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Shoot Characteristics Affect Oviposition Preference of the Willow Spittlebug Aphrophora Pectoralis (Homoptera: Aphrophoridae)

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Shoot Characteristics Affect Oviposition Preference of the Willow Spittlebug Aphrophora Pectoralis (Homoptera: Aphrophoridae) ECOLOGY AND POPULATION BIOLOGY Shoot Characteristics Affect Oviposition Preference of the Willow Spittlebug Aphrophora pectoralis (Homoptera: Aphrophoridae) 1 2 AKIYOSHI NOZAWA AND TAKAYUKI OHGUSHI Ann. Entomol. Soc. Am. 95(5): 552Ð557 (2002) ABSTRACT The relationships of shoot abscission, shoot toughness, and egg parasitism with shoot lengthwere investigated in relation to oviposition preference by thewillow spittlebug Aphrophora pectoralis Matsumura on Salix miyabeana, S. sachalinensis, and S. integra. Spittlebugs strongly preferred shoots Ͼ20 cm long even though this size class was a small proportion of all shoots. Oviposition increased with shoot length up to 40 cm but leveled off, or even decreased, on longer shoots. Shoot abscission rate decreased and toughness increased with increasing shoot length, but egg parasitism was not affected. Spittlebug oviposition preference is therefore likely to be affected by shoot abscission and shoot toughness. KEY WORDS Salix species, shoot abscission, shoot toughness, egg parasitism, xylem sucker OVIPOSITION PREFERENCE IS FUNDAMENTAL to understand- tree during winter. Because A. pectoralis eggs over- ing herbivore population dynamics (Ohgushi 1992, winter inside shoots, shoot abscission results in egg Price et al. 1995) and host plant selection (Thompson death. Spittlebug nymphs of A. pectoralis penetrate and Pellmyr 1991, Mayhew 1997). The patterns of shoots with their stylets to feed, and feeding sites are herbivore attack on host plants have been explained restricted by stem tissue hardness in the spittlebug by plant traits (e.g., age, growthrate, genotypes, re- Philaenus spumarius L. (Hoffman and McEvoy 1986, source quality, and chemical compounds) (Tahvanainen McEvoy 1986). Therefore, shoot abscission and tough- et al. 1985, Price et al. 1987a, Brodbeck et al. 1990, Woods ness may have signiÞcant roles in determining the et al. 1996, Craig et al. 1999, Dorn et al. 2001). oviposition preference for long shoots. Recently, Price (1991) proposed the plant vigor Natural enemies are another important factor de- hypothesis that herbivorous insects attack vigorous termining oviposition preference of herbivorous in- plants or plant modules more frequently than slower sects (enemy-free space hypothesis, see Thompson growing plants or plant modules. Many studies testing 1988). For example, the mistletoe butterßy Ogyris the plant vigor hypothesis have focused on galling amaryllis Hewitson has an oviposition preference for insects (Price et al. 1995, Price et al. 1997). For ex- plants of the genus Amyema tended by ants, even ample, the galling sawßy Euura mucronata Hartig ex- though the plants are low quality for larvae (Atsatt hibited a strong oviposition preference for longer, 1981). This preference apparently evolved because more vigorous shoots on which larval survival was high the presence of ants on the plants decreases egg par- due to high food quality in rapidly growing shoots asitism by a parasitoid, Centrodora sp. Although two (Price et al. 1987b). However, little attention has been egg parasitoids of the family Aphelinidae and Mymari- given to other herbivorous insects. dae were found in A. pectoralis (Craig and Ohgushi The spittlebug Aphrophora pectoralis Matsumura is 2002), the effects of egg parasitism on oviposition a xylem-sucking insect uses Salix species as host plants preference have not been investigated. (Komatsu 1997). Craig and Ohgushi (2002) demon- The purpose of this study was to determine the strated that ovipositing females of this species have a effects of shoot toughness, shoot abscission, and egg strong preference for long shoots and that oviposition parasitism on oviposition preference for long shoots in preference is correlated withlarval survival. These A. pectoralis. We investigated the relationship be- results suggest that larval survival is an important fac- tween shoot length and proportion of shoots in which tor in determining oviposition preference of the spittlebug oviposition occurred, the effects of shoot spittlebug. However, the question of what plant traits length on shoot abscission and shoot toughness, and determine the oviposition preference for long shoots the relationship between shoot length and rate of egg remains unresolved. Willow shoots often drop off a parasitism. 