Frugivory and the effects of ingestion by bats on the seed germination of three pioneering plants

The dispersion and seedling establishment of pioneering plants can be favoured by the presence of frugivorous bats because the bats usually improve seed germination after ingestion. Although seed germinability is known to vary greatly after ingestion by different bats, the relative contribution of each bat species to seed germination within plant communities is poorly understood. In this study, we first determined the fauna of frugivorous bats in a semideciduous seasonal forest remnant in southern Brazil and subsequently identified the plant species of the seeds passed through their guts. Second, the germination performance (i.e., germination percentage and speed) of the seeds of three pioneering plants (Piper aduncum, Piper hispidinervum and Solanum granuloso-leprosum) ingested by the most abundant bats was compared with that of the non-ingested seeds (seeds collected from fruits). Additionally, the effects on seed germination of different bat species were compared. During one year, five species of frugivorous bats were caught, and the seeds of eleven identifiable plant species (not counting those of undetermined species) were found in their faeces. We found that the germination performance of the seeds of Piper species was significantly enhanced after ingestion by bats, whereas S. granuloso-leprosum seeds had neutral or reduced germinability when seeds in faeces were compared with pulp-removed seeds. Our results revealed that the bat species that were captured exerted different effects upon seed germination; such a disparity is expected to result in different rates of early establishment of these pioneer plants in tropical forests, most likely affecting forest composition and structure, particularly during the initial stages of succession.     

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

相似文献   

Digestion time and intactness of seeds ingested by Sturnira lilium (E. Geoffroy, 1810) (Mammalia,Chiroptera)

Bats are responsible for many ecological services, such as seed dispersal of several plant species, contributing to the processes of succession and forest regeneration. A factor that can interfere with this process is the animal digestion, which can affect germination, altering the patterns of seedling distribution. The effects of seed passage through bats’ guts varies with the species, leading to some discrepancies in the literature. In this study, we tested the digestion time of one Phyllostomidae bat species, Sturnira lilium, in two Neotropical plants: Solanum paniculatum and Ficus organensis, and the effects on seed germination. The experiment was conducted in captivity and the germination tests were made in laboratory conditions. The results suggested that most seeds ingested by S. lilium are dispersed within 40 min for both species and the digestion seems not to significantly affect the germination of F. organensis, despite the slight acceleration of germination. In S. paniculatum, germination occurred only in the control (39%), whereas in the treatments, all the seeds remained dormant during the 25 experimental days. In this case, the digestion of S. lilium possibly contributes to the formation of seed banks, randomizing the temporal distribution of seedlings.     

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.     

棕果蝠取食对两种榕树种子萌发行为的影响

在实验室利用聚果榕（Fieus racemosa）和对叶榕（Fieus hispida）成熟的果实饲喂笼养棕果蝠（Rousettus leschenaulti）,比较了不同处理的3组种子的萌发行为：（1）棕果蝠粪便中的种子;（2）被吐出的果渣中的种子;（3）成熟果实中的种子（对照）。棕果蝠取食行为显著影响了两种榕树种子的萌发过程,3种不同处理的种子萌发过程及最终萌发率（GP）之间都存在显著的差异。聚果榕种子经过棕果蝠消化道后GP显著降低,而对叶榕种子的GP显著提高。棕果蝠粪便中的聚果榕种子萌发开始（GS）和最短萌发时间（Tmin）均比对照种子延迟了2d,但其粪便中的对叶榕种子G5比对照种子提前了1d,Tmin提前了2d;与之相似,前者种子萌发比果实中种子提前2d达到萌发总量的50％（T50）,但后者没有改变T50。不同种榕果果渣中的种子萌发行为也有重大差异：聚果榕果渣中种子的Tmin和T50均比对照种子延迟1d,GS没发生改变;而对叶榕果渣中种子的Tmin比对照种子提前了3d,GS提前1d,T50没有改变。棕果蝠取食两种榕果后在飞行过程中排泄,进而有效的散布种子;而且通过消化明显改变了种子萌发行为,使种子萌发类型更为多样,增加了种子在不同时空条件下萌发的可能性。     

