森林生態(tài)系統(tǒng)中植食性昆蟲(chóng)與寄主的互作機(jī)制、假說(shuō)與證據(jù)

曾凡勇，孫志強(qiáng)

(1. 中國(guó)林業(yè)科學(xué)研究院 科技管理處，北京 100091； 2. 國(guó)家林業(yè)局泡桐研究開(kāi)發(fā)中心， 鄭州 450003；3. 中國(guó)林科院經(jīng)濟(jì)林研究開(kāi)發(fā)中心， 鄭州 450003)

森林生態(tài)系統(tǒng)中植食性昆蟲(chóng)與寄主的互作機(jī)制、假說(shuō)與證據(jù)

曾凡勇1，孫志強(qiáng)2,3,*

(1. 中國(guó)林業(yè)科學(xué)研究院 科技管理處，北京 100091； 2. 國(guó)家林業(yè)局泡桐研究開(kāi)發(fā)中心， 鄭州 450003；3. 中國(guó)林科院經(jīng)濟(jì)林研究開(kāi)發(fā)中心， 鄭州 450003)

圍繞“多樣性穩(wěn)定性”假說(shuō)、“聯(lián)合抗性假說(shuō)”、“生長(zhǎng)勢(shì)假說(shuō)”、“脅迫假說(shuō)”、以及下調(diào)、上調(diào)和推拉等機(jī)制與假說(shuō)提出的背景與實(shí)驗(yàn)驗(yàn)證的證據(jù)，力圖辨析其概念以及它們之間的相互關(guān)系。作者認(rèn)為，多樣性-穩(wěn)定性機(jī)制關(guān)注森林生態(tài)系統(tǒng)的功能，是基于群落甚至景觀層次。多樣性條件下的聯(lián)合抗性機(jī)制和聯(lián)合易感性應(yīng)屬于穩(wěn)定性中的抵抗力范疇。聯(lián)合抗性機(jī)制的主要基礎(chǔ)是基于資源集中假說(shuō)和天敵假說(shuō)，這些觀點(diǎn)在種群層次上更易理解；上調(diào)力和下調(diào)力機(jī)制是以食物網(wǎng)底部的資源與頂端的天敵來(lái)探討這種互作關(guān)系。因此，資源集中與上調(diào)力有著對(duì)應(yīng)關(guān)系，而天敵假說(shuō)只是下調(diào)力機(jī)制中的一個(gè)層面而已。植物生長(zhǎng)勢(shì)假說(shuō)和植物脅迫假說(shuō)力圖從植物個(gè)體或種的群體的生長(zhǎng)狀態(tài)出發(fā)解析植食性動(dòng)物的對(duì)寄主的選擇趨勢(shì)。上述有關(guān)植食性昆蟲(chóng)與寄主互作的機(jī)制、假說(shuō)與證據(jù)是基于不同的層面提出的，因而在解析研究目標(biāo)時(shí)，由于基本面的差異有可能會(huì)得出不同的結(jié)論。以近年來(lái)的研究進(jìn)展和研究成果為依據(jù)有針對(duì)性地闡述這些理論對(duì)森林有害生物生態(tài)調(diào)控技術(shù)的指導(dǎo)作用，其中，聯(lián)合抗性和聯(lián)合易感性理論對(duì)指導(dǎo)森林有害生物生態(tài)控制具有更直接的指導(dǎo)作用。進(jìn)一步提出了相應(yīng)的亟待解決的科學(xué)問(wèn)題。

植食性昆蟲(chóng)；寄主；互作機(jī)制；多樣性穩(wěn)定性假說(shuō)；聯(lián)合抗性假說(shuō)

森林生態(tài)系統(tǒng)中主要的互作關(guān)系之一是植食性昆蟲(chóng)與其寄主間的關(guān)系，這種互作關(guān)系一直是森林生態(tài)系統(tǒng)及其功能研究的核心問(wèn)題[1- 3]，也是實(shí)施森林有害生物可持續(xù)控制的重要理論基礎(chǔ)[4- 5]。針對(duì)這種互作關(guān)系，人們從不同的層面和視角提出了許多機(jī)制和假說(shuō)，如以生物多樣性理論為基礎(chǔ)提出的“多樣性穩(wěn)定性”假說(shuō)[6- 7]、圍繞森林物種組成與結(jié)構(gòu)提出的“聯(lián)合抗性假說(shuō)”[8- 9]；以樹(shù)木個(gè)體和群體為對(duì)象提出的“生長(zhǎng)勢(shì)假說(shuō)”[10]、“脅迫假說(shuō)”[11]；以及以食物鏈為主導(dǎo)的下調(diào)、上調(diào)和推拉等相互制約機(jī)制[12- 16]。事實(shí)上, 這些理論和假說(shuō)為解釋森林生態(tài)系統(tǒng)自調(diào)控病蟲(chóng)災(zāi)害的機(jī)制提供了理論依據(jù)。

如何認(rèn)識(shí)上述這些假說(shuō)和機(jī)制，以及如何運(yùn)用這些理論指導(dǎo)森林管理實(shí)踐是森林生態(tài)學(xué)家和森林保護(hù)工作者的重要任務(wù)之一。本文針對(duì)人們提出的植食性昆蟲(chóng)與寄主間的互作關(guān)系的主要機(jī)制和假說(shuō)，試圖辨析其概念以及它們之間的相互關(guān)系，以近年來(lái)的研究進(jìn)展和研究成果為證據(jù)辯證地剖析這些機(jī)制和假說(shuō)對(duì)于森林有害生物生態(tài)調(diào)控的指導(dǎo)作用，并提出相應(yīng)的亟待解決的科學(xué)問(wèn)題。

