Ant seed removal in a non-myrmecochorous Neotropical shrub: Implications for seed dispersal

This study investigated ant seed removal of Piper sancti-felicis, an early successional Neotropical shrub. Neotropical Piper are a classic example of bat-dispersed plants, but we suggest that ants are underappreciated dispersal agents. We identified eleven ant species from the genera Aphaenogaster, Ectatomma, Paratrechina, Pheidole, Trachymyrmex, and Wasmannia recruiting to and harvesting P. sancti-felicis seeds in forest edge and secondary forest sites at La Selva, Costa Rica. We also tested for differences in ant recruitment to five states in which ants can commonly encounter seeds: unripe fruit, ripe fruit, overripe fruit, bat feces, and cleaned seeds. Overall, ants harvested more seeds from ripe and overripe fruits than other states, but this varied among species. To better understand the mechanisms behind ant preferences for ripe/overripe fruit, we also studied how alkenylphenols, secondary metabolites found in high concentrations in P. sancti-felicis fruits, affected foraging behavior in one genus of potential ant dispersers, Ectatomma. We found no effects of alkenylphenols on recruitment of Ectatomma to fruits, and thus, these compounds are unlikely to explain differences in ant recruitment among fruits of different maturity. Considering that P. sancti-felicis seeds have no apparent adaptations for ant dispersal, and few ants removed seeds that were cleaned of pulp, we hypothesize that most ants are harvesting its seeds for the nutritional rewards in the attached pulp. This study emphasizes the importance of ants as important additional dispersers of P. sancti-felicis and suggests that other non-myrmecochorous, vertebrate-dispersed plants may similarly benefit from the recruitment to fruit by ants.     

Trophic structure of a neotropical frugivore community: is there competition between birds and bats?

Summary Dietary overlap and competition between frugivorous birds and bats in the Neotropics have been presumed to be low, but comparative data have been lacking. We determined the diets of volant frugivores in an early successional patch of Costa Rican wet forest over a one month period. Ordination of the diet matrix by Reciprocal Averaging revealed that birds and bats tend to feed on different sets of fruits and that diets differed more among bat species than among bird species. However, there was overlap between Scarlet-rumped Tanagers and three Carollia bat species on fruits of several Piper species which comprised most of the diet of these bats. Day/night exclosure experiments on P. friedrichsthalli treetlets provided evidence that birds deplete the amount of ripe fruit available to bats. These results indicate that distantly related taxa may overlap in diet and compete for fruit, despite the apparent adaptation of animal-dispersed plant species for dispersal by particular animal taxa.     

Phenology of neotropical pepper plants (Piperaceae) and their association with their main dispersers, two short-tailed fruit bats, Carollia perspicillata and C. castanea (Phyllostomidae)

To relate differences in phenological strategies of a group of closely related plants to biotic (pollinators, dispersers) and abiotic (water, light) factors, we studied leafing, flowering, and fruiting phenology of 12 species of Piper (Piperaceae) in a neotropical lowland forest in Panama for 28 months. We asked how Piper may partition time and vertebrate frugivores to minimize possible competition for dispersal agents. Based on habitat preferences and physiological characteristics we discriminate between forest Piper species (eight species) and gap Piper species (four species). Forest Piper species flowered synchronously mostly at the end of the dry season. Gap Piper species had broader or multiple flowering peaks distributed throughout the year with a trend towards the wet season. Both groups of Piper species showed continuous fruit production. Fruiting peaks of forest Piper species were short and staggered. Gap Piper species had extended fruiting seasons with multiple or broad peaks. Both groups of Piper species also differed in their time of ripening and disperser spectrum. Forest Piper species ripened in late afternoon and had a narrow spectrum consisting mainly of two species of frugivorous bats: Carollia perspicillata and C. castanea (Phyllostomidae). Fruits of gap Piper species, in contrast, ripened early in the morning and were eaten by a broader range of diurnal and nocturnal visitors, including bats, birds, and ants. We conclude that the differences in flowering phenology of forest and gap Piper species are primarily caused by abiotic factors, particularly the availability of water and light, whereas differences in fruiting patterns are mostly influenced by biotic factors. The staggered fruiting pattern of forest Piper species may reflect competition for a limited spectrum of dispersers. The long and overlapping fruiting periods of gap Piper species are associated with a larger spectrum of dispersers and may be a strategy to overcome the difficulty of seed dispersal into spatially unpredictable germination sites with suitable light conditions.     

