Estimated coefficients and their standard error (SE) for the selected model after a stepwise procedure applied by means of a general lineal model, where fruit consumption was the response variable, and fruit chromatic contrast, fruit size, crop size, fruit exposure and fruit aggregation were the predictor variables. See Materials and methods and Appendix S4 for details 

Estimated coefficients and their standard error (SE) for the selected model after a stepwise procedure applied by means of a general lineal model, where fruit consumption was the response variable, and fruit chromatic contrast, fruit size, crop size, fruit exposure and fruit aggregation were the predictor variables. See Materials and methods and Appendix S4 for details 

Source publication
Article
Full-text available
In visually-driven seed dispersal mutualisms, natural selection should promote plant strategies that maximize fruit visibility to dispersers. Plants might increase seed dispersal profitability by increasing conspicuousness of fruit display, understood as a plant strategy to maximize fruit detectability by seed dispersers. The role of different pla...

Context in source publication

Context 1
... variables that best explained fruit consumption were crop size and fruit chromatic contrast (Table 1). The inter- action between crop size and fruit chromatic contrast was marginally significant and both variables were selected in the final model. ...

Citations

... Although results showed clear gradients in fruit conspicuousness, we did not investigate the relationship between fruit conspicuousness and their removal by birds. Previous work has documented clear relationships between conspicuousness and the behaviour of frugivores (Ordano et al. 2017). However, other fruit attributes, such as nutrient concentrations and secondary metabolites, can over-ride the importance fruit conspicuousness in determining the behaviour of frugivores (see Lim and Burns 2021). ...
Article
Full-text available
Many plants produce colour-polymorphic fruits. However, the processes responsible for the evolution and maintenance of fruit colour polymorphisms are poorly understood. We investigated the fruit colour polymorphism in Gaultheria depressa var. novae-zealandiae (Ericaceae), a predominantly bird-dispersed, alpine shrub from New Zealand, by testing whether colour morph frequencies vary geographically to maximise fruit-foliage colour contrasts. We also conducted a seed germination experiment to test whether fruit colour morphs vary in their susceptibility to UV damage. Results showed that ‘red’ fruits were more abundant at lower elevations, while ‘white’ fruits were predominant at higher elevations. Leaf colours shifted from ‘green’ in appearance at lower elevations to ‘red’ at higher elevations. Analyses of fruit-foliage colour contrasts showed that ‘red’ fruits were more conspicuous at lower elevations, and ‘white’ fruits were more conspicuous at higher elevations, which was consistent with the hypothesis that colour morph frequencies vary geographically to maximise their conspicuousness to dispersers. However, ‘red’ fruits were generally more conspicuous than ‘white’ fruits, regardless of elevation, indicating that the maintenance of the polymorphism could not be attributed to fruit-foliage colour contrasts alone. The seed germination experiment showed that ‘white’ fruits were more resistant to UV damage, suggesting the preponderance of ‘white’ fruited individuals in the landscape results from a greater degree of protection from UV damage. The fruit colour polymorphism in Gaultheria depressa var. novae-zealandiae therefore appears to be maintained by trade-offs between conspicuousness to dispersers and tolerance to UV damage, advocating a pluralistic approach to the problem in the future.
... By absorbing UV radiation, flavonoids present in stems and leaves are part of a system protecting the photosynthetic apparatus against the toxicity of this radiation. Flavonoids and anthocyanins are present in flowers and fruits as an attractant for pollinating insects [1]. Phenolic acids predominate in roots and seeds and constitute a chemical protective barrier protecting these tissues against infections. ...
