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浙江大学学报(农业与生命科学版)  2022, Vol. 48 Issue (6): 807-822    DOI: 10.3785/j.issn.1008-9209.2022.07.041
研究论文     
再生稻田拟环纹豹蛛与青翅蚁形隐翅甲间的集团内捕食及其影响因素
孙佳琦1(),王晨1(),王光华2,任应党2,祝增荣3,白耀宇1()
1.西南大学植物保护学院,重庆 400715
2.河南省农业科学院植物保护研究所,郑州 450002
3.浙江大学农业与生物技术学院昆虫科学研究所,农业农村部作物病虫分子生物学重点实验室,杭州 310058
Intraguild predation between Pardosa pseudoannulata and Paederus fuscipes in ratoon rice fields and its influencing factors
Jiaqi SUN1(),Chen WANG1(),Guanghua WANG2,Yingdang REN2,Zengrong ZHU3,Yaoyu BAI1()
1.College of Plant Protection, Southwest University, Chongqing 400715, China
2.Institute of Plant Protection, Henan Academy of Agricultural Sciences, Zhengzhou 450002, China
3.Ministry of Agriculture and Rural Affairs Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, China
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摘要:

重要广食性天敌间的集团内捕食(intraguild predation, IGP)水平关乎着农田系统其种群的发生和“绿色防控”策略的成效。本研究以再生稻田主要捕食者拟环纹豹蛛(Pardosa pseudoannulata)和青翅蚁形隐翅甲(Paederus fuscipes)为试验对象,首次建立和优化了实时荧光定量聚合酶链反应(quantitative real-time polymerase chain reaction, qPCR)探针法检测系统,利用该系统分析了再生稻田中这2种天敌间的IGP水平,并在室内条件下剖析了该IGP及其生物和非生物影响因素。结果表明:针对这2种天敌靶基因设计的引物和探针特异性强,建立和优化的qPCR探针法系统对靶基因的扩增重复性好且灵敏度高。通过该系统对再生稻田2种天敌1 527头个体的检测及室内IGP试验发现,这2种天敌间存在着普遍且较强的双向IGP作用,其中,捕食者和猎物角色的转化以及环境温度对该IGP水平的影响均与它们之间相对体型大小(发育阶段)密切相关;集团外猎物和非生物因素及其结合能不同程度地影响IGP水平。这些研究结果丰富了稻田系统捕食者间的IGP理论体系,为深入研究稻田捕食性天敌间IGP奠定了坚实的基础。

关键词: 捕食性天敌集团内猎物DNA检出率实时荧光定量聚合酶链反应天台刺齿跳虫环境温度集团内捕食水平    
Abstract:

The intraguild predation (IGP) level among the main generalist natural enemies is related to their population occurrence and the effectiveness of “green control” strategies for insect pests in agroecosystem. In this study, the detection systems of quantitative real-time polymerase chain reaction (qPCR) probe were first established and then optimized for analyzing the DNA of Pardosa pseudoannulata and Paederus fuscipes in ratoon rice fields. Then the detection systems were used to analyze the IGP levels between the two predators in ratoon rice fields. On this basis, the IGP and their biological and abiotic factors affecting the IGP level were studied under indoor conditions. The results showed that the primers and probes designed for the two predators had strong specificity. The established and optimized qPCR detection systems had good amplification repeatability and high sensitivity for the target genes of the two predators. After the system was used to detect 1 527 individuals of the two predators from ratoon rice fields and the indoor IGP tests, it was found that there was a ubiquitous and strong bidirectional IGP between the two predators in the rice field. The role transformation of intraguild predator or prey in the IGP and the influence of ambient temperature on the IGP level were closely related to their relative body sizes (developmental stages). The IGP level can be affected through extraguild preys and abiotic factors and their combination to various extents. These results enrich the IGP theory among arthropod predators in the rice ecosystem, and lay good foundations for further IGP study of natural enemies.