Vertebrate Fruit Removal and Ant Seed Dispersal in the Neotropical Ginger Renealmia alpinia (Zingiberaceae)*

Plants frequently display fruit characteristics that support multiple seed‐dispersal syndromes. These ambiguous characteristics may reflect the fact that seed dispersal is usually a complex process involving multiple dispersers. This is the case for the Neotropical ginger Renealmia alpinia (Zingiberaceae). It was originally suggested that the aromatic fruits of R. alpinia located at the base of the plant are adapted for terrestrial mammal seed dispersal. However, the dark‐purple coloration of the fruits and bright orange aril surrounding the seeds suggest that birds may play a role in R. alpinia seed dispersal. At La Selva Biological Station, Costa Rica, we used camera traps to record vertebrate visits to infructescences of R. alpinia. Most visitors were toucans and aracaris (Ramphastidae). However fruits were also removed by terrestrial mammals (coatis and armadillos). In addition to vertebrate fruit removal, some of the fruits dehisce and the seeds that fall on the ground are dispersed by ants. Fruitfall traps showed that 77 percent of fruits are removed by vertebrates. However, 15 percent of fruits fall to the base of parent plants to be potentially dispersed by ants. Experiments using a laboratory ant colony showed that ants are effective seed dispersers of R. alpinia. Ant seed manipulation increased germination success and reduced time to germination. In conclusion, primary seed dispersal in the Neotropical ginger R. alpinia is mostly performed by birds, additionally ants are effective dispersers at short distances. Seed dispersal in R. alpinia is a complex process involving a diverse array of dispersal agents.     

Seed Dispersal in the Dark: Shedding Light on the Role of Fruit Bats in Africa

In spite of their recognized importance as seed dispersers in other parts of the tropics, seed dispersal by fruit bats has received scant research attention in Africa. To evaluate the role of African fruit bats in seed dispersal, we studied fruits and seeds below 480 bat feeding roosts in the East Usambara Mountains of Tanzania. We compared these findings to those reported in other African localities to place our results in a broader context. We found 49 plant species dispersed by bats: 28 species, 18 genera, and one family are novel reports of bat dispersal in Africa. Approximately 20 percent of the submontane tree flora of the East Usambaras is bat‐dispersed, including both widespread and endemic trees. African fruit bats are important seed dispersers at our study site because they move seeds of dozens of species tens or hundreds of meters, even seeds that are too large to ingest (greater than 5 mm in length). Fruit bats are likely important seed dispersers in other Afrotropical forests, as bats elsewhere in Africa are known to consume 20 genera and 16 species of plants reported here. Insights from studying remains under bat feeding roosts offer a simple method to further document and substantially increase our understanding of the role of African fruit bats in seed dispersal.     

Geographic variation in fruit colour is associated with contrasting seed disperser assemblages in a south‐Andean mistletoe

Fruit colour influences fruit choice by seed dispersers. The mistletoe Tristerix corymbosus (Loranthaceae) produces mature fruits of two different colours in two different biomes: yellow in the Chilean matorral and green in the temperate forest of southern South America. We conducted field surveys to establish the association between fruit colour and disperser identity throughout the entire geographical range of T. corymbosus. We selected 22 populations, eight of which were located in the Chilean matorral and 14 in the temperate forest south of the matorral. To identify the seed dispersers of the mistletoe we used direct observation, camera traps, and live‐trapping of small mammals. We also report experiments to assess fruit selection by seed dispersers based on differences in colour. The assemblages of dispersers of T. corymbosus differ between the two biomes: yellow fruits in Chilean matorral are exclusively dispersed by three bird species while green fruits in the temperate forest are exclusively dispersed by a marsupial. The differences in the assemblages of seed dispersers can be explained by differences in food‐finding strategies between the two assemblages. Green fruits in temperate forest are not easily detected by birds, while colour might not be an important cue for the marsupial because it is nocturnal and uses other senses to locate food. We propose that the association between the marsupial and the green‐fruited mistletoe constitutes an ecological fitting rather than the outcome of a co‐evolutionary process. The marsupial might have allowed the mistletoe T. corymbosus to retain green coloration in mature fruit, a condition to which it is preadapted by a slower ripening process in temperate forest populations.     