The effect of bat (Rousettus aegyptiacus) dispersal on seed germination in eastern Mediterranean habitats

The fruit-bat Rousettus aegyptiacus (Pteropodidae) in Israel consumes a variety of cultivated and wild fruits. The aim of this study was to explore some of its qualities as a dispersal agent for six fruit-bearing plant species. The feeding roosts of the fruit-bat are located an average of 30 m from its feeding trees and thus the bats disperse the seeds away from the shade of the parent canopy. The bat spits out large seeds but may pass some (2%) of the small seeds (<4 mg) through its digestive tract. However, neither the deposited seeds nor the ejected seeds (except in one case) had a significantly higher percentage germinating than intact seeds. Although the fruit-bat did not increase the percentage germinating, seeds of three plant species subject to different feeding behaviors (deposited in feces or spat out as ejecta) had a different temporal pattern of germination from the intact seeds. The combined seed germination distribution generated by these different treatments is more even over time than for each treatment alone. It is sugested that this increases asynchronous germination and therefore enhances plant fitness by spreading the risks encountered during germination, especially in eastern Mediterranean habitats where the pattern of rainfall is unpredictable.     

Seed Dispersal of Morus macroura (Moraceae) by Two Frugivorous Bats in Xishuangbanna, SW China

The dispersal of Morus macroura seeds by two species of frugivorous bats ( Rousettus leschenaulti and Cynopterus sphinx ) was studied in a forest at Xishuangbanna Tropical Botanical Garden in Southwest China from March to May 2005. Feeding roosts were identified within 500 m around parent trees and the types and number of seed loads under each roost were recorded. We found feeding roost density decreased with increasing distance from the parent, but found no correlation between distance and seed deposition. The effect of bat digestion on seed germination was investigated, and we found that germination percentage of all treatments involving ingestion by bats was significantly lower than control seeds and some germination parameters of seeds from different treatments changed.     

Small Tent-Roosting Bats Promote Dispersal of Large-Seeded Plants in a Neotropical Forest

In Neotropical regions, fruit bats are among the most important components of the remaining fauna in disturbed landscapes. These relatively small-bodied bats are well-known dispersal agents for many small-seeded plant species, but are assumed to play a negligible role in the dispersal of large-seeded plants. We investigated the importance of the small tent-roosting bat Artibeus watsoni for dispersal of large seeds in the Sarapiquí Basin, Costa Rica. We registered at least 43 seed species > 8 mm beneath bat roosts, but a species accumulation curve suggests that this number would increase with further sampling. Samples collected beneath bat feeding roosts had, on average, 10 times more seeds and species than samples collected 5 m away from bat feeding roosts. This difference was generally smaller in small, disturbed forest patches. Species-specific abundance of seeds found beneath bat roosts was positively correlated with abundance of seedlings, suggesting that bat dispersal may influence seedling recruitment. Our study demonstrates a greater role of small frugivorous bats as dispersers of large seeds than previously thought, particularly in regions where populations of large-bodied seed dispersers have been reduced or extirpated by hunting.     

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.     

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.     

Effects of gut treatment on recovery and germinability of bovine and ovine ingested seeds of four woody species from the Sudanian savanna in West Africa

