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Fruit color and contrast in seasonal habitats – a case study from a cerrado savanna

Maria Gabriela G. Camargo, Eliana Cazetta, H. Martin Schaefer and L. Patrícia C. Morellato

M. G. G. Camargo (gabicamargo@yahoo.com) and L. P. C. Morellato, Depto de Botânica, Laboratório de Fenologia, Grupo de Fenologia e Dispersão de Sementes, Inst. de Biociências, Univ. Estadual Paulista (UNESP), Avenida 24A 1515, CEP 13506-900, Rio Claro, SP, Brazil. – E. Cazetta, Depto de Ciências Biológicas, Universidade Estadual de Santa Cruz, Rodovia Ilhéus-Itabuna km 16, CEP 45662-900, Ilhéus, BA, Brazil. – H. M. Schaefer, Dept of Evolutionary Biology and Animal Ecology, Faculty of Biology, Univ. of Freiburg, Hauptstr. 1, DE-79104 Freiburg, Germany.

Communication contributes to mediate the interactions between plants and the animals that disperse their genes. As yet, seasonal patterns in plant–animal communication are unknown, even though many habitats display pronounced seasonal-ity e.g. when leaves senescence. We thus hypothesized that the contrast between fruit displays and their background vary throughout the year in a seasonal habitat. If this variation is adaptive, we predicted higher contrasts between fruits and foliage during the fruiting season in a cerrado–savanna vegetation, southeastern Brazil. Based on a six-year data base of fruit ripening and a one-year data set of fruit biomass, we used reflectance measurements and contrast analysis to show that fruits with distinct colors differed in the beginning of ripening and the peak of fruit biomass. Black, and particularly red fruits, that have a high contrast against the leaf background, were highly seasonal, peaking in the wet season. Multicolored and yellow fruits were less seasonal, not limited to one season, with a bimodal pattern for yellow ones, represented by two peaks, one in each season. We further supported the hypothesis that seasonal changes in fruit contrasts can be adaptive because fruits contrasted more strongly against their own foliage in the wet season, when most fruits are ripe. Hence, the seasonal variation in fruit colors observed in the cerrado–savanna may be, at least partly, explicable as an adaptation to ensure high conspicuousness to seed dispersers.

Traditionally, fruit colors are thought to represent adap-tations to seed dispersers, which are regarded as the main selective pressure on fruit color evolution (Darwin 1862, Kerner 1895, Willson and Whelan 1990). During the 1980s and early 1990s, the influential ‘syndrome hypothesis’ assumed that seed dispersers have strong preferences for certain colors and that these preferences influence the evolution of fruit coloration (Janson 1983, Gautier-Hion et al. 1985). Although some studies reported color prefer-ences of fruit consumers (Puckey et al. 1996, Siitari et al. 1999, Whitney 2005), these preferences were often transient (Schmidt and Schaefer 2004), and most studies did not support the syndrome hypothesis owing to inconsistent color choices (Willson et al. 1990, Willson and Comet 1993, Traveset and Willson 1998, Schmidt et al. 2004).

Alternatively to color preferences, diurnal seed dispersers might select fruit colors by consistently detecting a color more easily (Kerner 1895). This hypothesis, termed later ‘contrast hypothesis’ (Schmidt et al. 2004) is consistent with the main tenet of signal theory: that detectability is one of the main factors driving the evolution of signals (Schluter and Price 1993). Supporting the contrast hypo-thesis, studies have documented that red and black, the most common colors of bird-dispersed fruits, contrast

more strongly against the background than other fruit colors (Lee et al. 1994, Schmidt et al. 2004). Furthermore, the rate at which birds pecked artificial fruits was a function of the conspicuousness of these fruits in southeastern Brazil (Cazetta et al. 2009). Thus, if seed dispersers select fruits mainly on the basis of their detectability, the contrasts between fruit and background (leaves, bark and structures associated with the fruit display) as they are perceived by animals are more important, from an evolutionary perspec-tive, than the color of a fruit per se (Schmidt et al. 2004, Melo et al. 2011). There is also evidence that secondary structures (non-green pedicels, capsules or unripe fruits associated with the ripe fruits, according to Schaefer and Schaefer 2007) increase the contrasts of fruit displays and influence fruit detection (Willson and Melampy 1983, Burns and Dalen 2002, Schaefer et al. 2007).

