啮齿动物对六盘山区辽东栎、野李和华山松种子的取食和搬运

doi:10.3724/SP.J.1003.2012.10193

摘要/Abstract

摘要：

为了阐明不同种子投放方式和覆盖处理对啮齿动物取食和搬运/贮藏种子行为的影响, 2010年春季, 我们在宁夏六盘山区的辽东栎幼林, 用塑料标签标记法研究了不同种子投放方式(单独投放、两两组合投放和混合投放)和覆盖处理(对照、凋落物覆盖和土壤覆盖)下啮齿动物对辽东栎、野李和华山松种子的取食和搬运特点。结果表明: (1)不同物种、不同种子投放方式和覆盖处理对种子的就地取食率、搬运后的取食率和贮藏率均具有显著影响, 种子较大或具有厚而坚硬的种皮(内果皮)、组合和混合投放及覆盖处理均不同程度地促进啮齿动物对种子的搬运; (2)3种植物的种子被搬运后取食和贮藏的平均距离范围均在5.5 m以内, 而且种子被搬运后贮藏的距离均大于搬运后取食的距离, 其中华山松种子被搬运后取食的距离显著大于辽东栎和野李种子, 但搬运后的贮藏距离显著小于后两者。(3)种子被搬运后单个种子的取食点和贮藏点占多数, 其他大小的取食点和贮藏点较少, 种子被搬运后以土壤埋藏为主要的贮藏方式。结果表明, 种子的种皮特征以及种子在群落中的分布方式和存在状态, 可能通过延长啮齿动物处理的时间而增大啮齿动物的被捕食风险, 使动物改变对种子的取食和搬运行为, 进而决定了种子的命运。

关键词: 啮齿动物, 种子命运, 分散贮藏, 种子扩散, 六盘山区

Abstract

We established a field experiment to explore effects of different releasing methods and coverage treatments on predation and removal of Quercus wutaishanica, Prunus salicina and Pinus armandii seeds by rodents. We used three release (separately releasing, assembly releasing, and blend releasing) and cover (control, litter coverage, and soil coverage) treatments in young Q. wutaishanica stands in the Liupan Mountains of Ningxia in spring 2010. We detected significant effects of seeds of different species, release methods, and coverage treatments on the in situ seed predation rate. Seed predation and hoarding rates after removal by rodents were influenced by seed size, thickness and hardness of seed testa (endocarp), release methods, and coverage treatments. Although the average distance of seed movement during predation and hoarding events was within 5 m, the hoarding distance was longer than the predation distance for all three species. Specifically, we found that the predation distance of P. armandii seeds was significantly longer than those of Q. wutaishanica and P. salicina seeds, whereas the hoarding distance of the former was significantly shorter than the other two species. Sites that rodents used as predation and cache sites tended to contain only a single seed at a majority of the detected cache and predation sites. Soil burial was the primary strategy that rodents used to cache seeds. In summary, seed physical characteristics, distributional patterns, and ground coverage in forest communities may affect seed predation and hoarding behaviors of rodents by extending seed handling time and increasing predation risk of estimation by rodents and as a result, determined seed fates.

Key words: rodent, seed fate, scatter hoarding, seed dispersal, Liupan Mountains

闫兴富, 余杨春, 周立彪, 周云峰 (2012) 啮齿动物对六盘山区辽东栎、野李和华山松种子的取食和搬运. 生物多样性, 20, 427-436. DOI: 10.3724/SP.J.1003.2012.10193.

Xingfu Yan, Yangchun Yu, Libiao Zhou, Yunfeng Zhou (2012) Seed predation and removal of Quercus wutaishanica, Prunus salicina and Pinus armandii by rodents in the Liupan Mountains. Biodiversity Science, 20, 427-436. DOI: 10.3724/SP.J.1003.2012.10193.

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链接本文: https://www.biodiversity-science.net/CN/10.3724/SP.J.1003.2012.10193

https://www.biodiversity-science.net/CN/Y2012/V20/I4/427

图/表 7

图1 不同覆盖处理的种子投放点在样带上的分布示意图(每一圆圈表示一个种子投放点)。C, 对照; LC, 凋落物覆盖; SC, 土壤覆盖。

Fig. 1 Distribution diagram of releasing plots of different coverage treatments in sample transect. Each circle indicates a releasing plot of seeds. C, Control; LC, Litter coverage; SC, Soil coverage.

