Macaques as Seed Dispersal Agents in Asian Forests: A Review

The role of primates in seed dispersal is well recognized. Macaques (Macaca spp.) are major primate seed dispersers in Asia, and recent studies have revealed their role as seed dispersal agents in this region. Here, we review present knowledge of the traits that define the role of macaques as seed dispersers. The size of seeds in fruit influences whether macaques swallow (0.5–17.1 mm; median: 3.0), spit (1–37 mm; median: 7.6), or drop (8.2–57.7 mm; median: 20.5) them. Dispersal distances via defecation are several hundreds of meters (median: 259 m, range: 0–1300 m), shorter than those achieved by some mammals and birds in tropical and temperate regions. However, macaques disperse seeds by defecation at comparable distances to omnivorous carnivores, and further than passerines. Seed dispersal distance by spitting is much shorter (median: 20 m, range: 0–405 m) than by defecation. Among Asian primates, seed dispersal distances resulting from macaque defecation are shorter than those for gibbons and longer than those for langurs. The effects of seed ingestion on the percentage and speed of germination vary among both plant and macaque species. The degree of frugivory, fruit/seed handling methods, seed dispersal distance, microhabitats of dispersed seeds, and effects of dispersal on seed germination vary seasonally and interannually, and long-term studies of the ecological role of macaques are needed. Researchers have begun to assess the effectiveness of seed dispersal by macaques, secondary dispersal of seeds originally dispersed by macaques, and the effects of provisioning on seed dispersal. Future studies should also test the effects of social factors (such as age and rank), which have received little attention in studies of seed dispersal.     

Reliability of macaques as seed dispersers

Seed dispersal is an ecological process crucial for forest regeneration and recruitment. To date, most studies on frugivore seed dispersal have used the seed dispersal effectiveness framework and have documented seed-handling mechanisms, dispersal distances and the effect of seed handling on germination. In contrast, there has been no exploration of “disperser reliability” which is essential to determine if a frugivore is an effective disperser only in particular regions/years/seasons or across a range of spatio-temporal scales. In this paper, we propose a practical framework to assess the spatial reliability of frugivores as seed dispersers. We suggest that a frugivore genus would be a reliable disperser of certain plant families/genera if: (a) fruits of these plant families/genera are represented in the diets of most of the species of that frugivore, (b) these are consumed by the frugivore genus across different kinds of habitats, and (c) these fruits feature among the yearly staples and preferred fruits in the diets of the frugivore genus. Using this framework, we reviewed frugivory by the genus Macaca across Asia to assess its spatial reliability as seed dispersers. We found that the macaques dispersed the seeds of 11 plant families and five plant genera including at least 82 species across habitats. Differences in fruit consumption/preference between different groups of macaques were driven by variation in plant community composition across habitats. We posit that it is essential to maintain viable populations of macaques across their range and keep human interventions at a minimum to ensure that they continue to reliably disperse the seeds of a broad range of plant species in the Anthropocene. We further suggest that this framework be used for assessing the spatial reliability of other taxonomic groups as seed dispersers.     

Primary seed shadow generated by gibbons in the rain forests of Barito Ulu, central Borneo

Gibbons are one of the main frugivores in the forests of Southeast Asia, and consequently have long been considered to be good seed dispersers. This is the first study in which the primary seed shadow they create by their ranging and foraging activities is evaluated in detail. I studied two gibbon groups over 12 months in lowland dipterocarp forest in central Borneo. The gibbons dispersed up to 81% of the species they consumed and destroyed the seeds of only 12%. Fruit with elongated seeds (up to 20 mm wide) were more likely to be dispersed than round seeds. Considering that the survival rate of seeds in the forest to one year was 8%, the gibbons effectively dispersed 13 seedlings ha(-1) group(-1) year(-1). Their effect on germination was very variable, although most species did eventually germinate. Most seeds were deposited along their major ranging routes and close to or under feeding trees.     

