小丑箭毒蛙 (Oophaga granulifera)紅色型 photo: ARKive

標題：NOT EVERYTHING IS BLACK AND WHITE: COLOR AND BEHAVIORAL VARIATION REVEAL A CONTINUUM BETWEEN CRYPTIC AND APOSEMATIC STRATEGIES IN A POLYMORPHIC POISON FROG

摘要

Aposematism and crypsis are often viewed as two extremes of a continuum of visual conspicuousness to predators. Theory predicts that behavioral and coloration conspicuousness should vary in tandem along the conspicuousness spectrum for antipredator strategies to be effective. Here we used visual modeling of contrast and behavioral observations to examine the conspicuousness of four populations of the granular poison frog, Oophaga granulifera, which exhibits almost continuous variation in dorsal color. The patterns of geographic variation in color, visual contrast, and behavior support a gradient of overall conspicuousness along the distribution of O. granulifera. Red and green populations, at the extremes of the color distribution, differ in all elements of color, contrast, and behavior, strongly reflecting aposematic and cryptic strategies. However, there is no smooth cline in any elements of behavior or coloration between the two extremes. Instead populations of intermediate colors attain intermediate conspicuousness by displaying different combinations of aposematic and cryptic traits. We argue that coloration divergence among populations may be linked to the evolution of a gradient of strategies to balance the costs of detection by predators and the benefits of learned aversion.

大山雀 (Great tit, Parus major) (wiki)

標題：How do predators learn to recognize a mimetic complex: Experiments with naive great tits and aposematic heteroptera.
摘要

We tested the importance of innate wariness, avoidance learning, memory and generalization for the formation of predatory behaviour in naive great tits (Parus major) towards mimetic complex of four aposematic species of true bugs (Insecta: Hemiptera: Heteroptera): Lygaeus equestris, Spilostethus saxatilis, Pyrrhocoris apterus and Graphosoma lineatum. The birds showed almost no innate wariness against the aposematically coloured bugs, although a hidden wariness elicited by defensive chemicals of some of the bug species is not excluded. Naive birds learned to avoid different species at different rates, which resulted in different prey mortalities. The avoidance learning was faster when the defensive chemicals produced an immediate irritating effect (particularly when squirted into distance – G. lineatum) than when they caused sickness several minutes after the consumption (P. apterus). The experience of birds from learning to avoid a particular species of bug affected their subsequent behaviour to other species – experience with better-defended species resulted in longer attack latencies, more cautious attacks, broader generalization and lower prey mortality. The least defended species, P. apterus, benefited from the experience of birds with better-defended species, whereas the birds’ experience with P. apterus did not reduce mortality risk of the other species comparably. Judging from the inexperienced young birds, the mimetic relation- ships are likely to be quasi-Batesian. However, as wild-caught great tits avoid all the four species to the same extent, the relationships may become more mutualistic (quasi-Müllerian) in later phases of learning under natural conditions. The relationships among species in the mimetic complex thus seem to depend on the amount of experience of the bird predators.

雖然很多討論擬態的文章以行為學的實驗來驗證假設，最常使用的是大山雀、藍山雀與家雞，除了好生好養好抓，對這種鳥的習性瞭解，更重要的行為學家認為這可以代表鳥類的捕食者。但有意思的是，雖然做過這麼多實驗，真的討論這些鳥種的基礎認知行為的證據似乎都很間接，通常是某個實驗做完後順便討論一下「這個鳥似乎天生有點怕某個東西」，因此雖然做了這麼多實驗，仍有許多的現象與理論發生衝突，有沒有可能因為對於我們所使用的鳥種還不夠瞭解？

大山雀亞成鳥 photo: Clarke Brunt

作者群因此想知道捕食者的辨識警戒性/擬態的重要認知因子的基礎能力，像是天然呆(X)，天生的警覺性(O)，避免再次吃到難吃獵物的學習力，記憶力，與概括認知能力等，最常採用討論相關理論的大山雀 (Parus major) 自然就是討論的目標首選。作者群讓完全沒有經驗，天真無邪的大山雀攻擊四種椿象：Lygaeus equuestris, Spilostethus saxatilis, Pyrrhocoris apterus, Graphosoma lineatum。這類的椿象大多具有紅黑條紋，體內有防禦機制，有些種類被攻擊時還會放出臭氣讓捕食者避忌。就這四種椿象來說的話，其防禦的程度P. apterus的臭氣是最低的。作者群25隻手養的大山雀，飼養過程中符合動物福利原則，在飼養的過程中餵食麵包蟲、家蟋蟀、食蟲鳥類綜合飼料、綠色與褐色的昆蟲(野外抓)、水煮蛋與維他命，確保幼鳥能取得多類型的營養平安又健康的長大，又不會被飼養中某些特殊顏色影響學習經驗。等到這些鳥長大到40-60天時，就開始進行實驗。實驗進行主要分為兩個部分：第一天是「避忌學習」(avoidance learning)，第二天是「概括學習」(generalization)。避免學習的實驗讓鳥試著學習避免上述四種椿象之一，然後在概括學習中同時呈現四種椿象。