Passage rate through the digestive tracts of zebu cattle and sheep, and subsequent germination of egested seeds of four woody species from the Sudanian savanna, Acacia dudgeoni, Acacia seyal, Burkea africana and Prosopis africana, were studied. The result indicates large differences in passage rate among woody species, as well as between animals. The values ranged from 46% to 87% for seeds ingested by cattle while the lowest passage rate was 2.3% and the highest being 74% for seeds ingested by sheep. Among plant species, seeds of Prosopis africana had the highest passage rate through the digestive tract of both cattle and sheep. Seed passage through the gut showed a significant positive correlation with seed mass and thickness for cattle and sheep, respectively. The gut treatment and the retention time in the gut did not improve germination capacity and the speed of germination of dormant seeds. For non-dormant seeds of Acacia dudgeoni, the germination capacity was higher for seeds ingested by cattle than sheep. The speed of germination was also significantly higher for egested seeds than the control. It can be concluded that large herbivores could play an essential role in long distance dispersal of seeds. Gut treatment alone was not effective in breaking seed coat-imposed dormancy, although it enhanced the rate of germination of non-dormant seeds. To get a complete picture of the effect of frugivore on the release of seed dormancy, the combined effect of initial mastication and subsequent gut treatment needs to be investigated.     

Effect of seed passage through vertebrate frugivores'' guts on germination: a review

The capacity of seeds to germinate after ingestion by frugivores is important for the population dynamics of some plant species and significant for the evolution of plant-frugivore interactions. In this paper the effects of different vertebrates on seed germination of nearly 200 plant species are reviewed, searching for patterns that predict the circumstances in which germination of seeds is enhanced, inhibited, or unaffected by the passage through the digestive tract of a seed disperser. It was found that seed dispersers commonly have an effect on the germinability of seeds, or on the rate of germination, or both, in about 50% of the plants they consume, although the diversity of animal species tested so far is still rather low (42 bird species, 28 non-flying mammals, 10–15 bats, 12 reptiles, 2 fishes). Enhancement of germination occurred about twice as often as inhibition.

In spite of the morphological and physiological differences in their digestive tracts, the different animal groups tested have similar effects on seed germination, although non-flying mammals tend to influence germination slightly more often than the other groups. Data on fishes are still too scarce for any generalization. Seed retention time in the dispersers' digestive tract is one factor affecting germination, and helps to explain the variation in seed responses observed among plant species, and even within a species. However other factors are also important; for example, the type of food ingested along with the fruits may affect germination through its influence on chemical or mechanical abrasion of the seed coat. Seed traits such as coat structure or thickness may themselves be responsible for some of the variation in seed retention times. Seeds of different sizes, which usually have different transit times through frugivores, and seeds of either fleshy or dry fruits, show often similar germination response to gut passage.

Seeds of different plants species differ strongly in their germination response after ingestion, even by the same frugivore species. Congeneric plants often show little consistency in their response. Even within a species variation is found which can be related to factors such as the environmental conditions under which germination takes place, seed morphology, seed age, and the season when the seeds are produced.

The effect of gut passage on germination differs between tropical and temperate zones. Seed germination of both shrubs and trees (data on herbaceous species are still scarce) in the temperate zone is more frequently enhanced than in the tropics. This result supports the hypothesis that enhanced germination may be more advantageous in unpredictable or less constant environments. Significant differences in frugivore-mediated germination are also found among different life forms. In both tropical and temperate zones, trees appear to be consistently more affected than shrubs or herbs. This might be due to an overall higher thickness of the seed coats, or to a higher frequency of seed-coat dormancy in tree species.

The influence of frugivory upon the population dynamics of a species has to be evaluated relative to other factors that influence germination and seedling recruitment at a particular site. Whether seed ingestion by dispersers is really advantageous to a plant (as has commonly been assumed) can only be assessed if we also determine the fate of the ingested seeds under natural conditions, and compare it to the fate of seeds that have not been ingested.     

