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台灣福山地區三種埋葬蟲的分布與尼泊爾埋葬蟲(Coleoptera: Silphidae) 的族群動態

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台灣福山地區三種埋葬蟲的分布與尼泊爾埋葬蟲(Coleoptera: Silphidae) 的族群動態 生物學報（2013）48：1-11 DOI：10.6248/BF.2013.48.01 台灣福山地區三種埋葬蟲的分布與尼泊爾埋葬蟲(Coleoptera: Silphidae) 的族群動態 1 2 黃文伯 葛兆年 * 1 國立台南大學生態科學與技術學系 2 行政院農業委員會林業試驗所森林保護組 （收稿日期：2013.2.1，接受日期：2013.4.15） 摘 要 本研究為探討福山地區三種埋葬蟲的棲地分布與季節性活躍，並標放尼泊爾埋葬蟲，來分析 該物種的族群動態。紅胸埋葬蟲與尼泊爾埋葬蟲有顯著的時空棲位區隔，紅胸埋葬蟲偏好在夏季的 草地活動，而尼泊爾埋葬蟲則偏好春秋季的林地。紅胸埋葬蟲、大黑埋葬蟲與尼泊爾埋葬蟲的活躍 期高峰，在海拔較高的阿玉山皆晚於海拔較低的福山。在阿玉山所捕獲的紅胸埋葬蟲與尼泊爾埋葬 蟲，其前胸背板寬皆顯著大於在福山的族群；不論在福山或阿玉山，紅胸埋葬蟲雄蟲個體大小皆較 大於雌蟲；尼泊爾埋葬蟲在阿玉山的族群，雌蟲大小顯著大於雄蟲，但於福山的族群則無差別。雖 然尼泊爾埋葬蟲的捕獲數量在2002年調查期間出現三個高峰值，但以Jolly-method估算，族群大小 穩定，僅在四月初出現高峰期。尼泊爾埋葬蟲在光週期L/D: 11/13、溫度20oC的條件下，世代所需 時間為44 ± 1.04日，四月中羽化的高峰期可對應到二月底成蟲活動的高峰期。尼泊爾埋葬蟲4日內 移動距離中位數為174.4 m，福山與阿玉山兩地族群未發現明顯交流的現象。 關鍵詞：埋葬蟲科、棲地分布、季節性活躍、尼泊爾埋葬蟲、標放再捕捉、Jolly 法、族群動態 緒 言 致昆蟲劇烈地競爭屍體資源(Wilson and Fudge, 1984; Wilson et al., 1984; Trumbo, 1990)。儘管埋 埋葬蟲科(Silphidae)甲蟲屬於動物屍體分解 葬蟲壽命可以長達四個月左右(Hwang and Shiao, 者，在物質轉換、能量循環中為重要角色之一。 2011)，但埋葬蟲要發現可適合做為繁殖用的屍體， 埋葬蟲科包含了Nicrophorinae和Silphinae兩亞科， 一生可能只有一次(Scott and Gladstein, 1993)。在 除少數物種為植食性外(Anderson and Peck, 發現屍體後，同種或異種之間的個體亦經常為了 1984)，本科大部份物種的成蟲與幼蟲皆以動物屍 爭奪屍體而打鬥(Pukowski, 1933; Bartlett and 體為營養來源。在Nicrophorinae的物種中，特別 Ashworth, 1988; Otronen, 1988; Müller et al., 是斑紋埋葬蟲屬(Nicrophorus spp.)因具有埋葬屍 1990)。在競爭排斥原理下，使用相似資源的物種， 體與撫育的行為，較為偏好利用小型(如鼠、鳥) 應在生態棲位上發生區隔的現象(Hutchinson, 屍體(Pukowski, 1933; Trumbo, 1992; Scott, 1998; 1958; MacArthur and Levins, 1964; Levins, 1968)。 Hwang and Shiao, 2008; Sikes, 2008)；而Silphinae 共域的埋葬蟲即存在日、夜與黃昏活動習性的差 的物種在無撫育行為下，則傾向利用大型屍體(> 異、季節性活躍高峰的差異，以及棲地偏好的差 300 g)進行繁殖(Ratcliffe, 1996; Hoback et al., 異(Scott, 1998)。 