1 Institute of Low Temperature Science, Hokkaido University, Sap- Materials and Methods poro, 060Ð0819 Japan, e-mail: [email protected] 2 Center for Ecological Research, Kyoto University, Otsu, 520Ð2113 Study Site. The study site was located on a bank of Japan. the Ishikari River in Hokkaido, northern Japan (43Њ 0013-8746/02/0552Ð0557$02.00/0 ᭧ 2002 Entomological Society of America September 2002 NOZAWA: AND OHGUSHI:OVIPOSITION PREFERENCE OF A. pectoralis 553 11Ј,N,141Њ 24Ј, E) that has been disturbed by dyke recorded the pressure in Newtons (N) required for building. Around the study area, six willow species, S. complete penetration in the apical region. Three mea- miyabeana Seemen, S. sachalinensis Fr. Schm., S. in- surements were made per shoot, and the average value tegra Thunb., S. hultenii Floderus, S. subfragilis was used as an index of shoot toughness. Anders., and S. pet-susu Kimura, occur sympatrically Egg Parasitism. In the study area, one egg parasitoid (Ishihara et al. 1999). Our study included three of of the family Aphelinidae and one of the Mymaridae these: S. miyabeana, S. sachalinensis, and S. integra, all were found (Craig and Ohgushi 2002). In early April of which were abundant at the study site. 1999, we randomly collected 30 shoots (1 yr old) These three species of willows are widely distrib- bearing eggs from S. miyabeana, 34 from S. sachalin- uted in Hokkaido and are dioecious, deciduous trees ensis, and 33 from S. integra. These shoots were kept often occurring on riverbanks. S. miyabeana grows up individually in a small plastic case withmoderate hu- to7m,S. sachalinensis up to 15 m, and S. integra up to midity. We recorded the number of emerged parasi- 1.5 m and in Ishikari ßower from mid-April to early toids and nymphs until late July. In early August, we May. After ßowering, budbreak occurs in May, and dissected these shoots and counted immature parasit- leaf expansion and shoot elongation continue until ized and nonparasitized eggs. It is possible to distin- mid-July. Most leaves become senescent by late Oc- guishbetween theparasitized and nonparasitized tober when new buds appear in leaf axils. eggs, because parasitized eggs are black and brown in Insect Life Cycle. The spittlebug A. pectoralis is a color and nonparasitized eggs are white. We calcu- xylem-sucking insect that utilizes Salicaceae as host lated the rate of egg parasitism as the proportion of plants (Komatsu 1997). It has a univoltine life cycle parasitized eggs to all eggs observed. and overwinters in the egg stage. Overwintered eggs Statistical Procedures. Chi-square goodness-of-Þt begin to hatch in early May, and nymphs produce analysis was used to determine whether distribution of spittle in which they live and feed. Adults begin to spittlebug oviposition in the Þeld was random with emerge in late June. Mating and oviposition occur respect to shoot length (Zar 1999). The Spearman from early August to mid-October. Females lay egg rank correlation was used to determine the relation- masses (Ϸ10 eggs per mass) inside the apex of current- ship between shoot abscission rate and shoot length. year growing shoots. The apical region of the shoots, Shoot toughness and egg parasitism among shoot within which generally oviposition occurs, die within lengthclasses were compared using a Kruskal-Wallis a week because of mechanical damage by the femaleÕs test followed by nonparametric Tukey-type multiple ovipositor. comparisons for each of the three willow species (Zar In this study, we counted each oviposition scar as an 1999). Shoots were assigned to Þve classes according egg mass. Although we did not compare the number to length. When compared among willow species, data of eggs per egg mass among three willow species, no from all shoot length classes were pooled before anal- signiÞcant difference was found in the length of ovi- ysis. position scars (mm) (S. miyabeana: 3.66 Ϯ 0.07 [mean Ϯ SE], n ϭ 40; S. sachalinensis: 3.57 Ϯ 0.06, n ϭ Results 40; S. integra: 3.67 Ϯ 0.06, n ϭ 40; Kruskal-Wallis test; df ϭ 2, H ϭ 1.1, P ϭ 0.59). The number of eggs was Distribution Pattern of Spittlebug Oviposition. In highly correlated with the length of oviposition scars three willow species, 80% of shoots were Ͻ20 cm (Fig. (Nozawa and Ohgushi 2002). This suggests that there 1). Nevertheless spittlebug females strongly preferred was no difference in the number of eggs per egg mass ovipositing in long (Ͼ20 cm) shoots (S. miyabeana: among three willow species. ␹2 ϭ 19.3, df ϭ 2, P Ͻ 0.001; S. sachalinensis. ␹2 ϭ 91.2, Measurement of Shoot Characteristics. In early May df ϭ 3, P Ͻ 0.001; S. integra: ␹2 ϭ 98.9, df ϭ 3, P Ͻ 1998, we randomly selected 117 shoots (1 yr old) from 0.001). The proportion of shoots with spittlebug eggs S. miyabeana, 107 from S. sachalinensis, and 96 from S. increased withshootlengthup to 40 cm. However, the integra. In early September 1998, we measured the incidence of eggs decreased again on Ͼ40 cm shoots length of all current-year shoots on the selected one- in S. miyabeana and leveled off in S. sachalinensis and year old shoots. In late September 1998, we recorded S. integra. Shoot Abscission. Shoot abscission rate de- the number of current-year shoots with oviposition on clined withincreasing shootlengthin threewillow ϭϪ ϭ each of the selected 1-yr-old shoots. To determine species (S. miyabeana: rS 0.93, P 0.05; S. sacha- ϭϪ ϭ ϭϪ ϭ abscission rate of the current-year shoots during win- linensis: rS 0.93, P 0.05; S. integra: rS 0.93, P ter, we recorded the number of the current-year 0.05; Fig.
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