蚂蚁筑巢对不同恢复阶段热带森林土壤易氧化有机碳时空动态的影响

doi:10.17520/biods.2019011

摘要/Abstract

摘要：

为探明热带森林恢复过程中蚂蚁筑巢对土壤易氧化有机碳(readily oxidizable carbon, ROC)时空动态的影响及机制, 本研究以西双版纳白背桐(Mallotus paniculatus)群落、野芭蕉(Musa acuminata)群落和崖豆藤(Mellettia leptobotrya)群落3种恢复阶段热带森林为研究对象, 设置“蚂蚁筑巢地”与“非巢地”2种处理进行野外控制实验, 对比分析蚁巢和非蚁巢土壤ROC含量的时空变化特征, 并揭示这些变化与土壤微生物生物量碳及理化性质之间的相互关系。结果表明: (1)蚂蚁筑巢显著影响热带森林土壤ROC含量(P < 0.05), 蚁巢土壤ROC含量较非蚁巢提高了14.2%。不同恢复阶段蚁巢与非蚁巢土壤ROC含量大小顺序为: 野芭蕉群落 > 崖豆藤群落 > 白背桐群落。(2)不同恢复阶段热带森林蚁巢与非蚁巢土壤ROC含量均呈单峰型的时间变化趋势(P < 0.05), 最大值出现在6月, 且各月份蚁巢土壤ROC含量均高于非蚁巢。(3)不同恢复阶段热带森林蚁巢和非蚁巢土壤ROC含量均随土层深度增加呈显著递减的垂直变化趋势(P < 0.05), 且蚁巢土壤ROC含量均大于非蚁巢(P < 0.05)。(4)蚂蚁筑巢引起的土壤理化性质变化对土壤ROC含量产生了一定的影响。土壤ROC含量与土壤pH和容重呈显著负相关(P < 0.05), 与土壤有机碳、微生物生物量碳、全氮、铵态氮及硝态氮呈显著正相关(P < 0.05)。土壤微生物生物量碳与总有机碳是蚁巢土壤ROC时空变化的主要贡献者, 而铵态氮、全氮和总有机碳是非蚁巢ROC时空变化的主控因子。因此, 蚂蚁筑巢改变热带森林土壤微生物量(如微生物生物量碳)及土壤理化性质(如总有机碳、铵态氮与全氮等), 进而显著影响土壤ROC的时空动态。

关键词: 蚂蚁筑巢, 易氧化有机碳, 土壤理化性质, 时空动态

Abstract

This study aimed to understand the mechanism of ant colonization on spatiotemporal variations of soil ROC (readily oxidizable carbon) during the restoration of tropical forests. The experiment was conduced with two treatments (ant nests and without nests) in three restoration stages of Xishuangbanna tropical forests (i.e. Mallotus paniculatus, Musa acuminata, and Mellettia leptobotrya communities). We compared the spatiotemporal dynamics of ROC concentrations in both treatments and concurrently measured soil microbial biomass carbon and physicochemical properties. The results showed that: (1) Ant colonization significantly affected soil ROC concentrations in the tropical forests (P < 0.05), and ROC concentrations in ant nests increased by 14% compared with the control soils. Soil ROC concentrations in three recovery stages were ranked as Musa acuminata community > Mellettia leptobotrya community > Mallotus paniculatus community. (2) ROC concentrations in ant nests and the control soils both showed unimodal temporal variations across the three restoration stages (P < 0.05). The maximum was observed in June, and monthly ROC concentrations were higher in ant nests than in the control soils. (3) ROC concentrations in ant nests and the control soils decreased along the soil profile across three restoration stages (P < 0.05), and they were higher in ant nests (P < 0.05). (4) Variations in soil physicochemical properties induced by ant colonization influenced soil ROC dynamics. Soil ROC was negatively correlated with soil pH and bulk density and positively correlated with soil organic carbon, microbial biomass carbon, total nitrogen, ammonium nitrogen and nitrate nitrogen (P < 0.05). Microbial biomass carbon and total organic carbon in soils were the main contributors to the spatiotemporal variation in ROC in ant nests, while ammonium nitrogen, total nitrogen and total organic carbon were the main controlling factors for the spatiotemporal variation in ROC in control soils. Overall, ant colonization significantly altered soil microbes (e.g. microbial biomass carbon) and soil physicochemical properties (e.g. total organic carbon, ammonium nitrogen and total nitrogen), which impacted spatiotemporal variations in ROC concentrations in the tropical forest soils.

