朱 敏,孟 玲,李保平

南京農(nóng)業(yè)大學(xué)植物保護(hù)學(xué)院, 農(nóng)作物生物災(zāi)害綜合治理教育部重點實驗室, 南京 210095

高CO2濃度和固氮菌對斜紋夜蛾幼蟲食物利用效率的影響

朱 敏,孟 玲,李保平*

南京農(nóng)業(yè)大學(xué)植物保護(hù)學(xué)院, 農(nóng)作物生物災(zāi)害綜合治理教育部重點實驗室, 南京 210095

“補償取食”假說認(rèn)為CO2濃度升高后植食性昆蟲會增大取食量以彌補植物組織中氮素營養(yǎng)的不足。但實證研究并非都支持該假說。用人工智能氣候箱設(shè)置CO2濃度(390μL/L 和 780μL/L)和固氮菌(有、無)等2因素4處理，種植菜豆飼喂剛蛻皮進(jìn)入4齡的斜紋夜蛾幼蟲，測定其取食和食物利用效率。協(xié)方差分析結(jié)果表明，CO2濃度與固氮菌互作對斜紋夜蛾幼蟲取食量具有顯著影響，在無固氮菌處理下，斜紋夜蛾幼蟲對高CO2濃度處理的菜豆取食量明顯高于當(dāng)前CO2濃度處理的；而在有固氮菌處理下，斜紋夜蛾幼蟲對高CO2濃度下菜豆的取食量又比當(dāng)前CO2濃度處理下的低。固氮菌對斜夜蛾4齡幼蟲最終體重沒有顯著影響，但高CO2濃度處理的4齡幼蟲終體重大于當(dāng)前CO2濃度處理的幼蟲。CO2濃度、固氮菌及其互作對斜紋夜蛾幼蟲的相對取食率(RCR)和相對生長率(RGR)具有顯著影響，在當(dāng)前CO2濃度處理下，斜紋夜蛾4齡幼蟲的RCR和RGR在有、無固氮菌處理之間沒有顯著差異；但在升高CO2濃度下，無固氮菌處理下的RCR和RGR顯著大于有固氮菌處理。CO2濃度及其與固氮菌互作顯著影響近似消化率(AD)，在無固氮菌處理下，CO2濃度升高使AD增大；但在有固氮菌、CO2濃度升高下，其AD略有降低。CO2濃度和固氮菌雙因素處理對消化食物轉(zhuǎn)化率(ECD)無顯著影響。研究結(jié)果支持“補償取食”假說。

CO2濃度升高; 固氮菌; 食物利用; 害蟲治理; 氣候變化生物學(xué)

