張憲德,徐婷婷,趙婷婷,萬冬梅,殷江霞

遼寧大學(xué)生命科學(xué)院, 遼寧省動物資源與疫病防治重點實驗室, 沈陽　110036

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配偶選擇中“聽眾效應(yīng)”及鳴唱對雌性灰文鳥行為的影響

張憲德,徐婷婷,趙婷婷,萬冬梅,殷江霞*

遼寧大學(xué)生命科學(xué)院, 遼寧省動物資源與疫病防治重點實驗室, 沈陽110036

配偶選擇是性選擇研究核心問題之一。雌性通過選擇高質(zhì)量的雄性配偶獲得直接利益,如資源、營養(yǎng)和保護等,也可以通過獲得高質(zhì)量雄性提高后代的適合度。配偶選擇研究對于研究性選擇機制和進化均具有重要意義。目前,對配偶選擇的研究主要集中在影響配偶選擇的因素及雌性“聽眾效應(yīng)”中雄性-雄性競爭方面。鳴唱對配偶選擇的影響和雄性“聽眾效應(yīng)”中雌性-雌性競爭的研究對于探索鳥類配偶選擇中信號交流、調(diào)整的方式及選擇策略均具有重要意義。以灰文鳥為對象,研究了雄性鳴唱對雌性配偶選擇的影響及雄性“聽眾效應(yīng)”對雌性灰文鳥同性競爭行為的影響進行了探討。實驗一利用雙向選擇裝置,以配偶鳴唱(求偶鳴唱或非求偶鳴唱)和非配偶鳴唱(求偶鳴唱或非求偶鳴唱)對雌鳥進行刺激,觀察雌鳥對兩端鳴唱的偏愛狀況。實驗二主要觀察雌鳥之間在無聽眾、聽眾為熟悉的雄性和聽眾為配偶條件下的競爭行為。結(jié)果表明,雌性灰文鳥大多偏愛配偶鳴唱,相對于配偶的非求偶鳴唱更偏愛非配偶的求偶鳴唱。求偶鳴唱比非求偶鳴唱更具有吸引力,求偶鳴唱更能刺激雌性灰文鳥配偶選擇的積極性,這種積極要付出更多的時間和資源,但雌鳥可以通過選擇更高質(zhì)量的雄性配偶獲益。在配偶雄性作為聽眾條件下雌鳥攻擊行為最高,顯著高于熟悉雄性為聽眾的條件下,并且兩者都顯著高于無聽眾條件下雌鳥的攻擊行為。雌性灰文鳥會基于不同“聽眾”而對雌-雌競爭行為做出適當調(diào)整。上述研究結(jié)果對于深入理解鳥類的性選擇行為機制具有重要幫助作用。

灰文鳥;配偶選擇;鳴唱;積極性;聽眾效應(yīng);雌-雌競爭

繁殖行為是鳥類行為的重要組成部分[1],而配偶選擇是繁殖行為研究的重要內(nèi)容[2],是性選擇的重要方式[3],更是性選擇研究的中心問題[4]。配偶選擇是一性個體對另一性個體的主動選擇,大多數(shù)由雌性主導(dǎo)[3],并且具有較強的可塑性以適應(yīng)外界環(huán)境和內(nèi)部條件的變化。雌性配偶選擇能夠影響進化的強度和方向[5],有利于雌性獲得一些直接利益,如獲得所選雄性提供的一些資源、營養(yǎng)、保護或在后代撫育中提供的幫助,并且可以通過遺傳間接為后代獲取利益[6]。

雌性通常會選擇高質(zhì)量的雄性進行交配,以獲得更好的基因或具有吸引力的后代[7]。它們會根據(jù)不同的信號對雄性質(zhì)量進行評估,包括鳴聲、行為表現(xiàn)、信息素和形態(tài)學(xué)特征[8]。在雌性選擇為主導(dǎo)的配偶選擇中,雄鳥會通過鳴聲或其他信息吸引雌性,雌性根據(jù)信息對雄鳥質(zhì)量做出評價,最終選擇高質(zhì)量的雄性作為配偶[9]。鳴禽中,雄鳥鳴聲在吸引和刺激雌鳥中發(fā)揮重要作用[10]。許多鳥類偏愛較復(fù)雜鳴聲[10],如水蒲葦鶯(Acrocephalusschoenobaenus)[11],北美歌雀(Melospizamelodia)[12]等;有些雌性偏愛較大的鳴聲輸出,如歐洲椋鳥(Sturnusvulgaris)[13]、白喉帶鹀(Zonotrichiaalbicollis)[14]等。鳴聲是一種求愛信號,能夠向雌性成鳥傳遞求愛信息[15],具有物種特異性和個體差異[16- 18],為其用于物種識別、區(qū)分個體提供了基礎(chǔ)[19],是許多鳥類選擇同種個體作為配偶的重要依據(jù),對于鳥類物種的形成具有重要意義[20- 22]。與此同時,鳴聲也是雄性質(zhì)量的可靠指示器,有利于雌性選擇優(yōu)秀的雄性作為配偶[23- 24],提高繁殖成功率并獲得優(yōu)秀的子代,有利于種族的進化和延續(xù)[3]。