Fig. 1 實驗中討論的四種椿象，與其在系統發生學上的特徵與相對親緣關係。

結果顯示這些鳥幾乎對這些警戒色沒有任何天生的警覺性（天然呆？），但對某些防禦性化學物質有警覺。這些天真的鳥對不同椿象的學習速度都不一樣。在「避忌學習」的結果中，會放出防禦性化學物的物種G. lineatum，能讓鳥學的比咬下去才知道難吃的學的快(P. apterus)。這些鳥基於學到的經驗，對於接下來的行為產生改變：有很難吃經驗的個體，在面對類似的警戒色時，攻擊延遲時間會比較長，更多謹慎的攻擊，讓這些獵物的死亡率較低。而這些椿象中防禦性最低的P. apterus，受惠於那些有過很難吃經驗的個體，反之，若鳥沒經歷過那些很難吃的，P. apterus的死亡率沒有顯著的降低。綜合以上的結果來看，這些椿象看起來像是準貝氏擬態(quasi-Batesian mimicry)的關係，但從野外抓回來的鳥的實驗來看，對於四種椿象都有避忌行為，因此作者群認為大山雀在野外學習到最後，會讓椿象的關係比較接近準穆氏擬態(quasi-Müllerian mimicry)。

這個實驗結果部分的揭開大山雀這個實驗物種的學習經歷，與這對警戒性/擬態物種的影響，但仍有些問題存在。像是其實我們對於鳥類的大腦發育與學習不如人類瞭解，手養鳥雖然可以避免某些額外的因子，但有沒有可能在飼養的過程中大腦的發育與認知就已經被限制，許多的飼養觀察也指出，手養鳥與野生鳥的行為差異極大，前兩年也有篇Nature的文章指出，實驗室飼養的果蠅比起野外的果蠅行為單一許多。這讓我們不得不考慮用手養鳥究竟是不是能解釋實驗動物的天生行為，但如果不手養，又有沒有什麼辦法測試這些內在因素？

而這樣的試驗是否又告訴我們，未來若要採用新的實驗動物前，必須要先瞭解動物的「內心」，才能進行進一步的試驗？

photo: Encyclopedia of Science

標題：Stimulus Salience as an Explanation for Imperfect Mimicry The theory of mimicry explains how a mimic species gains advantage by resembling a model species [1–3]. Selection for increased mimic-model similarity should then result in accurate mimicry, yet there are many surprising examples of poor mimicry in the natural world [4–8]. The existence of imperfect mimics remains a major unsolved conundrum. We propose and experimentally test a novel explanation of the phenomenon. We argue that predators perceive prey as having several traits, but that the traits differ in their importance for learning. When predators learn to discriminate prey, high-salience traits overshadow other traits, leaving them under little or no selection for similarity, and allow imperfect mimicry to succeed. We tested this idea experimentally, using blue tits as predators and artificial prey with three prominent traits: color, pattern, and shape. We found that otherwise imperfect color mimics were avoided about as much as perfect mimics, whereas pattern and shape mimics did not gain from their similarity to the model. All traits could separately be perceived and learned by the predators, but the color trait was learned at a higher rate, implying that it had higher salience. We conclude that difference in salience between components of prey appearance is of major importance in explaining imperfect mimicry.

Fig. 1 實驗中設計的有報酬與沒報酬的人工符號

Fig. S1 實際上進行的實驗設計

實驗中使用的捕食者藍山雀 (Cyanistes caeruleus) photo: rspb

標題：Hierarchical overshadowing of stimuli and its role in mimicry evolution

photo from content

標題：Multi-trait mimicry and the relative salience of individual traits

摘要

Mimicry occurs when one species gains protection from predators by resembling an unprofitable model species. The degree of mimic–model similarity is variable in nature and is closely related to the number of traits that the mimic shares with its model. Here, we experimentally test the hypothesis that the relative salience of traits, as perceived by a predator, is an important determinant of the degree of mimic–model similarity required for successful mimicry. We manipulated the relative salience of the traits of a two-trait artificial model prey, and subsequently tested the survival of mimics of the different traits. The unrewarded model prey had two colour traits, black and blue, and the rewarded prey had two combinations of green, brown and grey shades. Blue tits were used as predators. We found that the birds perceived the black and blue traits to be similarly salient in one treatment, and mimic–model similarity in both traits was then required for high mimic success. In a second treatment, the blue trait was the most salient trait, and mimic–model similarity in this trait alone achieved high success. Our results thus support the idea that similar salience of model traits can explain the occurrence of multi-trait mimicry.

