Blackwell Science, LtdOxford, UK ERE Ecological Research 0912-38142003 Ecological Society of Japan 182March 2003 543 Variations in insect-infested acorn fall X. Yu et al. 10.1046/j.0912-3814.2002.00543.x Original Article155164BEES SGML
Ecological Research (2003) 18, 155–164
Spatial and temporal variations in insect-infested acorn fall in a Quercus liaotungensis forest in North China XIAODONG YU, HONGZHANG ZHOU* AND TIANHONG LUO
Institute of Zoology, Chinese Academy of Sciences, Beijing, China Three plots with different aspects and slope characteristics were surveyed in 1999 and 2000 to clarify the spatial and temporal variations in insect-infested acorn fall patterns in a Quercus liaotungensis Koidz. forest in the Dongling Mountain region, North China. There was a significant difference in the proportion of infested acorns in the three plots in a low crop year, but not in a mast year. Within oakwoods on the southeast-facing slope, the insect infestation rate on the upper slope was significantly higher than on the lower slope, but not in the northwest-facing plot. Infestation rate in the low crop year in all three plots was significantly higher than infestation in the mast year. Most of the early fallen acorns had a higher proportion of insect infestation, and in the mast year it was much more obvious than in the low crop year. The proportion of infested acorns in seed bank along the topographic gradient showed a similar decreasing trend with acorn fall time, but the proportion on the upper slope was the highest and the proportion on the lower slope was the lowest. Larval emergence from acorns commenced just after acorns fell from the trees and lasted for 40–50 days, with peak emergence occurring from 24 to 32 days after acorn rain began. We conclude that insect-infested acorn distribution in Q. liaotungensis shows spatial and temporal heterogeneity, and an early drop of infested acorns can be a short-term defensive strategy against insect infestation. Key words: insect infestation; larval emergence; Quercus liaotungensis; seed-feeding insects; spatial variation; temporal variation.
INTRODUCTION The genus Quercus L. (Fagaceae) is widely distributed in the world and is an important component in many forest ecosystems (Willis 1973). Because of poor regeneration and the dwindling habitat of many oak species, many researchers have investigated the causes of failure of natural regeneration. Both biotic and abiotic aspects, including animal predation, soil types, planting positions and other environmental factors, were considered as possible factors affecting the natural regeneration of oakwoods (Watt 1919; Jones 1959; Shaw 1968a,b; Crawley & Long 1995). Of these, animal predation and dispersal of acorns have been considered as
*Author to whom correspondence should be addressed. Email:
[email protected] Received 25 April 2002. Accepted 27 August 2002.
important factors influencing the natural regeneration of oakwoods and have attracted a great deal of attention (Janzen 1971; Bossema 1979; Howe & Smallwood 1982; Herrera 1984; Smith & Reichman 1984; Jensen & Nielsen 1986; Scarlett & Smith 1991; Chambers & MacMahon 1994; Whelan et al. 1994; Kollmann & Schill 1996; Hammond et al. 1999; Wang et al. 1999). Recently, much attention has been paid to interactions between acorn production of oaks and acorn predation by insects (Andersson 1992; Fujii 1993; Crawley & Long 1995; Maeto 1995; Fukumoto & Kajimura 1999). However, the possible factors influencing these interactions have only been referred to occasionally (Matsuda 1982; Maeto 1995; Fukumoto & Kajimura 1999). It is a general phenomenon for insects to attack acorns because of their nutritional content. Moths (e.g. Cydia) and weevils of the genera Curculio and Conotrachelus are the most common seed-feeding insects, and have induced the loss of acorn produc-