大多數(shù)動物生活在一個信息網(wǎng)絡(luò)中[25],個體可以通過“偷聽”獲得有用的信息,如競爭對手和潛在配偶的活力、地位和品質(zhì)等[25- 26]。在許多動物中,雄性都有通過“偷聽”從雄性-雄性競爭行為中收集信息的現(xiàn)象,如新疆歌鴝(Lusciniamegarhynchos)[27- 28]、泰國斗魚(Bettasplendens)[29]、大山雀(Parusmajor)[30]、金絲雀(Serinuscanaria)[31- 32]等。雌性也會在早期配偶選擇中通過“偷聽”對潛在配偶進行評估選擇,如泰國斗魚[33],日本鵪鶉(CoturnixJaponica)[34- 35],金絲雀[36- 37]等。在婚外交配嘗試中也有這一行為,如大山雀[38],黑冕山雀(Poecileatricapilla)[39]等。在“偷聽”行為發(fā)生的過程中,被偷聽者也會由于聽眾的存在而調(diào)節(jié)自身信息的行為,即“聽眾效應(yīng)(audience effects)”[40- 42]?！奥牨娦?yīng)”能夠隱藏[40]或突出[43]被偷聽者的某些信息,或降低信息的可信度[44]。例如在對雄性家養(yǎng)金絲雀在有雌性“聽眾效應(yīng)”下的婚外行為和同性攻擊行為的研究中發(fā)現(xiàn),雄性在“聽眾效應(yīng)”下會隱藏他們的婚外行為,但會增強他們的同性競爭行為[45],充分說明個體會在第三方偷聽的條件下適當調(diào)節(jié)自身的行為。

目前,絕大多數(shù)對“聽眾效應(yīng)”的研究主要集中于雌性配偶選擇中雌性“聽眾效應(yīng)”對雄-雄競爭行為的影響,而雄性“聽眾效應(yīng)”對雌-雌競爭行為的研究尚未開展。雌性配偶選擇研究對于研究動物的性選擇機制[6]和進化過程均具有重要意義[3,6]。以灰文鳥(Paddaoryzivora)為研究對象,從雄性鳴唱及雄性“聽眾效應(yīng)”對雌性配偶選擇的影響兩個方面展開研究?；椅镍B,雀形目,文鳥科,是一種常見觀賞鳥類,容易購買且實驗成本較低,適應(yīng)性強極易飼養(yǎng),適合實驗室養(yǎng)殖。雄鳥叫聲尖而長,雌鳥叫聲短促,聲音采集較為方便?；椅镍B繁殖周期短,且在北方地區(qū),秋、冬、春三季均可繁殖,產(chǎn)卵頻率高,育雛時間短,適宜作為模式物種進行實驗研究[46- 48]。

1　研究對象和研究方法

1.1研究對象

將10只沒有親緣關(guān)系的成年雄性灰文鳥與10只成年雌性灰文鳥隨機配對,所有個體均在實驗室孵化成長,具有繁殖經(jīng)驗,且之前從未進行過此類實驗[45]。每對鳥飼養(yǎng)在一個籠子(35cm×30cm×25cm)中,籠子中有供鳥自由采食的食槽和水槽,活動跳躍的塑料棲木,繁殖產(chǎn)卵的草編鳥巢。首先將10個鳥籠放置于同一房間中飼養(yǎng)7d,相互之間能夠看到和聽到,使其相互熟悉,以避免雌鳥對配偶和其他雄鳥熟悉程度的不同對實驗的影響,之后在15∶9(光照∶黑暗)的光照周期[49]下喂食灰文鳥發(fā)情飼料(雞蛋米)刺激其繁殖[47],使灰文鳥經(jīng)歷第1次繁育周期以鞏固配偶關(guān)系。第1次繁育周期過程中以塑料模型替換產(chǎn)下的卵,直到最后一枚卵產(chǎn)下一周后將巢移走[45],這樣可以使所有鳥共同開始第2次繁育周期,以避免第2次繁育周期開始時間不同可能對性選擇偏愛造成影響[50]。待灰文鳥開始第2次繁育時,即可開始實驗。

1.2實驗一雄鳥鳴唱對雌鳥配偶選擇的影響

圖1　實驗一中使用的雙向選擇裝置Fig.1　Two-way choice device used in experiment 1

在飼養(yǎng)環(huán)境下,使用HYUNDAI便攜式錄音筆對實驗所用到的10只雄鳥進行了鳴聲采集,以雄鳥做出求偶炫耀動作,并且雌鳥做出CSD反應(yīng)時的鳴唱作為求偶鳴唱,反之則為非求偶鳴唱。非求偶鳴唱句子時長(4.63±1.64)s(n=10),求偶鳴唱句子時長(7.75±2.06)s(n=10)。以格式工廠軟件對錄音進行了篩選、音量調(diào)節(jié)等處理后的錄音作為播放錄音。實驗時將雌鳥置于雙向選擇實驗裝置中,類似Collins等在研究中使用的裝置[51]。該實驗裝置是一個(15cm×90cm×15cm)的長方體實驗籠,籠子兩端及中心區(qū)域均有食槽和水槽,兩端各有一個播放器(圖1)。由于上午是鳥類鳴唱的高峰期,所以實驗每天從08:00開始。實驗開始后先將雌鳥置于裝置中10 min熟悉環(huán)境,之后兩端同時以先科多功能擴音器12 min內(nèi)無間隔連續(xù)播放錄音,其中一端播放其配偶鳴唱(求偶鳴唱或非求偶鳴唱),另一端播放非配偶鳴唱(求偶鳴唱或非求偶鳴唱)。為避免雌性偏側(cè)效應(yīng),每種播放組合在播放完畢后需顛倒播放并記錄,即按照隨機順序在實驗裝置兩端按以下組合方式均衡不同的鳴唱聲音：

