Associated evolution of fruit size,fruit colour and spines in Neotropical palms

Understanding how ecological interactions have shaped the evolutionary dynamics of species traits remains a challenge in evolutionary ecology. Combining trait evolution models and phylogenies, we analysed the evolution of characters associated with seed dispersal (fruit size and colour) and herbivory (spines) in Neotropical palms to infer the role of these opposing animal–plant interactions in driving evolutionary patterns. We found that the evolution of fruit colour and fruit size was associated in Neotropical palms, supporting the adaptive interpretation of seed‐dispersal syndromes and highlighting the role of frugivores in shaping plant evolution. Furthermore, we revealed a positive association between fruit size and the presence of spines on palm leaves, bracteas and stems. We hypothesize that interactions between palms and large‐bodied frugivores/herbivores may explain the evolutionary relationship between fruit size and spines. Large‐bodied frugivores, such as extinct megafauna, besides consuming the fruits and dispersing large seeds, may also have consumed the leaves or damaged the plants, thus simultaneously favouring the evolution of large fruits and defensive structures. Our findings show how current trait patterns can be understood as the result of the interplay between antagonistic and mutualistic interactions that have happened throughout the evolutionary history of a clade.     

开花式样对传粉者行为及花粉散布的影响

理解植物花的特征可以从单花特征和群体特征两个层次入手。开花式样是植物的花在群体上的特征体现, 通过在开花数目、开花类型以及花的排列上的变化, 不同的开花式样对传粉者具有不同的吸引力, 影响昆虫在植株上的活动, 使花粉运动的方向发生相应变化, 从而影响着植物最终的交配结果。此外开花式样随环境改变也会发生一些变化。本文介绍了开花式样研究的进展, 对开花数目、开花类型以及花的排列等3个方面的已有研究进行了分别阐述, 并提出开花式样研究应更多地考虑影响传粉的各种因素。     

Floral colour versus phylogeny in structuring subalpine flowering communities

The relative number of seeds produced by competing species can influence the community structure; yet, traits that influence seed production, such as pollinator attraction and floral colour, have received little attention in community ecology. Here, we analyse floral colour using reflectance spectra that include near-UV and examined the phylogenetic signal of floral colour. We found that coflowering species within communities tended to be more divergent in floral colour than expected by chance. However, coflowering species were not phylogenetically dispersed, in part due to our finding that floral colour is a labile trait with a weak phylogenetic signal. Furthermore, while we found that locally rare and common species exhibited equivalent floral colour distances from their coflowering neighbours, frequent species (those found in more communities) exhibited higher colour distances from their coflowering neighbours. Our findings support recent studies, which have found that (i) plant lineages exhibit frequent floral colour transitions; and (ii) traits that influence local population dynamics contribute to community structure.     

Fruit Bats (Chiroptera: Pteropodidae) as Seed Dispersers and Pollinators in a Lowland Malaysian Rain Forest1

The aims of this study were to (1) characterize the food resources exploited by fruit bats (Pteropodidae) within an old‐growth Malaysian dipterocarp forest, (2) test the viability of the seeds they disperse, and (3) provide an estimate of the proportion of trees that are to some degree dependent upon bats for seed dispersal and/or pollination. Fruit species exploited by bats could be distinguished from those eaten by birds largely on the basis of color (as perceived by human beings). Bat‐dispersed fruits were typically inconspicuous shades of green–yellow or dull red–brown, whereas fruits eaten by birds were generally bright orange to red. Dietary overlap between bats and nonflying mammals was relatively high. In contrast to primates and squirrels, which were major seed predators for several of the plant species under investigation, fruit bats had no negative impact on seed viability. A botanical survey in 1 ha of old‐growth forest revealed that 13.7 percent of trees (?15 cm girth at breast height) were at least partially dependent upon fruit bats for pollination and/or seed dispersal.     

