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  • 1.
    Aronsson, Marianne
    et al.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen, Avdelningen för etologi.
    Gamberale-Stille, Gabriella
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen, Avdelningen för etologi.
    Colour and pattern similarity in mimicry - evidence for a hierarchical discriminative learning of warning colour pattern components.Manuskript (preprint) (Annet vitenskapelig)
  • 2.
    Aronsson, Marianne
    et al.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Gamberale-Stille, Gabriella
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Colour and pattern similarity in mimicry: evidence for a hierarchical discriminative learning of different components2012Inngår i: Animal Behaviour, ISSN 0003-3472, E-ISSN 1095-8282, Vol. 84, nr 4, s. 881-887Artikkel i tidsskrift (Fagfellevurdert)
    Abstract [en]

    Many aposematic species combine their bright colours with a black pattern that produces internal contrasts. Studies have shown that birds often pay attention to some parts of a signalling pattern and disregard others, which could be of importance in Batesian mimicry, where a palatable species copies the visual appearance of a distasteful model in order to deceive predators. We used domestic chicks, Gallus gallus domesticus, and artificial prey signals to investigate whether predators use different warning colour components for discrimination depending on the degree of information about prey quality they convey. This study supports earlier findings of the importance of colour for discrimination among prey but also provides evidence that other less associable signal properties such as internal patterning, when holding valuable discriminatory information, can be used to assess prey quality in a hierarchical manner. The results also suggest that, in certain circumstances, the presence of a palatable mimic can have positive effects on learning, resulting in 'super-Mullerian' effects. We propose that the degree of selection for perfect mimicry may be dependent on the proportion of well-educated predators in the population.

  • 3.
    Aronsson, Marianne
    et al.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Gamberale-Stille, Gabriella
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Domestic chicks primarily attend to colour, not pattern, when learning an aposematic coloration2008Inngår i: Animal Behaviour, ISSN 0003-3472, E-ISSN 1095-8282, Vol. 75, s. 417-423Artikkel i tidsskrift (Fagfellevurdert)
    Abstract [en]

    Aposematic conspicuous coloration consists of one or a few bright colours, often in combination with a black defined internal pattern. The function of conspicuousness in aposematism has been ascribed to signal efficacy, based on experimental evidence involving prey items with uniform colour that contrast with the background. Although there are several hypotheses about the existence of internal contrasts within warning coloration, little experimental evidence has been presented. Here we used domestic chicks, Gallus gallus domesticus, to investigate the relative importance of colour and pattern in avoidance learning. Birds in two groups were first trained to discriminate between a grey positive stimulus and a cyan negative stimulus with either black dots or stripes. Pieces of mealworms, untreated and palatable or made unpalatable by soaking in quinine were used as reinforcers. Secondly, to determine what birds had attended to when learning the discrimination, colour and/or pattern, we compared how they generalized their avoidance of the ‘training stimulus’ to either a ‘colour only’ or ‘pattern only’ stimulus. The chicks learned to avoid the unpalatable prey items but showed no difference in behaviour depending on the type of pattern presented. The generalization test showed that birds avoided the novel ‘colour only’ stimulus at least as much as the ‘training stimulus’, and did not generalize their avoidance to the ‘pattern only’ stimulus. We conclude that birds do not necessarily attend to complex patterns when learning a warning signal, and domestic chicks primarily learn a bright colour rather than an equally novel conspicuous black pattern.

  • 4.
    Aronsson, Marianne
    et al.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Gamberale-Stille, Gabriella
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Evidence of signaling benefits to contrasting internal color boundaries in warning coloration2013Inngår i: Behavioral Ecology, ISSN 1045-2249, E-ISSN 1465-7279, Vol. 24, nr 2, s. 349-354Artikkel i tidsskrift (Fagfellevurdert)
    Abstract [en]

    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.

  • 5.
    Aronsson, Marianne
    et al.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen, Avdelningen för etologi.
    Gamberale-Stille, Gabriella
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen, Avdelningen för etologi.
    Importance of internal pattern contrast and contrast against the background in aposematic signals.2009Inngår i: Behavioral Ecology, ISSN 1045-2249, E-ISSN 1465-7279, Vol. 20, nr 6, s. 1356-1362Artikkel i tidsskrift (Fagfellevurdert)
    Abstract [en]

    Aposematic color patterns that signal prey unprofitability are suggested to work best when there is high contrast within the animal color pattern or between the animal and its background. Studies show that prey contrast against the background increases the signal efficiency. This has occasionally been extended to also explain the presence of internal patterns. We used domestic chicks, Gallus gallus domesticus, to investigate the relative importance for avoidance learning of within-prey pattern contrast and prey contrast against the background. In a series of trials, birds were first trained to avoid artificially made aposematic mealworms that were plain red or red with black stripes, and to discriminate them from palatable brown mealworms, on either a red or a brown background. Second, we investigated how the birds generalized between striped and nonstriped prey. The chicks showed faster avoidance learning when the basic color of the aposematic prey (red) contrasted with the background color (brown). However, there was no similar effect of internal pattern contrast. The generalization test showed a complete generalization between the nonstriped and the striped prey. We conclude that contrasting internal patterns do not necessarily affect predator avoidance learning the same way as shown for prey-to-background contrast in aposematic prey.