1 多樣性-穩(wěn)定性機(jī)制的提出與驗(yàn)證

1.1 多樣性-穩(wěn)定性機(jī)制的提出

Elton[17]和Pimentel[18]首次描繪了在簡(jiǎn)單的生態(tài)系統(tǒng)(如人工純林)中，病蟲(chóng)害的發(fā)生比在復(fù)雜生態(tài)系統(tǒng)中嚴(yán)重。隨后有許多觀察數(shù)據(jù)(而非實(shí)驗(yàn)數(shù)據(jù))支持了森林生態(tài)系統(tǒng)的生物多樣性是抑制和降低病蟲(chóng)害暴發(fā)的重要因素[18]。多樣性-穩(wěn)定性機(jī)制認(rèn)為一個(gè)群體內(nèi)物種多樣性越豐富，其穩(wěn)定性越高，亦即害蟲(chóng)及其天敵種群數(shù)量在時(shí)間序列上表現(xiàn)較低的波動(dòng)幅度，從而避免了植食性昆蟲(chóng)種群數(shù)量的大規(guī)模暴發(fā)[7, 19]。最近通過(guò)數(shù)學(xué)方法證明，生物多樣性和害蟲(chóng)間的相互作用能夠影響系統(tǒng)穩(wěn)定性[20]。因此，森林的生物多樣性(如天然林)能夠自調(diào)控病蟲(chóng)害暴發(fā)和降低病蟲(chóng)害的為害損失成為森林可持續(xù)經(jīng)營(yíng)的一個(gè)經(jīng)典論據(jù)[21- 24]。

1.2 多樣性-穩(wěn)定性機(jī)制的驗(yàn)證

在農(nóng)業(yè)和草地系統(tǒng)[25]中均觀察到隨著植物多樣性增加，植食性為害減少，在森林生態(tài)系統(tǒng)中也有同樣的發(fā)現(xiàn)[26- 27]。但有些作者觀察到植物多樣性的相反[28]或根本沒(méi)有影響的結(jié)果[29]，并指出植食性動(dòng)物對(duì)植物具體種類的強(qiáng)烈的依賴性、而非植物多樣性的調(diào)控作用[27, 30]。環(huán)境中存在植食性動(dòng)物的寄主?；?，對(duì)植食性-植物多樣性關(guān)系產(chǎn)生影響[24- 25]。其他節(jié)肢動(dòng)物的研究顯示，多樣性-植食性關(guān)系是由群落水平的植物多樣性調(diào)控[31]。

Vehvil?inen[30]對(duì)芬蘭6個(gè)寒帶針葉林樣地和1個(gè)溫帶針葉林樣地開(kāi)展了長(zhǎng)期監(jiān)測(cè)。監(jiān)測(cè)的林分類型包括天然林、混交林及人工純林，監(jiān)測(cè)的主要內(nèi)容是不同生物多樣性條件下昆蟲(chóng)的發(fā)生情況，同時(shí)比較不同樹(shù)齡、采樣季節(jié)、以及不同試驗(yàn)設(shè)計(jì)(樣地大小、密度)條件下昆蟲(chóng)種類、昆蟲(chóng)取食方式的差異及其對(duì)系統(tǒng)穩(wěn)定性的影響。結(jié)果顯示昆蟲(chóng)在取食方式和寄主的選擇方面變化顯著。取食方式上，不考慮寄主種類時(shí)，混交林和人工純林中只有潛葉蛾(Phyllocnistisspp.)種群數(shù)量保持低密度且在時(shí)間序列上變化不大。但潛葉蛾在純林中表現(xiàn)出更強(qiáng)的年度波動(dòng)，驗(yàn)證了多樣性-穩(wěn)定性假說(shuō)，即多樣性豐富系統(tǒng)內(nèi)的波動(dòng)比簡(jiǎn)單系統(tǒng)小[32]。樺樹(shù)(Betulaplatyphylla)混交林內(nèi)的昆蟲(chóng)種群密度比純林中的明顯偏低，而櫟樹(shù)(Quercusaliena)和赤揚(yáng)(Alnusglutinosa)混交林內(nèi)的植食性昆蟲(chóng)數(shù)量比單一品種林(如櫟樹(shù)純林)內(nèi)更豐富。

Jactel和Brockerhoff[27]的結(jié)果表明，樹(shù)種多樣性的增加能有效減少林間昆蟲(chóng)數(shù)量。在由不同樹(shù)種所組成的群落中，寡食性昆蟲(chóng)的數(shù)量明顯較少，而雜食性昆蟲(chóng)數(shù)量存在一定的變化。他們認(rèn)為天然林樹(shù)種的組成比寄主樹(shù)種豐富度更為重要。這個(gè)研究得出了一些重要結(jié)論，如(1)樹(shù)種多樣性抑制害蟲(chóng)爆發(fā)的積極效果隨著相關(guān)樹(shù)木種類比例增加而增加；(2)系統(tǒng)發(fā)生越遠(yuǎn)的樹(shù)種組合越能表現(xiàn)對(duì)食葉害蟲(chóng)的抑制和調(diào)控的能力，如種子植物與裸子植物的混交；(3)系統(tǒng)發(fā)生相近的樹(shù)種混交增加了雜食性害蟲(chóng)為害的可能。在天然林中，特定樹(shù)種上寡食性昆蟲(chóng)數(shù)量的減少會(huì)導(dǎo)致相應(yīng)的雜食性昆蟲(chóng)總體數(shù)量的增加[33]。因此，在一個(gè)特定的森林生態(tài)系統(tǒng)中，生產(chǎn)者的物種多樣性可以減少消費(fèi)者對(duì)生產(chǎn)者的依賴。

與之相反，有些研究卻認(rèn)為隨著植物種類多樣性增加、植食性昆蟲(chóng)種類和數(shù)量隨之增加并增加了為害水平[29, 34- 36]。在中國(guó)亞熱帶森林開(kāi)展的一項(xiàng)植食性昆蟲(chóng)與植物多樣性關(guān)系的研究，分析了來(lái)自27個(gè)森林林分類型中的植食性昆蟲(chóng)的為害水平，目的是驗(yàn)證是否植物豐富度顯著影響昆蟲(chóng)的種類與為害水平[36]。作者認(rèn)為，作為植食性動(dòng)物-植物多樣性的正面關(guān)系是與資源集中假說(shuō)相聯(lián)系的，該假說(shuō)認(rèn)為隨著植物種類多樣性的增加使得寄主植物資源減少，從而導(dǎo)致寡食性動(dòng)物為害水平的降低。該文證明在多樣性豐富的亞熱帶森林系統(tǒng)，資源集中似乎不是總體植食性為害的主要決定因素。與傳統(tǒng)的結(jié)論相比，雜食性昆蟲(chóng)對(duì)系統(tǒng)的影響更強(qiáng)，因?yàn)檫@些種類在高度多樣性的植物群落中有著廣泛的食物來(lái)源[36]。在亞熱帶森林中植物多樣性與植食性動(dòng)物的種類和為害間有著整體的正相關(guān)性。這與多數(shù)無(wú)論是森林系統(tǒng)還是草地系統(tǒng)的研究的結(jié)論相反，那些研究通常認(rèn)為隨著多樣性增加植食性昆蟲(chóng)為害減少[25, 27, 37- 39]。