Recruitment trade-offs and the evolution of dispersal mechanisms in plants

In this study we place seed size vs. seed number trade-offs in the context of plant dispersal ability. The objective was to suggest explanations for the evolution of different seed dispersal mechanisms, in particular fleshy fruits, wind dispersal and the maintenance of unassisted dispersal. We suggest that selection for improved dispersal may act either by increasing the intercept of a dispersal curve (log seed number vs. distance) or by flattening the slope of the curve. 'Improved dispersal' is defined as a marginal increase in the number of recruits sited at some (arbitrary) distance away from the parent plant. Increasing the intercept of the dispersal curve, i.e. producing more seeds, is associated with a reduction in seed size, which in turn affects the recruitment ability, provided that this ability is related to seed size. If recruitment is related to seed size there will be a recruitment cost of evolving increased seed production. On the other hand, a flattening of the slope by evolving dispersal attributes is likely to be associated with a fecundity cost. An exception is wind dispersal where smaller (and hence more numerous) seeds may lead to more efficient dispersal. We derive two main predictions: If recruitment is strongly related to seed size, selection for improved dispersal acts on the slope of the dispersal curve, i.e. by favouring evolution of dispersal attributes on seeds or fruits. If, on the other hand, recruitment is only weakly related to seed size (or not related, or negatively related), selection for improved dispersal favours increased seed production. Despite its simplicity, the model suggests explanations for (i) why so many plant species lack special seed dispersal attributes, (ii) differences in dispersal spectra among plant communities, and (iii) adaptive radiation in seed size and dispersal attributes during angiosperm evolution. This revised version was published online in July 2006 with corrections to the Cover Date.     

Fossil floral and fruit evidence for the evolution of unusual developmental characters in Fagales

Flowers of many living Fagales exhibit unusual developmental characteristics. At anthesis, ovulate flowers have carpels bearing immature orthotropous ovules. After pollination, the ovules increase in size and become anatropous and the ovary enlarges. Simultaneously, the pollen tubes extend from the stigma to the ovules with several phases of growth and quiescence. Finally, after the first fertilization, the remaining ovules abort, resulting in a single‐seeded fruit. Three‐dimensionally preserved potentially fagaceous mesofossil flowers from the Campanian of Massachusetts, USA, provide evidence on the evolution of these characters. The fossils share putative synapomorphies with the Fagales (six tepals, mostly inferior, three‐carpellate ovary with each locule initially containing two pendant ovules, punctate‐rugulate, tricolporate pollen and fruit with a single seed). However, the fossil is bisexual and has nectaries, characters shared with the sister order Cucurbitales, and both lack the fagalean immature orthotropous developmental stage. The fossil shares synapomorphies of an inferior ovary and a single‐seeded indehiscent fruit with both living orders and appears to be transitional. Comparison of ontogenetic changes between the fossil and related fagalean taxa suggests independent stepwise changes in development in which some characters of the modern clades were in place at ～ 75 Myr and others evolved more recently. © 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2012, 168 , 353–376.     

Temporal and spatial variation in flower and fruit production in a food-deceptive orchid: a five-year study

Deceptive orchids are generally characterized by low levels of fruit set; however, there may be substantial variations in fruit set between sites and years. Within a single population, individual plants may also differ greatly in their reproductive output as a result of differences in inflorescence size or local density. In this study, we determined flower and fruit production over 5 years in two populations of the food-deceptive orchid, Orchis purpurea . All plants were monitored annually for survival and flowering at each site to determine whether flowering and fruiting induced costs. The number of flowers per inflorescence varied considerably from year to year (min: 36.6, max: 49.5). Average fruit set was low (7%) and varied considerably among years and populations. A considerable proportion of plants also failed to set any fruit. However, the probability of producing at least one fruit was not affected by inflorescence size or local density. The number of fruits was significantly related to inflorescence size, but proportional fruit set was not. Local density also did not affect the number of fruits, nor proportional fruit set. There was also no evidence that plants with large inflorescence size or high fruiting success had a larger probability of remaining vegetative the year after flowering than plants with small inflorescence size or low fruiting success. Our results suggest that pollinator-mediated selective forces on inflorescence size through female reproductive success alone are weak, most likely because of the low overall level of visitation and the resulting uncertainty of pollination at the individual level. Our results further demonstrate that investigation of patterns of fruit set over several years is needed to better understand the variability in female reproductive success that is typical of most plant–pollinator interactions.     

Primate origins and the evolution of angiosperms

Traditionally, the morphological traits of primates were assumed to be adaptations to an arboreal way of life. However, Cartmill [1972] pointed out that a number of morphological traits characteristic of primates are not found in many other arboreal mammals. He contends that orbital convergence and grasping extremities indicate that the initial divergence of primates involved visual predation on insects in the lower canopy and undergrowth of the tropical forest. However, recent research on nocturnal primates does not support the visually-oriented predation theory. Although insects were most likely important components of the diets of the earliest euprimates, it is argued here that visual predation was not the major impetus for the evolution of the adaptive traits of primates. Recent paleobotanical research has yielded evidence that a major evolutionary event occurred during the Eocene, involving the angiosperms and their dispersal agents. As a result of long-term diffuse coevolutionary interactions with flowering plants, modern primates, bats, and plant-feeding birds all first arose around the Paleocene-Eocene boundary and became the major seed dispersers of modern tropical flora during the Eocene. Thus, it is suggested here that the multitude of resources available on the terminal branches of the newly evolved angiosperm, rain forest trees led to the morphological adaptations of primates of modern aspect.     