  • 6.
    Aronsson, Marianne
    et al.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen, Avdelningen för etologi.
    Gamberale-Stille, Gabriella
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen, Avdelningen för etologi.
    Why do aposematic prey often have contrasting internal patterns: Evidence of benefits through predator avoidance learning and generalization.Manuskript (preprint) (Annet vitenskapelig)
  • 7.
    Balogh, Alexandra C.V.
    et al.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Gamberale-Stille, Gabriella
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen. Etologi.
    Leimar, Olof
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen. Etologi.
    Learning and the mimicry spectrum: from quasi-Bates to super-Müller2008Inngår i: Animal Behaviour, ISSN 0003-3472, Vol. 76, nr 5, s. 1591-1599Artikkel i tidsskrift (Fagfellevurdert)
    Abstract [en]

    Müllerian mimicry is the mutualistic resemblance between two defended species, while Batesian mimicry is the parasitic resemblance between a palatable species (the mimic) and an unpalatable one (the model). These two kinds of mimicry are traditionally seen as extreme ends of a mimicry spectrum. For the range in between, it has been suggested that mimetic relations between unequally defended species could be parasitic, and this phenomenon has been referred to as quasi-Batesian mimicry. Where a mimetic relation is placed along the mimicry spectrum depends on the assumptions made about predator learning. In this work, we use a variant of the Rescorla-Wagner learning model for virtual predators to analyse the different possible components of the mimicry spectrum. Our model entails that the rate of associative learning is influenced by variation in the stimuli to be learned. Variable stimuli, i.e. unequal defences, can increase the predator learning rate and thus lead to an increased level of mutualism in a mimetic relation. In our analysis, we make use of the concepts of super-Müllerian mimicry, where the benefit of mimicry is even greater than in traditional Müllerian mimicry, and quasi-Müllerian mimicry, where mimicry by a palatable mimic is mutualistic. We suggest that these types of mimicry should be included in the mimicry spectrum along with Müllerian, Batesian and quasi-Batesian mimicry.

  • 8.
    Balogh, Alexandra C.V.
    et al.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Gamberale-Stille, Gabriella
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Tullberg, Birgitta S.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Leimar, Olof
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Feature theory and the two-step hypothesis of Müllerian mimicry evolution2010Inngår i: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 64, nr 3, s. 810-822Artikkel i tidsskrift (Fagfellevurdert)
    Abstract [en]

    The two-step hypothesis of Müllerian mimicry evolution states that mimicry starts with a major mutational leap between adaptive peaks, followed by gradual fine-tuning. The hypothesis was suggested to solve the problem of apostatic selection producing a valley between adaptive peaks, and appears reasonable for a one-dimensional phenotype. Extending the hypothesis to the realistic scenario of multidimensional phenotypes controlled by multiple genetic loci can be problematic, because it is unlikely that major mutational leaps occur simultaneously in several traits. Here we consider the implications of predator psychology on the evolutionary process. According to feature theory, single prey traits may be used by predators as features to classify prey into discrete categories. A mutational leap in such a trait could initiate mimicry evolution. We conducted individual-based evolutionary simulations in which virtual predators both categorize prey according to features and generalize over total appearances. We found that an initial mutational leap towards feature similarity in one dimension facilitates mimicry evolution of multidimensional traits. We suggest that feature-based predator categorization together with predator generalization over total appearances solves the problem of applying the two-step hypothesis to complex phenotypes, and provides a basis for a theory of the evolution of mimicry rings.

