三種瓢蟲集團內捕食卵對初齡幼蟲生長發育的影響

郭佳妮,李保平,孟 玲

南京農業大學植物保護學院/農作物生物災害綜合治理教育部重點實驗室, 南京 210095

三種瓢蟲集團內捕食卵對初齡幼蟲生長發育的影響

郭佳妮,李保平,孟 玲*

南京農業大學植物保護學院/農作物生物災害綜合治理教育部重點實驗室, 南京 210095

種內和種間捕食卵現象常見于對食蚜瓢蟲的研究報道中。源自亞洲、入侵北美和歐洲的異色瓢蟲(Harmoniaaxyridis)由于卵含有生物堿而被認為可能是威脅本土瓢蟲生存的原因,但該推測只有在明確異色瓢蟲在原產地是否對本土瓢蟲具有類似負面影響后,才能確證。通過飼喂實驗,旨在明確異色瓢蟲在原產地是否對本土七星瓢蟲(Coccinellaseptempunctata)和龜紋瓢蟲(Propyleajaponica)具有食卵負面作用,為揭示異色瓢蟲入侵機理提供依據。實驗中用蚜蟲(對照)和3種瓢蟲卵對瓢蟲初孵1齡幼蟲進行飼喂處理,觀察幼蟲生長發育指標。對瓢蟲初齡幼蟲存活表現的分析結果表明：(1)龜紋瓢蟲初孵幼蟲取食同種卵和七星瓢蟲卵后存活至2齡的比率均高于取食異色瓢蟲卵的近7倍；(2)七星瓢蟲幼蟲取食異色瓢蟲卵未存活到2齡,但取食其他瓢蟲卵和蚜蟲后85%以上個體存活至2齡；(3)異色瓢蟲初孵幼蟲取食同種和其他2種瓢蟲卵后有90%以上存活至2齡。龜紋瓢蟲和七星瓢蟲1齡幼蟲取食異種卵比同種卵后的發育歷期顯著延長,但異色瓢蟲并未表現出差異。龜紋瓢蟲和異色瓢蟲1齡幼蟲取食同種和異種卵后的體增重相同,但七星瓢蟲取食龜紋瓢蟲卵后體增重比取食同種卵減小。研究結果說明,異色瓢蟲卵對七星瓢蟲和龜紋瓢蟲初孵幼蟲的生存具有負面影響,反之不然。所以,取食異色瓢蟲卵本身并非是導致北美和歐洲本土瓢蟲數量減少的原因。

營養生態學；捕食性瓢蟲；種間互作；集團內捕食；自殘

龜紋瓢蟲(Propyleajaponica)、七星瓢蟲(Coccinellaseptempunctata)和異色瓢蟲(Harmoniaaxyridis)是廣泛分布于我國的優勢捕食性天敵,常出現于同一生境。異色瓢蟲和七星瓢蟲作為多種蚜蟲和其它害蟲的天敵,被引入到美洲和歐洲等地用于生物防治[1]。在引入地,異色瓢蟲由于對同一生態位的本土捕食性瓢蟲種群構成威脅,而常被定性成為入侵種[2- 5]。但在原產地亞洲,異色瓢蟲雖常為優勢種[5- 7],但并未發現對本土其他瓢蟲生存構成威脅[8]。