Article
Full-text available
Natural defensive substances synthesized by plants that could replace synthetic pesticides in the protection of plants against insect invasions are constantly being sought. The study assessed changes in the qualitative and quantitative composition of secondary metabolites in horse chestnut leaves collected in different locations and differing in the sensitivity of the plant to the invasion by the horse-chestnut leaf miner. An attempt was made to identify compounds that are most responsible for the increased plant resistance to this threat. Additionally, changes in the anatomy of chestnut leaves affected by the pest were presented. It was noticed that the trees differed in the composition of secondary metabolites already in the initial growing season, which should be related to the influence of habitat conditions. The analysis of the profile of the compounds in non-infested and infested horse chestnut leaves revealed a clear response of the plant to the stress factor, i.e., the foraging of the horse-chestnut leaf miner. Catechins seem to be compounds involved in plant resistance. The leaf anatomy showed enhanced accumulation of phenolic compounds at the pest foraging sites. Hypertrophy and thickened and cracked cell walls of the spongy parenchyma were visible in the vicinity of the mines.
... This is remarkable, given the prevalence of quantitative cues for fruit selection among fruiteating birds in the subtropical Andes. For example, bird species use fruit abundance, crop size and pulp-to-seed ratio to choose between fruit species (Blendinger, Giannini, et al., 2015;Ordano et al., 2017;Palacio, Valoy, et al., 2017), while nutrient concentration would be more important in short-term foraging decisions involved in nutrient balance . ...
Article
According to diet‐regulation hypotheses, animals select food to regulate the intake of macronutrients or maximise energy feeding efficiency. Specifically, the nutrient balance model proposes that foraging is primarily a process of balancing multiple nutrients to achieve a nutritional intake target, while the energy maximisation model proposes that foraging aims to maximise energy. Here, we evaluate the adjustment of fruit diets (the fruit‐derived component of the diets) to nutritional and energy intake targets, characterizing the nutrient balance and energy maximisation strategies across fruit‐eating bird species with different fruit‐handling behaviours ("gulpers", which swallow whole fruits, and "mashers", which process the fruit in the beak) in subtropical Andean forests. Food‐handling behaviour determines the food intake rate and, consequently, influences animal efficiency to obtain nutrients and energy. We used extensive field data from the diet of fruit‐eating birds to test how species adjust their food intake. We used nutritional geometry to explore macronutrient balance and the effectiveness framework to explore energy‐acquisition effectiveness. Observed diets showed a good fit with predictions of a diet balanced in macronutrient proportions. With few exceptions, diets clustered near an optimal macronutrient mixture and did not differ from each other in terms of maximising energy intake. Moreover, when comparing our results with a random diet based on local fruit availability, birds tended to fit better to the nutritional target, and less to the energy target, than expected from a random diet. Fruit‐handling behaviour did not affect the ability of bird species to reach a nutritional target but it affected species energy acquisition, which was lower in mashers than in gulpers. This study explores for the first time different diet‐regulation strategies in wild fruit‐eating birds, and supports the argument that the diet reflects a specific regulation of macronutrients. Understanding why birds select fruits is a complex question requiring multiple considerations. The nutrient balance model explains the relevance of nutrient composition in the fruit selection by fruit‐eating birds, although it is still necessary to determine its relative importance with respect to other dietary drivers.
... We measured the reflectance of approx. 20 ripe fruits collected from 8-30 individual plants (see Ordano et al., 2017 for additional details). We used an Ocean Optics USB-2000 spectrometer with a PX-2 pulsed xenon light source to measure reflectance as the proportion of a standard white reference tile (WS-1-SS; Ocean Optics, Duiven, The Netherlands). ...
... We used a database of 10 243 fruit-disperser interactions compiled by P.G.B. from different sources. The heterogeneous characteristic of the data sources (systematic observations and faeces from different surveys; see Ordano et al., 2017) hindered the direct use of the frequencies of the observed interactions between plant and animal species to define functional groups of seed dispersers. Consequently, we merged the sources of information previously calculating the proportion in which each plant species interacted with each disperser species. ...
... The usefulness of utilizing colour to delimit seed dispersal syndromes could be a particular feature of the assemblage, making it difficult to extrapolate to conclusions based on different communities (Poisot et al., 2014). In addition, the role of display in fruits could be accomplished by multiple traits, beyond colour (Ordano et al., 2017;Valenta and Nevo 2020). Fruit odours are a key feature attracting potential dispersers, specially mammals, that are particularly sensitive to this signal (Kalko and Condon, 1998;Korine and Kalko, 2005;Lomáscolo et al., 2010). ...
