Functional diversity in fruit‐frugivore interactions: a field experiment with Mediterranean mammals

Using field seed sowings, we assessed how four mammal species (Meles meles, Vulpes vulpes, Sus scrofa, and Oryctolagus cuniculus) influenced seed germination in three fleshy‐fruited Mediterranean shrubs (Corema album, Pyrus bourgaeana, and Rubus ulmifolius). We predicted that gut passage and removal away from mother plants would enhance the quantity, speed, and asynchrony of seed germination. Results showed that percent germination was altered by gut passage, but that the magnitude and even the direction of such effects varied according to plant and disperser species. Likewise, dispersal away from mother plants affected the percentage and germination speed in some species but not others. Gut passage increased asynchrony of germination in Rubus and Pyrus, and removal from the mother plant increased asynchrony in Rubus, which likely enhances plant fitness in unpredictable environments. Gut passage generally had a stronger effect on germination than removal away from mother plants, but for some species both factors were similarly influential. Therefore, the combined effects of both seed dispersal services varied individually among fruit and frugivore species, leading to unusually high functional diversity in this seed dispersal mutualism.     

Role of Brycinus lateralis (Teleostei: Alestidae) in dispersal and germination of Nymphaea nouchali (Angiospermae: Nymphaeaceae) seeds on a seasonal floodplain of the Okavango Delta,Botswana

Seed passage through the gut of vertebrates can be important for seed dispersal, but might influence seed viability. The ability of seeds to germinate after ingestion by seed-eating fish is important for the population dynamics of some plant species, and significant in the evolution of plant–fish interactions. Certain fish in the Okavango Delta, Botswana, are fruit- and seed-eaters and could act as seed dispersers. We sampled 14 fish species in 2013, finding Nymphaea nouchali var. caerulea seeds in the digestive tracts of eight, most commonly in the striped robber Brycinus lateralis. Seeds extracted from the gut of this species had an overall mean germination success of 11.7%. This fish species might well be a legitimate seed disperser, having a positive effect on seed dispersal from parent plants in the Okavango Delta. The current study represents one of the first investigations of the likelihood of seed dispersal by fish on the African continent.     

How do primates affect seed germination? A meta‐analysis of gut passage effects on neotropical plants

Biotic seed dispersal is a key process maintaining biodiversity in tropical forests where most trees produce vertebrate‐dispersed seeds. Existing meta‐analyses suggest an overall positive effect of vertebrate gut passage on seed germination, but no significant effects for non‐flying mammals. However, previous meta‐analyses combined rodents (seed predators) and primates (seed dispersers) into the non‐flying mammals category, which may confound specific effects of each group on seed germination. However positive effects of monkeys on germination had previously been found in some studies. Here we disentangle the role of Neotropical primates as contributors to seed dispersal in tropical forests by running a meta‐analysis to determine the overall magnitude of gut passage effects on seed germination percentage and mean time to germination. We also compare effect sizes as a function of different feeding guilds, gut complexities, and seed size. Our results show a strong, positive effect of primates on seed germination percentage and on the number of days to first germination. Strictly frugivorous monkeys, the group most threatened by extinction, showed the highest dispersal quality, increasing germination percentage by 75%. Primates that include insects in their diets had no average effect on germination percentage or time. Gut passage had different outcomes on seeds with different sizes; both large and small seeds showed similar increases in germination percentages after gut passage, but only large seeds germinated faster than control seeds after gut passage. Our results show a relevant role for primates in providing high seed dispersal quality and as drivers of forest regeneration. The combined effects of defaunation and forest fragmentation may result in decreased regeneration of trees, which has the potential to affect negatively both forest structure and ecosystem processes. Finally, we provide general guidelines for standardizing research on seed dispersal by primates. Synthesis Consuming fleshy fruits and dispersing seeds is the main ecological service provided by vertebrates to plants. Vertebrate increases seed germination due to treatment given during digestive system passage. Previous meta‐analyses suggest an overall positive effect of vertebrate gut passage on germination, but no insights are available on its variation among different functional groups of mammals. Our analyses indicated that gut passage by Neotropical primates increased seed germination. Strict frugivores, the ones most threatened by extinction, were the most efficient. Our results show a relevant role for primates in providing high seed dispersal quality and as drivers of forest regeneration, which can be meaningful for conservation in a community scale.     