Modeling the Ecological and Phenological Predictors of Fruit Consumption by Gibbons (Hylobates albibarbis)

Understanding the ecological interactions between plant reproductive strategies and frugivore feeding behavior can offer insight into the maintenance of tropical forest biodiversity. We examined the role of plant ecological and phenological characteristics in influencing fruit consumption by the White‐bearded gibbon (Hylobates albibarbis) in Gunung Palung National Park, Indonesian Borneo. Gibbons are widespread across Borneo, highly frugivorous and perform important seed dispersal services. We compare multiple models using information criteria to identify the ecological and phenological predictors that most strongly influence gibbon fruit use of 154 plant genera. The most important predictors of resource use were the overall abundance of a genus and the consistency of fruit availability. Plant genera can maintain constant fruit availability as a result of (1) individual stems fruiting often or (2) stems fruiting out of synchrony with each other (asynchrony). Our results demonstrate that gibbons prefer to feed on plant genera that provide consistent fruit availability due to fruiting asynchrony. Because gibbons feed more often on genera that fruit asynchronously, gibbons are more likely to disperse seeds of plant genera with this reproductive strategy. Research on other frugivorous species is needed to determine whether the results for gibbons are generalizable more broadly. Finally, these results suggest that asynchronously fruiting plant genera may be particularly important for habitat restoration in tropical forests designed for frugivore conservation.     

Frugivory and Seed Dispersal by Northern Pigtailed Macaques (Macaca leonina), in Thailand

Tropical rain forest conservation requires a good understanding of plant–animal interactions. Seed dispersal provides a means for plant seeds to escape competition and density-dependent seed predators and pathogens and to colonize new habitats. This makes the role and effectiveness of frugivorous species in the seed dispersal process an important topic. Northern pigtailed macaques (Macaca leonina) may be effective seed dispersers because they have a diverse diet and process seeds in several ways (swallowing, spitting out, or dropping them). To investigate the seed dispersal effectiveness of a habituated group of pigtailed macaques in Khao Yai National Park, Thailand, we examined seed dispersal quantity (number of fruit species eaten, proportion in the diet, number of feces containing seeds, and number of seeds processed) and quality (processing methods used, seed viability and germination success, habitat type and distance from parent tree for the deposited seeds, and dispersal patterns) via focal and scan sampling, seed collection, and germination tests. We found thousands of seeds per feces, including seeds up to 58 mm in length and from 88 fruit species. Importantly, the macaques dispersed seeds from primary to secondary forests, via swallowing, spitting, and dropping. Of 21 species, the effect of swallowing and spitting was positive for two species (i.e., processed seeds had a higher % germination and % viability than control seeds), neutral for 13 species (no difference in % germination or viability), and negative (processed seeds had lower % germination and viability) for five species. For the final species, the effect was neutral for spat-out seeds but negative for swallowed seeds. We conclude that macaques are effective seed dispersers in both quantitative and qualitative terms and that they are of potential importance for tropical rain forest regeneration.     

Interactions between lar gibbons and pig-tailed macaques at fruit sources

Interactions are reported between white-handed gibbons (Hylobates lar) and pig-tailed macaques (Macaca nemestrina) in Khao Yai National Park, Thailand, in which gibbons selected ripe fruit from sources before macaques arrived on 4 occasions during June and July of 1989. The macaques foraged near gibbons or from shared fruit sources during 13% of gibbon observation time. Gibbons made their presence known in fruit trees when macaques approached on 3 occasions and macaques did not enter fruit trees occupied by gibbons. An aggressive interaction is reported in which a single white-handed gibbon vigorously excluded 22–28 macaques from a rare and valuable fruit tree (Sandoricum koetjape). The observations suggest that exploitative and interference competition may exist between these species.     

Seed dispersal effectiveness increases with body size in New Zealand alpine scree weta (Deinacrida connectens)

Weta are giant, flightless orthopterans that are endemic to New Zealand. Although they are known to consume fleshy fruits and disperse seeds after gut passage, which is unusual among insects, their effectiveness as seed dispersal mutualists is debated. We conducted a series of laboratory experiments on alpine scree weta (Deinacrida connectens) and mountain snowberries (Gaultheria depressa) to investigate how fruit consumption rates, the proportion of ingested seeds dispersed intact and weta movement patterns vary with weta body sizes. On average weta dispersed 252 snowberry seeds nightly and travelled at a rate of 4 m min^?1. However, seed dispersal effectiveness varied over three orders of magnitude and was strongly associated with body sizes. Smaller weta consumed few snowberry seeds and acted primarily as seed predators. On the other hand, the largest weta consumed and dispersed thousands of seeds each night and appear to be capable of transporting seeds over large distances. Overall results indicate that scree weta shift from being weakly interacting seed predators to strongly interacting, effective seed dispersers as they increase in size.     