  • 9. Bohlin, Titti
    et al.
    Gamberale-Stille, Gabriella
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Merilaita, Sami
    Exnerova, Alice
    Stys, Pavel
    Tullberg, Birgitta S.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    The detectability of the colour pattern in the aposematic firebug, Pyrrhocoris apterus: an image-based experiment with human 'predators'2012Inngår i: Biological Journal of the Linnean Society, ISSN 0024-4066, E-ISSN 1095-8312, Vol. 105, nr 4, s. 806-816Artikkel i tidsskrift (Fagfellevurdert)
    Abstract [en]

    Crypsis and aposematism are often regarded as two opposite protective strategies. However, there is large variation in prey appearance within both strategies. In this article, we investigated the conspicuousness of the aposematic red-and-black firebug, Pyrrhocoris apterus, by presenting images of natural and digitally manipulated phenotypes in their natural habitat on a computer screen to human predators, and comparing the detection times. We asked whether the natural colour pattern can be made more or less conspicuous by rearranging the spatial distribution of colour elements. Hence, we created a phenotype in which the black colour elements were moved to the body outline to test for a possible disruptive effect. In the black and red manipulations, we removed one of the two colours, creating two uniform colour variants. We found that some of our manipulations increased, but none reduced, the detection time significantly; this indicates that the naturally coloured firebug is highly conspicuous. The detection time varied among backgrounds and there was a significant relationship between detection time and chromatic similarity between the bug and the background for the natural and black phenotypes. Although background colour composition has an important effect on the signal, we argue that the coloration of P. apterus has evolved for high conspicuousness.

  • 10.
    Gamberale-Stille, Gabriella
    et al.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Balogh, Alexandra C. V.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Tullberg, Birgitta S.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Leimar, Olof
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    FEATURE SALTATION AND THE EVOLUTION OF MIMICRY2012Inngår i: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 66, nr 3, s. 807-817Artikkel i tidsskrift (Fagfellevurdert)
    Abstract [en]

    In Batesian mimicry, a harmless prey species imitates the warning coloration of an unpalatable model species. A traditional suggestion is that mimicry evolves in a two-step process, in which a large mutation first achieves approximate similarity to the model, after which smaller changes improve the likeness. However, it is not known which aspects of predator psychology cause the initial mutant to be perceived by predators as being similar to the model, leaving open the question of how the crucial first step of mimicry evolution occurs. Using theoretical evolutionary simulations and reconstruction of examples of mimicry evolution, we show that the evolution of Batesian mimicry can be initiated by a mutation that causes prey to acquire a trait that is used by predators as a feature to categorize potential prey as unsuitable. The theory that species gain entry to mimicry through feature saltation allows us to formulate scenarios of the sequence of events during mimicry evolution and to reconstruct an initial mimetic appearance for important examples of Batesian mimicry. Because feature-based categorization by predators entails a qualitative distinction between nonmimics and passable mimics, the theory can explain the occurrence of imperfect mimicry.

  • 11.
    Gamberale-Stille, Gabriella
    et al.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen, Avdelningen för etologi.
    Bragée, Carolina
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Tullberg, Birgitta S.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen, Avdelningen för zoologisk ekologi.
    Higher survival of aposematic prey in close encounters with predators – an experimental study of detection distance.2009Inngår i: Animal Behaviour, ISSN 0003-3472, E-ISSN 1095-8282, Vol. 78, s. 111-116Artikkel i tidsskrift (Fagfellevurdert)
    Abstract [en]

    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 shortdistance 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.

  • 12.
    Gamberale-Stille, Gabriella
    et al.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen. Etologi.
    Hall, Susanna
    Birgitta S., Tullberg
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen. Ekologi.
    Signals of profitability? Food colour preferences in migrating juvenile blackcaps differ for fruits and insects.2007Inngår i: Evolutionary Ecology, ISSN 0269-7653, nr 21, s. 99-108Artikkel i tidsskrift (Fagfellevurdert)
  • 13.
    Gamberale-Stille, Gabriella
    et al.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Johansen, Aleksandra I.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Tullberg, Birgitta S.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Change in protective coloration in the striated shieldbug Graphosoma lineatum (Heteroptera: Pentatomidae): predator avoidance and generalization among different  life stages2010Inngår i: Evolutionary Ecology, ISSN 0269-7653, E-ISSN 1573-8477, Vol. 24, nr 2, s. 423-432Artikkel i tidsskrift (Fagfellevurdert)
    Abstract [en]

    There are two major forms of protective coloration, camouflage and warning coloration, which often entail different colour pattern characteristics. Some species change strategy between or within life stages and one such example is the striated shieldbug, Graphosoma lineatum. The larvae and the pale brownish-and-black striated pre-diapause adults are more cryptic in the late summer environment than is the red-and black striation that the adults change to after diapause in spring. Here we investigate if the more cryptic pre-diapause adult and larval coloration may affect the aposematic function of the coloration as compared to the red adult form. In a series of trials we presented fifth instar larvae, pale or red adults to shieldbug-naïve domestic chicks, Gallus gallus domesticus, to investigate the birds’ initial wariness, avoidance learning, and generalization between the three prey types. The naïve chicks found the red adults most aversive followed by pale adults, and they found the larvae the least aversive. The birds did not find the larvae unpalatable and did not learn to avoid them, while they learned to avoid the two adult forms and then to a similar degree. Birds generalized asymmetrically between life stages, positively from larvae to adults and negatively from adults to larvae. We conclude that the lower conspicuousness in the pale forms of G. lineatum may entail a reduced aposematic function, namely a reduced initial wariness in inexperienced birds. The maintenance of the colour polymorphism is discussed

