Naota Ohsaki

Food Plant Choice of Pieris Butterflies as a Trade‐Off between Parasitoid Avoidance and Quality of Plants

This report assesses the role of specialist parasitoids in providing a major selection pressure for food plant preference in herbivorous insects. Three Pieris butterflies, P. rapae crucivora, P. melete, and P. napi japonica, use different sets of cruciferous larval food plants. P. rape is oligophagous and uses ephemeral plants. P. melete is polyphagous and uses persistent plants, as well as all of the ephemeral plants used by P. rape. On the other hand, P. napi is locally monophagous, using persistent Arabis. We assessed the intrinsic suitability of these crucifers by measuring survival rates, development times, and pupal mass of larvae growing on them at a constant temperature. All of the food plants of P. rape and P. melete are suitable for larvae of the three Pieris species. On the other hand, food plants of P. napi are the least suitable for all three species. Pieris larvae have two specialist parasitoids, the braconid wasp Cotesia glomerata (formerly Apanteles glomeratus) and the tachinid fly Epicampocera succincta. In newly established habitats, P. rapae can avoid both parasitoids. In long-lasting habitats, however, P. rape is heavily parasitized by both parasitoids. P. melete and P. napi, by contrast, live only in long-lasting habitats, where the parasitic pressure is potentially high. However, P. melete can partially avoid parasitism by killing the eggs of C. glomerata by encapsulation, though parasitized by E. succincta. On the other hand, P. napi seems to have evolved behavioral avoidance of parasitoids by specializing on Arabis plants. The different food plant preferences of the three Pieris species can be interpreted as resulting from differences in the balance of a trade-off between parasitoid avoidance and the intrinsic quality of potential food plants to Pieris species.

Avoidance mechanisms of three Pieris butterfly species against the parasitoid wasp Apanteles glomeratus.

Abstract. 1. Experimental studies have shown that larvae of threePieris butterflies, P.rapae L., P.melete Mènètriés and P.napi L., are attacked by a parasitoid wasp, Apanteles glomeratus L. Although P.rapae larvae are parasitized heavily in the field, P.melete and P.napi are infrequently parasitized successfully because they possess mechanisms for encapsulating parasitoid larvae and for avoiding parasitism.

Host‐habitat location by Apanteles glomeratus and effect of food‐plant exposure on host‐parasitism

ABSTRACT. 1. The study investigates differences in the oviposition pattern of a braconid parasitoid, Apanteles glomeratus L., in three Pieris species in Japan in relation to their use of different cruciferous foodplants.

The learning abilities of the white cabbage butterfly,Pieris rapae, foraging for flowers

This study examines the role of learning and memory in the butterflyPieris rapae crucivora Boisduval during foraging for flowers. In an outdoor cage with 6 flower species,P. rapae showed various visiting patterns: some visited only one species, while others visited several species in a day. The foraging process for flowers ofErigeron annuus (L.) Pers. could be divided into two successive steps: (1) landing on the nectaring caputs, and (2) finding the source of nectar in the caput. Butterflies learned to proceed through the two steps more efficiently with successive attempts: they gradually decreased landings on nectarless caputs and probings on the nectarless petals of ligulate flowers respectively. As a result, handling time per unit caputs became shorter, and apparent rewards per unit time, i.e. the efficiency of collecting nectar, increased. In addition, once learned,P. rapae could remember a rewarding flower color for 3 days, which was not interfered with by learning another flower color. This indicates thatP. rapae keeps memory for a period longer than 3 days, and that they can remember at least two flower species as suitable flower resources. Furthermore, data indicated that they sometimes can apply the foraging skills obtained on other flower species to a novel one. These abilities could enable butterflies to easily switch flower species, or to enhance labile preference. It has been known thatP. rapae also shows flower constancy, which may be due to memory constraints. Therefore, they may appropriately use two foraging tactics: visit consistency and labile preference, to get enough nectar according to their circumstances.