156
X. Yu et al.
tion from 0% to 100% (Jones 1959; Gibson 1964, 1971; Oliver & Chapin 1984; Lewis 1992; Fujii 1993; Scutareanu & Roques 1993; Crawley & Long 1995; Kelbel 1996; Yu et al. 2001). However, most of these studies were based on an oak stand or individual trees and spatial variation of infested acorns (e.g. topographic changes within an oak stand or among different oak stands) have rarely been examined. Mast seeding is believed to be a defensive strategy against seed-feeding insects (Silvertown 1980). It has been hypothesized that insect populations become satiated with seeds in mast years, thus, the number of seeds available for dispersal is greater (Janzen 1971; Crawley & Long 1995). Masting is a reproductive strategy that has evolved over a long period of time. In contrast, dropping infested acorns before the normal period of dispersal appears to be an immediate response to seed predation. Early drop of acorns is a common phenomenon in oak stands, but only a few investigators have paid attention to it and examined it quantitatively (Matsuda 1982; Gurnell 1993). To test early drop of infested acorns, the temporal distribution of infested acorns within the dispersal period must be clarified and quantified. Quercus liaotungensis Koidz. is a common species of oak in the cool temperate zone of North China. Its acorns are highly nutritious, and acorn production shows high year-to-year variation. Based on observations at Beijing Forestry Ecosystem Research Station (BFERS), the synchronous production of large seed crops appears every 3 or 4 years within populations in the Dongling Mountain region (Ma Keping, Director of BFERS, pers. comm., 2000). For example, a large acorn crop size was 123.0 seeds m-2 in 1996 (Sun & Chen 2000), whereas low acorn crop size was 80%), with a canopy height of 8–10 m, and each stand age was approximately 50 years old and covered an area of approximately 0.5 ha. At the NW plot, there were approximately 2840 trees ha-1 with d.b.h. >2 cm, 45% of which were Q. liaotungensis with a basal area of 2254 cm2 100 m-2. At the SE plot there were approximately 2970 trees ha-1 with d.b.h. >2 cm, 58% of which were Q. liaotungensis with a basal area of 2450 cm2 100 m-2. At the E plot there were approximately 2690 trees ha-1 with d.b.h. >2 cm, 42% of which were Q. liaotungensis with a basal area of 2130 cm2 100 m-2.
Acorn collection In this study, two methods, seed trapping and ground sampling, were used to collect acorns in
Variations in insect-infested acorn fall autumn 1999 and 2000. The former method was used to count the acorn crops of an oak stand only and the latter method was used to describe and measure spatial and temporal variation in insect infestation. Pyramidal seed traps were constructed of 2 mm polyester mesh that was sewn to a 0.5 m2 square iron frame. The traps were suspended 1 m above the ground to prevent consumption or removal of acorns by terrestrial vertebrates (after Wang & Ma 2000). Utilization of acorns by birds is minimal in this region (Meng & Zhang 1997). We randomly placed 20 seed traps under the canopies of oak trees in the SE and E plots. In addition, data from 47 seed traps randomly placed in the NW plot for other studies were also examined. Ground sampling using quadrats is a simple method to collect acorns within an oak stand. The sample area was a 2.25 m2 square with rope sides and rods at each corner inserted into the soil. In 1999, we randomly placed 20 quadrats to collect acorns under the canopy of oak trees in each plot. In 2000, 20 quadrats were also randomly placed in the E plot. However, according to the topographic characteristics of the oak stands, 10 quadrats were set up on the upper (1275 m, 20°), middle (1250 m, 23°) and lower (1225 m, 25°) slopes in the SE plot, and on the upper (1275 m, 20°) and lower slopes (1225 m, 22°) in the NW plot. Upper subplots were located at the top ridge of the oak stand and lower subplots were near the valley. All seed traps and ground quadrats were placed at the plots when the acorns were begin-
157
ning to ripen and were left in position until after all the acorns had been shed from the trees. Traps and quadrats were checked every second day between 11–28 September 1999 and 1–26 September 2000, corresponding with the periods of acorn rain in these years. The collected acorns were taken to the laboratory for counting and to examine the infestation rate under natural conditions. In this study, acorns from seed traps were only used to count acorn density, and those from ground samples were used to compare rates of insect infestation. The density of acorns was slightly lower in ground samples than in seed traps, but the differences were quite small. Aborted acorns without the grown cotyledon were not counted. Infestation rates were compared between the plots in 1999 and 2000 by using acorns from all plots. The possible effects of slope direction and topographic characteristic were tested with the acorns from the SE and NW plots in 2000. Temporal patterns were examined at the SE and NW plots in 1999 and at the SE and E plots in 2000. Larval emergence was observed in the SE and E plots in 2000. The size of the acorn crop and the number of infested acorns at each plot or subplot are given in Tables 1 and 2.