Non-native mammals are weak candidates to substitute ecological function of native avian seed dispersers in an island ecosystem

Although prominent examples exist of non-native species causing substantial ecological harm, many have neutral or positive effects, including filling surrogate roles once performed by extinct native organisms. We tested the ecological roles of two non-native mammals as seed dispersers or seed predators in Guåhan, which, due to invasive brown tree snakes (Boiga irregularis), is devoid of native seed dispersers–birds and bats. We conducted feeding trials with captive rats (Rattus spp.), which are present but uncommon due to predation by snakes, and pigs (Sus scrofa), which are abundant. We examined if and how they interacted with common forest fruits. We then compared how any gut-passed or animal-handled seeds germinated compared to seeds left in whole fruit or depulped seeds. Rats and pigs interacted with most of the fruits and seeds (>80%) that they were fed. Of those, most seeds were destroyed—78% for rats and 90% for pigs, across both native and non-native plant species. Compared to seeds germinating within whole fruits, rats improved germination of the seeds that they handled without ingesting, while pigs diminished the germination of seeds that they handled. The small percentage of seeds (approximately 1.5% for rats and 5% for pigs) that survived gut passage germinated in higher proportions than those in whole fruits. Percentages of seed survival to germination are lower than found in similar studies with native avian frugivores. Our results indicate that pigs and rats have mixed effects on seeds, but are not suitable surrogates for native seed dispersers.     

VARIATION IN AVERAGE SEED SIZE AND FRUIT SEEDINESS IN A FRUIT CROP OF A GUANACASTE TREE (LEGUMINOSAE: ENTEROLOBIUM CYCLOCARPUM)

A detailed examination of the ordinary 1980 fruit crop of an ordinary large adult guanacaste tree (Enterolobium cyclocarpum) in Guanacaste Province, Costa Rica (1980) shows that for fruits with about 6-16 seeds (range, 1-18 seeds per fruit) there is about ***1 g dry weight fruit tissue per seed (seeds averaging about 820 m each). Fruits that have about 1-5 seeds on average have 1.5-3 times as much dry fruit tissue per seed as do the seed-rich fruits, and also contain seeds that weigh about 8% more on average than the seeds in the seed-rich fruits. The average seed weight per fruit was found to decrease slightly if all sizes of fruits are considered, but to remain essentially constant over the range of 7-16-seeded fruits. This category contained 78% of the fruits. These findings suggest that different parts of the seed crop may end up in different dispersers and dispersers with different preferences for fruit seediness and tolerances for seed size may remove different portions of the seed crop.     

Fruit characteristics and factors affecting fruit removal in a Panamanian community of strangler figs

We describe fruiting characteristics for 12 species in a community of strangler figs (Moraceae: Urostigma) studied in Panama. We quantify diurnal and nocturnal removal rates and proportions of fruits removed, and relate them to the activities of the main dispersers of the figs: bats and birds. These results combined with previous studies show that there are clear differences between fig species with fruit that ripen red and those with fruit that remain green(ish). In the red-fruited species, the fruit are small, ripen asynchronously over relatively long periods, produce little scent, and are mainly taken during the day by birds. In contrast, in the green(ish)-fruited species, the fruits are larger, span a range of sizes, ripen relatively synchronously, produce very distinctive aromas, and are mainly taken at night by bats. This dichotomy in fruiting characteristics suggests coadaptive links between groups of dispersers and different species within the genus Ficus. All fig species produce a range of fruit crop sizes (10–155 fuits/m² canopy area) of which a high proportion were removed by seed dispersers (>80%). Removal rates (fruit removed per day) were positively correlated with crop size, suggesting that trees with large crop size attract more frugivores. Removal rates of green-fruited figs were significantly lower and persistence and abortion of ripe fruit were significant higher around full moon, apparently due to the reduced activity of bats. We further estimate the number of bats that are sustained by a tree fruit crop and account for the observed fruit removal. We then discuss the evidence for coadaptation between different groups of figs and their seed dispersers, Finally, we consider the conservation implications for figs as keystone resources in tropical forests. Received: 26 April 1999 / Accepted: 10 January 2000     

