Visual Signalling in Plant-Animal Interactions

<p>The process of visual signalling between plant and animals is often a combination of exciting discoveries and more often than not; highly controversial hypotheses. Plants and animals interact mutualistically and antagonistically creating a complex network of species relations to some extent suggesting a co evolutionary network. In this study, I investigate two basic research questions: the first is how plants utilize aposematic and cryptic colours? The second is how animals are affected by the colour signals broadcasted by plants? By using the avian eye model, I discover how visual signals/colours from plants are actually perceived, and the effects of these signals on birds (not human) perception. Aposematism and crypsis are common strategies utilized by animals, yet little evidence is known of such occurrences in plants. Aposematic and cryptic colours were evaluated by studying different colouration strategy through the ontogeny of two native heteroblastic New Zealand plants: Pseudopanax crassifolius and Elaeocarpus hookerianus. To determine the potential effect of colour signals on animals, I investigated an evolutionary theory of leaf colours constraining the conspicuousness of their fruit colour counterparts. Based on the available data, I also conducted a community level analysis about the effects of fruit colours and specific avian frugivores that might be attracted to them. Finally, I examined the fruit colour selection by a frugivorous seed dispersing insect; the Wellington Tree Weta (Hemideina crassidens). My result shows that aposematic and cryptic colours are successfully applied by plants to either warn or remain inconspicuous from browsing herbivores. The evidence I presented lends support to the Moa browsing hypothesis in relation to constraining the conspicuousness of their fruit colour counterparts. Based on the cryptic plant colourations. However, the same level of selective interaction could not be inferred for frugivore fruit colour selection based on avian vision. I demonstrated that leaf reflectance does not constrain/influence the conspicuousness of fruit colours. There was also no fruit colour diversity based on geographical location. Fruit colour alone is not sufficient to influence a specific frugivore assemblage. Other environmental factors and species interaction must be taken into account. Weta proved to possess colour vision capable of colour perception even in low light conditions. Weta also consistently selected naturally blue streaked and manipulated blue coloured fruits of Coprosma acerosa in a binary test. This supports the idea of weta co- evolving with fruit colours of certain divaricating plants in New Zealand. I suggest that the fruit colours of New Zealand are shaped by the combined selection pressure from birds, lizards/geckos and weta.</p>

Visual Signalling in Plant-Animal Interactions

<p>The process of visual signalling between plant and animals is often a combination of exciting discoveries and more often than not; highly controversial hypotheses. Plants and animals interact mutualistically and antagonistically creating a complex network of species relations to some extent suggesting a co evolutionary network. In this study, I investigate two basic research questions: the first is how plants utilize aposematic and cryptic colours? The second is how animals are affected by the colour signals broadcasted by plants? By using the avian eye model, I discover how visual signals/colours from plants are actually perceived, and the effects of these signals on birds (not human) perception. Aposematism and crypsis are common strategies utilized by animals, yet little evidence is known of such occurrences in plants. Aposematic and cryptic colours were evaluated by studying different colouration strategy through the ontogeny of two native heteroblastic New Zealand plants: Pseudopanax crassifolius and Elaeocarpus hookerianus. To determine the potential effect of colour signals on animals, I investigated an evolutionary theory of leaf colours constraining the conspicuousness of their fruit colour counterparts. Based on the available data, I also conducted a community level analysis about the effects of fruit colours and specific avian frugivores that might be attracted to them. Finally, I examined the fruit colour selection by a frugivorous seed dispersing insect; the Wellington Tree Weta (Hemideina crassidens). My result shows that aposematic and cryptic colours are successfully applied by plants to either warn or remain inconspicuous from browsing herbivores. The evidence I presented lends support to the Moa browsing hypothesis in relation to constraining the conspicuousness of their fruit colour counterparts. Based on the cryptic plant colourations. However, the same level of selective interaction could not be inferred for frugivore fruit colour selection based on avian vision. I demonstrated that leaf reflectance does not constrain/influence the conspicuousness of fruit colours. There was also no fruit colour diversity based on geographical location. Fruit colour alone is not sufficient to influence a specific frugivore assemblage. Other environmental factors and species interaction must be taken into account. Weta proved to possess colour vision capable of colour perception even in low light conditions. Weta also consistently selected naturally blue streaked and manipulated blue coloured fruits of Coprosma acerosa in a binary test. This supports the idea of weta co- evolving with fruit colours of certain divaricating plants in New Zealand. I suggest that the fruit colours of New Zealand are shaped by the combined selection pressure from birds, lizards/geckos and weta.</p>

