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 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 . 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). significantly different among years of larval maturity Negative autocorrelation was significant for a time lag of (Fig. 2). In even years, Curculio sikkimensis was more , 1 year (Fischer s method for combining probabilities, abundant than Curculio dentipes, but less abundant in odd −2∑lnP=30.63, df=16, P<0.02), but positive autocorrela- years. tion for a time lag of 2 years (−2∑lnP=16.34, df=16, Most Curculio weevils emerged after two winters, and P>0.1) and negative autocorrelation for a time lag of only a small portion emerged after three or four winters 3 years (−2∑lnP=22.53, df=16, P>0.1) were not signifi- (Fig. 3a–c). The overall percentage of weevils emerging cant. Autocorrelations for time lags of 1 and 3 years at the after two winters was 86.7%, 80.0% and 98.5% for population level were negative, although not significant Curculio sikkimensis, Curculio dentipes and Curculio

(Table 1). Alternate bearing was observed from 1990 to distinguendus, respectively. However, most of the moths ,

, ,,

1994 ( alternate bearing phase ), with this regular pattern (Cydia glandicolana) emerged after one winter (Fig. 3d).

, becoming disordered after 1994 ( , non-alternate bearing The odd-year populations of Curculio spp. decreased ,, phase ) (Fig. 1). abruptly from 1993 to 1995 with the decrease of acorns in Climatic variables were not significantly correlated with 1995 (Fig. 4a), while the even-year populations began to the mean number of mature acorns (P>0.05) during the increase after 1994 (Fig. 4b). The population of Cydia period April to September of the current and preceding year. Current-year precipitation in May was the only climatic variable whose difference between 1995 and 1996 (n=2) (when apparent alternate bearing was obstructed) and other years (n=9) was marginally significant (Mann- Whitney U-test, U=1, P=0.073). Precipitation in May (mean±SD, mm) was 88.5±13.4 in 1995 and 1996, but 53.9±22.2 in other years.

Prolonged diapause and density of acorn-feeding insects

Principal feeders of pre-dispersal mature acorns were curculionid weevils (Curculio spp.) and a tortricid moth Fig. 2 Individual proportions of three Curculio weevils that [Cydia glandicolana (Danilevsky)]. The weevils included emerged from unglazed pots in which the weevil larvae had been three species [Curculio sikkimensis (Heller), Curculio released in 1990, 1991, 1992 and 1993. Figures indicate the number dentipes (Roelofs), and Curculio distinguendus (Roelofs)], of individuals. Proportions were significantly different among years (χ2=18.29, df=6, P<0.01)

Table 1 Autocorrelation coeffi- Tree Time lag (year) cients for the log-transformed number of mature acorns in each 123456 tree (individual level) and for the log-transformed mean num- Individual level I −0.187 −0.194 −0.469 0.238 0.246 −0.103 ber of mature acorns (population II −0.536 0.186 −0.212 0.063 0.228 −0.189 level). Values with a significant level of P<0.05 are shown in III −0.302 0.445 −0.232 0.086 −0.020 −0.176 bold type IV −0.200 0.077 −0.253 −0.141 −0.029 −0.037 V −0.410 −0.093 −0.158 0.197 0.059 −0.207 VI −0.351 0.046 −0.175 −0.022 0.184 0.130 VII −0.653 0.265 −0.131 −0.068 0.303 −0.387 VIII −0.350 0.040 −0.295 0.192 −0.171 0.067 Population level −0.316 0.125 −0.349 0.087 0.251 −0.115 395 Fig. 3a–d Adult emergence of Curculio spp. and Cydia glan- dicolana from unglazed pots in which mature larvae had been released in 1990, 1991, 1992 and 1993

glandicolana was depressed after 1994 irrespective of the was significant or marginally significant from 1995 to , , ,, number of mature acorns present (Fig. 4c). 2000 during the non-alternate bearing phase (Fig. 5). Both the mean proportion of mature acorns injured by all insects and by Curculio spp. decreased significantly (or Occurrence of predator satiation marginally significantly) with an increase of the relative abundance of mature acorns to the mean number of The mean proportion of mature acorns injured by all Curculio larvae that had matured 2 years previously insects, by Curculio spp., and by Cydia glandicolana, (Fig. 6a). However, the proportion of acorns injured by all ranged from 32 to 84%, 25 to 70% and 3 to 24%, insects did not decrease with an increase of the relative respectively (Fig. 5). After seed predation by these insects, abundance of mature acorns to the number of Cydia the CV of the mean number of acorns increased from 53% glandicolana larvae that had matured 1 year previously, (all mature acorns) to 83% (sound acorns only) (Fig. 1). while that of acorns injured by Cydia glandicolana A significant negative correlation between the mean decreased significantly (but marginally so) with the proportion of mature acorns injured by insects and the increase (Fig. 6b). These show that the relative number

mean number of mature acorns was not observed for all of Curculio adults emerged to the number of current