Article
Background and Aims Fruit traits and their interrelations can affect foraging choices by frugivores, and hence, the probability of mutualistic interactions. Certain combinations of fruit traits that determine the interaction with specific seed dispersers are known as dispersal syndromes. The dispersal syndrome hypothesis (DSH) states that seed dispersers influence the combination of fruit traits found in fruits. Therefore, fruit traits can predict the type of dispersers with which plant species interact. Here, we analysed whether fruit traits’ relationships can be explained by DSH. To do so, we estimated the interrelation between morphological, chemical and display groups of fruit traits. In addition, we tested the importance of each trait-group defining seed dispersal syndromes. Methods Using phylogenetically corrected fruit traits’ data and fruit-seed disperser networks, we tested the relationships among morphological, chemical and display fruit traits with Pearson’s correlations and phenotypic integration indices. Then, we used perMANOVA to test if the fruit traits involved in the analysis supported seed dispersers’ functional types. Key results Morphological traits showed strong intra-group relationships, contrasting to chemical and display traits whose intra-group trait relationships were weak or null. Accordingly, only the morphological group of traits supported three broad seed disperser functional types (birds, terrestrial mammals and bats), consistently with the DSH. Conclusions Altogether, our results give some support to the DSH. Here, the three groups of traits interacted in different ways with seed dispersers’ biology. Broad functional types of seed dispersers would adjust fruit consumption to anatomical limitations imposed by fruit morphology. Once this anatomic filter is surpassed, seed dispersers use almost all the range of variation in chemical and display fruit traits. This suggests that the effect of seed dispersers on fruit traits is modulated by hierarchical decisions. First, morphological constraints define which interactions can actually occur; subsequently, display and composition determine fruit preferences.
... Higher quantities of ripe fruits are expected to increase the probability of detection and frequency of dispersal by frugivores (i.e., "the crop size hypothesis, " Snow, 1971). Plants, therefore, trade-off costs of growth with the frequency and intensity of reproduction that allows for effective interactions with seed dispersers (Obeso, 2002;Ordano et al., 2017). Two alternative fruit production strategies by bird-dispersed plants have consistently been recognized in tropical forests (Howe & Estabrook, 1977;Howe & Smallwood, 1982;Janzen, 1970;McKey, 1975;Snow, 1971). ...
Article
Seed dispersal mutualisms evolve in complex communities of plants and frugivorous animals, within which indirect interactions such as competition and facilitation can occur. Many tropical plants reproduce subannually in multiple episodes per year. Yet, the consequences of episodic reproduction on interactions with seed dispers-ers remain largely unexplored. We studied Guarea guidonia (Meliaceae), a subannually reproducing tree, to examine temporal variation in seed dispersal within a tropical for-ested landscape in the central Dominican Republic. We hypothesized that foraging by dispersers would (a) increase with daily ripe fruit set on focal trees, (b) decrease with increasing ripe fruit biomass of neighboring plants, and (c) decrease in response to the fruiting periods of other taxa at the landscape scale. Over 18 months, we tracked the phenology of 24 focal trees and quantified foraging during fruiting phases through repeated observations, simultaneously measuring seed dispersal in traps beneath isolated bird perches across the study landscape. Date was the only clear predictor of frugivore visitation, with early and late peaks in activity during the 5-month fruiting period. The midseason decline in foraging at focal trees matched a decline in Guarea dispersal to seed traps independently of fruit abundance. Declines in Guarea dispersal were inversely related to peak dispersal of higher quality lipid-rich fruiting species. Our results suggest that multiple flowering episodes and subsequent asynchronous fruit ripening of low-quality fruits can reduce competitive pressure from other higher quality fruiting species, implying that this potential bet-hedging strategy may be an overlooked factor in the evolution of subannual reproduction. Abstract in Spanish is available with online material.