The role of chromatic and achromatic signals for fruit detection by birds

Fruit color changes during ripening are typically viewed asan adaptation to increase signal efficacy to seed dispersers.Plants can increase signal efficacy by enhancing chromatic (wavelengthrelated) and/or achromatic (intensity related) contrasts betweenfruit and background. To assess how these contrasts determinethe detectability of fruit signals, we conducted 2 experimentswith free-flying crows (Corvus ossifragus) under seminaturalconditions in a 2025 m² aviary. Crows searched first for artificialred and black fruits and detected red fruits from a larger distance.Because artificial red fruits had higher chromatic and lowerachromatic contrasts against foliage than artificial black fruits,crows apparently prioritized chromatic contrasts. Thus, thecommon change in fruit color from red to black during ripeningdoes not increase signal efficacy to crows. In a second trial,crows searched for UV-reflecting and black blueberries (Vaccinummyrtillus) against backgrounds of foliage and sand. Againstfoliage, UV-reflecting berries had higher chromatic and achromaticcontrasts than black berries, and crows detected them from alarger distance. Against sand, UV-reflecting berries had lowachromatic contrasts and black berries low chromatic contrasts.Crows detected both fruit types equally, suggesting that theyused chromatic contrasts to detect UV-reflecting berries andachromatic contrasts to detect black berries. Birds prioritizedchromatic contrasts when searching for artificial red fruitsin foliage but not when searching for blueberries on sand. Wesuggest that the relative importance of chromatic and achromaticcontrasts is contingent on the chromatic and achromatic varianceof the background. Models of signal perception can be improvedby incorporating background-specific effects.     

The evolution of staminodes in angiosperms: patterns of stamen reduction, loss, and functional re-invention

Stamens that have lost their primary function of pollen production, or staminodes, occur uncommonly within angiosperms, but frequently fulfill important secondary floral functions. The phylogenetic distribution of staminodes suggests that they typically arise during evolutionary reduction of the androecium. Differences in the genetic control and patterns of stamen loss between actinomorphic and zygomorphic flowers shape staminode development. In clades with actinomorphic flowers, staminodes generally replace an entire stamen whorl and staminode loss seems irreversible. In contrast, in clades with zygomorphic flowers staminodes evolve from a subset of the stamens in a whorl and staminodes can reappear in a lineage after being lost (e.g., Cheloneae, Scrophulariaceae). If staminodes do not adopt new functions during androecium reduction they are lost quickly, so that nonfunctional staminodes appear only in recently derived taxa. Alternatively, when staminodes assume new floral roles, either directly or indirectly after a nonfunctional period, they can become integral floral components which perpetuate within clades (e.g., Orchidaceae). Indirect evolution of staminode function allows greater flexibility of function by allowing staminodes to take over roles not performed by stamens, such as involvement in mechanisms to prevent self-pollination and mechanisms of explosive pollination. Multifunctional staminodes characterize lineages with universal or widespread staminodes.     

Constraints on plant signals and rewards to multiple mutualists?

Many plants invest substantial resources in signaling to and rewarding two kinds of ‘interguild’ mutualists, pollinators and seed dispersers. The signals and rewards are expressed via traits of flowers and fruits. Pollinators and seed dispersers could act in synergistic or antagonistic ways to influence selection on these traits. Here, we address the issue of whether plant species might be constrained in signaling to and rewarding multiple mutualists that provide different types of benefits to plants. Specifically, does investment in one type of mutualist limit investment in another? We examined the correlation between flower size and fruit size for 472 plant species spanning three regional floras. Our analyses made the assumption that structure size is related to plant investment in signals and/or rewards. We expect that a constraint due to interguild mutualisms would be evidenced by a negative correlation between flower and fruit size. Instead, we found significantly positive relationships between flower size and fruit size in all three regional floras. These relationships remained robust after correcting for plant evolutionary history using phylogenetically independent contrasts. These patterns may reflect synergies in selection by pollinators and seed dispersers, genetically-based or resource-based constraints on investment in reproductive tissues, and/or an underlying trade-off in structure size versus number.     

