Predating Strategy of Rodents on Acorns of Quercusaliena Var

ACTA ECOLOGICA SINICA Volume 26, Issue 11, November 2006 Online English edition of the Chinese language journal

Cite this article as: Acta Ecologica Sinica, 2006, 26(11), 3533−3541. RESEARCH PAPER

Predating strategy of rodents on acorns of Quercusaliena var. acuteserrata under different predating risks and fate of acorns

Wang Zhonglei1,2, Gao Xianming1,*

1 Laboratory of Quantitative Vegetation Ecology, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China 2 Graduate School of Chinese Academy of Sciences, Beijing 100039, China

Abstract: The effects of rodents on forest regeneration have been highlighted in many ecological studies. In 2002 and 2003, the acorns of Quercus aliena var. acuteserrata were subjected to 12 different treatments. The daily dynamics and the amount of acorns that were finally left intact, predated in situ, or removed off were examined and documented. The ratios of acorns that were infested by bugs before and after predation by rodents were carefully documented. It was found that: (1) the ratios of acorns infested by bugs before and after predation by rodents showed significant difference (P > 0.05), suggesting that rodents would not prey on acorns during the predating process if acorns had been already infested by bugs. (2) When compared with the controls, the fate of acorns could be roughly classified into four types: ①acorns that were simply buried or placed on black paper showed no significant differ- ences with the controls in their response to rodents, suggesting that rodents have no sensitivity to the little change of odor resulting from burying and may be more adapted to black background. ②Acorns attached with strings, dyed with black ink, cut into halves, or placed on white/green/red paper were predated in situ with much lower predation rates and lasted the same duration. Compared with the controls, the acorns were removed away by rodents with the same first day rate and the removal lasted longer. The final removal rate of the acorns by rodents was increased, whereas that of predation in situ was decreased, and none were left in the spot. This may suggest that rodents in this case increased their predation risk expectation and adopted a strategy of “less predation proportion in situ”. ③Acorns that were burnt were not predated in situ as well as removed in the first day, but the rates were raised to the maxi- mum in the forth and fifth day and then declined to zero. Consequently, the final ratios of predation in situ and removal considerably decreased with many acorns, nearly 50%, being left intact. It can be hypothesized that the rodents responded to the change in odor of acorns by using the strategies of “less predation proportion in situ” and “less predating activities”, thereby resulting in larger number of acorns remained intact. ④ Acorns that were enwrapped were barely predated in situ, removed in the first day with a normal predation rate, which declined to nearly zero in the second day and then increased till it declined again from the fourth day to the final day. The final rate of predation in situ was lower than 5% without acorns remained intact, and the rate of removal of acorns showed a considerable relative increase. This suggests that when there was a change in both odor and status of acorns, rodents also adopted the “spying” and “less predation proportion in situ” strategy, Because the predation risk is critical, the sense of sight would play an important role in rodent’s living. (3) Definite amounts of acorns were predated in situ, discarded, removed away, predated ex situ, lost and hoarded separately.

Key Words: sharptooth oak (Quercus aliena var. acuteserrata); rodent; acorn; predation strategy; forest regeneration; oak.

1 Introduction the last century. As a genera, Quercus includes more than 400 species, many of which are also the dominant species in the The effect of animals on the regeneration of oak forests has vegetation of temperate and sub-tropical regions[1]. Quercus been under intensive study for ecologists and foresters since aliena var. acuteserrata is widely distributed in many prov-