... We found an increase in the fruit ingestion probability for birds when more fruits were on the feeders. The positive relationship might be explained first by the increased visual appeal when the fruits were more abundant which increased the fruits' conspicuity (Martin Schaefer et al. 2007), but also as a chromatic contrast, making them more attractive for visually oriented birds (Ordano et al. 2017). Such visual appeal could decrease neophobia from feeders, acting as a signal of a less dangerous resource than if a single or few fruit specimens were found (Greenberg and Mettke-Hofmann 2001). ...
Article
Full-text available
Anthropocentric defaunation affects critical ecological processes, such as seed dispersal, putting ecosystems and biomes at risk, and leading to habitat impoverishment. Diverse restoration techniques could reverse the process of habitat impoverishment. However, in most of the restoration efforts, only vegetation cover is targeted. Fauna and flora are treated as isolated components, neglecting a key component of ecosystems' functioning, the ecological interactions. We tested whether the resilient frugivorous generalist fauna can improve habitat quality by dispersing native plant species through the use of fruit feeders as in a semideciduous seasonal urban forest fragment. A total of 32 sampling points was selected at a heavily degraded 251-ha urban forest fragment, with feeders installed at two heights monitored by camera-traps. Variable quantities of native fruits of 27 zoochorous species were offered alternately in the feeders. Based on more than 36,000 h of video records, Turdus leucomelas (Class Aves), Sapajus nigritus (Class Mammalia), and Salvator merianae (Class Reptilia) were recorded ingesting the highest fruit species richness. Didelphis albiventris (Class Mammalia) was the most frequent visitor but consumed only pulp in most of the visits. The frugivorous birds were recorded at a high visitation rate and consumed a wider variety of fruits. Our study opens a new avenue to combine the traditional approach of ecosystems recovery and ecological interactions restauration in an urban forest fragment. Supplementary information: The online version contains supplementary material available at 10.1007/s11252-020-01080-5.
... In bird-plant frugivory interactions, certain fruit characteristics influence how they are selected, determine their consumption rate by birds, and ultimately rule how their networks are structured. Examples of such characteristics are nutritional content (Gautier-Hion et al., 1985;Jordano, 2000;Cazetta et al., 2012;Blendinger et al., 2015), fruit size, seed quantity, and seed size (Wheelwright, 1985), and detectability as determined by their color (Van der Pijl, 1982;Schaefer and Schmidt, 2004;Schmidt et al., 2004;Cazetta et al., 2012;Duan et al., 2014;Ordano et al., 2017). In addition to characteristics of fruit availability, the organization of these bird-plant frugivory interactions can be affected by the relationship between a bird's bill and fruit morphology (González-Castro et al., 2015;Bender et al., 2018), the spatiotemporal overlap of species (Ramos-Robles et al., 2016), and the relative abundance of fruits and birds (González-Castro et al., 2015). ...
... We also expected that nutritional content and chromatic contrast would have a considerable predictive value since birds actively seek to fulfill certain dietary needs through fruit consumption (Petchey et al., 2008). In the case of chromatic contrast, our prediction was that fruits that have a higher background contrast would also have a higher detectability Ordano et al., 2017). Last, we expected morphological matching would have the lowest predictive value since disturbed areas have a higher trait similarity (e.g., fruit and bird bill sizes), and less network-wide morphological limitations due to fruits of large size and frugivores capable of consuming them (Corlett, 2005;Galetti et al., 2013). ...
... Because fruit detectability, the ease to stand out against its background, has been demonstrated to influence fruit consumption (Schaefer et al., 2007(Schaefer et al., , 2014Ordano et al., 2017), we used chromatic contrast as a detectability proxy. We determined the reflectance of each plant by collecting spectrophotometry values of five different fruits and five different leaves per species. ...