(1) 灰文鳥雌鳥配偶的非求偶鳴唱與熟悉雄鳥的非求偶鳴唱;(2)配偶的非求偶鳴唱與熟悉雄鳥的求偶鳴唱;(3)配偶的求偶鳴唱與熟悉雄鳥的非求偶鳴唱;(4)配偶的求偶鳴唱與熟悉雄鳥的求偶鳴唱。

以雌鳥位置偏向一側(cè)并且面向這一側(cè)定義為積極偏愛[52]。播放開始后,給雌鳥2 min時間讓其定位,隨后觀察者于距離裝置1.5m的帷幕后[52]觀察記錄雌鳥的積極偏愛次數(shù),15s記錄1次,每組記錄10 min。通過比較雌鳥C偏向A、B兩個方向的積極偏愛次數(shù),確定雌鳥的偏愛選擇。

1.3實驗二灰文鳥雌-雌競爭

實驗前對實驗用鳥進行10h饑餓處理,將實驗雌鳥和競爭雌鳥放置到一個(35cm×30cm×25cm)籠即實驗籠中,中間以鐵絲網(wǎng)隔開,以避免其身體接觸。實驗籠旁放置一聽眾籠(15cm×15cm×15cm),適應(yīng)30 min后,撤去隔網(wǎng),投食開始后記錄。根據(jù)聽眾籠分為3個連續(xù)的實驗階段,即：(1)無聽眾,(2)一只熟悉雄性做聽眾(競爭對手的配偶),(3)雄性配偶做聽眾(競爭對手的熟悉雄性),每個階段均持續(xù)10 min。實驗中,允許實驗籠和聽眾籠中鳥的視覺和聽覺交流,通過記錄不同聽眾籠條件下雌性的攻擊行為次數(shù)來評估雌性的反映。攻擊行為包括掠食嘗試、防止掠食成功和反擊追逐。為避免實驗者偏向,觀察者并不知道聽眾的身份直到數(shù)據(jù)被分析[45]。

1.4數(shù)據(jù)處理

實驗一樣本容量等于30和實驗二樣本容量大于30,均可近似按正態(tài)分布處理。實驗一數(shù)據(jù)使用成對樣本T檢驗進行統(tǒng)計分析;實驗二數(shù)據(jù)以聽眾類別為自變量以攻擊行為次數(shù)為因變量進行單因素方差分析(One-way ANOVA),主要比較各方的均值關(guān)系及差異顯著性,統(tǒng)計性顯著水平設(shè)為0. 05。以上分析均使用統(tǒng)計軟件SPSS(version 17. 0)進行。

2　結(jié)果

2.1實驗一鳴唱對配偶選擇的影響2.1.1雌性偏愛鳴唱的類型和來源

雌性灰文鳥對配偶非求偶鳴唱的積極偏愛次數(shù)顯著高于非配偶非求偶鳴唱(t=2.959,P<0.05;圖2),對配偶求偶鳴唱的積極偏愛次數(shù)顯著高于非配偶非求偶鳴唱(t=7.681,P<0.05;圖2),對配偶求偶鳴唱的積極偏愛次數(shù)顯著高于非配偶求偶鳴唱(t=4.799,P<0.05;圖2),對配偶非求偶鳴唱的積極偏愛次數(shù)顯著低于非配偶求偶鳴唱(t=-3.192,P<0.05;圖2)。

圖2　雌性灰文鳥對不同類型的鳴唱的響應(yīng) (平均值±標準差)Fig.2　The female preference of different types of song (mean±SD)

2.1.2鳴唱類型對雌性偏愛的影響

雌性灰文鳥對配偶求偶和非求偶鳴唱的響應(yīng)會受到環(huán)境中非配偶鳴唱類型的影響。主要表現(xiàn)在：當一端播放配偶求偶鳴唱而另外一端分別播放非配偶求偶鳴唱或非配偶非求偶鳴唱時,雌性灰文鳥對配偶求偶鳴唱的積極偏愛次數(shù)在播放非配偶求偶鳴唱時要顯著低于播放非配偶非求偶鳴唱(t=-2.218,P<0.05;圖3);同樣,當一端播放配偶非求偶鳴唱,而另外一端分別播放非配偶求偶鳴唱或非配偶非求偶鳴唱時,雌性灰文鳥對配偶非求偶鳴唱的積極偏愛次數(shù)在播放非配偶求偶鳴唱時要顯著低于播放非配偶非求偶鳴唱(t=-3.645,P<0.05;圖3)。上述說明相比而言非配偶的求偶鳴唱比非求偶鳴唱更加具有吸引力,對雌鳥配偶選擇影響更大。

