姚凤銮^{1, 2,},
郑宇¹,
丁雪玲¹,
卢学松¹,
何玉仙^{1, 2,,},
翁启勇^{1, 2,,}
1.农业部福州作物有害生物科学观测实验站/福建省作物有害生物监测与治理重点实验室/福建省农业科学院植物保护研究所 福州 350013
2.闽台作物有害生物生态防控国家重点实验室/福建农林大学 福州 350002
基金项目: 福建省属公益类科研院所基本科研专项2017R1025-1
福建省科技重大专项2017NZ0003-1
福建省农业科学院创新团队项目STIT2017-1-8

详细信息

作者简介:姚凤銮, 主要研究方向为农业昆虫与害虫防治。E-mail:yaofengluan@126.com

通讯作者:何玉仙, 主要研究方向为农业昆虫与害虫防治, E-mail:yuxianhe_faas@sina.cn
翁启勇, 主要研究方向为植物保护, E-mail:wengqy@faas.cn

中图分类号:Q969

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出版历程

收稿日期:2018-12-11
录用日期:2019-02-15
刊出日期:2019-06-01

Overwintering population density and cold tolerance of Bemisia tabaci in greenhouses and open fields in the Fujian Province

YAO Fengluan^{1, 2,},
ZHENG Yu¹,
DING Xueling¹,
LU Xuesong¹,
HE Yuxian^{1, 2,,},
WENG Qiyong^{1, 2,,}
1. Fuzhou Scientific Observing and Experimental Station of Crop Pests of Ministry of Agriculture/Fujian Key Laboratory for Monitoring and Integrated Management of Crop Pests/Institute of Plant Protection, Fujian Academy of Agricultural Sciences, Fuzhou 350013, China
2. State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops/Fujian Agriculture and Forestry University, Fuzhou 350002, China
Funds: the Basic Special Fund for Scientific Research Organizations on Public Interest of Fujian Province, China2017R1025-1
the Special Fund for Key Program of Science and Technology of Fujian Province, China2017NZ0003-1
the Innovation Teams of Fujian Academy of Agricultural Sciences, ChinaSTIT2017-1-8

More Information

Corresponding author:HE Yuxian, E-mail: yuxianhe_faas@sina.cn;WENG Qiyong, E-mail: wengqy@faas.cn