到本世紀(jì)末大氣CO2濃度將會從當(dāng)前水平的380μL/L升到500—750 μL/L[1]，CO2濃度升高普遍促進(jìn)植物光合作用[2- 3]，降低葉片的氮含量和含水量，增加植物葉片的C/N[4- 6]。但植物對CO2濃度升高的響應(yīng)在不同類植物間存在差異，非豆科C3植物的氮平均下降15%[7]，而由于豆科植物固氮的總量在CO2濃度升高時會增加，豆科植物葉片的氮含量平均僅降低7%[8- 10]。在豆科作物和豆科牧草的試驗中，CO2濃度升高下光合作用產(chǎn)物的可利用性增強，CO2濃度升高能有效刺激N2固定作用的假說已被廣泛證實[11- 13]。CO2濃度升高下共生固氮菌固氮作用的相對增強能增加植物總氮量的結(jié)果在一系列研究中都有報道[14- 15]。如在自由大氣CO2升高(FACE)條件下，大豆(Glycinemax)和三葉草(Trifoliumrepens)固氮作用增強，葉片的氮含量并未明顯下降[11, 16- 17]。植物的氮含量能顯著影響昆蟲的取食行為[18- 21]。取食CO2濃度升高的葉片，植食昆蟲一般會產(chǎn)生補償性取食來彌補氮營養(yǎng)的不足，但同時會出現(xiàn)存活率下降和生長減緩的現(xiàn)象，即被稱為“營養(yǎng)補償假說”[22- 25]。由于CO2主要是通過改變植物的氮含量來作用于植食性昆蟲，因此取食豆科植物的昆蟲將會相對較少的受到CO2濃度升高帶來的不利影響[26]。盡管豆科植物在生態(tài)和農(nóng)業(yè)上均發(fā)揮著重要的作用，但僅有少量的研究涉及到CO2濃度升高對取食豆科昆蟲的影響[27]。例如，尺蠖(Semiothisacinerearia)取食CO2濃度升高下大豆的生長率沒有下降[6, 28]；擬尺蠖(TrichoplusianiHubner)取食CO2濃度升高下未施肥的利馬豆(Phaseoluslunatus)的生長率沒有下降[29]；但CO2濃度升高下百脈根三葉草(Lotuscorniculatus)對灰蝶(Coliasphilodice)幼蟲有利[30]；Karowe[4]研究表明，CO2濃度增加對豆科植物C/N比及C、N次生化合物變化的影響比非固氮C3植物小，取食高CO2濃度大豆葉片尺蠖的取食營養(yǎng)效應(yīng)及發(fā)育特征與正常CO2濃度下相比差異均不顯著。但迄今未見通過控制固氮菌來說明高CO2濃度下植物碳/氮比的變化對植食性昆蟲的影響，而這樣的試驗可避免由于用不同植物進(jìn)行比較而產(chǎn)生的背景條件不一致所造成的差異。

斜紋夜蛾(ProdenialituraFabricius)屬間歇性猖獗的多食性和暴食性害蟲，危害蔬菜以及糧食、經(jīng)濟(jì)作物等近100科300多種植物[31]。斜紋夜蛾危害損失率一般在10%—20%，嚴(yán)重的高達(dá)35%以上，導(dǎo)致大豆以及豆科主要蔬菜的產(chǎn)量下降，品質(zhì)變差，影響農(nóng)民收入的增加，制約了大豆等產(chǎn)業(yè)的發(fā)展[32- 33]。鑒于斜紋夜蛾的危害性及豆科植物及其植食者對CO2濃度升高響應(yīng)的研究對農(nóng)業(yè)和生態(tài)系統(tǒng)的重要性，本研究以斜紋夜蛾與寄主植物菜豆(Phaseolusvulgaris)為例，探討了CO2濃度升高對豆科植食者相互作用關(guān)系的影響。假設(shè)在無固氮菌條件下，取食高CO2濃度下菜豆葉片的斜紋夜蛾的取食營養(yǎng)效應(yīng)將會顯著低于當(dāng)前CO2濃度下；而在有固氮菌時，取食高CO2濃度下菜豆葉片的斜紋夜蛾取食營養(yǎng)效應(yīng)將不會與當(dāng)前CO2濃度下有顯著差異。

1 材料與方法

1.1 試驗材料

供試菜豆品種為‘江蔬81- 6號’，由江蘇省農(nóng)業(yè)科學(xué)研究院蔬菜研究所提供。菜豆野生型固氮菌(Rhizobiumetli)CFN42品系由南京農(nóng)業(yè)大學(xué)生命科學(xué)學(xué)院微生物實驗室提供。供試寄主斜紋夜蛾是2010年采自江蘇省南京市浦口區(qū)大豆田，在養(yǎng)蟲室(溫度(24 ± 1)℃、光照14∶10h、RH 為(60±10)%)中用人工飼料繁殖多代的蟲源。