photo from The Haunted Pen

警戒性的物種身上通常會有不只一個顏色，而是透過複合式的顏色組合成某種「樣式」，形成強烈的對比色，這個樣式會讓捕食者產生警醒的認知，避免捕食這類的獵物。可是若扯到兩個物種間的擬態就比較複雜了，因為警戒性的物種若成為model，可是身上的顏色不只一種，那麼有作用的是哪個部分，而mimic只會演化出有用的又明顯的那個部分嗎？或是必須拷貝整體的「樣式」才有用呢？

這個研究利用人工的模型，與藍山雀做為捕食者討論這個問題。作者設定的警戒色是「藍＋黑」，選擇藍色是為了避免藍山雀因為以前的經驗影響實驗結果。實驗設計如上圖，主要分為兩個部分，一個測試整體認知，一個測試顏色突出認知，其中設計以藍色是最為明顯的顏色，兩個部分都有1對1與1對多的設計。第一個結果顯示mimic的對比度與「藍+黑」最接近的最為成功，第二個結果顯示對比度與藍色最接近的最成功。這證據支持mimic的顏色突出度必須與model接近才有可能降低天擇的選汰。

如果這樣就有趣了，意思就是mimic的斑紋演化上來說，無法先變出A部分再變出B部分，看起來是必須整體同時出現，也就是題目所說的「複合式」斑紋。那麼如果不是像毒蝶那樣可以透過基因滲透傳遞性狀的族群，要如何一次性的出現相似的斑紋呢？這個研究的結果是不是比較支持「兩步演化」理論（two-step theory）呢？

標題：PREDATOR PERCEPTION OF BATESIAN MIMICRY AND CONSPICUOUSNESS IN A SALAMANDER

摘要

In Batesian mimicry a palatable mimic deceives predators by resembling an unpalatable model. The evolution of Batesian mimicry relies on the visual capabilities of the potential predators, as prey detection provides the selective force driving evolutionary change. We compared the visual capabilities of several potential predators to test predictions stemming from the hypothesis of Batesian mimicry between two salamanders: the model species Notophthalmus viridescens, and polymorphic mimic, Plethodon cinereus. First, we found mimicry to be restricted to coloration, but not brightness. Second, only bird predators appeared able to discriminate between the colors of models and nonmimic P. cinereus. Third, estimates of salamander conspicuousness were background dependent, corresponding to predictions only for backgrounds against which salamanders are most active. These results support the hypothesis that birds influence the evolution of Batesian mimicry in P. cinereus, as they are the only group examined capable of differentiating N. viridescens and nonmimetic P. cinereus. Additionally, patterns of conspicuousness suggest that selection from predators may drive the evolution of conspicuousness in this system. This study confirms the expectation that the visual abilities of predators may influence the evolution of Batesian mimicry, but the role of conspicuousness may be more complex than previously thought.

對擬態/警戒性的物種來說，重要的是這些顏色相對於背景來說夠不夠明顯，捕食者能不能看見，進而產生知覺的連結，費心經過天擇篩選出來的體色才能在自然界中綻放其光彩。

這個研究就在測試這個簡單的概念，對象是分佈於北美洲的火焰蠑螈 (Notophthalmus viridescens)與紅背蠑螈 (Plethodon cinereus)這個貝氏擬態群，藉由測量背部單點的反射光譜，與泥土、濕葉子、乾葉子的反射光譜相比，並且套用東方襪帶蛇 (Thamnophis sirtalis)、十三線地松鼠 (Spermophilus tridecemlineatus)與藍山雀 (Cyanistes caeruleus)分別代表三種不同的捕食者的視覺模型，統計有哪些捕食者可以看的到。結果顯示這個擬態的現象侷限於顏色(color)，而不是亮度(brightness)；視覺模型的統計中，只有鳥類能分辨火焰蠑螈與非擬態的紅背蠑螈；與背景比較的話，這些蠑螈與預期的一樣十分明顯。

不過如果仔細看內文的統計數據會發現一些有趣的事情，作者用三種不同的背景比較顯眼度，雖然著墨不多，但其實蛇與哺乳類對於不同背景的亮度還是有統計上的差異，若只從視覺模型這點來看，我想這些捕食者還是看的到某些東西，而我們對於蛇類與除了白鼠外的小型哺乳類的認知幾乎一無所知，即使只能透過亮度的差異，是不是就能達到警戒性的功用也未可知，作者把結論導向這個選汰的主力是鳥類捕食者，也只是因為在顏色的辨別達到統計上的顯著差異，未來透過同類型的捕食者的行為實驗或許能帶來更多結果。