2004)。 屍體分解速率與溫度、溼度、棲地類型和季 節肢動物是屍體微棲地中主要的生物類群， 節有關(Payne, 1965; Nabaglo, 1973; Swift et al., 雙翅目(Diptera)、鞘翅目(Coleoptera)、膜翅目 1979)。而屍體分解速率則影響屍體資源可利用的 (Hymenoptera)與蜘蛛目(Araneae)在屍體上即佔 時效，進而影響分解者的族群密度與群聚的物種 了78%~90%的個體組成(Payne, 1965; Johnson, 組成(Hanski and Cambefort, 1991 ; Martin-Piera 1975)。動物屍體對昆蟲來說，是較為稀少的資源 and Lobo, 1993)。在野外，蠅類幼蟲與螞蟻是優 (Wilson, 1971; Hanski and Cambefort, 1991)，此導 勢的屍體分解者(Hwang, 2011)，在溫度較高的環 ＊通信作者：葛兆年（Chao-Nien Koh）；FAX：886-2-23078755；E-mail：[email protected] 黃文伯 葛兆年 境中，屍體先被蠅類與螞蟻發現並被迅速分解的 屍體誘餌。兩種棲地類型所有誘餌陷阱皆於兩小 機率較高(Putman, 1978; Easton, 1979)。這造成埋 時內同步置放誘餌，每個陷阱中每月各置放兩隻 葬蟲可用做繁殖的屍體資源過少，而影響埋葬蟲 4 ~ 5週齡ICR品系小鼠屍體(約20 g重)，每次放置 的繁殖成功率(Scott et al., 1987)。研究指出埋葬 一隻，每隻小鼠屍體皆放置4日，並統計兩個4日 蟲族群密度在海拔較高處大於海拔較低處 中陷阱內的埋葬蟲個體。為確定埋葬蟲受屍體誘 (McKinnerney, 1978; Halffter et al., 1983)，而同種 餌吸引，距離每個誘餌掉落式陷阱的5 m外，另 埋葬蟲的體型在較高海拔則大於較低海拔的個 設置一個僅含PVC水管擋土牆、漏斗與集蟲杯的 體(Smith et al., 2000)。較低的溫度可增加埋葬蟲 無誘餌掉落式陷阱，以統計確認屍體的吸引效 繁殖成功率(Trumbo, 1990)，即可能基於環境溫度 果。 的差異，影響埋葬蟲在不同海拔高度的族群密度。 2002年2月至同年6月除了於福山樣區調查 此外，昆蟲幼蟲生長發育所需的時間，在不同海 外，並在與福山直線距離約4 km遠、海拔高度 拔高度的差異(Danks, 1994; Sparks et al., 1995; 1200 ~ 1300 m的阿玉山樣區(24o46’N, 121o36’E) Sota, 1996)，亦可能是同種埋葬蟲的體型在不同 進行調查，該樣區棲地與福山溪谷林地相似，皆 海拔高度存在差異的原因。 為鬱閉闊葉林所覆蓋，穿越線為沿稜線的登山步 本研究即調查福山地區三種埋葬蟲的季節 道，陷阱設於步道兩側。此期間於福山與阿玉山 性活躍與棲地偏好，以及海拔高度對個體活躍與 兩樣區穿越線的林地內，分別設置15個與上述結 體型的影響。利用標放再捕捉尼泊爾埋葬蟲 構相同的誘餌掉落式陷阱，陷阱間距為100 m以 (Nicrophorus nepalensis Hope)個體的方法分析該 上，每月放置一隻4 ~ 5週齡Wistar品系大鼠屍體 物種的族群動態，並了解尼泊爾埋葬蟲的生活史 (約130 g重)，並計算兩樣區每個月於4日內所捕獲 週期，比對野外新羽化個體之親代的繁殖時間點， 的埋葬蟲個體數量。同時以游標尺測量兩樣區紅 和探討該物種個體移動能力與族群間交流的可 胸埋葬蟲與尼泊爾埋葬蟲個體的前胸背板寬度， 能性。 以比較兩樣區族群或性別的個體大小差異。 