Olfactory attraction of the larval parasitoid, Hyposoter horticola, to plants infested with eggs of the host butterfly, Melitaea cinxia

Abstract

Parasitoids locate inconspicuous hosts in a heterogeneous habitat using plant volatiles, some of which are induced by the hosts. Hyposoter horticola Gravenhost (Hymenoptera: Ichneumonidae) is a parasitoid of the Glanville fritillary butterfly Melitaea cinxia L. (Lepidoptera: Nymphalidae). Melitaea cinxia lays eggs in clusters on leaves of Plantago lanceolata L. (Lamiales: Plantaginaceae) and Veronica spicata L. (Lamiales: Plantaginaceae). The parasitoid oviposits into host larvae that have not yet hatched from the egg. Thus, though H. horticola is a parasitoid of Melitaea cinxia larvae, it must find host eggs on plants that have not been fed on by the larvae. Using a Y-tube olfactometer, the response of H. horticola to odors of Melitaea cinxia and extracts of the attacked plant species were tested. Three week-old eggs (near hatching) were attractive to young H. horticola, but one week-old eggs were attractive only to old or experienced H. horticola. Melitaea cinxia larvae were not attractive. A water extract of P. lanceolata was attractive, but ethanol or hexane extracts were not. None of the extracts of V. spicata were attractive. Leaves of V. spicata were attractive only if harboring eggs, but P. lanceolata leaves with eggs were not. Free flying H. horticola in a large outdoor enclosure were presented with host and plant cues. As in the olfactometer, V. spicata was attractive only when eggs were on it, and P. lanceolata was somewhat attractive with or without eggs. This study shows for the first time that a parasitoid of larvae uses egg volatiles or oviposition-induced plant volatiles, to find host larvae, and that Melitaea cinxia eggs or traces of oviposition induce the production of these volatiles by the plant. Based on the results, and given the natural distribution of the plants and M. cinxia eggs, parasitism of Melitaea cinxia eggs on P. lanceolata would be expected to be low. Instead, under natural conditions, a fraction of the eggs in virtually all egg clusters are parasitized on both plant species. The mismatch between the experimental results and the natural pattern of host-parasitoid interactions is discussed in terms of the expected coupling foraging cues with foraging success.

Figure 1.

Response of old Hyposoter horticola females to one week (1W), two week (2W) and three week (3W) old eggs and newly hatched larvae of their host, Melitaea cinxia (Experiment 1). Asterisks denote statistically significant difference in response between the test and control odor, Chi-square, p < 0.05. Note: N° tested H. horticola: 60, 83, 50 and 50, respectively; N° non-responding H. horticola: 22, 26, 12 and 18, respectively. High quality figures are available online.

Figure 2.

Response of Hyposoter horticola to hexane (H), ethanol (E) and water (W) extracts of leaves of Melitaea cinxia host plants: Veronica spicata (VS) and Plantago lanceolata (PL) (Experiment 2). Asterisks denote statistically significant difference in response between the test and control odor, Chi-square, p < 0.05. Note: N° tested H. horticola on V. spicata in: H = 45, E = 45, and W = 52; and on P. lanceolata in: H = 45, E = 45, and W = 52; N° non-responding H. horticola on V. spicata in: H = 12, E = 13, and W = 9; and on P. lanceolata in H = 6, E = 11, and W = 6. High quality figures are available online.

Figure 3.

Response of Hyposoter horticola to Veronica spicata (VS) and Plantago lanceolata (PL) harboring eggs of their host, Melitaea cinxia (Experiment 3). Asterisks denote statistically significant difference in response between the test and control odor, Chi-square, p < 0.05. Note: N° tested H. horticola: 31 and 31, respectively; N° non-responding H. horticola: 7 and 9, respectively. High quality figures are available online.

Figure 4.

The number of Hyposoter horticola finding host egg clusters in each of the treatments in the free-flying parasitoid experiment. The black portion of each bar is the first trial, and the grey portion is the second trial. The dotted line marks the mean number of H. horticola individuals visiting, excluding the plants alone (P and V) that were not observed to be visited. The two solid lines indicate the SD of the mean. The visited treatments were Plantago lanceolata with eggs on (PE) and next to (P+E) it, Veronica spicata with eggs on (VE) and next to (V+E) it, and eggs alone (E). Note that there were twice as many replicates of the eggs alone treatment (E) as each of the other treatments. High quality figures are available online.