不過有意思的是，作者在之後的研究（看這裡）裡說兩種蠑螈的亮度是隨族群有差異的，如果這個擬態群只有顏色影響其作用的話，那麼亮度為何需要變動？（或許是為了其他理由，如求偶）反過來說，亮度的變動有沒有可能反而是為了那些看不到顏色的捕食者，讓牠們能「看見」（警戒）或「看不見」（隱蔽）？

標題：Five species of passerine bird differ in their ability to detect Batesian mimics

摘要

Multiple predators affect the evolution of aposematic signals in nature and these predators may substantially differ in terms of ecological and cognitive parameters. However, most experimental studies testing the evolution of Batesian mimics use only a single species of predator (usually the great tit or a domestic chick). Therefore, in the present study, we experimentally tested the responses of five passerine predators to an artificially made Batesian mimic (a cockroach equipped with the warning pattern of the red firebug) with respect to their dietary ecology. Half of the individuals of each species were fed on unmodified roaches before the experiment, whereas the other half were fed with mealworms and thus had no previous experience with roaches. We found that Batesian mimics were better protected than inconspicuous prey against inexperienced great tits and robins alone. The other three bird species showed high level of neophobia; therefore, the effect of warning coloration could not be assessed. We also found that experienced birds attacked a greater number of Batesian mimics compared to inexperienced individuals of all tested species, with the exception of blackcaps. In the great tits, robins, and blue tits, a significant number of experienced birds attacked the Batesian mimic, which was possibly the result of a learned search image for a roach. Our results suggest that using a limited array of predators to describe evolutionary processes forming the diversity of antipredatory strategies of the prey may be biased and need not describe the situation occurring in nature.

標題：A bird's eye view of two mimetic tropical butterflies: coloration matches predator's sensitivity

摘要

Unprofitable prey with conspicuous warning signals are often mimicked by other species, which then gain protection from predators. How closely two mimetic spe- cies resemble one another depends upon the visual perception of the signal recei- ver. However, most studies of mimetic coloration have been conducted using only the human visual system, which differs greatly from that of most animals. To bet- ter understand mimicry, we should study mimetic visual signals through the eyes of the intended receiver. Here, we use avian visual models to test predictions of putative Batesian mimicry in two Amazonian butterflies, Mimoides pausanias and Heliconius sara. We calculated Just Noticeable Differences (JNDs) and tetrahedral color volumes for 11 different patches: iridescent blue, yellow bars, red spots and black background. Several color patches were not visually discriminable for both avian visual systems (UV/VIS and V/VIS), and visual discrimination (i.e. degree of mimicry) of color patches depended upon the avian visual system. These two but- terfly species are more mimetic when viewed by their likely avian predators, which have V/VIS vision. Therefore, this mimetic assemblage may have evolved to be more spectrally accurate in the non-UV wavelengths which their avian predators are able to see. However, while many color patches of the two species were mod- eled to be difficult to discriminate, most color patches were not perfect matches regardless of visual system, and several patches were very poor mimics. Through this study we demonstrate the importance of testing putative mimetic assemblages using known predator perceptual models and lay a foundation for behavioral studies to further test mimicry in H. sara and M. pausanius.

原文標題：Evidence of signaling benefits to contrasting internal color boundaries in warning coloration

[摘要][原文網址]
It has been suggested that the common existence of regular patterning in aposematic prey animals makes them “stand out” from the background, improving detection and recognition. Another suggestion is that internal patterns could have a similar positive effect on predator aversion learning as prey-to-background contrast. We used wild caught blue tits (Cyanistes caeruleus) and artificial prey signals to investigate if internal color boundaries, pattern regularity and pattern symmetry affect learning. Birds in different treatments were trained, on a complex background, to discriminate between artificial prey with different nonrewarding color stimuli with a black pattern and rewarding stimuli without a black pattern, followed by a generalization test. This study provides evidence of learning benefits to internally contrasting patterns as the striped prey stimuli were learned faster than the unstriped. Also, we found no beneficial effects of pattern regularity and symmetry. The birds generalized more between prey with different black patterns than to the profitable prey, suggesting that color is of foremost importance. The generalization test also showed a greater avoidance of striped than that of unstriped prey, suggesting some attention on patterns. Thus, internal patterning may affect signal salience and in some circumstances benefit prey due to both a faster avoidance learning and generalization behavior.

簡單說明一下這篇文章大概在幹嘛，警戒色這東西就比較大眾化的了解，不外乎就是顏色很鮮豔，也就是跟背景對比明顯，容易被捕食者發現，捕食者知道這東西不能吃這樣，可是我們可以發現自然界中並不是每種有警戒斑紋的東西長得都一樣，有的條紋一樣顏色不一樣，有的顏色一樣花紋不一樣，有的對稱有的不對稱，那麼怎樣的組合才是能有最大效益的，就是這篇文章討論的重點，而其實這篇文章的作者Gabriella Gamberale-Stille有一系列的文章在討論這個問題，容我未來慢慢介紹。