瓢蟲作為卵生動物的一種,其卵經常會面臨強大的捕食壓力,因為它們包含了足夠的營養物質以完成胚胎發育[9]。應對捕食風險的一個基本策略是所產卵中含有毒化學物質(如：生物堿),通常有明顯的著色(警戒色)[9- 11]。瓢蟲卵色彩鮮艷且含生物堿,分別從視覺信號和化學防御兩方面阻止捕食者[12]。即便如此,自殘現象和集團內捕食仍存在于捕食性瓢蟲中[5,13- 14]。在瓢蟲的整個發育階段,卵期最容易被捕食,其次是幼蟲期,然后是成蟲期[15- 16]。有研究發現,瓢蟲長期攝食異種瓢蟲卵會對其存活率和繁殖力有不利的影響[17]；在入侵地,七星瓢蟲捕食異色瓢蟲卵后存活率很低,甚至死亡,但是異色瓢蟲捕食七星瓢蟲卵后的存活率不受影響[15,18-19]。Sato和Dixon[15]在英國的研究發現,二斑瓢蟲(Adaliabipunctata)捕食異色瓢蟲卵后也會全部死亡。因此,有猜測認為異色瓢蟲卵的生物堿毒性可能是導致當地本土瓢蟲數量降低的原因之一[20- 24]。但在不清楚異色瓢蟲在原產地與其他瓢蟲之間捕食卵后是否存在非對稱反應之前,尚無法證明該推測是否成立。迄今,異色瓢蟲在原產地是否也對本土瓢蟲具有食卵毒性,卻知之甚少。在我國,有關異色瓢蟲捕食其他瓢蟲卵的研究僅見1篇報道[25],發現異色瓢蟲取食同種和異種卵均可完成生長發育,與取食蚜蟲相比,1齡幼蟲發育歷期明顯縮短,存活率明顯提高。但該研究未觀察其他瓢蟲捕食異色瓢蟲卵后的反應。

對此,本研究以龜紋瓢蟲、七星瓢蟲和異色瓢蟲為材料,采用飼喂實驗觀察初孵幼蟲取食蚜蟲(對照)、同種和異種瓢蟲卵等處理后發育至2齡期的生存和發育指標,以探究以下問題：(1)異色瓢蟲卵對其他瓢蟲是否具有毒性作用？(2)其他瓢蟲卵對異色瓢蟲是否具有毒性作用？對該問題的回答將為探究異色瓢蟲的入侵性提供參考。

1 材料和方法

1.1 供試蟲源

龜紋瓢蟲、七星瓢蟲、異色瓢蟲成蟲和豌豆修尾蚜 (Megourajaponica) 于2014年3—5月采自南京市郊的蠶豆(Viciafaba)田中。在養蟲室內(25—28℃、16L∶8D)用盆栽蠶豆苗飼養豌豆修尾蚜,作為對照食物。用圓形食品塑料盒(直徑=15 cm,高=7.5 cm)飼養瓢蟲,每盒8—9頭,每天喂食充足的豌豆修尾蚜,提供一張折皺的牛皮紙(3 cm×5 cm)供其產卵,每天更換新的飼養盒以減少對卵的自相殘殺。當雌蟲產卵后,收集卵保存于冰箱內供試。

1.2 試驗方法

取孵化后4 h內的1齡幼蟲,以避免初孵幼蟲取食尚未孵化的卵或營養卵[26],因為1齡幼蟲對食物品質非常敏感,常作為測定昆蟲食物選擇性的理想蟲期[27]。首先,稱取每頭試蟲的鮮重(Mettler Toledo電子天平XS105DU,精確至0.00001 g),單獨飼養于玻璃試管(直徑=20 mm,高=30 mm)中,并在底部放一片濕潤的濾紙以保證管內濕度。設4種食物處理：2種其他種瓢蟲的卵、同種卵和蚜蟲(對照),足量提供卵和2—3齡若蚜。每2 h觀察1次,記錄死亡或發育到2齡的時間,發育到2齡后于2 h內稱體重；由于供試七星瓢蟲取食異色瓢蟲卵后無一存活至2齡,故試驗觀察到2齡為止。每處理重復30次以上。

1.3 數據分析

將瓢蟲種類作為一個因素與食物因素一起進行分析,通過檢驗兩個因素是否存在互作來推斷食物處理是否在3種瓢蟲間具有相同的影響。由于1齡幼蟲存活至2齡的觀測數據為二進制變量(是或否),符合二項分布型,故采用logistic回歸模型擬合1齡到2齡的存活率；當發現食物類型和瓢蟲種類因素之間有顯著互作時,單獨比較每種瓢蟲內不同食物處理間的差異[28]。用雙因素方差分析比較成功發育到2齡的幼蟲發育時間和體增重,當發現顯著互作后,用單因素方差分析每種瓢蟲內不同食物處理的差異,若有顯著差異,再用Tukey HSD 測驗進行多重比較。采樣Wilson置信域方法(95%)計算存活率的95%置信域,因為該方法在樣本量< 40的情況下可更準確地估計二進制數據的置信域[29]。數據分析使用R統計軟件[30]。