Acorn censuses Larvae usually grew to maturation in the acorns and penetrated the seed coat, ready to enter the earth (Yu et al. 2001). The presence of a fresh exit hole indicated the end of larval growth in the
Table 1 Number of Quercus liaotungensis acorns collected from ground samples (2.25-m2 quadrat) at the three plots in the Dongling Mountain region SE plot Year
Subplot
Measures
Total
1999
–
2000
–
Sum (n) Mean ± SE Sum (n) Mean ± SE Sum (n) Mean ± SE Sum (n) Mean ± SE Sum (n) Mean ± SE
195 (20) 9.8 ± 1.8 6364 (30) 212.1 ± 24.4 1704 (10) 170.4 ± 22.4 1061 (10) 106.1 ± 15.6 3599 (10) 359.9 ± 33.7
Upper Middle Lower
NW plot Infested
Infested
Total
127 (20) 6.4 ± 1.2 1806 (30) 60.2 ± 7.4 665 (10) 66.5 ± 11.8 350 (10) 35.0 ± 6.8 792 (10) 79.2 ± 15.2
189 (20) 9.5 ± 1.7 4009 (20) 200.5 ± 18.4 1995 (10) 199.5 ± 26.4 – – 2014 (10) 201.4 ± 27.1
104 (20) 5.2 ± 1.2 897 (20) 44.9 ± 7.9 473 (10) 47.3 ± 13.8 – – 424 (10) 42.4 ± 8.6
E plot Total
Infested
269 (20) 13.5 ± 2.0 5648 (20) 282.4 ± 23.9 – – – – – –
210 (20) 10.5 ± 1.6 2033 (20) 101.7 ± 17.1 – – – – – –
158
X. Yu et al.
Table 2 Density of Quercus liaotungensis acorns collected from seed traps (0.5-m2 trap) at all plots in Dongling Mountain region Year
Measures
SE plot (n = 20) Total Infested
NW plot (n = 47) Total Infested
1999
Sum Density Sum Density
54 5.4 970 97.0
119 5.1 2123 90.3
2000
32 3.2 272 27.2
acorns. Thus, acorns were judged to be infested when larval exit holes were present. Acorns with no new exit holes were dissected and examined for remaining larvae. Observations for exit holes lasted approximately 2 months. Together the number of acorns with exit holes and those with larvae gave us the proportion of infested acorns. In addition, to observe larval emergence in detail, acorns from the SE and E plots in 2000 were examined to count the new exit holes every second day. Generally, the infestation rate is the proportion of infested acorns to all acorns in the seed bank and we used this definition when discussing spatial variation in infested acorns. To aid discussions examining temporal patterns of infestation, we introduced two new expressions of infestation rate: daily infestation rate and accumulative infestation rate. The former was used to describe the proportion of infested acorns to fallen seeds in the 2 day sampling period. The latter was used to describe the proportion of infested acorns to all shed seeds throughout the collecting day. If the collecting day was the last day of acorn rain, the accumulative infestation rate was actually the percentage of infested acorns in the seed bank.
Statistical analyses Data were analyzed graphically and statistically. Arcsine transforms were used for the percentage data of insect-infestation rate. ANOVA and LSD were used to test for differences in the proportion of infested acorns between the three plots. An independent t-test was used to compare differences in the two crop years, the two topographic locations and slope directions. All tests were twotailed and the level of significance was set at
64 2.7 470 20.0
E plot (n = 20) Total Infested 62 6.2 1386 138.6
44 4.4 491 49.1
Total (n = 87) Total Infested 235 5.4 4479 103.0
140 3.2 1233 28.3
P < 0.05. All statistical calculations were performed using the SPSS/PC+ program package (Brosius 1989).
RESULTS Acorn crop size of Q. liaotungensis The average acorn crop size from the Q. liaotungensis forest in Dongling Mountain was only 5.40 seeds m-2 in 1999, but was 102.97 seeds m-2 in 2000 (Table 2). Thus, 1999 can be described as a low crop year and 2000 as a mast year.
Spatial variation in infestation rate Infestation rates were significantly different between the three plots in the low crop year (F = 9.81; d.f. = 2, 57; P < 0.001). The E plot showed a higher infestation rate than the NW and SE plots. In the mast year, infestation rates also showed a similar tendency between the three plots. However, no overall significant differences among all three plots were recorded (F = 2.92; d.f. = 2, 67; P = 0.06) (Fig. 1). When different topographic locations in the NW and SE plots were considered separately in the mast year, infestation rates were significantly different on the upper subplot (t = 2.23, P < 0.05), but not on the lower subplot (t = 0.05, P = 0.96) (Fig. 2). The infestation rate was significantly higher on the upper subplot than on the lower subplot in the SE plot (t = 2.73, P < 0.05). At the NW plot, the infestation rate on the upper subplot was also slightly higher, but no significant difference was recorded (t = 0.21, P = 0.83) (Fig. 2).