因此，研究者普遍認(rèn)為特定環(huán)境中存在的植物種類以及植食性動(dòng)物的寄主?；?，對(duì)植食性-植物多樣性關(guān)系產(chǎn)生影響[24- 25]。同時(shí)，樹(shù)種多樣性對(duì)昆蟲(chóng)數(shù)量及其為害的影響在人工林、混交林和天然林中普遍依賴于昆蟲(chóng)取食方式和樹(shù)種。但目前在群落水平上開(kāi)展有關(guān)植物多樣性調(diào)控害蟲(chóng)發(fā)生與為害的研究還很少見(jiàn)。

2 聯(lián)合抗性假說(shuō)(Associational resistance hypothesis)和聯(lián)合易感性假說(shuō)(Associational susceptibility hypothesis)的提出與驗(yàn)證

2.1 聯(lián)合抗性假說(shuō)的提出

Tahvanainen等提出，在特定森林生態(tài)系統(tǒng)中除寄主樹(shù)木本身的抗性外，寄主樹(shù)木與臨近的其它物種整體上會(huì)表現(xiàn)出對(duì)植食性動(dòng)物的“聯(lián)合抗性”。因此，聯(lián)合抗性常用來(lái)描述多樣性豐富的植物群落中低水平的害蟲(chóng)為害[8, 40- 41]。支持聯(lián)合抗性的主要假說(shuō)包括天敵假說(shuō)和資源集中假說(shuō)[9]。

天敵假說(shuō)認(rèn)為天然林內(nèi)豐富的、多樣性的或有效的天敵群體控制植食性昆蟲(chóng)種群密度從而抑制其暴發(fā)；而資源集中假說(shuō)試圖預(yù)測(cè)植食性昆蟲(chóng)搜尋、發(fā)現(xiàn)和定居在寄主豐富的斑塊的能力和趨向性，正如Root所強(qiáng)調(diào)的，“植食性昆蟲(chóng)更易發(fā)現(xiàn)并停留在寄主集中或近似于純林林分中”[9]。大量的有關(guān)資源集中假說(shuō)的研究來(lái)自于農(nóng)業(yè)害蟲(chóng)，如對(duì)比在單一品種和低多樣性水平的混交時(shí)害蟲(chóng)的群體行為[37, 42]。許多林分或小樣地水平的研究支持該假說(shuō)[9, 43- 45]，Bach進(jìn)一步在種群水平上發(fā)現(xiàn)昆蟲(chóng)多度的增加降低了集中種植的單一品種寄主的生長(zhǎng)[46]。Long等在群落水平上對(duì)該假說(shuō)展開(kāi)了深入研究，發(fā)現(xiàn)寡食性甲蟲(chóng)(Trirhabdavirgata)降低了廢棄耕地上其?；闹髑秣梓?Solidagoaltissima)的生物量，并進(jìn)而導(dǎo)致植物豐富度增加。該地區(qū)整體生物量的降低全部歸功于由甲蟲(chóng)為害而造成的寄主生物量的降低，而這種植物是當(dāng)?shù)刂参锶郝涞膬?yōu)勢(shì)種。他們的結(jié)果證實(shí)，當(dāng)優(yōu)勢(shì)種密度增加，斑塊中高密度寄主吸引了更多的甲蟲(chóng)[47]。

在另一項(xiàng)研究中，Knops等[48]觀察到在不同多樣性梯度水平下，寡食性昆蟲(chóng)種群對(duì)寄主植物資源集中度有兩種截然不同的響應(yīng)，而樣地中植物豐富度對(duì)這種響應(yīng)的影響較小。一方面，當(dāng)寄主植物多度更高時(shí)，昆蟲(chóng)寄生的也高；另一方面，隨著寄主植物密度增加，昆蟲(chóng)數(shù)量隨之減少，Otway等將這種情況稱之為資源稀釋假說(shuō)[35]。因此，該研究?jī)H部分地支持資源集中假說(shuō)。同樣的，Knops 等[48]，Koricheva等[49]和Haddad等[50]等的研究證實(shí)，至少對(duì)某些寡食性昆蟲(chóng)來(lái)說(shuō)，其種群發(fā)生符合資源集中假說(shuō)。但另一些研究同樣展現(xiàn)了資源稀釋發(fā)生的證據(jù)[42, 51- 52]。

2.2 聯(lián)合易感性假說(shuō)的提出

White和Whitham指出，當(dāng)系統(tǒng)中主要害蟲(chóng)是雜食性昆蟲(chóng)，而首要寄主與次級(jí)寄主混交時(shí)，首要寄主會(huì)因資源的快速減少，導(dǎo)致害蟲(chóng)“溢出”到次級(jí)寄主上，使得這類天然林或混交林受雜食性昆蟲(chóng)為害比純林內(nèi)更為嚴(yán)重，這種現(xiàn)象被稱為群體“聯(lián)合易感性”[53- 54]?！奥?lián)合易感性”普遍存在于森林中次級(jí)寄主上，尤其是當(dāng)昆蟲(chóng)是雜食性且其食物來(lái)源具有等級(jí)性時(shí)(如同是闊葉樹(shù)或同是針葉樹(shù))，會(huì)導(dǎo)致昆蟲(chóng)種群呈現(xiàn)周期性的高密度的暴發(fā)[53, 55]