The contrast between fruit displays and their background are not necessarily constant. In seasonal habitats contrast can change during the year, e.g. when leaves senesce and are shed during the dry season. Burns and Dalen (2002) suggest that temporal changes in the availability of fruits with different colors are explicable by changes in fruit conspicuousness against seasonal changes in foliage color-ation. However, Burns and Dalen (2002) characterized fruit

Oikos 122: 1335–1342, 2013 doi: 10.1111/j.1600-0706.2013.00328.x

© 2013 The Authors. Oikos © 2013 Nordic Society Oikos Subject Editor: Paulo Guimarães Jr. Accepted 21 January 2013

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conspicuousness according to human perception, not accounting for the visual perception of seed dispersers.

In a Brazilian cerrado vegetation, where marked changes in leaf color are observed between dry and wet seasons and most fruit species are dispersed by birds (Gottsberger and Silberbauer-Gottsberger 2006), we tested: 1) if there is a seasonal pattern of fruit color and 2) if the contrast between fruit and foliage is higher, and hence fruits are more detectable in the fruiting season compared to the non-fruiting season.

We first evaluated fruit phenology to describe the overall pattern of fruit color timing, diversity and biomass. If there are seasonal changes in the background and if the contrast hypothesis applies generally to fruit coloration in the cerrado–savanna, we predicted that the proportion of more contrasting fruits against the leaf background, like black and red ones, changes over the seasons, whereas such changes are less pronounced in less contrasting fruits. Specifically, red and black fruits should be more common during the wet season than during the dry season because they are particularly conspicuous against green back-grounds predominating in the wet season (Lee et al. 1994, Schmidt et al. 2004). Conversely, we expect the fruiting time of less conspicuous fruits e.g. yellow, white and orange to be less seasonal. We also expect that multicolored fruits are present in both seasons, since the presence of secondary structures can increase fruit contrasts as they are perceived by birds (Schaefer et al. 2007). Finally, we predicted stronger fruit color contrast (as seen by birds) against their own leaves at the time when fruits are ripe (mostly the wet season) compared to the leaves in the other season.

Material and methods

Study site

The study was conducted in a cerrado savanna area of about 260 ha located at Itirapina, São Paulo State, southeastern Brazil (22°10′31.41″S, 47°52′26.13″W). The regional cli-mate is Cwa type according to the Köeppen system (1948), with a dry winter and a wet summer. The mean climate (1972 to 2002) shows a mean total annual rainfall of 1524 mm and a mean annual temperature of 20.7°C, a wet season from October to March, a dry season from April to

September, and a water deficit from June to August (Camargo et al. 2011).

During the dry season there are marked changes in leaf coloration with many leaves turning yellowish mainly in July, in the peak of leaf fall (Fig. 1). At the end of the dry season in August, the new leaves start to flush, peaking in September. From October onwards most individuals present mature, dark green leaves in wet season (Fig. 1).

The vegetation is classified as cerrado sensu stricto (Coutinho 1978), a savanna-like vegetation with a discon-tinuous woody canopy reaching six to seven meters high, or up to 12 m high in denser patches, and a continuous herbaceous layer. The most important tree species are Anadenanthera falcata, Bauhinia rufa (Fabaceae), Myrcia guianensis (Myrtaceae), Xylopia aromatica (Annonaceae), Virola sebifera (Myristicaceae) and Miconia albicans (Melastomataceae). From 190 species surveyed in the study site flora, 107 are dispersed by animals, and of this, 101 are potential dispersed by birds or by birds associated with other animals, like lizards or mammals.

Phenological data

We established 36 transects of 25 2 m (total sam-pling 0.18 ha) and sampled all individuals 3 cm of circumference at ground level. The transects were set up 50 m apart from each other and disposed along the natural environmental and structural gradient of the study site (Camargo et al. 2011). We registered monthly, from January 2005 to December 2010, the presence or absence of ripe fruits (according to Morellato et al. 1989) in a total of 1414 individuals sampled, belonging to 50 fleshy-fruiting species and 26 families (Supplementary material Appendix 1 Table A1). We also counted, from January to December 2006, the number of ripe fruits produced by those individuals. A further 14 species were present at our transects but did not fruit during the five years of phenological observation and were excluded from all ana-lyses except for the calculation of the proportion of species fruiting at a given time in our community. In addition to the 50 species sampled, we also determined the fruiting period of 12 species that fruited outside our phenological transects, the fruiting pattern of these 12 species were not included in the statistical analyses but are presented in the Supplementary material Appendix 2 Fig. A2. We collected

Figure 1. Average monthly percentage of individuals in leaf fall and leaf flush and the mean total rainfall (2005 to 2010) at Itirapina, in a woody cerrado savanna community, southeastern Brazil.