  • 14.
    Gamberale-Stille, Gabriella
    et al.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Kazemi, Baharan
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Balogh, Alexandra
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Leimar, Olof
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Biased generalization of salient traits drives the evolution of warning signals2018Inngår i: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 285, nr 1877, artikkel-id 20180283Artikkel i tidsskrift (Fagfellevurdert)
    Abstract [en]

    The importance of receiver biases in shaping the evolution of many signalling systems is widely acknowledged. Here, we show that receiver bias can explain which traits evolve to become warning signals. For warning coloration, a generalization bias for a signalling trait can result from predators learning to discriminate unprofitable from profitable prey. However, because the colour patterns of prey are complex traits with multiple components, it is crucial to understand which of the many aspects of prey appearance evolve into signals. We provide experimental evidence that the more salient differences in prey traits give rise to greater generalization bias, corresponding to stronger selection towards trait exaggeration. Our results are based on experiments with domestic chickens as predators in a Skinner-box-like setting, and imply that the difference in appearance between profitable and unprofitable prey that is most rapidly learnt produces the greatest generalization bias. As a consequence, certain salient traits of unprofitable prey are selected towards exaggeration to even higher salience, driving the evolution of warning coloration. This general idea may also help to explain the evolution of many other striking signalling traits found in nature.

  • 15.
    Gamberale-Stille, Gabriella
    et al.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Schäpers, Alexander
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Janz, Niklas
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Nylin, Sören
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Selective attention by priming in host search behavior of 2 generalist butterflies2019Inngår i: Behavioral Ecology, ISSN 1045-2249, E-ISSN 1465-7279, Vol. 30, nr 1, s. 142-149Artikkel i tidsskrift (Fagfellevurdert)
    Abstract [en]

    We show that females of 2 generalist butterflies improve their search efficacy after previous encounters of the same host in a way similar to search-image formation, especially if the butterfly-host relationship is historically old. Thus, by targeting a single host at a time, host search efficacy may be improved and constitute a selection pressure for specialization. This result can help explain the evolutionary trend toward host specialization in phytophagous insects that is not well understood. Abstract In phytophagous insects such as butterflies, there is an evolutionary trend toward specialization in host plant use. One contributing mechanism for this pattern may be found in female host search behavior. Since search attention is limited, generalist females searching for hosts for oviposition may potentially increase their search efficacy by aiming their attention on a single host species at a time, a behavior consistent with search image formation. Using laboratory reared and mated females of 2 species of generalist butterflies, the comma, Polygonia c-album, and the painted lady, Vanessa cardui (Lepidoptera: Nymphalidae), we investigated the probability of finding a specific target host (among nonhost distractors) immediately after being primed with an oviposition experience of the same host as compared with different host in indoor cages. We used species-specific host plants that varied with respect to growth form, historical age of the butterfly-host association, and relative preference ranking. We found improved search efficacy after previous encounters of the same host for some but not all host species. Positive priming effects were found only in hosts with which the butterfly has a historically old relationship and these hosts are sometimes also highly preferred. Our findings provides additional support for the importance of behavioral factors in shaping the host range of phytophagous insects, and show that butterflies can attune their search behavior to compensate for negative effects of divided attention between multiple hosts.

  • 16.
    Gamberale-Stille, Gabriella
    et al.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Söderlind, Lina
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Janz, Niklas
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Nylin, Sören
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Host plant choice in the comma butterfly-larval choosiness may ameliorate effects of indiscriminate oviposition2014Inngår i: Insect Science, ISSN 1672-9609, E-ISSN 1744-7917, Vol. 21, nr 4, s. 499-506Artikkel i tidsskrift (Fagfellevurdert)
    Abstract [en]

    In most phytophagous insects, the larval diet strongly affects future fitness and in species that do not feed on plant parts as adults, larval diet is the main source of nitrogen. In many of these insect host plant systems, the immature larvae are considered to be fully dependent on the choice of the mothers, who, in turn, possess a highly developed host recognition system. This circumstance allows for a potential mother-offspring conflict, resulting in the female maximizing her fecundity at the expense of larval performance on suboptimal hosts. In two experiments, we aimed to investigate this relationship in the polyphagous comma butterfly, Polygonia c-album, by comparing the relative acceptance of low- and medium-ranked hosts between females and neonate larvae both within individuals between life stages, and between mothers and their offspring. The study shows a variation between females in oviposition acceptance of low-ranked hosts, and that the degree of acceptance in the mothers correlates with the probability of acceptance of the same host in the larvae. We also found a negative relationship between stages within individuals as there was a higher acceptance of lower ranked hosts in females who had abandoned said host as a larva. Notably, however, neonate larvae of the comma butterfly did not unconditionally accept to feed from the least favorable host species even when it was the only food source. Our results suggest the possibility that the disadvantages associated with a generalist oviposition strategy can be decreased by larval participation in host plant choice.