Cryptic clades, fruit wall morphology and biology of Andira (Leguminosae: Papilionoideae)

Andira comprises 29 species distributed throughout tropical America, with two subspecies in Africa. Its fruits are unusual for a papilionoid legume because they are drupes. The majority of species have fruits dispersed by bats, but eight species have larger fruits dispersed by-rodents. Some fruits of both dispersal types are secondarily dispersed by water. Cladistic analysis of chloroplast DNA (cpDNA) restriction site characters discovered four well-supported clades of Andira species. None of these 'cryptic' clades had been recognized by previous workers, because they are not apparently marked by any known morphological innovations. This prompted a search for new characters that might support these groupings. An anatomical study of fruit walls of 25 Andira species revealed the presence of three principal endocarp types, dominated by (1) parenchyma, (2) fibres, or (3) stone cells. These features arc best coded as a single unordered multistate character. When incorporated into a simultaneous cladistic analysis of previously gathered molecular and morphological data, states of this endocarp character are shown to be apomorphies for two of the well-supported clades evident in the cpDNA restriction site data. The most likely plesiomorphic state for the endocarp is parenchyma-dominated. Thicker, stronger endocarps of fibres and stone cells may have evolved in response to the need to protect the seed from predators.     

Quantifying hummingbird preference for floral trait combinations: The role of selection on trait interactions in the evolution of pollination syndromes

Darwin recognized the flower's importance for the study of adaptation and emphasized that the flower's functionality reflects the coordinated action of multiple traits. Here we use a multitrait manipulative approach to quantify the potential role of selection acting on floral trait combinations underlying the divergence and maintenance of three related North American species of Silene (Caryophyllaceae). We artificially generated 48 plant phenotypes corresponding to all combinations of key attractive traits differing among the three Silene species (color, height, inflorescence architecture, flower orientation, and corolla‐tube width). We quantified main and interaction effects of trait manipulation on hummingbird visitation preference using experimental arrays. The main effects of floral display height and floral orientation strongly influenced hummingbird visitation, with hummingbirds preferring flowers held high above the ground and vertically to the sky. Hummingbirds also prefer traits in a nonadditive manner as multiple two‐way and higher order interaction effects were important predictors of hummingbird visitation. Contemporary trait combinations found in hummingbird pollinated S. virginica are mostly preferred. Our study demonstrates the likelihood of pollination syndromes evolving due to selection on trait combinations and highlights the importance of trait interactions in understanding the evolution of complex adaptations.     

Character displacement among bat-pollinated flowers of the genus Burmeistera: analysis of mechanism, process and pattern

Coexisting plants that share pollinators can compete through interspecific pollen transfer. A long-standing idea holds that divergence in floral morphology may reduce this competition by placing pollen on different regions of the pollinator's bodies. However, surprisingly little empirical support for this idea exists. Burmeistera is a diverse neotropical genus that exhibits wide interspecific variation in the degree to which the reproductive parts are exserted outside the corolla. Coexisting Burmeistera share bats as their primary pollinators, and the degree of exsertion determines the site of pollen deposition on the bats' heads. Here we study the mechanism, process and pattern of floral character displacement for assemblages of coexisting Burmeistera. Flight cage experiments with bats and pairs of Burmeistera species demonstrate that the greater the divergence in exsertion length, the less pollen transferred interspecifically. Null model analyses of exsertion lengths for 19 species of Burmeistera across 18 sites (each containing two to four species) demonstrate that observed assemblage structure is significantly overdispersed relative to what would be expected by chance. Local evolution, rather than ecological sorting, appears to be the primary process driving this pattern of overdispersion because local adaptation of the nine widespread species accounts for a large portion of the observed pattern. Taken together, results of this study provide strong support for the idea that competition through interspecific pollen transfer can drive character displacement in plants.     

Coloured nectar: distribution, ecology, and evolution of an enigmatic floral trait

While coloured nectar has been known to science at least since 1785, it has only recently received focused scientific attention. However, information about this rare floral trait is scattered and hard to find. Here, we document coloured nectar in 67 taxa worldwide, with a wide taxonomical and geographical distribution. We summarise what is currently known about coloured nectar in each of the lineages where it occurs. The most common nectar colours are in the spectrum from yellow to red, but also brown, black, green, and blue colours are found. Colour intensity of the nectar varies, sometimes even within one taxa, as does the level of contrast between flower petals and nectar. Coloured nectar has evolved independently throughout the angiosperms at least 15 times at the level of family, and is in many cases correlated with one or more of three parameters: (1) vertebrate pollination, known or hypothesised, (2) insularity -- many species are from islands or insular mainland habitats, and (3) altitude -- many species are found at relatively high altitudes. We discuss the evolution and speculate on possible ecological functions of coloured nectar. Apart from being a non-functional, perhaps pleiotropic, trait, we present several hypotheses on possible ecological functions of coloured nectar. Firstly, for some plant species it can be interpreted as an honest signal, leading to high pollination efficiency. Secondly, it can function as a deterrent against nectar-thieves or inefficient pollinators, thus acting as a floral filter. Thirdly, nectar colour-pigments can have anti-microbial qualities that may protect the nectar in long-lived flowers. Neither of these possibilities are mutually exclusive. Recent studies have provided experimental evidence for the first two hypotheses, and we suggest promising avenues for future research into this little-known floral trait.     

