Conspicuousness, not colour as foraging cue in plant–animal signalling

The global prevalence of red and black fruits has still not been explained. Hypotheses based on innate consumer preferences have been tested and rejected. Though colour itself plays an important role in animal foraging, it is only one component of signals. Another major component are colour contrasts against background achieving the conspicuousness of signals. In order to evaluate which signal component determines consumers behaviour, we measured fruit colour and colour contrasts of 43 species against their natural background under ambient light conditions. Red and black fruits exhibit stronger contrasts and are therefore more conspicuous to consumers than fruits of other colours. Subsequently, trials were carried out to determine whether colour or conspicuousness influences avian food choice. Four bird species strongly preferred contrasting red–green or black–green over uni-coloured red, green, or black fruit displays, while no preference for particular hues was found. We therefore hypothesize that conspicuousness determines avian food selection and define the contrast hypothesis: Diurnal dispersers select fruit colours based on their conspicuousness and not their colour itself.
Because colour vision is an ancient trait, the entire heterogeneous group of frugivorous birds most likely perceives conspicuousness uniformly over evolutionary time spans. Conspicuousness has thus the potential to explain the global prevalence of red and black fruits.     

Weta and the evolution of fleshy fruits in New Zealand

Fleshy fruits are typically coloured either red or black and are displayed in conspicuous locations where they can be easily located by birds. However, fleshy fruits in New Zealand are often white or translucently coloured and are displayed in the inner recesses of plant canopies. These characteristics have been attributed to coevolution with reptiles. I describe seed dispersal by a ground weta in Nelson lakes National Park, and hypothesise that the unusual characteristics of fleshy fruits in New Zealand may result from coevolution with weta.     

Signals of profitability? Food colour preferences in migrating juvenile blackcaps differ for fruits and insects

Red is a common colour signal in both aposematic warning displays, and in fruit displays. One common feature is that red is conspicuous against the natural background of the prey and fruits. However, there is a potential conflict between fruits and aposematic prey in how a bird predator should react to red colours, where fruits aim to attract birds and aposematic insects aim to ward off, often the same bird individuals. Here we investigate possible differences in red/green colour preferences of frugivorous, wild-caught, young blackcaps (Sylvia atricapilla), when food is either a fruit or an insect. Birds in two groups were presented with a series of pairs of food items that had been artificially painted red and green, in the order of (I) fruits, crickets and maggots, or (II) crickets, fruits, and maggots. Birds first presented with crickets or fruits differed in first attacks directed at the two colours: They showed no colour preference between fruits, but showed a clear preference for green over red crickets. Also, birds in both experimental groups clearly preferred green to red maggots. These results provide evidence that wild, frugivorous birds are able to differentiate between prey types, and show different colour preferences depending on whether food is insect or fruit. We conclude that blackcaps show an attack bias against red insects, and that one important function of the signal in insects, is to inhibit attack after discovery. However, the lack of preference for red fruits suggests other functions to red fruit displays, such as facilitating discovery per se, rather than directly stimulating attack after discovery.     

Mutualism or opportunism? Tree fuchsia (Fuchsia excorticata) and tree weta (Hemideina) interactions

Mutualisms or interspecific interactions involving net mutual benefits, are an important component of ecological theory, although effectively demonstrating mutualism is notoriously difficult. Among two New Zealand endemics, a slightly elevated germination rate of Fuchsia excorticata (Onagraceae) seeds after passage through tree weta (Orthoptera: Anostostomatidae) compared with seeds manually extracted from fruit, led to the proposal that a mutualistic relationship exists between this plant and animal. An improved germination rate, or any other single trait, however, does not alone constitute evidence for mutualism; the relative costs and benefits of numerous components of the interaction need to be accounted for. We considered the costs and benefits to F. excorticata of the putative seed dispersal mutualism with tree weta. Tree weta provided with F. excorticata fruits destroyed 78% of the seeds they consumed, did not move fruit; and faeces containing seeds were deposited near their roost holes (which are naturally in trees). The seeds remaining after fruit consumption and those that are ingested but survive gut passage are unlikely to be deposited in suitable habitat for seedling survival. Plant food preferences of captive tree weta assessed using pairwise leaf choice tests showed that the leaves of F. excorticata were the least preferred of six commonly encountered plants. In addition, we found that tree weta did not show a preference for F. excorticata fruit over a standard leafy diet, indicating they are unlikely to be actively seeking fruit in preference to other sources of food. These observations indicate that any interaction between tree weta and F. excorticata is likely to be opportunistic rather than mutualistic, and highlight the difficulty of characterizing such interactions.     