Key words: ant colonization, readily oxidizable carbon, soil physicochemical properties, spatiotemporal dynamics

张哲, 王邵军, 陈闽昆, 曹润, 李少辉 (2019) 蚂蚁筑巢对不同恢复阶段热带森林土壤易氧化有机碳时空动态的影响. 生物多样性, 27, 658-666. DOI: 10.17520/biods.2019011.

Zhang Zhe, Wang Shaojun, Chen Minkun, Cao Run, Li Shaohui (2019) Effect of ant colonization on spatiotemporal dynamics of readily oxidizable soil carbon across different restoration stages of tropical forests. Biodiversity Science, 27, 658-666. DOI: 10.17520/biods.2019011.

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链接本文: https://www.biodiversity-science.net/CN/10.17520/biods.2019011

https://www.biodiversity-science.net/CN/Y2019/V27/I6/658

图/表 5

图1 不同恢复阶段热带森林蚁巢与非蚁巢土壤易氧化有机碳含量比较。不同字母表示蚁巢与非蚁巢土壤易氧化有机碳含量差异显著(P < 0.05)。

Fig. 1 Comparison of readily oxidizable carbon (ROC) concentrations in ant nests and the control soils across the three restoration stages of tropical forests. Different letters indicate significant differences between ant nests and control soils (P < 0.05).

图2 不同恢复阶段热带森林蚁巢与非蚁巢土壤易氧化有机碳含量的时间变化。不同字母表示蚁巢与非蚁巢土壤易氧化有机碳含量在同一月份间差异显著(P < 0.05)。

Fig. 2 Temporal changes of readily oxidizable carbon (ROC) concentrations in ant nests and control soils across the three restoration stages of tropical forests. Different letters indicate significant difference between ant nests and the control soils (P < 0.05).

图3 不同恢复阶段热带森林群落蚁巢与非蚁巢土壤易氧化有机碳含量的垂直变化。同一群落类型中不同字母表示蚁巢与非蚁巢土壤易氧化有机碳含量垂直分布差异性显著(P < 0.05)。

Fig. 3 Vertical variation of readily oxidizable carbon (ROC) concentrations in ant nests and the control soils across the three restoration stages of tropical forests. Different letters indicate differences in vertical variations of ROC concentrations in ant nests and control soils (P < 0.05).

表1 不同恢复阶段热带森林群落蚁巢和非蚁巢土壤理化性质

Soil physicochemical properties in ant nests and the control soils across the three restoration stages of tropical forests

图4 不同恢复阶段热带森林土壤理化性质对蚁巢和非蚁巢土壤易氧化有机碳(ROC)影响的主成分分析。A: 蚁巢; B: 非蚁巢。1: 白背桐群落; 2: 野芭蕉群落; 3: 崖豆藤群落。SOC: 土壤有机碳; MBC: 微生物生物量碳; TN: 全氮; HN: 水解氮; NH4+-N: 铵态氮; NO3--N: 硝态氮; SW: 土壤水分; ST: 土壤温度; BD: 容重。

Fig. 4 Principal component analysis for the effect of soil physicochemical properties on readily oxidizable carbon (ROC) in ant nests and the control soils across three forest restoration stages. A, Ant nests; B, Without ant nests. 1, Mallotus paniculatus community; 2, Musa acuminata community; 3, Mellettia leptobotrya community. SOC, Soil organic carbon; MBC, Microbial biomass carbon; TN, Total nitrogen; HN, Hydrolyzable nitrogen; NH4+-N, Ammonium nitrogen; NO3--N, Nitrate nitrogen; SW, Soil water; ST, Soil temperature; BD, Bulk density.