2.3 聯(lián)合抗性假說(shuō)和聯(lián)合易感性假說(shuō)的驗(yàn)證

Barbosa等提出[56],聯(lián)合抗性和聯(lián)合易感性的形成有非生物和生物機(jī)制兩方面。非生物促進(jìn)機(jī)制包括土壤條件、小氣候影響等。土壤條件能影響關(guān)鍵植物周圍的其他植物，并進(jìn)一步改變了關(guān)鍵植物生長(zhǎng)與抗性所需的土壤營(yíng)養(yǎng)，如理論上，固氮植物近旁的其他植物最終會(huì)通過(guò)固氮植物組織的死亡和分解獲得較豐富的氮源[57]，類似的土壤變化可以通過(guò)植食性動(dòng)物的取食，糞便的分解導(dǎo)致土壤營(yíng)養(yǎng)成分的變化并促進(jìn)關(guān)鍵植物近旁的植物生長(zhǎng)或改變他們的抵抗力[58]。經(jīng)由鄰近植物的存在而形成的小氣候會(huì)影響植食性動(dòng)物的習(xí)性及其天敵。盡管鮮有研究揭示這些機(jī)制是否會(huì)導(dǎo)致聯(lián)合抗性或聯(lián)合易感性的形成，但小氣候(如光強(qiáng)度、溫度、濕度)的變化通過(guò)改變昆蟲(chóng)的產(chǎn)卵和壽命的確影響了其聚集及其對(duì)關(guān)鍵植物的取食；同時(shí)小氣候通過(guò)影響天敵的搜尋、交配等行為，間接地影響植食性昆蟲(chóng)的數(shù)量和為害程度。以上的一條或全部的原因有可能決定了聯(lián)合抗性/易感性形成的可能。

生物因素促進(jìn)聯(lián)合抗性/易感性形成是機(jī)制包括：

(1)相鄰植物的特性直接改變?nèi)∈酬P(guān)鍵植物昆蟲(chóng)的習(xí)性、存活及其天敵

目前，關(guān)于聯(lián)合抗性或聯(lián)合易感性的形成機(jī)制的研究還多停留在個(gè)體和種群水平上。如從植物的物理特征如色澤，各個(gè)器官的結(jié)構(gòu)特點(diǎn)來(lái)判斷促進(jìn)或阻礙聯(lián)合抗性機(jī)制或聯(lián)合易感性的形成。在群落內(nèi),鄰近植物可能通過(guò)簡(jiǎn)單的視覺(jué)阻隔效果或通過(guò)阻礙植食性動(dòng)物的移動(dòng)方向來(lái)降低關(guān)鍵植物被侵害的可能性[59- 60]。但鄰居植物也可能作為吸引者而使植食性動(dòng)物匯集在這些植物體上[8]，進(jìn)而減少了在關(guān)鍵植物的聚集和為害，即“推-拉”理論[61]。在人工管理的棲息地，采用這種推拉理論在農(nóng)作物的害蟲(chóng)防治上取得了一定的效果[61- 62]。但也有例外，即由于鄰居植物的吸引效果而使害蟲(chóng)“溢出”到關(guān)鍵植物上導(dǎo)致“聯(lián)合易感性”的發(fā)生[53, 63]。另外，鄰居植物對(duì)關(guān)鍵植物的影響很可能由化學(xué)信號(hào)和視覺(jué)效應(yīng)調(diào)控。鄰居植物上的取食者能產(chǎn)生揮發(fā)物從而影響鄰近的關(guān)鍵植物抵抗和(或)受害的可能性。如鄰近植物為天敵提供食物(如花粉，蜜等)，直接促進(jìn)天敵的聚集并進(jìn)而間接地降低了取食者的密度，由此引發(fā)“聯(lián)合抗性”發(fā)生[64]。反之，當(dāng)鄰近植物為關(guān)鍵植物提供互為補(bǔ)充的食物資源時(shí)，“聯(lián)合易感性”隨之發(fā)生。

聯(lián)合作用廣泛地存在于植物對(duì)植食性動(dòng)物的相互作用關(guān)系中。但植食性動(dòng)物間的相互作用有可能因被捕食者、病原或寄生天敵影響從而導(dǎo)致聯(lián)合抗性/易感性的發(fā)生[65]。特定植食性動(dòng)物引起的聯(lián)合抗性/易感性的潛力與另一個(gè)概念有所區(qū)別，即天敵的不同響應(yīng)機(jī)制能夠調(diào)控(或成為作用機(jī)制導(dǎo)致)植物間聯(lián)合抗性/易感性的發(fā)生[66]。Stenberg等發(fā)現(xiàn)植食性動(dòng)物之間同樣存在聯(lián)合易感性的[67]。多年生草本植物繡線菊(Filipendulaulmaria)和紫珍珠菜(Lythrumsalicaria)影響著昆蟲(chóng)為害水平，因?yàn)槟こ崮考纳鞌骋T托小蜂(Asecodesmento)同時(shí)寄生2種植物上各自專性甲蟲(chóng)。在繡線菊上的林奈球蟲(chóng)葉甲(Galerucellatenella)和紫珍珠菜上的紫珍珠菜甲蟲(chóng)(G.calmariensis)。林奈球蟲(chóng)葉甲的寄生率與繡線菊葉面積損失率呈負(fù)相關(guān)。混交的繡線菊和紫珍珠菜中共享的寄生天敵椰門托小蜂密度更高，因?yàn)槔C線菊的花吸引的椰門托小蜂的量是紫珍珠菜的2倍。

Barbosa 和Caldas的研究結(jié)果盡管是間接證據(jù)，但仍表明聯(lián)合易感性在協(xié)同發(fā)生的植食性動(dòng)物間普遍發(fā)生[68]。有著相同特征的鱗翅目昆蟲(chóng)幼蟲(chóng)被同一類寄生天敵寄生的機(jī)會(huì)更多，顯示了聯(lián)合易感性的潛力。Shiojiri等[69]和Heimpel等[70]在相關(guān)研究中，強(qiáng)調(diào)了聯(lián)合抗性/聯(lián)合易感性的形成機(jī)制，雖然他們的研究并未直接針對(duì)聯(lián)合抗性或聯(lián)合易感性。他們指出，形成聯(lián)合抗性/聯(lián)合易感性的潛在影響機(jī)制，包括寄生性天敵在不同寄主上的聚集、這些寄生天敵卵的成活率，以及從一種或二種昆蟲(chóng)所取食寄主植物分泌物的差異如何影響寄生天敵對(duì)其寄主的搜尋。