Ecology of the fruit-colour polymorphism in Rubus spectabilis

Although some studies have focused on the colour polymorphisms of flowers and fruits, little is known of their ecological and evolutionary significance. We investigated the potential contribution of several factors to the maintenance of fruit-colour polymorphism in Rubus spectabilis, a common shrub in the temperate rainforests of southeast Alaska. Fruits occur in two colours (red and orange), whose frequencies vary geographically. The two colour morphs have similar size, weight, seed load and nutrient composition. Colour preferences of avian frugivores, in the aviary and in the field, varied among individuals, but the majority favoured red fruits. Seed predators (mostly rodents) did not discriminate between seeds from different morphs. The effect of seed passage through the digestive tract of frugivores (birds and bears) on germination was similar for both morphs, although there were significant differences among frugivores. The type of soil on which the seeds are deposited influenced their germination behaviour, suggesting that some soils could favour one morph over the other. Such differences may contribute to the regional differences in frequencies of the two morphs. This study emphasizes the need to investigate fruit and seed characteristics that correlate with fruit colour; the colour preferences of consumers is only one of several selection pressures that determine the frequency distribution of fruit colours. This revised version was published online in July 2006 with corrections to the Cover Date.     

Fruit Colour Preferences of Redwings (Turdus iliacus): Experiments with Hand-Raised Juveniles and Wild-Caught Adults

Certain fruit colours and their contrast with the background coloration are suggested to attract frugivorous birds. To test the attractiveness of different colours, we performed three experiments in laboratory with controlled light conditions. In the first two experiments, we studied the fruit colour preferences of naive juvenile redwings. In the third experiment, we continued to investigate whether the contrast of the fruit colour with the background coloration affects the preference of both naive juveniles and experienced adult redwings. In the first experiment, juvenile birds preferred black, UV‐blue and red berries, to white ones. In pairwise trials, a new set of juveniles still preferred red berries to white ones. When testing the effect of contrasts on their choice, juveniles preferred UV‐blue berries to red ones on a UV‐blue background. However, no preference was found, when the background was either red or green. Adult redwings preferred UV‐blue berries to red ones on all backgrounds. According to these results, juveniles seem to have an innate avoidance of white berries. Furthermore, the foraging decisions of fruit‐eating birds are affected more by fruit colour than its contrast with background coloration, at least when contrasting displays are encountered from relatively short distances. Differences in preferences of adult and juvenile birds also indicate that learning seems to play a role in fruit choices.     

Effects of forest edges, fruit display size, and fruit colour on bird seed dispersal in a New Zealand mistletoe,

This study examined how forest edges, fruit display size, and fruit colour influenced rates of seed dispersal in an endemic, bird-dispersed, New Zealand mistletoe species, Alepis flavida. To examine rates of seed dispersal, fruit removal rates were compared between plants growing on forest edges and in forest interior, and also between two morphs of plants with different coloured fruits. Two aspects of fruit display size were examined: plant size and the neighbourhood of conspecific plants. There was no overall difference in fruit removal rates on forest edges and in forest interior, but birds removed fruits from red-fruited plants at a faster rate than from orange-fruited plants. Proximity of plant neighbours interacted with edges to influence fruit removal rates. The smaller the distance to nearest neighbours, the greater the fruit removal rates for orange-fruited plants in both habitats, but this relationship was significant for red-fruited plants only in the interior. Plant size affected fruit removal rates for orange-fruited plants, but not for red-fruited plants, and these differences were consistent in both habitats. Thus, fruit colour had the strongest effects on rates of fruit removal in this system, but forest edges also affected fruit removal rates, via altering the effects of neighbouring plants. Although birds prefer red fruits, there appears to be little selection pressure against orange-fruited plants because fruit removal rates are very high for both morphs.     

