掠食者的保守食性使得稀少且醒目的獵物得以生存

Marples NM, Mappes J. (2011) Can the dietary conservatism of predators compensate for positive frequency dependent selection against rare, conspicuous prey? Evol Ecol. 25:737–749. DOI: 10.1007/s10682-010-9434-x

簡介
由於顯眼性色彩容易吸引天敵的注意，警戒色在演化初期對獵物來說是不利且少見的，但若長期只供給相同獵物時，此獵物顯眼性表型中的anti-apostatic個體將被選汰出來。因此，作者以大山雀作為捕食者，杏仁作為人工獵物，測試於隱蔽獵物中19代顯眼性個體和捕食者的捕食行為之關係。結果發現，顯眼性獵物在初級的被攻擊率最高，使具警戒功能的顯眼性個體無法存活，但期捕食者有17隻(24%)會拒決捕食顯眼性獵物。因此，顯眼性獵物要在隱蔽族群中存活是困難的，但在捕食者的捕食行為篩選下，會促使警戒色在演化中被保存。

捕食者對車前燈蛾(Parasemia plantaginis)翅紋警戒色之方向性選擇及強度

Lindstedt C, Eager H, Ihalainen E, Kahilainen A, Stevens M, Mappesa J. (2011) Direction and strength of selection by predators for the color of the aposematic wood tiger moth. Behav. Ecol. doi:10.1093/beheco/arr017[full text]

簡介
在本篇研究中，作者以Parasemia plantaginis的雌性作為顯眼性獵物，該物種具有雌性多態型(紅/橘/黃三種翅紋色彩)，以Galleria sp.作為隱蔽性獵物，並以pied flycatchers及Great tits作為捕食者進行了四個實驗：
(a) 同時提供顯眼性與隱蔽性獵物，去看在不同獵物下，捕食者的攻擊行為是否有差異；
(b)針對Para. plantaginis翅紋的差異及實驗背景，去進行色彩及亮度的標定，再去比較捕食者視神經的接收比率、製成模型比較；
(c)以兩種不同翅紋的Para. plantaginis去探討捕食者迴避學習的程度差異；
(d)於野外實驗探討捕食者對顯眼性獵物和隱蔽性獵物存活率的影響，以及紅色及橘色顯眼性獵物存活率上的差異。
結果發現：具警戒的顯眼性獵物較具有存活優勢，並且高度的對比色可以加快捕食者的迴避學習，但由於Para. plantaginis本身的化學防禦性物質的影響，使Para. plantaginis的雌性多態型於演化中得以保存，但本研究中所有數據於統計上均無顯著差異存在。

無翅紅蝽警戒色對捕食者的影響

文獻出處：
Exnerová, A., Svádová, K., Štys, P., Barcalová, S., Landová, E., Prokopová, M., Fuchs, R. & Socha, R. (2006) Importance of colour in the reaction of passerine predators to aposematic prey: experiments with mutants of Pyrrhocoris apterus (Heteroptera). Biological Journal of the Linnean Society 88: 143-153. [Full text]
Prokopová, M., Veselý, P., Fuchs, R. & Zrzavý, J. (2010) The role of size and colour pattern in protection of developmental stages of the red firebug (Pyrrhocoris apterus) against avian predators. Biological Journal of the Linnean Society 100(4): 890–898. [Abstract]

無翅紅蝽(Pyrrhocoris apterus)是半翅目(Hemiptera)昆蟲綱(Insecta)的物種，成蟲體長9-13 mm，發育過程中有五次蛻皮，可以借由蛻皮改變身上的斑紋，體色也可能隨著溫度變化而有些許改變。Alice Exnerová et al. (2006)於1999年至2002年間進行測試，探討無翅紅蝽警戒色的持久性問題、體色和背景色效應的關係，以及體色多態型的起源和警戒色的維持，他以大山雀(Parus major), 藍山雀(Cyanistes caeruleus), 歐亞鴝(Erithacus rubecula)和黑冠鶯(Sylvia atricapilla)作為捕食者，並且實驗過程中所使用的所有物種均於實驗前(一年內)捕獲，再經人工飼養而來。其結果得知，顏色的多態性可以說明：物種的演化是經由隱性突變所造成。