(2)關(guān)鍵植物及其鄰居植物的相對(duì)豐富度的差異直接或間接影響植食性動(dòng)物的聚集[56]

通過(guò)一項(xiàng)連續(xù)2a對(duì)歐洲赤松(Pinussylvestris)純林和與50%樺樹(shù)(Betulapendula)混交林松樹(shù)上的歐洲松葉蜂(Neodiprionsertifer(Hymenoptera,Diprionidae))數(shù)量、幼蟲(chóng)和卵的存活，捕食性天敵數(shù)量監(jiān)測(cè)的結(jié)果顯示：與純林相比，混交林中松樹(shù)上葉蜂的幼蟲(chóng)和卵的比例降低[71]。這與混交林中螞蟻數(shù)量多有關(guān)。其他葉蜂天敵(如蜘蛛和捕食性半翅目昆蟲(chóng))在不同地點(diǎn)有差異并與螞蟻數(shù)量呈負(fù)相關(guān)，說(shuō)明這些組分的相互作用。盡管混交林葉蜂存活低、提供了聯(lián)合抗性的證據(jù)，相關(guān)研究表明這些樹(shù)上有著比純林更高的蚜蟲(chóng)群體，而這些蚜蟲(chóng)與螞蟻放牧有關(guān)。因此，相比于考慮對(duì)單一植食性物種的聯(lián)合抗性，將更大的系統(tǒng)如林分整體對(duì)普遍的植食性動(dòng)物的聯(lián)合抗性是更加實(shí)際的[71]。

筆者以昆崳山天然赤松(Pinusdensiflora)林和寡食性食葉昆蟲(chóng)-昆崳山腮扁葉蜂(Cephalciakunyushanica)為研究對(duì)象，對(duì)比樹(shù)種組成類型、多樣性、立地和林分因子對(duì)昆崳山腮扁葉蜂種群密度的影響，研究結(jié)果以量化的方式證明在昆崳山赤松自然保護(hù)區(qū)，樹(shù)種組成對(duì)昆崳山腮扁葉蜂種群的影響更為重要，赤松與其親緣關(guān)系較近樹(shù)種混交，昆蟲(chóng)種群穩(wěn)定性較差，赤松與相鄰樹(shù)種形成對(duì)昆崳山腮扁葉蜂聯(lián)合易感作用，而與其它親緣關(guān)系較遠(yuǎn)的樹(shù)種混交，使害蟲(chóng)種群穩(wěn)定性增強(qiáng)，進(jìn)而形成聯(lián)合抗性作用[72]。

在特定群落中，鄰近植物的適口性(即被取食的程度)顯著影響植食性昆蟲(chóng)的多度，以及被哺乳動(dòng)物為害的程度，但不影響被昆蟲(chóng)取食所造成的為害程度。當(dāng)周圍植物不適口時(shí)，關(guān)鍵植物的植食性動(dòng)物數(shù)量減少(即聯(lián)合抗性)；若周圍植物同樣適口時(shí)，關(guān)鍵植物和鄰近植物的植食性動(dòng)物數(shù)量沒(méi)有差異[56]。但分類上差別較大的植物雖然能影響植食性動(dòng)物多度，但不影響其所受到的為害程度。Barbosa等的研究結(jié)果表明，當(dāng)以植食性動(dòng)物多度作為因變量時(shí)，發(fā)現(xiàn)“聯(lián)合抗性”多存在于植物分類地位較遠(yuǎn)的物種組合中(如不同的目之間)；若鄰近植物與關(guān)鍵植物屬同一科、或?qū)?、或種時(shí)，對(duì)“聯(lián)合抗性”的形成不會(huì)有任何影響。在人工棲息地(如農(nóng)田)，“聯(lián)合抗性”和“聯(lián)合易感性”能夠通過(guò)斑塊間相鄰植物的運(yùn)用或非作物植物的運(yùn)用而形成。作者認(rèn)為，在景觀水平上，這種“聯(lián)合抗性”和“聯(lián)合易感性”也能夠形成[56]。

3 植物脅迫假說(shuō)(Plant stress hypothesis)和植物生長(zhǎng)勢(shì)假說(shuō)(Plant vigor hypothesis) 的提出與驗(yàn)證

3.1 植物脅迫假說(shuō)和植物生長(zhǎng)勢(shì)假說(shuō)的提出

White提出“植物脅迫假說(shuō)”，指出由于環(huán)境條件惡化改變了植物器官中生物化學(xué)物質(zhì)合成以及葉部組織的化學(xué)成分，導(dǎo)致植物化學(xué)抗性物質(zhì)降低，使得受脅迫的植物寄主更適合昆蟲(chóng)取食，因而這些植物體上的植食性昆蟲(chóng)種類和數(shù)量更多[73]。而在1991年，Price提出了“植物生長(zhǎng)勢(shì)假說(shuō)”，他認(rèn)為許多植食性昆蟲(chóng)更傾向于取食生長(zhǎng)勢(shì)旺盛的植物，由此與“植物脅迫假說(shuō)”相對(duì)應(yīng)[10]。 “植物生長(zhǎng)勢(shì)假說(shuō)”適于揭示與植物生長(zhǎng)過(guò)程有關(guān)的害蟲(chóng)發(fā)生情況；同時(shí)它還揭示了在某些情況下，尤其是在那些干旱的立地條件下，植物早期的抗性誘導(dǎo)的機(jī)制和后期抗性增強(qiáng)的機(jī)制。