Key words: predatory natural enemy    DNA detection rate of intraguild prey    quantitative real-time polymerase chain reaction    Homidia tiantaiensis    ambient temperature    intraguild predation level
收稿日期: 2022-07-04 出版日期: 2022-12-25
CLC:  S 476.2  
基金资助: 国家自然科学基金项目(31772161);国家重点研发计划项目(2021YFD1401105)
通讯作者: 白耀宇     E-mail: sjq031015@163.com;w05240813@163.com;yybai711@163.com
作者简介: 孙佳琦(https://orcid.org/0000-0002-0294-0122),E-mail:sjq031015@163.com|王晨(https://orcid.org/0000-0002?4109?0191),E-mail:w05240813@163.com
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引用本文:

孙佳琦,王晨,王光华,任应党,祝增荣,白耀宇. 再生稻田拟环纹豹蛛与青翅蚁形隐翅甲间的集团内捕食及其影响因素[J]. 浙江大学学报(农业与生命科学版), 2022, 48(6): 807-822.

Jiaqi SUN,Chen WANG,Guanghua WANG,Yingdang REN,Zengrong ZHU,Yaoyu BAI. Intraguild predation between Pardosa pseudoannulata and Paederus fuscipes in ratoon rice fields and its influencing factors. Journal of Zhejiang University (Agriculture and Life Sciences), 2022, 48(6): 807-822.

链接本文:

https://www.zjujournals.com/agr/CN/10.3785/j.issn.1008-9209.2022.07.041        https://www.zjujournals.com/agr/CN/Y2022/V48/I6/807

图1  稻秆放置示意图

物种

Species

基因

Gene

引物与探针序列(5→3

Primer and probe sequences (5→3)

扩增序列长度

Amplified sequence

length/bp

GenBank登录号

GenBank accession No.

拟环纹豹蛛

Pp

COⅠF: CTTTTCTATTGATATTCCAGTCACC153

MZ149257、

MZ149265

R: CCACCGTTAGCGTCTACRG
Probe: Texas Red-CCCCAGCCAAATGAAGAGAAAA-BHQ2

青翅蚁形隐翅甲

Pf

ITSF: GGCGAAAGTAATCTGTTC139MZ172410
R: CGTTCAGGGTAATCTTTTAG
Probe: FAM-AGGTCCTCCGCTTACATCGC-MGB
表1  qPCR检测体系的引物与探针信息
图2  青翅蚁形隐翅甲和拟环纹豹蛛qPCR检测体系的扩增曲线

物种

Species

DNA浓度

DNA concentration

循环阈值 Cycle threshold (CT)

组内变异

Intragroup

variation/%

组间变异

Intergroup

variation/%

重复1

Repetition 1

重复2

Repetition 2

重复3

Repetition 3

青翅蚁形隐翅甲

Pf

1×10621.1020.8821.020.520.53
20.9820.7520.770.62
21.1720.6221.291.71
1×10525.0924.4824.951.290.88
24.5324.8424.620.65
25.1425.0625.060.20
1×10428.0327.1127.521.671.69
26.5626.7126.770.41
27.4027.3027.460.29

拟环纹豹蛛

Pp

1×10717.8818.6518.102.201.46
19.0118.7818.451.49
18.5818.6118.470.38
1×10621.1220.7621.100.952.28
21.2521.3421.691.07
22.1322.0321.711.00
1×10524.6524.5423.961.521.53
24.0223.6824.201.08
24.8024.2524.001.68
表2  针对2种捕食者建立和优化后的qPCR检测体系的扩增重复性分析

捕食者

Predator

采样点1

Sampling site 1

采样点2

Sampling site 2

统计参数

Statistical parameter

统计参数 Statistical parameterH=472.58, P<0.001H=410.83, P<0.001

隐翅甲成虫

Adult Pf

7.31±0.07b7.51±0.08bt=-1.86, P>0.05

豹蛛中龄幼蛛

Middle-instar juvenile Pp

5.76±0.04c5.87±0.05cZ=-1.90, P>0.05

豹蛛亚成蛛/成蛛

Subadult/adult Pp

8.48±0.07a8.42±0.06aZ=-0.25, P>0.05
表3  用于IGP中集团内猎物DNA检测的捕食者体长分析 (mm)
图3  拟环纹豹蛛和青翅蚁形隐翅甲间IGP中的集团内猎物DNA检出率A. 隐翅甲成虫捕食豹蛛;B. 豹蛛中龄幼蛛捕食隐翅甲;C. 豹蛛亚成蛛/成蛛捕食隐翅甲。图4同。**表示DNA检出率在P<0.01水平差异有高度统计学意义(卡方检验)。
  
集团内捕食 IGP采样点1 Sampling site 1采样点2 Sampling site 2

9月

Sep.

