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.     

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.     

云南拉沙山黑白仰鼻猴对种子传播潜力的评估

灵长类是森林生态系统中植物种子的主要传播者,有助于森林植被的更新,然而受研究方法的限制,灵长类种子传播潜力常被低估。为全面评估温带灵长类动物的种子传播潜力,采用直接观察法和粪便分析法评估珍稀濒危灵长类动物黑白仰鼻猴的种子传播潜力。于2018年11月—2019年10月采用直接观察法(瞬时扫描取样法)收集云岭省级自然保护区拉沙山黑白仰鼻猴的活动时间分配数据,获取每月取食果实的比例;同时每月收集黑白仰鼻猴的粪便,采用粪便分析法分拣猴粪中残留的植物种子,统计有完整种子残留的月份和粪便比例,应用这两种方法评估黑白仰鼻猴种子传播潜力及其差异。结果表明：直接观察法收集到黑白仰鼻猴取食果实的月份数为6个月(7—12月),月均取食果实的比例为(15.31±20.15)%,共取食13种果实;而粪便分析法发现黑白仰鼻猴粪粒内全年都有完整种子残留,粪便中月均完整种子残留比例(35.19±35.43)%,其中9月至第二年1月粪便中种子残留比例都大于50%,共取食18种果实;综合两种方法发现云南拉沙山黑白仰鼻猴共取食20种植物果实,具有较高的种子传播潜力。直接观察法可确定黑白仰鼻猴取食果实的物种数,而粪便分析法能...     

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.     

A field observation on color selection by New World sympatric primates,Pithecia pithecia and Alouatta seniculus

This work characterizes differences in selection ofTalisia retusa fruits by two sympatric Neotropical primates,Pithecia pithecia (white-faced sakis) andAlouatta seniculus (red howlers). Color appears to be the criterion by which fruits were selected. Greenish fruits were mainly eaten byPithecia, while yellowish fruits byAlouatta. The characteristics of these primates in relation to seed predation and seed dispersal are discussed in the context of theTalisia retusa fruit color spectrum. Furthermore, a possible differential acquisition of chemical components, like tannins, is hypothetically treated considering the variation in fruit color.     

Diets of fruit-eating birds: what are the causes of interspecific differences?

Differences in fruit choice among the bird species of a Spanish shrubland were related to the size of fruits and to the lipid content of pulp. Lipid-rich fruits were selected by the bird species with slower food passage rates through the digestive tract. These bird species also fed frequently on insects and seeds. Bird species with faster food passage rates fed less on insects and seeds, and ate mainly fruits with pulp poor in lipids (rich in sugars and water). Studies of digestion in birds indicate that lipids require slower food passage rates for efficient digestion and intestinal transport than simple sugars. The available evidence indicates that the European bird species that show stronger preferences for lipid-rich fruits are no better as seed dispersers, from the point of view of the plants, than species choosing lipidpoor fruits. Thus, the degree of frugivory of birds, their fruit choice patterns and their effects on seed dispersal do not seem to be related to each other in the ways expected by the early models of the evolution of fleshy fruits.     

Interactions between birds and fruit in a temperate woodland

Summary The phenology of fruit trees and avian consumption of fruit were examined in Wytham wood, Oxford in 1979–1980. Ripe fruit was available to and fed upon by birds from late August until early May. Observations made on a daily transect indicated that most of the fruit was eaten by tits and thrushes, but the two families differed in the seasonal consumption and species of fruit taken. Tits took fruits of Elder, Bramble, White Bryony, Honeysuckle, Black Bryony, and Woody Nightshade at the beginning of the season only, while thrushes consumed fruits of Elder, Bramble, Hawthorn, Sloe, Rose, and Ivy mainly in the middle and end of the season. Members of these two families also visited different habitat types following the consumption of fruit, probably effecting different patterns of dispersal. There was no correlation between feeding preferences and the abundance or profitabilities (as defined by Pyke et al. 1977) of fruits with respect to total nitrogen, total proteins, total carbohydrates, total fats, or kilocalories. It is concluded that other factors such as palatability or content of other nutrients may be important in determining the feeding preferences of different species of frugivorous birds.     