  • 17.
    Johansen, Aleksandra I.
    et al.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Exnerová, Alice
    Hotová Svádová, Katerina
    Stys, Pavel
    Gamberale-Stille, Gabriella
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Tullberg, Birgitta S.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Adaptive change in protective coloration in adultstriated shieldbugs Graphosoma lineatum (Heteroptera:Pentatomidae): test of detectability of two colour formsby avian predators2010Inngår i: Ecological Entomology, ISSN 0307-6946, E-ISSN 1365-2311, Vol. 35, nr 5, s. 602-610Artikkel i tidsskrift (Fagfellevurdert)
    Abstract [en]

    1. Protective coloration in insects may be aposematic or cryptic, and some species change defensive strategy between instars. In Sweden, the adult striated shieldbugs Graphosoma lineatum (Heteroptera: Pentatomidae) undergo a seasonal colour change from pale brown and black striation in the pre-hibernating adults, to red and black striation in the same post-hibernating individuals. To the human eye the pre-hibernating adults appear cryptic against the withered late summer vegetation, whereas the red and black post-hibernating adults appear aposematic. This suggests a possibility of a functional colour change. However, what is cryptic to the human eye is not necessarily cryptic to a potential predator.

    2. Therefore we tested the effect of coloration in adult G. lineatum on their detectability for avian predators. Great tits (Parus major) were trained to eat sunflower seeds hidden inside the emptied exoskeletons of pale or red G. lineatum. Then the detection time for both colour forms was measured in a dry vegetation environment.

    3. The birds required a longer time to find the pale form of G. lineatum than the red one. The pale form appears more cryptic on withered late summer vegetation than the red form, not only to the human eye but also to avian predators. The result supports the idea that the adult individuals of G. lineatum undergo a functional change from a cryptic protective coloration to an aposematic one.

  • 18.
    Johansen, Aleksandra I.
    et al.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Exnerová, Alice
    Svádová, Katerina Hotová
    Pavel, Stys
    Tullberg, Birgitta S.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Gamberale-Stille, Gabriella
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Anti-Predatory defences in the shieldbug Graphosoma lineatum (Heteroptera: Pentatomidae) differ between life stages and colour forms: an experiment with hand reared great tits (Parus major) as predatorsManuskript (preprint) (Annet vitenskapelig)
    Abstract [en]

    Crypsis and aposematism are strategies used to avoid predation. Cryptic coloration helps prey to avoid detection and aposematic coloration signals unpalatability to the predator. In the Swedish populations of striated shieldbug Graphosoma lineatum there is a change in coloration and presumably protective strategy that coincides with a change of season and the natural background in the environment. We have compared effectiveness of warning function of colour patterns and chemical defence of three consecutive instars of G. lineatum: the cryptic fifth-instar larvae, the cryptic pale brown and black pre-hibernation adults and the aposematic red and black post-hibernation adults. In experiments with hand reared great tits (Parus major) we investigated the birds’ initial response, avoidance learning and generalisation between forms. We also noted if bugs used their scent glands on attack and if they survived attacks or not. Birds attacked the larvae faster and to a higher extent than the adults, both in naïve birds and after experience, but we found no difference between the adult colour forms in this regard. However, birds generalised asymmetrically between adults and larvae. Previous experience of adults benefited the larvae, but previous experience with larvae increased attack risk on adults and significantly more on the pale than the red adults. Spraying the defensive secretion increased the survival of adults but not the larvae. We conclude that the life stages of G. lineatum differ in defensive strategy against bird predators so that larvae rely on crypsis and the red adults rely mainly on aposematism, whereas the pale adult form seems to do both.