Implications of Behavior and Gut Passage for Seed Dispersal Quality: The Case of Black and Gold Howler Monkeys

The most generalized mechanism of seed dispersal in tropical and subtropical forests is dispersal by vertebrates. The pattern of seed dispersal and germination capacity of dispersed seeds can determine the seed disperser quality because both affect the postdispersal fate of dispersed seeds. Animals' behavior is an important determinant of seed deposition pattern. One of most abundant frugivores of Neotropical forests are howler monkeys Alouatta spp., so my aim was to evaluate the potential quality of Alouatta caraya as a seed disperser, obtaining details of: (1) seed deposition pattern, (2) behavioral context of defecations, and (3) germination capacity of dispersed seeds. During 2 years the seed shadow created by howlers and the behavioral context of depositions was examined in the Paraná flooded forest, and germination tests were conducted in the laboratory. Black and gold howler monkeys consumed fruits of five canopy trees, three understory trees, one shrub, and two vines. Howlers dispersed seeds in a complex pattern: 35 percent (337 scats) of scats were deposited individually, and 65 percent were deposited in big latrines associated with the main sleeping trees and in small latrines associated with secondary sleeping trees and confrontations at territory edges. From 261 dispersal distances recorded, 20 and 40 m were the mode, but 57 percent of distances were >50 m and 31 percent were >100 m. Germination speed increased significantly in ingested seeds of Banara arguta, Ocotea diospyrifolia and Eugenia punicifolia . The seed deposition pattern generated by A. caraya may produce a diversification of environmental conditions for dispersed seeds that should be considered in future evaluations.     

Coevolution of mistletoes and frugivorous birds?*

Small frugivorous birds that feed largely on the fruits of stem-parasitic mistletoes have independently evolved in various parts of the world. Local populations of mistletoes may be dispersed almost exclusively by these birds. Four attributes of mistletoe dispersal systems may have enhanced the evolution of reciprocal dependence between mistletoes and specialized dispersers: (1) Safe sites for mistletoe seeds (i.e. the young branches of a compatible host) are precisely defined in space and time. (2) The viscidity of mistletoe seeds induces smaller dispersers to deposit seeds in safe sites. (3) Frugivores differ markedly in the efficiency with which they disperse mistletoe seeds to safe sites. (4) Relatively large viscid fruits and adaptive fruiting displays exclude or deter most members of the potential disperser guild. Some birds have anatomical adaptations as a result of dietary specialization on mistletoe fruit, and some mistletoes have fruiting displays that target specialized birds or a narrow disperser spectrum. Coevolution between guilds of mistletoes and specialized dispersers is therefore probable. The uncoupled selective pressures that might have driven their coevolution are the mistletoes’ provision of fruit crops that are unavailable to more generalized frugivores, in return for seed dispersal to the small stems most suitable for infection. As in other mutualistic seed dispersal systems, phylogenetic, ecological and life history factors constrain the evolution of monophyletic interdependence, resulting in varying degrees and patterns of reciprocal specificity between mistletoes and dispersers.     

Evolutionary ecology of climacteric and non-climacteric fruits

Fleshy fruits can be divided between climacteric (CL, showing a typical rise in respiration and ethylene production with ripening after harvest) and non-climacteric (NC, showing no rise). However, despite the importance of the CL/NC traits in horticulture and the fruit industry, the evolutionary significance of the distinction remains untested. In this study, we tested the hypothesis that NC fruits, which ripen only on the plant, are adapted to tree dispersers (feeding in the tree), and CL fruits, which ripen after falling from the plant, are adapted to ground dispersers. A literature review of 276 reports of 80 edible fruits found a strong correlation between CL/NC traits and the type of seed disperser: fruits dispersed by tree dispersers are more likely to be NC, and those dispersed by ground dispersers are more likely to be CL. NC fruits are more likely to have red–black skin and smaller seeds (preferred by birds), and CL fruits to have green–brownish skin and larger seeds (preferred by large mammals). These results suggest that the CL/NC traits have an important but overlooked seed dispersal function, and CL fruits may have an adaptive advantage in reducing ineffective frugivory by tree dispersers by falling before ripening.     