Can Functional Traits Predict Ecological Interactions? A Case Study Using Rain forest Frugivores and Plants in Australia

In rain forest, the large numbers of species of fleshy-fruited plants and frugivorous animals result in a large number of potential fruit–frugivore interactions, which are challenging to survey in the field. Yet, knowledge of these relationships is needed to predict consequences of changes in the frugivore assemblage for seed dispersal. In the absence of comprehensive dietary information, it may be possible to delineate between frugivores that disperse different plants using ‘functional traits,’ or morphological and behavioral attributes of frugivores that interact with differences in salient characteristics of plant species. Here we use data on the consumption of 244 Australian rain forest plant species by 38 bird species to test for associations between patterns of frugivory and birds': (1) degree of frugivory, (2) gape width, and (3) seed treatment (seed crushing or seed dispersing). Degree of frugivory and gape width explain 74 percent of the variation in the sizes of fruits consumed by frugivorous birds. Among birds that consume a substantial dietary proportion of fruit, birds with wider gapes consume larger fruits. In contrast, this relationship was not shown by birds for which fruit is only a minor dietary component. Degree of frugivory and gape width, together with seed treatment, also strongly predict the overall taxonomic composition and diversity of plants consumed by bird species. Functional classifications of frugivore species may prove useful in developing a predictive understanding of fruit–frugivore interactions in other rain forest regions where detailed dietary information is not available for most frugivores.     

The fruits of selectivity: how birds forage on Goupia glabra fruits of different ripeness

Although many studies have been published on avian fruit selection, few have addressed the effects of fruit scarcity on the patterns of fruit choice. Here, we compared the consumption of seven bird species for six simultaneously present maturation stages of Goupia glabra fruits. Ripe G. glabra fruits contain more lipids, carbohydrates and energy, and fewer phenols, than unripe fruits. All bird species selected from among ripening stages and removed a higher proportion of ripe fruits than of intermediate or unripe fruits. Importantly, however, fruit choice was flexible in all species. Whether birds preferred or avoided fruits of intermediate ripeness depended on the overall fruit supply. When ripe fruits were scarce, birds showed a higher acceptance of fruits of intermediate ripeness, but still rejected the least ripe fruit stages. In a foraging bout, most birds fed on fruits of the same ripeness. By doing so, birds maximised instantaneous energy gain per time, because search time was longer for riper fruits while energy intake was lower for less ripe fruits. The results suggest that birds select fruits based on fine-scale differences in profitability, but accept less profitable fruits during low fruit abundance. If environmental factors such as overall fruit availability influence avian fruit choice, we suggest that the potential for directional selective pressures on fruit compounds is restricted.     

Nutrients in fruits as determinants of resource tracking by birds

Fruit pulp is an important source of nutrients for many bird species. Fruit‐eating birds use a variety of strategies to cope with changes in the availability of fruits, exhibiting a remarkable ability to track resources. We assessed the role of nutrient availability in the fruiting environment as a factor driving resource tracking by fruit‐eating birds. Fruit consumption by the four most common frugivorous species in a 6‐ha plot in the Southern Yungas montane forest of Argentina was assessed. We determined the content of selected nutrients (soluble carbohydrates, proteins, phenols, ascorbic acid and essential minerals) in 22 fruiting plant species eaten by birds, and measured fruit–frugivore interactions and the availability of nutrients and dry fruit pulp mass over 2 years. There was strong temporal covariation in the availability of the selected nutrients in fruits across the study period. Similarly, the availability of nutrients in the fruiting environment covaried with pulp mass. Fruit consumption by the four commonest bird species and the abundance of most species were positively associated with nutrient availability and dry pulp mass. Nutrient availability was a good predictor of temporal fruit tracking by three of the four commonest frugivores. Despite large differences in particular nutrient concentrations in fruits, overall nutrient (and pulp) quantity in the fruiting environment played a greater role in fruit tracking than did the nutritional quality of individual fruits. While overall nutrient availability (i.e. across fruit) and total pulp mass were important determinants of fruit tracking, we suggest that plant species‐specific differences in fruit nutrient concentration may be important in short‐term foraging decisions involved in fruit choice and nutritional balance of birds.     