The effect of unripe fruits on ripe fruit removal by birds in Pistacia terebinthus: flag or handicap?

The shrub Pistacia terebinthus produces crowded infructescences with up to several hundred fruits, which are bright red when unripe and turn green when ripe. Most fruits contain an empty seed and never reach maturity. More ripe fruits were removed by birds from experimental bicolored fruit displays (consisting of infructescences with ten ripe fruits and stripped of unripe fruits, paired with infructescences with only unripe fruits) than from monocolored ones (single infructescences with ten ripe fruits and stripped of unripe fruits). Thus, the presence of unripe fruits seems to increase the conspicuousness or attractiveness of fruit displays to fruit-eating birds. A second experiment compared ripe fruit removal from experimental infructescences having only ripe fruits, with that from control infructescences containing both ripe fruits and natural numbers of unripe fruits, all on P. terebinthus plants. Unlike the first experiment, each bicolored display in this case consisted of a single infructescence with both unripe and ripe fruits. A higher proportion of ripe fruits was removed by birds from infructescences free of unripe fruits. This result suggests that the presence of unripe fruits reduces the accessibility of ripe fruits for fruit-eating birds. This is further supported by field observations of bird foraging behavior.     

Iridoid glycosides from fruits reduce the growth of fungi associated with fruit rot

Aims Ripe, fleshy fruits generally function as rewards to attract mutualistic seed dispersers, but many fruits also contain high concentrations of toxic secondary metabolites. These compounds may serve a variety of adaptive roles in seed dispersal or as a defense against non-dispersing seed predators or pathogens. We tested the effects of iridoid glycosides from fruits of a hybrid bush honeysuckle, Lonicera × bella, on the growth of two pathogenic fungal strains associated with fruit rot, Alternaria tenuissima and Aspergillus tubingensis.Methods Fungi were isolated from field-collected L. × bella fruits and identified using molecular techniques. Their growth rates were assessed in vitro in the presence of varying concentrations of pure loganin, one of the most abundant iridoid glycosides in fruits, as well as fruit extracts containing a mix of at least seven different iridoid glycosides.Important findings Loganin had strong dose-dependent negative effects on the growth of both fungi. Extracts from fruits had no effect on Aspergillus but a strong antifungal effect on Alternaria that increased with fruit ripening. Total iridoid glycoside concentrations in extracts were not good predictors of variation in fungal growth, but several individual compounds had significant negative effects. Although iridoid glycosides have primarily been studied as antiherbivore defenses in leaves, these results indicate that they can also function to reduce the growth of fungi associated with fruit rot.     

Crop Size and Fruit Neighborhood Effects on Bird Visitation to Fruiting Schefflera morototoni Trees in Puerto Rico1

Studies of zoochorous seed dispersal systems often consider crop size, yet seldom consider the kinds and amounts of fruits surrounding parent plants (the fruit neighborhood) when attempting to explain among‐plant variation in fruit removal. We studied avian frugivory at 24 Schefflera morototoni trees from February to May 1998 in central Puerto Rico. The number of fruits removed by avian seed dispersers per visit was similar among focal trees (typically 2–4). In contrast, visitation rate was highly variable (range: 0–71 visits per 4 h). We used multiple regression analyses to evaluate the relative roles of crop size (focal tree ripe fruit abundance) and fruit neighborhood variables (measured within 30 m of focal trees) in affecting visitation to focal trees by avian frugivores. Visitation rate was positively related to crop size (although this variable was only significant in one of four regression models considered) and negatively related to the presence or abundance of conspecific fruits, suggesting that trees competed intraspecifically for dispersers. Relationships between visitation and heterospecific fruits were mixed—some kinds of fruits appeared to enhance visitation to focal trees, while others seemed to reduce visitation. In most regression models, neighborhood variables had larger effects on visitation than focal tree fruit crop size. Our results highlight the important effects of local fruiting environments on the ability of individual plants to attract seed dispersers.     