Comparative population studies of threePieris butterflies,P. rapae, P. melete andP. napi, living in the same area: I. Ecological requirements for habitat resources in the adults

The adult populations of threePieris butterflies,P. rapae, P. melete andP. napi, were studied in an area of their coexistence throughout the flight seasons by using the mark-and-recapture method. The study area, about 3×1.5 km, was set up in a farm village surrounded by the mountainous area in Inabu, Aichi Prefecture. The habitats were qualified by the four factors, i. e., oviposition plants, adult nector plants, roosting-sites and light conditions. BetweenP. rapae andP. napi, there were sharp differences with regards to overall habitat preferences.P. melete had the widest preferences for all the habitat resources, which overlapped greately with requirements ofP. rapae andP. napi. P. melete andP. rapae showed similar preferences for oviposition plants, but the former preferred shaded habitats while the latter preferred sunny places.P. melete andP. napi, having similar preferences for shaded situations, showed differences in the preferences for oviposition plants. Moreover, three species ofPieris were different in their preferences for adult nector plants. Thus, they were more likely to partition habitat resources rather than competing for them. The habitat structures of each species in respect of time, space and stability to weather changes were much different each other in the same area. The habitat ofP. rapae was temporary, localized and unstable. While, that ofP. melete was more permanent, widespread and stable than that ofP. rapae. P. napi seemed to live in the intermediate habitat, i. e., permanent, localized and stable one.

Cotesia glomerata Female Wasps Use Fatty Acids from Plant–Herbivore Complex in Host Searching

Cotesia glomerata parasitizes early instars of the cabbage butterfly,Pieris rapae, in Japan. Female wasps antennatedRorippa indica leaves damaged by feeding ofP. rapae larva, but ignored artificially damaged leaves. Females also antennated filter paper containingR. indica leaf juice plusP. rapae regurgitant. Chemical analysis revealed five compounds in higher amounts in the infested edges of leaves than in artificially damaged edges. Among them, we identified palmitic acid, oleic acid, and stearic acid. Female wasps antennated filter paper containing each of these three acids. We discuss the function of these acids in the tritrophic context.

Behavioral manipulation of host caterpillars by the primary parasitoid wasp Cotesia glomerata (L.) to construct defensive webs against hyperparasitism

Many parasitoids control the behavior of their hosts to achieve more preferable conditions. Decreasing predation pressure is a main aim of host manipulation. Some parasitoids control host behavior to escape from their enemies, whereas others manipulate hosts into constructing defensive structures as barriers against hyperparasitism. Larvae of the parasitoid wasp Cotesia glomerata form cocoon clusters after egression from the parasitized host caterpillar of the butterfly Pieris brassicae. After the egression of parasitoids, the perforated host caterpillar lives for a short period and constructs a silk web that covers the cocoon cluster. We examined whether these silk webs protect C. glomerata cocoons against the hyperparasitoid wasp Trichomalopsis apanteroctena. In cocoon clusters that were not covered by silk webs (“bare” clusters), only cocoons hidden beneath others avoided hyperparasitism. In covered cocoon clusters, both cocoons hidden beneath others and those with a space between them and the silk web avoided hyperparasitism, whereas cocoons that contacted the silk webs were parasitized. The frequency of cocoons that were hidden beneath others increased with the increasing number of cocoons in a cluster, but the defensive effect of cluster size was thought to be lower than that of silk webs. However, the rate of hyperparasitism did not differ between covered and bare clusters when we allowed the hyperparasitoids to attack the cocoon clusters in an experimental arena. This result was thought to have been caused by low oviposition frequency by these hyperparasitoids. As a result, silk webs did not guard the cocoons from hyperparasitoids in our experiments, but would protect cocoons under high hyperparasitism pressure by forming a space through which the ovipositors could not reach the cocoons.