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30 ripe fruits of five individuals randomly selected outside the transects to obtain the average weight of fresh fruits per species and to estimate the biomass of fruits produced per individual and species. We estimated fruit biomass for 550 individuals belonging to 27 species and 15 families (Supplementary material Appendix 1 Table A1).

Fruit color and contrasts

We measured the reflectance spectra of fruits, leaves and secondary structures (non-green pedicels, capsules) with a spectrometer between 300–850 nm. We thus included the visual range of all frugivorous animals, including that of birds which are sensitive to 300–700 nm. Reflectance was measured as a proportion of a standard white surface. For color measurements we used an optical sensor inside a black box to avoid the influence of the ambient light. The reflectance spectra were processed with Spectra Suite soft-ware and binned into 5 nm intervals. We measured the reflectance of 20 fruits and 20 leaves or accessory structures of 41 species (Supplementary material Appendix 1 Table A1), and used the means of these measurements for all analyses. We also measured leaf reflectance of 15 leaves from 60 species in the dry and wet seasons, independent of fruit presence, to evaluate seasonal changes in leaf coloration. We measured leaf reflectance in November, when most of the species have mature and green leaves and again in July, during the peak of leaf fall. For leaf measurements we calculated three variables that characterize reflectance spectra: total bright-ness, chroma and hue (Endler 1990, Cazetta et al. 2012).

To account for avian vision we additionally calculated chromatic and achromatic contrasts, that is related only to variations in reflected light (Osorio et al. 1999, Cazetta et al. 2009) between the mean reflectance of fruits and leaves or secondary structures and leaves according to an eye model of avian vision (Vorobyev and Osorio 1998). We used an eye model based on the spectral sensitivities of the blue tit Cyanistes caeruleus with a UVS cone (Hart et al. 2000). The model first calculated the quantum catch of each class of single cones present in a tetrachromatic visual system (LWS, MWS, SWS, UVS), based on the analytical approximation of cone visual pigments and oil droplet spectra (Hart et al. 2000). The quantum catches are used to determine the relative contrasts of fruits against the background. Contrasts were characterized in units of ‘just noticeable differences’ (jnd), following the model of Vorobyev and Osorio (1998). One jnd is the threshold of discrimination; higher values indicate increasing dis-crimination of fruits and the background (leaf or second-ary structure). Experimental data show that this model predicts fruit detection rates well in a Brazilian forest (Cazetta et al. 2009). We used an avian model because most of the species in the study area, and almost all the species included in our contrast analyses are dispersed exclusively by birds (73%) or birds and mammals or reptiles (24%) (Supplementary material Appendix 1 Table A1).

Data analysis

To calculate the monthly fruit biomass we multiplied the average weight of fresh fruits for each species by the number of fruits produced every two weeks per species in the transects

and the total value was divided by the total sampled area (1800 m2).

Phenological patterns were described based on the average number of species and individuals per species with ripe fruits in each month. Additionally we recorded the proportion of individuals within a species that shed or developed leaves. For simplicity, we represented fruiting patterns by grouping the species by fruit color, categorized as seen by humans in: red, black, brown, yellow, green and multicolored. The human categorization was used because we could not collect spectral data for all species that we included in phenological observations. However, to compare fruit conspicuousness among seasons we used an eye model of avian vision. Fruits displays were considered permanently multicolored if they had secondary structures such as non-green bracts or stems or temporally multi-colored if they had non-green unripe fruits associated with the ripe fruits (Schaefer and Schaefer 2007).

For the 12 species collected outside transects but not included in the phenology survey, the fruiting date was indi-cated by the months in which we found fruits in the field.

We applied circular statistics to test whether differently colored fruits differed in the seasonality of the peak of their fruit biomass and in the onset of fruiting as described in Morellato et al. (2000, 2010; for a brief explanation see Supplementary material Appendix 3). We applied the Rayleigh test (Z), to test the significance of the estimated mean angle (mean date, Morellato et al. 2000). If the mean angle was significant, the pattern was considered sea-sonal and the length of the mean vector (r) is considered as the degree of seasonality of peak biomass and the onset of fruiting for each color (see Morellato et al. 2000, 2010 for details and calculations). All circular analyses were performed in Oriana 3.0 (Kovach Computing Services).