圖3　非配偶鳴唱類型對灰文鳥對配偶鳴唱響應(yīng)的影響(平均值±標準差)Fig.3　The effects of different song types of other males on the responses of females to the songs of their spouse (mean±SD)

2.1.3鳴唱品質(zhì)對雌鳥配偶選擇積極性的影響

雌鳥配偶選擇的積極性以每種實驗播放組合中雌性對裝置A、B兩端積極偏愛的總次數(shù)進行評估。當A、B兩端均播放求偶鳴唱(配偶求偶鳴唱+非配偶求偶鳴唱)時雌性對兩端鳴唱的總偏愛次數(shù)顯著高于只有一端播放求偶鳴唱(配偶求偶鳴唱+非配偶非求偶鳴唱,t=2.636,P<0.05;配偶非求偶鳴唱+非配偶求偶鳴唱,t=4.049,P<0.05;)時的總偏愛次數(shù);只有一端播放配偶求偶鳴唱(配偶求偶鳴唱+非配偶非求偶鳴唱)時雌性對兩端鳴唱的總偏愛次數(shù)顯著高于只有一端播放非配偶求偶鳴唱(配偶非求偶鳴唱+非配偶求偶鳴唱)時的總偏愛次數(shù)(t=2.437,P<0.05;)。當A、B兩端均播放非求偶鳴唱(配偶非求偶鳴唱+非配偶非求偶鳴唱)時雌性對兩端鳴唱的總偏愛次數(shù)最低,顯著低于其他條件下(P<0.05)。

2.2實驗二：雄鳥“聽眾效應(yīng)”對雌-雌競爭的影響

圖4　不同聽眾類別條件下雌鳥所表現(xiàn)出的攻擊行為(平均值±標準差)Fig.4　Agonistic behaviours expressed by females according to the presented audience (mean±SD)

應(yīng)用單因素分析(One-way ANOVA)對不同聽眾條件下的雌-雌競爭進行了對比。分析發(fā)現(xiàn)：雌鳥的攻擊行為受到聽眾條件的顯著影響(F=11.72,P< 0.001;圖4)。在配偶雄性作為聽眾條件下雌鳥攻擊行為最高,顯著高于熟悉雄性為聽眾的條件下,并且兩者都顯著高于無聽眾條件下雌鳥的攻擊行為(圖4)。

3　討論

本研究中,在配偶鳴唱和非配偶鳴唱之間,雌性灰文鳥更偏愛自身配偶的鳴唱,而非其他雄鳥的鳴唱,說明灰文鳥能夠根據(jù)鳴唱識別雄性個體。許多研究已證明鳥類對同種鳴聲具有分辨能力,如大山雀[53],虎皮鸚鵡(Melopsittacusundulatus)[54]和斑胸草雀(Poephilaguttata)[55]等。鳴聲結(jié)構(gòu)的復(fù)雜性和多樣性既具有種屬特征,也存在普遍的個體差異[56],這種個體差異是雌性灰文鳥根據(jù)鳴唱識別個體的關(guān)鍵。本實驗中,灰文鳥對配偶鳴唱的偏愛顯著較高,一方面是由于配偶關(guān)系的存在,另一方面可能是由于配偶鳴唱對雌鳥的作用時間更長,雌鳥對配偶鳴唱的感知和分辨更加靈敏。

在配偶的非求偶鳴唱和非配偶的求偶鳴唱之間,雌性更偏愛非配偶的求偶鳴唱,可能是由于求偶鳴唱能夠反映出雄鳥較高的質(zhì)量[24]。相對于非求偶鳴唱而言,求偶鳴唱對雌性配偶選擇的影響更大：非配偶的求偶鳴唱比非求偶鳴唱更能減弱雌性對配偶鳴唱的偏愛(圖3),說明求偶鳴唱比非求偶鳴唱更能吸引雌鳥,對雌性配偶選擇的影響更大。Forstmeier等對褐柳鶯(Phylloscopusfuscatus)的研究中發(fā)現(xiàn)褐柳鶯對鳴曲的偏愛可能與雄性鳴唱的音節(jié)類型和鳴唱方式有關(guān)[57]。雌鳥更加偏愛于那些具有性感音節(jié)、鳴唱難度大的鳴唱。由于雄鳥求偶鳴唱和非求偶鳴唱擔(dān)負著不同的功能,而求偶鳴唱的音節(jié)結(jié)構(gòu)復(fù)雜,具有更多的性感音節(jié),鳴唱難度更大,能夠傳遞求愛信號,因而更能吸引雌性灰文鳥,對雌性配偶選擇的影響更大;而配偶的非求偶鳴唱的音節(jié)結(jié)構(gòu)簡單,具有更少的性感音節(jié),鳴唱難度較低,對雌性灰文鳥鳴唱偏愛和配偶選擇的影響較小。這一研究結(jié)果說明,當鳴唱作為雌鳥評估雄鳥質(zhì)量的標準時,擁有結(jié)構(gòu)復(fù)雜的性感音節(jié)和鳴唱難度大的求偶鳴唱,更有可能成為雌鳥配偶選擇和婚外嘗試的誘因之一。