3.2 植物脅迫假說(shuō)和植物生長(zhǎng)勢(shì)假說(shuō)的驗(yàn)證

“植物脅迫假說(shuō)”在提出的早期得到了普遍認(rèn)可，而且實(shí)驗(yàn)證據(jù)普遍支持受到中等脅迫的寄主由于其營(yíng)養(yǎng)物質(zhì)的增加而有利于植食性昆蟲(chóng)取食[74- 75]，同時(shí)在一些樹(shù)種、農(nóng)作物中發(fā)現(xiàn)植食性昆蟲(chóng)危害與植物受脅迫強(qiáng)度成正相關(guān)[75- 76]。但后期的研究，如通過(guò)采用元分析(meta-analyses)開(kāi)展受水脅迫的植物寄主對(duì)植食性昆蟲(chóng)發(fā)生影響的研究發(fā)現(xiàn)，受脅迫植物對(duì)刺吸式昆蟲(chóng)表現(xiàn)出顯著的負(fù)效應(yīng)，對(duì)咀嚼式式昆蟲(chóng)沒(méi)有顯著影響，同時(shí)，受脅迫的植物體上蟲(chóng)癭密度減少[77- 78]；而對(duì)其他一些昆蟲(chóng)，如天牛、潛葉蛾等的發(fā)生沒(méi)有顯著影響或這種影響具有不穩(wěn)定性。整體上，Huberty和Denno的研究結(jié)果并不支持植食性昆蟲(chóng)在受水脅迫后的植物寄主體上呈現(xiàn)更高的豐富度和種群密度的假設(shè)[78]。

植物生長(zhǎng)勢(shì)，亦被稱為“活力Vigor”，被定義為任何植物或植物模塊的成長(zhǎng)較平均生長(zhǎng)速率更快，體積更大[79]。Price提出，與植物生長(zhǎng)過(guò)程有關(guān)的昆蟲(chóng)更傾向于在長(zhǎng)勢(shì)旺盛的寄主體上產(chǎn)卵，以保障幼蟲(chóng)的發(fā)育[10]；雖然Cobb等指出“植物生長(zhǎng)勢(shì)假說(shuō)”并未證明任何機(jī)制來(lái)說(shuō)明植食性昆蟲(chóng)更好地存活與植物活力(生長(zhǎng)勢(shì))間的正相關(guān)關(guān)系，但他同時(shí)也承認(rèn)一些可能的因素促使這種結(jié)果的發(fā)生，如資源的增加、食物質(zhì)量的提高、和/或植物體內(nèi)防御物質(zhì)的減少，等[80]。“植物生長(zhǎng)勢(shì)假說(shuō)”早期以蟲(chóng)癭類昆蟲(chóng)為試驗(yàn)?zāi)０?，目前該假說(shuō)適于揭示更多不同取食方式的昆蟲(chóng)，如潛葉蠅、天牛、咀嚼式口器昆蟲(chóng)、刺吸式口器昆蟲(chóng)及卷葉蛾等[81- 82]。最近，Cornelissen等的研究結(jié)果進(jìn)一步肯定了生長(zhǎng)勢(shì)旺盛的植物體更加并且顯著地吸引植食性昆蟲(chóng)，但他們同時(shí)也強(qiáng)調(diào)植物活力對(duì)昆蟲(chóng)的存活并無(wú)顯著影響。從取食方式看，對(duì)旺盛生長(zhǎng)植物依賴性最強(qiáng)的昆蟲(chóng)是刺吸式口器昆蟲(chóng)、潛葉蠅和蟲(chóng)癭類昆蟲(chóng)[83]。因此，作者同時(shí)指出，許多以植物活力為標(biāo)準(zhǔn)的品種選擇應(yīng)考慮其受危害的潛在風(fēng)險(xiǎn)[83]。

4 上調(diào)力和下調(diào)力的提出與驗(yàn)證

4.1 上調(diào)力和下調(diào)力的提出

天然林中病蟲(chóng)害另一個(gè)調(diào)節(jié)機(jī)制來(lái)自于食物鏈和食物網(wǎng)結(jié)構(gòu)，即上調(diào)力“Bottom-Up forces”和下調(diào)力“Top-Down forces”機(jī)制[84]。Hairston等提出“綠色世界”假說(shuō)，認(rèn)為自然界中天敵制約著植食性動(dòng)物的種群數(shù)量(即下調(diào)力)，并使之保持在無(wú)法消耗完寄主資源的較低種群密度，使得自然界保持“綠色”[85]。上調(diào)力是指在每個(gè)營(yíng)養(yǎng)水平均存在資源制約、即生產(chǎn)者制約機(jī)制，而下調(diào)力是捕食性制約機(jī)制。在特定生態(tài)系統(tǒng)的食物鏈上，生物體即可成為捕食者、也可成為食物資源制約者。White認(rèn)為，除非植物處在環(huán)境脅迫下，植食性動(dòng)物并不能明顯地和顯著地消耗其棲息地中所有植物資源，所有營(yíng)養(yǎng)水平均由食物資源所制約[86]。

4.2 上調(diào)力和下調(diào)力的驗(yàn)證

上調(diào)力主要是通過(guò)植物本身的物理性狀如蠟質(zhì)層和保衛(wèi)細(xì)胞[87- 88]、化學(xué)成分如毒素[89]以及信號(hào)揮發(fā)系統(tǒng)[90]、等，來(lái)抵抗昆蟲(chóng)的為害。植物的這些特點(diǎn)在空間上從植物個(gè)體的不同部位到不同植物種類之間存在顯著變化[91- 92]。上調(diào)力的這種空間變化是其他營(yíng)養(yǎng)級(jí)關(guān)系的主要基礎(chǔ)。而下調(diào)力的影響主要表現(xiàn)在強(qiáng)度上。大多數(shù)學(xué)者認(rèn)為寄生物、捕食者和病原有時(shí)會(huì)引起植食性昆蟲(chóng)的高死亡率，如有時(shí)寄生率非常高使得上調(diào)力幾乎不發(fā)揮效果。但這種高寄生率或被捕食率在大地理尺度[93]和小的空間尺度的效果差異是明顯的[94]。因此，這種立地條件的變化使得在某一地點(diǎn)量化的下調(diào)力不能適應(yīng)于更大的系統(tǒng)或尺度。

盡管這些爭(zhēng)論有時(shí)呈現(xiàn)極度的兩級(jí)分化[95- 96]，但目前絕大多數(shù)生態(tài)學(xué)家贊同無(wú)論是上調(diào)力還是下調(diào)力，均對(duì)調(diào)控植食性昆蟲(chóng)起到重要作用[94, 97]。關(guān)鍵是這些調(diào)控作用如何在時(shí)空序列中保持相對(duì)的平衡[97]。