Bird‐mediated seed dispersal: reduced digestive efficiency in active birds modulates the dispersal capacity of plant seeds

Plant populations in fragmented ecosystems rely largely on internal dispersal by animals. To unravel the mechanisms underlying this mode of dispersal, an increasing number of experimental feeding studies is carried out. However, while physical activity is known to affect vertebrate digestive processes, almost all current knowledge on mechanisms of internal seed dispersal has been obtained from experiments with resting animals. We investigated how physical activity of the mallard Anas platyrhynchos, probably the quantitatively most important biotic dispersal agent in aquatic habitats in the entire Northern Hemisphere, affects gut passage survival and retention time of ingested plant seeds. We fed seeds of nine common wetland plants to mallards trained to subsequently swim for six hours in a flume tank at different swimming speeds (activity levels). We compared gut passage survival and retention times of seeds against a control treatment with mallards resting in a conventional dry cage. Intact gut passage of seeds increased significantly with mallard activity (up to 80% in the fastest swimming treatment compared to the control), identifying reduced digestive efficiency due to increased metabolic rates as a mechanism enhancing the dispersal potential of ingested seeds. Gut passage speed was modestly accelerated (13% on average) by increased mallard activity, an effect partly obscured by the interaction between seed retention time and probability of digestion. Gut passage acceleration will be more pronounced in digestion‐resilient seed species, thereby modulating their dispersal distances. Our findings imply that seed dispersal potential by mallards calculated from previous experiments with resting birds is highly underestimated, while dispersal distances may be overestimated for some plant species. Similar effects of physical activity on digestive efficiency of mammals suggests that endozoochorous dispersal of plant seeds by vertebrates is more effective and plays a quantitatively more important ecological role in both terrestrial and aquatic ecosystems than previously thought.     

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.     

Asian Tapirs Are No Elephants When It Comes To Seed Dispersal

The elimination of the largest herbivores (elephants and rhinoceroses) from many forests in tropical East Asia may have severe consequences for plant species that depend on them for seed dispersal. We assessed the capacity of Malayan tapirs Tapirus indicus—the next largest nonruminant herbivore in the region—as a substitute for the lost megafauna in this role by studying their ability to disperse the seeds of nine fleshy‐fruited plants with seeds 5–97 mm in length. We combined information from feeding trials, germination tests, and field telemetry to assess the effect of tapir consumption on seed viability and to estimate how far the seeds would be dispersed. The tapirs (N=8) ingested few seeds. Seed survival through gut passage was moderately high for small‐seeded plants (e.g., 36.9% for Dillenia indica) but very low for medium‐ (e.g., 7.6% for Tamarindus indica) and large‐seeded (e.g., 2.8% for Artocarpus integer) plants. Mean seed gut passage times were long (63–236 h) and only the smallest seeds germinated afterwards. Using movement data from four wild tapirs in Peninsular Malaysia we estimated mean dispersal distances of 917–1287 m (range=22–3289 m) for small‐seeded plants. Malayan tapirs effectively dispersed small‐seeded plants but acted as seed predators for the large‐seeded plants included in our study, suggesting that they cannot replace larger herbivores in seed dispersal. With the absence of elephants and rhinos many megafaunal‐syndrome plants in tropical East Asia are expected to face severe dispersal limitation problems.     

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 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.     

Seed mass,hardness, and phylogeny explain the potential for endozoochory by granivorous waterbirds