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摘要
摘要:2017年1月9—12日和2月21—24日，在南平建瓯、三明将乐、三明三元、福州闽侯、龙岩新罗以及漳州龙海等6个地区，调查了大棚和露地烟粉虱越冬寄主及种群密度，以期明确福建省露地及设施蔬菜烟粉虱越冬规律，为烟粉虱的综合治理提供理论依据。共记录烟粉虱越冬寄主6科16种，主要包括栽培蔬菜花椰菜、番茄、茄子以及阔叶类杂草龙葵、小飞蓬、辣子草和胜红蓟。在露地花椰菜上，烟粉虱越冬虫口密度1月份显著高于2月份；花椰菜采后残株上的越冬虫口密度显著高于莲座期和花球形成期。在温室大棚中，休耕大棚中越冬虫口密度显著高于生产大棚。无论是蔬菜还是杂草，温室大棚中的越冬虫口密度显著高于露地。烟粉虱各虫态均可在各地温室大棚和漳州露地越冬，而在南平和三明等温度较低的地区以卵和伪蛹在露地越冬。在蔬菜上发现越冬烟粉虱有MEAM1隐种和MED隐种，温室大棚中两隐种数量分别为57只和111只，温室大棚可能有助于MED隐种定殖。室内耐寒性测定证实卵和高龄若虫比低龄若虫以及成虫更耐寒，烟粉虱在花椰菜、龙葵和辣子草上的世代存活率分别为83.7%、79.3%和81.6%，世代发育历期分别为18.9 d、16.7 d和18.8 d，龙葵和辣子草是烟粉虱适宜的越冬杂草寄主。综上，烟粉虱可在福建省露地越冬，温室大棚加重了烟粉虱的发生为害。
关键词:烟粉虱/
越冬寄主/
种群密度/
蔬菜/
耐寒性/
福建省
Abstract:In order to clarify the overwintering mechanisms of sweetpotato whitefly[Bemisia tabaci (Gennadius)] in open fields and greenhouse vegetable production systems in Fujian Province, China, and to provide a theoretical basis for integrated pest management of B. tabaci, field surveys were conducted at six sites (Jian'ou County of Nanping City; Jiangle County and Sanyuan District of Sanming City; Minhou County of Fuzhou City; Xinluo District of Longyan City; and Longhai County of Zhangzhou City) in January 9-12 and February 21-24, 2017. Sixteen B. tabaci host plants belonging to six families were found, which included the following vegetables:broccoli (Brassica oleracea var. botrytis L.), tomato (Lycopersicon esculentum Mill.), and eggplant (Solanum melongena L.), and broadleaved weeds:Solanum nigrum L., Conyza canadensis (L.) Cronq., Ranunculus sieboldii Miq., and Ageratum conyzoides L. For broccoli grown in open fields, significantly greater densities of overwintering B. tabaci were found in January than in February, and substantially greater densities of B. tabaci were detected on postharvest broccoli residuals than those on broccoli at the rosette and the head development stages. There were significantly higher densities of overwintering B. tabaci in fallow greenhouses than in productive greenhouses. Markedly greater densities of overwintering B. tabaci were found in greenhouses than in open fields, regardless of whether the host plants were vegetables or broadleaved weeds. All life stages for overwintering B. tabaci were found in greenhouses across the province and in open fields in Zhangzhou, but eggs and pseudopupa were found in open fields in the Nanping and Sanming areas, where the temperature was low. Overwintering B. tabaci cryptic species MEAM1 and MED were detected in vegetables; in all, there were 57 and 111 individuals, respectively, of the two cryptic species. We inferred that the usage of greenhouses may promote the establishment of the cryptic species MED in the Fujian Province. We then carried out laboratory experiments to test the cold tolerance of B. tabaci and to test the suitability of broadleaved weeds for the development of B. tabaci. We demonstrated that eggs and old nymphs of B. tabaci could tolerate cold stress better than adults and young nymph. B. tabaci had comparable generational survival rates on broadleaved weeds S. nigrum (79.3%) and R. sieboldii (81.1%), lower than that on B. oleracea var. botrytis (83.6%), a common crop widely grown in Fujian Province during winter. The generational developmental duration of B. tabaci was significantly shorter on S. nigrum (16.7 d) than on B. oleracea var. botrytis (18.9 d), which was similar to that on R. sieboldii (18.8 d), implying that broadleaved weeds serve as important potential alternatives to vegetable crops as host plants for B. tabaci in winter. In summary, B. tabaci can overwinter successfully in the open fields in Fujian Province, and the establishment of greenhouses promotes the development of overwintering B. tabaci.
Key words:Sweetpotato whitefly/
Overwintering host/
Population density/
Vegetable/
Cold tolerance/
Fujian Province

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图1各调查点2017年1—2月每日最高温和最低温
Figure1.Daily maximum and minimum temperatures of each sampling site in January and February of 2017


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表1福建省烟粉虱越冬寄主植物种类
Table1.Overwintering host plant species of Bemisia tabaci (Gennadius) in Fujian Province

寄主植物Host plant	植物类型Plant type	栽培方式Culture type
茄科Solanaceae
??辣椒Capsicum annuum L.	栽培蔬菜Vegetable	大棚Greenhouse
??茄子Solanum melongena L.	栽培蔬菜Vegetable	大棚Greenhouse
??番茄Lycopersicon esculentum Mill.	栽培蔬菜Vegetable	大棚、露地Greenhouse, open field
??龙葵Solanum nigrum L.	杂草Weed	大棚、露地Greenhouse, open field
十字花科Brassicaceae
??花椰菜Brassica oleracea L. var. botrytis L.	栽培蔬菜Vegetable	大棚、露地Greenhouse, open field
??结球甘蓝Brassica oleracea L. var. capitata L.	栽培蔬菜Vegetable	大棚、露地Greenhouse, open field
葫芦科Cucurbitaceae
??黄瓜Cucumis sativus L.	栽培蔬菜Vegetable	大棚Greenhouse
豆科Fabaceae
??豇豆Vigna unguiculata (L.) Walp	栽培蔬菜Vegetable	大棚Greenhouse
菊科Asteraceae
??辣子草Ranunculus sieboldii Miq.	杂草Weed	大棚、露地Greenhouse, open field
??胜红蓟Ageratum conyzoides L.	杂草Weed	大棚Greenhouse
??小飞蓬Conyza canadensis (L.) Cronq.	杂草Weed	大棚、露地Greenhouse, open field
??石胡荽Centipeda minima (L.)	杂草Weed	大棚Greenhouse
??鲤肠EcIipta prostrata L.	杂草Weed	大棚Greenhouse
??鱼眼草Dichrocephala auriculata (Thunb.) Druce	杂草Weed	大棚、露地Greenhouse, open field
??梁子菜Erechtites hieracifolia (L.)	杂草Weed	大棚、露地Greenhouse, open field
唇形花科Labiatae
??瘦风轮Clinopodium gracile (Benth.) Matsum	杂草Weed	大棚、露地Greenhouse, open field