, years combined, or from 1990–1994 during the , alternate acorns is critical to the level of acorn predation by insects. ,, bearing phase (Fig. 5). However, a negative correlation

Fig. 4a–c Relationships between the mean number of mature acorns and the number of mature larvae (mean±SE, n=8 trees). Odd-year populations (a), and even-year populations (b)ofCurculio spp., and the Cydia glandicolana population (c) 396

Fig. 5a–c Relationships between the mean number of mature n=6, P<0.05); those in b were not significant for all years combined acorns and the mean proportion of acorns injured by all insects (a), (τ=−0.018, n=11, P>0.1) and for 1990–1994 (τ=0.400, n=5, P>0.1), – τ − by Curculio spp. (b)orbyCydia glandicolana, (c), from 1990 to and marginally significant for 1995 2000 ( = 0.600, n=6, P<0.1); 1994 (○) and from 1995 to 2000 (●). Kendall s rank correlation those in c were not significant for all years combined (τ=−0.273, coefficients for a were not significant for all years combined (τ= n=11, P>0.1) and for 1990–1994 (τ=0.000, n=5, P>0.1), and −0.127, n=11, P>0.1), marginally significant for 1990–1994 marginally significant for 1995–2000 (τ=−0.600, n=6, P<0.1) (τ=0.800, n=5, P<0.1), and significant for 1995–2000 (τ=−0.867,

Discussion relation at a time lag of 2 years and negative autocorrela- tion at a time lag of 3 years were not significant, possibly Does Quercus crispula show a regular pattern of due to an insufficient number of years in the study.

masting? It appears that there were two phases of acorn

,

production at the population level, i.e. an , alternate , ,, , As shown in many other temperate (Sork at al. 1993; bearing phase in 1990–1994 and a non-alternate bearing ,, Koenig et al. 1994; Crawley and Long 1995), Q. crispula phase in 1995–1998, although this was not statistically showed considerable variation in production of mature proven. Similar crop phases of Q. crispula have been acorns among years, and the inter-year production was reported by Imada et al. (1990), who observed alternate significantly synchronous within a population. Synchro- bearing (1966–1974) with following non-alternate bearing nous acorn production could be caused by climate, but in (1974–1985) in two populations in Hokkaido. It is most the present study we found no climatic variable correlated likely that alternate bearing is a basic pattern of acorn with acorn production. production in Q. crispula but this regular bearing is often We found a negative autocorrelation of acorn produc- disturbed by climatic factors. Alternate bearing of Q. tion at a time lag of 1 year at the individual level, crispula was obstructed in 1995 and 1996 in our study supporting the hypothesis that trees deplete their nutri- site. After the lean year of 1994, many more acorns were tional resources when they produce large seed crops (Kelly expected in 1995 but lean crops continued at least for 1994; Koenig and Knops 1998). It indicates an intrinsic another 2 years (1995 and 1996). Our climatic data tendency to alternate bearing, although positive autocor- indicated that precipitation in May in 1995 and 1996 was