Use of Fruit Essential Oils to Assist Forest Regeneration by Bats

Frugivorous bats can be attracted with essential oils from ripe chiropterochoric fruit. We evaluated the efficiency of these oils to attract bats in degraded areas within the Atlantic Rain Forest, particularly pasture and agricultural land. We hypothesized that induction units (IUs), each containing a rubber septum impregnated with oil, would have more bat activity than their respective control units (CUs; without the oil). To test this hypothesis we monitored bat flight activity with night‐vision infrared visors in eight IU and CU from August 2006 to July 2007. We also verified the probability of arrival of chiropterochoric seeds by analyzing the diet of bats captured in a neighboring forest area. Our initial hypothesis that units with odor would lead to greater bat activity was confirmed. Results indicated a rich community of fruit‐eating bats, and dietary analysis revealed a huge potential for dispersion of a vast amount of seeds from different plant species at the IU. Although our study does not reveal with certainty which bat species are attracted to the oil, the flying patterns coincide with those described for the foraging behavior of fruit‐eating phyllostomids. Furthermore, the fact that the bats spend more time flying around the odor source compared to flying time around CU suggest an increase in seed rain. Taken together, these results suggest that the use of essential oils from chiropterochoric fruits induces a qualitative and quantitative increase in seed dispersal in areas that otherwise would not be frequently visited by frugivorous bats.     

Avian Seed Dispersal of an Invasive Shrub

The incorporation of an animal-dispersed exotic plant species into the diet of native frugivores can be an important step to that species becoming invasive. We investigated bird dispersal of Lonicera maackii, an Asian shrub invasive in eastern North America. We (i) determined which species of birds disperse viable L. maackii seeds, (ii) tested the effect of gut passage on L. maackii seeds, and (iii) projected the seed shadow based on habitat use by a major disperser. We found that four native and one exotic bird species dispersed viable L. maackii seeds. Gut passage through American robins did not inhibit germination, but gut passage through cedar waxwings did. American robins moved mostly along woodlot edges and fencerows, leading us to project that most viable seeds would be defecated in such habitats, which are very suitable for L. maackii. We conclude that L. maackii has been successfully incorporated into the diets of native and exotic birds and that American robins preferentially disperse seeds to suitable habitat.     

Effects of Passage Through Tamarin Guts on the Germination Potential of Dispersed Seeds

Passage through tamarin guts may have an effect on seed germination potential. To examine these effects, and the variation between 2 sympatric tamarin species, we studied Saguinus mystax and S. fuscicollis in northeastern Peruvian Amazonia. For most of 39 plant species, neither germination success nor latency was modified by gut passage. Neutral effects on seed germination potential suggest that tamarins may fulfill criteria for effective seed dispersal.     

Flower Visitation by Bats in Cloud Forests of Western Ecuador1

The importance of bat pollination has been demonstrated for many plant species. Yet this mutualism has rarely been studied on a community–wide level. In this paper we present results of a yearlong study of a bat–flower community in cloud forests on the western slopes of the Ecuadoran Andes. Of eight plant–visiting bat species caught, only Anoura caudifera and A. geoffroyi were carrying pollen. These species of Anoura supplement their diets with insects. Unlike glossophagines in other environments, however, which switch completely to a frugivorous or insectivorous diet during certain seasons, they are nectarivorous year–round and were never found with seeds or fruit pulp in their feces. Of the 13 morphotypes of pollen carried by the bats, 11 were identified to genus and 7 to species. Floral characteristics of all of these plants fit the traditional chiropterophilous syndrome well. Our study represents the first direct evidence of bat pollination for those plants identified to species, including four species of Burmeistera (Campanulaceae), as well as the first record of bat pollination for a plant of the genus Meriania (Melastomataceae). While overlap in the diets of the two Anoura was high, significant differences in visitation frequencies to particular plant species were detected. The larger bat species (A. geoffroyi) preferred large flowers, whereas the smaller species (A. caudifera) preferred small flowers.     