Seed dispersal of fleshy-fruited invasive plants by birds: contributing factors and management options

The ecology of seed dispersal by vertebrates has been investigated extensively over recent decades, yet only limited research has been conducted on how suites of invasive plants and frugivorous birds interact. In this review, we examine how plant fruit traits (morphology, colour and display, nutritional quality, accessibility and phenology), avian traits (fruit handling techniques, gut passage time and effect, bird movements and social behaviour and dietary composition) and landscape structure (fruit neighbourhood, habitat loss and fragmentation and perch tree effects) affect frugivory and seed dispersal in invasive plants. This functional approach could be used to develop generic models of seed dispersal distributions for suites of invasive plant species and improve management efficiencies. Four broad research approaches are described that could direct management of bird‐dispersed invasive plants at the landscape scale, by manipulating dispersal. First, research is needed to quantify the effect of biological control agents on dispersal, particularly how changes in fruit production and/or quality affect fruit choice by frugivores, dispersal distributions of seed and post‐dispersal processes. Second, we explore how seed dispersal could be directed, such as by manipulating perch structures and/or vegetation density to attract frugivorous birds after they have been foraging on invasive plant fruits. Third, the major sources of seed spread could be identified and removed (i.e. targeting core or satellite infestations, particular habitats and creating barrier zones). Fourth, alternative food resources could be provided for frugivores, to replace fruits of invasive plants, and their use quantified.     

Relationships between bird-dispersed plants and avian fruit consumers with different feeding strategies in Japan

We examined the interactions between bird-dispersed plants and fruit-consuming birds with various feeding strategies, by reviewing the plant species consumed by 14 bird species in Japan with four feeding types: gulpers (five species), grinders (four species), crushers (four species), and peckers (one species). Our literature review provided information on the plant species consumed by the birds in Japan and the morphological traits of the fruits: fruit volume, seed mass and number, pulp type (fleshy, dry, or arillate), and plant height (tall, medium, or small). Using these data, we examined the diversity of plant species consumed by each bird and the fruit morphological traits that affected fruit selection. The five gulpers consumed fruits from the largest number of plants, followed by the four grinders, the four crushers, and the one pecker. The gulpers and grinders consumed a wider variety of fruits than were consumed by the crushers and the pecker. Logistic regression analysis revealed that some crushers and the pecker preferred plants with dry or arillate pulp around the seeds. Our results suggest that a frugivorous bird’s feeding strategies, and particularly its fruit-handling behaviors and the fruit parts it ingests, influence the diversity of plants it consumes. The crushers and the pecker, which feed exclusively on seeds, require more effort and time to consume this type of food, and this might cause a strong preference for specific fruit traits and thus, consumption of a lower diversity of plant species.     

植物次生代谢物含量的季节性变化及其对高原鼠兔食物选择的影响

2008 年6 ～9 月在中国科学院海北高寒草甸生态系统定位站通过自助餐式食物选择实验测定了高原鼠兔对20 种植物的取食量,采用紫外可见分光光度计法测定了不同季节20 种植物中黄酮、缩合单宁、简单酚和总酚4种植物次生代谢物的含量,分析了植物次生代谢物含量与高原鼠兔食物选择之间的相互关系。结果表明,在选定的20 种植物中高原鼠兔喜食的植物有7 种,可食的植物有7 种,厌食的植物有6 种。植物次生代谢物的含量在不同的植物间表现出一定的差异,且有生长季节早期含量低,随后逐渐增高的季节性变化趋势。高原鼠兔对植物的选择性与植物中黄酮含量有显著的负相关性,喜食植物的黄酮含量显著低于厌食植物,喜食植物的单宁含量显著小于可食植物,可食植物的单宁含量显著大于厌食植物。在喜食植物中,高原鼠兔取食量与简单酚和总酚含量呈显著负相关性。以上结果部分验证了植物次生代谢物作为植物的防御对策明显影响高原鼠兔对食物选择的假说。黄酮类次生代谢物明显抑制高原鼠兔的取食,缩合单宁对高原鼠兔食物选择也有一定的抑制作用,高原鼠兔有少量取食但避免大量取食简单酚和总酚含量高的植物的选择策略。     

The Ecology and Evolution of Fruit Odor: Implications for Primate Seed Dispersal

Primates are now known to possess a keen sense of smell that serves them in various contexts, including feeding. Many primate species are frugivorous and provide essential seed dispersal services to a variety of plants. Studies of pollination ecology, and recently seed dispersal ecology, indicate that animal mutualist behavior exerts selection pressures that drive changes in flower and fruit traits. As a result, the use of olfaction in in primate feeding ecology may have affected the evolution of fruit odor in species that rely on primate seed dispersal. However, this hypothesis is seldom tested. Here, we summarize the available information on how primates may have affected the evolution of fruit odor. We ask what the chemistry of primate fruit odor may look like, what information fruit odor may convey, whether there are geographical differences in fruit odor, and what other factors may affect the odor of fruits consumed by primates. We identify many gaps in the available data and offer research questions, hypotheses, and predictions for future studies. Finally, to facilitate standardization in the field, we discuss methodological issues in the process of odor sampling and analysis.     