WANG Zhonglei et al. / Acta Ecologica Sinica, 2006, 26(11): 3533–3541 inces of China, such as Liaoning, Shanxi, Gansu, Shandong, were located in Mati Village of Mao County, Sichuan province, Henan, Hubei, Hunan, Jiangsu, Sichuan, as well as many re- China. The general information on the sites was also collected gions of the Korean peninsula and Japan[2]. Seeds of the gen- (Table 1). Further details on the location of the study site have era, often called acorns, are usually large and nutritious, and been provided in other papers by the authors[15]. therefore serve as a nutritional source of food for some birds 2.2 General approach and many mammals. Although rodents predate on most of the Forty-eight points were randomly selected in three sites of seed crops, they play pivotal roles in the redistribution of Mati Village on September, 2002; ten acorns of Quercus acorns[4]. Several reports are available on predation, hoarding, aliena var. acuteserrata were placed on the ground at each or deposition of acorns by rodents; in the interaction among point, and were treated in two ways: 1) as controls; 2) a 50cm rodent activity, environmental conditions, and predating risks; yellow fine plastic string was fixed at the lower part of each in the differentiation of acorns by rodents[5－14]. Rodents usu- acorn by pulling it on. The statistics of acorns under different ally predate, remove, discard, leave, and hoard acorns, and fates were completed 3 days later. The discarded acorns, this process is often largely affected by the environmental which were slightly broken by rodents were collected and factors, the changes in the status of acorns, etc. However, very examined to check if they were healthy, that is, if they were few studies have ever focused on the following questions: damaged by pests or bacteria, or were rotten. A total of 400 How do rodents "feel" these factors? What is their response or acorns were also randomly collected and examined in the predating strategy to the variation in environments or the same way. It was also noteworthy to check whether the string status change of acorns? How will the final fate of rodents be was broken. affected? A large amount of acorns were also randomly collected and This paper focused on further understanding of these as- placed on the two sites of the Ecological Station, and 12 dif- pects by trying to know that, under certain treatment, how the ferent kinds of treatments were performed on them: 1) to burn fate of acorns varies in the dynamics and final result, and what until they were completely charcoalized; 2) to enwrap fully the pattern is. Further experiments were also carried out to with transparent plastic tape; 3) to enwrap fully with yellow analyze if rodents can discriminate the health status of acorns opaque plastic tape; 4) to fix fine transparent plastic string at before predation. the lower part of each acorn by pulling it on, and mark the Cage capture experiments and individual observation were information of its position on it; 5) to place acorns on white combined to estimate the species inventory of small animals. paper of 20cm×20cm size; 6) to place acorns on green paper And the results suggested that the following animal species of 20cm×20cm size; 7) to place acorns on red paper of 20cm predated acorns in three main different vegetation types of the ×20cm size; 8) to enwrap the acorns to a depth of 2–3 cm region, which includes Pinus tabulaefomis forest, deciduous with litter and a small amount of soil; 9) to dye the acorns coniferous mixed forest, and bushes, Niveventer excelsior, with black charcoal ink; 10) to place acorns on black paper of Rattus norvegicus, Rattus nitidus, Apodemus draco, Apodemus 20cm×20cm size; 11) to cut the acorns into halves, each half chevrieri, Apodemnus latronum, Eothenomys inez, and Sci- as an individual; 12) as controls. Ten acorns under one treat- urotamias davidianus. ment were considered 1 unit, and 12 different units formed 1 group. Twenty- five such groups were placed in 1 site, and 2 2 Methods sites of the Ecological Station were finished. Observations were made on a daily basis to determine the exact number of 2.1 Study site the acorns that remained intact, predated in situ, or removed Field studies were conducted in five sites: Two were located away until each kind of acorns were dispersed or consumed or in the Ecology Station of Mao County, Chengdu Institute of remained unchanged for a long time. Acorns with fixed strings Biology, Chinese Academy of Sciences, China; the other three