  • 19.
    Johansen, Aleksandra I.
    et al.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Tullberg, Birgitta S.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Gamberale-Stille, Gabriella
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Motion level in Graphosoma lineatum coincides with ontogenetic change in defensive colorationInngår i: Entomologia Experimentalis et Applicata, ISSN 0013-8703, E-ISSN 1570-7458Artikkel i tidsskrift (Fagfellevurdert)
    Abstract [en]

    Crypsis and aposematism are two different approaches to predation avoidance. Theoretically, the chosen strategy depends on the prevailing possibilities and constraints to the animal. Consequently, insects often change strategy between life stages, but a switch in strategy within a life stage is quite uncommon. In the Swedish shieldbug, Graphosoma lineatum L. (Heteroptera: Pentatomidae), there is a colour change from the pre-hibernating to the post-hibernating adults that alters their protective strategy from effective crypsis to aposematism, although both stages are distasteful to predators. The change in colour occurs as there is a shift of seasons, which alters the environmental background. Here we investigate if there is a change in behaviour in G. lineatum connected to the change in coloration and protective strategy. We therefore measured the motion levels in the two different colour forms of G. lineatum, both in the field and in a more controlled laboratory set up. Our result clearly shows that there is a change in behaviour connected to the change in colour. Thus, we found that the cryptic pre-hibernation form has a significantly lower motion level than the aposematic post-hibernation form, which is in line with the expectation from the fact that motion disrupts crypsis, but not aposematism. 

  • 20.
    Johansen, Aleksandra Irene
    et al.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Tullberg, Birgitta S.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Gamberale-Stille, Gabriella
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Motion level in Graphosoma lineatum coincides with ontogenetic change in defensive colouration2011Inngår i: Entomologia Experimentalis et Applicata, ISSN 0013-8703, E-ISSN 1570-7458, Vol. 141, nr 2, s. 163-167Artikkel i tidsskrift (Fagfellevurdert)
    Abstract [en]

    Crypsis and aposematism are two different approaches to predation avoidance. Theoretically, the chosen strategy depends on the prevailing possibilities and constraints to the animal. Consequently, insects often change strategy between life stages, but a switch in strategy within a life stage is quite uncommon. In the Swedish shieldbug, Graphosoma lineatum L. (Heteroptera: Pentatomidae), there is a colour change from the pre-hibernating to the post-hibernating adults that alters their protective strategy from effective crypsis to aposematism, although both stages are distasteful to predators. The change in colour occurs as there is a shift of seasons, which alters the environmental background. Here, we investigate whether there is a change in behaviour in G. lineatum connected to the change in colouration and protective strategy. We therefore measured the motion levels in the two different colour forms of G. lineatum, both in the field and in a more controlled laboratory set up. Our result clearly shows that there is a change in behaviour connected to the change in colour. Thus, we found that the cryptic pre-hibernation form has a significantly lower motion level than the aposematic post-hibernation form, which is in line with the fact that motion disrupts crypsis, but not aposematism.

  • 21.
    Kazemi, Baharan
    et al.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Gamberale Stille, Gabriella
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Tullberg, Birgitta S.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Leimar, Olof
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Stimulus Salience as an Explanation for Imperfect Mimicry2014Inngår i: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 24, nr 9, s. 965-969Artikkel i tidsskrift (Fagfellevurdert)
    Abstract [en]

    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.

  • 22.
    Kazemi, Baharan
    et al.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Gamberale-Stille, Gabriella
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Leimar, Olof
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Multi-trait mimicry and the relative salience of individual traits2015Inngår i: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 282, nr 1818, artikkel-id 20152127Artikkel i tidsskrift (Fagfellevurdert)
    Abstract [en]

    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 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.

  • 23.
    Kazemi, Baharan
    et al.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Gamberale-Stille, Gabriella
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Wåtz, Therese
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Wiklund, Christer
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Leimar, Olof
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Learning of salient prey traits explains Batesian mimicry evolution2018Inngår i: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 72, nr 3, s. 531-539Artikkel i tidsskrift (Fagfellevurdert)
    Abstract [en]

    Batesian mimicry evolution involves an initial major mutation that produces a rough resemblance to the model, followed by smaller improving changes. To examine the learning psychology of this process, we applied established ideas about mimicry in Papilio polyxenes asterius of the model Battus philenor. We performed experiments with wild birds as predators and butterfly wings as semiartificial prey. Wings of hybrids of P. p. asterius and Papilio machaon were used to approximate the first mutant, with melanism as the hypothesized first mimetic trait. Based on previous results about learning psychology and imperfect mimicry, we predicted that: melanism should have high salience (i.e., being noticeable and prominent), meaning that predators readily discriminate a melanistic mutant from appearances similar to P. machaon; the difference between the first mutant and the model should have intermediate salience to allow further improvement of mimicry; and the final difference in appearance between P. p. asterius and B. philenor should have very low salience, causing improvement to level off. Our results supported both the traditional hypothesis and all our predictions about relative salience. We conclude that there is good agreement between long-held ideas about how Batesian mimicry evolves and recent insights from learning psychology about the role of salience in mimicry evolution.