Field studies have shown that waterbirds, especially members of the Anatidae family, are major vectors of dispersal by endozoochory for a broad range of plants lacking a fleshy fruit, yet whose propagules can survive gut passage. Widely adopted dispersal syndromes ignore this dispersal mechanism, and we currently have little understanding of what traits determine the potential of angiosperms for endozoochory by waterbirds. Results from previous experimental studies have been inconsistent as to how seed traits affect seed survival and retention time in the gut and have failed to control for the influence of plant phylogeny. Using 13 angiosperm species from aquatic and terrestrial habitats representing nine families, we examined the effects of seed size, shape, and hardness on the proportion of seeds surviving gut passage through mallards (Anas platyrhynchos) and their retention time within the gut. We compiled a molecular phylogeny for these species and controlled for the nonindependence of taxa due to common descent in our analyses. Intact seeds from all 13 species were egested, but seed survival was strongly determined by phylogeny and by partial effects of seed mass and hardness (wet load): species with seeds harder than expected from their size, and smaller than expected from their loading, had greater survival. Once phylogeny was controlled for, a positive partial effect of seed roundness on seed survival was also revealed. Species with seeds harder than expected from their size had a longer mean retention time, a result retained after controlling for phylogeny. Our study is the first to demonstrate that seed shape and phylogeny are important predictors of seed survival in the avian gut. Our results demonstrate that the importance of controlling simultaneously for multiple traits and relating single traits (e.g., seed size) alone to seed survival or retention time is not a reliable way to detect important patterns, especially when phylogenetic effects are ignored.     

When condition trumps location: seed consumption by fruit‐eating birds removes pathogens and predator attractants

Seed ingestion by frugivorous vertebrates commonly benefits plants by moving seeds to locations with fewer predators and pathogens than under the parent. For plants with high local population densities, however, movement from the parent plant is unlikely to result in ‘escape’ from predators and pathogens. Changes to seed condition caused by gut passage may also provide benefits, yet are rarely evaluated as an alternative. Here, we use a common bird‐dispersed chilli pepper (Capsicum chacoense) to conduct the first experimental comparison of escape‐related benefits to condition‐related benefits of animal‐mediated seed dispersal. Within chilli populations, seeds dispersed far from parent plants gained no advantage from escape alone, but seed consumption by birds increased seed survival by 370% – regardless of dispersal distance – due to removal during gut passage of fungal pathogens and chemical attractants to granivores. These results call into question the pre‐eminence of escape as the primary advantage of dispersal within populations and document two overlooked mechanisms by which frugivores can benefit fruiting plants.     

Cecropia as a food resource for bats in French Guiana and the significance of fruit structure in seed dispersal and longevity

Cecropia (Cecropiaceae) is a Neotropical genus of pioneer plants. A review of bat/plant dispersal interactions revealed that 15 species of Cecropia are consumed by 32 species of bats. In French Guiana, bats were captured in primary and secondary forests, yielding 936 fecal samples with diaspores, among which 162 contained fruits of C. obtusa, C. palmata, and C. sciadophylla. A comparative morphological and anatomical study of fruits and seeds taken directly from herbarium specimens, bat feces, and an experimental soil seed bank was made. Contrary to previous reports, the dispersal unit of Cecropia is the fruit not the seed. Bats consume the infructescence, digest pulp derived from the enlarged, fleshy perianth, and defecate the fruits. The mucilaginous pericarp of Cecropia is described. The external mucilage production of Cecropia may facilitate endozoochory. The exocarp and part of the mesocarp may be lost after passage through the digestive tract of bats, but fruits buried for a year in the soil seed bank remain structurally unchanged. Fruit characters were found to be useful for identifying species of bat-dispersed Cecropia. Bat dispersal is not necessary for seed germination but it increases seed survival and subsequent germination. Fruit structure plays a significant role in seed longevity.     

Diaspore removal and potential dispersers of the rare and protected Paeonia officinalis L. (Paeoniaceae) in a changing landscape

Paeonia officinalis L., a rare and protected species, mostly occurs in open and semi‐open habitats and is often threatened by forest and shrubland spread. To explore the still undocumented dispersal features of this species, we address the following questions. What are the relative roles of ants, small rodents, and birds as diaspore removers in open habitat and woodland? Which animal groups constitute the potential disperser assemblage and how do they shape the spatial patterns of seed dispersal? Do diaspores fit the ornithochory syndrome or do they only mimic fleshy fruits? Two experiments were performed to quantify diaspore fall and diaspore removal by animal groups, above ground and on the ground. Ants did not contribute to dispersal. In open habitats, no seed removal was detected, either on follicles or once diaspores had fallen to the ground. In woodland, diaspores were weakly removed by vertebrates on follicles and were mainly removed by rodents on the ground. As a consequence, we suggest that long‐distance dispersal events are very rare, weakening the possible escape into space of populations subject to forest spread. Several traits indicate that diaspores fit the ornithochory syndrome, but other traits are strongly reminiscent of mimetic diaspores deceiving bird dispersers. © 2007 CNRS. Journal compilation © 2007 The Linnean Society of London, Botanical Journal of the Linnean Society, 2007, 154 , 13–25.     