Fig. 6a, b Relationships between the relative abundance of mature coefficients were significant for ● in a (τ=−0.556, n=9, P<0.05), acorns to Curculio larvae that matured 2 years previously (a)orto marginally significant for + in a (τ=−0.444, n=9, P<0.1) and ○ in b Cydia glandicolana larvae that matured 1 year previously (b) and (τ=−0.467, n=10, P<0.1), but not significant for + in b (τ=−0.200, the mean proportion of acorns injured by all insects, (+), by Curculio n=10, P>0.1) spp. (●)orbyCydia glandicolana (○). Kendall s rank correlation 397 greater than that in normal years. Higher rainfall in May negatively correlated with the relative abundance of could contribute to unsuccessful pollination of Q. crispula, acorns related to the number of weevils that had matured which comes into blossom in late May (Kikuzawa 1991), 2 years previously, indicating that the number of weevils but this needs to be confirmed by further studies into emerging after two winters greatly affects the intensity of climate, flowering and seeding. acorn injury. Due to the prolonged diapause of the Curculio weevils, predator satiation did not occur during the period of alternate bearing. Consequently, a chance How long do principal seed predators remain in interruption of alternate bearing, probably due to climatic diapause? disturbance, should be essential to provide a rich crop of sound acorns, as occurred in 1998. Pre-dispersal mature acorns of Q. crispula were frequently For two Quercus species in a mixed temperate forest in injured by the larvae of Curculio weevils and less central Japan, Shibata et al. (2002) also reported a negative frequently by larvae of the moth Cydia glandicolana. relationship between the rate of acorns injured by insects All the Curculio weevils spent two or (rarely) more and the ratio of the number of acorns in the current year to winters before emergence while the moth usually emerged that of 2 years previous, but not between the injury rate after one winter. Two-year life-cycles of the Curculio and the number of acorns. They did not determine what weevils would contribute to the observed alternation of the seed-feeding insects were, but their observation dominant species between even and odd years. strongly indicates that the principal feeders of acorns Prolonged diapause has often been reported for have a 2-year life-cycle. The failure of simple predator Curculio species (Brezner 1960; Manu and Debouzie predation due to a prolonged diapause of seed insects 1993; Harris et al. 1996), probably because larvae are able seems to be not unusual in seed production in oaks. to remain deep in the soil where there may be fewer If alternate bearing of Q. crispula is primarily directed predators than in the humus layer. Dependence on specific against acorn-feeding insects, the weevils may have host species should also be important in the evolution of successfully overcome the Q. crispula defense strategy prolonged diapause. Curculio dentipes and Curculio through acquisition of a 2-year prolonged diapause. It may distinguendus are specific to Quercus, and Curculio also be noteworthy that a small proportion of weevils sikkimensis is specific to Quercus and Castanea (Mor- spend three or more winters before emergence. Once imoto 1981; Maeto 1993; Ueda 2000). In the inland forests alternate bearing is interrupted, lean years can last for 2 or of Hokkaido, Q. crispula is the super-dominant species of more years. Therefore, only weevil individuals with a Quercus, whereas Castanea and other species of Quercus prolonged diapause of more than two winters can survive occur sporadically (Horikawa 1972). The 2-year life-cycle to the next mast year. However, the evolution of a of the Curculio species may have evolved as an adaptation prolonged diapause in acorn insects is open to question. to the alternate bearing pattern of Q. crispula. Crawley and Long (1995), who investigated acorn production of Q. robur, pointed out that invertebrate seed feeders are important because they can determine which of How do seed predators affect the pattern of predator the peak years produce sufficient sound seeds to satiate satiation? vertebrate herbivores. Our study also shows the impor- tance of seed-feeders that have a prolonged diapause in Predator satiation in seed-feeding insects has been firmly determining the peak year of sound-seed production, demonstrated in various tree species (Mattson 1971; through their ability to overwhelm the rich crops of an Silvertown 1980; Crawley and Long 1995; Shibata et al. alternate bearing system. Prolonged diapause is observed 1998, 2002). If continuous rich crops are interrupted by a in not a few seed-feeding insects (Janzen 1971; Hanski lean year, populations of seed-feeding insects will be 1988). It is thus most important to examine the life-history depressed and the rate of injured seeds will decline in the and population dynamics of insects in order to determine coming rich year. However, if diapause in seed-feeding patterns of sound-seed production. insects is highly synchronized with the periodic reproduc- tion of trees, simple predator satiation in mast years is not Acknowledgements We thank Simon Lawson, Naoto Kamata and always expected, as predicted by Janzen (1971). This is Mitsue Shibata for commenting on an earlier draft of the manuscript, probably the case with Q. crispula and its acorn-feeding and Katsura Morimoto and Furumi Komai for the identification of weevils and moths, respectively. Our thanks are also due to Chikara Curculio weevils. Koizumi and Kenji Fukuyama for their continuous encouragement. Although Curculio spp. weevils were the principal This study was supported in part by a grant-in-aid (Bio Cosmos feeders on Q. crispula acorns, no significant negative Program) from the Japan Ministry of Agriculture, Forestry and relationship was found between the rate of injury by the Fisheries. weevils and the density of mature acorns. 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