氣候暖化與螞蟻密度如何影響螞蟻、蚜蟲與瓢蟲的交互作用以及農作物的表現

Abstract

氣候暖化可改變生物的交互作用，進而對農業活動產生深遠的影響。在農業系統中，生物的交互作用常跨越植物、植食者、與掠食者等三營養階層系統(tri-trophic system)。然而，這些系統往往因為螞蟻(具多種生態角色)的出現而變得更複雜。螞蟻一方面對農業有某些益處，然而另一方面又可能促進一些農業害蟲的生長，例如蚜蟲。值得一提的是，螞蟻和蚜蟲的關係雖然一般被歸類為互利共生(mutualism)，但是兩者的關係其實從互利共生到利用(exploitation)都有，而且受到很多生物和非生物因子的影響。由於螞蟻對植食性昆蟲(蚜蟲) 影響很大，螞蟻引起的交互作用有可能會產生營養瀑布(trophic cascade)，進而影響到植物(包括農業作物)。由於這些生物交互作用的重要性，許多研究已探討螞蟻與蚜蟲的交互作用(ant–aphid interactions)和螞蟻與植物的營養瀑布(ant–plant cascades)。然而，目前還不清楚螞蟻密度如何影響螞蟻與蚜蟲的交互作用、螞蟻與植物的營養瀑布，及氣候暖化如何影響以上的交互作用。為了回答這些問題，本研究探討 1) 螞蟻密度對螞蟻與蚜蟲交互作用(蚜蟲數量)的影響，2) 螞蟻密度對作用在植物上的營養瀑布之影響(如植物生長、防禦、生殖表現)，3) 溫度上升對以上交互作用的影響。我們設計了一個有著附加螞蟻的三階層系統(大豆、蚜蟲、瓢蟲)，並進行了一個3x3複因子的實驗，包括三種溫度處理(控制組、+ 3°C、+ 6°C)和三種螞蟻密度處理(0隻[控制組]、15隻、30隻)。在實驗期間，我們記錄了大豆蚜(Aphis glycines)數量和大豆(Glycine max)的生長、防禦、與生殖性狀。這個系統使用七星瓢蟲(Coccinella septempunctata)作為蚜蟲的掠食者，及熱帶火蟻(Solenopsis geminata)作為蚜蟲的互利共生夥伴。實驗結果顯示，螞蟻密度是影響螞蟻與蚜蟲交互作用、螞蟻與植物的營養瀑布的重要因子。高螞蟻密度提升了蚜蟲數量(互利共生)，並可能透過營養瀑布的作用，減少大豆葉片數量和增加大豆葉片硬度；另外，也可能減少大豆豆莢和種子的數量。然而，這些趨勢在暖化下變得不顯著，可能是由於暖化對於蚜蟲的直接正面作用，導致蚜蟲數達到大豆的承載量(carrying capacity)，進而掩蓋了螞蟻密度的作用。出乎意料之外，高螞蟻密度增加的大豆植株的高度，推測是透過螞蟻的直接影響作用。此外，暖化會顯著地直接影響植物生長(正負都有)，卻幾乎不影響植物生殖表現。綜合上述結果，由於 暖化會降低生物交互作用(互利共生、營養瀑布)的影響力，我們推測暖化的直接作用很可能成為這世紀影響植物表現的主要因子。

Climate warming has had tremendous impact on agriculture, a lot of which can be attributed to altered biotic interactions under warming. In agricultural systems, biotic interactions often take on the form of tri-trophic systems consisting of plants, herbivores, and predators. Such systems, however, are often made more complex with the presence of ants, which can play multiple ecological roles. While ants have certain benefits to agriculture, they might also facilitate agricultural pests such as aphids. However, ant–aphid interactions, typically described as mutualism, actually range from mutualism to exploitation, and are contingent upon a variety of biotic and abiotic factors. Moreover, due to their ability to influence herbivores (aphids), the outcome of such interactions may generate trophic cascades on plants (crops). On account of their ecological significance, many studies have investigated ant-aphid interactions and ant–plant cascades. Nonetheless, it remains unclear how ant density affects ant-aphid interactions and thereby plant performance (via trophic cascades), and how these effects are mediated by climate warming. To help fill these knowledge gaps, this study examined 1) the effect of ant density on ant–aphid interactions (i.e., aphid population size), 2) the effect of ant density on plants via trophic cascades (i.e., plant growth, defense, and reproduction), and 3) the impact of climate warming on the aforementioned processes. We designed a tri-trophic system (soybean, aphid, ladybug) with the addition of ants, and conducted a 3x3 factorial experiment including temperature (control, + 3°C, + 6°C) and ant density treatments (0 ants [control], 15 ants, 30 ants). We recorded the number of soybean aphids (Aphis glycines), along with the growth, defense, and reproductive traits of soybean plants (Glycine max). The study system included seven-spotted ladybugs (Coccinella septempunctata) as aphid predators and tropical fire ants (Solenopsis geminata) as the aphids’ ant mutualists. Our results show that ant density, overlooked in previous studies, played an important role in ant–aphid interactions and ant–plant cascades. Higher ant density increased aphid number (mutualism), which likely resulted in trophic cascades that reduced leaf number, increased leaf toughness, and possibly reduced pod number and seed number. However, these trends became less obvious under warming. This was probably because warming generated a strong, positive direct effect on aphid population, which may have reached the carrying capacity of soybeans, thus obscuring the effect of ant density. Surprisingly, higher ant density increased plant height, possibly due to some direct ant effect instead of trophic cascades. In addition, warming had a strong direct impact on plant growth, though not reproduction; these effects ranged from positive to negative. Since the effect of biotic interactions (mutualism, trophic cascades) diminished under warming, it is likely that these direct warming effects became the primary influence on plant performance. To conclude, this study showed that warming reduced the effects of biotic interactions (mutualism and trophic cascades), suggesting that abiotic effects (warming) may become the dominant factor in determining crop performance.