1.2 培養(yǎng)液配方

Fahraeus無氮營養(yǎng)液[34](每升純水)：Na2HPO40.15g，KH2PO40.1g，MgSO4·7H2O 0.120 g，CaCl2·2H2O 0.1g，F(xiàn)ecitrate 0.005 g，pH 6.5；Gibson微量元素培養(yǎng)液[35](每L純水)：H2BO32．86 g，MnSO4·4H2O 2．03 g，ZnSO4·7H2O 0.22 g，CuSO4·5 H2O 0.08 g，Na2MoO4·2H2O 0.08g。試驗中在每升 Fahraeus無氮營養(yǎng)液中滴入1mL Gibson微量元素培養(yǎng)液。

1.3 處理方法

1.3.1 菜豆培育方法

將萌發(fā)2 d的菜豆種子用0.6%的NaClO溶液消毒1 min，然后浸泡在稀釋過的野生型固氮菌的菌懸液(濃度約1×107mL-1)中30 min(用作對照的種子用清水浸泡30 min)，處理后在無菌條件下種植于加入上述營養(yǎng)液1 L，培養(yǎng)基為蛭石，直徑為15cm的花盆中(花盆與蛭石已滅菌)，然后將花盆置于不同處理的人工智能氣候箱內(nèi)(武漢瑞華HP300GS型)。實驗條件為溫度(25±1)℃、相對濕度60%—80%、光周期為L∶D=14∶10 (L:8:30—22:30; D:22:30—8:30)。實驗設(shè)4個處理：無固氮菌+高CO2濃度(780μL/L)，固氮菌+高CO2濃度，無固氮菌+當(dāng)前CO2濃度(390μL/L)，固氮菌+當(dāng)前CO2濃度。每組各栽培20盆，每盆內(nèi)種5株。試驗期間各處理澆無菌水，且各處理每花盆每周澆1L的無菌營養(yǎng)液。

1.3.2 CO2濃度與固氮菌互作對斜紋夜蛾幼蟲營養(yǎng)效應(yīng)的影響

隨機選取在人工飼料下飼養(yǎng)長至3齡末期的斜紋夜蛾幼蟲共4組，每組50頭，饑餓處理12 h后選擇脫皮進(jìn)入四齡幼蟲各組35頭，稱量初始體重(預(yù)試驗表明斜紋夜蛾從4齡開始進(jìn)入暴食期)。將其中10頭烘干稱重，提供濕/干轉(zhuǎn)換系數(shù)，估計處理幼蟲的干重。每天稱取各處理環(huán)境下的新鮮菜豆(固氮菌從侵染根系到結(jié)瘤需要2周，因此菜豆葉片3周后摘用)葉片若干投喂供試幼蟲，且保證至少一半的葉片被取食，減少系統(tǒng)誤差。且取同一處理環(huán)境下的新鮮菜豆葉片若干作為空白對照用來提供濕/干轉(zhuǎn)換系數(shù)從而估計供試幼蟲每天取食的葉片干重。每天更換新鮮菜豆葉片，且將每天幼蟲取食后的剩余葉片、作為對照的葉片及幼蟲的糞便置于60℃的恒溫烘箱(森信公司，DGG- 9070A型)內(nèi)烘24 h后稱重(Mettler電子天平 AL204- 1C，萬分之一精度)。連續(xù)進(jìn)行3 d，最后1 d將試蟲烘干稱重記為終期體重(同上)。記錄脫皮情況，若有脫皮或死亡則去除該重復(fù)。

斜紋夜蛾幼蟲的營養(yǎng)效應(yīng)指標(biāo)采用4個營養(yǎng)利用指標(biāo)，相對生長率 (RGR) 、 相對取食率 (RCR) 、近似消化率(AD)和消化食物轉(zhuǎn)化率(ECD)[36]。