Leaf reflectance spectra and their variables: total bright-ness, hue and chroma, were compared intra-specifically between dry and wet seasons with a paired t-test. The color contrast between fruits and secondary structures against their own background was compared with the contrast against the background of the dry season with a paired t-test. We tested whether the variance of contrasts values differed among fruit colors using Levene test (Zar 1999).

Results

Of the 62 species monitored, 36% had multicolored fruit displays, 27% yellow fruits, 14% red fruits, 11% black fruits, 5% green fruits and 6% brown fruits. Of the 27 fruit species included in the biomass estimation, 48% were multicolored, 26% yellow, 19% black, and 7% red.

Categorizing fruits according to diaspore coloration, and hence excluding the ‘multicolored’ category, 27% of fruits included in phenological observations were yellow, 27% were black, 17% red, 6% green, 6% white, 6% brown and 11% presented other fruit colors. Among the black fruits, 55% are associated with red accessory structures.

Patterns of fruit production

Fruits of all colors were observed throughout the year, but were produced mainly during the wet season (Fig. 2A).

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Fruit color seasonality

All fruit colors had seasonal fruiting pattern with the length of the mean vector r ranging from 0.52 to 0.92 (Table 1, Fig. 3, Supplementary material Appendix 4 Fig. A4). Yellow fruiting species were the only exception with a bimodal pattern, presenting two peaks, one in the wet and another one in the dry season (Fig. 3). The peak of black fruit production occurred mainly at the end of the wet season (mean date 12 February, Table 1), while the mean date of fruit onset was 12 December (Fig. 3, Table 1). Red fruits were highly seasonal (r 0.92) and restricted to the wet season. The mean onset and peak production dates of red fruits were at the end of October and November (Fig. 3, Table 1). Multicolored fruits were produced all year long, but mainly in the first part of the wet season, with mean onset and peak dates in November (Fig. 3, Table 1). Yellow fruits presented two peaks of fruit onset and biomass: one in the wet season in November and another in the dry season in May (Fig. 3). The bimodal pattern prevents the application of Rayleigh test to yellow fruits (Morellato et al. 2010).

Leaf color

Leaves changed colors in the dry season, with significant difference in the leaf reflectance spectra between dry and wet seasons (t 210.67; DF 74; p 0.01). Leaves were becoming brighter during the dry season (t 22.59; DF 59; p 0.01) and leaf hue was also slightly higher during the dry season (t 22.32; DF 59; p 0.02) indicating that leaves became more yellowish at that time (mean values of hue in dry season 558 and in wet sea-son 550) (Supplementary material Appendix 5 Fig. 5A). Leaf chroma also differed between seasons, with higher values in the wet season (t 4.85; DF 59; p 0.01).

Fruit contrasts

We found that the chromatic contrast between fruits and their own leaves at the time of fruit maturation (mostly in the wet season) was stronger than the contrast in the season when these fruits were not produced (t 2.11; DF 40; p 0.04; Fig. 4). There was no significant difference for the achromatic contrast (t 0.19; DF 40; p 0.84).

The contrast between multicolored fruits and their correspondent secondary structures was not higher than the contrast between these multicolored fruits and the foli-age at the time of fruit maturation (chromatic contrast t 21.17, DF 17, p 0.26; achromatic contrast t 0.64,

The peak of biomass for black fruits occurred in the second part of the wet season (Fig. 2A), just before the start of the main period of changes in leaf coloration and senes-cence (Fig. 1). Multicolored and red fruits peaked in the first part of the wet season (Fig. 2A), when leaves are already mature and green (Fig. 1). There was a high pro-duction of yellow fruits in both seasons, with the highest biomass production of the woody community (Fig. 2A).

The diversity of fruit colors available throughout the year showed a pattern similar to that observed for biomass production, peaking in the wet season (Fig. 2B). However we observed a high diversity of colors even in the dry season. The multicolored fruit species prevailed most of the time, followed by yellow and black fruits (Fig. 2B). Species with red fruits were restricted to the wet season (Fig. 2B), with the exception of three species which also fruited in the dry season but whose fruiting peaked in the wet season (Supplementary material Appendix 2 Fig. A2). Despite the overall small number of individuals fruiting during the dry season, some multicolored and yellow fruit species peaked in the dry season.

Table 1. Descriptive variables of the circular statistics analysis and results for the Rayleigh-test (Z) applied to the peak date of fruit biomass and fruiting onset date of individuals per fruit color (except for yellow fruits that presented a bimodal pattern).