10月

Oct.

统计参数

Statistical

parameter

9月

Sep.

10月

Oct.

统计参数

Statistical parameter

隐翅甲成虫捕食豹蛛

Adult Pf preying on Pp

3.4×104±5.5×

103a, n=21

6.7×105±3.3×

105a, n=61

Z=-1.17,

P=0.24

8.4×104±3.0×

104b, n=31

1.3×105±1.8×

104a, n=68

Z=-3.46,

P=0.001

豹蛛中龄幼蛛捕食隐翅甲

Middle-instar juvenile Pp preying on Pf

9.1×104±4.1×

104, n=10

5.0×103, n=1

1.6×105±1.0×

105a, n=4

4.6×104±2.6×

104a, n=4

Z=-0.58,

P=0.56

豹蛛亚成蛛/成蛛捕食隐翅甲

Subadult/adult Pp preying on Pf

1.7×105±9.4×

104, n=62

6.5×104±4.6×

103, n=2

8.4×104±1.7×

104a, n=50

6.9×104±3.3×

104a, n=7

Z=-0.80,

P=0.42

表4  拟环纹豹蛛和青翅蚁形隐翅甲肠道内集团内猎物DNA拷贝数
图4  拟环纹豹蛛和青翅蚁形隐翅甲间IGP中的集团内猎物DNA检出率与环境温度变化的相关性
图5  拟环纹豹蛛和青翅蚁形隐翅甲间IGP中温度对集团内猎物DNA检出率的影响在拟合方程中,D代表集团内猎物DNA检出率,T代表环境温度。
图6  22 ℃下培养皿共存系统中饥饿(A)和未饥饿(B)拟环纹豹蛛成蛛与未饥饿青翅蚁形隐翅甲成虫间的IGP分析*表示相同试验时间2组间在P<0.05水平差异有统计学意义(Mann-Whitney U检验)。
图7  22 ℃下培养皿共存系统中饥饿(A1~A2 )和未饥饿(B1~B2 )青翅蚁形隐翅甲成虫与未饥饿拟环纹豹蛛低龄幼蛛间的IGP分析*和**分别表示相同试验时间2组间在P<0.05和P<0.01水平差异有统计学意义(Mann-Whitney U检验)

参量

Parameter

豹蛛成蛛×隐翅甲成虫(未饥饿)

Adult Pp×adult Pf (non-starvation)

豹蛛低龄幼蛛(未饥饿)×隐翅甲成虫

Low-instar juvenile Pp (non-starvation)×adult Pf

试验前饥饿处理豹蛛

Starvation treatment

on Pp before test (T1)

试验前未饥饿处理豹蛛

Non-starvation treatment

on Pp before test (T2)

试验前饥饿处理隐翅甲

Starvation treatment

on Pf before test (T3)

试验前未饥饿处理隐翅甲

Non-starvation treatment

on Pf before test (T4)