Birds and guelder rose <Emphasis Type="Italic">Viburnum opulus</Emphasis>: selective consumption and dispersal via regurgitation of small-sized fruits and seeds

The evolution of fleshy fruit size, in particular in bird-dispersed plants, is believed to be influenced by the size of seed-dispersing vertebrates through gape limitation. Also, it has been demonstrated that seed size correlates positively with fruit size, especially in single- or few-seeded fruits. However, there is little evidence of current selection pressure by disperser birds on fruit and seed size within populations of a particular plant species. In the present study, this aspect was investigated in guelder rose Viburnum opulus (Caprifoliaceae) fruit consumption by birds in an area in NW Spain. Guelder rose fruits are sub-globose drupes that can exceed 11 mm in width, with a single hard seed of up to 8.5 mm in width. Most of the seeds were dispersed by the robin Erithacus rubecula (gape width < 8 mm) and a small thrush, the song thrush Turdus philomelos (gape width < 11 mm), which swallowed the fruits whole, and some were destroyed by the bullfinch Pyrrhula pyrrhula. Most of the seeds were regurgitated rather than defecated by disperser birds, probably because seed size limited gut processing. The mean size of the ingested seeds was smaller than the mean diameter of Turdus droppings, which in turn was smaller than the mean size of the seeds of the fruits available on the plants. As winter progressed, only larger fruits and seeds remained on the plants (seed and fruit size were positively correlated), and the size of ingested seeds increased. Thus, the largest fruits were consumed less by seed-dispersing birds and were exposed to seed-predators (bullfinches and climbing rodents) for longer. Selection pressure on smaller guelder rose seeds must therefore be effective in the dispersal stage in the study area.     

Beans with bugs: Covert carnivory and infested seed selection by the red-nosed cuxiú monkey

Members of the Neotropical primate genus Chiropotes eat large volumes of immature seeds. However, such items are often low in available proteins, and digestion of seeds is further inhibited by tannins. This suggests that overall plant-derived protein intake is relatively low. We examined the presence of insect larvae in partially eaten fruits, compared with intact fruit on trees, and examined fecal pellets for the presence of larvae. We found that red-nosed cuxiú (Chiropotes albinasus) individuals may supplement their limited seed-derived protein intake by ingesting seed-inhabiting insects. Comparison of fruits partially eaten for their seeds with those sampled directly from trees showed that fruits with insect-containing seeds were positively selected in 20 of the 41 C. albinasus diet items tested, suggesting that fruits with infested seeds are actively selected by foraging animals. We found no differences in accessibility to seeds, that is, no differences in husk penetrability between fruits with infested and uninfested seeds excluding the likelihood that insect-infestation results in easier access to the seeds in such fruits. Additionally, none of the C. albinasus fecal samples showed any evidence of living pupae or larvae, indicating that infesting larvae are digested. Our findings raise the possibility that these seed-predating primates might provide net benefits to the plant species they feed on, since they feed from many species of plants and their actions may reduce the populations of seed-infesting insects.     

Factors affecting seed rain beneath fleshy-fruited plants

We investigated factors affecting seed rain beneath nine fleshy-fruited fruiting plant species growing in a 1-ha plot of planted Pinus thunbergii in central Japan. We tested whether the numbers of seeds and seed species dropped by birds beneath fruiting plants were correlated with the number of fruits removed by birds from the plants. Most of fruiting plant species with high fruit removal had significantly high seed rain. Both the numbers of seeds and seed species dropped were significantly, positively correlated with the number of fruits removed across for all fruiting plant species. Therefore, fruit removal predicted the difference among heterospecific fruiting plants in seed rain. We also tested whether the number of fruits removed from fruiting plants by birds was related with fruit crop size, fruit size, and height of the plants, and the numbers of fruits and fruit species of neighboring plants near the plants. Most of fruiting plant species with high fruit crop size had significantly high fruit removal. The number of fruits removed was significantly, positively correlated with both the fruit crop size and the number of neighboring fruits across the nine fruiting plant species. However, the effect of the neighboring fruit density on fruit removal was lower remarkably than that of fruit crop size. Therefore, fruit crop size best predicted the differences among heterospecific fruiting plants in fruit removal. We suggest that fruiting plant species with high fruit crop size and high fruit removal contribute to intensive seed rain beneath them. This revised version was published online in June 2006 with corrections to the Cover Date.     