  • 24.
    Nylin, Sören
    et al.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen, Avdelningen för zoologisk ekologi.
    Söderlind, Lina
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen, Avdelningen för zoologisk ekologi.
    Gamberale-Stille, Gabriella
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen, Avdelningen för etologi.
    Audusseau, Hélène
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen, Avdelningen för zoologisk ekologi.
    Celorio-Mancera, Maria de la Paz
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen, Avdelningen för zoologisk ekologi.
    Janz, Niklas
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen, Avdelningen för zoologisk ekologi.
    Sperling, Felix A. H.
    Vestiges of an ancestral host plant: preference and performance in the butterfly Polygonia faunus and its sister species P. c-album2015Inngår i: Ecological Entomology, ISSN 0307-6946, E-ISSN 1365-2311, Vol. 40, nr 3, s. 307-315Artikkel i tidsskrift (Fagfellevurdert)
    Abstract [en]

    1. In the study of the evolution of insect-host plant interactions, important information is provided by host ranking correspondences among female preference, offspring preference, and offspring performance. Here, we contrast such patterns in two polyphagous sister species in the butterfly family Nymphalidae, the Nearctic Polygonia faunus, and the Palearctic P. c-album. 2. These two species have similar host ranges, but according to the literature P. faunus does not use the ancestral host plant clade-the urticalean rosids'. Comparisons of the species can thus test the effects of a change in insect-plant associations over a long time scale. Cage experiments confirmed that P. faunus females avoid laying eggs on Urtica dioica (the preferred host of P. c-album), instead preferring Salix, Betula, and Ribes.3. However, newly hatched larvae of both species readily accept and grow well on U. dioica, supporting the general theory that evolutionary changes in host range are initiated through shifts in female host preferences, whereas larvae are more conservative and also can retain the capacity to perform well on ancestral hosts over long time spans.4. Similar rankings of host plants among female preference, offspring preference, and offspring performance were observed in P. c-album but not in P. faunus. This is probably a result of vestiges of larval adaptations to the lost ancestral host taxon in the latter species. 5. Female and larval preferences seem to be largely free to evolve independently, and consequently larval preferences warrant more attention.

  • 25.
    Schäpers, Alexander
    et al.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen, Avdelningen för zoologisk ekologi.
    Carlsson, Mikael A.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen, Avdelningen för funktionell zoomorfologi.
    Gamberale Stille, Gabriella
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen, Avdelningen för etologi.
    Janz, Niklas
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen, Avdelningen för zoologisk ekologi.
    The Role of Olfactory Cues for the Search Behavior of a Specialist and Generalist Butterfly2015Inngår i: Journal of insect behavior, ISSN 0892-7553, E-ISSN 1572-8889, Vol. 28, nr 1, s. 77-87Artikkel i tidsskrift (Fagfellevurdert)
    Abstract [en]

    Searching for resources is often a challenging task, especially for small organisms such as insects. Complex stimuli have to be extracted from the environment and translated into a relevant behavioral output. A first step in this process is to investigate the relative roles of the different senses during search for various resources. While the role of olfaction is well documented in nocturnal moths, the olfactory abilities of the closely related diurnal butterflies are poorly explored. Here we investigated how olfactory information is used in the search for host plants and asked if these abilities varied with levels of stimulus complexity. Thus, we tested two nymphalid butterfly species with divergent host plant range in a two-choice olfactometer testing different combinations of host and non-host plants. The experiments show both the monophagous Aglais urticae and the polyphagous Polygonia c-album could navigate towards an odor source, but this ability varied with context. While mated females exhibited a preference for their host plant, unmated females of both species did not show a preference for host plant cues. Furthermore, both species showed inabilities to make fine-tuned decisions between hosts. We conclude that olfactory cues are important for butterflies to navigate towards targets. We argue that there are limitations on how much information can be extracted from host volatiles. These results are discussed in the light of neural processing limitations and degree of host plant specialization, suggesting the necessity of other sensory modalities to sharpen the decision process and facilitate the final oviposition event.

  • 26.
    Söderlind, Lina
    et al.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Janz, Niklas
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Gamberale-Stille, Gabriella
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Nylin, Sören
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    When mother does not know best: Contrasting host plant choice across life stages in individuals of the comma butterflyManuskript (preprint) (Annet vitenskapelig)
    Abstract [en]

    Since host plant choice is often crucial for the fitness of herbivorous insects we investigated if individual variation in such decisions is consistent throughout life. In the comma butterfly, Polygonia c-album, (Nymphalidae, Nymphalini) newly hatched larvae and adult females have been found to rank hosts plants similarly, suggesting that the host plant recognition mechanisms could be preserved through metamorphosis. 