本研究還發(fā)現(xiàn)求偶鳴唱能夠刺激雌性灰文鳥配偶選擇的積極性,性選擇中雄性通過競爭爭奪配偶,雌性對雄性進行評估選擇配偶,因此在雌性主導(dǎo)的配偶選擇中雌性成為積極的一方[8]。不積極可能對雌鳥有利,因為這樣可以減少尋找潛在配偶所投入的資源和時間[58],因而在兩端均播放非求偶鳴唱時雌鳥顯得最不積極,因為這些鳴唱不值得雌鳥花費時間評估,而在播放求偶鳴唱時雌鳥變得積極,這樣有利于雌鳥選擇優(yōu)質(zhì)的配偶。盡管這意味著要投入更多的資源和時間,但總體而言這對雌鳥是有利的。兩端均播放求偶鳴唱時雌鳥比僅在一端播放求偶鳴唱時更加積極,是因為這時可供選擇的鳴唱更多,雌鳥需要對兩種鳴唱均進行評估,因而更加積極。我們還發(fā)現(xiàn),雌性個體在只播放配偶求偶鳴唱時比只播放非配偶求偶鳴唱時更加積極,這可能是由于求偶行為能夠刺激雌性性欲[59],而求偶鳴唱是求偶行為的重要組成,所以在求偶鳴唱條件下雌性交配欲望更加強烈。而配偶的求偶鳴唱比非配偶的求偶鳴唱更能刺激雌鳥交配欲望,因而表現(xiàn)得更加積極。

很多情況下配偶選擇由雌性主導(dǎo)。雌性能夠觀察雄-雄競爭對配偶及婚外潛在配偶進行評估,雄性會根據(jù)雌性聽眾的不同適當調(diào)節(jié)自身行為,這種現(xiàn)象即為“聽眾效應(yīng)”[45]。目前對“聽眾效應(yīng)”的研究主要集中在雌性“聽眾效應(yīng)”對配偶選擇的影響,如Price等對孔雀魚(Poeciliareticulata)[60]和Tachon等對黃斑黑蟋蟀(Gryllusbimaculatus)[61]的研究均發(fā)現(xiàn)雄性在雌性“聽眾效應(yīng)”下攻擊行為增強。而在鳥類中也有這種現(xiàn)象,如Baltz等對虎皮鸚鵡研究中發(fā)現(xiàn)雌性“聽眾效應(yīng)”下雄性會收斂婚外行為[62],而Davy Ung等對金絲雀的研究中也發(fā)現(xiàn)在雌性“聽眾效應(yīng)”條件下雄性會收斂婚外行為,雄-雄競爭行為增強[45]。本研究發(fā)現(xiàn)雌-雌競爭也受到“聽眾效應(yīng)”的影響,在有聽眾條件下的攻擊行為明顯高于無聽眾條件的攻擊行為;而在配偶聽眾條件下,雌性的攻擊明顯高于熟悉雄性聽眾條件下的攻擊行為。這一發(fā)現(xiàn)與Davy Ung等對雌性“聽眾效應(yīng)”對雄性家養(yǎng)金絲雀雄-雄競爭影響[45]的結(jié)果類似。雌性在雄性“聽眾效應(yīng)”影響下雌-雌競爭行為明顯增強,可能與雄-雄競爭配偶類似,雄性也可以通過偷聽雌-雌競爭對雌鳥品質(zhì)進行評估選擇配偶。自然界條件下,配偶爭奪多是雄性個體之間競爭雌性個體,同樣雌性個體也會相互競爭爭奪配偶[63],如斑腹磯鷸(Actitismacularia)[64- 65],海馬(Hippocampus)[66]等,從而與多個雄性交配中獲得直接或間接的利益[67- 68]。配偶雄性“聽眾效應(yīng)”下的雌-雌競爭行為明顯高于熟悉雄性“聽眾效應(yīng)”下的雌-雌競爭行為,原因可能是配偶做聽眾條件下,如果競爭失敗將付出更大的的代價,她們將失去與更多雄鳥的交配機會。鳥類在野生環(huán)境下的雌-雌競爭還有待于進一步的研究。

4　結(jié)論

鳴唱在灰文鳥配偶選擇中發(fā)揮著重要作用,雌性灰文鳥更加偏愛配偶鳴唱,說明求偶鳴唱和非求偶鳴唱均具有個體識別功能。但相對于配偶的非求偶鳴唱雌鳥更加偏愛于非配偶的求偶鳴唱,求偶鳴唱比非求偶鳴唱更能吸引雌性灰文鳥,說明求偶鳴唱具有吸引雌性的作用,而且這有可能會成為婚外行為發(fā)生的誘因之一?？晒┻x擇的求偶鳴唱更多時雌性變得更加積極,而求偶鳴唱能夠刺激雌性灰文鳥配偶選擇的積極性,可能與求偶鳴唱能夠刺激雌鳥性欲有關(guān)。雌性灰文鳥會由于雄性“聽眾效應(yīng)”對雌-雌競爭行為做出適當調(diào)整,但是否是由于雄鳥會根據(jù)雌-雌競爭對雌性灰文鳥進性評估進而選擇交配對象,還需進一步研究。

[1]鄭光美, 張正旺. 鳥類生態(tài)學(xué)的發(fā)展趨勢. 動物學(xué)雜志, 1989, 24(4): 43- 45, 54- 54.