Working with mahouts to explore the diet of work elephants in Myanmar (Burma)

At an elephant camp in central Myanmar (Burma), we interviewed mahouts and veterinarians to describe the diet of Asian elephants (Elephas maximus) in a mixed-deciduous forest. Elephants showed a broad dietary breadth (103 plant species from 42 families); consumed mostly browse (94% of plant species); and were very selective about plant parts [e.g., many trees were eaten exclusively for their bark (22%) or fruits (14%)]. The fruits from 29 plant species were recorded to be eaten by elephants. Several of these were found as fruit remains, seeds, or seedlings in elephant dung, suggesting a role of Asian elephants in seed dispersal. Work elephants and their mahouts prove to be a rich source of information to understand wild elephant ecology.     

Feeding ecology and seed dispersal of sympatric cheirogaleid lemurs (Microcebus murinus, Cheirogaleus medius, Cheirogaleus major) in the littoral rainforest of south-east Madagascar

The lemurs of Madagascar are known for their extraordinary species diversity. The mechanisms that allow the coexistence of these species are still poorly known. Here feeding patterns were investigated for three small nocturnal lemur species of Cheirogaleidae ( Microcebus murinus , Cheirogaleus medius and Cheirogaleus major ) occurring sympatrically in a littoral rainforest in south-east Madagascar. During three rainy seasons, the plant species eaten by these three lemurs were described in relation to morphological and biochemical characteristics. All three species were mainly frugivorous and fed on 68 different plant species with small- and medium-sized fruits. A total of 91% of these forage plant species was visited by all three lemur species. Fruits larger than 25–30 mm were avoided. Seeds of a total of 51 food plant species were swallowed and passed the gut unharmed. Thus, even these smaller lemur species play an important role in seed dispersal. There were no differences in the morphological and biochemical characteristics of fruits eaten between the three species, but the feeding height was significantly different between the species. Thus, competition avoidance and niche separation are presumably not based on different feeding patterns of M. murinus , C. medius and C. major in the littoral rainforest, but on different habitat utilization.     

脊椎动物传播植物肉质果中的次生物质及其生态作用

在种子植物-动物的互惠关系中,植物果实成熟后需要吸引种子传播者取食果实,传播其种子至适宜萌发的生境,同时又要防御种子捕食者过度消耗种子。果实内的次生物质(如:配糖生物碱、大黄素、辣椒素)在此过程中起到重要的调控作用。依赖脊椎动物传播的肉质果中往往含有与植物茎、叶内相同的次生物质,其种类繁多,主要分为含氮化合物、酚类化合物和萜类化合物。未成熟果实内富含次生物质(如:单宁、大黄素),主要保护未成熟种子不被潜在的捕食者和食果动物取食,这些次生物质的含量通常随果实成熟而降低;其它次生物质(如:脱辅基类胡萝卜素)的含量随果实成熟而增多,可能起到吸引食果动物的作用。在对脊椎动物捕食的抵御中,果实内不同类型的次生物质促使成熟果实对所有脊椎动物都有毒性(专毒性)或者仅对种子捕食者有毒性(泛毒性)。肉质果内的次生物质对植物-食果动物相互关系的调控作用,还可以通过调节动物取食频次和数量、抑制和促进种子萌发、改变种子在肠道的滞留时间、吸引传播者等生态作用而实现。某种次生物质往往集多种生态作用于一身。目前对肉质果内次生物质与脊椎动物相互关系的探讨还不够深入。未来研究需要综合考虑植物次生物质与果实生理生化、形态学等特征对食果者的综合调控机理;次生物质在种子传播后的调控作用对植物种群或群落结构和分布格局的影响;从动植物协同进化角度探讨植物次生物质的产生、防御和吸引策略与脊椎动物对果实的选择和消费之间的关系等。开展脊椎动物传播肉质果实中次生物质的研究,对完善种子传播机制、植物繁殖和更新格局,丰富动植物相互作用、协同进化理论具有重要的意义。