另外，無翅紅蝽成蟲和幼蟲雖然都具有紅色及黑色的體色，但體形大小、色彩和紋路相異，被捕食的頻率則有所差異。Milena Prokopová et al. (2010)假設體型大小會影響捕食者光化學信號的傳遞，而以大山雀(Parus major)和藍山雀(Cyanistes caeruleus)這兩種生態性相似的物種做為捕食者，來探討體型大小不同的鳥類，對無翅紅蝽的體型比例、顏色模式和捕食訊號之間關係的影響。結果顯示捕食者第一次遇到紅蝽時，體型不影響攻擊；但多次後，體型小的獵物較容易被攻擊、取食，並且獵物對兩種捕食者的保護信號有所不同(化學及光學信號)，就連色彩模式也影響捕食者的意願，所以雖然幼蟲和成蟲同時具有紅色和黑色外表，但幼蟲的色彩並沒有提供良好的保護作用。

Higher survival of aposematic prey in close encounters with predators: an experimental study of detection distance

Animal Behavior, Vol. 78, No. 1, 111-116

Gabriella Gamberale-Stille, Carolina Bragée and Birgitta S. Tullberg

Department of Zoology, Stockholm University, Sweden

Aposematic animals are often conspicuous. It has been hypothesized that one function of conspicuousness in such prey is to be detected from afar by potential predators: the ‘detection distance hypothesis’. The hypothesis states that predators are less prone to attack at long detection range because more time is allowed for making the ‘correct’ decision not to attack the unprofitable prey. The detection distance hypothesis has gained some experimental support in that time-limited predators make more mistakes. To investigate effects of prey presentation distance we performed two experiments. First, in experiment 1, we investigated at what distance chicks, Gallus gallus domesticus, could see the difference in colour between aposematic and plain mealworms. Birds chose the correct track in a two-way choice when prey were at 20, 40 and 60 cm distance but not at 80 cm. Second, in experiment 2, fifth-instar larvae of the aposematic bug Lygaeus equestris were presented to experienced chicks at 2, 20 or 60 cm distance. We found no difference in attack probability between distances. However, prey mortality was significantly lower for the shortest presentation distance. In conclusion, we found no support for the hypothesis that aposematic prey benefit from long-range detection; in fact they benefit from short-distance detection. This result, and others, suggests that the conspicuousness of aposematic prey at a distance may simply be a by-product of an efficient signalling function after detection.

Keywords: attack mortality; attention; detection distance; domestic chick; foraging behaviour; Gallus gallus domesticus; Lygaeus equestris; warning coloration

Butterfly effects in mimicry? Combining signal and taste can twist the relationship of Müllerian co-mimics

Butterfly effects in mimicry? Combining signal and taste can twist the relationship of Müllerian co-mimics

Behavioural Evology and Sociobiology, Vol. 62, No. 8, 1267-1276

Eira Ihalainen, Leena Lindström, Johanna Mappes and Sari Puolakkainen
Department of Biological and Environmental Science, FI-40014 University of Jyväskylä

Müllerian co-mimics are aposematic species that resemble each other; sharing a warning signal is thought to be mutually beneficial for the co-mimics by reducing per capita predation risk. In Batesian mimicry, edible mimics avoid predation by resembling an aposematic model species. The protection of both the model and the mimic is weakened when the mimics are abundant compared to the models. The quasi-Batesian view suggests that defended (Müllerian) co-mimics, when unequal in their defences, could also show a Batesian-like trend of increasing mortality with increasing abundance of a less defended “mimic”. We manipulated frequencies of unequally distasteful artificial co-mimics that were prey for great tits. The co-mimics had different signals (imperfect mimicry) but were equally preferred by the birds when palatable. Unexpectedly, when unpalatable, one of the signals was easier for the birds to learn to avoid. Consequently, during predator learning, the signal design of the prey strongly affected mortality of the co-mimics; there was an interaction between the signal and frequency treatments, but increasing the frequency of a less defended “mimic” did not increase co-mimic mortalities as predicted. In contrast, in a memory test that followed, the effect of signal design disappeared; if the birds had experienced high frequency of “mimics” during learning, co-mimic mortalities did subsequently increase. Since the effect of co-mimic frequencies on mortalities changed depending on the signal design of the prey and predator experience, the results suggest that mimetic relationship may be an unpredictable interplay of several factors in addition to taste and abundance.