Major Flower Pigments Originate Different Colour Signals to Pollinators

Flower colour is mainly due to the presence and type of pigments. Pollinator preferences impose selection on flower colour that ultimately acts on flower pigments. Knowing how pollinators perceive flowers with different pigments becomes crucial for a comprehensive understanding of plant-pollinator communication and flower colour evolution. Based on colour space models, we studied whether main groups of pollinators, specifically hymenopterans, dipterans, lepidopterans and birds, differentially perceive flower colours generated by major pigment groups. We obtain reflectance data and conspicuousness to pollinators of flowers containing one of the pigment groups more frequent in flowers: chlorophylls, carotenoids and flavonoids. Flavonoids were subsequently classified in UV-absorbing flavonoids, aurones-chalcones and the anthocyanins cyanidin, pelargonidin, delphinidin, and malvidin derivatives. We found that flower colour loci of chlorophylls, carotenoids, UV-absorbing flavonoids, aurones-chalcones, and anthocyanins occupied different regions of the colour space models of these pollinators. The four groups of anthocyanins produced a unique cluster of colour loci. Interestingly, differences in colour conspicuousness among the pigment groups were almost similar in the bee, fly, butterfly, and bird visual space models. Aurones-chalcones showed the highest chromatic contrast values, carotenoids displayed intermediate values, and chlorophylls, UV-absorbing flavonoids and anthocyanins presented the lowest values. In the visual model of bees, flowers with UV-absorbing flavonoids (i.e., white flowers) generated the highest achromatic contrasts. Ours findings suggest that in spite of the almost omnipresence of floral anthocyanins in angiosperms, carotenoids and aurones-chalcones generates higher colour conspicuousness for main functional groups of pollinators.

Variation in colour signals among Sarracenia pitcher plants and the potential role of areoles in the attraction of flying Hymenoptera

Sarracenia insectivorous plants show a diversity of visual features in their pitchers but their perception by insects and their role in attraction, have received little attention. They also vary in prey composition, with some species trapping more flying Hymenoptera, such as bees. To test the hypothesis of a link between visual signal variability and prey segregation ability, and to identify which signal could attract flying Hymenoptera, we characterised, the colour patterns of 32 pitchers belonging to four taxa, modelled their perception by flying Hymenoptera, and examined the prey they trapped. The pitchers of the four taxa differed in colour patterns, with notably two long-leaved taxa displaying clear areoles, which contrasted strongly in colour and brightness with the vegetative background and with other pitcher areas in the eyes of flying Hymenoptera. These taxa trapped high proportion of flying hymenoptera. This suggests that contrasting areoles may act as a visual lure for flying Hymenoptera, making plants particularly visible to these insects. Prey capture also differed according to pitcher stage, morphology, season and visual characteristics. Further studies on prey visitation are needed to better understand the link between prey capture and attraction feature.

