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

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

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

Effect of Bat Exclusion on Patterns of Seed Rain in Tropical Rain Forest in French Guiana

To assess the impact of bats on seed dispersal in a tropical mature forest (Nouragues, French Guiana), we conducted a bat exclusion experiment and tested the hypotheses that an artificial reduction in the abundance of bats would result in: (1) a decrease in seed species diversity, at the community level; and (2) an increase in seed limitation (a failure of seeds to reach all suitable sites for germination) at the species level. Seed rain was sampled in two contiguous forest plots for a total of 120 d, using 49 seed traps (1 m²) arranged in 7 × 7 grids and spaced at 5-m intervals. Using mist nets, bat activity was reduced in one forest plot for a total of 60 nights. Thirty-nine plant species, or species groups, likely to be consumed and dispersed by bats, were collected within a total sample of 50,063 seeds. The overall seed rain was dominated by epiphytic Araceae and Cyclanthaceae (83.3%) and tree species within the genera Cecropia and Ficus (16.0%). Seeds from bat-dispersed shrubs and treelets ( Piper , Solanum , and Vismia ) were relatively rare (0.7%). The bat exclusion resulted in a 30.5 percent reduction in seed species richness and increased seed limitation for most of the species sampled. Seed limitation was caused mainly by a reduced seed rain (seed source limitation) rather than a decrease in seed dispersal uniformity (seed dispersal limitation). Therefore, bat-dispersed plants with low seed production are likely to be particularly affected by a decline in bat abundance, as a result of anthropogenic change.     

Scale‐dependent effects of forest restoration on Neotropical fruit bats

Neotropical fruit bats (family Phyllostomidae) facilitate forest regeneration on degraded lands by dispersing shrub and tree seeds. Accordingly, if fruit bats can be attracted to restoration sites, seed dispersal could be enhanced. We surveyed bat communities at 10 sites in southern Costa Rica to evaluate whether restoration treatments attracted more fruit bats if trees were planted on degraded farmlands in plantations or island configurations versus natural regeneration. We also compared the relative influence of tree cover at local and landscape spatial scales on bat abundances. We captured 68% more fruit bat individuals in tree plantations as in controls, whereas tree island plots were intermediate. Bat activity also responded to landscape tree cover within a 200‐m radius of restoration plots, with greater abundance but lower species richness in deforested landscapes. Fruit bat captures in controls and tree island plots declined with increasing landscape tree cover, but captures in plantations were relatively constant. Individual species responded differentially to tree cover measured at different spatial scales. We attribute restoration effects primarily to habitat structure rather than food resources because no planted trees produced fruits regularly eaten by bats. The magnitude of tree planting effects on fruit bats was less than previous studies have found for frugivorous birds, suggesting that bats may play a particularly important role in dispersing seeds in heavily deforested and naturally regenerating areas. Nonetheless, our results show that larger tree plantations in more intact landscapes are more likely to attract diverse fruit bats, potentially enhancing seed dispersal.     

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.     

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.     

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。     

Fruit Bats (Chiroptera: Pteropodidae) as Seed Dispersers and Pollinators in a Lowland Malaysian Rain Forest1

The aims of this study were to (1) characterize the food resources exploited by fruit bats (Pteropodidae) within an old‐growth Malaysian dipterocarp forest, (2) test the viability of the seeds they disperse, and (3) provide an estimate of the proportion of trees that are to some degree dependent upon bats for seed dispersal and/or pollination. Fruit species exploited by bats could be distinguished from those eaten by birds largely on the basis of color (as perceived by human beings). Bat‐dispersed fruits were typically inconspicuous shades of green–yellow or dull red–brown, whereas fruits eaten by birds were generally bright orange to red. Dietary overlap between bats and nonflying mammals was relatively high. In contrast to primates and squirrels, which were major seed predators for several of the plant species under investigation, fruit bats had no negative impact on seed viability. A botanical survey in 1 ha of old‐growth forest revealed that 13.7 percent of trees (?15 cm girth at breast height) were at least partially dependent upon fruit bats for pollination and/or seed dispersal.     

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.     

Germination responses of four pioneer plant species after passage through the gut of a frugivorous Neotropical bat

Seed passage through the guts of bats potentially influences germination in different ways: physically, chemically and biologically. To evaluate the influence of a Neotropical bat on the seed germination of four pioneer plant species, an experiment was conducted. Considering the positive influence of bats on germination and the possibility of observing non-viability caused by microorganisms, we hypothesized that (i) seeds subjected to passage through bat guts without the influence of microorganisms have a higher germination potential. Considering the different ecological requirements for the germination of plant species, we also hypothesized that (ii) the four plant species present different germination parameters. The germination of seeds from feces and fruits in the presence and absence of microorganisms was compared for each plant species and among the four plant species. The ingestion of seeds by bats and the presence of microorganisms either improved or did not influence the germination parameters of plants, but the direction of the effects did not support the hypothesis in all cases. The germination parameters differed among most plant species except between Ficus adhatodifolia and F. guaranitica. Our findings indicate that the influence of bats on seeds depends on the microorganisms and singularities of plant species.     