Article
Full-text available
Frugivory interactions between birds and fruit-bearing plants are shaped by the abundance of its interacting species, their temporal overlap, the matching of their morphologies, as well as fruit and seed characteristics. Our study evaluates the role of seven factors of fruits and plants in determining the frequency of whole-fruit consumption by birds. We studied the frugivory network of a Neotropical periurban park in Xalapa, Veracruz, Mexico, and quantified relative abundance and phenology of birds and fruit, as well as fruit morphology, chromatic and achromatic contrast, and nutritional content. Using a maximum likelihood approach, we compared the observed interaction network with 62 single- and multiple-variable probabilistic models. Our network is composed of 11 plants and 17 birds involved in 81 frugivory interactions. This network is nested, modular, and relatively specialized. However, the frequency of pairwise interactions is not explained by the variables examined in our probabilistic models and found the null model has the best performance. This indicates that no single predictor or combination of them is better at explaining the observed frequency of pairwise interactions than the null model. The subsequent four top-ranking models, with ΔAIC values < 100, are single-variable ones: carbohydrate content, lipid content, chromatic contrast, and morphology. Two- and three-variable models show the poorest fit to observed data. The lack of a deterministic pattern does not support any of our predictions nor neutral- or niche-based processes shaping the observed pattern of fruit consumption in our interaction network. It may also mean that fruit consumption by birds in this periurban park is a random process. Although our study failed to find a pattern, our work exemplifies how investigations done in urban settings, poor in species and interactions, can help us understand the role of disturbance in the organization of frugivory networks and the processes governing their structure.
... PSMs that determine fruit color, odor, and flavor can also be general attractants that allow a disperser to detect and decide to visit a plant ( Figure 1B) [26,27]. Fruit color is typically composed of PSMs that act as pigments, such as carotenoids, flavonoids, and betalains [28], that often make fruits more visually conspicuous and can also serve as nutrients for dispersers such as diurnal birds and mammals [27,29]. ...
... PSMs that determine fruit color, odor, and flavor can also be general attractants that allow a disperser to detect and decide to visit a plant ( Figure 1B) [26,27]. Fruit color is typically composed of PSMs that act as pigments, such as carotenoids, flavonoids, and betalains [28], that often make fruits more visually conspicuous and can also serve as nutrients for dispersers such as diurnal birds and mammals [27,29]. Fruit odor and flavor consist of tens to hundreds of unique volatile PSMsprimarily terpenoids, fatty acid derivatives, aromatic compounds, and nitrogenand sulfur-containing compoundsthat typically attract dispersers such as ants and mammals [26,[30][31][32]. ...
... Fruit odor and flavor consist of tens to hundreds of unique volatile PSMsprimarily terpenoids, fatty acid derivatives, aromatic compounds, and nitrogenand sulfur-containing compoundsthat typically attract dispersers such as ants and mammals [26,[30][31][32]. A plant may receive more visits if it produces many fruits with high amounts of attractive PSMs [27]. A plant could also potentially receive more visits if it produces fruit with more complex blends of PSMs, which may increase their detectability or specificity of signaling ( Figure 1B) if dispersers rely on mixtures of PSMs to select fruits to remove [33]. ...
Article
Plant secondary metabolites (PSMs) play a central role in seed dispersal and fruit defense, with potential for large impacts on plant fitness and demography. Yet because PSMs can have multiple interactive functions across seed dispersal stages, we must systematically study their effects to determine the net consequences for plant fitness. To tackle this issue, we integrate the role of fruit PSMs into the seed dispersal effectiveness (SDE) framework. We describe PSM effects on the quantity and quality of animal-mediated seed dispersal, both in pairwise interactions and diverse disperser communities, as well as trade-offs that occur across dispersal stages. By doing so, this review provides structure to a rapidly growing field and yields insights into a critical process shaping plant populations.
... Fruit crop size is a crucial determinant of frugivore-mediated selection, as the number of fruits produced is a strong attraction signal in visually driven seed dispersal mutualisms (Snow 1971;Ordano et al. 2017;Palacio and Ordano 2018). Our results showed that fruit crop size was the most important selection target, as it showed the highest selection strength across the three populations (Table 2). ...
