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.     

Effects of Seed Dispersal by Three Ateline Monkey Species on Seed Germination at Tinigua National Park, Colombia

We examined the effect of seed ingestion by three ateline primates: woolly monkeys, Lagothrix lagothricha; spider monkeys, Ateles belzebuth; and, red howler, Alouatta seniculus on germination rates and latency periods of seeds of several plant species in Tinigua National Park, Colombia. We collected dispersed seeds from feces and control seeds from the parental trees and washed them for germination trials. For the majority of plants, dispersed seeds germinated as well or better than control seeds did. Although spider monkeys depend more heavily on fruits than the other monkey species do, they were not more efficient than howlers or woolly monkeys at improving germination rates. A considerable proportion of the seeds dispersed by howlers and woolly monkeys showed reduced latency periods to germination, but spider monkeys showed less effect on reducing germination time. This result may be related to longer gut retention times, but such a trend has not been observed in other primate species. We conclude that, like many other primates, ateline monkeys are effective seed dispersers in terms of their effects on the seeds they swallow because they rarely decrease their germination rates. We discuss problems that make interspecific comparisons difficult, such as inappropriate control seeds and differences associated with germination substrates, and we stress the importance of studying other components of seed dispersal effectiveness.     

Post‐Dispersal Seed Removal and Germination Selected Tree Species Dispersed by Cebus capucinus on Barro Colorado Island,Panama1

Dispersal quality, an important component of seed disperser effectiveness, may strongly affect the rate of plant recruitment. Here we evaluated the quality of Cebus monkey dispersal by comparing the secondary removal fate and germination of fresh and Cebus‐ingested seeds of nine tree species on Barro Colorado Island, Panama. Overall, rates of secondary seed removal by vertebrates were low, with most Cebus defecations remaining undisturbed for extended periods on the forest floor. Only four of 30 feces were completely buried by dung beetles, and we found significantly higher vertebrate removal of defecated seeds than control seeds for only one species, Cordia bicolor. Seed germination varied greatly between plant taxa. Seeds of 3 out of 9 species showed significantly higher percent germination after monkey gut passage than control fresh seeds. Germination times tended to be shorter for defecated than for control seeds but were significantly different only for one of nine species, Cecropia insignis. Low rates of seed removal from Cebus feces, coupled with high germination probabilities, suggest high dispersal effectiveness for Cebus and contrasts strongly with patterns of post‐dispersal seed fate recorded for other primate species.     

Seed dispersal by pygmy chimpanzees (Pan paniscus): A preliminary report

The role in seed dispersal played by the pygmy chimpanzees (Pan paniscus) inhabiting Wamba, Republic of Zaïre, was studied. Germination was tested for seeds of 17 plant species recovered from the feces of pygmy chimpanzees at Wamba. The fecal seeds of 13 species germinated, and in six of the species the germination rate for the fecal seeds was higher than that of control seeds. Although five other species showed a higher germination rate in the control seeds than in the fecal seeds, the remaining two species revealed no difference in germination rate between the fecal and control seeds. There was no great difference in germination velocity between the fecal and control seeds of the same species. For comparison, seeds of four plant species collected from the feces of common chimpanzees (Pan troglodytes) and gibbons (Hylobates lar) in captivity in Okinawa were tested for their germinability. In this test, although the seeds had passed through the digestive tract, their germinability demonstrated little change. Based on the behavioral characteristics of the pygmy chimpanzee at Wamba and observations of the captive primates on Okinawa, it seems that pygmy chimpanzees may play an important role in the seed dispersal of fruit plant species at Wamba.     