Facultative ripening in Hamelia patens (Rubiaceae): effects of fruit removal and rotting

Summary In Costa Rica individual Hamelia patens trees produce fruit throughout the year and experience dramatic changes in rates of fruit removal and rotting. During some moths, most fruits rot because they are not removed. Rotting fruits increase the probability that other fruits on the same infructescence will rot. When removal rates are high, fruits are taken as soon as their seeds become viable but before the fruit is completely ripe. Experimental removal of fruits produced significantly higher ripening rates than on control infructescences. This response allows Hamelia to ripen more fruit and increase the number of fruits taken when dispersers are abundant (e.g., during migration). The proximate mechanism of this response probably includes reallocation of energy conserved when partially ripe fruits are removed. Responding to fluctuating disperser populations likely increases dispersal success and may function as the ultimate cause.     

Predispersal seed predation on five Piper species in tropical rainforest

Absolute number of seeds lost to predispersal seed predators and proportion of total seeds lost per infructescence were compared among five Costa Rican Piper species of different annual fecundities. Mean seed number and mean seed size in the five species were negatively correlated. The impact of predation on these species was inversely related to the number of seeds they produced. The two early successional species had very high fecundities, a combination of many seeds per infructescence, many infructescences per plant, and, in one species, year-round reproduction. Although seed predators destroyed as many or more seeds of these early successional species than they did of the less fecund, late successional species, this loss accounted for a relatively minor proportion (9 and 12%) of the seeds of the early successional species. In contrast, late successional species produced fewer, larger seeds in a smaller number of infructescences and were not continually in fruit. One of these species, which produced intermediate numbers of intermediately sized seeds, lost 30% of the seeds in each infructescence on average. Seed predators destroyed a larger proportion (65 and 76%) of the seeds per infructescence in the two species with fewest seeds per infructescence. High levels of insect damage in these late successional species caused many of their infructescences to abort prematurely. Taken together these factors resulted in annual fecundities several orders of magnitude smaller in shade-tolerant Piper species than the annual fecundities of shade-intolerant, early successional species. Seedlings of the two early successional species were common in large gaps and other sunny clearings and seedlings of the species with 30% seed loss were occasional, whereas no seedlings were seen of the two species with the highest proportional seed loss, suggesting that seed predation on the latter species may limit seedling recruitment.     

Impact on fruit removal and seed predation of a secondary metabolite, emodin, in Rhamnus alaternus fruit pulp

There are two contradictory approaches to explaining the presence of secondary metabolites in ripe fruits. One holds that they evolved toward enhancing dispersal success (adaptive approach); the other claims that they evolved primarily to deter herbivores from eating leaves and seeds and that their presence in ripe fruits is a byproduct of that function (non‐adaptive approach). We tested the validity of three hypotheses of the adaptive approach that explain the presence of secondary metabolites in ripe fruits. We explored the current function of a secondary metabolite, emodin, in Mediterranean buckthorn (Rhamnus alaternus, Rhamnaceae) fruits by relating intraspecific variation and seasonal patterns of concentration to fruit removal and seed damage and by conducting feeding trials with captive birds presented artificial fruits that varied in emodin concentration. The concentration of emodin in the pulp of 10–13 Rhamnus plants from the same population was determined by HPLC every month during two fruiting seasons. Fruit removal by birds and seed predation by invertebrates and microbes were determined for the same plants. Emodin concentration rose during the first stages of ripening, reaching a peak before the fruits were ripe, and then decreased to a minimum when the fruits were ripe. No significant correlation between emodin concentration and ripe fruit removal rate among trees was observed in the first year, whereas in the second year the correlation was positive and significant. Thus, the impact of emodin on fruit selection varied between years, suggesting that emodin concentration does not solely govern fruit selection. A significant negative correlation was found in the first year between emodin concentration and seed predation during the first fruiting month. The yellow‐vented bulbul (Pycnonotus xanthopygos), a seed dispersing bird, distinguished between artificial foods that differed in emodin concentration (control, 0.001% and 0.002%), always preferring the lower concentration. In contrast, house sparrows, (Passer domesticus), a seed predator, did not detect such differences in emodin concentration but did distinguish between control foods and food with 0.005% and 0.001% emodin. We suggest that emodin has an ecological role, preventing seed predation by invertebrates and microbes without decreasing fruit removal by avian dispersers.     