表1 不同物种、投放方式和覆盖处理对啮齿动物取食、搬运辽东栎、野李和华山松种子影响的多因素方差分析

Table 1 Multi-way analysis of variance on effects of different species, releasing methods and coverage treatments on seed predation and removal of Quercus wutaishanica, Prunus salicina and Pinus armandii by rodents

变量 Variable	就地取食 Predation in situ			搬运后取食 Predation after removal			搬运后贮藏 Hoarding after removal
变量 Variable	df	F	P	df	F	P	df	F	P
S	2	37.1	0.000	2	7.1	0.001	2	7.7	0.001
RM	2	8.7	0.000	2	7.7	0.001	2	9	0.000
CT	2	1.3	0.281	2	11.7	0.000	2	3.4	0.038
S×RM	4	8.3	0.000	4	7.1	0.000	4	4.6	0.002
S×CT	4	3.5	0.011	4	4.1	0.004	4	10.8	0.000
RM×CT	4	1.1	0.358	4	2.1	0.095	4	5.6	0.001
S×RM×CT	8	1.5	0.177	8	1.9	0.064	8	1.5	0.171

表2 不同覆盖处理和投放方式下辽东栎、野李和华山松种子在六盘山区辽东栎幼林投放点的命运

Table 2 Fates of Quercus wutaishanica, Prunus salicina and Pinus armandii seeds in releasing plots of young Q. wutaishanica stands in Liupan Mountains under different coverage treatments and releasing methods

投放方式 Releasing method	覆盖处理 Coverage treatment	辽东栎 Quercus wutaishanica			野李 Prunus salicina			华山松 Pinus armandii
投放方式 Releasing method	覆盖处理 Coverage treatment	PIS (%)	PAR (%)	HAR (%)	PIS (%)	PAR (%)	HAR (%)	PIS (%)	PAR (%)	HAR (%)
单独投放 Seperately releasing	对照 Control	15.7 ± 4.2	0	2.8 ± 4.8	0	11.1 ± 7.3	29.6 ± 20.5	0	23.1 ± 4.2	0.9 ± 1.6
	凋落物覆盖 Litter coverage	5.6 ± 4.8	50.0 ± 17.3	5.6 ± 2.8	0	0	24.1 ± 14.0	0.9 ± 1.6	55.6 ± 9.6	0.9 ± 1.6
	土壤覆盖 Soil coverage	23.1 ± 3.2	25.0 ± 4.8	8.3 ±.8.0	0	0	0	0.9 ± 1.6	33.3 ± 15.5	0
组合投放 Assembly releasing	对照 Control	4.6 ± 4.1	0.9 ± 2.3	13.9 ± 10.4	0	0	34.3 ± 16.3	0	8.3 ± 11.5	13.9 ± 16.0
	凋落物覆盖 Litter coverage	0.9 ± 2.3	28.7 ± 24.4	9.3 ± 7.6	0	9.3 ± 12.5	25.9 ± 18.8	0.9 ± 2.7	17.6 ± 21.2	3.7 ± 6.7
	土壤覆盖 Soil coverage	4.6 ± 7.4	26.9 ± 28.4	4.6 ± 5.5	0	42.6 ± 47.4	5.6 ± 7.0	0	7.4 ± 10.9	1.9 ± 2.9
混合投放 Blend releasing	对照 Control	0	0	2.8 ± 4.8	0	19.4 ± 9.6	25.0 ± 8.3	2.8 ± 4.8	36.1 ± 4.8	30.6 ± 4.8
	凋落物覆盖 Litter coverage	2.8 ± 4.8	27.8 ± 12.7	13.9 ± 12.7	0	58.3 ± 25.0	16.7 ± 8.3	2.8 ± 4.8	55.6 ± 9.6	5.6 ± 9.6
	土壤覆盖 Soil coverage	5.6 ± 4.8	8.3 ± 8.3	25.0 ± 16.7	0	11.1 ± 4.8	8.3 ± 8.3	0	25.0 ± 16.7	50.0 ± 8.3

图2 辽东栎、野李和华山松种子在六盘山区辽东栎幼林被啮齿动物搬运后的取食和贮藏距离(平均值±SD)。同一命运类型不同物种间的不同字母表示差异显著。

Fig. 2 Seed predation and hoarding distances of Quercus wutaishanica(QW), Prunus salicina(PS) and Pinus armandii (PA) after removal by rodents in young Q. wutaishanica stands of Liupan Mountains. Different letters in different species within the same seed fate type indicate significant difference at P = 0.05 level.