Effectiveness of Spider Monkeys (<Emphasis Type="Italic">Ateles geoffroyi vellerosus</Emphasis>) as Seed Dispersers in Continuous and Fragmented Rain Forests in Southern Mexico

Seed dispersal is considered a key process determining spatial structure and dynamics of plant populations, and has crucial implications for forest regeneration. We evaluated the effectiveness of spider monkeys (Ateles geoffroyi) as seed dispersers in continuous and fragmented habitats to test if this interaction is altered in forest fragments. We documented fruit and seed handling, defecation patterns, diversity and composition of seeds in feces, and seed germination of defecated and control seeds in the Lacandona rainforest, Mexico. For most species contributing to 80% of total fruit feeding time, monkeys swallowed and spat seeds, but swallowing was the most frequent seed handling category in continuous and fragmented forests. However, the proportion of feeding records of swallowed seeds was higher in continuous forest (0.59) than in fragments (0.46), whereas the opposite was true for proportion of dropped seeds (0.16 vs. 0.31). This pattern was reflected in the number of fecal samples containing seeds, which was greater in continuous (95.5%) than in fragmented forests (82.5%). Seeds in fecal samples included a total of 71 species from 23 plant families. The numbers of defecated seed species were similar between forest conditions, and in both cases most seeds (>86%) were undamaged. Defecated seeds showed greater germination percentages than control seeds in all of the five species evaluated. Although we identified some differences in seed handling and the percentage of feces with seeds between continuous forest and fragments, our results indicate that, in general terms, spider monkeys are effective seed dispersers in both forest conditions.     

Seed dispersal potential of Asian elephants

Elephants, the largest terrestrial mega-herbivores, play an important ecological role in maintaining forest ecosystem diversity. While several plant species strongly rely on African elephants (Loxodonta africana; L. cyclotis) as seed dispersers, little is known about the dispersal potential of Asian elephants (Elephas maximus). We examined the effects of elephant fruit consumption on potential seed dispersal using the example of a tree species with mega-faunal characteristics, Dillenia indica L., in Thailand. We conducted feeding trials with Asian elephants to quantify seed survival and gut passage times (GPT). In total, 1200 ingested and non-ingested control seeds were planted in soil and in elephant dung to quantify differences in germination rates in terms of GPT and dung treatment. We used survival analysis as a novel approach to account for the right-censored nature of the data obtained from germination experiments. The average seed survival rate was 79% and the mean GPT was 35 h. The minimum and maximum GPT were 20 h and 72 h, respectively. Ingested seeds were significantly more likely to germinate and to do so earlier than non-ingested control seeds (P = 0.0002). Seeds with the longest GPT displayed the highest germination success over time. Unexpectedly, seeds planted with dung had longer germination times than those planted without. We conclude that D. indica does not solely depend on but benefits from dispersal by elephants. The declining numbers of these mega-faunal seed dispersers might, therefore, have long-term negative consequences for the recruitment and dispersal dynamics of populations of certain tree species.     

The role of avian frugivores in germination of seeds of fleshy-fruited invasive alien plants

Many highly invasive plant species have fleshy fruits which are eaten by native frugivorous animals. These frugivores play an important role in long-distance seed dispersal, and may also affect germination success. The aim of this study was to determine whether generalist frugivores enhance or decrease seed germination of invasive alien species through pulp removal or seed coat abrasion, besides serving as dispersal agents. Fruits of four fleshy-fruited invasive alien plant species, namely Solanum mauritianum, Cinnamomum camphora, Lantana camara and Psidium guajava, were fed to three generalist avian frugivorous species, which have been observed feeding on these fruits in the wild. Seed retention time was recorded as this affects dispersal distance and the duration that seeds are exposed to the effects of the gut. Seeds removed from excreta, seeds from manually de-pulped fruit, and whole fruit were planted in soil trays housed in a greenhouse. Daily germination counts were done. Seed retention times differed significantly between bird species for all fruits, except those of C. camphora. However, all frugivores had a similar effect on the germination success of seeds of S. mauritianum, L. camara and P. guajava, showing that gut retention time was not important. Germination of seeds from manually de-pulped fruits did not differ from that of ingested seeds of all plant species, suggesting that seed coat abrasion was also not important. Pulp removal resulted in significantly higher germination rates, both in the two species with larger, multi-seeded fruit (S. mauritianum and P. guajava), and in the two species having single-seeded fruit with waxy exocarps (C. camphora and L. camara). Pulp removal also resulted in significantly earlier germination of L. camara and P. guajava seeds. Therefore, frugivores not only accelerate dispersal, but also greatly enhance seed germination of all fleshy-fruited invasive alien species in this study.     

