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Prolonged Diapause of Specialist Seed-Feeders Makes Predator Satiation Unstable in Masting of Quercus Crispula

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Prolonged Diapause of Specialist Seed-Feeders Makes Predator Satiation Unstable in Masting of Quercus Crispula Oecologia (2003) 137: 392–398 DOI 10.1007/s00442-003-1381-6 PLANT ANIMAL INTERACTIONS Kaoru Maeto . Kennichi Ozaki Prolonged diapause of specialist seed-feeders makes predator satiation unstable in masting of Quercus crispula Received: 10 February 2003 / Accepted: 11 August 2003 / Published online: 16 September 2003 # Springer-Verlag 2003 Abstract Quercus crispula (=Q. mongolica var. grosse- Introduction serrata) is the predominant tree species in cool temperate, mixed broadleaf/conifer forests in northern Japan. We The synchronous production of large seed crops by a compared 11 years of data on acorn production in a population of plants is a phenomenon known as masting, population of Q. crispula, with data on seed-insect mast fruiting or mast seeding (Kelly 1994). It is generally populations, to try to answer the following questions: (1) documented that some climatic factors affect annual Does Q. crispula show a regular pattern of masting? (2) variations in seed production (e.g. Houle 1999). Econo- How long do principal seed predators remain in diapause? mies of scale, involving pollination, seed predator satiation (3) How do the seed predators affect the pattern of and/or seed dispersal, are also believed to have evolved predator satiation? Q. crispula showed a tendency to masting as resource switching between reproduction and alternate bearing, with significant synchrony between growth or reserves (Silvertown 1980; Kelly 1994; Kelly individual trees. The principal acorn-feeding insects and Sullivan 1997; Koenig and Knops 1998). (Curculio spp. weevils), which infested 25%–70% of Seed-feeding insects, such as weevils, moths and wasps, matured acorns, generally exhibited a prolonged diapause are effective agents in promoting masting due to predator of 2 years. No significant negative relationship was found satiation in mast years, because most are univoltine between the rate of injury by the weevils and the density of specialist herbivores and so their population size ought mature acorns, indicating that simple predator satiation to be limited in a lean year prior to a mast year. Indeed, a fails due to the synchrony of the life-cycle of acorn- negative correlation between seed crop size and percen- feeding insects and the periodical production of acorns. tage predation by seed insects has been reported for many However, the rate of injury by the weevils was negatively temperate tree species (Mattson 1971; Silvertown 1980; correlated with the relative abundance of mature acorns to Crawley and Long 1995; Shibata et al. 1998, 2002). Quite the number of weevil larvae that had matured 2 years a few cone and seed insects, however, are known to previously. Thus, the proportion of sound acorns notably exhibit prolonged diapause, i.e. spending two or more increased in a rich crop after a disturbance in alternate winters before adult emergence (Janzen 1971; Hanski bearing. Prolonged diapause of specific seed predators is 1988). Mast-year populations of these insects may endure critical in determining the peak year of sound-seed until the next mast year without being reduced in lean year production. (s). Where diapause in seed-eating insects is highly synchronized with the periodic reproduction of trees, Keywords Acorn production . Curculio . Insect life- simple predator satiation in mast years may not always cycle . Mast fruiting . Seed predation occur (Janzen 1971). We were interested to understand how prolonged diapause of seed predators affects predator satiation and the pattern of sound seed production in a K. Maeto (*) predominant Japanese oak. Laboratory of Insect Science, Faculty of Agriculture, Kobe A deciduous oak, Quercus crispula Blume (=Q. University, Rokkodai 1-1, Nada-ku, mongolica Fisher var. grosseserrata (Blume) Rehd. et 657-8501 Kobe, Japan Wils.), is the most dominant tree species in cool temperate, e-mail: [email protected] mixed broadleaf/conifer forests in northern Japan (Hor- Fax: +81-78-8035871 ikawa 1972). Though it shows a distinct pattern of masting K. Ozaki (Kanazawa 1982; Imada et al. 1990; Shibata et al. 2002), Forestry and Forest Products Research Institute, Maeto (1995) reported that the pre-dispersal acorns were Japan seriously damaged by the mature-acorn feeding (MAF) 393 guild of insects (Fukumoto and Kajimura 2001) in both From 1990 to 1993, some of the insect larvae that had emerged rich and lean years. It may be expected that prolonged from the acorns were released in unglazed pots filled with sterilized soil. The pots were buried in the ground and the upper opening was diapause of the seed weevils negates predator satiation and covered by plastic mesh. Emergence of insect adults was observed changes the year-to-year production of sound acorns. weekly from June to September for 4 years. To test this speculation, we compared 11 years of data Daily rainfall and daily maximum