The role of parasitoids in evolution of habitat and larval food plant preference by three Pieris butterflies

This article attempts to explain that parasitoids provide the evolutionary pressure responsible for relationships between habitat use and larval food plant use in herbivorous insects. Three species of butterflies of the genus Pieris, P. rapae, P. melete, and P. napi use different sets of cruciferous plants. They prefer different habitats composed of similar sets of cruciferous plants. In our study, P. rapae used temporary habitats with ephemeral plants, P. melete used permanent habitat with persistent plants, although they also used temporary habitats, and P. napi used only permanent habitat. The choice experiment in the field cages indicated that each of the three butterfly species avoided oviposition on plants usually unused in its own habitat, but accepted the unused plants which grew outside its own habitat. Their habitat use and plant use were not explained by intrinsic plant quality examined in terms of larval performance. Pieris larvae collected from persistent plants or more long lasting habitats were more heavily parasitized by two specialist parasitoids, the braconid wasp Cotesia glomerata and the tachinid fly Epicampocera succincta. The results suggest that Pieris habitat and larval food plant use patterns can be explained by two principles. The evolution of habitat preference may have been driven by various factors including escape from parasitism. Once habitat preference has evolved, selection favors the evolution of larval food plant preferences by discriminating against unsuitable plants, including those which are associated with high parasitism pressures.

Body temperatures and behavioural thermoregulation strategies of threePieris butterflies in relation to solar radiation

Behavioural thermoregulation of 3Pieris butterfly species,P. rapae, P. melete andP. napi, was examined in relation to the intensity of solar radiation. To evaluate solar radiation intensity, the temperature (Twr) was measured with a mercury thermometer whose bulb was covered with white cloth and exposed to direct sunlight. On clear days, the diurnal air temperature was between 16 and 28°C. The Twt varied between 18 and 45°C, while the temperature in the shade was under 25°C. When the Twt was under 28°C, the body temperatures (Th) of butterflies closely coincided with it. Butterflies with Tbs under 26°C were resting, while those with Tbs between 26 and 28°C were basking. When Twr was between 28 and 40°C, the butterflies were active and their Tbs were always lower than Twr, never exceeding 36°C, though body temperatures could be artificially elevated easily up to the level of Twr. When Twr exceeded 40°C, butterflies showed species-specific heat-avoiding behaviour.P. rapae, whose habitat resources exist in the sun, intercepted solar radiation by closing the wings over the body.P. melete andP. napi, however, whose main habitat resources exist in the shade, moved into the shade. Strictly speaking, it is concluded that both butterflies, in many cases, leave shaded habitats for sunny habitats to elevate their Tb rather than enter the shaded habitats for heat-avoiding.

Sequential rapid adaptation of indigenous parasitoid wasps to the invasive butterfly Pieris brassicae.

Abstract The introduction of a new species can change the characteristics of other species within a community. These changes may affect discontiguous trophic levels via adjacent trophic levels. The invasion of an exotic host species may provide the opportunity to observe the dynamics of changing interspecific interactions among parasitoids belonging to different trophic levels. The exotic large white butterfly Pieris brassicae invaded Hokkaido Island, Japan, and quickly spread throughout the island. Prior to the invasion, the small white butterfly P. rapae was the host of the primary parasitoid Cotesia glomerata, on which both the larval hyperparasitoid Baryscapus galactopus and the pupal hyperparasitoid Trichomalopsis apanteroctena depended. At the time of the invasion, C. glomerata generally laid eggs exclusively in P. rapae. During the five years following the invasion, however, the clutch size of C. glomerata in P. rapae gradually decreased, whereas the clutch size in P. brassicae increased. The field results corresponded well with laboratory experiments showing an increase in the rate of parasitism in P. brassicae. The host expansion of C. glomerata provided the two hyperparasitoids with an opportunity to choose between alternative hosts, that is, C. glomerata within P. brassicae and C. glomerata within P. rapae. Indeed, the pupal hyperparasitoid T. apanteroctena shifted its preference gradually to C. glomerata in P. brassicae, whereas the larval hyperparasitoid B. galactopus maintained a preference for C. glomerata in P. rapae. These changes in host preference may result from differential suitability of the two host types. The larval hyperparasitoid preferred C. glomerata within P. rapae to C. glomerata within P. brassicae, presumably because P. brassicae larvae attacked aggressively, thereby hindering the parasitization, whereas the pupal hyperparasitoid could take advantage of the competition-free resource by shifting its host preference. Consequently, the invasion of P. brassicae has changed the host use of the primary parasitoid C. glomerata and the pupal hyperparasitoid T. apanteroctena within a very short time.