隐翅甲作为猎物的数量

Number of Pf acted as

the prey

2100

隐翅甲作为捕食者的数量

Number of Pf acted

as the predator

002416

IGP水平

IGP level/%

54.56053

IGP对称性指数

Symmetry index of IGP/%

100100100100
表5  22 ℃下培养皿共存系统中拟环纹豹蛛和青翅蚁形隐翅甲间的IGP分析
图8  各因素对拟环纹豹蛛低龄幼蛛和青翅蚁形隐翅甲成虫间IGP中集团内猎物存活率的影响
1 宋开付,张广斌,徐华,等.中国再生稻种植的影响因素及可持续性研究进展[J].土壤学报,2020,57(6):1365-1377. DOI:10.11766/trxb201907170371
SONG K F, ZHANG G B, XU H, et al. A review of research on influencing factors and sustainability of ratoon rice cultivation in China[J]. Acta Pedologica Sinica, 2020, 57(6): 1365-1377. (in Chinese with English abstract)
doi: 10.11766/trxb201907170371
2 POLIS G A, MYERS C A, HOLT R D. The ecology and evolution of intraguild predation: potential competitors that eat each other[J]. Annual Review of Ecology and Systematics, 1989, 20: 297-330.
3 ROUBINET E, BIRKHOFER K, MALSHER G, et al. Diet of generalist predators reflects effects of cropping period and farming system on extra- and intraguild prey[J]. Ecological Applications, 2017, 27(4): 1167-1177. DOI:10.1002/eap.1510
doi: 10.1002/eap.1510
4 LUCAS É, CODERRE D, BRODEUR J. Intraguild predation among three aphid predators: characterization and influence of extra-guild prey density[J]. Ecology, 1998, 79(3): 1084-1092.
5 JANSSEN A, SABELIS M W, MAGALHÃES S, et al. Habitat structure affects intraguild predation[J]. Ecology, 2007, 88(11): 2713-2719. DOI:10.1890/06-1408.1
doi: 10.1890/06-1408.1
6 RYPSTRA A L, SCHMIDT J M, REIF B D, et al. Tradeoffs involved in site selection and foraging in a wolf spider: effects of substrate structure and predation risk[J]. Oikos, 2007, 116(5): 853-863. DOI:10.1111/j.2007.0030-1299.15622.x
doi: 10.1111/j.2007.0030-1299.15622.x
7 FRANCES D N, MCCAULEY S J. Warming drives higher rates of prey consumption and increases rates of intraguild predation[J]. Oecologia, 2018, 187(3): 585-596. DOI:10.1007/s00442-018-4146-y
doi: 10.1007/s00442-018-4146-y
8 ROGERS T L, GOUHIER T C, KIMBRO D L. Temperature dependency of intraguild predation between native and invasive crabs[J]. Ecology, 2018, 99(4): 885-895. DOI:10.1002/ecy.2157
doi: 10.1002/ecy.2157
9 YU X L, ZHANG Y J, ZUO J F, et al. Rising temperatures affect the interspecific interference competition between Harmonia axyridis and Propylea japonica, and their predation rate on Myzus persicae [J]. Journal of Pest Science, 2022.
10 刘雨芳,张古忍,古德祥,等.用ELISA方法研究稻田节肢动物的食物关系[J].昆虫学报,2002,45(3):352-358. DOI:10.3321/j.issn:0454-6296.2002.03.013
LIU Y F, ZHANG G R, GU D X, et al. Enzyme linked immunosorbent assay used to detect the food relationship of the arthropods in paddy fields[J]. Acta Entomologica Sinica, 2002, 45(3): 352-358. (in Chinese with English abstract)
doi: 10.3321/j.issn:0454-6296.2002.03.013
11 乔飞,王光华,王雪芹,等.稻田穗期主要捕食性天敌对两种盲蝽集团内捕食的初步研究[J].应用昆虫学报,2016,53(5):1091-1102. DOI:10.7679/j.issn.20951353.2016.134
QIAO F, WANG G H, WANG X Q, et al. Preliminary study of intraguild predation by generalist predators on two mirids in ear-stage paddy fields[J]. Chinese Journal of Applied Entomology, 2016, 53(5): 1091-1102. (in Chinese with English abstract)
doi: 10.7679/j.issn.20951353.2016.134
12 SIGSGAARD L. Early season natural control of the brown planthopper, Nilaparvata lugens: the contribution and interaction of two spider species and a predatory bug[J]. Bulletin of Entomological Research, 2007, 97(5): 533-544. DOI:10.1017/S0007485307005196
doi: 10.1017/S0007485307005196