2 結果

2.1 攝食同種或異種卵對初齡幼蟲存活的影響

食物處理與瓢蟲種類互作顯著影響1齡幼蟲發育到2齡的存活率(logistic回歸模型,Wald似然比測驗；食物處理：χ2=125.36,P<0.001; 瓢蟲：χ2=38.87,P<0.001；互作:χ2=96.56,P<0.001)。對不同瓢蟲種下取食處理間的比較結果表明,龜紋瓢蟲1齡幼蟲取食同種卵的存活率是取食異色瓢蟲卵的6.97倍,與取食蚜蟲處理之間有顯著差異，與取食七星瓢蟲卵之間沒有顯著差異(圖1)。七星瓢蟲1齡幼蟲取食異色瓢蟲卵后均未存活到2齡,但取食其他食物后存活率均在85% 以上(圖1)。異色瓢蟲1齡幼蟲取食同種和其他種瓢蟲的卵后的存活率均在90%以上,之間沒有顯著差異,但均高于取食蚜蟲的存活率(圖1)?？傊?異色瓢蟲卵對另2種瓢蟲1齡幼蟲具有幾乎致死作用,反之不然。

圖1 食物處理對龜紋瓢蟲(A)、七星瓢蟲(B)和異色瓢蟲(C)1齡幼蟲存活至2齡比率的影響Fig.1 Survival of P. japonica (A), C. septempunctata (B) and H. axyridis (C) 1st instar larvae to the 2nd as affected by food treatments短柄代表95% Wilson置信域； 圖中從左至右食物處理的樣本量分別為：A圖， 39、31、33和36；B圖,38、38和35；C圖,35、35、35和48；圖柱上的不同小寫字母代表不同食物處理間差異顯著(P<0.05)

2.2 攝食同種或異種卵對初齡幼蟲發育歷期的影響

食物處理與瓢蟲種類互作顯著影響1齡幼蟲的歷期(雙因素方差分析；食物處理：F3, 433=2.57,P=0.05；瓢蟲種類：F2, 433=9.10,P<0.001；互作：F6, 433=23.76,P<0.001)。龜紋瓢蟲1齡幼蟲取食七星瓢蟲卵后發育至2齡的歷期顯著延長,比取食同種卵延長近1.6倍,比取食蚜蟲的歷期延長1.4倍,但與取食異色瓢蟲卵的歷期沒有顯著差異(圖2)。七星瓢蟲1齡幼蟲取食龜紋瓢蟲卵的發育歷期比取食同種卵的顯著延長近1.3倍,與取食蚜蟲的發育歷期相同；取食異色瓢蟲卵未完成1齡期生長(圖2)。異色瓢蟲1齡幼蟲取食同種卵的發育歷期與取食異種卵的相同,比取食蚜蟲的歷期顯著縮短近1/3(圖2)。總之,龜紋瓢蟲和七星瓢蟲1齡幼蟲取食異種卵比同種卵的發育歷期顯著延長,但異色瓢蟲并未表現出差異。

圖2 食物處理對龜紋瓢蟲(A)、七星瓢蟲(B)和異色瓢蟲(C)1齡幼蟲發育歷期的影響Fig.2 Developmental duration of P. japonica (A), C. septempunctata (B) and H. axyridis (C) 1st instar larvae as affected by food treatments

2.3 攝食同種或異種卵對初齡幼蟲體增重的影響

圖3 食物處理對龜紋瓢蟲(A)、七星瓢蟲(B)和異色瓢蟲(C)1齡幼蟲發育至2齡體增重的影響Fig.3 Body weight gain of P. japonica (A), C. septempunctata (B) and H. axyridis (C) 1st instar larvae developed to the 2nd as affected by food treatments