有學(xué)者提出廣泛的調(diào)控作用不但應(yīng)包含上調(diào)力、下調(diào)力等縱向的作用力，還應(yīng)包括水平方向的同一營(yíng)養(yǎng)級(jí)內(nèi)和不同營(yíng)養(yǎng)級(jí)間的作用。水平作用力主要是指植食性昆蟲(chóng)種內(nèi)和種間競(jìng)爭(zhēng)[98]。盡管植食性動(dòng)物間的競(jìng)爭(zhēng)不能從本質(zhì)上解釋世界之“綠”，但它具有影響種特異性密度的效果[99]。因此，要了解影響蟲(chóng)口密度的各種因素及其強(qiáng)度，這種水平作用力必須加以考慮。

同時(shí)，上述任何力量的強(qiáng)弱會(huì)應(yīng)立地條件的不同而不同，因而對(duì)于比較上調(diào)力相對(duì)下調(diào)力的研究常常遲滯于空間的變化[16]。從景觀生態(tài)學(xué)的角度出發(fā)，由于景觀是由不同棲息地的斑塊所組成，許多調(diào)控力量、甚至大多數(shù)的調(diào)控力的強(qiáng)度會(huì)隨著立地條件的變化而變化。同時(shí)，有學(xué)者提出與傳統(tǒng)的上調(diào)力和下調(diào)力理論完全不同的一組影響力量，即非生物影響因素[16]。植食性昆蟲(chóng)種群密度受非生物因素影響的觀點(diǎn)由來(lái)已久[100]，非生物條件的影響程度隨空間而變，例如小氣候影響昆蟲(chóng)的存活、對(duì)資源的選擇以及昆蟲(chóng)的分布[101- 102]。非生物條件影響的效果往往通過(guò)營(yíng)養(yǎng)關(guān)系，如通過(guò)影響寄主植物的質(zhì)量[103]或相互作用物種的種群動(dòng)態(tài)[104]等而受到調(diào)控。因此，無(wú)論其作用效果是直接或是間接，由非生物因子引起的不同空間的植食性昆蟲(chóng)死亡率的差異應(yīng)當(dāng)包含在影響當(dāng)中。

5 結(jié)語(yǔ)

森林生態(tài)系統(tǒng)所具有的結(jié)構(gòu)復(fù)雜性、時(shí)空穩(wěn)定性和對(duì)病蟲(chóng)災(zāi)害較高的耐害性與自我補(bǔ)償能力等特點(diǎn)，是實(shí)現(xiàn)病蟲(chóng)害可持續(xù)控制的基礎(chǔ)條件；而森林生態(tài)系統(tǒng)自調(diào)控病蟲(chóng)害的能力，不但與森林生態(tài)系統(tǒng)植物群落的結(jié)構(gòu)和樹(shù)種組成特征有關(guān)，也與天然林中物種多樣性較高有關(guān)[105]?？v觀上述這些植食性昆蟲(chóng)與植物寄主互作的假說(shuō)或機(jī)制，它們是基于不同的層面或尺度提出的，因而在解析研究目標(biāo)時(shí)，由于基本面的差異有可能會(huì)得出不同的結(jié)論。深入辨析這些植食性昆蟲(chóng)與植物寄主互作的假說(shuō)或機(jī)制的適用方位可以看到，它們之間存在著辯證統(tǒng)一的關(guān)系。

多樣性-穩(wěn)定性機(jī)制關(guān)注森林生態(tài)系統(tǒng)的功能，是基于群落甚至景觀層次。森林病蟲(chóng)害干擾所涉及的穩(wěn)定性概念主要是指森林生態(tài)系統(tǒng)遭受生物干擾后系統(tǒng)的抵抗力和恢復(fù)力。如同其他的相互作用，如消費(fèi)者-資源相互關(guān)系、競(jìng)爭(zhēng)、共生等，聯(lián)合抗性和聯(lián)合易感性通常包含了兩種有機(jī)體之間的相互作用，以及這種相互作用的結(jié)果如何影響第3個(gè)物種(植食性動(dòng)物)或被植食性動(dòng)物影響。因此，多樣性條件下的聯(lián)合抗性機(jī)制和聯(lián)合易感性應(yīng)屬于穩(wěn)定性中的抵抗力范疇。聯(lián)合抗性機(jī)制的主要基礎(chǔ)是基于資源集中假說(shuō)和天敵假說(shuō)，這些觀點(diǎn)在種群層次上更易理解；而基于食物鏈和食物網(wǎng)結(jié)構(gòu)提出的即上調(diào)力和下調(diào)力機(jī)制，以生態(tài)系統(tǒng)食物網(wǎng)底部的資源與頂端的天敵來(lái)探討其中的相互作用關(guān)系。因此，資源集中與上調(diào)力有著對(duì)應(yīng)關(guān)系，但各自的出發(fā)點(diǎn)不同，資源集中重在探討植食性昆蟲(chóng)可利用的資源總量、而下調(diào)力更側(cè)重于這種食物鏈的營(yíng)養(yǎng)關(guān)系；類似的，天敵假說(shuō)只是下調(diào)力機(jī)制中的一個(gè)層面而已(圖1)[106]。植物生長(zhǎng)勢(shì)假說(shuō)和植物脅迫假說(shuō)力圖從植物個(gè)體的狀態(tài)出發(fā)解析植食性動(dòng)物的選擇趨勢(shì)，實(shí)際上，更多地是探討資源的屬性問(wèn)題。因而，可以從其個(gè)體或種的群體的角度進(jìn)行研究。其中，植物脅迫假說(shuō)更多地與植物所處的棲息地環(huán)境有關(guān)。

圖1 天然林調(diào)控病蟲(chóng)害機(jī)制與假說(shuō)關(guān)系圖[106]Fig.1 Relations among mechanism and hypothesis of natural forest mediating pests[106]