材料與方法 尼泊爾埋葬蟲的族群動態 2002 年 2 月 24 日至 4 月 22 日於福山樣區， 埋葬蟲的採集與形態測量 將每 4 天所捕捉的尼泊爾埋葬蟲個體於翅鞘上以 2001年2月至2002年1月的研究樣區位於台 1 號蟲針戳孔編碼標放。翅鞘戳孔後，在無外力 灣福山的哈盆自然保留區(24o45’N, 121o34’E，以 損傷下，該孔洞皆能長久保留，且在橙色斑塊處 下簡稱福山)，海拔高度為600 ~ 800 m之間，沿哈 戳孔，孔緣發黑明顯，可清楚以肉眼辨識。編碼 盆溪河岸規劃穿越線，於開闊的草地與鬱閉的林 方式為採用 Müller (1977)所設計，將翅鞘畫分為 地兩種類型棲地相隔內，每200 m設置一個誘餌 四個區塊，每一個區塊最多戳兩孔，並以孔洞位 掉落式陷阱，兩種棲地類型各設置8個取樣點。 置的排列對應出 1 ~ 9 的數字編碼，四個區塊分 誘餌掉落式陷阱結構為將一個20 cm高、內 別對應個位數、十位數、百位數和千位數，起始 徑15 cm的PVC空水管埋入地面下做為擋土牆，水 數字 1 皆接近翅鞘中線，翅鞘左右兩面編碼為鏡 管上方切面邊緣與地面齊平；管內置放一個出口 像對稱，以此編碼方式，每隻甲蟲最多僅戳 8 孔， 為內徑2 cm寬的漏斗，漏斗上緣為直徑15 cm以 且最多可編 9999 隻甲蟲(圖一)。 契合水管內徑，漏斗插入500 ml附有杯蓋的塑膠 集蟲杯中，杯底用圖釘鑿孔以排放積水；為避免 將埋葬蟲以個體識別的程度編碼標放後，透 腐食性脊椎動物取食誘餌，在埋管的地表鋪設60 過再捕捉的機率，以 Jolly-method 估算族群的大 x 60 cm2的鐵絲網，以營釘固定，並剪除鐵絲網 小(Mühlenberg 1993)，族群大小的計算方式為： 中間16 x 16 cm2的面積以開放漏斗上方；鐵絲網 P =((a x Z / R ) + r ) n / r 與漏斗上方置有一個16 x 16 x 8 cm3下方開放的 t t t t t t t 2 鐵籠，鐵籠網目為2 x 2 cm ，用8條尼龍束帶將鐵 其中 絲網與鐵籠束緊，以防止脊椎動物挖掘侵入，鐵 Pt：為時間 t 的族群大小 2 籠上方覆蓋一塊20 x 20 cm 的壓克力板擋雨；鐵 nt：為時間 t 的總捕獲數 籠內、漏斗正上方懸掛塑膠培養皿，以承載小鼠 at：為時間 t 所標放的個體數 2 埋葬蟲分布與族群動態 a rt：為時間 t 再捕獲有標記的個體數 b Rt：為時間 t 所標放且時間 t 之後再捕獲的 總數 Zt：為時間 t 前標放且時間 t 之後再捕獲的 總數 在無外力影響且食物充分的情況下，尼泊爾 埋葬蟲壽命約為121天(Hwang and Shiao, 2011)， 圖一、翅鞘戳孔編碼示意圖：(a)將翅鞘畫分為四個區 羽化後個體翅鞘約在 5 日內完全硬化，以 1 號蟲 塊，分別對應個位數、十位數、百位數和千位數；(b) 針戳孔時會產生阻力。因此在翅鞘戳孔時，同時 單一區塊內，孔洞排列的位置所對應1 ~ 9的數字編 檢測翅鞘硬度，若翅鞘較軟，戳孔時無阻力，則 碼。 視為剛羽化的個體。編碼標放的個體亦紀錄釋放 Figure 1. Schematic diagram of puncture coding on 時的 GPS 座標，以及再捕獲的時間與地點座標， elytra: (a) Elytra are divided into four blocks, which 基於捕捉標放的時間間隔幾乎都是 4 日，因此在 correspond to a 1-digit, 10-digit, 100-digit and 1000-digit block; (b) the arranged hole positions correspond to 1 to 評估埋葬蟲的移動能力時，皆換算為 4 日內的直 9 in the digital code in a single block. 