Does seed ingestion by bats enhance germination? A new meta‐analysis 15 years later

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Seed dispersal and predation by Yakushima macaques, Macaca fuscata yakui, in a warm temperate forest of Yakushima Island, southern Japan

The relationships between fruit morphology and the foraging behavior of the Yakushima macaque, Macaca fuscata yakui were studied during a 9-month field study and series of laboratory experiments on Yakushima Island, southern Japan. These relationships may affect seed germination traits through seed dispersal. The macaques foraging behavior was observed in order to obtain data concerning the treatment of pulp and seeds. Seeds in feces and spat seeds were collected and analyzed. A linear discriminant analysis of the data led to the following results: (i) an increase in the relative flesh volume of a fruit was one of the potential factors which increased the probability of seed dispersal by the macaques; and (ii) seed size was an important parameter in relation to the type of seed dispersal (by defecation or spitting out). The germination test was conducted in a laboratory, then the germination rates and delays of dispersed seeds were compared with those of seeds collected directly from trees. The germination of dispersed seeds of Ficus thunbergii, Eurya japonica, and Vaccinium bracteatum, was significantly enhanced by passage through the macaques gut. The enhanced germination behavior was not seen in larger seeds, such as those of Psychotria serpens, Myrsine seguinii, Diospyros morrisiana, and Neolitsea sericea. The germination enhancement in small-seeded plants could be due to a sorting effect from the passage through the gut, which selects seeds with a narrower range of germination traits.     

The effect of frugivory on postdispersal seed removal and germination in the pantropical forest tree Antiaris toxicaria Leschenault

The quality of seed treatment by frugivores has an effect on seed removal after dispersal, seed germination and tree recruitment. We provide information on postdispersal seed removal, germination and subsequent recruitment in tropical forest tree species Antiaris toxicaria in Ghana. We tested whether postdispersal seed removal and germination rates were differentially affected by the following seed treatments: seeds that were spat out by monkeys with all fruit pulp removed and spitting seeds with fruit pulp partially removed as observed in some birds and bats. We used seeds of intact ripened fruits as control. Frugivore seed treatment and distance from bole affected seed removal patterns, whereas intact seeds were significantly removed from all seed stations. The germination success was greater for seeds that were spat out by monkeys and poor for seeds with fruit pulp partially removed and intact fruits. More recruits were recorded at the edge of the adult A. toxicaria canopy radius. There was weak relationship (r² = 0.042) between the number of recruits and distance away from the adult tree. Results suggest that the subsequent recruitment in tropical forest tree species may be enhanced by some frugivore fruit‐handling behaviour where fruit pulp is removed from the seeds without destroying the seeds.     

Neglected seed dispersers: endozoochory by Javan lutungs (Trachypithecus auratus) in Indonesia

Leaf monkeys are known to be leaf eaters, and thus, their potential role as seed dispersers has been neglected. However, they do also feed on fruits. To examine the role of leaf monkeys as endozoochorous seed dispersers, we studied the Javan lutung (Trachypithecus auratus) in Indonesia. We compared multiple aspects of seed dispersal processes (amount and diversity of seeds ingested, dispersal distance, and germination rate) of lutungs with that of the sympatric long‐tailed macaque (Macaca fascicularis). Over the study period, 54 percent of the lutung feces contained intact seeds, which was equivalent to the macaque feces contained seeds (62%). Seeds of at least six plant species were detected in the lutung feces, which was less than those found in the macaque feces (>19 plant species). The main species of seeds defecated by both lutungs and macaques was Ficus spp. (seed size: 0.7 mm). Seed shadow, estimated from travel distance (range: 1–299 m) and gut passage rate (24–96 h), had a unimodal‐distribution with a peak at 51–100 m, and was shorter than that reported in published accounts of macaques and other similar and smaller sized frugivores. Finally, germination rates of Ficus spp. seeds ingested by both lutungs and macaques were lower than that of the control seeds. These results imply that the dispersal effectiveness of lutungs would be lower than that of the sympatric primate frugivores. However, at a population level, lutungs could play a significant role as seed dispersers for the small‐seeded species, and therefore, more research into their frugivorous habits is warranted.     