Variations in insect-infested acorn fall
Fig. 1. Mean insect infestation rate ± SE of three Quercus liaotungensis plots with NW-, SE- and E-facing slopes in the Dongling Mountain region. Bars of the same factor and with the same letter (and superscript) are not significantly different (ANOVA, LSD, P < 0.05). Asterisks of each plot indicate significant difference between the 2 years (t-test, P < 0.001). (), 1999 (low crop year; (), 2000 (mast year).
159
Fig. 2. Mean insect infestation rate ± SE of two topographic locations at two Quercus liaotungensis plots with NW- and SE-facing slopes in 2000 (mast year) in the Dongling Mountain region. Bars of the same factor with the same letter (and superscript) are not significantly different (t-test, P < 0.05). Asterisks of SE plot indicate a significant difference between the two topographic locations (t-test, P < 0.01). (), Upper slope; (), lower slope.
Temporal patterns in infestation rate
Larval emergence
There were significant differences in infestation rates between the 2 years at the NW plot (t = 5.09, P < 0.001), at the SE plot (t = 7.30, P < 0.001) and at the E plot (t = 6.75, P < 0.001). Infestation rate in the low crop year was higher than in the mast year (Fig. 1). After acorn rain began, the accumulative infestation rate decreased gradually over time (Figs 3 and 4). Daily infestation rate showed a similar tendency, but with irregular fluctuations (Fig. 3). The accumulative infestation rate decreased slowly from 0.79 to 0.65 in the SE plot, but stayed within a range of 0.51–0.56 with no obvious drop over time in the NW plot. Daily infestation rates at both plots with opposite slope changed greatly with acorn fall time and irregular fluctuations were recorded ranging from 0.25 to 0.90 (Fig 3a,c). Both accumulative and daily infestation rates showed a more regular decrease with time in the mast year than in the low crop year at the SE plot (Fig 3a,b). The accumulative infestation rate showed the same tendency to decrease along the elevation gradient in the SE plot. The accumulative infestation rate was always highest at the upper subplot and lowest at the lower subplot (Fig. 4).
Larvae usually cut a hole slightly larger than their head capsule through the seed coat immediately prior to emergence. One or more larvae may emerge through a single hole, and there may be up to 3–4 exit holes in the one acorn. Of 3839 infested acorns from the SE and E plots in 2000, over 90% of these acorns had only one hole. Larval emergence from acorns commenced in early September and continued through until the middle of October, lasting 48 days at the SE plot and 46 days at the E plot. The interval of 24– 32 days after the beginning of the acorn rain was the peak time for larval emergence (Fig. 5).
DISCUSSION Based on our results and other studies (Sun & Chen 2000; Wang & Ma 2000; Wang et al. 2000), Q. liaotungensis was observed to have large acorn crops in 1996 and 2000 and small crops in 1997, 1998 and 1999. In our study, the mast year had 20-fold more acorns per m2 than the low-crop year, and the percentage of insect-infested acorns was significantly lower in the mast year than in the low crop year. Thus, a great amount of acorns in the
160
X. Yu et al.
Fig. 3. Temporal pattern of infestation rate in Quercus liaotungensis acorns in the Dongling Mountain region. (), Daily infestation rate; (▲), accumulative infestation rate. (a) SE plot in 1999 (low crop year), (b) SE plot in 2000 (mast year), (c) NW plot in 1999 (low crop year) and (d) E plot in 2000 (mast year).