Keywords: Aposematism - Quasi-Batesian mimicry - Predator psychology - Avoidance learning - Memory

The role of predator selection on polymorphic aposematic poison frogs

The role of predator selection on polymorphic aposematic poison frogs

Biology letters (2009) Vol. 5, No. 1, 51-54
Brice P. Noonan, Aaron A. Comeault
Department of Biology, University of Mississippi, University

Demonstrations of interactions between diverse selective forces on bright coloration in defended species are rare. Recent work has suggested that not only do the bright colours of Neotropical poison frogs serve to deter predators, but they also play a role in sexual selection, with females preferring males similar to themselves. These studies report an interaction between the selective forces of mate choice and predation. However, evidence demonstrating phenotypic discrimination by potential predators on these polymorphic species is lacking. The possibility remains that visual (avian) predators possess an inherent avoidance of brightly coloured diurnal anurans and purifying selection against novel phenotypes within populations is due solely to non-random mating. Here, we examine the influence of predation on phenotypic variation in a polymorphic species of poison frog, Dendrobates tinctorius. Using clay models, we demonstrate a purifying role for predator selection, as brightly coloured novel forms are more likely to suffer an attack than both local aposematic and cryptic forms. Additionally, local aposematic forms are attacked, though infrequently, indicating ongoing testing/learning and a lack of innate avoidance. These results demonstrate predator-driven phenotypic purification within populations and suggest colour patterns of poison frogs may truly represent a ‘magic trait’.

Keywords: aposematic, selection, Dendrobates, magic trait

Warning displays may function as honest signals of toxicity

Warning displays may function as honest signals of toxicity

Proceedings of Royal Society B (2009) Vol. 276, No. 1658, 871-877
Jonathan D. Blount(1), Michael P. Speed(2), Graeme D. Ruxton(3), Philip A. Stephens(4)
1 Centre for Ecology and Conservation, School of Biosciences, University of Exeter, Cornwall Campus
2 School of Biological Sciences, Bioscience Building, University of Liverpool
3Division of Environmental and Evolutionary Biology, Institute of Biomedical and Life Sciences, University of Glasgow
4 School of Biological and Biomedical Sciences, University of Durham

Many prey species use colourful ‘aposematic’ signalling to advertise the fact that they are toxic. Some recent studies have shown that the brightness of aposematic displays correlates positively with the strength of toxicity, suggesting that aposematic displays are a form of handicap signal, the conspicuousness of which reliably indicates the level of toxicity. The theoretical consensus in the literature is, however, at odds with this finding. It is commonly assumed that the most toxic prey should have less bright advertisements because they have better chances of surviving attacks and can therefore reduce the costs incurred by signalling. Using a novel theoretical model, we show that aposematic signals can indeed function as handicaps. To generate this prediction, we make a key assumption that the expression of bright displays and the storage of anti-predator toxins compete for resources within prey individuals. One shared currency is energy. However, competition for antioxidant molecules, which serve dual roles as pigments and in protecting prey against oxidative stress when they accumulate toxins, provides a specific candidate resource that could explain signal honesty. Thus, contrary to the prevailing theoretical orthodoxy, warning displays may in fact be honest signals of the level of (rather than simply the existence of) toxicity.

