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

7 pages, 2 figures.-- Supplementary material available: The list of fruit species, their colour as perceived by humans, their provenance and main disperser types. The dispersal category "mixed" refers to species consumed by birds and mammals (XLS, 43 kb).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.H.M.S. was sponsored by a Deutsche Forschungsgemeinschaft (DFG) grant (Scha 1008/4-1). E.C. was sponsored by Fundaçao de Amparo à Pesquisa do Estado de Sao Paulo (Fapesp) and a Deutscher Akademischer Austausch Dienst (DAAD) fellowship. M.G. was sponsored by Fapesp and receives a research fellowship from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), and E.C. a Fapesp fellowship. A.V. was supported by the Marie Curie European programme (grant MERG-CT-2004-510260), I3P [Consejo Superior de Investigaciones Científicas (CSIC)] and Acción Integrada (HA2006-0038; Ministerio de Educación y Ciencia).Peer reviewe

Variação morfológica e química dos frutos na escolha dos animais frugívoros da Mata Atlântica

As características dos frutos como morfologia e química têm sido tradicionalmente explicadas como resultado da seleção dos dispersores de sementes. Mas a importância dos frugívoros em moldar as características dos frutos tem sido recentemente questionada sob diferentes perspectivas. Alguns estudos sugerem que outras interações podem simultaneamente atuar sobre a evolução das características dos frutos. Muitos organismos atuam como predadores de sementes e seus efeitos precisam ser considerados. Desta maneira, as plantas enfrentam um dilema evolutivo entre atração aos legítimos dispersores de sementes e defesa contra predadores e patógenos. Neste estudo, primeiramente nós avaliamos as características dos frutos relacionadas com atração e defesa em uma ampla amostra de frutos da Mata Atlântica, da Ilha do Cardoso, São Paulo, Brasil. Posteriormente, nós testamos como algumas características específicas influenciam o consumo pelas aves frugívoras. Nós observamos que as características morfológicas e químicas dos frutos apresentam sinal filogenético e em geral padrões independentes de co-variação. Ao contrário, as cores e os contrates dos frutos não apresentam sinal filogenético e frutos mais saturados são ricos em lipídeos e energia mas pobres em carboidratos. Portanto, nós sugerimos que o grau de saturação da cor pode indicar a qualidade nutricional dos frutos. As aves detectaram consistentemente frutos com maior contraste cromático do que o contraste acromático. Além disso, as aves frugívoras selecionam frutos ricos em lipídeos e energia e pobres em compostos secundários. Nós concluímos que a preferência das aves por determinadas características dos frutos não afeta necessariamente a evolução das mesmas, uma vez que, para isso ocorrer é necessário que as aves selecionem entre indivíduos...Fruit characteristics such as morphology and chemistry have traditionally been explained as the result of adaptations to their seed dispersers. But the importance of frugivores in shaping fruit traits has now been questioned from a number of perspectives. Some studies suggested that other interactions simultaneously shape the evolution of fruit traits. Many organisms act as seed predators and their effects must be taken into account. Therefore, plants are faced with an evolutionary dilemma between attraction to legitimate seed dispersers and defense against seed predators and pathogens. In this study we focused on fruit traits related to attractiveness and defense. We first evaluated how fruit characteristics interact in a broad sample of Atlantic rainforest species, at Cardoso Island, São Paulo, Brazil, after accounting for phylogeny. We then evaluated specific fruit characteristics to test whether they influence consumption by birds. We found that morphological and nutritional traits showed phylogenetic signal and in general independent patterns of covariation. On the contrary, fruit color and contrast did not present phylogenetic signal and saturated fruits are rich in energy and lipids, and poor in carbohydrates. Thus we suggest that saturated fruits may indicate fruit quality. Birds consistently detected fruits with higher chromatic contrasts rather than achromatic ones. Frugivorous birds also selected lipid and energyrich fruits and fruits low defended by secondary compounds. We conclude that in spite of bird’s preferences these processes do not operate on the evolution of fruit traits, since this requires birds to differentiate between plant individual of the same and not different species. Therefore, in our study we observed that fruit traits are in general weak associate, with the exception of fruit color, that may indicate fruit adaptation to frugivores

The Crab-eating Fox (Cerdocyon thous) as a secondary seed disperser of Eugenia umbelliflora (Myrtaceae) in a Restinga forest of southeastern Brazil

The crab-eating fox (Cerdocyon thous) exhibits a very generalist habit and fruits compose a large proportion of its diet. However, few studies evaluated the importance of this animal as seed disperser. In the Restinga forest, in the Atlantic forest of Brazil, C. thous consumes fruits of Eugenia umbelliflora, a Myrtaceae species, which is dispersed chiefly by birds. This study evaluated the effects of gut transit on seed germination, and size selection of E. umbelliflora fruits by the crab-eating fox. We did not find differences on germination rates between seeds dispersed by foxes and control ones, but seeds dispersed by foxes germinated faster, which may be important for plant recruitment. Seeds consumed by C. thous were smaller than those available on the ground, indicating selection for small fruits. Regardless of the selection of small fruits, C. thous appears to be an important secondary disperser of E. umbelliflora, distributing large quantities of viable seeds of this Myrtaceae in the Restinga forest