How human disturbance of tropical rainforest can influence avian fruit removal

Fruit consumption by birds is an important ecological interaction that contributes to seed dispersal in tropical rainforests. In this field experiment, we asked whether moderate human disturbance alters patterns of avian frugivory: we measured fruit removal by birds in the lower montane rainforest of Tobago, West Indies, using artificial infructescences made with natural fruits from two common woody plants of the forest understory (Psychotria spp., Rubiaceae). Displays were mounted simultaneously in three forest habitats chosen to represent a gradient of increasing habitat disturbance (primary, intermediate and disturbed), caused by subsistence land use adjacent to a protected forest reserve. We measured the numbers of fruits removed and the effect of fruit position on the likelihood of removal, along with the abundances of all fruits and fruit‐eating birds at the study sites. Fruit removal was highly variable and there was not a significant difference in removal rate among forest habitats; however, the trend was for higher rates of removal from displays in primary forest. Canopy cover, natural fruit availability, and frugivore abundance were not good predictors of fruit removal. Birds preferred more accessible fruits (those proximal to the perch) in all habitats, but in disturbed forest, there was a tendency for distal fruits to be chosen more frequently than in the other forest types. One possible explanation for this pattern is that birds in disturbed forests were larger than those in other habitats, and hence were better able to reach the distal fruits. Coupled with differences in bird community composition among the forest types, this suggests that different suites of birds were removing fruit in primary versus disturbed forest. As frugivore species have different effectiveness as seed dispersers, the among‐habitat differences in fruit removal patterns that we observed could have important implications for plant species experiencing disturbance; these possible implications include altered amounts of seed deposition and seedling recruitment in Tobago's tropical rainforest.     

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 São 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.     

Diet and trophic structure in assemblages of montane frugivorous phyllostomid bats

Neotropical frugivorous bats display a trophic structure composed of bat species with dietary preferences of core plant taxa (Artibeus-Ficus  +  Cecropia, Carollia-Piper, Sturnira- Solanum  +  Piper). This structure is hypothesized to be an ancestral trait, suggesting that similar diets would be observed throughout a species' range. However, most evidence comes from lowlands where data from montane habitats are scarce. In high mountain environments both diversity of bats and plants decreases with altitude; such decline in plant diversity produces less plants to feed from, which should ultimately affect the trophic structure of frugivorous bats in mountain environments. Here, we present a comprehensive review of the diet of frugivorous bats in Neotropical montane environments and evaluate their trophic structure in middle and higher elevations by combining a literature database with field data. We use the concept of modularity to test whether frugivorous montane bats have dietary preferences on core plant taxa. Our database revealed 47 species of montane bats feeding on 211 plant species. We find that the networks are modular, reflecting the trophic structure previously reported. We also found that in highlands the tribe Ectophyllini are Cecropia  +  Cavendishia-specialists rather than Ficus-specialists, and we describe new interactions reflecting 14 species of plants, including three botanical families previously not reported to be consumed by bats.     