Table 1 Characteristics of plots

Sites Plots Acorn number Area (m2) Arbor/Brush coverage (%) Dominant plants*

Mati Village Gap 16×20 400 15/20 1, 2, and 3

Forest Edge 16×20 400 50/40 4, 5, and 2

Gap 16×10 520 20/30 6 and 4

Ecological Station Slope beside the Shanzha field 12×10×25 800 10/90 4, 2, and 7

Wayao Valley 12×10×25 1200 30/70 8, 7, and 9

*The numbers indicate the following:1 Cariaria sinica; 2 Rosa sp.; 3 Pyrus sp.; 4 Quercus aliena var.acuteserrata; 5 Ilex purpurea; 6 ferns; 7 Corylus het- erophylla var. sutchuenensis; 8 Pinus armandi.; 9 Fargesia sp. WANG Zhonglei et al. / Acta Ecologica Sinica, 2006, 26(11): 3533–3541 were searched in the whole region, and the distance and direc- 3.1 Dynamics tion from the original place to the found place for the found The dynamics of acorns that were kept in situ, predated in acorns,as well as the information of whether they were buried situ, and removed were displayed (Fig.1). Acorns in 3 kinds of and the strings were broken were recorded. fates were analyzed according to the corresponding curves, 2.3 Data analysis and the speed on the first day when the steepest change had The dynamics of each kind of acorns were displayed by us- occurred was defined as the initial rate of predation. ing time-number curves, and the confidence level of 0.05 was 3.2 Acorns that were left intact calculated and marked. ANOVA was used to compare the The initial rate of predation of this kind of acorns under 12 acorns under different treatments. The mean ratio of the treatments were significantly different (F = 28.816, df = 11, healthy acorns before and after predation was also calculated. p < 0.01) and could be ranked in a descending order by multi- A plot was constructed to show the distance and direction of ple comparison as follows: {1(treatment 1, the same for other the removed acorns from the original place to the found place. numbers)} >> {2, 3} > {4, 5, 6, 7} > {8, 9, 10, 11} > {12}, where {} means a group where no significant difference can 3 Results be found between treatments within a group, and therefore, all treatments among one group could be considered to be the

Fig. 1 Dynamics of acorns 1 acorns completely burned; 2 acorns enwrapped with translucent plastic tape; 3 acorns enwrapped with yellow plastic tape; 4 acorns attached with strings; 5 acorns placed on white paper; 6 acorns placed on green paper; 7 acorns placed on red paper; 8 acorns that were buried; 9 acorns dyed with black coal ink; 10 acorns placed on black paper; 11 acorns cut into halves; 12 acorns as controls. WANG Zhonglei et al. / Acta Ecologica Sinica, 2006, 26(11): 3533–3541 same; the groups in front of ">>" showed significant differ- acorns under different treatments, and the following results ence with all other ones behind ">>". Besides, only the groups were obtained: for acorns that remained intact, the ranking that were adjacent to each other and connected by 1 ">" order (from large to small; the same applies to all the acorns showed no difference between each other. This symbol system under different treatments) is: {1}>> {2, 3, 4, 5, 6, 7, 8, 9, 10, is used in this article. The rate of predation under all treat- 11, 12}; for acorns that were removed, the ranking order is: ments except those for 1, 2 and 3 began to decrease after the {2,3}>> {4,5,6,7,9,11}>>{12, 10, 8}>>{1}; for acorns that first day, and corresponded to a "hyperbola" curve. were predated in situ, the ranking order is: {12,10,8} >> 3.3 Acorns that were predated in situ {4,5,6,7,8,11}>>{1} <<{2,3}. The initial rate of predation of this kind of acorns under 12 3.6 The differentiation of the status of acorns by rodents treatments were significantly different (F = 16.074, df = 11, In 2002, the unhealthy acorns accounted for 30% of the to- p < 0.01) and can be ranked in a descending order by multiple tal number of acorns (N = 400), whereas the unhealthy acorns comparison as follows: {12, 8}> {10} > {4, 5, 6, 7, 9, 11} >> accounted for 82% (N = 74) of the total number of acorns that {1, 2, 3}. The rate of predation under all treatments except were discarded by rodents, thereby suggesting a significant those for 1, 2, and 3 began to decrease after the first day and increase. A total of 266 acorns; were collected in 2003, and corresponded to a "hyperbola" curve, and no predation in situ these acorns did not germinate in moist sands for 4 weeks. It was observed after 5 days, except that the acorns that were has been reported that the acorns can germinate once they burnt showed a peak corresponding to predation in situ on the come in contact with the ground and acquire sufficient mois- 4th day. ture[15]. Therefore, these acorns might be severely damaged 3.4 Acorns that were removed because of the predation by rodents or by their own dysfunc- The initial rate of predation of this kind of acorns under 12 tion. treatments were significantly different (F = 15.364, df = 11, 3.7 Distance and direction of removed acorns and their p < 0.01) and could be ranked in a descending order by multi- general fates ple comparison as follows: {2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12} >> 31.6% of the total acorns in Mati Village were predated in {1}. The rate of predation (removing in this case) under all situ and 37.6% were removed after 3 days. The removing dis- treatments except those for 1, 2, and 3 began to decrease after tance for 82.3% of the removed acorns was over 5 meters (N = the first and second days, and corresponded to a "hyperbola" 334). 42.4% of the acorns that were removed less than 5 me- curve. Almost no acorns that were burnt (#1) were removed, ters away were predated in other places, 18.6% of which were but a peak of removing appeared on the 5th day. Acorns that hoarded in holes which is 1 meter deep, and the remaining were enwrapped (2 and 3) showed a decrease in the predation (39.0%) were lost under the forests in an intact status. 6.25% rate on the second day and a peak on the 4th day. (N=240) of the strings attached to the acorns were broken 3.5 Final fate of acorns down without any intertwisting with ground or branches. This The final rate of acorns, that is, the ratio of acorns that re- indicated that rodents identified the strings attached to the mained intact, predated in situ, and removed was displayed acorns and, broke them down. The reason that these ratios are (Table 2). different between Mati Village and the Ecological Station was Multiple comparisons were made among the final counts of that the experiments in the latter place lasted till constant