Feeding of the Bat,Sturnira lilium,on Fruits of Solanum riparium Influences Dispersal of this Pioneer Tree in Forests of Northwestern Argentina

The influence of fruit ingestion by the bat, Sturnira lilium, on germination of the seeds of the tree Solanum riparium was studied in a secondary rain forest in northwestern Argentina. Bat frequencies in disturbed areas were analyzed by mist net captures. Germination rates were determined for seeds collected from trees and bat feces. S. lilium was the most abundant fruit bat in the study area. Fruit digestion and the passage of seeds through the intestine did not significantly affect germination in S. riparium. In this case the fruit bats, therefore, probably provide only seed dispersal.     

The role of the brown-eared bulbulHypsypetes amaurotis as a seed dispersal agent

The role of the brown-eared bulbul,Hypsypetes amaurotis, as a dispersal agent for seeds of fruiting plants was studied by field observations for two years, in parallel with laboratory experiments on seed germination. Bulbuls consumed fruits of 53 species from 24 plant families. The fruits of these plants had similar color and size, and these characteristics were likely to enhance the feeding efficiency of the frugivore. Laboratory experiments on 20 food plant species demonstrated that: (1) no seeds were injured by passing through the bulbul's gut; (2) seeds that had passed through the bulbul's gut were still able to germinate and (3) fruit pulp reduced germination ability. When pulp was removed by passing through bulbul's gut, or by hand, germination was improved. An estimate of the home range of six bulbuls suggested that they may transport seeds for at least 300 m.     

Feeding Behavior of Purple‐throated Fruitcrow (Querula purpurata: Cotingidae) in the Colombian Amazon and Its Implications for Seed Dispersal1

We studied some feeding behaviors of the purple‐throated fruitcrow (Querula purpurata) in two Colombian Amazonian forests, which affect the primary seed dispersal of the plants on which it feeds. Visit length, number of fruits removed and dispersed, feeding rates, and fruit‐handling times were compared to those obtained for two other cotingas feeding on the same fruiting trees. Querula purpurata exhibited shorter visits (98 sec) and fruit‐handling times (4 sec), and higher mean feeding rates (1.6 fruits/min) than Phoenicircus nigricollis and Cotinga cayana. In contrast, P. nigricollis dispersed the highest number of seeds of four of the five tree species studied. Although Q. purpurata and P. nigricollis exhibited feeding behaviors that increase seed dispersal, Q. purpurata may be more important in the transport of seeds between habitats, while P. nigricollis may be a major seed disperser within the primary forest.     

Consequences of southern cassowary (Casuarius casuarius,L.) gut passage and deposition pattern on the germination of rainforest seeds

In Australia's tropical rainforests the endangered southern cassowary, Casuarius casuarius, L., is the largest native frugivore and many plant species, because of the size of their fruits or seeds, are thought to be largely dependent on cassowaries for their dispersal. In this study we asked whether the contribution of cassowaries to plant recruitment extends beyond removing seeds from the vicinity of the parent. To do this we conducted germination trials involving 17 rainforest plant species to test whether cassowary consumption and seed deposition pattern alter germination probability or time to germination. Twenty‐four per cent of species showed changed germination probabilities, with one species showing no germination without cassowary consumption, and 35% showed changed time to germination. However these differences did not translate into any significant effects when considered across all species. We examined gut scarification, fruit pulp removal (de‐inhibition) and deposition in faecal material as mechanisms for changing germination success; each contributed to the changed success of individual species. There was a negative effect of seed clumping on five species. We conclude that cassowary consumption can modify germination performance in a minority of rainforest plants and that the effect is generally positive. Although the effect on large seeded species was small it is most likely to be important as the cassowary is the only animal in Australia able to internally process large numbers of these seeds.     