Evolution of angiosperm seed disperser mutualisms: the timing of origins and their consequences for coevolutionary interactions between angiosperms and frugivores

The origins of interactions between angiosperms and fruit‐eating seed dispersers have attracted much attention following a seminal paper on this topic by Tiffney (1984). This review synthesizes evidence pertaining to key events during the evolution of angiosperm–frugivore interactions and suggests some implications of this evidence for interpretations of angiosperm–frugivore coevolution. The most important conclusions are: (i) the diversification of angiosperm seed size and fleshy fruits commenced around 80 million years ago (Mya). The diversity of seed sizes, fruit sizes and fruit types peaked in the Eocene around 55 to 50 Mya. During this first phase of the interaction, angiosperms and animals evolving frugivory expanded into niche space not previously utilized by these groups, as frugivores and previously not existing fruit traits appeared. From the Eocene until the present, angiosperm–frugivore interactions have occurred within a broad frame of existing niche space, as defined by fruit traits and frugivory, motivating a separation of the angiosperm–frugivore interactions into two phases, before and after the peak in the early Eocene. (ii) The extinct multituberculates were probably the most important frugivores during the early radiation phase of angiosperm seeds and fleshy fruits. Primates and rodents are likely to have been important in the latter part of this first phase. (iii) Flying frugivores, birds and bats, evolved during the second phase, mainly during the Oligocene and Miocene, thus exploiting an existing diversity of fleshy fruits. (iv) A drastic climate shift around the Eocene–Oligocene boundary (around 34 Mya) resulted in more semi‐open woodland vegetation, creating patchily occurring food resources for frugivores. This promoted evolution of a ‘flying frugivore niche’ exploited by birds and bats. In particular, passerines became a dominant frugivore group worldwide. (v) Fleshy fruits evolved at numerous occasions in many angiosperm families, and many of the originations of fleshy fruits occurred well after the peak in the early Eocene. (vi) During periods associated with environmental change altering coevolutionary networks and opening of niche space, reciprocal coevolution may result in strong directional selection formative for both fruit and frugivore evolution. Further evidence is needed to test this hypothesis. Based on the abundance of plant lineages with various forms of fleshy fruits, and the diversity of frugivores, it is suggested that periods of rapid coevolution in angiosperms and frugivores occurred numerous times during the 80 million years of angiosperm–frugivore evolution.     

Frugivory and seed dispersal by foxes in relation to mammalian prey abundance in a semiarid thornscrub

Abstract We examine the role of the native fox, Pseudalopex culpaeus, as a frugivore and seed disperser in a semiarid thornscrub of Chile. We quantified the fruit and animal components in its diet versus the availability of fruits and small mammals in the field over a 2‐year period (January 1998 through February 2000). We tested the legitimacy and effectiveness of foxes as dispersers by quantifying the percentages of seed viability and of germination of seeds that passed through fox gut versus those picked from plants. We also studied their efficiency as dispersers, monitoring the fate of seeds in faeces placed in the field. The highest frequencies of fruit consumption by foxes were observed when abundances of small mammal prey were <6 individuals per hectare, regardless of fruit abundance in the field. Thus, foxes consumed fruits as a supplementary food resource. Based on 326 faeces, the total number of fruits consumed was about 34 000 over the 2‐year study period, and fruits from the alien shrub Schinus molle represented 98% of that total, with the native Porlieria chilensis a distant second. Germination and viability of defecated seeds of P. chilensis were reduced by 66% and 48%, respectively, in comparison to controls. In contrast, germination of seeds of S. molle increased by 50% and no effect on viability was observed. With regard to P. chilensis, foxes were legitimate (they defecated viable seeds), but ineffective (seeds in faeces had lower germination than those taken directly from parental plants and there was no seedling establishment in the field) and inefficient dispersers (seeds in faeces were deposited on microhabitats hostile to seed germination and seedling establishment). However, with regard to S. molle, foxes were legitimate, effective (seeds in faeces had higher germination than those taken directly from parental plants; there was germination but no establishment in the field), and efficient dispersers (over 41% of seeds were deposited on safe microsites). Thus, a native fox may be contributing to the spread of an alien shrub, co‐opting existing community processes.