Table 2 Amounts (ratios) of acorns that were moved, predated in situ, or left intact

Treatment* Acorns moved Acorns predated in situ Acorns moved/predated Acorns left intact in situ 1 3.78 (37.8%) 1.26 (12.6%) 3.00 4.96 (49.6%) 2 9.72 (97.2%) 0.28 (2.8%) 34.7 0 3 9.58 (95.8%) 0.42 (4.2%) 22.8 0 4 7.74 (77.4%) 2.26 (22.6％) 3.42 0.02 (0.2%) 5 7.38 (73.8%) 2.62 (26.2%) 2.82 0 6 7.76 (77.6%) 2.24 (22.4%) 3.46 0 7 7.78 (77.8%) 2.22 (22.2%) 3.50 0 8 6.22 (62.2%) 3.78 (37.8%) 1.65 0 9 7.69 (76.9%) 2.30 (23.0%) 3.34 0.02 (0.2%) 10 7.02 (70.2%) 2.98 (29.8%) 2.36 0 11 8.16 (81.6%) 1.84 (18.4%) 4.43 0 12 6.48 (64.8%) 3.52 (35.2%) 1.84 0 Total average # 7.87 (78.7%) 2.14 (21.4%) 3.68 0.004 (0.04%) *The meaning of the number is the same as in the legend of fig. 1.# This data did not include that of acorns being burned WANG Zhonglei et al. / Acta Ecologica Sinica, 2006, 26(11): 3533–3541