Seed dispersal of Diospyros virginiana in the past and the present: Evidence for a generalist evolutionary strategy

Several North American trees are hypothesized to have lost their co‐evolved seed disperser during the late‐Pleistocene extinction and are therefore considered anachronistic. We tested this hypothesis for the American persimmon (Diospyros virginiana) by studying the effects of gut passage of proposed seed dispersers on seedling survival and growth, natural fruiting characteristics, and modern animal consumption patterns. We tested gut passage effects on persimmon seeds using three native living species, the raccoon (Procyon lotor), Virginia opossum (Didelphis virginiana), and coyote (Canis latrans), and two Pleistocene analogs; the Asian elephant (Elephas maximus) and alpaca (Vicugna pacos). Persimmon seeds excreted by raccoons, coyotes, and elephants survived gut transit. Gut passage did not affect sprouting success, but did tend to decrease time to sprout and increase seedling quality. Under field conditions, persimmon fruits were palatable on the parent tree and on the ground for an equal duration, but most fruits were consumed on the ground. Seven vertebrate species fed upon persimmon fruits, with the white‐tailed deer (Odocoileus virginianus)—a species not capable of dispersing persimmon seeds—comprising over 90% of detections. Conversely, potential living seed dispersers were rarely detected. Our results suggest the American persimmon evolved to attract a variety of seed dispersers and thus is not anachronistic. However, human‐induced changes in mammal communities could be affecting successful seed dispersal. We argue that changes in the relative abundance of mammals during the Anthropocene may be modifying seed dispersal patterns, leading to potential changes in forest community composition.     

脊椎动物传播植物肉质果中的次生物质及其生态作用

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

Ant-mediated expansion of an obligate seeder species during the first years after fire

Most obligate seeder species build up a soil seed bank that is associated with massive seed germination in the year immediately after a fire. These species are also shade‐intolerant and disappear when vegetation cover closes, creating unsuitable conditions for seedling recruitment. The only way for these plants to expand their populations is when habitats suitable for seedling recruitment arise (i.e. in years immediately after a fire). However, short primary seed dispersal of obligate seeders does not allow these plants to colonise the suitable habitats, and these habitats can only be colonised by secondary seed dispersion. We hypothesised that Fumana ericoides, an obligate‐seeding small shrub, not only establishes abundantly in the first year after fire, but also expands its local range in the following years due to secondary dispersal by ants while suitable habitats are still available. We tested this hypothesis using experimental studies and a simulation model of potential population expansion in a recently burned area. Results showed that F. ericoides not only established prolifically in the year immediately after fire, but was also able to recruit new individuals and expand its population in the years following the fire, despite a low germination rate and short primary seed dispersal. Ant‐mediated seed dispersal and availability of suitable habitats were key factors in this phenomenon: ants redistributed seeds in suitable habitats while they were available, which accelerated the expansion of F. ericoides because new plants established far away from the core population.     

Die Tricks der Stinkenden Nieswurz

The tricks of stinking hellebore The stinking hellebore (Helleborus foetidus) uses ingenious tricks in order to attract pollinators and to achieve the dispersal of its seeds. Yeasts metabolise sugar available in nectar und thereby warm it up to attract bees and bumble bees in cold, early spring. This remarkable heating system allows the flowers to already attract pollinators at a time, when competition by other flower species is still low and visits by pollinators are often limited by low temperatures. Early flowering in turn allows seed set in late spring and early summer. The seeds have a fleshy structure attached, an elaiosome that contains lipids, sugars and vitamins. This makes them highly attractive to ants during a season when high-quality foods are still in short supply and leads to dispersal of the seeds (myrmecochory). The elaiosome also contains a fatty acid that acts as an olfactory attractant. But what attracts ants, is also attractive for other seed predators such as mice. Long-term survival of seeds (and thus germination) therefore greatly depends on the detachment of the elaiosome from the seed by the ants. There is much more than meets the eye with respect of stinking hellebore pollination and seed dispersal. It is an example of the highly complex interdependencies between plants, their blossoms, different animal species as well as yeasts and bacteria.     