图3 辽东栎、野李和华山松种子在六盘山区辽东栎幼林被啮齿动物搬运后取食(A)和贮藏(B)距离的分布频次

Fig. 3 Distribution frequency of predation (A) and hoarding (B) distance of Quercus wutaishanica, Prunus salicina and Pinus armandii seeds after removal by rodents in young Q. wutaishanica stands of Liupan Mountains.

表3 辽东栎、野李和华山松种子被啮齿动物搬运后不同大小的取食点和贮藏点数量(括号内数字为占总数的百分比)

Table 3 Numbers of different size of seed predation site and cache site of Quercus wutaishanica, Prunus salicina and Pinus armandii after removal by rodents (The number in bracket is the percentage of total )

取食点/贮藏点大小 Size of predation site/ cache site	取食点 Predation site			贮藏点 Cache site
取食点/贮藏点大小 Size of predation site/ cache site	辽东栎 Quercus wutaishanica	野李 Prunus salicina	华山松 Pinus armandii	辽东栎 Quercus wutaishanica	野李 Prunus salicina	华山松 Pinus armandii
1	58 (82.9)	3 (23.1)	40 (62.5)	53 (94.6)	131 (94.2)	39 (83.0)
2	2 (2.9)	2 (15.4)	7 (10.9)	2 (3.6)	4 (2.9)	3 (6.4)
3	1 (1.4)	1 (7.7)	3 (4.7)	1 (1.8)	1 (0.7)	3 (6.4)
4	3 (4.3)	2 (15.4)	3 (4.7)	-	2 (1.4)	1 (0.7)
5	1 (1.4)	-	-	-	1 (0.7)	1 (0.7)
6	1 (1.4)	-	-	-	-	-
7	-	1 (7.7)	1 (1.6)	-	-	-
9	-	-	2 (3.1)	-	-	-
10	-	-	1 (1.6)	-	-	-
11	-	-	2 (3.1)	-	-	-
12	-	-	1 (1.6)	-	-	-
15	1 (1.4)	1 (7.7)	-	-	-	-
19	-	1 (7.7)	1 (1.6)	-	-	-
23	-	-	1 (1.6)	-	-	-
25	-	-	1 (1.6)	-	-	-
40	1 (1.4)	-	-	-	-	-
46	1 (1.4)	1 (7.7)	1 (1.6)	-	-	-
72	1 (1.4)	1 (7.7)	-	-	-	-

图4 辽东栎、野李和华山松种子在六盘山区辽东栎幼林被啮齿动物搬运后不同贮藏方式和丢弃种子的百分比。同一贮藏类型(或丢弃)的不同物种间的不同字母表示差异显著。

Fig. 4 Seeds proportion of different hoarding / discarding types of Quercus wutaishanica (QW), Prunus salicina (PS) and Pinus armandii (PA) after removal by rodents in young Q. wutaishanica stands of Liupan Mountains. Different letters in different species within the same hoarding / discarding types indicate significant difference at P = 0.05 level.