Keywords: aposematism, handicap signal, toxicity, trade-off

Role of different colours of aposematic insects in learning, memory and generalization of naïve bird predators

Role of different colours of aposematic insects in learning, memory and generalization of naïve bird predators

Animal Behaviour (2009) Vol. 77, No. 2, 327-336
Kateřina Svádová(a, b), Alice Exnerová(a), Pavel Štys(a), Eva Landová(a), Jan Valenta(c), Anna Fučíková(c) and Radomír Socha(d)
aDepartment of Zoology, Charles University, Praha, Czech Republic
bDepartment of Biology, University Hradec Králové, Czech Republic
cDepartment of Chemical Physics and Optics, Charles University, Praha, Czech Republic
dBiology Center ASCR, Institute of Entomology, České Budějovice, Czech Republic

Among the various properties of visual warning signals, colour seems to be especially important for avian predators. We tested the role of particular colours of an aposematic insect (firebug, Pyrrhocoris apterus; Heteroptera: Pyrrhocoridae) in unlearned avoidance, learning, memory and generalization of a naïve avian predator (great tit, Parus major). The wild type of the firebug is aposematic, red-and-black, and its colour mutants (white, yellow, orange) retain the same black pattern; the bug can be made artificially nonaposematic (painted uniformly brown). Wild-caught great tits avoid the firebug depending on colour, and their reaction to variously coloured prey is a result of avoidance learning and may vary according to their experience. We trained naïve great tits to avoid firebugs of different colours, and then gave some birds a memory test with firebugs of the same colour and other birds a generalization test with firebugs of a different colour. Naïve, hand-reared great tits showed no initial avoidance and attacked firebugs irrespective of colour. They learned to avoid all the colour forms at a similar rate. The generalization was asymmetric: birds that learned to avoid red firebugs did not generalize their experience to yellow or white mutants whereas birds that learned to avoid yellow mutants generalized their experience to red firebugs. The red colour thus represents a more effective signal than the yellow; predation by birds could have played a crucial role in selectively favoured evolutionary transitions from yellow to red coloration in pyrrhocorids.

Keywords: asymmetric generalization; avoidance learning; firebug; great tit; Parus major; peak shift; Pyrrhocoris apterus; signal memorability; warning signal

The protective value of conspicuous signals is not impaired by shape, size, or position asymmetry

The protective value of conspicuous signals is not impaired by shape, size, or position asymmetry

Behavioral Ecology (2009) Vol. 20, No. 1, 96-102
Martin Stevens, Sarah A. Castor-Perry, and Jessica R.F. Price
Department of Zoology, University of Cambridge

Various conspicuous signals in nature promote initial and learned avoidance by predators. It is widely thought that such signals are most effective when highly symmetrical in features such as size and shape, supported by recent laboratory experiments with domestic chicks and artificial prey. However, no study has investigated the effect of asymmetry on conspicuous signals in a natural setting, where viewing distances, angles, predator species, and light conditions vary and where predators encounter prey sequentially rather than simultaneously. We undertook 2 field experiments with artificial gray-scale prey, marked with a pair of white markings presented to wild avian predators, to test the effect of asymmetry on the survival value of conspicuous signals in the field. Experiment 1 had treatments with symmetrical spots or with spots asymmetrical in area between 5 and 50%. All marked
treatments survived better than unmarked controls, but there was no benefit of being symmetrical. Experiment 2 tested the effect of possessing markings asymmetrical for shape or position and any additive effect of these 2 features. Again, symmetry conferred no benefit and targets with markings asymmetrical for position and/or shape survived equally well as those with symmetrical arrangements. These findings indicate that asymmetry in warning signals may not be costly to prey in nature or be of less importance compared with other features of the signal, such as color and overall size.

Keywords: antipredator coloration, aposematism, birds, eyespots, predation, symmetry.