線移動距離。 為確認新羽化個體在先前季節被親代產下 離的影響。統計顯著性的 alpha level 皆設定在 的時間點，將野外個體攜回實驗室，使其繁殖在 0.05。 較為接近野外日長與溫度的條件中，以估計世代 時間。野外成蟲以二氧化碳麻醉，在解剖顯微鏡 結 果 下以鑷子挑掉蟎類後，成對埋葬蟲置於直徑 11 cm 高 8.5 cm 內置 4 cm 厚培養土的透明塑膠容器 埋葬蟲的時空分布 中，並給予一隻約 20 g 的 ICR 品系小鼠屍體。將 由2001年2月至2002年1月於福山共捕獲紅 容器置於日長 11 hr 與溫度 20°C 的生長箱中，伺 胸埋葬蟲(Calosilpha cyaneocephala Portevin)、大 幼蟲離巢欲化蛹時，使用同樣規格的容器裝盛 4 黑埋葬蟲(Nicrophorus concolor Kraatz)與尼泊爾 cm 厚培養土，最多置入 8 隻幼蟲使其化蛹，並 埋葬蟲(Nicrophorus nepalensis Hope)個體共175 計算各對埋葬蟲從給予屍體至該巢後代羽化所 隻次，分析十二個月份具誘餌陷阱與不具誘餌陷 需的時間。 阱中所捕獲的三種埋葬蟲數，三種埋葬蟲皆受到 屍體誘引(Wilcoxon Signed Ranks Test: p < 0.05, n 統計分析 = 12)。其中大黑埋葬蟲較為零星出現，在九月時 本研究比較不同種埋葬蟲受屍體的吸引程 捕獲最多，但僅有5隻個體。另外兩種埋葬蟲在 度，以及在林地棲地與草地棲地的偏好，採用 時間上則有較明顯的區隔，尼泊爾埋葬蟲於福山 Wilcoxon Signed Ranks Test 分析 12 個月份個體 出現的時間為春秋兩季，而在夏季則完全消失； 數量的相依性數據。不同種埋葬蟲五個月份的活 紅胸埋葬蟲出現的時間為春末至秋季，五月時為 躍期比較，各於福山與阿玉山兩地檢定多組條件 活躍期最高峰，七至九月亦相當頻繁地出現(圖 下卡方分布(chi-square distribution)的同質性，在 二)。 計算出所試驗的卡方值後，對應該試驗所屬的自 以十二個月份分析埋葬蟲物種對林地或草 2 由度，當獲得之同質性機率低於 5%時 (χ -test: p 地的偏好，除大黑埋葬蟲因個體數目過少，無法 < 0.05)，即表示該試驗各組間存在顯著差異。埋 區分其棲地偏好外(Wilcoxon Signed Ranks Test: 葬蟲的個體大小分析，採用獨立樣本 t 檢定 p = 0.24, n = 12)，紅胸埋葬蟲顯著偏好在草地出 (Independent Sample t-Test)比較在福山與阿玉山 現(Wilcoxon Signed Ranks Test: p < 0.05, n = 12)， 兩地族群的差異，以及單一族群中兩性別個體大 而尼泊爾埋葬蟲則偏好以林地做為主要的活動 小的差異。分析影響尼泊爾埋葬蟲移動能力的因 空間(Wilcoxon Signed Ranks Test: p < 0.05, n = 子，使用簡單線性迴歸(Simple Linear Regression) 12)，後兩者的棲位出現時間性與空間性的區隔。 探討移動距離與個體大小(前胸背板寬度)的關係， 2002 年 2 月至同年6 月在海拔高度600 至 以及以 Mann-Whitney U-test 比較性別對移動距 800m福山樣線與在海拔高度1200至1300m的阿 3 黃文伯 葛兆年 350 30 C. cyaneocephala a 300 N. concolor 25 250 N. nepalensis 200 20 150 15 100 number 50 10 0 23456 5 0 14 b 234567891011121 12 month 10 8 圖二、2001年2月至2002年1月各月份於福山哈盆自然 number 6 保留區所捕獲的紅胸埋葬蟲(Calosilpha 4 cyaneocephala)、大黑埋葬蟲(Nicrophorus concolor)與 2 0 尼泊爾埋葬蟲(Nicrophorus nepalensis)之個體數量。 