Endozoochory and Fire as Germination Triggers in Neotropical Dry Forests: an Experimental Test

Endozoochory and fire are crucial ecological factors determining germination success and recruitment in many plant species. Fire is a well‐known germination trigger while endozoochory may allow seed dispersal along with an increase in germination. Their interaction has rarely been addressed, however, even though both factors are pervasive in human‐transformed ecosystems like most Neotropical Dry Forests (NDF). For three common Mesoamerican tree species (Acacia pennatula, Enterolobium cyclocarpum, and Guazuma ulmifolia), we used feeding trials to assess the preference of cattle, which are their main seed dispersal agent. We also experimentally tested the interaction between gut passage and fire as triggers of germination. The fruits of the three species were eaten by cattle, but the small seeds of G. ulmifolia were ingested 10‐fold more than those of the other species. While gut passage did not have any effect on germination, heat‐shocks above 90 °C increased the number of germinating seeds by 15 percent. These results suggest that cattle may be a key dispersal vector in NDF, but that fire may be an important germination trigger. Physical dormancy in these species may have been selected for by extinct megaherbivores because it was a key trait ensuring seed survival after gut passage. However, in light of the recent expansion of cattle‐ranching and fire occurrence in NDF, it has become a useful exaptation facilitating the colonization of disturbed areas.     

Interactions between Ants and Non‐myrmecochorous Fruits in Miconia (Melastomataceae) in a Neotropical Savanna

The aim of this study was to evaluate the role of ants as secondary seed dispersers of six primarily bird‐dispersed Miconia species in the cerrados of southeastern Brazil. Vertebrate exclosure and seed germination experiments were performed for M. albicans, M. alborufescens, M. corallina, M. ferruginata, M. ibaguensis, and M. irwinii. Excluding vertebrates did not significantly alter fruit removal rate for any of the Miconia species relative to open controls. Fruits on stalks and fallen fruits were removed and transported to nests mainly by species of Atta, Acromyrmex, and Ectatomma (dispersal distance ranging from 0.1 to 45.2 m), while Camponotus ants tended to be observed removing the fruit pulp (seed cleaning) where the fruits were found. Seed manipulation by Atta decreased germination of M. irwinii, but not M. ferruginata. Germination did not occur in intact fruits, and thus seed cleaning was an important service provided by the ants. Ant nest soils did not inhibit germination of any of the Miconia species, suggesting they are a good substrate for long‐lived Miconia seeds. We conclude that ant activity could have important effects on the fate of Miconia seeds adapted for bird dispersal.     

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 consumption and dispersal of ant-dispersed plants by slugs

In beech-dominated forests in Central Europe, many spring geophytes show adaptations to seed dispersal by ants (myrmecochory). Ants, however, can be rare in such moist forests. Motivated by observations of slug feeding on seeds we investigated the seed consumption of two plant species, Anemone nemorosa and Asarum europaeum, by slugs, in a series of experiments. In a seed predation experiment in a beech forest, we found that seed removal was strongly reduced when gastropods were excluded from the seed depots. The contribution of insects, including ants, and rodents to seed removal was relatively less but differed between May and July. In the laboratory, slug species, in particular Arion sp., consumed seeds of both plant species. Slugs either consumed the elaiosomes of seeds or swallowed seeds intact. Swallowed seeds were defecated undamaged and germinated as well as control seeds when buried overwinter, indicating the potential for seed dispersal by slugs. We also recovered seeds of myrmecochores in the faeces of several slugs caught in forests. In a slug release experiment in the forest, slugs moved up to 14.6 m (mean 4.4 m) in 15 h, which is the median gut passage time of seeds based on measurements made in the laboratory. We also found that when slug-defecated seeds were offered to rodents, these were less attractive than control seeds, suggesting that passage through the slug gut reduces seed predation risk. Our results demonstrate that slugs are significant consumers of elaiosomes or entire seeds of ant-dispersed plants and that they can function as seed dispersers of these plants.