... It should be noted that fitness differences may be the result of larger crop sizes, rather than of selective removal. Although the debate of the role of frugivores in the evolution of fruit and seed traits remains contentious (Herrera 1985;Jordano 1995;Harrison et al. 2012), fruit crop size is one of the fruit traits frequently reported as a target of frugivore-mediated selection across populations of the same species (Ortiz-Pulido and Rico-Gray 2000;Sobral et al. 2013;Palacio and Ordano 2018), as well as across species (Izhaki 2002;Ordano et al. 2017). Although fruit crop size is not a phenological trait per se, fruit availability of a given plant changes through time (Fig. 4). ...
Article
Full-text available
Fruiting phenology is a critical aspect of plant fitness, as it is directly linked to the next-generation offspring delivery. Both abiotic and biotic factors presumably exert natural selection on plant phenology. Despite the role of climate in shaping fruiting phenology is well established, whether frugivores exert phenotypic selection on fruiting phenology has not yet been tested. We estimated the regime and magnitude of frugivore-mediated selection on fruiting phenology in three distant (> 500 km) populations of the Blue Passionflower (Passiflora caerulea) along one year. We measured phenological fruit traits (fruiting onset, fruiting peak, length of the fruiting season) and fruit crop size, and used animal fruit removal as a fitness component. We found highly variable fruiting phenologies between populations, yet phenological stages in lower latitudes were longer than in higher latitudes. One population showed a positive relationship between fruiting onset and fruiting peak among individuals, indicating that fruiting later in the season delayed the fruiting peak. Frugivores favored large fruit crop sizes in the three populations and early fruiting onsets in two populations. In two populations, frugivores selected favorable combinations of fruit crop size and fruiting peak (favoring plants with large crops and early fruiting peaks), as well as favorable combinations of fruiting peak and the length of the fruiting season (favoring plants with early fruiting peaks and extended fruiting seasons). Some degree of similarity in selection patterns among populations suggests that, despite strong geographic variation in climate and animal assemblage composition, some level of functional redundancy occurs in terms of phenotypic trait selection. Overall, our results show that fruiting phenology may be a highly variable life-history trait of plant populations, and support the idea that biotic interactors, conditional on heritable traits and selection pressures sustained over time, could potentially shape phenological fruiting characteristics.
... We have previously described the morphological and chemical traits of 43 fruit species included in the diet of the three frugivore species used in the study (Blendinger et al., 2012;Ordano et al., 2017;Ruggera et al., 2016;S anchez, Giannini, & Barquez, 2012;S anchez, Carrizo, et al., 2012). We randomly collected ripe fruits from various native plant individuals, which came from 10e30 different individual plants depending on the fruit and plant availability in the field. ...
Article
Full-text available
Several hypotheses explain how sensory, anatomical and physiological constraints drive fruit preference in frugivores. Optimal diet theory (ODT) states that frugivores make decisions based on the energy contained in food. In contrast, geometry of nutrition (GN) states that animals balance their macronutrient intake instead, opting for rough energy. The defence trade-off hypothesis (DTH) assumes a negative relationship between secondary compounds and fruit preference. Finally, the size-matching hypothesis (SMH) states that frugivores are more attracted to fruits that are easier to handle and consume. We tested these four hypotheses by offering paired fruit species to three fruit-eating animal species in captivity that either chew fruit in the beak or mouth (‘masher’: 1 bird species, 1 bat species) or swallow whole fruits (‘gulper’: 1 bird species), from which we built a ranking of fruit preference. We then explored the importance of 13 fruit traits in explaining fruit preference. The masher bird was the only species whose fruit preference pattern corresponded with GN. Fruit preference of the masher and gulper bird species supported DTH and SMH, while fruit preference by the bat species was not related to any analysed trait. More than one single rule governs fruit preference in different frugivore species. Fruit preferences of functionally different frugivore species are affected by particular fruit traits, which they either select or avoid. The search for specific macronutrients, while avoiding toxicity in fruits matching the anatomical limitations of frugivores, could lead to complementary foraging choices. Variability between seed disperser species in their search for easily manageable fruits allows achieving a complementary fruit diet, with preferred and avoided traits. It can be an important driver of fruit trait diversity in fleshy-fruited plant assemblages.