Plant variable Fruit color n Mean vector (m) Mean date Mean vector (r) Rayleigh-test (Z) Rayleigh-test (p)

biomass peak multicolored 235 329.1° 29 Nov 0.52 63.1 1 10212

black 156 43.3° 12 Feb 0.66 68.0 1 10212

red 56 315.4° 15 Nov 0.92 47.1 1 10212

fruiting onset multicolored 317 310.8° 11 Nov 0.52 84.5 1 10212

black 214 342.4° 13 Dec 0.58 72.9 1 10212

red 72 296.5° 27 Oct 0.83 50.0 1 10212

brown 18 216.0° 7 Aug 0.53 5.1 0.004

0

3

6

9

12

15

18

J F M A M J J A S O N D

g m

–2

Multicoloured Red Black Yellow

0

5

10

15

20

J F M A M J J A S O N D

Mea

n nu

mbe

r of s

peci

es

Black Yellow Dark-red Multicoloured Green Red

(A)

(B)

Figure 2. Fruit biomass during the year 2007 (A) and the mean number of species fruiting by fruit colors between 2005 and 2010 (B) in a woody cerrado savanna community, southeastern Brazil. The light blue area indicates the wet season.

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Figure 3. Circular histograms for the frequency of fruiting onset dates per fruit colors in a woody cerrado savanna community, southeastern Brazil. The vector arrow indicates the mean angle (mean date) and the arrow length corresponds to the mean vector (r) value, except for yellow fruits that showed a bimodal distribution (details in Methods).

DF 17, p 0.53). The contrast also did not change sea-sonally – no significant difference was detected in the contrast between the secondary structures and the foliage at the time of fruit maturation and foliage of the dry season (chromatic contrast t 1.62, DF 17, p 0.12; achro-matic contrast t 0.39, DF 17, p 0.70).

Red fruits presented higher chromatic contrast and a lower achromatic contrast against their own leaves at the time of fruit maturation compared to the leaves from the

dry season. The variance of chromatic contrast was signifi-cant higher for red fruits than for black fruits against leaves of the fruiting season (F 12.2; p 0.001) and from the dry season (F 5.75; p 0.03) and for black fruits than for the yellow fruits against leaves of the fruiting season (F 60.0; p 0.00). For the achromatic contrast only black fruits had a significant higher variance than the red fruits against the leaves from the dry season (F 6.83; p 0.02).

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indicated that the contrasts of black fruits were generally less variable against foliage than those of red fruits during the transition from mature to senescent leaves. While the species we analyzed included the most common fleshy-fruited species, further changes in the overall background occur due to seasonality in leaf flush and senescence of the whole plant community. However, there is no method established to measure the background contrast or any comparison of fruit contrast against leaf and background. Overall, wet season fruit production is consistent with birds selecting for red and black fruits against a green back-ground where they are particularly contrasting (Schmidt et al. 2004, Schaefer and Ruxton 2011). Hence, our data on seasonal fruit contrasts lend support to the hypothesis that fruit-foliage contrasts are an important characteristic of fruit displays.

As expected, the fruiting pattern of multicolored fruits was less seasonal than that of black and red fruits. However, the lower seasonality may not be fully explicable by the internal contrast provided by the multicolored fruit displays, but by a lesser dependence on contrasts to the foliage, because multicolored fruits contrasted as strongly to secondary structures as they did to the leaves. Along these lines, our findings disagree with the study by Schaefer et al. (2007) which showed that fruits had a greater contrast against their secondary structures compared to the contrast between these fruits and their foliage. If secondary structures are not adaptive to enhance fruit detection by birds in cerrado savanna, we suggest that these structures can rather be explained by physiological and morphological constraints. Such constraints can be a long maturation period leading to the simultaneous pre-sentation of pre-ripe non-green fruits and ripe fruits as well as the presence of dry and senescent capsules that expose their seeds and that are colorful owing to the link between senescence and redness in vegetative tissue (Gould 2004).

Discussion

Fruits of distinct colors differed in the onset of ripening and in the peak of biomass in the cerrado savanna. Additionally, black, and particularly, red fruits were highly seasonal, while multicolored and yellow fruits were less restricted to the wet season. We also found that fruits were more contrasting to leaves at the time of fruiting compared to the same leaves in the dry season.