[Article]Being conspicuous and defended: selective benefits for the individual

Being conspicuous and defended: selective benefits for the individual

Christina G. Halpin, John Skelhorn and Candy Rowe

Centre for Behaviour and Evolution, Institute of Neuroscience, Newcastle University, Henry Wellcome Building, Framlington Place, Newcastle upon Tyne, NE2 4HH, UK

Aposematic insects conspicuously advertise their unprofitability to potential predators. However, when these prey initially evolved, they were likely to have been rare and presumably at a greater risk of being detected and killed by naive predators. Both kin and individual selection theories have been used in attempts to explain this apparent paradox, with much of the empirical research supporting kin selection–based theories. Here, we experimentally test how chemical defence levels in prey and avian color biases influence the probability of a rare conspicuous morph having an initial survival advantage. We used newly hatched domestic chicks (Gallus gallus domesticus) foraging on green and purple prey, on a green or purple background, to model the evolutionary scenario of a rare conspicuous morph arising in a population of already defended cryptic prey. Defended prey were produced by spraying them with quinine solution, which the birds readily detect and can learn to avoid. Although attack rates were initially similar for both defended prey types, the chicks only learned to avoid defended prey when they were conspicuous, not when they were cryptic. In addition, defended conspicuous prey were more likely to be rejected on attack than defended cryptic prey, even when first encountered by a predator. These data suggest that there could be a selective advantage for a rare conspicuous morph to arise in a population of cryptic defended prey due to increased avoidance learning and taste-rejection in naive predators. Our findings also suggest that being a non-preferred color and/or highly defended will increase the probability of this evolutionary scenario.

keywords: aposematism, avoidance learning, color bias, predation, receiver psychology, taste-rejection, warning signal.

[Article]Dazzle coloration and prey movement

Dazzle coloration and prey movement

Martin Stevens1, Daniella H. Yule1, Graeme D. Ruxton2

1Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK
2Faculty of Biomedical and Life Sciences, University of Glasgow, Glasgow G12 8QQ, UK

Many traits in animals reduce the rate of attack from visually hunting predators, including camouflage, warning signals and mimicry. In addition, some animal markings may reduce the likelihood that an attack ends in successful capture. These might include dazzle markings, high-contrast patterns that make the estimation of speed and trajectory difficult. However, until now, no study has experimentally tested whether some markings may achieve such an effect. We developed a computer ‘game’ where human ‘predators’ have to capture computer-generated prey moving across a background. In two experiments, we find that although uniform camouflaged targets were among the hardest to capture, so were a range of high-contrast conspicuous patterns, such as bands and zigzags. Prey were also more difficult to capture against more heterogeneous than uniform backgrounds, and at faster speeds of movement. As such, we find the first experimental evidence that conspicuous patterns, similar to those found in a wide range of real animals, make the capture of moving prey more challenging. Various anti-predator markings may work prey during motion, and some animals may combine such dazzle patterns with other functions, such as camouflage, thermoregulation, sexual and warning signals.

keywords: protective coloration, motion, conspicuousness, vision, predation, dazzle

[Article]Multimodal warning signals for a multiple predator world

Nature 455, 96-99 (4 September 2008) | doi:10.1038/nature07087; Received 10 February 2008; Accepted 14 May 2008

Multimodal warning signals for a multiple predator world

John M. Ratcliffe^1,3 & Marie L. Nydam^2,3

1. Center for Sound Communication, Institute of Biology, University of Southern Denmark, DK-5230 Odense M, Denmark
2. Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, New York 14853, USA
3. These authors contributed equally to this work.

Correspondence to: John M. Ratcliffe^1,3Marie L. Nydam^2,3 Correspondence and requests for materials should be addressed to M.L.N. (Email: mln32@cornell.edu) or J.M.R. (Email: jmr@biology.sdu.dk).