Pre‐dispersal seed predators and fungi differ in their effect on Luehea seemannii capsule development,seed germination,and dormancy across two Panamanian forests

Pre‐dispersal seed predation can greatly reduce crop size affecting recruitment success. In addition, non‐fatal damage by seed predators may allow infection by fungi responsible for post‐dispersal seed losses. The objectives of this study were (1) to quantify pre‐dispersal seed predation and fungal infection in a Neotropical tree species, Luehea seemannii, that produces dehiscent fruits and wind‐dispersed seeds, and (2) to link pre‐dispersal effects on seed quality to seed survival in the soil. To examine how seed predators and fungi influence seed losses, mesh exclosures, fungicide, and the combination of both treatments were applied to separate branches in the canopy of trees in Gamboa and Parque Natural Metropolitano (PNM), Panama. To determine if treatments affect seed viability and survival in the soil, half of the seeds collected from each treatment were buried for 4 weeks in forest soils and subsequently allowed to germinate before and after the breaking of dormancy. Overall, 24 percent of developing fruit were lost to insect attack. In contrast, fungi infected only 3 percent of seeds at the pre‐dispersal stage. For seeds germinated directly after collection, fungicide significantly increased germination in the wetter site (Gamboa) but decreased germination in the drier site (PNM). The pre‐dispersal insect exclosure treatment increased the fraction of seeds that remained dormant after burial in the soil. This result suggests that exposure to insect predators may cause physical damage to seeds that results in the loss of physical dormancy but does not necessarily increase the susceptibility of seeds to pathogen attack in the soil.     

Seed dispersal effectiveness of the western lowland gorilla (Gorilla gorilla gorilla) in Gabon

The quantitative and qualitative aspects of seed dispersal by the western lowland gorilla (Gorilla gorilla gorilla) were investigated in Gabon. Fresh faeces were collected and washed to identify and count the seeds. Seed germinability after gut passage was estimated with trials in a nursery at the study site. To assess the impact of gut passage on germination success and delay, comparative trials were run with four treatments: (i) gut passed seeds cleaned of faeces, (ii) gut passed seeds within a faecal matrix, (iii) seeds from fresh fruits surrounded by pulp, and (iv) seeds from fresh fruits cleaned of pulp. The analysis of 180 faecal units resulted in the identification of 58 species of seed. Germination trials were realized for 55 species and the mean germination success reached 46%. The impact of gut passage was investigated for Santiria trimera and Chrysophyllum lacourtianum; both species displayed higher germination success after ingestion. This study shows that gorillas effectively disperse seeds of numerous plant species, many of which provide timber or nontimber forest products or are typical of Gabonese forests. Considering the high‐quality of gorilla deposition sites, gorillas is thought to play a unique role in the dynamics of Central African forest.     

Introduction of mammalian seed predators and the loss of an endemic flightless bird impair seed dispersal of the New Zealand tree Elaeocarpus dentatus

Understanding the mutualistic services provided by species is critical when considering both the consequences of their loss or the benefits of their reintroduction. Like many other Pacific islands, New Zealand seed dispersal networks have been changed by both significant losses of large frugivorous birds and the introduction of invasive mammals. These changes are particularly concerning when important dispersers remain unidentified. We tested the impact of frugivore declines and invasive seed predators on seed dispersal for an endemic tree, hinau Elaeocarpus dentatus, by comparing seed dispersal and predation rates on the mainland of New Zealand with offshore sanctuary islands with higher bird and lower mammal numbers. We used cameras and seed traps to measure predation and dispersal from the ground and canopy, respectively. We found that canopy fruit handling rates (an index of dispersal quantity) were poor even on island sanctuaries (only 14% of seeds captured below parent trees on islands had passed through a bird), which suggests that hinau may be adapted for ground‐based dispersal by flightless birds. Ground‐based dispersal of hinau was low on the New Zealand mainland compared to sanctuary islands (4% of seeds dispersed on the mainland vs. 76% dispersed on islands), due to low frugivore numbers. A flightless endemic rail (Gallirallus australis) conducted the majority of ground‐based fruit removal on islands. Despite being threatened, this rail is controversial in restoration projects because of its predatory impacts on native fauna. Our study demonstrates the importance of testing which species perform important mutualistic services, rather than simply relying on logical assumptions.     