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.     

濒危树种闽楠种子和幼苗生态学研究

从1995至1998年,通过种子收集器布设、不同程度圈围的样方处理、实验室和野外发芽实验、相邻格子样方调查和土壤中种子的筛选等一系列方法,对福建罗卜岩闽楠种子质资源保护区内闽楠为优势的常绿阔叶林群落中闽楠种群的果实、种子库、种子散布、果实／种子捕良、种子萌发和幼苗存活等进行了研究。结果表明：1995至1996年果实量为116个／m^2,成熟高峰期在1996年1月中旬。1997年至1998年为103个/m^2,成熟高峰期在1997年12月中旬。1997年至1998年,绝大部分（90．1％）的果实直接从母树上掉落,低于9．5％的果实由鸟类传播。实验室的种子发芽率为93％,而在野外仅为12％。野外发芽率低多由种子霉烂引起。闽楠的种子寿命较短,其种子在次年4月初开始萌发,7月之后地面种子即丧夫活力。动物捕食不仅影响种子的存活,同时也影响幼苗的死亡率,未经圈围与样地中被取食的果实和幼苗数量有显著差异。在新形成的林窗中或远离母树均降低了果实的迁移和幼苗的死亡率。但各因素交互作用有所不同。密度相关效应发生在2－3个月的幼苗阶段,之后,密度高低对果实被取食和幼苗死亡没有显著的影响。这些结果表明,闽楠种子和幼苗经历较大的环境压力,即在高湿度生境中母树树冠下的种子不仅易受到土壤病原菌的感染,同样容易遭受动物所捕食,从而导致较低的野外种子发芽率和幼苗存活率。这是闽楠致濒的重要原因之一。     

Dyssochroma viridiflorum (Solanaceae): a reproductively bat-dependent epiphyte from the Atlantic rainforest in Brazil

Few Neotropical plant species seem to depend on the same animal type both for pollination and seed dispersal, and the known instances refer mostly to birds as the agents in these two phases of a plant reproductive cycle. Dyssochroma viridiflorum (Solanaceae), an epiphyte endemic to the Atlantic rainforest in south-eastern Brazil, was found to be visited by phyllostomid bats for nectar as well as for fruits, with the pollination and seed dispersal of the plant ensured by these flying mammals. The greenish flowers open at night and are visited by the nectar-feeding bat Glossophaga soricina, whereas the yellowish-white fruits are consumed by two species of fruit-eating bats, Carollia perspicillata and Sturnira lilium. Only clinging visits, an uncommon behavioural pattern for glossophagine bats while feeding on flowers, were recorded. The small seeds of D. viridiflorum are swallowed along with the fruit pulp and later defecated on the bats' flying pathways. It is suggested that species of Dyssochroma and two other solanaceous bat-pollinated genera, Merinthopodium and Trianaea, form a derived and bat-dependent clade within the Juanulloeae.     

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.     

Is the endangered Apium repens (Jacq.) Lag. rare because of a narrow regeneration niche?

The conservation of rare plant species is an important aspect of global biodiversity protection, but in many cases these species and the reasons why they are rare are poorly understood. The perennial umbellifer Apium repens is generally regarded to be a rare species all over its European range. We hypothesized that its rarity might be caused by a restricted regeneration niche, that is, highly specific requirements for sexual regeneration, low seed dispersal potential and low endurance capacity of seeds in the ground. We conducted several experimental investigations on its germination ecology, hydrochorous dispersal potential and soil seed bank properties. Apium repens showed high germination success under a variety of abiotic conditions. Either light or cold-wet stratification was necessary to stimulate germination. Seeds were able to float for more than 50 days when protected from precipitation, and soil seed bank sampling revealed that at least some seeds of A. repens were contained in soil depths of up to 10 cm. Overall, our findings do not support the hypothesis that the rarity of A. repens is caused by highly specific requirements for its sexual regeneration. Nonetheless, its germination ecology should be considered when designing conservation measures for this endangered 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.     

Seed bank assembly follows vegetation succession in dune slacks

Question: Is the seed bank in dune slacks during the whole successional range mainly composed of early successional species or does it vary according to the changing vegetation? Location: Belgium, western part of the coast. Methods: We investigated the soil seed bank composition using a seedling germination method in a chronosequence of 20 dune slacks, ranging in age from five to 55 yr. Results: Both seed density and species richness in the seed bank were very low in the first successional stages and increased with age, mainly as a result of increasing seed production. The similarity between seed bank and vegetation was higher in older slacks. A comparison of characteristics between seed bank and vegetation showed that the seed bank was, to a large extent, composed of later successional species. Occurrence patterns of individual species also showed that seeds become incorporated in the soil after the species has established in the vegetation. Conclusion: The seed bank is not likely to be the driving force for successional changes in the vegetation, and successional changes rely on dispersal. Some early successional species persist in the seed bank, but generally only in low numbers. The results also confirm that most typical dune slack species do not form persistent seeds, so that re‐establishment from the seed bank is not to be expected when the species has disappeared from the vegetation.     