食物處理與瓢蟲種類因素之間互作顯著影響1齡幼蟲發育至2齡的體增重(雙因素方差分析；食物種類：F3, 319=17.10,P<0.001；瓢蟲種類：F2, 319=83.67,P<0.001；互作：F5, 319=9.51,P<0.001)。龜紋瓢蟲1齡幼蟲發育至2齡的體增重在食物處理間沒有顯著差異(F3, 88=1.88,P=0.14) (圖3)；七星瓢蟲1齡到2齡的體增重在不同食物處理間存在顯著差異(F2, 100=19.7,P<0.001),取食異色瓢蟲卵均未成功發育到2齡,取食同種卵的體增重與取食蚜蟲的相同,均大于取食龜紋瓢蟲卵的1.4倍 (圖3)。異色瓢蟲1齡到2齡的體增重在食物處理間存在顯著差異(F3, 129=14.07,P<0.001),異色瓢蟲取食同種和其他2種瓢蟲卵的體增重相同,但均小于取食蚜蟲的體增重(圖3)?？傊?龜紋瓢蟲和異色瓢蟲1齡幼蟲取食同種和異種卵后的體增重沒有差異,但七星瓢蟲取食龜紋瓢蟲卵后體增重比取食同種卵的減小。

3 討論

對龜紋瓢蟲、七星瓢蟲和異色瓢蟲1齡幼蟲取食同種或異種卵后的存活和生長表現進行的觀察表明,異色瓢蟲取食其他種瓢蟲卵后對存活沒有明顯負面影響,但七星瓢蟲和龜紋瓢蟲1齡幼蟲取食異色瓢蟲卵后的存活率大幅降低。該結果與在美國的研究類似,Sato和Dixon[15]在異色瓢蟲入侵地英國的研究表明,二斑瓢蟲和七星瓢蟲取食異色瓢蟲卵后全部死亡；Rieder等[18]的研究也表明,七星瓢蟲取食異色瓢蟲卵后,與取食同種卵相比死亡率更高、發育速度更慢、卵的攝食量和增重都有所減少,尤其是攝食來自日本的異色瓢蟲卵后不利影響最為嚴重；Kajita 等[19]的研究也獲得類似的結果：七星瓢蟲攝食異色瓢蟲卵后全部死亡,只是存活時間(<3 d)較短于本研究(平均3.7 d)。這些研究說明,無論在原產地還是入侵地,異色瓢蟲卵對其他瓢蟲均具有負面作用。

取食同種卵有利于瓢蟲1齡幼蟲的生長發育：3種瓢蟲取食同種卵后存活率在90%以上,龜紋瓢蟲和異色瓢蟲1齡幼蟲取食同種卵后的存活率甚至大于取食蚜蟲；七星瓢蟲和異色瓢蟲取食同種卵后,發育歷期顯著縮短。這與Sato和Dixon[15]在美國的研究結果類似,他們發現,異色瓢蟲、七星瓢蟲和二斑瓢蟲攝食同種卵后全部存活。杜迎剛等[25]在異色瓢蟲原產地的研究也表明,自然條件下高死亡率的異色瓢蟲1齡幼蟲取食同種卵后,存活率明顯提高、發育歷期明顯縮短。這些研究結果從一個側面解釋了捕食性瓢蟲產營養卵的適應意義。許多捕食性瓢蟲在一個卵塊中產幾粒胚胎不發育的卵即營養卵,供初孵幼蟲取食,對于后者生存具有至關重要的促進作用[31]。

當異色瓢蟲1齡幼蟲取食七星瓢蟲和龜紋瓢蟲卵后,雖然存活率很高(90%以上),但體增重卻減小。類似表現也出現于杜迎剛等[25]和Rieder 等[18]的研究。其原因可能是：其他瓢蟲卵也含有生物堿毒素,雖不能對異色瓢蟲1齡幼蟲的存活造成明顯負面影響,但對其生長發育仍有少許的不利影響。