Asymmetrical Dependence Between a Neotropical Mistletoe and its Avian Seed Disperser

The degree of interdependence among interacting species has major implications for our understanding of the coevolutionary process and biodiversity maintenance. However, the mutualism strength among fruiting plants and their seed dispersers remains poorly understood in tropical ecosystems. We evaluated simultaneously the effectiveness of the avian seed dispersers of the mistletoe Struthanthus flexicaulis (Loranthaceae) and the contribution of its fruits to their diets in a highland rocky savanna in southeastern Brazil. The mistletoe fruits are small lipid‐rich pseudoberries available throughout the year. Four passerine birds fed on fruits, but Elaenia cristata (Tyrannidae) was the most effective disperser, responsible for more than 96 percent of the dispersed seeds. This bird swallowed fruits whole, expelling and depositing undamaged seeds by regurgitation and bill wiping on perches. From 646 dispersed seeds, 56 percent were deposited on safe sites, thin live twigs of 38 susceptible host species. Elaenia cristata were predominantly frugivorous, feeding on typically ornithocoric fruits of at least 12 species, but also on arthropods. Although fruits represented 75 percent of the feeding bouts along the year, S. flexicaulis fruits represented only 34 percent of the E. cristata diet. Our results highlight the asymmetrical nature of this mutualistic interaction, with the mistletoe life cycle locally linked to one highly effective seed disperser that is more weakly dependent on mistletoes fruits as a food source. We suggest that merging the seed dispersal effectiveness framework with diet assessment of seed dispersers is needed to clarify the asymmetries in mutualistic pairwise interactions involving plants and their animal partners.     

Primates,Provisioning and Plants: Impacts of Human Cultural Behaviours on Primate Ecological Functions

Human provisioning of wildlife with food is a widespread global practice that occurs in multiple socio-cultural circumstances. Provisioning may indirectly alter ecosystem functioning through changes in the eco-ethology of animals, but few studies have quantified this aspect. Provisioning of primates by humans is known to impact their activity budgets, diets and ranging patterns. Primates are also keystone species in tropical forests through their role as seed dispersers; yet there is no information on how provisioning might affect primate ecological functions. The rhesus macaque is a major human-commensal species but is also an important seed disperser in the wild. In this study, we investigated the potential impacts of provisioning on the role of rhesus macaques as seed dispersers in the Buxa Tiger Reserve, India. We studied a troop of macaques which were provisioned for a part of the year and were dependent on natural resources for the rest. We observed feeding behaviour, seed handling techniques and ranging patterns of the macaques and monitored availability of wild fruits. Irrespective of fruit availability, frugivory and seed dispersal activities decreased when the macaques were provisioned. Provisioned macaques also had shortened daily ranges implying shorter dispersal distances. Finally, during provisioning periods, seeds were deposited on tarmac roads that were unconducive for germination. Provisioning promotes human-primate conflict, as commensal primates are often involved in aggressive encounters with humans over resources, leading to negative consequences for both parties involved. Preventing or curbing provisioning is not an easy task as feeding wild animals is a socio-cultural tradition across much of South and South-East Asia, including India. We recommend the initiation of literacy programmes that educate lay citizens about the ill-effects of provisioning and strongly caution them against the practice.     

Standard yet unusual mechanisms of long-distance dispersal: seed dispersal of Corymbia torelliana by bees

Mellitochory, seed dispersal by bees, has been implicated in long-distance dispersal of the tropical rain forest tree, Corymbia torelliana (Myrtaceae). We examined natural and introduced populations of C. torelliana for 4 years to determine the species of bees that disperse seeds, and the extent and distance of seed dispersal. The mechanism of seed dispersal by bees was also investigated, including fruit traits that promote dispersal, foraging behaviour of bees at fruits, and the fate of seeds. The fruit structure of C. torelliana , with seed presented in a resin reward, is a unique trait that promotes seed dispersal by bees and often results in long-distance dispersal. We discovered that a guild of four species of stingless bees, Trigona carbonaria, T. clypearis, T. sapiens , and T. hockingsi, dispersed seeds of C. torelliana in its natural range. More than half of the nests found within 250 m of fruiting trees had evidence of seed transport. Seeds were transported minimum distances of 20–220 m by bees. Approximately 88% of seeds were dispersed by gravity but almost all fruits retained one or two seeds embedded in resin for bee dispersal. Bee foraging for resin peaked immediately after fruit opening and corresponded to a peak of seed dispersal at the hive. There were strong correlations between numbers of seeds brought in and taken out of each hive by bees ( r =  0.753–0.992, P  < 0.05), and germination rates were 95 ± 5%. These results showed that bee-transported seeds were effectively dispersed outside of the hive soon after release from fruits. Seed dispersal by bees is a non-standard dispersal mechanism for C. torelliana, as most seeds are dispersed by gravity before bees can enter fruits. However, many C. torelliana seeds are dispersed by bees, since seeds are retained in almost all fruits, and all of these are dispersed by bees.     

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.     