23456 Figure 2. Number of C. cyaneocephala, N. concolor, and N. nepalensis captured per month in Hahpen Nature 400 350 c Preserve in Fushan from February 2001 to January 2002. 300 250 玉山樣線進行調查，三種埋葬蟲在較高海拔阿玉 200 150 山樣線的活躍期皆顯著晚於較低海拔的福山樣 100 線(χ2-test: 紅胸埋葬蟲: p < 0.001, 大黑埋葬蟲: p 50 0 < 0.01, 尼泊爾埋葬蟲: p < 0.001)。紅胸埋葬蟲在 23456 month 福山樣線出現時間較早，2月即有捕獲紀錄，但 月捕獲數量皆在100隻以下，但3月在阿玉山樣線 圖三、2002年2月至6月在福山樣線(—)與阿玉山樣線 出現後，於4月的捕獲數量即超過100隻，於5、6 (---) 所捕獲三種埋葬蟲的數量，(a) 紅胸埋葬蟲 月仍持續增加；大黑埋葬蟲在福山樣線出現的時 (Calosilpha cyaneocephala) 、 (b) 大黑埋葬蟲 間亦早於阿玉山樣線一個月，在福山活躍的高峰 (Nicrophorus concolor)、(c)尼泊爾埋葬蟲(Nicrophorus 期為5月，而捕獲的數量在阿玉山樣線則是在5月 nepalensis)；三種埋葬蟲的數量高峰月份皆有顯著不 2 過後陡增；尼泊爾埋葬蟲在福山樣線於2月突然 同(χ -test, p皆 < 0.01)。 大量出現，但其捕獲量隨即逐漸降低，並於5月 Figure 3. Number of carrion beetles (per species) captured per month in Fushan (—) and Ayushan (---) 時無捕獲紀錄，在阿玉山樣線捕獲數量則是於4 from February 2002 to June 2002. (a) C. cyaneocephala 月達到高峰，雖然在兩樣線2月份皆有個體出現， (χ2-test: p < 0.001), (b) N. concolor (χ2-test: p < 0.01), 但活躍期高峰在阿玉山樣線延後了兩個月(圖 and (c) N. nepalensis (χ2-test: p < 0.001). The peaks of 三)。 the beetle numbers in Fushan and Ayushan were significantly different for three carrion beetle species 除了此三種埋葬蟲在實驗期間被捕獲外，亦 (χ2-test, all p < 0.01) 捕獲另外兩種埋葬蟲，粗腿埋葬蟲(Necrodes nigricornis Harold)於2001年1月進行前測時於草 在福山與阿玉山兩地族群體型上的差異，兩物種 地捕獲11隻，而雙斑埋葬蟲(Diamesus bimaculatus 位於較高海拔阿玉山的甲蟲族群，前胸背板寬度 Portevin)則是在2003年12月於林地陷阱中捕獲1 皆大於較低海拔福山的族群(t-Test: p < 0.001；紅 隻，並於2001年夏天在山羌(Muntiacus reevesi 胸埋葬蟲：福山 平均值 = 8.91 ± 0.65 mm，n = micrurus Sclater)屍體上觀察到，粗腿埋葬蟲與雙 195、阿玉山 平均值 = 9.34 ± 0.57 mm，n = 334； 斑埋葬蟲於實驗期間皆未受小鼠或大鼠屍體吸 尼泊爾埋葬蟲：福山 平均值 = 4.71 ± 0.62 mm， 引而捕獲。 