参考文献 41

[1]	Acea MJ, Carballas T ( 1990) Principal components analysis of the soil microbial populations of humid zone of Galicia (Spain). Soil Biology and Biochemistry, 22, 749-759. DOI URL
[2]	Blair GJ, Lefroy RDB, Lisle L ( 1995) Soil carbon fractions based on their degree of oxidation and the development of a carbon management index for agricultural systems. Australian Journal of Agricultural Research, 46, 1459-1466. DOI URL
[3]	Chen J, Cao JJ, Zhang SY, Fan YL, Wang XF, Wei YL ( 2013) Ants’ hill-building activities on the plant community structure in alpine meadow grassland in the northern Qinghai Lake, China. Journal of Earth Environment, 4, 1461-1469. (in Chinese with English abstract)
	[ 陈骥, 曹军骥, 张思毅, 樊云龙, 王小菲, 魏永林 ( 2013) 蚂蚁扰动对青海湖北岸高寒草甸草原群落结构影响. 地球环境学报, 4, 1461-1469.]
[4]	Chen XH, Yang QQ, Chen ZZ, Yu XB, Yang Q, Lei JR ( 2017) Distribution of soil easily oxidized organic carbon and its response to soil factors in the tropical coastal forest of Hainan Island, China. Journal of Central South University of Forestry & Technology, 37, 140-145. (in Chinese with English abstract)
	[ 陈小花, 杨青青, 陈宗铸, 余雪标, 杨琦, 雷金睿 ( 2017) 海南岛热带海岸森林土壤易氧化有机碳分布规律及其对土壤因子的响应. 中南林业科技大学学报, 37, 140-145.]
[5]	Chen XX, Liang AZ, Zhang XP ( 2012) Research methods of carbon sequestration by soil aggregates: A review. Chinese Journal of Applied Ecology, 23, 1999-2006. (in Chinese with English abstract)
	[ 陈晓侠, 梁爱珍, 张晓平 ( 2012) 土壤团聚体固碳的研究方法. 应用生态学报, 23, 1999-2006.]
[6]	Chen YW, Li XR, Su YG, Dou CH, Jia XH, Zhang ZS ( 2007) Study on the eco-functions of Formica cunicularia (Hymenoptera: Formicidae) in a revegetated area on the southeast fringe of Tengger Desert, North China. Acta Ecologica Sinica, 27, 1508-1514. (in Chinese with English abstract)
	[ 陈应武, 李新荣, 苏延桂, 窦彩虹, 贾晓红, 张志山 ( 2007) 腾格里沙漠人工植被区掘穴蚁(Formica cunicularia)的生态功能. 生态学报, 27, 1508-1514.]
[7]	Chen YY, Wei C, He H, Wang YG ( 2012) Correlation of physicochemical characteristics and microbial biomass among nest soil of Camponotus japonicus and Pachycondyla astute in Qinling Mountains. Journal of Northwest Forestry University, 27, 121-126. (in Chinese with English abstract)
	[ 陈元瑶, 魏琮, 贺虹, 王云果 ( 2012) 秦岭地区2种蚂蚁巢内土壤理化性质和微生物量的相关性研究. 西北林学院学报, 27, 121-126.]
[8]	Chen ZJ, Geng SC, Zhang JH, Setälä H, Gu Y, Wang F, Zhang X, Wang XX, Han SJ ( 2017) Addition of nitrogen enhances stability of soil organic matter in a temperate forest. European Journal of Soil Science, 68, 189-199. DOI URL
[9]	Diaz-Ravifia M, Acea MJ, Carballas T ( 1995) Seasonal changes in microbial biomass and nutrient flush in forest soils. Biology and Fertility of Soils, 19, 220-226. DOI URL
[10]	Duval ME, Galantinib JA, Martíneza JM, López FM, Wall LG ( 2016) Sensitivity of different soil quality indicators to assess sustainable land management: Influence of site features and seasonality. Soil & Tillage Research, 159, 9-22.