1.4 數(shù)據(jù)分析

經(jīng)典的基于比率食物利用效率指數(shù)存在諸多弊病，而協(xié)方差分析具有很多優(yōu)勢[37]。運用協(xié)方差分析，以試蟲初始體重為協(xié)變量，比較CO2濃度和固氮菌處理對斜紋夜蛾幼蟲體重及取食量的影響。為了與此前的相關(guān)研究進(jìn)行比較，仍運用經(jīng)典的基于比率的食物利用效率指數(shù)進(jìn)行分析，數(shù)據(jù)分析前先進(jìn)行適當(dāng)?shù)臄?shù)據(jù)轉(zhuǎn)換，以滿足方差分析的要求(正態(tài)分布和方差整齊)。其中對RGR進(jìn)行先平方根再反正弦轉(zhuǎn)換, 對RCR進(jìn)行自然對數(shù)轉(zhuǎn)換。用R統(tǒng)計分析軟件分析數(shù)據(jù)[38]。

2 結(jié)果與分析

2.1 CO2與固氮菌對斜紋夜蛾幼蟲取食量與體增重的影響

一般線性模型分析表明，CO2濃度與固氮菌對斜紋夜蛾幼蟲取食量均無顯著影響，但二者存在顯著互作影響(表1)。在無固氮菌處理下，高CO2濃度下斜紋夜蛾幼蟲的取食量要明顯高于當(dāng)前CO2濃度處理下的；而在有固氮菌處理下，高CO2濃度下斜紋夜蛾幼蟲取食量又比當(dāng)前CO2濃度處理下的低(圖1)。同時CO2濃度對斜夜蛾幼蟲終期體重影響顯著，但固氮菌沒有顯著影響(表1)，高CO2濃度下斜紋夜蛾幼蟲終期體重顯著大于當(dāng)前CO2濃度處理下的(圖2)。

2.2 CO2濃度和固氮菌對斜紋夜蛾幼蟲食物利用效率的影響

CO2濃度、固氮菌及其互作對斜紋夜蛾幼蟲的相對取食率(RCR)和相對生長率(RGR)具有顯著影響(表2)，在當(dāng)前CO2濃度下，斜紋夜蛾4齡幼蟲的RCR和RGR在有與無固氮菌處理之間沒有顯著差異；但在CO2濃度升高下，無固氮菌處理下的RCR和RGR顯著大于有固氮菌處理(圖3)。CO2濃度及其與固氮菌互作顯著影響近似消化率(AD) (表2)，在無固氮菌處理下，CO2濃度升高使AD增大；但在有固氮菌時，CO2濃度升高使AD略有下降(圖3)。CO2濃度和固氮菌對消化食物轉(zhuǎn)化率(ECD)沒有顯著影響(圖3)。

表1 擬合CO2濃度和固氮菌處理影響斜紋夜蛾葉片取食量和體增重的一般線性模型參數(shù)

Table 1 Parameters of the simple linear model fit to consumption and finial body weight as affected by CO2and NFB treatments inP.litura

觀測變量Observationvariable變量Variable系數(shù)Coefficient標(biāo)準(zhǔn)誤StandarderrortP取食量截距Intercept-0.010.03-0.400.69Consumption初體重Initialbodyweight2.854.390.650.52高CO2ElevatedCO2-0.0050.06-0.080.94固氮菌NFB0.080.071.100.28初體重×高CO2Initialbodyweight×ElevatedCO23.129.050.350.73初體重×固氮菌Initialbodyweight×NFB-1.009.34-1.070.29高CO2×固氮菌ElevatedCO2×NFB-0.020.01-2.410.02擬優(yōu)度GoodnessoffitR2=0.251,N=49,P=0.002終體重Finalbodyweight截距Intercept0.0020.0020.870.39初體重Initialbodyweight1.210.343.56<0.01高CO2ElevatedCO20.0010.00042.510.01固氮菌NFB0.00050.00041.180.24擬優(yōu)度GoodnessoffitR2=0.218,N=72,P<0.01

圖1 CO2濃度和固氮菌對斜紋夜蛾幼蟲取食率的影響 Fig.1 Effects of CO2 and NFB on consumption in the 4th instar larva of P. litura短柄代表平均值的標(biāo)準(zhǔn)誤 Bars are the standard error of the mean