n = 469、阿玉山 平均值 = 5.25 ± 0.67 mm，n = 281). 埋葬蟲在不同海拔高度下的個體大小差異 紅胸埋葬蟲不論是在福山或是阿玉山，兩地 在不同海拔高度的埋葬蟲，呈現個體大小的 族群的雄蟲前胸背板寬度皆顯著大於雌蟲(t-Test: 差異分布。分別比較紅胸埋葬蟲與尼泊爾埋葬蟲 p < 0.001；福山：雄蟲平均值 = 9.34 ± 0.50 mm， 4 埋葬蟲分布與族群動態 圖五、2002 年 2 月 24 日至4 月 22 日尼泊爾埋葬蟲 (Nicrophorus nepalensis)在福山的捕獲數(---)，以及使 用Jolly-method所估算的族群大小(—)。 Figure 5. Number of captured N. nepalensis (---) and population size estimated using the Jolly method (—) in Fushan from 24 February to 22 April, 2002. 蟲，並於翅鞘上戳洞編碼標放。尼泊爾埋葬蟲捕 獲的數量於此期間出現三個高峰值，分別在2月 28日、3月24日與4月18日。但以Jolly-method統計 圖四、2002年2月至6月兩種埋葬蟲雌雄個體前胸背板 寬度，各別在福山或阿玉山的比較。(a)紅胸埋葬蟲 族群數量密度，於可估算的日期中發現3月24日 (Calosilpha cyaneocephala)(福 山：雄 蟲 n = 89、雌 蟲 n 前族群密度呈現穩定的狀態，而族群於之後8日 = 106; 阿玉山：雄蟲 n = 196、雌 蟲 n = 138； t-Test： 內增加了約5倍的大小，至4月14日再恢復為先前 兩地皆為 p < 0.001)；(b)尼泊爾埋葬蟲(Nicrophorus 的族群密度(圖五)。 nepalensis)(福山：雄蟲 n = 273、雌蟲 n = 196，t-Test: 為了解族群密度動態變化的原因，對2002年 p = 0.927；阿 玉 山：雄 蟲 n = 119、雌 蟲 n = 162，t-Test: 2月24日至4月22日同時期所捕獲的尼泊爾埋葬 p < 0.001)(mean ± SE)。 蟲，在翅鞘戳洞編碼時，同時檢測翅鞘硬度，並 Figure 4. Pronotum width of male and female carrion 統計剛羽化出來的個體佔該日捕獲數量的比例。 beetles captured in Fushan or Ayushan from February 2002 to June 2002. (a) C. cyaneocephala: male: n = 89, 在捕獲個體數量高峰值的三個日期(2月28日、3 female: n = 106 in Fushan; male: n = 196, female: n = 月24日與4月18日)前，剛羽化個體所佔的比例， 138 in Ayushan (t-Test: p < 0.001 for both sites); (b) N. 即在2月24日、3月16日與4月14日達到高峰值(圖 nepalensis: male: n = 237, female: n = 196 in Fushan 六)。在光週期L/D: 11/13、溫度20oC的條件下， (t-Test: p = 0.927) ; male: n = 119, female: n = 162 in Ayushan (t-Test: p < 0.001; mean ± SE). 尼泊爾埋葬蟲發現屍體後，至下一個世代羽化出
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