mast year could satiate the pest population and more sound acorns could survive to be potential seedlings the following year. This result is consistent with the widely accepted ‘predator satiation’ hypothesis (Crawley & Long 1995). Periodic synchronous seed production in long-lived plants is considered to be an adaptation to allow satiation of seed-feeding animals, thus increasing the probability of seedling recruitment following years of peak seed production (Janzen 1971; Silvertown 1980; Fenner 1991; Sork et al. 1993; Waller 1993; Koenig et al. 1994; Crawley & Long 1995). Matsuda (1982) found that insect attacks to acorns of konara oak (Q. serrata Thunb.) in early developmental stages had an effect of thinning excess fruit with a small amount of material loss; however, later insect attacks only caused a waste of material. Based on this result, we can infer that during the later developmental stage of acorns, earlier drop of acorns attacked by insects would reduce the loss of material. Our observations con-
ducted during the period of acorn rain, namely the later developmental stage of the fruit, and the higher proportion of infested acorns that fell during the early period of acorn rain showed the phenomenon of early drop in Q. liaotungensis. Moreover, our previous data demonstrated that acorns infested with weevils (Curculio dentipes Roelofs) were less than 16.05% of the weight of sound acorns under the same experimental conditions (Yu et al. 2001). Therefore, a tree might save a substantial amount of energy if the growth of infested seeds was discontinued and these acorns were shed early. Because the probability of infested acorns contributing to the seedling bank is very low ( Jones 1959; Yu et al. 2001), it is advantageous for a tree to avoid further wastage of its resources by ceasing to grow insect-infested acorns. Thus, based on the perspectives of evolution, early drop of insect-infested acorns might be considered to be an immediate weak response of this oak species to insect infestation. But more
Variations in insect-infested acorn fall data and studies of more tree species are needed to determine whether the early drop of fruit has evolved as a result of direct selection for energy conservation, or whether early drop is just due to a breakdown in the normal physiological process of fruit development. Our results suggest that slope direction and topographic characteristics influenced insect infestation between oak woods and plots. Lewis (1992) found that insect-infested acorns were distributed unevenly within a tree of Quercus agrifolia Neé, and
Fig. 4. Spatial and temporal variations in infestation rate in Quercus liaotungensis acorns in the SE plot in 2000 (mast year). (▲), Upper slope; (), middle slope; (), lower slope.
161
inferred that the uneven distribution might be a result of temperature differences. An eastern facing slope is cooler and damper than a NW or SE facing slope, and escaping heat and high humidity may cause higher infestation rates at eastern facing plots. The effect of topographic characteristics may result from different locations in an oak stand. Upper subplots were located at the top ridge of slopes where strong winds mean that trees in this area will have a smaller canopy height than trees growing in lower subplots. Eikenbary and Raney (1973) reported that adults of a pecan weevil, Curculio caryae (Horn), were more abundant in the lower proportions of pecan trees, and suggested that this occurred because of the inferior mobility of adult weevils. Topographic characteristics in our experiment may also be explained based on the inferior mobility of adult weevils, Curculio dentipes Roelofs, which attacked over 70% of the infested acorns in the present study. Because most acorns are concentrated in the canopy of oak trees, female weevils may find it easier to oviposite on acorns in the lower canopy. Thus, acorns might be more heavily attacked/infested on upper slopes than on lower slopes. The characteristics of larval emergence were reflected in the life history of the weevil, Curculio dentipes Roelofs. Most adult weevils began to lay
Fig. 5. Larval emergence from Quercus liaotungensis acorns in the Dongling Mountain region in 2000 (mast year). (a) SE plot and (b) E plot.
162
X. Yu et al.
eggs in July, with peak oviposition in August, continuing into September (Cheng & Hsu 1959). Larvae need approximately 40 days to grow to maturity. Thus, we found that larval emergence varied from 0 to 50 days and was concentrated in late September and early October. Oliver and Chapin (1984) also recorded similar larval emergence of Curculio fulvus Chittenden in the live oak, Quercus virginiana Miller, in Louisiana from 1979 to 1983. In general, our results supported higher infestation rates in low crop years, but the slope direction between oak stands and the topographic characteristics in an oak stand also influence the rates of infestation of Q. liaotungensis in any year. Moreover, early drop of insect-infested acorns occurring in the early period of normal fall of acorns is believed to be a short-term defensive strategy for oak trees against insect attack. Additional information about the life history of the main infesting insects and the process of acorn germination and maturation in Q. liaotungensis is necessary before we can understand how oak trees defend against insect attacks in the short term.
ACKNOWLEDGEMENTS We are indebted to Dr Ma Ke-ping, Gao Xianming, Wang Wei, Li Qing-kang and Yan Wen-jie from the Institute of Botany, Chinese Academy of Sciences, for helping with the field experiments and offering some important references. We thank Dr Jonathan Cooter (Herefored Museum, England) for checking the language in the manuscript. This study was supported in part by a State Key Basic Research and Development Plan from the Ministry of Science and Technology of China (no. G2000046801), a major program (no. 39893360) of the National Natural Science Foundation of China, and the Chinese Academy of Sciences (CAS) Innovation Program.