[2]尚玉昌. 行為生態(tài)學(xué). 北京: 北京大學(xué)出版社, 1998: 20- 29, 141- 149, 240- 270.

[3]尚玉昌. 動物行為研究的新進展 (六): 性選擇和配偶選擇. 自然雜志, 2013, 35(3): 207- 210.

[4]Frame A M, Mills A F. Condition-dependent mate choice: A stochastic dynamic programming approach. Theoretical Population Biology, 2014, 96: 1- 7.

[5]Atwell A, Wagner W E Jr. Female mate choice plasticity is affected by the interaction between male density and female age in a field cricket. Animal Behaviour, 2014, 98: 177- 183.

[6]張建軍, 張知彬. 動物的性選擇. 生態(tài)學(xué)雜志, 2003, 22(4): 60- 64.

[7]Kirkpatrick M. Sexual selection by female choice in polygynous animals. Annual Review of Ecology and Systematics, 1987, 18: 43- 70.

[8]Andersson M. Sexual Selection. Princeton: Princeton University Press, 1994.

[9]Dunning J L, Pant S, Bass A, Coburn Z, Prather J F. Mate choice in adult female bengalese finches: females express consistent preferences for individual males and prefer female-directed song performances. PLoS One, 2014, 9(2): e89438.

[10]Catchpole C K, Slater P J B. Bird Song: Biological Themes and Variations. Cambridge: Cambridge University Press, 1995.

[11]Catchpole C K, Dittami J, Leisler B. Differential responses to male song repertoires in female songbirds implanted with oestradiol. Nature, 1984, 312(5994): 563- 564.

[12]Searcy W A, Marler P. A test for responsiveness to song structure and programming in female sparrows. Science, 1981, 213(4510): 926- 928.

[13]Eens M, Pinxten R, Verheyen R F. Male song as a cue for mate choice in the European starling. Behaviour, 1991, 116(3): 210- 238.

[14]Wasserman F E, Cigliano J A. Song output and stimulation of the female in white-throated sparrows. Behavioral Ecology and Sociobiology, 1991, 29(1): 55- 59.

[15]Hernandez A M, Phillmore L S, MacDougall-Shackleton S A. Effects of learning on song preferences and Zenk expression in female songbirds. Behavioural processes, 2008, 77(2): 278- 284.

[16]Marler P. Bird songs and mate selection // Lanyon W E, Tavolga W, eds. Animal Sounds and Communication. Washington: American Institute of Behavioral Science, 1960: 348- 367.

[17]Baker M C. Vocal dialect recognition and population genetic consequences. American Zoologist, 1982, 22(3): 561- 569.

[18]Lambrechts M M, Dhondt A A. Individual voice discrimination in birds. Current Ornithology, 1995, 12: 115- 139.

[19]王愛真, 雷富民, 賈志云. 雌性選擇與雄鳥鳴唱的進化. 動物學(xué)研究, 2003, 24(4): 305- 310.

[20]Ptacek M B. The role of mating preference in shaping interspecific divergence in mating signal s in vertebrates. Behavioural Processes, 2000, 51(1/3): 111- 134.

[21]雷富民. 鳥類鳴聲結(jié)構(gòu)地理變異及其分類學(xué)意義. 動物分類學(xué)報, 1999, 24(2): 232- 240.

[22]雷富民, 王鋼. 鳥類鳴聲行為對其物種分化和新種形成影響. 動物分類學(xué)報, 2002, 27(3): 641- 648.

[23]Vallet E, Beme I, Kreutzer M. Two-note syllables in canary songs elicit high levels of sexual display. Animal Behaviour, 1998, 55(2): 291- 297.

[24]Zahavi A. Mate selection—a selection for a handicap. Journal of Theoretical Biology, 1975, 53(1): 205- 214.

[25]Kroodsma D E, Miller E H. Ecology and evolution of acoustic communication in birds. Comstock: Cornell University Press, 1996: 409- 425.

[26]Mcgregor P K. Animal communication networks. Cambridge: Cambridge University Press, 2005.

[27]Naguib M, Todt D. Effects of dyadic vocal interactions on other conspecific receivers in nightingales. Animal Behaviour, 1997, 54(6): 1535- 1543.

[28]Naguib M, Fichtel C, Todt D. Nightingales respond more strongly to vocal leaders of simulated dyadic interactions. Proceedings of the Royal Society of London. Series B: Biological Sciences, 1999, 266(1419): 537- 542.

[29]Oliveira R F, McGregor P K, Latruffe C. Know thine enemy: fighting fish gather information from observing conspecific interactions. Proceedings of the Royal Society of London. Series B: Biological Sciences, 1998, 265(1401): 1045- 1049.

[30]Peake T M, Terry A M R, McGregor P K, Dabelsteen T. Male great tits eavesdrop on simulated male-to-male vocal interactions. Proceedings of the Royal Society of London. Series B: Biological Sciences, 2001, 268(1472): 1183- 1187.

[31]Amy M, Leboucher G. Male canaries can visually eavesdrop on conspecific food interactions. Animal Behaviour, 2007, 74(1): 57- 62.

[32]Amy M, Leboucher G. Effects of eavesdropping on subsequent signalling behaviours in male canaries. Ethology, 2009, 115(3): 239- 246.