Geographic patterns in fruit colour diversity: do leaves constrain the colour of fleshy fruits?

We tested for geographic patterns in fruit colour diversity. Fruit colours are thought to promote detection by seed dispersers. Because seed dispersers differ in their spectral sensitivities, we predicted that fruit colour diversity would be higher in regions with higher seed disperser diversity (i.e. the tropics). We collected reflectance data on 232 fruiting plant species and their natural backgrounds in seven localities in Europe, North and South America, and analysed fruit colour diversity according to the visual system of birds—the primary consumer types of these fruits. We found no evidence that fruit colours are either more conspicuous or more diverse in tropical areas characterised by higher seed disperser diversity. Instead, fruit colour diversity was lowest in central Brazil, suggesting that fruit colours may be more diverse in temperate regions. Although we found little evidence for geographic variation in fruit hues, the spectral properties of fruits were positively associated with the spectral properties of backgrounds. This result implies that fruit colours may be influenced by selection on the reflectance properties of leaves, thus constraining the evolution of fruit colour. Overall, the results suggest that fruit colours in the tropics are neither more diverse nor more conspicuous than temperate fruits, and that fruit colours may be influenced by correlated selection on leaf reflectance properties. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Signal convergence in fruits: a result of selection by frugivores?

The Dispersal Syndrome hypothesis remains contentious, stating that apparently nonrandom associations of fruit characteristics result from selection by seed dispersers. We examine a key assumption under this hypothesis, i.e. that fruit traits can be used as reliable signals by frugivores. We first test this assumption by looking at whether fruit colour allows birds and primates to distinguish between fruits commonly dispersed by birds or primates. Second, we test whether the colours of fruits dispersed by primates are more contrasting to primates than the colours of bird‐dispersed fruits, expected if fruit colour is an adaptation to facilitate the detection by seed dispersers. Third, we test whether fruit colour has converged in unrelated plant species dispersed by similar frugivores. We use vision models based on peak sensitivities of birds’ and primates’ cone cells. We base our analyses on the visual systems of two types of birds (violet and ultraviolet based) and three types of primates (trichromatic primates from the Old and the New Worlds, and a dichromatic New World monkey). Using a Discriminant Function Analysis, we find that all frugivore groups can reliably discriminate between bird‐ and primate‐dispersed fruits. Fruit colour can be a reliable signal to different seed dispersers. However, the colours of primate‐dispersed fruits are less contrasting to primates than those of bird‐dispersed fruits. Fruit colour convergence in unrelated plants is independent of phylogeny and can be better explained by disperser type, which supports the hypothesis that frugivores are important in fruit evolution. We discuss adaptive and nonadaptive hypotheses that can potentially explain the pattern we found.     

Seed dispersal effectiveness increases with body size in New Zealand alpine scree weta (Deinacrida connectens)

Weta are giant, flightless orthopterans that are endemic to New Zealand. Although they are known to consume fleshy fruits and disperse seeds after gut passage, which is unusual among insects, their effectiveness as seed dispersal mutualists is debated. We conducted a series of laboratory experiments on alpine scree weta (Deinacrida connectens) and mountain snowberries (Gaultheria depressa) to investigate how fruit consumption rates, the proportion of ingested seeds dispersed intact and weta movement patterns vary with weta body sizes. On average weta dispersed 252 snowberry seeds nightly and travelled at a rate of 4 m min^?1. However, seed dispersal effectiveness varied over three orders of magnitude and was strongly associated with body sizes. Smaller weta consumed few snowberry seeds and acted primarily as seed predators. On the other hand, the largest weta consumed and dispersed thousands of seeds each night and appear to be capable of transporting seeds over large distances. Overall results indicate that scree weta shift from being weakly interacting seed predators to strongly interacting, effective seed dispersers as they increase in size.     

