests: Aphids, Their Biology, Natural Enemies, and Control" Elsevier 259-270, 1988

2 Volk, S., "Untersuchungen zur Eiablage von Syrphus corollae Fabr. (Diptera:Syrphidae)" 54 : 365-386, 1964

3 Cortesero, A. M., "Understanding and manipulating plant attributes to enhance biological control" 17 : 35-49, 2000

4 Budenberg, W. J., "The role of honeydew as an ovipositional stimulant for two species of syrphids" 64 : 57-61, 1992

5 Ninkovic, V., "The influence of aphid-induced plant volatiles on ladybird beetle searching behavior" 21 (21): 191-195, 2001

6 Benestad Hågvar, E., "The effect of intra- and interspecific larval competition for food (Myzus persicae) on the development at 20 °C of Syrphus ribesii and Syrphus corollae (Diptera, Syrphidae)" 17 (17): 71-77, 1972

7 Sadeghi, H., "The effect of egg load and host deprivation on oviposition behaviour in aphidophagous hoverflies" 25 (25): 101-108, 2000

8 Fahey, J. W., "The chemical diversity and distribution of glucosinolates and isothiocyanates among plants" 56 (56): 5-51, 2001

9 Gilbert, F., "Syrphid aphidophagous predators in a food-web context" 102 (102): 325-333, 2005

10 Dixon, T. J., "Studies on behaviour of Syrphidae (Diptera)" 111 : 57-80, 1959

11 Chandler, A. E. F., "Some factors influencing the occurrence and site of oviposition by aphidophagous Syrphidae (Diptera)" 61 : 435-446, 1968

12 Nishida, R., "Sequestration of defensive substances from plants by Lepidoptera" 47 : 57-92, 2002

13 Bell, W. J., "Searching behavior patterns in insects" 35 : 447-467, 1990

14 Almohamad, R., "Searching and oviposition behavior of aphidophagous hoverflies (Diptera: Syrphidae): a review" 13 (13): 467-481, 2009

15 Harmel, N., "Role of terpenes from aphid-infested potato on searching and oviposition behavior of Episyrphusbalteatus" 14 : 57-63, 2007

16 Hopkins, R. J., "Role of glucosinolates in insect-plant relationships and multitrophic interactions" 54 : 57-83, 2009

17 Ali Reza Amiri-Jami, "Responses of Episyrphus balteatus DeGeer (Diptera: Syrphidae) in relation to prey density and predator size" 한국응용곤충학회 17 (17): 207-211, 2014

18 Michaud, J. P., "Repellency of conspecific and heterospecific larval residues to Hippodamiaconvergens (Coleoptera: Coccinellidae) ovipositing on sorghum plants" 104 : 399-405, 2007

19 Kos, M., "Prey-mediated effects of glucosinolates on aphid predators" 36 : 377-388, 2011

20 Almohamad, R., "Predatory hoverflies select their oviposition site according to aphid host plant and aphid species" 125 (125): 13-21, 2007

21 Gols, R., "Plant-mediated effects in the Brassicaceae on the performance and behaviour of parasitoids" 8 : 187-206, 2009

22 Singer, M. C., "Plant-feeding insect" Springer-Verlag 65-94, 1986

23 Ode, P. J., "Plant chemistry and natural enemy fitness: effects on herbivore and natural enemy interactions" 51 : 163-185, 2006

24 Optiz, S. E. W., "Plant chemistry and insect sequestration" 19 (19): 117-154, 2009

25 Ruzicka, Z., "Oviposition-deterring pheromone in chrysopids: intra- and interspecific effects" 93 : 161-166, 1996

26 Ruzicka, Z., "Oviposition-deterring pheromone in Chrysopa oculata (Neuroptera, Chrysopidae)" 91 : 361-370, 1994

27 Scholz, D., "Oviposition site selection of Episyrphus balteatus" 94 : 149-158, 2000

28 Sadeghi, H., "Oviposition preferences of aphidophagous hoverflies" 25 : 91-100, 2000

29 Vanhaelen, N., "Oviposition preferences of Episyrphus balteatus. Meded. Fac. Landbouwwet." 66 (66): 269-275, 2001

30 Putra, N. S., "Oviposition preference of two hoverfly species in response to risk of intraguild predation" 44 : 29-36, 2009

31 Sutherland, J. P., "Oviposition behaviour and host colony size discrimination in Episyrphus balteatus (Diptera: Syrphidae)" 91 (91): 411-418, 2001