treatments, such as burning, enwrapping, attaching strings, dying with color, cutting and placing on papers of different colors, and adopt different strategies to lower the risk. The acorns that were buried showed no difference with the controls, indicating that, although Johnson et al.[19] found that all rodents had decreased ability for searching the hoarding point as its depth increases, simple burying of the acorns as described in this paper had no effect on the behavior of the rodents. It can be deduced that the ability of rodents in identi- fying hoarded acorns only decreases when the acorns are hoarded to a certain level of depth or coverage. The acorns that were placed on black paper showed no difference with the controls, whereas acorns that were placed on white, red, and green papers all had significant difference with the controls in terms of response of the rodents. This might indicate that this difference results mainly from the difference in colors of the back flook, and rodents are more adapted to Fig. 2 Sketch map of the fate of acorns moved by rodents black background. Other research had proved that the colors of fruits varied; however, the brown and yellow colors pre- number of acorns was obtained. The distance and direction of dominated compared with other colors[20], and the background acorns that were removed were shown in Fig. 2. in the floor led to different responses of the rodents to acorns From Fig. 2, it is found that acorns within a removing dis- and, as a consequence, results in the evolution of the various tance of 6 meters were removed in all directions. 28.5% of the colors of fruits[21]. These results indicate that the background removed acorns were not hoarded, and the remaining were is important to animals, which is in agreement with the results hoarded (N=41). 77.0% (N=41) of the strings attached to of this study. acorns were gnawed and broken in situ or in other places, When compared with the controls, acorns that were at- 8.2% remained, and the left was lost unfound. This indicates tached with strings, dyed with black ink, cut into halves, and that rodents are sensitive to strings, and aroused new difficul- placed on white/green/red papers were predated in situ with ties for future research by this kind of labeling. decreased rate of predation, but the removing rate remained 4 Discussions constant at the beginning and then accelerated, and the moving lasted longer, resulting in higher proportions of removal 4.1 The interaction between the status and the back and lower proportions of predation in situ, and the number of floor of acorns and the activities of rodents acorns that were left intact was nearly 0. It might suggest that The initial ratios of predation for acorns that were removed if the status of acorns, such as whether they are attached to and acorns that were predated in situ had no direct relation- strings, what is the color of acorns, whether they are complete ships between each other, indicating that the dynamics of and what is the background color, changes but the odor of these two processes are independent, and the 12 treatments acorns keeps almost the same, suggesting that the quality of should have different effects on them. The predating risk is the food resources is not reduced, rodents raise their estimation to most important among all factors that influence the foraging predation risk, and adopt a sort of "less predation proportion [16] strategy of rodents, and this risk is widespread . Foraging in situ" strategy. under this pressure, rodents would make a trade-off between Burning resulted in considerable loss of odor of acorns, but risk and benefits, and change their behavior accordingly. Và did not necessarily charcoalize the acorns completely. The [17] squez found that Phyllotis darwini tended to seek safety and initial rate of predation for both predation in situ and remov- predated only in the central region of an environmental patch ing decreased to nearly 0, and then reached a small peak and when they were faced with predation risk. Zhenglong Wang decreased to 0 again with 49.6% remained intact. Especially, found that the predation risk had a blocking effect on the the relative proportion of predation in situ showed a consider- preying activity of Microtus oeconomus, thereby resulting in able decrease when compared with the controls. The dual much shorter duration of preying. change in odor and status of burnt acorns might mean raised Moving acorns concerns whether they are reliable food re- risk and poor quality of food; consequently, rodents regulated sources, but foraging concerns the factors that affect predation their predation peak time, causing the removing and predating risk, such as the safety of predation place and the availability activities to increase slowly to the peak. This phenomenon of food resources. Therefore, rodents responded differently to may suggest a "spying" strategy, which, combined with a "less WANG Zhonglei et al. / Acta Ecologica Sinica, 2006, 26(11): 3533–3541 predation proportion in situ" strategy, may lower the risk, and that were discarded, 82% was unhealthy while of the natural a "less predating activity" strategy which was used to deal acorns, 30% was unhealthy, suggesting that rodents would with low food quality. But the extent to which the odor of discard unhealthy rodents after they broke them and that they acorns was reduced should reach a "threshold" because, as possess highly developed sense of odor[33]. But a threshold discussed before, rodents do not respond to the simple burying should still be applied in this case. For example, if the reduc- of acorns. tion in the odor had the same extent as that of burning, then The rate of predation in situ of acorns that were enwrapped rodents would not predate as much as they usually did in was nearly 0 and corresponded to a "V" shaped curve. The healthy acorns. It may also be a relative