Frugivory and host specificity in the mistletoe Phoradendron rubrum (L.) Griseb. (Viscaceae)

Investigou-se o comportamento das aves dispersoras e as características individuais dos hospedeiros que podem afetar a presença e abundância das ervas-de-passarinho (Viscaceae) na Floresta Estadual Edmundo Navarro de Andrade, Rio Claro, São Paulo - Brasil. Durante 90 horas de observações focais foram registradas 280 visitas de aves, sendo Euphonia chlorotica e E. cyanocephala os principais dispersores, responsáveis por 98,21% das visitas. foi observado parasitando apenas duas espécies de árvores: Tabebuia ochracea (Cham.) Standl. (Bignoniaceae) e Melia azedarach L. (Meliaceae). A localização na copa do hospedeiro e o tamanho do galho de inserção afetam a presença de infestações. As ervas-de-passarinho são encontradas principalmente no estrato superior da copa e em classes de diâmetro pequenas (entre 1,1 e 2,0 cm). As características relacionadas ao tamanho do hospedeiro (altura, DAP e diâmetro da copa) também estão relacionadas com o número de infestações. A presença e abundância das ervas-de-passarinho pode ser influenciada pelo comportamento dos dispersores e pelas características dos hospedeiros.We investigated the behavior of avian seed disperser and host characteristics that influence the presence and abundance of the mistletoe Phoradendron rubrum (Viscaceae) on Floresta Estadual Edmundo Navarro de Andrade, Rio Claro, São Paulo - Brazil. During 90 hours of focal observation we recorded 280 bird visits, Euphonia chlorotica and E. cyanocephala were the main seed disperser, responsible for 98,21% of the visits. Phoradendron rubrum parasitized two tree species: Tabebuia ochracea (Cham.) Standl. (Bignoniaceae) and Melia azedarach L. (Meliaceae). The location in the canopy and the size of the branch affected the presence of mistletoes. The frequency of P. rubrum was higher in the upper canopy and in branches between 1.1 and 2.0 cm in diameter. Characteristics related to the host size (height, DBH and canopy diameter) also affect the number of infection. Mistletoe presence and abundance can be influenced by disperser behavior and characteristics of host plants

Why are fruits colorful? The relative importance of achromatic and chromatic contrasts for detection by birds

The colors of fruits and flowers are traditionally viewed as an adaptation to increase the detectability of plant organs to animal vectors. The detectability of visual signals increases with increasing contrasts between target and background. Contrasts consist of a chromatic aspect (color) and an achromatic aspect (light intensity), which are perceived separately by animals. To evaluate the relative importance of fruits' chromatic and achromatic contrasts for the detection by avian fruit consumers we conducted an experiment with artificial fruits of four different colors in a tropical forest. We displayed the fruits against two different backgrounds, an artificial background and a natural one, because they differed in achromatic properties. We found no effect of the type of background on fruit detection rates. Detection rates differed for the four fruit colors. The probability of detection was explained by the chromatic contrast between fruits and their background, not by the achromatic contrasts. We suggest that birds attend primarily to chromatic contrast probably because these are more reliably detected under variable light conditions. Consistent with this hypothesis, we found habitat-specific differences in the conspicuousness of natural fruit colors in the study area. Fruits of understory species that are subjected to the variable light conditions within a forest displayed higher chromatic contrasts than species growing in the open restinga forest with constant bright illumination. There was no such difference for achromatic contrasts. In sum, we suggest that fruit colors differ between habitats because fruit colors that have strong chromatic contrasts against background can increase plants' reproductive success, particularly under variable light conditions.Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq

Does attraction to frugivores or defense against pathogens shape fruit pulp composition?

Fruit traits evolve in response to an evolutionary triad between plants, seed dispersers, and antagonists that consume fruits but do not disperse seeds. The defense trade-off hypothesis predicts that the composition of nutrients and of secondary compounds in fruit pulp is shaped by a trade-off between defense against antagonists and attraction to seed dispersers. The removal rate model of this hypothesis predicts a negative relationship between nutrients and secondary compounds, whereas the toxin-titration model predicts a positive relationship. To test these alternative models, we evaluated whether the contents of nutrients and secondary compounds can be used to predict fruit removal by mutualists and pathogens in 14 bird-dispersed plants on a subtropical island in Sao Paulo state, southeastern Brazil. We selected eight to ten individuals of each species and prevented fruit removal by covering four branches with a net and left fruits on four other branches available to both, vertebrate fruit consumers and pathogens. The persistence of ripe fruits was drastically different among species for bagged and open fruits, and all fruit species persisted longer when protected against seed dispersers. We found that those fruits that are quickly removed by vertebrates are nutrient-rich, but although the attack rate of pathogens is also high, these fruits have low contents of quantitative defenses such as tannins and phenols. Thus, we suggest that the fruit removal rate by seed dispersers is the primary factor selecting the levels of fruit defense. Likewise, nutrient-poor fruits have low removal of seed dispersers and low probability of attack by pathogens. These species retain ripe fruits in an intact condition for a prolonged period because they are highly defended by secondary compounds, which reduce overall attractiveness. However, this strategy might be advantageous for plants that depend on rare or unreliable dispersers