and minimum air temperatures on acorn production in a population of Q. crispula in were recorded from 1989 to 2000 at the Forestry and Forest Products Research Institute Hokkaido Research Center (147 m a.s.l.) northern Japan with data on seed insect populations. We at Hitsujigaoka, about 1 km away from the study site. especially wanted to answer three questions: (1) does Q. crispula show a regular pattern of masting? (2) How long do principal seed predators remain in diapause? (3) How Data analyses do the seed predators affect the pattern of predator satiation? To measure the intensity of annual variation in acorn production, a coefficient of variation (CV) as an index of masting (Silvertown 1980; Kelly 1994) was calculated for the mean number of mature acorns. Overall synchrony of annual variation in acorn production Materials and methods between trees was evaluated with a repeated-measures ANOVA on the log-transformed number of mature acorns. Autocorrelation Study site coefficients were calculated for the log-transformed number of mature acorns for each tree to examine the intrinsic periodicity of The study was conducted in Todo-yama, a naturally regenerated acorn production (at the individual level), and also for the log- forest (42°58′N, 141°23′E, 110–130 m a.s.l.) at Hitsujigaoka, transformed, mean number of mature acorns (at the population level). Sapporo City, Hokkaido, northern Japan. Dominant canopy species Fischer s method for combining probabilities (Sokal and Rohlf include Q. crispula, Acer mono Maxim., Ostrya japonica Sarg., 1995) was applied to test the overall significance of autocorrelation Kalopanax pictus (Thunb.) Nakai, Tilia spp., Betula spp. and Abies at the individual level. sachalinensis (Fr. Schm.) Mast. Q. crispula was the only species of To evaluate the effect of climate on acorn production, we oak (genus Quercus) found in the forest. We established a census calculated Pearson correlation coefficients between the log-trans- plot of ca. 0.4 ha, where the basal area of Q. crispula [diameter at formed mean number of mature acorns and climatic variables breast height (DBH) >20 cm] was 11.9 m2 ha−1. (monthly rainfall, monthly mean of maximum temperature, and monthly mean of minimum temperature from April to September) for the year in question and the previous year. The variables were also compared between 1995 and 1996 (n=2), when apparent Field methods alternate bearing was obstructed (Fig. 1), and other years (n=9) by a Mann-Whitney U-test to look for the factor that may disturb Within the census plot, we initially chose three and then an alternate bearing. additional five trees of Q. crispula (DBH=35.0–56.7 cm measured To examine whether predator, satiation had occurred in acorn in 1994) in the early summers of 1990 and 1991, respectively. We feeding by insects, Kendall s rank correlation coefficients (τ) placed four seed-collecting traps (total trap area=1.5 m2) under the between the mean proportion of injured acorns, and the mean canopy of each tree until 2000. Acorns in the traps were collected number of mature acorns were tested. Kendall s rank correlation weekly from mid-August to mid-October when acorn fall ceased. coefficients (τ) were also tested between the mean proportion of Acorns with an apex protruding from the cup were classified as injured acorns and the relative abundance of mature acorns to mean mature (Kanazawa 1975) and counted. These were placed number of insect larvae that had matured 1 or 2 years previous. individually in glass or plastic vials and observed once or twice a All data analyses were conducted using STATISTICA 5.1 week to identify and count insect larvae that emerged from them. In (StatSoft 1998). November, all the acorns were cut to verify whether they were intact or injured by insects. Insect larvae remaining inside the acorn were identified and counted. Fig. 1 Mature and sound seed crops (mean±SE, n=8 trees) of Quercus crispula for the period 1990–2000 at Hitsujigaoka, Sapporo, Hokkaido. Coeffi- cients of variation (CV) were calculated for the mean values 394 Results although these could not be distinguished in the larval stage. Annual variation of acorn production From the unglazed pots in which weevil larvae had been matured and released in 1990, 1991, 1992 and 1993, a The oak population showed considerable annual variation total of 20, 213, 55 and 22 adult weevils and their braconid in acorn production (Fig. 1) with a coefficient of variation parasitoids (Triaspis curculiovorus Papp et Maeto) (Papp of acorn production of 52.8%. A repeated-measures and Maeto 1992) emerged within the following 4 years, ANOVA showed that overall synchrony of acorn produc- respectively. Percentage parasitism by the braconid para- tion between individual trees was significant (F10,20=8.55, sitoid was 5.0%, 14.1%, 18.2% and 4.5% for the weevils P<0.001). Autocorrelation coefficients were negative at a that matured in 1990, 1991, 1992 and 1993, respectively. time lag of 1 year and 3 years for all individual trees, and Relative abundance of the three Curculio species was positive at a time lag of 2 years for many trees (Table 1).
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