圖2 CO2濃度和NFB對斜紋夜蛾4齡幼蟲體重的影響 Fig.2 Effects of CO2 and NFB on body weight in the 4th instar larva of P. litura虛線代表當(dāng)前CO2濃度處理 The dotted line is the ambient CO2 treatment； 實線代表升高CO2處理The solid line is the elevated CO2 treatment

3 討論

相對生長率(RGR)是衡量試驗因子對植食性昆蟲體重增加和發(fā)育時間的重要綜合評價指標(biāo)[26]，RGR越大，說明植食性昆蟲在短時間內(nèi)能將消化的食物轉(zhuǎn)化成自身營養(yǎng)的能力越強，生長發(fā)育越好。本研究結(jié)果表明CO2濃度與固氮菌均顯著互作于斜紋夜蛾的RGR。在無氮菌處理下，高CO2濃度處理下斜紋夜蛾幼蟲取食更多的葉片，對葉片的消化能力增強，即相對取食消耗率(RCR)、近似消化率(AD)顯著增高，雖然食物轉(zhuǎn)化率(ECD)差異不明顯，即取食高CO2濃度下更多葉片的幼蟲并沒有最大限度的將吸收的營養(yǎng)轉(zhuǎn)化為體重，但幼蟲的RGR更大，仍然可以得出以下結(jié)論：在無固氮菌條件下取食高CO2濃度下生長的菜豆葉片的幼蟲取食量增加，營養(yǎng)利用效率更高，高CO2濃度對斜紋夜蛾發(fā)生更有利。相反，在有固氮菌處理下，高CO2濃度對斜紋夜蛾的影響與當(dāng)前CO2濃度處理下對斜紋夜蛾的RGR影響并不顯著。高CO2濃度下斜紋夜蛾取食菜豆葉片的量下降，但對消化葉片的吸收也略高，幼蟲RGR下降的并不明顯，高CO2濃度處理并未顯著改變斜紋夜蛾的食物營養(yǎng)利用效率。

表2 CO2濃度和固氮菌互作對斜紋夜蛾食物利用效率影響的方差分析結(jié)果Table 2 ANOVA results for effects of different CO2 and NFB treatments on food utilization parameters of P.litura

① 經(jīng)反正玄平方根轉(zhuǎn)換 Data were arcsine square root transformation; ② 經(jīng)自然對數(shù)轉(zhuǎn)換 Data were natural log transformation

圖3 CO2濃度和NFB對斜紋夜蛾幼蟲食物利用效率的影響Fig.3 Effects of CO2 and NFB on food utilization efficiency of P. litura larvae

本試驗的結(jié)果與Karowe[26]的結(jié)果一致，即由于豆科植物可以利用固氮菌固氮的特征，在CO2濃度升高下，取食豆科植物的植食性昆蟲相比于取食非豆科植物的植食性昆蟲營養(yǎng)的改變要小得多。前人研究結(jié)果表明取食CO2濃度升高下美國山楊舞毒蛾(Lymantriadispar)幼蟲RGR降低63%，森林天幕毛蟲(MalacosomaneustriatestaceaMotsch)的RGR下降25%[23]；舞毒蛾(L.dispar)幼蟲取食CO2升高下無?；?Quercuspetraea)時，RGR降低30%[9]。取食山艾(Vacciniumuliginosum)的異黑蝗(Melanoplusdifferentialis)在CO2濃度升高下(650 μL/L)RGR降低40%[39]。而本試驗中有固氮菌處理下，高CO2濃度下斜紋夜蛾幼蟲的RGR僅僅下降13%，與當(dāng)前CO2濃度處理差異并不顯著，而在無固氮菌條件下， CO2濃度升高更有利斜紋夜蛾幼蟲的發(fā)生，這與先前許多研究CO2濃度升高對取食非豆科C3植物的植食者營養(yǎng)效率的結(jié)果不太一致[40]。究其原因可能是在無法固氮時，CO2濃度升高下菜豆植物的C/N比發(fā)生改變，特別是含氮的次生化合物如蛋白酶抑制劑的減少造成的。如Zavala[13]研究表明在CO2濃度升高(大豆FACE系統(tǒng))下日本金龜甲(Popilliajaponica)取食大豆葉片的量大大增加，原因是CO2濃度升高大豆蛋白酶抑制劑表達(dá)量的下降，更有利于甲蟲的取食，同時葉片糖分的增加也促進(jìn)甲蟲取食。當(dāng)然本試驗僅是推測，還需要后續(xù)驗證。