13 孙佳琦,王光华,任应党,等.温度变化对休耕期冬水田天敌捕食猎物的影响及天敌耐冷性分析[J].生态学报,2022,42(7):2943-2961. DOI:10.5846/stxb202104231073
SUN J Q, WANG G H, REN Y D, et al. Effect of temperature change on the predation of predatory arthropods from winter-spring fallow waterlogged paddy fields on their prey and the cold tolerance of the predators[J]. Acta Ecologica Sinica, 2022, 42(7): 2943-2961. (in Chinese with English abstract)
doi: 10.5846/stxb202104231073
14 YANG F, WANG Q, WANG D M, et al. Intraguild predation among three common coccinellids (Coleoptera: Coccinellidae) in China: detection using DNA-based gut-content analysis[J]. Environmental Entomology, 2017, 46(1): 1-10. DOI:10.1093/ee/nvw154
doi: 10.1093/ee/nvw154
15 MICHALKO R, PEKÁR S. The behavioral type of a top predator drives the short-term dynamic of intraguild predation[J]. The American Naturalist, 2017, 189(3): 242-253. DOI:10.1086/690501
doi: 10.1086/690501
16 SUN J Q, PANG S, WANG X Q, et al. Molecular quantification of spider preying on springtails in winter-spring fallow waterlogged paddy fields[J]. Applied Entomology and Zoology, 2021, 56: 165-172. DOI:10.1007/s13355-020-00712-8
doi: 10.1007/s13355-020-00712-8
17 白耀宇,庞帅,殷禄燕,等.冬水田典型生境类型节肢动物群落多样性及生物量特征[J].生态学报,2018,38(23):8630-8651. DOI:10.5846/stxb201801240187
BAI Y Y, PANG S, YIN L Y, et al. Arthropod species diversity and biomass of fallow waterlogged paddy fields in Chongqing, China[J]. Acta Ecologica Sinica, 2018, 38(23): 8630-8651. (in Chinese with English abstract)
doi: 10.5846/stxb201801240187
18 FOLMER O, BLACK M, HOEH W, et al. DNA primers for amplification of mitochondrial cytochrome C oxidase subunitⅠfrom diverse metazoan invertebrates[J]. Molecular Marine Biology and Biotechnology, 1994, 3(5): 294-299.
19 JI Y J, ZHANG D X, HE L J. Evolutionary conservation and versatility of a new set of primers for amplifying the ribosomal internal transcribed spacer regions in insects and other invertebrates[J]. Molecular Ecology Notes, 2003, 3(4): 581-585. DOI:10.1046/j.1471-8286.2003.00519.x
doi: 10.1046/j.1471-8286.2003.00519.x
20 MACÍAS-HERNÁNDEZ N, ATHEY K, TONZO V, et al. Molecular gut content analysis of different spider body parts[J]. PLoS ONE, 2018, 13(5): e0196589. DOI:10.1371/journal.pone.0196589
doi: 10.1371/journal.pone.0196589
21 王智.拟环纹豹蛛的生物生态学研究[J].昆虫学报,2007,50(9):927-932. DOI:10.16380/j.kcxb.2007.09.012
WANG Z. Bionomics and behavior of the wolf spider, Pardosa pseudoannulata (Araneae: Lycosidae)[J]. Acta Ento-mologica Sinica, 2007, 50(9): 927-932. (in Chinese with English abstract)
doi: 10.16380/j.kcxb.2007.09.012
22 KING R A, READ D S, TRAUGOTT M, et al. Molecular analysis of predation: a review of best practice for DNA-based approaches[J]. Molecular Ecology, 2008, 17(4): 947-963. DOI:10.1111/j.1365-294X.2007.03613.x
doi: 10.1111/j.1365-294X.2007.03613.x
23 ARMSBY M, TISCH N. Intraguild predation and canni-balism in a size-structured community of marine amphipods[J]. Journal of Experimental Marine Biology and Ecology, 2006, 333(2): 286-295. DOI:10.1016/j.jembe.2006.01.004
doi: 10.1016/j.jembe.2006.01.004
24 ZAREI M, MADADI H, ZAMANI A A, et al. Intraguild predation between Chrysoperla carnea (Neuroptera: Chrysopi-dae) and Hippodamia variegata (Coleoptera: Coccinellidae) at various extraguild prey densities and arena complexities[J]. Insects, 2020, 11(5): 288. DOI:10.3390/insects11050288
doi: 10.3390/insects11050288