Red oilseed rape? The potential for manipulation of petal colour in control strategies for the pollen beetle (Meligethes aeneus)

The pollen beetle (Meligethes aeneus) is a major pest of oilseed rape (Brassica napus) at the inflorescence stage and is well known to prefer colours called yellow by human observers over many other colours. While commercial cultivars of oilseed rape have yellow flowers, little is known about the potential to manipulate host plant location and reduce subsequent infestation by this pest through variation in flower colour. We investigated the responses of pollen beetles to flowers of a white-petalled oilseed rape variety that had been dyed different colours in semi-field arena and field experiments. Flowers dyed blue or red were less heavily infested than those dyed yellow or the white flowers, indicating that blue and red flowers were less attractive than yellow and white ones. This response was most likely due to differences in petal colour because olfactometer studies showed that beetle responses to the odours of the coloured treatments did not differ. The comparatively high infestation of untreated white flowers is interpreted as a consequence of their high UV reflectance; the presence of a UV receptor in M. aeneus is suggested, and its role in visually guided insect–plant interactions in this species described. The potential for manipulation of petal colour in control strategies for the pollen beetle is discussed.     

Fruit size preference in the New Zealand pigeon (Hemiphaga novaeseelandiae)

Abstract We investigated whether the New Zealand pigeon Hemiphaga novaeseelandiae (Columbidae) exhibits size‐based preferences for fruits. We tested the hypothesis that in small‐fruited species, pigeons would prefer larger fruits, but in larger‐fruited species, this preference would reverse as the pigeons become increasingly limited by their gape size. We collected undispersed fruits and bird‐dispersed seeds of 10 plant species, some over several sites or years (13 datasets in total). We estimated the fruit size of dispersed seeds by fitting regressions of fruit diameter to seed diameter in intact fruits. We were able to predict fruit diameter from seed diameter in 12 of the 13 populations, although the relationship was stronger in single‐seeded species than in multi‐seeded species. Seven of the 12 populations tested showed a significant difference in seed diameter among undispersed and dispersed seeds. However, our results showed no consistent pattern in fruit size preference by the New Zealand pigeon and did not support our hypothesis. The large‐bodied New Zealand pigeon is generally not gape limited and fruit size preferences appear to be independent of mean fruit size.     

Learning and discrimination of coloured papers in the walking blowfly,Lucilia cuprina

Summary A new training and testing paradigm for walking sheep blowflies, Lucilia cuprina, is described. A fly is trained by presenting it with a droplet of sugar solution on a patch of coloured paper. After having consumed the sugar droplet, the fly starts a systematic search. While searching, it is confronted with an array of colour marks consisting of four colours displayed on the test cardboard (Fig. 1). Colours used for training and test include blue, green, yellow, orange, red, white and black.Before training, naive flies are tested for their spontaneous colour preferences on the test array. Yellow is visited most frequently, green least frequently (Table 2). Spontaneous colour preferences do not simply depend on subjective brightness (Table 1).The flies trained to one of the colours prefer this colour significantly (Figs. 5 and 9–11). This behaviour reflects true learning rather than sensitisation (Figs. 6–7). The blue and yellow marks are learned easily and discriminated well (Figs. 5, 9, 11). White is also discriminated well, although the response frequencies are lower than to blue and yellow (Fig. 11). Green is discriminated from blue but weakly from yellow and orange (Figs. 5, 9, 10). Red is a stimulus as weak as black (Figs. 8, 9). These features of colour discrimination reflect the spectral loci of colours in the colour triangle (Fig. 14).The coloured papers seem to be discriminated mainly by the hue of colours (Fig. 12), but brightness may also be used to discriminate colour stimuli (Fig. 13).     

Colour preferences in North Island robins (

There is growing awareness and concern in New Zealand about native birds eating poisonous baits intended for pest species such as brushtail possums (Trichosurus vulpecula) and rats (Rattus rattus, R.,norvegicus, R. exulans). We investigated the colour preferences of North Island robins (Petroica australis) a species known to be vulnerable to poisoning. The main aims were to determine if: (1) robins had colour preferences, (2) the preferences were consistent between two separate populations and 3) the preferences were similar to those found previously in weka (Gallirallus australis), another native species. Robins in Pureora Forest Park and Te Urewera National Park were individually offered a choice between differently coloured versions of a novel food (red, yellow, brown, green, light blue and medium blue) daily, for six consecutive days. Robins showed food colour preferences pecking more at the red, yellow and green cake than the medium blue, light blue or brown cake. No difference was evident in the colour preferences of the two populations. The colour preferences of robins were similar to those reported previously with weka. Dyeing poisonous baits may be sufficient to stop a proportion of robins from eating them. Further work is needed to determine how colour preferences vary across seasons, populations and species.     