[11]	Folgarait PJ ( 1998) Ant biodiversity and its relationship to ecosystem functioning: A review. Biodiversity & Conservation, 7, 1221-1244.
[12]	Folgarait PJ, Perelman S, Gorosito N, Pizzio R, Fernández J ( 2002) Effects of Camponotus punctulatus ants on plant community composition and soil properties across land-use histories. Plant Ecology, 163, 1-13. DOI URL
[13]	Frouz J ( 2000) The effect of nest moisture on daily temperature regime in the nests of Formica polyctena wood ants. Insectes Sociaux, 47, 229-235. DOI URL
[14]	Frouz J, Holec M, Kalčík J ( 2003) The effect of Lasius niger (Hymenoptera, Formicidae) ant nest on selected soil chemical properties. Pedobiologia, 47, 205-212. DOI URL
[15]	He H, Wei C, Wang YG, Gao ZH ( 2011) The fungal diversity in nests of three soil-nesting ant species (Hymenoptera: Formicidae) in pine forests of Louguantai National Forest Park, China. Journal of Northwest Forestry University, 26, 129-134. (in Chinese with English abstract)
	[ 贺虹, 魏琮, 王云果, 高智辉 ( 2011) 秦岭楼观台油松林地3种土栖性蚂蚁巢内真菌多样性研究. 西北林学院学报, 26, 129-134.]
[16]	Holec M, Frouz J ( 2006) The effect of two ant species Lasius niger and Lasius flavus on soil properties in two contrasting habitats. European Journal of Soil Biology, 42, 213-217. DOI URL
[17]	Hou JH, Zhou DW, Jiang SC ( 2002) The effect of hill-building activities of ants on the species diversity of plant communities in Songnen grassland. Acta Phytoecologica Sinica, 26, 323-329. (in Chinese with English abstract)
	[ 侯继华, 周道玮, 姜世成 ( 2002) 蚂蚁筑丘活动对松嫩草地植物群落多样性的影响. 植物生态学报, 26, 323-329.]
[18]	Jiang PK ( 2005) Soil active carbon pool under different types of vegetation. Scientia Silvae Sinicae, 41(1), 10-13. (in Chinese with English abstract) DOI
	[ 姜培坤 ( 2005) 不同林分下土壤活性有机碳库研究. 林业科学, 41(1), 10-13.] DOI
[19]	Kilpelinen J, Finér L, Niemel P, Domisch T, Neuvonen S, Ohashi M, Risch AC, Sundström L ( 2007) Carbon, nitrogen and phosphorus dynamics of ant mounds (Formica rufa group) in managed boreal forests of different successional stages. Applied Soil Ecology, 36, 156-163. DOI URL
[20]	Liang J ( 2016) The Flooding Behavior and Structure Characteristics of Soil Dissolved Organic Matter in Water-Level- Fluctuating Zone of Three Gorges Reservoir Areas. PhD dissertation, Southwest University, Chongqing. (in Chinese with English abstract)
	[ 梁俭 ( 2016) 三峡库区消落带土壤溶解性有机质淹水释放行为与结构表征. 博士学位论文, 西南大学, 重庆.]
[21]	Liu MH, Sun X, Yu WJ, Qin LW, Feng FJ ( 2018) Seasonal dynamics of soil active organic carbon content in the original Pinus koraiensis forest in Changbai Mountains, China. Journal of Nanjing Forestry University (Natural Sciences Edition), 42(2), 67-74. (in Chinese with English abstract)
	[ 刘明慧, 孙雪, 于文杰, 秦立武, 冯富娟 ( 2018) 长白山不同海拔原始红松林土壤活性有机碳含量的生长季动态. 南京林业大学学报(自然科学版), 42(2), 67-74.]