25 ROUBINET E, JONSSON T, MALSHER G, et al. High redundancy as well as complementary prey choice characterize generalist predator food webs in agroecosystems[J]. Scientific Reports, 2018, 8: 8054. DOI:10.1038/s41598-018-26191-0
doi: 10.1038/s41598-018-26191-0
26 白月亮,周文武,祝增荣.气候变暖对天敌昆虫的影响[J].浙江大学学报(农业与生命科学版),2022,48(3):269-278. DOI:10.3785/j.issn.1008-9209.2021.05.171
BAI Y L, ZHOU W W, ZHU Z R. Effects of global warming on insect natural enemies[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2022, 48(3): 269-278. (in Chinese with English abstract)
doi: 10.3785/j.issn.1008-9209.2021.05.171
27 UITERWAAL S F, DELONG J P. Using patterns in prey DNA digestion rates to quantify predator diets[J]. Molecular Ecology Resources, 2020, 20(6): 1723-1732. DOI:10.1111/1755-0998.13231
doi: 10.1111/1755-0998.13231
28 VON BERG K, TRAUGOTT M, SYMONDSON W O C, et al. The effects of temperature on detection of prey DNA in two species of carabid beetle[J]. Bulletin of Entomological Research, 2008, 98(3): 263-269. DOI:10.1017/S0007485308006020
doi: 10.1017/S0007485308006020
29 KOBAYASHI T, TAKADA M, TAKAGI S, et al. Spider predation on a mirid pest in Japanese rice fields[J]. Basic and Applied Ecology, 2011, 12(6): 532-539. DOI:10.1016/j.baae.2011.07.007
doi: 10.1016/j.baae.2011.07.007
30 MCMILLAN S, KUUSK A K, CASSEL-LUNDHAGEN A, et al. The influence of time and temperature on molecular gut content analysis: Adalia bipunctata fed with Rhopalosiphum padi [J]. Insect Science, 2007, 14(5): 353-358. DOI:10.1111/j.1744-7917.2007.00152.x-i1
doi: 10.1111/j.1744-7917.2007.00152.x-i1
31 WEBER D C, LUNDGREN J G. Detection of predation using qPCR: effect of prey quantity, elapsed time, chaser diet, and sample preservation on detectable quantity of prey DNA[J]. Journal of Insect Science, 2009, 9(1): 41. DOI:10.1673/031.009.4101
doi: 10.1673/031.009.4101
32 PÉREZ-GUERRERO S, GELAN-BEGNA A, VARGAS-OSUNA E. Compatibility of Orius laevigatus and Cheiracan-thium pelasgicum for predation on Helicoverpa armigera eggs: effects of density and day/night activity on intraguild predation[J]. BioControl, 2015, 60(6): 783-793. DOI:10.1007/s10526-015-9681-4
doi: 10.1007/s10526-015-9681-4
33 YU X L, FENG Y, FU W Y, et al. Intraguild predation between Harmonia axyridis and Aphidius gifuensis: effects of starvation period, plant dimension and extraguild prey density[J]. BioControl, 2019, 64(1): 55-64. DOI:10.1007/s 10526-018-09913-1
doi: 10.1007/s
34 RANJBAR F, MICHAUD J P, JALALI M A, et al. Intraguild predation between two lady beetle predators is more sensitive to density than species of extraguild prey[J]. BioControl, 2020, 65(6): 713-725. DOI:10.1007/s10526-020-10036-9
doi: 10.1007/s10526-020-10036-9
35 杨国庆,吴进才,王洪全,等.水对稻田蜘蛛捕食功能的影响[J].生态学报,2003,23(4):681-687. DOI:10.3321/j.issn:1000-0933.2003.04.008
YANG G Q, WU J C, WANG H Q, et al. The effects of water on predacious function of paddy field spiders[J]. Acta Ecologica Sinica, 2003, 23(4): 681-687. (in Chinese with English abstract)
doi: 10.3321/j.issn:1000-0933.2003.04.008
36 RICKERS S, LANGEL R, SCHEU S. Stable isotope analyses document intraguild predation in wolf spiders (Araneae: Lycosidae) and underline beneficial effects of alternative prey and microhabitat structure on intraguild prey survival[J]. Oikos, 2006, 114(3): 471-478. DOI:10.1111/j.2006.0030-1299.14421.x
doi: 10.1111/j.2006.0030-1299.14421.x
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