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表2福建省不同地点露地花椰菜上烟粉虱越冬虫口密度
Table2.Density of overwintering Bemisia tabaci (Gennadius) on Brassica oleracea L. var. botrytis L. grown in open fields in different investigated sites in Fujian Province

地点(市, 县/区) Site (County/District, City)	月份 Month	生育期 Growth stage	样地量 Number of sample fields	虫口密度Number of B. tabaci per leaf
				卵Egg	若虫Larvae	成虫Adult
南平建瓯Jian’ou, Nanping	1	莲座期Rosette stage	3	0.98±0.09a	0.57±0.10a	0.13±0.02a
	2	花球形成期Head development stage	3	0.29±0.21b	0.22±0.12a	0.00±0.00b
三明将乐Jiangle, Sanming	1	莲座期Rosette stage	3	1.09±0.17a	0.61±0.17a	0.15±0.03a
	2	花球形成期Head development stage	3	0.04±0.04b	0.09±0.05b	0.00±0.00b
三明三元Sanyuan, Sanming	1	莲座期Rosette stage	3	0.69±0.04a	0.84±0.13a	0.12±0.04a
	2	花球形成期Head development stage	3	0.48±0.11a	0.31±0.16a	0.00±0.00b
福州闽侯Minhou, Fuzhou	1	莲座期Rosette stage	3	0.51±0.13a	0.36±0.14a	0.05±0.01a
	2	花球形成期Head development stage	3	0.49±0.11a	0.32±0.12a	0.06±0.02a
龙岩新罗Xinluo, Longyan	1	莲座期Rosette stage	3	0.42±0.08a	0.39±0.21a	0.05±0.01a
	2	花球形成期Head development stage	3	0.20±0.15a	0.16±0.08a	0.02±0.01a
漳州龙海Longhai, Zhangzhou	1	莲座期Rosette stage	4	2.33±0.15b	0.87±0.07b	0.13±0.02c
		花球形成期Head development stage	3	17.66±0.89a	13.78±1.65a	5.23±0.27a
	2	花球形成期Head development stage	4	3.39±1.16b	1.68±0.59b	0.38±0.11b
		采后残株期Postharvest phase	3	17.34±1.27a	10.90±1.77a	6.31±0.65a
表中数据为平均数±标准误。不同小写字母表示每个调查地点烟粉虱同一虫态虫口密度在不同生育期间差异显著。Data shown in the table are mean ± S.E. Different lowercase letters mean significant differences in B. tabaci density at the same insect life stage between different crop growth stages in the same site.

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表3福建省不同地点温室大棚中烟粉虱越冬虫口密度
Table3.Density of Bemisia tabaci (Gennadius) overwintering in greenhouses in different investigated sites in Fujian Province