Decoding of EEG signals reveals non-uniformities in the neural geometry of colour

The idea of colour opponency maintains that colour vision arises through the comparison of two chromatic mechanisms, red versus green (RG) and yellow versus blue (YB). The four unique hues, red, green, blue, and yellow, are assumed to appear at the null points of these the two chromatic systems. However, whether unique hues have a distinct signature that can be reliably discerned in neural activity is still an open question. Here we hypothesise that, if unique hues represent a tractable cortical state, they should elicit more robust activity compared to non-unique hues. We use a spatiotemporal decoding approach to reconstruct an activation space for a set of unique and intermediate hues across a range of luminance values. We show that electroencephalographic (EEG) responses carry robust information about isoluminant unique hues within a 100-300 ms window from stimulus onset. Decoding is possible in both passive and active viewing tasks, but is compromised when concurrent high luminance contrast is added to the colour signals. The efficiency of hue decoding is not entirely predicted by their mutual distance in a nominally uniform colour space. Instead, the encoding space shows pivotal non-uniformities which suggest that anisotropies in neurometric hue-spaces are likely to represent perceptual unique hues. Furthermore, the neural code for hue temporally coincides with the neural code for luminance contrast, thus explaining why potential neural correlates of unique hues have remained so elusive until now.

Colour Discrimination From Perceived Differences by Birds

The ability of visual generalists to see and perceive displayed colour signals is essential to understanding decision making in natural environments. Whilst modelling approaches have typically considered relatively simple physiological explanations of how colour may be processed, data on key bee species reveals that colour is a complex multistage perception largely generated by opponent neural representations in a brain. Thus, a biologically meaningful unit of colour information must consider the psychophysics responses of an animal engaged in colour decision making. We extracted previously collected psychophysics data for a Violet-Sensitive (VS) bird, the pigeon (Columba livia), and used a non-linear function that reliably represents the behavioural choices of hymenopteran and dipteran pollinators to produce the first behaviourally validated and biologically meaningful representation of how VS birds use colour information in a probabilistic way. The function describes how similar or dis-similar spectral information can lead to different choice behaviours in birds, even though all such spectral information is above discrimination threshold. This new representation of bird vision will enable enhanced modelling representations of how bird vision can sense and use colour information in complex environments.

Inter-Individual Differences in Ornamental Colouration in a Mediterranean Lizard in Relation to Altitude, Season, Sex, Age, and Body Traits

Animals frequently show complex colour patterns involved in social communication, which attracts great interest in evolutionary and behavioural ecology. Most researchers interpret that each colour in animals with multiple patches may either signal a different bearer’s trait or redundantly convey the same information. Colour signals, moreover, may vary geographically and according to bearer qualities. In this study, we analyse different sources of colour variation in the eastern clade of the lizard Psammodromus algirus. Sexual dichromatism markedly differs between clades; both possess lateral blue eyespots, but whereas males in the western populations display strikingly colourful orange-red throats during the breeding season, eastern lizards only show some commissure pigmentation and light yellow throats. We analyse how different colour traits (commissure and throat colouration, and the number of blue eyespots) vary according to body size, head size (an indicator of fighting ability), and sex along an elevational gradient. Our findings show that blue eyespots function independently from colour patches in the commissure and throat, which were interrelated. Males had more eyespots and orange commissures (which were yellow or colourless in females). Throat colour saturation and the presence of coloured commissures increased in older lizards. The number of eyespots, presence of a coloured commissure, and throat colour saturation positively related to head size. However, while the number of eyespots was maximal at lowlands, throat colour saturation increased with altitude. Overall, our results suggest that this lizard harbours several colour signals, which altitudinally differ in their importance, but generally provide redundant information. The relevance of each signal may depend on the context. For example, all signals indicate head size, but commissure colouration may work well at a short distance and when the lizard opens the mouth, while both throat and eyespots might work better at long distance. Meanwhile, throat colouration and eyespots probably work better in different light conditions, which might explain the altitudinal variation in the relative importance of each colour component.