Gut passage effect of the introduced red‐whiskered bulbul (Pycnonotus jocosus) on germination of invasive plant species in Mauritius

In Mauritius, many of the worst invasive plant species have fleshy fruits and rely on animals for dispersal. The introduced red‐whiskered bulbul (Pycnonotus jocosus) feeds on many fleshy‐fruited species, and often moves from invaded and degraded habitats into higher quality native forests, thus potentially acting as a mediator of continued plant invasion into these areas. Furthermore, gut passage may influence seed germination. To investigate this, we fed fleshy fruits of two invasive plant species, Ligustrum robustum and Clidemia hirta, to red‐whiskered bulbuls. Gut passage times of seeds were recorded. Gut‐passed seeds were sown and their germination rate and germination success compared with that of hand‐cleaned seeds, as well as that of seeds in whole fruits. Gut passage and hand‐cleaning had significant positive effects on germination of both species. Gut‐passed seeds of both C. hirta and L. robustum germinated faster than hand‐cleaned seeds. However, for L. robustum, this was only true when compared with hand‐cleaned seeds with intact endocarp; when compared with hand‐cleaned seeds without endocarp, there was no difference. For overall germination success, there was a positive effect of gut passage for C. hirta, but not for L. robustum. For both C. hirta and L. robustum, no seeds in intact fruits geminated, suggesting that removal of pulp is essential for germination. Our results suggest that, first, the initial invasion of native forests in Mauritius may not have happened so rapidly without efficient avian seed dispersers like the red‐whiskered bulbul. Second, the bulbul is likely to be a major factor in the continued re‐invasion of C. hirta and L. robustum into weeded and restored conservation management areas.     

Seed dispersal by the Florida box turtle (<Emphasis Type="Italic">Terrapene carolina bauri</Emphasis>) in pine rockland forests of the lower Florida Keys,United States

Seed dispersal by animals is one of the most important plant-animal mutualisms, but saurochory, the dispersal of seeds by reptiles, has received little attention. We investigated the role of the Florida box turtle (Terrapene carolina bauri) as a seed dispersal agent in pine rockland forests of the lower Florida Keys and examined the effect of turtle digestion on seed germination. We obtained seeds of 11 species with fleshy fruits and 2 species with non-fleshy fruits (a grass and legume) from the feces of 145 box turtles collected on Key Deer National Wildlife Refuge from 1999 to 2000. We planted the seeds of nine species and germination percentage (percentage of seeds that germinated during the experiment) varied from 10% to 80%. Comparative germination experiments were conducted with Thrinax morrissii, Serenoa repens, and Byrsonima lucida. We compared the germination percentage and germination rate (number of days from planting to seedling emergence) of seeds from three treatments (seeds recovered from feces, control seeds with pulp, and control seeds without pulp) and continued these experiments for up to 2 years. Passage through the box turtle digestive tract greatly enhanced the germination percentage and germination rate of S. repens, but decreased the germination percentage of B. lucida and T. morrissii, and decreased germination rate for T. morrissii. Subsequent destructive seed viability tests revealed that many ungerminated T. morrissii seeds remained viable, suggesting long-term seed dormancy may occur, even after passage through the turtle digestive system. In addition, the proportion of ungerminated seeds which remained viable was greater for seeds recovered from turtle feces than from control seeds with pulp. Furthermore, removal of fleshy pulp either manually or by the turtle digestive system may allow T. morrissii to escape insect predation.