地点(市, 县/区) Site (County/ District, City)	温室类型 Type of greenhouse	寄主 Host	生育期 Growth stage	样地量 Number of sample fields	虫口密度Number of B. tabaci per leaf
					卵Egg	若虫Larvae	成虫Adult
南平建瓯 Jian’ou, Nanping	生产大棚 Cultivated	茄子Solanum melongena L.	座果期 Fruit-setting stage	2	1.80±0.80a	1.88±0.25b	0.27±0.06a
	休耕大棚 Fallow	辣椒Capsicum annuum L.	采后残株期 Postharvest stage	2	0.00±0.00b	6.68±1.42a	0.00±0.00b
		龙葵Solanum nigrum L.	生长期Growing stage	3	49.10±38.89ab	18.11±13.12ab	5.53±4.57ab
		小飞蓬 Conyza canadensis (L.) Cronq.	生长期Growing stage	3	10.69±6.15ab	7.69±4.20ab	4.47±4.05ab
三明将乐 Jiangle, Sanming	生产大棚 Cultivated	花椰菜 Brassica oleracea L. var. botrytis L.	莲座期Rosette stage	3	0.59±0.11a	0.43±0.13b	0.08±0.02a
			花球形成期 Head development stage	4	3.43±1.22b	1.45±0.38a	0.29±0.12a
	休耕大棚 Fallow	黄瓜Cucumis sativus L.	采后残株期 Postharvest stage	3	48.63±7.36a	35.97±5.53a	5.88±1.10a
		龙葵Solanum nigrum L.	生长期Growing stage	3	45.74±2.51a	25.79±1.23a	4.54±0.76a
		辣子草 Ranunculus sieboldii Miq.	生长期Growing stage	2	13.08±2.02b	9.93±2.03b	1.96±0.50b
		小飞蓬 Conyza canadensis (L.) Cronq.	生长期Growing stage	3	61.84±30.55ab	27.30±10.87ab	6.13±3.68ab
龙岩新罗 Xinluo, Longyan	生产大棚 Cultivated	花椰菜 Brassica oleracea L. var. botrytis L.	花球形成期 Head development stage	3	1.20±0.20a	0.61±0.13a	0.12±0.02b
	休耕大棚 Fallow	豇豆 Vigna unguiculata (L.) Walp	采后残株期 Postharvest stage	2	0.00±0.00b	3.97±1.40a	0.00±0.00c
		龙葵Solanum nigrum L.	生长期Growing stage	3	67.57±50.20ab	20.91±16.53a	1.98±1.06abc
		胜红蓟 Ageratum conyzoides L.	生长期Growing stage	3	8.32±3.60a	2.93±1.35a	0.43±0.05a
表中数据为平均数±标准误。不同小写字母表示每个调查地点烟粉虱同一虫态虫口密度在不同寄主植物(生育期)间差异显著。Data shown in the table are mean ± S.E. Different lowercase letters mean significant differences in B. tabaci density at the same insect life stage among different plant growth stages at the same site.

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表4福建省不同地点温室大棚和露地花椰菜上烟粉虱越冬虫口密度
Table4.Density of Bemisia tabaci (Gennadius) overwintering on Brassica oleracea L. var. botrytis L. grown in greenhouses and open fields in different investigated sites in Fujian Province

地点(市, 县/区) Site (County/District, City)	栽培方式 Culture type	生育期 Growth stage	样地量 Number of sample fields	虫口密度Number of B. tabaci per leaf
				卵Egg	若虫Larvae	成虫Adult
三明将乐 Jiangle, Sanming	温室大棚 Greenhouse	花球形成期 Head development stage	4	3.43±1.22a	1.45±0.38a	0.29±0.12a
	露地* Open field*	花球形成期 Head development stage	3	0.04±0.04b	0.09±0.05b	0.00±0.00b
龙岩新罗 Xinluo, Longyan	温室大棚 Greenhouse	花球形成期 Head development stage	3	1.20±0.20a	0.61±0.13a	0.12±0.02a
	露地** Open field**	花球形成期 Head development stage	3	0.20±0.15b	0.16±0.08b	0.02±0.01b
表中数据为平均数±标准误。*表示大棚外侧露地; **表示周围无大棚。不同小写字母表示每个调查地点烟粉虱同一虫态虫口密度在不同栽培方式间差异显著。Data shown in the table are mean ± S.E. * represents open fields adjacent to greenhouse; ** represents there are no greenhouses around the open fields. Different lowercase letters mean significant differences in B. tabaci density at the same insect life stage between different culture types at the same site.