植冠与土壤种子库储存种子的萌发特性及策略

为明确黄土丘陵沟壑区植物种子库如何调控种子萌发来提高个体适合度,选择研究区7种具有种子库的主要物种为研究对象,以刚成熟和室内储存种子为对照,比较植冠宿存(5个宿存期)和土壤埋藏(5a埋藏期)对植物种子萌发特性的影响,探讨植冠种子库与土壤种子库储存下的种子萌发策略。结果表明:7种植物种子经过不同种子库储存后萌发特性表现出明显的种间差异,黄刺玫(Rosa xanthina)和水栒子(Cotoneaster multiflorus)种子萌发力表现为植冠宿存不变型、土壤储存增强型,土壤储存明显提高水栒子种子萌发速率;达乌里胡枝子(Lespedeza davurica)和狼牙刺(Sophora davidii)种子萌发力表现为植冠宿存增强型、土壤储存减弱型,种子萌发历时表现为植冠宿存延长型,土壤种子库储存还可加快达乌里胡枝子萌发速率、缩短萌发历时;茭蒿(Artemisia giralaii)和铁杆蒿(Artemisia gmelinii),种子萌发率随植冠宿存时间先升高后降低,随土壤储存时间先降低后升高,土壤储存可推迟其萌发,铁杆蒿种子萌发速率在植冠与土壤储存后均加快;紫丁香(Syringa oblata)种子萌发率随植冠宿存先升高后降低,土壤储存明显加快其种子启动萌发与速率。在黄土丘陵沟壑区,植物种子经过植冠或土壤种子库储存,或增加、加快、提早萌发充分利用有利条件提高占据性,或减少、减缓、推迟萌发分摊不利条件的风险;而且该区植物植冠与土壤储存后种子萌发特性间的关系,体现各自适应环境与应对干扰的分工与协作策略,主要表现为:单一主导型和相辅相成型。     

Role of trichomes and pericarp in the seed biology of the desert annual Lachnoloma lehmannii (Brassicaceae)

In many angiosperms, the fruit rather than the seed is the dispersal/germination unit, and this is the case with Lachnoloma lehmannii, a desert annual ephemeral in central southwestern Asia with indehiscent nonmucilaginuous silicles covered with trichomes. The primary aim of this study was to assess the role of trichomes and pericarp in dispersal, anchorage of diaspores, and seed germination of this species. Mature silicles are dispersed by wind and gravity, and trichomes not only significantly increased their dispersal distance, adherence to sandy soil particles, mass of water imbibed and moisture content, but also decreased the rate of water loss and moisture content of seeds. A significantly higher percentage of seeds within silicles than of isolated seeds retained viability after exposure to 60 °C for 24 h. Seed dormancy is due to the pericarp and to nondeep physiological dormancy, as shown by the increase in germination percentage of isolated seeds following dry storage and treatment with GA₃. Removal of pericarp increased germination of 6-month-old seeds from 0 to 80–90 %, and leachate from both pericarp and trichomes significantly inhibited germination of isolated seeds. Ninety-five percent of seeds within silicles buried in soil for 2 years were viable, but only 28 % of them germinated in light at 15/2 °C; thus L. lehmannii forms a persistent soil seed bank. The pericarp and its trichomes may maximize plant fitness by determining the settlement location of silicles, thus helping to ensure that seeds germinate during the cool season for seedling survival in the desert environment.     

Seed bank patterns of Festuca pallescens in semiarid Patagonia (Argentina): a possible limit to bunch reestablishment

The pre- and postdispersal spatial patterns of the germinable seed bank of Festuca pallescens were evaluated in semiarid grasslands of Patagonia disturbed by sheep grazing. Before dispersal, the seed bank showed spatial heterogeneity and was significantly smaller than the postdispersal seed bank. The postdispersal seed bank was uniformly distributed in patches of bare soil. The size of the germinable seed bank varied with the topographic condition of sites. On slopes, bunches exhibited more panicles and the germinable seed bank was larger after dispersal and smaller before dispersal as compared with upland sites. Losses of the germinable seed bank during autumn and spring are partially accounted for by germination rates. Predominant westerly winds influenced the patterns of seed dispersal, but other agents such as predation or sheet wash may also be active, especially on slopes. The low persistence of the seed bank of F. pallescens, particularly at canopy gaps, indicates that this may constitute a primary control of the regeneration of this species in semiarid grasslands of Patagonia. Management of these grasslands for restoration should accordingly include practices oriented to an adequate replenishment of the germinable seed bank at these places.