Why birds eat colourful grit: colour preferences revealed by the colour of gizzard stones

Colour preferences from sexual or social contexts are assumed to have arisen owing to preferences for specific kinds of food, representing a sensory bias, but once colour preferences have evolved in a sexual context, they may also be expressed during foraging. We tested whether preferences for specific body colours (i.e. plumage and soft parts) were related to colour preferences for grit ingested by birds. Birds eat grit to facilitate break down of food by the gizzard, and this function is independent of the colour of grit, but depends on the physical properties of stones. Bird species were significantly consistent in colour of grit, and grit of different colours varied in prevalence among species, even when analyses were restricted to a sample from a single locality. There were positive correlations between presence of lilac and red grit in the gizzard and presence of sexually dichromatic lilac and red colour on the body. There was a positive correlation between red grit colour and red sexually monochromatic body colour. Bird species with many different sexual colours, but not sexually monochromatic colours on their body had many different colours of grit. Males had more lilac and red grit than females, with this effect differing among species, whereas that was not the case for grit of other colours. These findings are consistent with the sensory bias hypothesis that birds express preferences for grit of specific colours and a high diversity of colours related to sexual colouration of the body, even when the colour of such grit is only visible to the individual at the moment of ingestion.     

Insect colour preference compared to flower colours in the Australian Alps

An apparent predominance of plant taxa with pale flowers in the alpine floras of Australia and New Zealand may be due to the prevalence of insects, such as flies, that prefer pale colours and the absence of other types of potential pollinators that are attracted to bright colours such as social bees and birds. In this study, the diversity of flower colours, and the preference of insects for different colours were examined for the largest contiguous alpine area in Australia, around Mt Kosciuszko. Out of an alpine flora of 204 taxa, 127 species were found to have large showy flowers. The most common flower colour among these taxa was white (53.5%), then yellow (21.3%), followed by pink (6.3%), and cream (6.3%). Only a handful of taxa had red, blue, brown, green, orange or purple flowers. When the colour preference of insects was tested using five different coloured traps (white, yellow, orange, red and purple), the most successful traps were white then yellow, with these two colours accounting for 66% of all individual insects collected. Diptera were the most common insects caught (576 insects greater than 4 mm in length, 31 morphotaxa) showing an apparent preference for white and yellow coloured traps over others. Therefore, the results add some support to the proposition that the 'white' flora of the Australian Alps may be associated with the colour preference of flies, which have previously been found to be the most common type of pollinators in the Kosciuszko alpine zone.     

Mistletoe fruit‐colour polymorphism and differential success in a habitat mosaic

Abstract Polymorphisms in fruit colour are common in nature, but mechanistic explanations for the factor(s) responsible for their maintenance are for the most part lacking. Past studies have focused on frugivore colour preferences and fruit removal rates, but until recently there has been no evidence that these factors are responsible for the maintenance of the polymorphisms. For other types of genetic polymorphisms, habitat heterogeneity has been shown to play a role in their maintenance. Here we test the habitat heterogeneity hypothesis for a polymorphic New Zealand mistletoe. We show that red‐fruited and orange‐fruited morphs of the mistletoe Alepis flavida (Hook. F) Tiegh. (Loranthaceae) differ in their growth, mortality and flowering on forest edges and in forest interior. Red‐fruited morphs, which are preferred by dispersers, grew, survived and flowered as well as orange‐fruited morphs on edges, whereas orange‐fruited morphs had much greater growth, survival, and flowering than red‐fruited morphs in the forest interior. This is the first evidence that habitat‐specific differences in growth and survival may contribute to maintaining fruit‐colour polymorphisms.     