REFERENCES A NDERSSON C. (1992) The effect of weevil and fungal attacks on the germination of Quercus robur acorns. Forest Ecology and Management 50: 247– 251.
B OSSEMA I. (1979) Jays and oaks: an eco-ethological study of a symbiosis. Behaviour 70: 1–117. B ROSIUS G. (1989) SPSS/PC+ Advanced Statistics and Tables. McGraw-Hill, Hamburg. C HAMBERS J. C. & M AC M AHON J. A. (1994) A day in the life of a seed: movements and fates of seeds and their implications for natural and managed systems. Annual Review of Ecology and Systematics 25: 263–292. C HENG H-Y. & H SU T-S. (1959) On the life history and control measures of the acorn weevil, Curculio (Balaninus) dentipes Roelofs. Forestry Science (Beijing) 5: 68–75. C RAWLEY M. J. & L ONG C. R. (1995) Alternate bearing, predator satiation and seedling recruitment in Quercus robur L. Journal of Ecology 83: 683– 696. E IKENBARY R. D. & R ANEY H. G. (1973) Intratree dispersal of the pecan weevil. Environmental Entomology 2: 927–930. F ENNER M. (1991) Irregular seed crops in forest trees. Quarterly Journal of Forestry 85: 166– 172. F UJII S. (1993) Studies on acorn production and seed predation in Quercus serrata: growth, falling phenology, estimation of production, and insect seed predators. Bulletin of Osaka Museum of Natural History 47: 1–17. F UKUMOTO H. & K AJIMURA H. (1999) Seedinsect fauna of pre-dispersal acorns and acorn seasonal fall patterns of Quercus variabilis and Q. serrata. Central Japan. Entomological Science 2: 197– 203. G IBSON L. P. (1964) Biology and life history of acorn-infesting weevils of the genus Conotrachelus (Coleoptera: Curculionidae). Annals of the Entomological Society of America 57: 521–526. G IBSON L. P. (1971) Insects of bur oak acorns. Annals of the Entomological Society of America 64: 232–234. G URNELL J. (1993) Tree seed production and food conditions for rodents in an oak wood in southern England. Forestry 66: 291–315. H AMMOND D. S., B ROWN V. K. & Z AGT R. (1999) Spatial and temporal patterns of seed attack and germination in a large-seeded neotropical tree species. Oecologia 119: 208–218. H ERRERA C. M. (1984) Seed dispersal and fitness determinants in wild rose: combined effects of hawthorn, birds, mice, and browsing ungulates. Oecologia 63: 386–393. H OWE H. F. & S MALLWOOD J. (1982) Ecology of seed dispersal. Annual Review of Ecology and Systematics 13: 201–228.
Variations in insect-infested acorn fall J ANZEN D. H. (1971) Seed predation by animals. Annual Review of Ecology and Systematics 2: 465– 492. J ENSEN T. S. & N IELSEN O. F. (1986) Rodents as seed dispersers in a heath: oak wood succession. Oecologia 70: 214–221. J ONES E. W. (1959) Biological flora of the British Isles: Quercus L. Journal of Ecology 47: 169– 222. K ELBEL P. (1996) Damage to acorns by insects in Slovakia. Biologia (Bratislava) 51: 575–582. K OENIG W. D., M UMME R. L., C ARMEN W. J. & S TANBACK M. T. (1994) Acorn production by oaks in central coastal California: variation within and among years. Ecology 75: 99–109. K OLLMANN J. & S CHILL H. P. (1996) Spatial patterns of dispersal, seed predation and germination during colonization of abandoned grassland by Quercus petrea and Corylus avellana. Vegetatio 125: 193–205. L EWIS V. R. (1992) Within-tree distribution of acorns infested by Curculio occidentis (Coleoptera: Curculionidae) and Cydia latiferreana (Lepidoptera: Tortricidae) on the coast live oak. Environmental Entomology 21: 975–982. M A K., C HEN L., Y U S., H UANG J., G AO X. & L IU C. (1997) The major community types in Dongling Mountain Region. In: The Study on Structure and Function of Forest Ecosystem in Warm Temperate Zone (eds L. Chen & J. Huang), pp. 56– 75. Beijing Science Press, Beijing. M AETO K. (1995) Relationships between size and mortality of Quercus mongolica var. grosseserrata acorns due to predispersal infestation by frugivorous insects. Journal of the Japanese Forestry Society 77: 213–219. M AO S. & S ONG F. (1997) The study on the climatic characteristics of the research site of Beijing Forest Ecosystem Research Station (BFERS). In: The Study on Structure and Function of Forest Ecosystem in Warm Temperate Zone (eds L. Chen & J. Huang), pp. 28–37. Beijing Science Press, Beijing. M ATSUDA K. (1982) Studies on the early phase of the regeneration of a konara oak (Quercus serrata Thunb.) secondary forest. I. Development and premature abscissions of konara oak acorns. Japanese Journal of Ecology 32: 293–302. M ENG Z. & Z HANG Z. (1997) The species and habitats of bird and mammal and the characteristics of rodent community in the mountain area of Beijing. In: The Study on Structure and Function of Forest Ecosystem in Warm Temperate Zone (eds L. Chen & J. Huang), pp. 76–87. Beijing Science Press, Beijing.