The evolution of key functional floral traits in the early divergent angiosperm family Annonaceae

Potential key functional floral traits are assessed in the species‐rich early divergent angiosperm family Annonaceae. Pollinators (generally beetles) are attracted by various cues (particularly visual, olfactory, and thermogenic), with pollinators rewarded by nectar (generally as stigmatic exudate), heat, and protection within the partially enclosed floral chamber. Petals sometimes function as pollinator brood sites, although this could be deceptive. Annonaceae species are self‐compatible, with outcrossing promoted by a combination of protogyny, herkogamy, floral synchrony, and dicliny. Pollination efficiency is enhanced by pollen aggregation, changes in anthesis duration, and pollinator trapping involving a close alignment between petal movements and the circadian rhythms of pollinators. Most Annonaceae flowers are apocarpous, with syncarpy restricted to very few lineages; fertilization is therefore optimized by intercarpellary growth of pollen tubes, either by stigmatic exudate (suprastylar extragynoecial compitum) or possibly the floral receptacle (infrastylar extragynoecial compitum). Although Annonaceae lack a distinct style, the stigmas in several lineages are elongated to form “pseudostyles” that are hypothesized to function as sites for pollen competition. Flowers can be regarded as immature fruits in which the ovules are yet to be fertilized, with floral traits that may have little selective advantage during anthesis theoretically promoting fruit and seed dispersal. The plesiomorphic apocarpous trait may have been perpetuated in Annonaceae flowers as it promotes the independent dispersal of fruit monocarps (derived from separate carpels), thereby maximizing the spatial/temporal distance between seedlings. This might compensate for the lack of genetic diversity among seeds within fruits arising from the limited diversity of pollen donors.     

Reproductive ecology of Ocotea catharinensis,an endangered tree species

• Ocotea catharinensis (Lauraceae) is an endangered tree species from the Brazilian Atlantic Rainforest. Currently, little is known about the reproductive ecology of this species. Aiming to propose conservation measures, we described aspects related to phenology, floral biology, pollination, seed dispersal and mating system of O. catharinensis.
• We conducted phenological observations in 62 individuals for 2 years. In one reproductive event, we evaluated nectar production, stigmatic receptivity and pollen viability. Floral visitors were observed, identified and classified on a scale of pollination effectiveness. Seed dispersers were observed and identified using camera traps. Finally, the mating system was evaluated through pollen/ovule ratios, experimental pollination treatments and genetic analysis with molecular markers.
• Ocotea catharinensis presented a supra‐annual fruiting pattern with a substantial reduction of reproducing individuals from bud phase to ripe fruit phase. Several mechanisms prompting cross‐fertilisation were identified, such as attractive, herkogamic and protogynic flowers. The main floral visitors and pollinators were from the Diptera order, and all seed dispersers were birds. The species presented a predominantly outcrossed mixed mating system with significant selfing rate (17.3%).
• Although based on restricted evidence, we hypothesised that selfing is an escape mechanism for situations unfavourable to cross‐fertilisation. Specifically, for the studied population selfing is a response to reduced population size, which is caused by the non‐reproduction of all potentially reproductive individuals and by past exploitation events. Therefore, conservation efforts should be able to enhance population sizes, as well as prevent overexploitation.

     

Digestion time and intactness of seeds ingested by Sturnira lilium (E. Geoffroy, 1810) (Mammalia,Chiroptera)

Bats are responsible for many ecological services, such as seed dispersal of several plant species, contributing to the processes of succession and forest regeneration. A factor that can interfere with this process is the animal digestion, which can affect germination, altering the patterns of seedling distribution. The effects of seed passage through bats’ guts varies with the species, leading to some discrepancies in the literature. In this study, we tested the digestion time of one Phyllostomidae bat species, Sturnira lilium, in two Neotropical plants: Solanum paniculatum and Ficus organensis, and the effects on seed germination. The experiment was conducted in captivity and the germination tests were made in laboratory conditions. The results suggested that most seeds ingested by S. lilium are dispersed within 40 min for both species and the digestion seems not to significantly affect the germination of F. organensis, despite the slight acceleration of germination. In S. paniculatum, germination occurred only in the control (39%), whereas in the treatments, all the seeds remained dormant during the 25 experimental days. In this case, the digestion of S. lilium possibly contributes to the formation of seed banks, randomizing the temporal distribution of seedlings.