本試驗僅研究了高CO2濃度與固氮菌處理對斜紋夜蛾幼蟲單個齡期的影響，處理的時間比較短，而已有的CO2濃度升高對取食非豆科植物的鱗翅目昆蟲的影響大都研究了昆蟲的整個生活史特征，甚至是不同代數(shù)下的[41]，而且不同的昆蟲對不同的植物的取食生活史特征也可能會不同[26]。因此下一步可以研究CO2濃度升高對取食豆科植物的昆蟲多個世代的響應(yīng)或取食豆科植物與非豆科植物的同一植食昆蟲(或親緣關(guān)系比較近的昆蟲)對CO2濃度升高的的響應(yīng)。

致謝：南京農(nóng)業(yè)大學(xué)生命科學(xué)學(xué)院鐘曾濤和凌軍提供固氮菌菌株,植物保護(hù)學(xué)院程峰、盧笛、王以一等對試驗給予幫助，特此致謝。

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Effects of elevated CO2and nitrogen-fixing bacteria on food utilization efficiency inProdenialituraFabricius (Lepidoptera: Noctuidae)

ZHU Min, MENG Ling, LI Baoping*

DepartmentofEntomology,NanjingAgriculturalUniversity;AgriculturalPestsManagementLaboratoryofMinistryofEducation,Nanjing210095,China

The “compensatory feeding hypothesis” proposes that herbivorous insects may increase their plant consumption to compensate for the deficiency of Nitrogen in the plant tissue consumed under elevated CO2concentration. The empirical studies however are not overall in line with this prediction. In this study laboratory trails were conducted in growth chambers by manipulating CO2concentration (390μL/L, 780μL/L) and the nitrogen-fixing bacteria (NFB) (with, without) for the common beanPhaseolusvulgarisin a factorial design.Prodenialituralarvae at the 4thstadium were fed with the bean plants cultured in aforementioned treatments, and testedfor food consumption and utilization. ANCOVA results showed that CO2and NFB had significant effects both independently and in interaction on the 4thinstar larva in relative consumption (RCR) and relative growth rate (RGR). Under ambient CO2there were no differences in RCR and RGR between NFB treatments, but in elevated CO2RCR and RGR increased in the absence as opposed to the presence of NFB. CO2and its interaction with NFB had significant influence on approximate digestibility (AD), where AD increased in elevated CO2as opposed to ambient CO2in the absence of NFB but slightly reduced in the presence of NFB. CO2and NFB treatments did not influence efficiency of conversion of ingested food (ECI). The results of this study lend support for the prediction of the compensatory feeding hypothesis.

elevated CO2; nitrogen-fixing bacteria; food utilization; pest management; climate change biology

國家公益性行業(yè)(農(nóng)業(yè))科研專項(200903003, 201103032)

2013- 03- 25;

日期:2014- 03- 25

10.5846/stxb201303250507

*通訊作者Corresponding author.E-mail: lbp@njau.edu.cn

朱敏,孟玲,李保平.高CO2濃度和固氮菌對斜紋夜蛾幼蟲食物利用效率的影響.生態(tài)學(xué)報,2015,35(2):333- 339.

Zhu M, Meng L, Li B P.Effects of elevated CO2and nitrogen-fixing bacteria on food utilization efficiency inProdenialituraFabricius (Lepidoptera: Noctuidae).Acta Ecologica Sinica,2015,35(2):333- 339.