異色瓢蟲與同域其他瓢蟲之間互為捕食卵后出現的非對稱反應,可以解釋它們在時間和空間分布上的分異。研究發現,在七星瓢蟲和異色瓢蟲出現于同一生境的情況下,七星瓢蟲離開越冬地的時間和產卵時間都早于異色瓢蟲,并且七星瓢蟲會遷移到其他地方以避開異色瓢蟲的捕食[5- 6]。在野外,七星瓢蟲幼蟲和異色瓢蟲卵之間的時間重疊要比異色瓢蟲幼蟲和七星瓢蟲卵之間的時間重疊更多[18]。今后,有必要在異色瓢蟲原產地開展研究,明確其他瓢蟲是否具有應對異色瓢蟲的產卵選擇對策。

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Effects of intra-guild egg predation on neonate larva development in three ladybird beetles (Coleoptera: Coccinellidae)

GUO Jiani, LI Baoping, MENG Ling*

CollegeofPlantProtection/KeyLaboratoryofManagementforPlantDiseasesandInsectPests,MinistryofAgriculture,NanjingAgriculturalUniversity,Nanjing210095,China

Intra- and inter-specific predation of eggs is well documented in aphidophagous ladybird beetles. Chemical defenses of eggs of Asia-originated invasiveHarmoniaaxyridisis the possible reason for population declines of native ladybirds in North America and Europe. However, this supposition cannot be confirmed without determining whetherH.axyridiseggs are toxic to native ladybirds in its original areas. To investigate mechanisms responsible forH.axyridisinvasion, we conducted a feeding experiment to examine neonate developmental performance of three sympatric ladybird beetles,Propyleajaponica,Coccinellaseptempunctata, andH.axyridis, which fed on aphids (control), conspecific or heterospecific eggs. The results indicated thatH.axyridiseggs were lethal or sub-lethal toP.japonicaandC.septempunctataneonate larvae, whereas the reverse was not the case. Survival from the 1stto the 2ndinstar stage inP.japonicawas almost seven-fold higher when feeding on conspecific andC.septempunctataeggs than onH.axyridiseggs.C.septempunctataneonates did not survive to the next instar when feeding onH.axyridiseggs, whereas over 85% survived when feeding on other types of food. In contrast, survival ofH.axyridisneonates to the next instar was over 90% when feeding on either conspecific or heterospecific eggs. AlthoughP.japonicaandC.septempunctataneonate developmental duration to the next instar was prolonged when feeding on heterospecific as opposed to conspecific eggs,H.axyridisneonates did not exhibit the difference between feeding heterospecific and conspecific eggs. BothP.japonicaandH.axyridisneonate larvae ended up with body weight gain at molting into the 2ndinstar as same when feeding on conspecific eggs as when feeding on heterospecific eggs, whereasC.septempunctataneonate larvae decreased body weight gain when feeding onP.japonicaeggs as compared to feeding on conspecific eggs. Our study results suggest thatH.axyridiseggs are toxic to bothC.septempunctataandP.japonicaneonate larvae, but the reverse is not true, thereby not confirming the supposition that chemical defense ofH.axyridiseggs is a potential factor for population declines of native ladybirds in North America and Europe.

nutrition ecology; predatory ladybirds; interspecific interaction; intraguild predation; cannibalism

國家公益性行業(農業)科研專項(201103002)

2015- 11- 13;

日期:2016- 08- 02

10.5846/stxb201511132306

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

郭佳妮,李保平,孟玲.三種瓢蟲集團內捕食卵對初齡幼蟲生長發育的影響.生態學報,2017,37(6):1826- 1831.

Guo J N, Li B P, Meng L.Effects of intra-guild egg predation on neonate larva development in three ladybird beetles (Coleoptera: Coccinellidae).Acta Ecologica Sinica,2017,37(6):1826- 1831.