[22]	Liu RT, Zhao HL, Zhao XY ( 2009) Distribution of mound of Formica cunicularia and its affecting factors on mobile dune in Horqin Sandy Land. Chinese Journal of Applied Ecology, 20, 376-380. (in Chinese with English abstract)
	[ 刘任涛, 赵哈林, 赵学勇 ( 2009) 科尔沁沙地流动沙丘掘穴蚁蚁丘分布及影响因素. 应用生态学报, 20, 376-380.]
[23]	Liu YH, Wang YH, Yu PT, Xiong W, Hao J, Zhang XB, Xu LH ( 2012) Soil organic carbon contents of Larix principis-rupprechtii plantations in the southern part of Liupan Mountains. Scientia Silvae Sinicae, 48(12), 1-9. (in Chinese with English abstract) DOI
	[ 刘延惠, 王彦辉, 于澎涛, 熊伟, 郝佳, 张晓蓓, 徐丽宏 ( 2012) 六盘山南部华北落叶松人工林土壤有机碳含量. 林业科学, 48(12), 1-9.] DOI
[24]	Ma HP, Guo QQ, Liu HM, Qian DF ( 2012) Variations of soil microbial biomass and readily oxidizable organic carbon along elevation gradient in Sejila Mountain, Tibet. Journal of Soil and Water Conservation, 26, 163-166. (in Chinese with English abstract)
	[ 马和平, 郭其强, 刘合满, 钱登锋 ( 2012) 西藏色季拉山土壤微生物量碳和易氧化态碳沿海拔梯度的变化. 水土保持学报, 26, 163-166.]
[25]	Macmahon JA, Mull JF, Crist TO ( 2000) Harvester ants (Pogonomyrmex spp.): Their community and ecosystem influences. Annual Review of Ecology & Systematics, 31, 265-291.
[26]	Matías L, Castro J, Zamora R ( 2012) Effect of simulated climate change on soil respiration in a Mediterranean-type ecosystem: Rainfall and habitat type are more important than temperature or the soil carbon pool. Ecosystems, 15, 299-310. DOI URL
[27]	Piao HC, Hong YT, Yuan ZY ( 2000) Seasonal changes of microbial biomass carbon related to climatic factors in soils from areas of southwest China. Biology and Fertility of Soils, 30, 294-297. DOI URL
[28]	Tripathi N, Singha RS, Hills CD ( 2016) Soil carbon development in rejuvenated Indian coal mine spoil. Ecological Engineering, 90, 482-490. DOI URL
[29]	Wang QK, Wang SL, Feng ZW, Huang Y ( 2005) Active soil organic matter and its relationship with soil quality. Acta Ecologica Sinica, 25, 513-519. (in Chinese with English abstract)
	[ 王清奎, 汪思龙, 冯宗炜, 黄宇 ( 2005) 土壤活性有机质及其与土壤质量的关系. 生态学报, 25, 513-519.]
[30]	Wang SJ, Wang H, Li JH ( 2016) Distribution characteristics of ant mounds and correlating factors across different succession stages of tropical forests in Xishuangbanna. Biodiversity Science, 24, 916-921. (in Chinese with English abstract)
	[ 王邵军, 王红, 李霁航 ( 2016) 热带森林不同演替阶段蚂蚁巢穴的分布特征及其影响因素. 生物多样性, 24, 916-921.]
[31]	Wang SJ, Wang H, Li JH, Zhang Z ( 2017) Ants can exert a diverse effect on soil carbon and nitrogen pools in a Xishuangbanna tropical forest. Soil Biology and Biochemistry, 113, 45-52. DOI URL
[32]	Wang Y, Ruan HH, Huang LL, Feng YQ, Qi Y ( 2010) Soil labile organic carbon with different land uses in reclaimed land area from Taihu Lake. Soil Science, 175, 624-630. DOI URL
[33]	Wo XT, Tian SY, Han LD, Shao YN, Liu YL ( 2014) Study on soil organic carbon under two types of vegetation in small Xing’an Mountains. Research of Soil and Water Conservation, 21, 13-17. (in Chinese with English abstract)