Helophyte germination in a Mediterranean salt marsh: Gut‐passage by ducks changes seed response to salinity

Question: In seeds which are regularly consumed by waterbirds in the field, how does gut‐passage modify their response to salinity gradients? Location: Doñana National Park salt marsh, south‐west of Spain. Methods: Seeds of Scirpus litoralis and Scirpus maritimus were collected and force fed to mallards (Anas platyrhynchos). Both the ingested seeds (passage) and non‐ingested seeds (controls) were exposed, in germination chambers, to a salinity range similar to that observed in the field (0–32 dS/m). After 30 days, the total percentage germination, the duration of the dormancy period and the germination speed were computed. The response of the different germination parameters to ingestion and salinity was analyzed using generalized lineal models. Recovery tests on seeds that did not germinate in the various treatments and tests of the effect of ingestion on the intrinsic variability in seed response were also performed. Results: An increase in salinity reduced germinability and increased the length of dormancy, while gut pas sage increased the intrinsic variability of the temporal seed response in both species. In S. litoralis there was a significant interaction between the effects of salinity and passage on germination rate. Passage increased germination rate at low salinities (≤2 dS/m) but decreased it at high salinities (≥4 dS/m). Conclusion: Gut‐passage by ducks significantly changes seed response to salinity. The outcome of plant‐animal interactions can be influenced by environmental gradients. Studies of germination in response to gut passage that do not take such gradients into account may produce misleading results.     

Wahlberg’s epauletted fruit bat (<Emphasis Type="Italic">Epomophorus wahlbergi</Emphasis>) as a potential dispersal agent for fleshy-fruited invasive alien plants: effects of handling behaviour on seed germination

The spread of invasive alien plants into natural habitats is of growing global concern. Several studies have investigated the role that avian frugivores play in the dispersal of these seeds and their effects on germination success. Fruit bats have however received little attention as important dispersal agents of invasive alien plants, despite their recognized role as long distance dispersal agents of various native flora. We investigated whether Wahlberg’s epauletted fruit bats, Epomophorus wahlbergi, would positively influence the germination of seeds of invasive alien plants. These fruit bats were fed fruits of four invasive alien plant species—Psidium guajava, Melia azedarach, Eriobotrya japonica, and Morus alba. Epomophorus wahlbergi were able to process more fruit per gram body mass than birds have been observed to do. Spat and de-pulped control seeds had similar germination success and germinated at approximately the same time for most species. While seeds retained in whole fruit had significantly less germination success than spat seeds for all species, except M. azedarach, they mostly germinated at approximately the same time. Epomophorus wahlbergi can swallow small seeds (< 2 mm), while seeds larger than this are generally spat out. Large fruit are usually carried away to feeding roosts where seeds are dropped, thereby dispersing seeds and fruits which are too large for some bird species to ingest. Epomophorus wahlbergi should not be underestimated as dispersers of these invasive alien plants as they consume proportionally large amounts (0.62 ± 0.09 to 0.99 ± 0.11 g.g⁻¹ body mass) of fruit, except for M. azedarach, and positively affect their seed germination rates.     

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.     

The Diet and Reproductive Schedules of Leptonycteris curasoae curasoae and Glossophaga longirostris elongata (Chiroptera: Glossophaginae) on Curaçao

Two bat species, Leptonyrteris curasoae and Glossophaga longirostris, are the principal pollinators of at least two of the three species of columnar cacti that grow on the semiarid island of Curaçao, Netherlands Antilles. I examined the importance of the cacti in the diets of the bats and found that 85–91 percent of their diet samples contained cactus pollen and seeds. At least 43 percent of the samples from each species contained cactus pollen andlor seeds exclusively. Leptonycteris curasoae consumes nectar and pollen of Ceiba pentandra and Agave spp. at the beginning of the dry season and G. longirostris also consumes a few other plant products in the wet season, but both bat species depend nutritionally on cacti. Female bats give birth to one pup per year, and the periods of parturition and lactation in each species correspond to peaks in the reproductive phenology of the two most abundant columnar cactus species. From personal observations and a review of the literature, I determined that bats were unlikely to fly to the mainland to feed, although L. curasoae may do so. I conclude that the interdependence of bats and cacti is suggestive of coevolution, and that columnar cacti are critical for the survival and persistence of nectar-feeding bats on Curaçao.