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表5福建省不同地点休耕温室大棚和露地杂草上烟粉虱越冬虫口密度
Table5.Density of Bemisia tabaci (Gennadius) overwintering on weeds grown in fallow greenhouses and open fields in different investigated sites in Fujian Province

地点(市, 县/区) Site (County/District, City)	栽培方式 Culture type	寄主 Host	样地量 Number of sample fields	虫口密度Number of B. tabaci per leaf
				卵Egg	若虫Larvae	成虫Adult
南平建瓯 Jian’ou, Nanping	温室大棚 Greenhouse	龙葵Solanum nigrum L.	3	49.10±38.89a	18.11±13.12a	5.53±4.57a
		小飞蓬 Conyza canadensis (L.) Cronq.	3	10.69±6.15a	7.69±4.20a	4.47±4.05a
	露地* Open field*	龙葵Solanum nigrum L.	3	0.00±0.00a	0.00±0.00a	0.00±0.00a
		小飞蓬 Conyza canadensis (L.) Cronq.	2	0.00±0.00a	0.00±0.00a	0.00±0.00a
三明将乐 Jiangle, Sanming	温室大棚 Greenhouse	龙葵Solanum nigrum L.	3	45.74±2.51a	25.79±1.23a	4.54±0.76a
		辣子草 Ranunculus sieboldii Miq.	2	13.08±2.02b	9.93±2.03b	1.96±0.50b
		小飞蓬 Conyza canadensis (L.) Cronq.	3	61.84±30.55ab	27.30±10.87ab	6.13±3.68ab
	露地* Open field*	龙葵Solanum nigrum L.	2	0.33±0.08d	0.00±0.00c	0.37±0.13c
		小飞蓬 Conyza canadensis (L.) Cronq.	2	0.75±0.08c	0.00± 0.00c	0.45±0.11c
	露地** Open field**	龙葵Solanum nigrum L.	2	0.21±0.04d	0.08±0.08c	0.00±0.00d
		小飞蓬 Conyza canadensis (L.) Cronq.	2	0.13±0.04d	0.14±0.08c	0.00±0.00d
	露地*** Open field***	龙葵Solanum nigrum L.	3	0.00±0.00e	0.00±0.00c	0.00±0.00d
		小飞蓬 Conyza canadensis (L.) Cronq.	3	0.00±0.00e	0.00±0.00c	0.00±0.00d
龙岩新罗 Xinluo, Longyan	温室大棚 Greenhouse	龙葵Solanum nigrum L.	3	67.57±50.20ab	20.91±16.53ab	1.98±1.06ab
		胜红蓟 Ageratum conyzoides L.	3	8.32±3.60a	2.93±1.35a	0.43±0.05a
	露地* Open field*	龙葵Solanum nigrum L.	2	0.00±0.00b	0.00±0.00b	0.00±0.00b
		小飞蓬 Conyza canadensis (L.) Cronq.	3	0.00±0.00b	0.00±0.00b	0.00±0.00b
表中数据为平均数±标准误。*表示大棚外侧露地; **表示距离大棚10~20 m; ***表示周围无大棚。不同小写字母表示每个调查地点烟粉虱同一虫态虫口密度在不同栽培方式(杂草)间差异显著。Data shown in the table are mean ± S.E. * represents open fields adjacent to greenhouse; ** represents open fields are 10-20 m away from the greenhouse; *** represents there are no greenhouses around the open fields. Different lowercase letters mean significant differences in B. tabaci density at the same insect life stage between different cultural types (host) at the same site.

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表6低温对烟粉虱各虫态存活的影响
Table6.Effect of low temperatures on the survival rate of Bemisia tabaci (Gennadius) at various life stages