[33]Doutrelant C, McGregor P K. Eavesdropping and mate choice in female fighting fish. Behaviour, 2000, 137(12): 1655- 1668.

[34]Ophir A G, Galef Jr B G. Female Japanese quail that ‘eavesdrop’ on fighting males prefer losers to winners. Animal Behaviour, 2003, 66(2): 399- 407.

[35]Ophir A G, Persaud K N, Galef Jr B G. Avoidance of relatively aggressive male Japanese quail (Coturnixjaponica) by sexually experienced conspecific females. Journal of Comparative Psychology, 2005, 119(1): 3- 7.

[36]Leboucher G, Pallot K. Is he all he says he is? Intersexual eavesdropping in the domestic canary,Serinuscanaria. Animal Behaviour, 2004, 68(4): 957- 963.

[37]Amy M, Monbureau M, Durand C, Gomez D, Thery M, Leboucher G. Female canary mate preferences: differential use of information from two types of male-male interaction. Animal Behaviour, 2008, 76(3): 971- 982.

[38]Otter K, McGregor P K, Terry A M R, Burford F R L, Peake T M, Dabelsteen T. Do female great tits (Parusmajor) assess males by eavesdropping? A field study using interactive song playback. Proceedings of the Royal Society of London. Series B: Biological Sciences, 1999, 266(1426): 1305- 1309.

[39]Mennill D J, Ratcliffe L M, Boag P T. Female eavesdropping on male song contests in songbirds. Science, 2002, 296(5569): 873- 873.

[40]Doutrelant C, McGregor P K, Oliveira R F. The effect of an audience on intrasexual communication in male Siamese fighting fish,Bettasplendens. Behavioral Ecology, 2001, 12(3): 283- 286.

[41]Matos R J, Schlupp I. Performing in front of an audience: signallers and the social environment // McGregor P K, ed. Animal Communication Networks. Cambridge: Cambridge University Press, 2005: 63- 83.

[42]McGregor P K, Peake T M. Communication networks: social environments for receiving and signalling behaviour. Acta Ethologica, 2000, 2(2): 71- 81.

[43]Bitetti M S D. Food-associated calls and audience effects in tufted capuchin monkeys,Cebusapellanigritus. Animal Behaviour, 2005, 69(4): 911- 919.

[44]Plath M, Blum D, Schlupp I, Tiedemann R. Audience effect alters mating preferences in a livebearing fish, the Atlantic molly,Poeciliamexicana. Animal Behaviour, 2008, 75(1): 21- 29.

[45]Ung D, Amy M, Leboucher G. Heaven it′s my wife! Male canaries conceal extra-pair courtships but increase aggressions when their mate watches. PLoS One, 2011, 6(8): e22686.

[46]陳云霜. 灰文鳥的飼養(yǎng). 園林, 1999, 6: 41- 41.

[47]李順才, 張坤. 灰文鳥的人工養(yǎng)殖技術(shù). 中國家禽, 2004, 26(10): 26- 27.

[48]徐磊. 灰文鳥的飼養(yǎng)與繁殖. 特種經(jīng)濟動植物, 2004, (4): 13- 13.

[49]Follett B K, Hinde R A, Steel E, Nicholls T J. The influence of photoperiod on nest building, ovarian development and luteinizing hormone secretion in canaries (Serinuscanarius). Journal of Endocrinology, 1973, 59(1): 151- 162.

[50]Beguin N, Leboucher G, Bruckert L, Kreutzer M. Mate preferences in female canaries (Serinuscanaria) within a breeding season. Acta Ethologica, 2006, 9(2): 65- 70.

[51]Collins S A, Hubbard C, Houtman A M. Female mate choice in the zebra finch—the effect of male beak colour and male song. Behavioral Ecology and Sociobiology, 1994, 35(1): 21- 25.

[52]Rutstein, A N, Brazill-Boast J, Griffith S C. Evaluating mate choice in the zebra finch. Animal Behavior, 2007, 74(5): 1277- 1284

[53]Weary D M. Categorical perception of bird song: How do great tits (Parusmajor) perceive temporal variation in their song?. Journal of Comparative Psychology, 1989, 103(4): 320- 325.

[54]Okanoya K, Dooling R J. Perception of distance calls by budgerigars (Melopsittacusundulatus) and zebra finches (Poephilaguttata): Assessing species-specific advantages. Journal of Comparative Psychology, 1991, 105(1): 60- 72.

[55]Cynx J. Conspecific song perception in zebra finches (Taeniopygiaguttata). Journal of Comparative Psychology, 1993, 107(4): 395- 402.

[56]Weeden J S, Falls J B. Differential responses of male ovenbirds to recorded songs of neighboring and more distant individuals. The Auk, 1959, 76(3): 343- 351.

[57]Forstmeier W, Kempenaers B, Meyer A, Leisler B. A novel song parameter correlates with extra-pair paternity and reflects male longevity. Proceedings of the Royal Society of London. Series B: Biological Sciences, 2002, 269(1499): 1479- 1485.

[58]Cotton S, Small J, Pomiankowski A. Sexual selection and condition-dependent mate preferences. Current Biology, 2006, 16(17): R755-R765.