The color range of cerrado–savanna fruits

The cerrado–savanna had many species with multicoloured fruits, but different from other florae with predominantly bird dispersed fruits (Schaefer and Ruxton 2011), yellow fruits were commoner than black, red and white fruits. A higher frequency of yellow and green fruits than red fruits is also reported for a Pantanal cerrado savanna, in central Brazil (Donatti et al. 2007). However, fleshy fruits of the Pantanal are likely dispersed by large mammals i.e. mega-fauna fruits (Donatti et al. 2007). Conversely, at our southeastern Brazil cerrado–savanna site, fruits are smaller and most yellow fruits are small to medium size and present a predominant bird or mixed bird–mammal seed dispersal system (Guaraldo et al. unpubl.).

Seasonal patterns of leaf and fruit colors and their contrast

Confirming our prediction on the seasonality of contrast-ing fruits, black and red fruits were produced mainly in the wet season when leaves are flushing or turning mature. Red fruits were more seasonal than black fruits. Black fruits occurred primarily at the end of the wet season. The distinct seasonality of red and black fruits might be expli-cable because the contrasts of some black fruits actually increased towards the dry season. Also, the Levene test

Figure 4. Seasonal changes in the chromatic contrast of 41 species. To minimise interspecific variance, contrasts are standardized for each species to 100% in the fruiting season and expressed as relative contrasts. Line colors corresponds to diaspore color (only white is ploted in gray), numbers indicate the relative contrasts of fruits outside of the range of the y-axis.

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the field work at the farm. The study was supported by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (07/59779-6) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). MGGC received scholarships from FAPESP and LPCM receives a Research Productivity fellowship and grant from CNPq. This work is a contribution from the Laboratory of Phenology and the Plant Phenology and Seed Dispersal Group. HMS was benefited by a FAPESP grant (10/52113-5) and the Plant Biology Graduation Program at UNESP Rio Claro.

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Consistent with our hypothesis that less contrasting fruits are less seasonal, we found that yellow fruits ripened year-round with a bimodal peak of fruiting. This pattern may be explicable because yellow fruits are dispersed by a mixed assemblage of birds, mammals and reptiles (Gautier-Hion et al. 1985, Lomáscolo and Schaefer 2010). Hence, other sensory modes apart from vision e.g. the texture and odor of fruits can be important for fruit removal by mammals.

Apart from mutualistic seed dispersers, the colors of fruits and flowers can also be influenced by abiotic conditions (Whitney and Lister 2004, Schemske and Bierzychudeck 2007). For example, Whitney and Lister (2004) showed a clinal pattern of fruit color polymor-phism in Acacia ligulata with yellow fruits being more common in arid conditions than red fruits. Therefore, the occurrence of yellow fruits in the dry season could also be explicable by them being well adapted to dry conditions (Whitney and Lister 2004). However, the proximate mechanism for how abiotic factors are related to differential fitness of fruit color morphs is not yet known.

Finally, we demonstrated differences in leaf reflectance pattern between the dry and wet seasons in the cerrado savanna. During the dry season leaves of deciduous or semi-deciduous species lose chlorophyll and carotenoids are thus more visible in the reflectance pattern. The higher reflectance of leaves in the dry season at wavelength above 550 nm, and consequently, their higher brightness, is likely a consequence of chlorophyll degradation (Merzlyak et al. 1999). Merzlyak et al. (1999) proposed that the persistence of carotenoids within the leaves causes reflectance in the range from 440–550 nm to be constant. In contrast, our results showed leaf color vary in this range: dry season leaves had higher hue than wet season leaves.

Seasons, fruit colors and contrast

The seasonal pattern in fruit color in the cerrado savanna likely increases fruit detection by birds, because fruits contrasted more strongly against leaves at the time of fruit ripeness compared to leaves in the dry season. This result adds support to the fruiting strategy proposed by Burns and Dalen (2002), but now tested in different seasonal vegetation and based on a model of avian vision. In addition, we show for the first time that fruits with higher contrast against the leaf background, such as red fruits, had the highest seasonality, while less contrasting colors were less seasonal.

Frugivores are deemed to be important in fruit color evolution, and the convergence in fruit color has been related to the selection pressure exerted by frugivores, independent of plant phylogeny (Valido et al. 2011, Lomáscolo and Schaefer 2010). We contend that the seasonal variation in fruit colors observed in the cerrado savanna is at least partly explicable as an adaptation to ensure high conspicu-ousness to seed dispersers. Linking contrasts to seasonality is a novel approach that – although it cannot provide conclu-sive evidence of selection – nevertheless suggests that color traits are not selectively neutral.

Acknowledgements – We thank the owners of Fazenda São José and IAB – Instituto Arruda Botelho for allowing the conduct of

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Supplementary material (Appendix oik-00328 at www.oikosoffice.lu.se/appendix ). Appendix 1–5.