参考文献 38

[1]	Chang G, Xiao ZS, Zhang ZB (2009) Hoarding decisions by Edward’s long-tailed rats (Leopoldamys edwardsi) and South China field mice( Apodemus draco): the responses to seed size and germination schedule in acorns. Behavioral Processes, 82, 7-11.
[2]	Chen F (陈帆), Chen J (陈进) (2011) Effects of Pinus armandii seed size on rodents caching behavior and its spatio-temporal variations. Zoological Research (动物学研究), 32, 435-441. (in Chinese with English abstract) DOI URL PMID
[3]	Cheng JR (程瑾瑞), Xiao ZS (肖治术), Zhang ZB (张知彬) (2007) Effects of burial and coating on acorn survival of Quercus variabilis and Q. serrata under rodent predation. Chinese Journal of Ecology (生态学杂志), 26, 668-672. (in Chinese with English abstract)
[4]	Dally JM, Clayton NS, Emery NJ (2006) The behaviour and evolution of cache protection and pilferage. Animal Behaviour, 72, 13-23.
[5]	Fedriani JM, Manzaneda AJ (2005) Pre- and post-dispersal seed predation by rodents: balance of food and safety. Behavioral Ecology, 16, 1018-1024.
[6]	Gómez JM, Puerta-Piñero C, Schupp EW (2008) Effectiveness of rodents as local seed dispersers of Holm oaks. Oecologia, 155, 529-537. URL PMID
[7]	Grubb PJ (1977) The maintenance of species-richness in plant communities: the importance of the regeneration niche. Biological Reviews, 52, 107-145.
[8]	Howe HF, Brown JS (2001) The ghost of granivory past. Ecology Letters, 4, 371-378.
[9]	Hulme PE (2002) Seed-eaters: seed dispersal, destruction and demography. In: Seed Dispersal and Frugivory: Ecology, Evolution and Conservation (eds Levey DJ, Silva WR, Galetti M), pp. 257-273. CAB International Publishing, Wallingford.
[10]	Jansen PA, Bongers F, Hemerik L (2004) Seed mass and mast seeding enhance dispersal by a neotropical scatter-hoarding rodent. Ecological Monographs, 74, 569-589. DOI URL
[11]	Jennifer FH, Karen EF (2009) Postdispersal sugar maple (Acer saccharum) seed predation by small mammals in a northern hardwood forest. The American Midland Naturalist, 162, 213-223.
[12]	Li HJ, Zhang ZB (2003) Effect of rodents on acorn dispersal and survival of the Liaodong oak (Quercus liaotungensis Koidz.). Forest Ecology and Management, 176, 387-396.
[13]	Lima SL, Dill LM (1990) Behavioral decision made under the risk of predation: a review and prospectus. Canadian Journal of Zoology, 68, 619-640.
[14]	Lu JQ (路纪琪), Zhang ZB (张知彬) (2004) Seed-hoarding behavior of wild apricot and Liaodong oak by small rodents. Acta Theriologica Sinica (兽类学报), 24, 132-138. (in Chinese with English abstract)
[15]	Lu JQ (路纪琪), Zhang ZB (张知彬) (2005) Effects of high and low shrubs on acorn hoarding and dispersal of Liaodong oak (Quercus liaotungensis) by small rodents. Acta Zoologica Sinica (动物学报), 51, 195-204. (in Chinese with English abstract)
[16]	Martínez I, González-Taboada F (2009) Seed dispersal patterns in a temperate forest during a mast event: performance of alternative dispersal kernels. Oecologia, 159, 389-400. DOI URL PMID
[17]	Moore JE, McEuen AB, Swihart RK, Contreras TA, Steele MA (2007) Determinants of seed removal distance by scatter-hoarding rodents in deciduous forests. Ecology, 88, 2529-2540. DOI URL PMID
[18]	Purves DW, Zavala MA, Ogle K, Prieto F, Rey Benayas JM (2007) Environmental heterogeneity, birdmediated directed dispersal, and oak woodland dynamics in Mediterranean Spain. Ecological Monographs, 77, 77-97.
[19]	Reed AW, Kaufman GA, Kaufman DW (2006) Effect of plant litter on seed predation in three prairie types. American Midland Naturalists, 15, 278-285.
[20]	Sun MY (孙明洋), Ma QL (马庆亮), Tian SL (田澍辽), Wang JD (王建东), Lu JQ (路纪琪) (2011) Effects of seed productivity on dispersal of nuts of Quercus variabilis by rodents. Acta Theriologica Sinica (兽类学报), 31, 265-271. (in Chinese with English abstract)
[21]	Sun SC (孙书存), Chen LZ (陈灵芝) (2001) The effects of animal removal and groundcover on the fate of seeds of Quercus liaotungensis. Acta Ecologica Sinica (生态学报), 21, 80-85. (in Chinese with English abstract)