[59]邵明勤, 阿布力米提·阿布都卡迪爾, 高行宜, 孫銘娟. 鳥類行為研究進展. 干旱區(qū)研究, 2002, 19(2): 75- 80.

[60]Price A C, Rodd F H. The effect of social environment on male-male competition in guppies (Poeciliareticulata). Ethology, 2006, 112(1): 22- 32.

[61]Tachon G, Murray A M, Gray D A, Cade W H. Agonistic displays and the benefits of fighting in the field cricket,Gryllusbimaculatus. Journal of Insect Behavior, 1999, 12(4): 533- 543.

[62]Baltz A P, Clark A B. Extra-pair courtship behaviour of male budgerigars and the effect of an audience. Animal Behaviour, 1997, 53(5): 1017- 1024.

[63]Clutton-Brock T. Sexual selection in females. Animal Behaviour, 2009, 77(1): 3- 11.

[64]Oring L W, Colwell M A, Reed J M. Lifetime reproductive success in the spotted sandpiper (Actitismacularia): sex differences and variance components. Behavioral Ecology and Sociobiology, 1991, 28(6): 425- 432.

[65]Oring L W, Reed J M, Colwell M A, Lank D B, Maxson S J. Factors regulating annual mating success and reproductive success in spotted sandpipers (Actitismacularia). Behavioral Ecology and Sociobiology, 1991, 28(6): 433- 442.

[66]Kvarnemo C, Moore G I, Jones A G. Sexually selected females in the monogamous Western Australian seahorse. Proceedings of the Royal Society of London, Series B: Biological Sciences, 2007, 274(1609): 521- 525.

[67]Tregenza T, Wedell N. Benets of multiple mates in the cricketGryllusbimaculatus. Evolution, 1998, 52(6): 1726- 1730.

[68]Fisher D O, Double M C, Blomberg S P, Jennions M D, Cockburn A. Post-mating sexual selection increases lifetimetness of polyandrous females in the wild. Nature, 2006, 444(7115): 89- 91.

Effects of “audience effects” and song on femalePaddaoryzivoramate choice behavior

ZHANG Xiande, XU Tingting, ZHAO Tingting, WAN Dongmei, YIN Jiangxia*

KeyLaboratoryofAnimalResourceandEpidemicDiseasePrevention,DepartmentofLifeSciences,LiaoningUniversity;Liaoning,Shenyang110036,China

Mate choice is one of the most important aspects of sexual selection, and uncovering the mechanisms behind mate choice is a central issue in sexual selection studies. Females choose high-quality males as mates to obtain direct benefits such as resources, nutrition, and protection, and in doing so they acquire indirect genetic benefits for future generations. Further studies of female mate choice would improve our understanding of sexual selection and evolutionary processes. Song is one of the most important secondary sexual characteristics in birds and can reflect male territory quality and genetic and physiological status. Females can extract information about male quality by assessing their songs, and more complex songs are preferred over simple ones. Birds inhabit a communication network in which individuals can assess the quality of potential mates by visual and auditory observation of their interactions. In addition, individuals being observed may adjust their signaling behavior. Audience effects are defined as changes in signaling behavior of an individual engaged in an interaction due to the presence of an audience consisting of a conspecific witnessing the interaction. To date, studies of sexual selection have mainly focused on the driving factors of mate choice and on female audience effects on female-female competition. In contrast, there is limited knowledge about the effects of bird song on mate choice and about male audience effects on female-female competition. Here, we investigated the effects of male song on female mate choice and the male audience effect on female-female competition inPaddaoryzivora. In the first part of the study, we used a two-way choice device and stimulated the female by courtship or other songs of a spouse and other males, and we observed female song preference. In the second part of the study, females were observed under three conditions: (a) in the absence of an audience, (b) in the presence of a familiar male, and (c) in the presence of a mate. Our results showed that femaleP.oryzivorapreferred the spouse′s song and preferred courtship songs of other males to the non-courtship song of their mates. The courtship song was more attractive than other songs, and its effects were much stronger in stimulating positive female mate choice. The courtship chirp caused a positive response in the female. Females expended more time and resources, but also benefited more, by selecting higher-quality mates. FemaleP.oryzivorawere more aggressive in the presence than in the absence of a male and were more aggressive in the presence of the mate than in the presence of a familiar male. Females appropriately adjust female-female competition behavior when under the male audience effect; whether this is a result of males choosing mates by observing this competition remains to be examined, as does female-female competition in the wild. These results improve our understanding of the underlying mechanism of mate choice behavior in birds.

Paddaoryzivora; mate choice; bird song; positivity; audience effects; female-female competition

國家自然科學(xué)基金項目(31100271)

2015- 01- 29; 網(wǎng)絡(luò)出版日期:2015- 11- 30

Corresponding author.E-mail: yinjiangxia@gmail.com

10.5846/stxb201501290238

張憲德,徐婷婷,趙婷婷,萬冬梅,殷江霞.配偶選擇中“聽眾效應(yīng)”及鳴唱對雌性灰文鳥行為的影響.生態(tài)學(xué)報,2016,36(16):5247- 5255.

Zhang X D, Xu T T, Zhao T T, Wan D M, Yin J X.Effects of “audience effects” and song on femalePaddaoryzivoramate choice behavior.Acta Ecologica Sinica,2016,36(16):5247- 5255.