The yellow-cheeked gibbon (Hylobates gabriellae) in nam bai cat tien (southern vietnam) revisited

Data concerning the status, habitat, and vocalizations of yellow-cheeked crested gibbons (Hylobates gabriellae) were collected during a short field trip to the Nam Bai Cat Tien National Park (southern Vietnam). Nam Bai Cat Tien may be the southernmost locality where crested gibbons (i.e. theHylobates concolor group) still survive. Fewer songs were heard at Nam Bai Cat Tien National Park than at other crested gibbon sites visited by the author. At least two gibbon groups appear to have been greatly reduced in number since previous surveys in the park. There is some evidence that both the gibbon population and the gibbon habitat in Nam Bai Cat Tien are disturbed. The first case of a great call solo song in wild gibbons of theconcolor group is reported. Great calls ofH. gabriellae are described and documented with sonagrams for the first time. They differ from those previously described forH. leucogenys.     

Mammalian seed dispersal in Cantabrian woodland pastures: Network structure and response to forest loss

We evaluated the role of wild large mammals as dispersers of fleshy-fruited woody plants in woodland pastures of the Cantabrian range (N Spain). By searching for seeds in mammal scats across four localities, we addressed how extensive seed dispersal was in relation to the fleshy-fruited plant community, and applied a network approach to identify the relative role of mammal species in the seed dispersal process. We also tested the response of mammalian dispersers to forest availability at increasing spatial scales. Five carnivores and three ungulates dispersed seeds of eight fleshy-fruited trees and shrubs. Mammalian seed dispersal did not mirror community-wide fruit availability, as abundant fruiting trees were scarce whereas thorny shrubs were over-represented among dispersed species. The dispersal network was dominated by bramble (Rubus ulmifolius/fruticosus), the remaining plants being rarer and showing more restricted disperser coteries. Fox (Vulpes vulpes), badger (Meles meles), and wild boar (Sus scrofa) dispersed mostly bramble, whereas martens (Martes sp.) dispersed mostly wild rose (Rosa sp.). Ungulates occasionally dispersed holly (Ilex aquifolium) and hawthorn (Crataegus monogyna). The empirical network reflected a skewed distribution of interactions and some functional complementarity (as judged from the low levels of connectance and nestedness), but also some degree of specialization. Mammals overused uncovered microsites for seed deposition, and increased their disperser activity in those landscape sectors devoid of forest. Combined with previous findings on avian seed dispersal, this study suggest a strong functional complementarity coming from the low overlap in the main plant types that mammals and birds disperse – thorny shrubs and trees, respectively – and the differential patterns of seed deposition, with mammals mostly dispersing into deforested areas, and birds into forest-rich landscapes.     

WIND DISPERSAL OF FRUITS WITH VARIABLE SEED NUMBER IN A TROPICAL TREE (LONCHOCARPUS PENTAPHYLLUS: LEGUMINOSAE)

The tropical tree, Lonchocarpus pentaphyllus (Poir.) DC. (Leguminosae-Papilionoideae), matures indehiscent wind-dispersed fruits containing 0–4 seeds. Most fruits are one-seeded (82%) while less than 2% are three-seeded. An increase in seed number per fruit correlates with increases in four characteristics expected to affect dispersal distance under field conditions: fruit weight, fruit area, square root of wing-loading, and rate of descent in still air. The dry weight of a seed decreases with an increase in seed number per fruit. Under field conditions nearly 40% of the mature fruits fall within the radius of the tree crown. Fruits with more intact seeds are dispersed shorter distances; fruits with no developed seeds travel the farthest. Among one-seeded fruits dispersed beyond the crown radius, dispersal distance is inversely proportional to the square root of wing-loading. The weight of seed in these one-seeded fruits, however, is independent of dispersal distance. Fruits with more seeds have a higher proportion of underdeveloped seeds. However, a greater proportion of two- and three-seeded fruits have at least one intact mature seed than do one-seeded fruits. This comparative study illustrates that changes in fruit morphology and weight associated with different numbers of seeds per fruit affect dispersal properties as well. A decrease in seed number per fruit increases both seed weight and dispersal distance, but it decreases the probability that a given dispersal event results in movement of an intact seed.     