[22]	Tamura N, Katsuki T, Hayashi F (2005) Walnut seed dispersal: mixed effects of tree squirrels and field mice with different hoarding ability. In: Seed Fate: Predation, Dispersal and Seedling Establishment (eds Forget PM, Lambert JE, Hulme PE, Vander Wall SB), pp. 241-252. CAB International Publishing, Wallingford.
[23]	Tong L (仝磊), Lu JQ (路纪琪) (2010) Community structure and its seasonal variation of small mammals in Xishuangbanna of Yunnan, China. Chinese Journal of Ecology (生态学杂志), 29, 1770-1776. (in Chinese with English abstract)
[24]	Vander Wall SB (1990) Food Hoarding in Animals. The University of Chicago Press, Chicago.
[25]	Vander Wall SB (1995) The effects of seed value on the caching behavior of yellow pine chipmunks. Oikos, 74, 533-537.
[26]	Vander Wall SB, Longland WS (2005) Diplochory and the evolution of seed dispersal. In: Seed Fate: Predation, Dispersal and Seedling Establishment (eds Forget PM, Lambert JE, Hulme PE, Vander Wall SB), pp. 297-314. CAB International Publishing, Wallingford.
[27]	Wang B, Chen J (2009) Seed size, more than nutrient or tannin content, affects seed caching behavior of a common genus of Old World rodents. Ecology, 90, 3023-3032. DOI URL PMID
[28]	Xiao ZS, Zhang ZB, Wang YS, Cheng JR (2004) Acorn predation and removal of Quercus serratain in a shrubland in Dujiangyan Region, China. Acta Zoologica Sinica, 50, 536-540.
[29]	Xiao ZS, Wang YS, Harris M, Zhang ZB (2006) Spatial and temporal variation of seed predation and removal of sympatric large-seeded species in relation to innate seed traits in a subtropical forest, Southwest China. Forest Ecology and Management, 222, 46-54.
[30]	Xiao ZS, Zhang ZB, Wang YS (2005) Effect of seed size on dispersal distance in five rodents-dispersed Fagaceous species. Acta Oecologica, 28, 221-229.
[31]	Xiao ZS (肖治术), Zhang ZB (张知彬), Wang YS (王玉山) (2003) Observations on tree seed selection and caching by Edward’s long-tailed rat (Leopoldamys edwardsi). Acta Theriologica Sinica (兽类学报), 23, 208-213. (in Chinese with English abstract)
[32]	Yi XF, Yang YQ (2011) Scatterhoarding of Manchurian walnut Juglans mandshurica by small mammals: response to seed familiarity and seed size. Acta Theriologica, 56, 141-147.
[33]	Yu F (于飞), Niu KK (牛可坤), Jiao GQ (焦广强), Lü HQ (吕浩秋), Yi XF (易现峰) (2011) Effect of small rodents on seed dispersal of five tree species in Xiaoxing’an Mountains. Journal of Northeast Forestry University (东北林业大学学报), 39(1), 11-13. (in Chinese with English abstract)
[34]	Zhang HM, Chen Y, Zhang ZB (2008a) Differences of disper-sal fitness of large and small acorns of Liaodong oak (Quercus liaotungensis) before and after seed caching by small rodents in a warm temperate forest, China. Forest Ecology and Management, 255, 1243-1250.
[35]	Zhang HM, Cheng JR, Xiao ZS, Zhang ZB (2008b) Effects of seed abundance on seed scatter-hoarding of Edward’s rat (Leopoldamys edwardsi Muridae) at the individual level. Oecologia, 158, 57-63. DOI URL PMID
[36]	Zhang ZB (张知彬), Wang FS (王福生) (2001) Effect of burial on acorn survival and seedling recruitment of Liaodong oak (Quercus liaotungensis) under rodent predation. Acta Theriologica Sinica (兽类学报), 21, 35-43. (in Chinese with English abstract)
[37]	Zhang ZB, Xiao ZS, Li HJ (2005) Impact of small rodents on tree seeds in temperate and subtropical forests, China. In: Seed Fate: Predation, Dispersal and Seedling Establishment (eds Forget PM, Lambert JE, Hulme PE, Vander Wall SB), pp. 269-282. CAB International Publishing, Wallingford.
[38]	Zong C, Wauters LA, Van Dongen S, Mari V, Romeo C, Martinoli A, Preatoni D, Tosi G (2010) Annual variation in predation and dispersal of Arolla pine (Pinus cembra L.) seeds by Eurasian red squirrels and other seed-eaters. Forest Ecology and Management, 260, 587-594.