	[ 沃晓棠, 田松岩, 韩丽冬, 邵英男, 刘玉龙 ( 2014) 小兴安岭两种林型的土壤有机碳研究. 水土保持研究, 21, 13-17.]
[34]	Xu YY, Gong YB, Fu WQ, Cui YX, Chen YJ, Zhang HT ( 2016) Effect of different reform measures on soil carbon and nitrogen characteristics and carbon stability in low efficiency forest of Pinus massoniana in southern Sichuan Province. Journal of Soil and Water Conservation, 30, 226-230. (in Chinese with English abstract)
	[ 徐云岩, 宫渊波, 付万权, 崔亚潇, 陈耀嘉, 张海涛 ( 2016) 川南马尾松低效林不同改造措施对土壤碳、氮特征及其碳稳定性的影响. 水土保持学报, 30, 226-230.]
[35]	Yang XD, She YP, Zhang ZY, Cao M, Deng XB ( 2001) Studies on structure and diversity of ant groups in the fragmentary tropical rainforests of ‘Holy Hills’ of Dai nationality in Xishuangbanna, China. Acta Ecologica Sinica, 21, 1321-1328. (in Chinese with English abstract)
	[ 杨效东, 佘宇平, 张智英, 曹敏, 邓晓保 ( 2001) 西双版纳傣族“龙山”片断热带雨林蚂蚁类群结构与多样性研究. 生态学报, 21, 1321-1328.]
[36]	Yu XJ, Pu XP, Huang SJ, Fang QE, Xu N, Xu CL ( 2010) Effects of ants (Tetramorium sp.) on eastern Qilian Mountains alpine grassland ecosystem. Acta Prataculturae Sinica, 19, 140-145. (in Chinese with English abstract)
	[ 鱼小军, 蒲小鹏, 黄世杰, 方强恩, 徐宁, 徐长林 ( 2010) 蚂蚁对东祁连山高寒草地生态系统的影响. 草业学报, 19, 140-145.]
[37]	Zhai KY, Ma TY, Jin XM, Yuan ZX, Chen B, Guan QW ( 2017) Effects of thinning intensity on soil active organic carbon in Pinus massoniana plantation. Chinese Journal of Ecology, 36, 609-615. (in Chinese with English abstract)
	[ 翟凯燕, 马婷瑶, 金雪梅, 袁在翔, 陈斌, 关庆伟 ( 2017) 间伐对马尾松人工林土壤活性有机碳的影响. 生态学杂志, 36, 609-615.]
[38]	Zhang H, Huang YM, An SS, Xing XY ( 2013) Soil active organic carbon with different plant communities on the Loess Plateau. Research of Soil and Water Conservation, 20, 65-70. (in Chinese with English abstract)
	[ 张宏, 黄懿梅, 安韶山, 邢肖毅 ( 2013) 黄土高原森林带植被群落下土壤活性有机碳研究. 水土保持研究, 20, 65-70.]
[39]	Zhang X, Han SJ, Wang SQ, Gu Y, Yue LY, Feng Y, Geng SC, Chen ZJ ( 2016) Change of soil organic carbon fractions at different successional stages of Betula platyphylla forest in Changbai Mountains. Chinese Journal of Ecology, 35, 282-289. (in Chinese with English abstract)
	[ 张雪, 韩士杰, 王树起, 谷越, 岳琳艳, 冯月, 耿世聪, 陈志杰 ( 2016) 长白山白桦林不同演替阶段土壤有机碳组分的变化. 生态学杂志, 35, 282-289.]
[40]	Zhang Z, Wang SJ, Li JH, Cao R, Chen MK, Li SH ( 2019) Response of soil readily oxidizable organic carbon to plant community recovery of Xishuangbanna tropical forests. Acta Ecologica Sinica, doi: 10.5846/stxb201806021230. (in Chinese with English abstract)
	[ 张哲, 王邵军, 李霁航, 曹润, 陈闽昆, 李少辉 ( 2019) 土壤易氧化有机碳对西双版纳热带森林植物群落恢复的响应. 生态学报 , doi: 10.5846/stxb201806021230.]
[41]	Zhao XZ ( 2010) Soil Organic Carbon Pool and Turnover of Main Forest Community Type in Small Xing’an Mountains. PhD dissertation, Northeast Forestry University, Harbin. (in Chinese with English abstract)
	[ 赵溪竹 ( 2010) 小兴安岭主要森林群落类型土壤有机碳库及其周转. 博士学位论文, 东北林业大学, 哈尔滨.]