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Abstract

Aposematism is an anti-predator defence, dependent on a predator's ability to associate unprofitable prey with a prey-borne signal¹. Multimodal signals should vary in efficacy according to the sensory systems of different predators; however, until now, the impact of multiple predator classes on the evolution of these signals had not been investigated^{2, 3}. Here, using a community-level molecular phylogeny to generate phylogenetically independent contrasts, we show that warning signals of tiger moths vary according to the seasonal and daily activity patterns of birds and bats—predators with divergent sensory capacities. Many tiger moths advertise chemical defence^{4, 5} using conspicuous colouration and/or ultrasonic clicks^{3, 6}. During spring, when birds are active and bats less so, we found that tiger moths did not produce ultrasonic clicks. Throughout both spring and summer, tiger moths most active during the day were visually conspicuous. Those species emerging later in the season produced ultrasonic clicks; those that were most nocturnal were visually cryptic. Our results indicate that selective pressures from multiple predator classes have distinct roles in the evolution of multimodal warning displays now effective against a single predator class. We also suggest that the evolution of acoustic warning signals may lack the theoretical difficulties associated with the origination of conspicuous colouration.

[Article]Conflict btw natural & sexual selection due to mmicry

Interspecific sexual attraction because of convergence in warning colouration: is there a conflict between natural and sexual selection in mimetic species?

Journal of Evolutionary Biology

Volume 21 Issue 3 Page 749-760, May 2008

Citation: C. ESTRADA, C. D. JIGGINS (2008) Interspecific sexual attraction because of convergence in warning colouration: is there a conflict between natural and sexual selection in mimetic species? Journal of Evolutionary Biology 21 (3) , 749–760 doi:10.1111/j.1420-9101.2008.01517.x

Abstract

When species converge in their colour patterns because of mimicry, and those patterns are also used in mate recognition, there is a probability of conflicting selection pressures. Closely related species that mimic one another are particularly likely to face such confusion because of similarities in their courtship behaviour and ecology. We conducted experiments in greenhouse conditions to study interspecific attraction between two mimetic butterfly species, Heliconius erato and Heliconius melpomene. Both species spent considerable time approaching and courting females of the co-mimic species. Experiments using wing models demonstrated the importance of colour pattern in this interspecific attraction. Although males of H. melpomene were attracted to their co-mimics as much as to their own females, H. erato males were more efficient at distinguishing conspecifics, possibly using wing odours. Although preliminary, these results suggest that the use of additional cues may have evolved in H. erato to reduce the cost of convergence in visual signals with H. melpomene. Overall, our results showed that there might be a cost of mimetic convergence because of a reduction in the efficiency of species recognition. Such cost may contribute to explain the apparently stable diversity in Müllerian mimetic patterns in many tropical butterfly assemblages.

[Article]A Conserved Supergene Locus Controls Colour Pattern Diversity in Heliconius Butterflies

Link: http://0rz.tw/733NG
Abstract: We studied whether similar developmental genetic mechanisms are involved in both convergent and divergent evolution. Mimetic insects are known for their diversity of patterns as well as their remarkable evolutionary convergence, and they have played an important role in controversies over the respective roles of selection and constraints in adaptive evolution. Here we contrast three butterfly species, all classic examples of Müllerian mimicry. We used a genetic linkage map to show that a locus, Yb, which controls the presence of a yellow band in geographic races of Heliconius melpomene, maps precisely to the same location as the locus Cr, which has very similar phenotypic effects in its co-mimic H. erato. Furthermore, the same genomic location acts as a “supergene”, determining multiple sympatric morphs in a third species, H. numata. H. numata is a species with a very different phenotypic appearance, whose many forms mimic different unrelated ithomiine butterflies in the genus Melinaea. Other unlinked colour pattern loci map to a homologous linkage group in the co-mimics H. melpomene and H. erato, but they are not involved in mimetic polymorphism in H. numata. Hence, a single region from the multilocus colour pattern architecture of H. melpomene and H. erato appears to have gained control of the entire wing-pattern variability in H. numata, presumably as a result of selection for mimetic “supergene” polymorphism without intermediates. Although we cannot at this stage confirm the homology of the loci segregating in the three species, our results imply that a conserved yet relatively unconstrained mechanism underlying pattern switching can affect mimicry in radically different ways. We also show that adaptive evolution, both convergent and diversifying, can occur by the repeated involvement of the same genomic regions.