Frugivory by the fish Brycon hilarii (Characidae) in western Brazil

Frugivory and seed dispersal have been poorly studied in Neotropical freshwater fishes. We studied frugivory and seed dispersal by the piraputanga fish (Brycon hilarii, Characidae) in the Formoso River, Bonito, western Brazil. We examined the stomach contents of 87 fish and found the diet of piraputanga consisted of 24% animal prey (arthropods, snails, and vertebrates), 31% seeds/fruits and 45% other plant material (algae/macrophytes/leaves/flowers). The piraputangas fed on 12 fruit species, and were considered as seed dispersers of eight species. Fruits with soft seeds larger than 10 mm were triturated, but all species with small seeds (e.g. Ficus, Psidium) and one species with large hard seed (Chrysophyllum gonocarpum) were dispersed. Piraputangas eat more fruits in the dry season just before the migration, but not during the spawning season. Fish length had a positive relation with the presence of fruits in their guts. The gallery forest of the Formoso River apparently does not have any plant species that depend exclusively on B. hilarii for seed dispersal because all fruit species are also dispersed by birds and mammals. Based on seed size and husk hardness of the riparian plant community of Formoso River, however, the piraputangas may potentially disperse at least 50% of the riparian fleshy fruit species and may be particularly important for long-distance dispersal. Therefore, overfishing or other anthropogenic disturbances to the populations of piraputanga may have negative consequences for the riparian forests in this region.     

Tree dispersal strategies in the littoral forest of Sainte Luce (SE-Madagascar)

Zoochory is the most common mode of seed dispersal for the majority of plant species in the tropics. Based on the assumption of tight plant-animal interactions several hypotheses have been developed to investigate the origin of life history traits of plant diaspores and their dispersers, such as species-specific co-evolution, the low/high investment model (low investment in single fruits but massive fruiting to attract many different frugivores versus high investment in single fruits and fruit production for extended periods to provide food for few frugivores), and the evolution of syndromes which represent plant adaptations to disperser groups (e.g. birds, mammals, mixed). To test these hypotheses the dispersal strategies of 34 tree species were determined in the littoral forest of Sainte Luce (SE-Madagascar) with the help of fruit traps and tree watches. The impact of fruit consumers on the seeds was determined based on detailed behavioral observations. Phenological, morphological and biochemical fruit traits from tree species were measured to look for co-variation with different types of dispersal. No indication for species-specific co-evolution could be found nor any support for the low/high investment model. However dispersal syndromes could be distinguished as diaspores dispersed by birds, mammals or both groups (mixed) differ in the size of their fruits and seeds, fruit shape, and seed number, but not in biochemical traits. Five large-seeded tree species seem to depend critically on the largest lemur, Eulemur fulvus collaris, for seed dispersal. However, this does not represent a case of tight species-specific co-evolution. Rather it seems to be the consequence of the extinction of the larger frugivorous birds and lemurs which might also have fed on these large fruits. Nevertheless these interactions are of crucial importance to conserve the integrity of the forest.     

Seed dispersal anachronisms: rethinking the fruits extinct megafauna ate

Background

Some neotropical, fleshy-fruited plants have fruits structurally similar to paleotropical fruits dispersed by megafauna (mammals >10³ kg), yet these dispersers were extinct in South America 10–15 Kyr BP. Anachronic dispersal systems are best explained by interactions with extinct animals and show impaired dispersal resulting in altered seed dispersal dynamics.

Methodology/Principal Findings

We introduce an operational definition of megafaunal fruits and perform a comparative analysis of 103 Neotropical fruit species fitting this dispersal mode. We define two megafaunal fruit types based on previous analyses of elephant fruits: fruits 4–10 cm in diameter with up to five large seeds, and fruits >10 cm diameter with numerous small seeds. Megafaunal fruits are well represented in unrelated families such as Sapotaceae, Fabaceae, Solanaceae, Apocynaceae, Malvaceae, Caryocaraceae, and Arecaceae and combine an overbuilt design (large fruit mass and size) with either a single or few (<3 seeds) extremely large seeds or many small seeds (usually >100 seeds). Within-family and within-genus contrasts between megafaunal and non-megafaunal groups of species indicate a marked difference in fruit diameter and fruit mass but less so for individual seed mass, with a significant trend for megafaunal fruits to have larger seeds and seediness.

Conclusions/Significance

Megafaunal fruits allow plants to circumvent the trade-off between seed size and dispersal by relying on frugivores able to disperse enormous seed loads over long-distances. Present-day seed dispersal by scatter-hoarding rodents, introduced livestock, runoff, flooding, gravity, and human-mediated dispersal allowed survival of megafauna-dependent fruit species after extinction of the major seed dispersers. Megafauna extinction had several potential consequences, such as a scale shift reducing the seed dispersal distances, increasingly clumped spatial patterns, reduced geographic ranges and limited genetic variation and increased among-population structuring. These effects could be extended to other plant species dispersed by large vertebrates in present-day, defaunated communities.