32 Amiri-Jami, A. R., "On the role of sinigrin (mustard oil) in a tritrophic context: plant-aphid-aphidophagous hoverfly" 41 : 138-142, 2016

33 Francis, F., "Olfactory responses to aphid and host plant volatile releases: (E)-beta-farnesene an effective kairomone for the predator Adalia bipunctata" 30 : 741-755, 2004

34 Janssen, A., "Odour-mediated avoidance of competition in Drosophila parasitoids: the ghost of competition" 73 : 356-366, 1995

35 Frechette, B., "Intraguild predation between syrphids and mirids: who is the prey? Who is the predator?" 52 : 175-191, 2007

36 Hindayana, D., "Intraguild predation among the hoverfly Episyrphus balteatus De Geer (Diptera: Syrphidae) and other aphidophagous predators" 20 : 236-246, 2001

37 Birch, M. C., "Influence of chemically mediated behavior on host tree colonization by four cohabiting species of bark beetles" 5 : 395-414, 1980

38 Sadeghi, H., "Individual variation in oviposition preference and its interaction with larval performance, in an insect predator" 118 (118): 405-411, 1999

39 Sadeghi, H., "Host preferences of aphidophagous hoverflies from field distribution of their larvae" 16 : 1-16, 2014

40 Ode, P. J., "Host plant, host-plant chemistry, and the polyembryonic parasitoid Copidosoma sosares: indirect effects in a tritrophic interaction" 104 : 388-400, 2004

41 Honek, A., "Habitat preferences of aphidophagous coccinellids (Coleoptera)" 30 : 253-264, 1985

42 Hodek, I., "Habitat and food specificity in aphidophagous predators" 3 : 91-100, 1993

43 Almohamad, R., "Evaluation of hoverfly Episyrphus balteatus DeGeer (Diptera: Syrphidae) oviposition behaviour toward aphid-infested plants using a leaf disc system" Ghent University 71 : 403-412, 2006

44 Ruzicka, Z., "Effects of oviposition-deterring pheromone and allomones on Aphidoletesaphidimyza (Diptera: Cecidomyiidae)" 95 : 211-216, 1998

45 Agarwala, B. K., "Effects of conspecific and heterospecific competitors on feeding and oviposition of a predatory ladybird: a laboratory study" 106 : 219-226, 2003

46 Francis, F., "Effects of allelochemicals from first (Brassicaceae) and second (Myzus persicae and Brevicoryne brassicae) trophic levels on Adalia bipunctata" 27 : 243-256, 2001

47 Almohamad, R., "Discrimination of parasitized aphids by a hoverfly predator: effects on larval performance, foraging, and oviposition behavior" 128 : 73-80, 2008

48 Chaplin-Kramer, R., "Chemically mediated tritrophic interactions: opposing effects of glucosinolates on a specialist herbivore and its predators" 48 : 880-887, 2011

49 Branquart, E., "Cannibalism in Episyrphus balteatus (Dipt.: Syrphidae)" 42 (42): 145-152, 1997

50 Byers, J. A., "Attractive and inhibitory pheromones produced in the bark beetle, Dendroctonus brevicomis, during host colonization:regulation of inter- and intraspecific competition" 10 : 861-877, 1984

51 Doumbia, M., "Assessment of patch quality by ladybirds: role of larval tracks" 113 : 197-202, 1998

52 Almohamad, R., "Assessment of oviposition site quality by aphidophagous hoverflies: reaction to conspecific larvae" 79 : 589-594, 2010

53 Dicke, M., "Are herbivore-induced plant volatiles reliable indicators of herbivore identity to foraging carnivorous arthropods?" 91 (91): 131-142, 1999

54 Sadeghi, H., "Aphid suitability and its relationship to oviposition preference in predatory hoverflies" 69 : 771-784, 2000

55 Verheggen, F. J., "Aphid and plant volatiles induce oviposition in an aphidophagous hoverfly" 34 : 301-307, 2008

56 Frechette, B., "Age and experience influence patch assessment for oviposition by an insect predator" 29 (29): 578-583, 2004

57 Courtney, S. P., "A generalmodel for individual host selection" 55 : 55-65, 1989

58 Amorós-Jiménez, R., "A differential role of volatiles from conspecific and heterospecific competitors in the selection of oviposition sites by the aphidophagous hoverfly Sphaerophoria rueppellii" 41 (41): 493-500, 2015