温度 Temperature (℃)	虫态 Life stage	存活率Survival rate (%)
		6 h	24 h	48 h	96 h	144 h
0	卵Egg	90.9±1.8b	90.4±1.5c	89.4±1.9a	61.7±1.2a	4.7±0.8ab
	低龄若虫Young nymph	65.4±1.5c	65.8±1.6d	43.6±2.2c	16.8±0.6b	3.5±0.6b
	高龄若虫Old nymph	98.8±0.6a	97.3±0.8b	95.1±1.1a	54.5±2.1a	8.7±1.4a
	成虫Adult	100.0±0.0a	100.0±0.0a	82.2±0.8b	0.0±0.0c	0.0±0.0c
4	卵Egg	92.1±1.4b	91.0±2.0b	91.4±1.6b	89.8±0.9b	28.2±1.6b
	低龄若虫Young nymph	65.4±2.0c	65.6±1.3c	55.5±1.1c	24.1±1.9d	9.0±0.8d
	高龄若虫Old nymph	99.1±0.9a	98.9±0.6a	97.8±1.1a	96.9±0.9a	46.5±1.9a
	成虫Adult	100.0±0.0a	100.0±0.0a	90.4±1.0b	50.5±2.4c	9.7±1.0c
8	卵Egg	92.0±1.7b	92.9±2.3b	92.2±1.1b	92.2±1.0b	64.7±3.0a
	低龄若虫Young nymph	64.5±1.7c	64.8±1.9c	65.9±1.4c	28.1±1.9d	25.7±0.8d
	高龄若虫Old nymph	98.3±0.7a	97.8±1.1b	98.5±0.8a	97.7±0.2a	55.3±1.6b
	成虫Adult	100.0±0.0a	100.0±0.0a	90.9±1.3b	54.7±1.7c	39.6±2.4c
表中数据为平均数±标准误。不同字母表示在同一温度同一处理时间下, 不同虫态之间存活率差异显著。在25 ℃, 卵、低龄若虫、高龄若虫和成虫的存活率(%)分别为91.8±1.16, 64.5±1.55, 99.3±0.74和100.0±0.00。Data are mean ± S.E. Different lowercase letters mean significant differences in survival rate among different life stages under the same temperature treatment for the same treatment time. At 25 ℃, the survival rates (%) of egg, young nymph, old nymph and adult are 91.8±1.16, 64.5±1.55, 99.3±0.74 and 100.0±0.00, respectively.

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表7烟粉虱在不同越冬寄主上的生长发育
Table7.Development of Bemisia tabaci (Gennadius) on different overwintering plants

生长发育参数 Developmental parameter	越冬寄主Host
	花椰菜 Brassica oleracea L. var. botrytis L.	龙葵 Solanum nigrum L.	辣子草 Ranunculus sieboldii Miq.
世代存活率Generational survival rate (%)	83.6±6.28a	79.3±6.76a	81.1±5.07a
世代发育历期Generational developmental duration (d)	18.9±0.11a	16.7±0.17b	18.8±0.42a
表中数据为平均数±标准误。同行不同字母表示越冬寄主植物间生长发育参数差异显著。Data shown in the table are mean ± S.E. Different lowercase letters in the same row mean significant differences among overwintering plants.

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表8福建省不同地区冬季烟粉虱隐种发生情况
Table8.Number of cryptic species of Bemisia tabaci (Gennadius) overwintering in Fujian Province

地点(市, 县/区, 乡镇) Site (City, County/District, Town)	栽培方式 Culture type	寄主植物 Host	隐种数量 Cryptic species number
			MEAM1	MED
南平、建瓯、小松Nanping, Jian’ou, Xiaosong	温室大棚Greenhouse	辣椒Capsicum annuum L.	4	20
		小飞蓬Conyza canadensis (L.) Cronq.	2	22
三明、将乐、光明Sanming, Jiangle, Guangming	温室大棚Greenhouse	黄瓜Cucumis sativus L.	0	24
三明、三元、中村Sanming, Sanyuan, Zhongcun	温室大棚Greenhouse	花椰菜Brassica oleracea L. var. botrytis L.	23	1
福州、闽侯、南通Fuzhou, Minhou, Nantong	温室大棚Greenhouse	番茄Lycopersicon esculentum Mill.	23	1
龙岩、新罗、东肖Longyan, Xinluo, Dongxiao	温室大棚Greenhouse	豇豆Vigna unguiculata (Linn.) Walp	2	22
		龙葵Solanum nigrum L.	3	21
漳州、龙海、东园Zhangzhou, Longhai, Dongyuan	露地Open field	花椰菜Brassica oleracea L. var. botrytis L.	24	0
		番茄Lycopersicon esculentum Mill.	24	0

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