Simulations with Australian dragon lizards suggest movement-based signal effectiveness is dependent on display structure and environmental conditions

Habitat-specific characteristics can affect signal transmission such that different habitats dictate the optimal signal. One way to examine how the environment influences signals is by comparing changes in signal effectiveness in different habitats. Examinations of signal effectiveness between different habitats has helped to explain signal divergence/convergence between populations and species using acoustic and colour signals. Although previous research has provided evidence for local adaptations and signal divergence in many species of lizards, comparative studies in movement-based signals are rare due to technical difficulties in quantifying movements in nature and ethical restrictions in translocating animals between habitats. We demonstrate herein that these issues can be addressed using 3D animations, and compared the relative performance of the displays of four Australian lizard species in the habitats of each species under varying environmental conditions. Our simulations show that habitats differentially affect signal performance, and an interaction between display and habitat structure. Interestingly, our results are consistent with the hypothesis that the signal adapted to the noisier environment does not show an advantage in signal effectiveness, but the noisy habitat was detrimental to the performance of all displays. Our study is one of the first studies for movement-based signals that directly compares signal performance in multiple habitats, and our approach has laid the foundation for future investigations in motion ecology that have been intractable to conventional research methods.

Sex-specific signalling of individual personality by a mutual plumage ornament in a passerine

The significance of colour signals in species with strong sexual dimorphism and/or elaborated visual ornaments is rather well-understood. Less attention has, however, been devoted to study colour signals in species with weak or no apparent sexual dimorphism. In such species, an interesting possibility arises as both sexes can bear the same colour ornament(s) (i.e. sexes are mutually ornamented), but their signalling value might differ in males and females. We aimed to explore this possibility by investigating the phenotypic correlates of the black bib, a melanin-based plumage ornament, in the Eurasian tree sparrow (Passer montanus). More specifically, we studied the sex-dependent relationships between bib size and three aspects of individuals’ phenotype: body condition (i.e. size-corrected body mass), physiology (i.e. cellular innate immunity/inflammation status, expressed through total leucocyte counts, and chronic physiological stress, expressed through the ratio of heterophils to lymphocytes) and individual personality (i.e. activity in a novel environment). We found that bib size was not associated with body condition and cellular innate immunity/inflammation status, but was positively related to physiological stress levels independent of sex. Furthermore, bib size was negatively associated with activity in males but positively in females. Our findings bring important correlative evidence that mutual ornamental traits may have sex-specific signalling value. Significance statement The signalling role of elaborated colourful ornaments, that are usually possessed only by males in sexually dimorphic species, is well-established. The function of various colour traits which are borne by both sexes (i.e. mutual ornaments), however, is less obvious. Do they have a signalling value in both sexes? If yes, do they signal the same information in males and females? Or, most intriguingly, can they convey different information in the two sexes? To test these alternatives, we studied the signalling value of the black bib, a melanin-based mutual plumage ornament, in Eurasian tree sparrows (Passer montanus). Apart from being correlated with chronic stress in both sexes, bib size was positively related to activity in females but negatively in males. Our results suggest that the information content of the same colour trait in males and females can be different in mutually ornamented species.

Effectiveness of movement-based animal signals is a function of display structure and habitat characteristics: simulations of Australian dragons

Habitat-specific characteristics can affect signal transmission such that different habitats dictate the optimal signal. One way to examine how the environment influences signals is by comparing changes in signal efficacy in different habitats. Examinations of signal efficacy between different habitats has helped to explain signal divergence/convergence between populations and species utilising acoustic and colour signals. Although previous research has provided evidence for local adaptations and signal divergence in many species of lizards, comparative studies in movement-based signals are rare due to technical difficulties in quantifying movements in nature and ethical restrictions in translocating animals between habitats. We demonstrate herein that these issues can be addressed using 3D animations, and compared the relative performance of the displays of four Australian lizard species in the habitats of each species under varying environmental conditions. Our simulations show that habitats differentially affect signal performance, and an interaction between display and habitat structure. Interestingly, the signal adapted to the noisier environment did not show an advantage in signal efficacy, but the noisy habitat was detrimental to the performance of all displays. Our study is one of the first studies for movement-based signals that directly compares signal performance in multiple habitats, and our approach has laid the foundation for future investigations in motion ecology that have been intractable to conventional research methods.