    We measured preference for Urtica dioica relative to Salix cinerea when the plants were encountered by the same individuals in the two different life stages, finding no relationship between the two measurements. This was however found when we instead measured acceptance of a suboptimal host: First instar larvae were placed on the suboptimal S. cinerea, and were scored as to whether they accepted this host or if they instead moved to feed on the generally more preferred host U. dioica. The same individuals were then tested once more as ovipositing females, in a cage setup arranged so that females would encounter the low-ranked hosts S. cinerea and Betula pubescens more often than the high-ranked host U. dioica.

    Individuals that chose to abandon S. cinerea as larvae differed in oviposition behaviour later in life from those that accepted this low-ranked host, but did so by laying a higher proportion eggs on the low-ranked hosts as adults. We interpret this initially unexpected result as a result of possible genetic correlation between female host-plant specificity and larval acceptance for the plant chosen by their mother: Offspring of ‘choosy’ specialist mothers have a strong tendency to remain on their original host, whereas less discriminating generalist mothers beget larvae with lower acceptance for their original plant when it is suboptimal. Ecologically, this presents a further explanation for how a generalist oviposition strategy can be sustained since larval mobility to some extent compensates for poor female choice.

  • 27.
    Tullberg, Birgitta S.
    et al.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen. Zoologisk ekologi.
    Gamberale-Stille, Gabriella
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen. Etologi.
    Bohlin, Titti
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen. Zoologisk ekologi.
    Merilaita, Sami
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen. Zoologisk ekologi.
    Seasonal ontogenetic colour plasticity in the adult striated shieldbug Graphosoma lineatum (Heteroptera) and its effect on detectability2008Inngår i: Behavioral Ecology and Sociobiology, ISSN 1432-0762, Vol. 62, nr 9, s. 1389-1396Artikkel i tidsskrift (Fagfellevurdert)
    Abstract [en]

    Camouflage and warning colouration are two important forms of protective colouration. We have studied the detectability of two seasonal colourations in the aposematic striated shieldbug, Graphosoma lineatum. The typical colouration of this insect is red and black, which is also the colouration of the reproductive post-hibernation bugs in our study area in south central Sweden. However, the majority of newly eclosed adults in late summer exhibit a ‘pale’ (light brownish, non-red) and black striation, and these bugs appear quite cryptic to the human eye when sitting on the dried stems and umbels of their host plants. In experiments using photographs of prey in the late-summer habitat shown on a computer screen, we compared the time to detection by human subjects of bugs, which had been manipulated to show either of the two typical seasonal colourations. Time to detection was significantly longer for the pale and black than for the red-and-black striation in images with the bug photographed at two different distances. This indicates that the pale pre-hibernation striation may have a cryptic function. In a separate experiment, we tested detectability of striated and non-striated manipulations of bug pre-hibernation colouration against the late-summer background, and found that time to detection was significantly longer for the striated bugs. We discuss potential functional explanations for the seasonal ontogenetic colour plasticity and suggest that the epidermal pale colour in the late summer provides a benefit of increased camouflage.

  • 28.
    Van Dijk, Laura J. A.
    et al.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Janz, Niklas
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Schäpers, Alexander
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Gamberale-Stille, Gabriella
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Carlsson, Mikael A.
    Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
    Experience-dependent mushroom body plasticity in butterflies: consequences of search complexity and host range2017Inngår i: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 284, nr 1866, artikkel-id 20171594Artikkel i tidsskrift (Fagfellevurdert)
    Abstract [en]

    An ovipositing insect experiences many sensory challenges during her search for a suitable host plant. These sensory challenges become exceedingly pronounced when host range increases, as larger varieties of sensory inputs have to be perceived and processed in the brain. Neural capacities can be exceeded upon information overload, inflicting costs on oviposition accuracy. One presumed generalist strategy to diminish information overload is the acquisition of a focused search during its lifetime based on experiences within the current environment, a strategy opposed to a more genetically determined focus expected to be seen in relative specialists. We hypothesized that a broader host range is positively correlated with mushroom body (MB) plasticity, a brain structure related to learning and memory. To test this hypothesis, butterflies with diverging host ranges (Polygonia c-album, Aglais io and Aglais urticae) were subjected to differential environmental complexities for oviposition, after which ontogenetic MB calyx volume differences were compared among species. We found that the relative generalist species exhibited remarkable plasticity in ontogenetic MB volumes; MB growth was differentially stimulated based on the complexity of the experienced environment. For relative specialists, MB volume was more canalized. All in all, this study strongly suggests an impact of host range on brain plasticity in Nymphalid butterflies.

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