discrimination. This number of acorns that were left intact were nearly 0, and less conclusion was also supported by certain research that mam- than 5% was predated in situ, whereas the proportion of mals and birds discriminated acorns which were preyed on by acorns that were removed considerably increased. This re- bugs, thereby avoiding predating preyed seeds[34].. sponse may suggest that enwrapping produced dual change in 4.3 Relationship between rodents and the regeneration odor and status, which also considerably increased the preda- of forests tion risk and decreased the quality of food. Rodents adopted a In this research, only 0.4% acorns remained intact in the "spying" strategy, as supported by the "V" shape of removing natural environments of the experiments of this study. But the speed, and a "less predation proportion in situ" strategy with predating activities of rodents are usually randomly affected much more acorns removed than those left intact when com- by environmental conditions, status of acorns, and predation pared even with other treatments which also led the same risk; moreover, acorns are produced in large amounts, and strategy. However, the lowered odor intensity produced by seedling can also produce seeds during its early age; all these enwrapping might not be as low as that by burning; therefore, make it difficult to conclude that rodents controlled the regen- less acorns were left intact. Howard and Cole also reported eration of oak forests. However, the almost zero ratio of pre- that animals are highly sensitive in the detection of seeds by dation remaining, and the fact that the discarded ones cannot odor[22,23], and the results of this study also support their con- germinate also indicates that rodents might be an important clusions. factor in the regeneration of oak forest. Rodents generally adopted a "less predation proportion in In 2003, 78.66% (N = 5500) of the acorns was removed, situ" strategy to fit the increased predation risk. During this and 21.32% was predated in situ. According to the data from process, they also rely on other sensory facilities. For example, the Ecological Station, 71.5% (N = 51) of the removed ones their sense to the background color, the intactness of acorns, were hoarded, and 28.5% were lost during the removing proc- and whether acorns are attached with other objects would ess. And in Mati Village, 18.5% of the acorns that were re- necessarily depend on the sense of sight or the light. There are moved less than 5 m away from the original points were also other reports proving that rodents depend on three meth- hoarded, 42.4% were predated in other places, and 39.0% ods to rediscover the hoarding sites[24]: spacial memory[25], the were lost in the forest. These removing and hoarding activities sense of odor, and the sense of sight. Pyare concluded that would largely help the distribution of acorns and also the ger- Kangaroo Rat depend on both sense of odor and sense of sight mination of acorns[35]. As a result, rodents may play a role in for finding a hoarding place[26]. the regeneration of oak forests by hoarding or removing All these researches agree with the conclusions of this study acorns to new environments. Wild oak forests are often found and emphasize the importance of sight to the predating be- spreading toward high elevation in continuous or discrete havior of rodents. The observations of this study indicate that manner, suggesting an effect of rodents. However, other re- rodents also gnawed the strings when they "saw" the strings. It searchers have found that only under the conditions of mass may be concluded that the predation activity belongs to a production, with huge hoarding and without severe re-dis- mixed pattern with emphasis on the sense of odor and the covery and predation, would hoarding play a role in the re- sense of sight. generation of forests[36－38]. Besides, rodents adopted a "less 4.2 Discrimination of the health status of acorns by ro- predation proportion in situ" strategy to poor quality of acorns, dents leading to a much higher proportion of unhealthy acorns in the Jerome[27] found that rodents cannot discriminate whether hoarded ones. This makes the fate of acorns even more com- acorns are ill matured or preyed by bugs, whereas others plex. proved that rodents cannot tell acorns that are preyed from A substantial proportion of acorns were predated in other acorns that are healthy[28－31]. For example, of the 136 seeds of than the original places, indicating that rodents also select Aesculus hippocastanum hoarded by Sciurus carolinensis in their predating sites. It was also observed in this study that New Jersey, 11% were completely rotten and 57% were par- many acorns that were removed were predated in high and dry tially rotten[32]. This study indirectly confirmed this conclusion, slopes, which was relatively safe to them. This fact further but in addition it included a new conclusion. Of the acorns supports the conclusion that predating activities are always WANG Zhonglei et al. / Acta Ecologica Sinica, 2006, 26(11): 3533–3541 related to a highly developed sense and an estimation of risks Ecologica Sinica, 2001, 21(3): 374–384. by rodents. [12] Xiao Z S, Zhang Z B, Wang Y S, Cheng J R. Acorn predation Finally, the effects of rodents on seedling establishment and and removal of Quercus serrata in a shrubland in Dujiangyan forest regeneration are beneficial in terms of the redistribution Region. China Acta Zoologica Sinica, 2004, 50(4): 535–540. of acorns to safe and favorable sites where germination and [13] Sun S C, Chen L Z. The effects of animal removal and seedling establishment might be much easier than other sites, groundcover on the fate of seeds of Quercus liaotungensis. but they might be harmful in terms of the consumption of Acta Ecologica Sinica, 2001, 21(1): 80–85. most biomass of acorns. 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