163
O LIVER A. D. & C HAPIN J. B. (1984) Curculio fulvus (Coleoptera: Curculionidae) and its effects on acorns of live oaks, Quercus virginiana Miller. Environmental Entomology 13: 1507–1510. S CARLETT T. L. & S MITH K. G. (1991) Acorn preference of urban blue jays (Cyanocitta cristata) during fall and spring in northwestern Arkansas. Condor 93: 438–442. S CUTAREANU P. & R OQUES A. (1993) Insect damage to male catkins, female flowers and acorns of Quercus spp. in Romania. Journal of Applied Entomology 115: 321–328. S HAW M. W. (1968a) Factors affecting the natural regeneration of sessile oak (Quercus petraea) in North Wales. I. A preliminary study of acorn production, viability and losses. Journal of Ecology 56: 565–583. S HAW M. W. (1968b) Factors affecting the natural regeneration of sessile oak (Quercus petraea) in North Wales. II. Acorn losses and germination under field conditions. Journal of Ecology 56: 647– 660. S ILVERTOWN J. W. (1980) The evolutionary ecology of mast seeding in trees. Biological Journal of the Linnean Society 14: 235–250. S MITH C. C. & R EICHMAN O. J. (1984) The evolution of food caching by birds and mammals. Annual Review of Ecology and Systematics 15: 329– 351. S ORK V. L., B RAMBLE J. & S EXTON O. (1993) Ecology of mast-fruiting in three species of North American deciduous oaks. Ecology 74: 528–541. S UN S. & C HEN L. (2000) Seed demography of Quercus liaotungensis in Dongling Mountain region. Acata Phytoecologica Sinica 24: 215–221. W ALLER D. W. (1993) How does mast-fruiting get started? Trends in Ecology and Evolution 8: 122– 123. W ANG W. & M A K. (2000) Acorn demography of Quercus liaotungensis Koidz. in broad-leaved deciduous forests of Dongling Mountain Region. Ecology (Bratislava) 19: 27–38. W ANG W., M A K. & G AO X. (1999) Removal and predation of Quercus liaotungensis Koidz. acorns by animals. Ecological Research 14: 225–232. W ANG W., M A K. & L IU C. (2000) Seed shadow of Quercus liaotungensis in a broad-leaved forest in Dongling Mountain. Acta Botanica Sinica 42: 195–202. W ATT A. S. (1919) On the causes of failure of natural regeneration in British oakwoods. Journal of Ecology 7: 173–203. W HELAN C. R., W ILLSON M. F., T UMA C. A. & S OUZA -P INTO I. (1994) Spatial and temporal
164
X. Yu et al.
patterns of postdispersal seed predation. Canadian Journal of Botany 69: 428–436. W ILLIS J. C. A. (1973) A Dictionary of the Flowering Plants and Ferns, 7th edn. revised by H. K. Airy Shaw). Cambridge University Press, Cambridge.
Y U X., Z HOU H., L UO T., H E J. & Z HANG Z. (2001) Insect infestation and acorn fate in Quercus liaotungensis. Acta Entomologica Sinica 44: 518– 524.