A generalised mimicry system involving angiosperm flower colour, pollen and bumblebees’ innate colour preferences

Flower colour is a major advertisement signal of zoophilous plants for pollinators. Bees, the main pollinators, exhibit innate colour preferences, which have often been attributed to only one single floral colour, though most flowers display a pattern of two or several colours. The existing studies of floral colour patterns are mostly qualitative studies. Using a model of bee colour vision we quantitatively investigate two questions: whether or not component colours of floral colour patterns may mimic pollen signals, and whether or not bumblebees exhibit innate preferences for distinct parameters of naturally existing floral colour patterns. We analysed the spectral reflectances of 162 plant species with multicoloured flowers and inflorescences, distiniguishing between inner and outer colours of floral colour patterns irrespective of the particular structures so coloured.We found that:– The inner colour of radially symmetrical flowers and inflorescences and of zygomorphic flowers appears less diverse to bees than the peripheral colour.– The inner colour of most radial flowers and inflorescences as well as the inner colour of a large number of non-related zygomorphic flowers appears to bees to be very similar to that of pollen.– Bumblebees (Bombus terrestris) exhibit innate preferences for two-coloured over single-coloured dummy flowers in a spontaneous choice test.– Bumblebees exhibit innate preferences for dummy flowers with a large over those with a small centre area.– Bumblebees exhibit innate preferences for dummy flowers with a centre colour similar to that of pollen over those with another centre colour.Our findings support the hypotheses that the inner component of floral colour patterns could be interpreted as a generalised and little recognised form of mimicry of the colour of visually displayed pollen, that bumblebees exhibit innate preferences regarding colour and size parameters of floral colour patterns, and that these correspond to visually displayed pollen. These findings together suggest a prominent role of floral colour patterns in advertisement to and guidance of naive flower visitors.     

Do colours that deter birds affect cereal bait acceptance by possums (

Poisonous baits used for pest control in New Zealand commonly contain green dye and cinnamon oil to make them less attractive to birds. Research aimed at reducing the impact of poison based pest control on birds has shown that some birds are initially deterred from feeding on blue or, to a lesser extent, green coloured food and are attracted to yellow or red food. We determined whether colours that deter or attract birds affected the acceptance of non-toxic and toxic cereal baits by captive brushtail possums (Trichosurus vulpecula). Individual possums were offered, daily, a choice between a standard green dyed non-toxic cereal bait and either a blue dyed(17 possums) or yellow dyed non-toxic bait (16 possums) for 10 days. Following this, for the first group of 17 possums, 1080 toxin was added to either the green bait (9 possums) or blue bait (8 possums) and possums were offered the green versus blue choice again. Two additional groups that had not previously been fed cereal baits were also given a choice between blue and green baits, one of which was toxic. All possums offered non-toxic bait ate less on the first day of presentation than on subsequent days. There was no difference in acceptance of either blue or yellow coloured non-toxic bait compared to the standard green non- toxic bait on any days. Bait colour appeared to be unimportant in cereal bait choice and did not deter possums from eating any of the baits. The addition of toxin to baits did not significantly alter bait choice in any groups, although some individuals which had no previous experience with baits ate more toxic than non-toxic bait. These data suggest that adding a stronger bird deterring colour (i.e., blue) to poisonous baits is unlikely to adversely affect the acceptance of baits by possums.     

Evidence from the domestication of apple for the maintenance of autumn colours by coevolution

The adaptive value of autumn colours is still a puzzle for evolutionary biology. It has been suggested that autumn colours are a warning signal to insects that use the trees as a host. I show that aphids (Dysaphis plantaginea) avoid apple trees (Malus pumila) with red leaves in autumn and that their fitness in spring is lower on these trees, which suggests that red leaves are an honest signal of the quality of the tree as a host. Autumn colours are common in wild populations but not among cultivated apple varieties, which are no longer under natural selection against insects. I show that autumn colours remain only in the varieties that are very susceptible to the effects of a common insect-borne disease, fire blight, and therefore are more in need of avoiding insects. Moreover, varieties with red leaves have smaller fruits, which shows that they have been under less effective artificial selection. This suggests a possible trade off between fruit size, leaf colour and resistance to parasites. These results are consistent with the hypothesis that autumn colours are a warning signal to insects, but not with other hypotheses.