其中，聯(lián)合抗性和聯(lián)合易感性理論對(duì)指導(dǎo)森林有害生物生態(tài)控制具有更直接的指導(dǎo)作用。但這些理論仍然需要進(jìn)一步完善。有研究初步揭示，森林生態(tài)系統(tǒng)中關(guān)鍵植物和鄰居植物的相對(duì)多度對(duì)在景觀水平上形成“聯(lián)合抗性”或“聯(lián)合易感性”顯得重要[56]。景觀水平的“聯(lián)合易感性”的形成很大程度上依賴于主要植食性動(dòng)物的食物資源是否分布在周圍的棲息地中，或周圍的棲息地的條件是否能促進(jìn)植食性動(dòng)物的越冬存活率[107]。鄰近棲息地也可能成為景觀中動(dòng)物擴(kuò)散的障礙，從而創(chuàng)造出景觀水平的聯(lián)合抗性[108]。但這類研究還很不系統(tǒng)，尚未形成對(duì)森林經(jīng)營(yíng)和管理具有指導(dǎo)意義的理論；同時(shí)，“聯(lián)合抗性”和“聯(lián)合易感性”的強(qiáng)度、穩(wěn)定性以及對(duì)植物適應(yīng)性的影響也可能隨著時(shí)間變化、環(huán)境條件的改變以及植食性動(dòng)物和植物的多度的變化而變化[56]。長(zhǎng)期的種群和群落水平的“聯(lián)合抗性”和“聯(lián)合易感性”的效應(yīng)的研究很少，這可能是未來(lái)需要努力的方向，而這些研究對(duì)指導(dǎo)森林的經(jīng)營(yíng)管理具有現(xiàn)實(shí)的指導(dǎo)意義。

我國(guó)森林病蟲(chóng)害的防控技術(shù)體系盡管經(jīng)過(guò)了50年的不斷完善，提出了適合中國(guó)國(guó)情的防治策略和方法，但是，可持續(xù)控制病蟲(chóng)災(zāi)害的核心技術(shù)問(wèn)題仍未取得突破性進(jìn)展，根本原因在于森林食葉害蟲(chóng)與寄主互作機(jī)制研究一直未能取得突破[109- 110]。森林保護(hù)學(xué)必須與生態(tài)學(xué)緊密結(jié)合，只有深刻了解森林有害生物對(duì)森林組成、結(jié)構(gòu)的相互影響的過(guò)程，才能真正實(shí)現(xiàn)森林植食性昆蟲(chóng)的可持續(xù)控制。

致謝: 澳大利亞CSIRO王應(yīng)平博士對(duì)本文寫作提供幫助。

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Mechanism, hypothesis and evidence of herbivorous insect-host interactions in forest ecosystem

ZENG Fanyong1，SUN Zhiqiang2,3,*

1ScienceandTechnologyManagementOffice,ChineseAcademyofForestry,Beijing100091,China2PaulowniaR&DCenterofChina,ChineseAcademyofForestry,Zhengzhou450003,China3Non-timberForestryR&DCenter,ChineseAcademyofForestry,Zhengzhou450003,China

This paper analyzed the concepts, different mechanisms of herbivorous insect-host interactions and hypotheses based on their academic origins and recent experimental evidence. The theories we analyzed include diversity-stability mechanism, associational resistance hypothesis, associational susceptibility hypothesis, plant vigor hypothesis, plant stress hypothesis, bottom-up forces, top-down forces, and push-pull mechanism, etc. Diversity-stability mechanism focuses on functioning of forest ecosystem that is developed using evidence collected at community and landscape scale. Associational resistance and associational susceptibility is a resistance type of diversity-stability. The foundation for associational resistance hypothesis was built based on resource concentration hypothesis and natural enemy hypothesis. The resource concentration hypothesis predicted that herbivores were more likely to be found in patches where their host plants were abundant. The enemy hypothesis can explain why herbivores are fewer in forest ecosystems with a more abundant and diverse community of natural enemies. This was consistent with the diversity-stability hypothesis, which predicts that a community becomes more stable with higher diversity. These theories were easily understandable at population scale. Bottom-up forces and Top-down forces discuss the interaction between herbivorous insects and host plants along the food chains, in which bottom-up refers to restriction mechanism caused by resources on the bottom of food web while Top-down refers to natural enemies on the top of food chain. Therefore, there was a corresponding relationship between resources concentration hypothesis and bottom-up forces, and enemy hypothesis corresponds to top-down forces. Plant vigor hypothesis and plant stress hypothesis predict that herbivores tend to select host plants based on their growth conditions population size. The above herbivore-host interaction theories are proposed based on different levels in a forest ecosystem, which might result in different conclusion due to the differences in ecosystem levels. This paper then elaborated the guiding roles of these theories on forest pest control based on recent progresses. Among these theories, Associational resistance and associational susceptibility may be applicable to guide forest management, specifically forest pest control. The evidence suggested that associational resistance and associational susceptibility interactions may be mediated by biotic and abiotic mechanisms. However, there were few studies on how habitats, the spatial and temporal availability of resources determine landscape-level impacts of associational resistance and associational susceptibility, and how the strength, consistency, and relative impact of associational resistance and associational susceptibility on plant fitness vary temporally and spatially as environmental conditions, herbivore and plant abundance change. These are the questions urgently needed to be answered in this field.

herbivorous insect; host; insect-host interaction mechanism; diversity-stability mechanism; associational resistance hypothesis

國(guó)家林業(yè)公益性行業(yè)科研專項(xiàng)項(xiàng)目(201304406);國(guó)家“十二五”科技支撐計(jì)劃項(xiàng)目(2012BAD19B0801)資助

2013- 04- 27;

2013- 09- 22

10.5846/stxb201304270830

*通訊作者Corresponding author.E-mail: sun371@ 163.com

曾凡勇，孫志強(qiáng).森林生態(tài)系統(tǒng)中植食性昆蟲(chóng)與寄主的互作機(jī)制、假說(shuō)與證據(jù).生態(tài)學(xué)報(bào),2014,34(5):1061- 1071.

Zeng F Y，Sun Z Q.Mechanism, hypothesis and evidence of herbivorous insect-host interactions in forest ecosystem.Acta Ecologica Sinica,2014,34(5):1061- 1071.