Effects of seed traits on the potential for seed dispersal by fish with contrasting modes of feeding

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The effect of seed morphology on the potential dispersal of aquatic macrophytes by the common carp (Cyprinus carpio)

1. The potential for seed dispersal by fish (ichthyochory) will vary among aquatic plants because of differences in seed size and morphology. 2. To examine how seed morphology influences the probability of dispersal by the common carp (Cyprinus carpio), we studied seed ingestion, retention time and subsequent egestion and germination of seeds of Sparganium emersum and Sagittaria sagittifolia, two aquatic plant species with similar sized but morphologically different seeds. 3. We compared dispersal probabilities between the two plant species, in which the probability of dispersal is assumed to be a function of the probabilities of seed ingestion, egestion and germination, and the dispersal distance is assumed to be a function of seed egestion rate over time. 4. We found that, although the soft seeds of S. sagittifolia had an approximately 1.5 times higher probability of being ingested by the carp than the hard seeds of S. emersum (83.15% ± 1.8% versus 56.16% ± 2.7%, respectively), the latter had an almost twofold higher probability of surviving the passage through the digestive tract (38.58% ± 2.7% versus 20.97% ± 1.5%, respectively). Patterns of seed egestion over time did not differ between the two plant species, despite the difference in seed morphology. Gut passage had a different effect on seed germination between plant species. Compared with non‐ingested controls, seeds of S. emersum showed a 12.6% increase in germination and a 2.1 day acceleration in germination rate, whereas seeds of S. sagittifolia displayed a 47.3% decrease and 5.1 day delay, respectively. 5. Our results suggest that seed morphology affects the dispersal probability and postdispersal establishment, but not the dispersal distance, of aquatic plants that are dispersed by fish.     

Neotropical fish–fruit interactions: eco‐evolutionary dynamics and conservation

Frugivorous fish play a prominent role in seed dispersal and reproductive dynamics of plant communities in riparian and floodplain habitats of tropical regions worldwide. In Neotropical wetlands, many plant species have fleshy fruits and synchronize their fruiting with the flood season, when fruit‐eating fish forage in forest and savannahs for periods of up to 7 months. We conducted a comprehensive analysis to examine the evolutionary origin of fish–fruit interactions, describe fruit traits associated with seed dispersal and seed predation, and assess the influence of fish size on the effectiveness of seed dispersal by fish (ichthyochory). To date, 62 studies have documented 566 species of fruits and seeds from 82 plant families in the diets of 69 Neotropical fish species. Fish interactions with flowering plants are likely to be as old as 70 million years in the Neotropics, pre‐dating most modern bird–fruit and mammal–fruit interactions, and contributing to long‐distance seed dispersal and possibly the radiation of early angiosperms. Ichthyochory occurs across the angiosperm phylogeny, and is more frequent among advanced eudicots. Numerous fish species are capable of dispersing small seeds, but only a limited number of species can disperse large seeds. The size of dispersed seeds and the probability of seed dispersal both increase with fish size. Large‐bodied species are the most effective seed dispersal agents and remain the primary target of fishing activities in the Neotropics. Thus, conservation efforts should focus on these species to ensure continuity of plant recruitment dynamics and maintenance of plant diversity in riparian and floodplain ecosystems.     

Three–way interactions between Acacia, large mammalian herbivores and bruchid beetles - a review

Large mammalian herbivores are both predators and dispersers of Acacia seeds. While some of the seeds are destroyed during passage through the herbivore's digestive tract, others are defecated unharmed. Ingestion by large herbivores facilitates germination by scarification of the seed coat. The extent of the influence of herbivores on seed dispersal and germination depends on seed retention time and tooth size, which are both positively correlated with body size. Infestation by bruchid beetles (Bruchidae) reduces Acacia germination. Herbivores may reduce bruchid infestation in several ways. Larvae in recently infested seeds are killed by stomach acids penetrating the seed through the larval entry hole. Seeds that are partly excavated by burrowing larvae in more advanced stages may be crushed by the herbivore's teeth. Lastly, but probably most crucially, herbivores simply remove seeds from the natal tree prior to infestation or at least prior to reinfestation. The timing and magnitude of herbivory is crucial for both the reduction of bruchid infestation and Acacia seedling establishment. Although it is widely agreed that a three–way interaction exists between bruchid beetles, Acacia trees and large mammalian herbivores, it is also apparent that the relationship is highly complex and is not yet completely understood.     

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.     

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.     

Reduced germination success of temperate grassland seeds sown in dung: consequences for post‐dispersal seed fate

• Endozoochory is one of the main drivers shaping temperate grassland communities by maintaining plant populations of its constituents and enabling plants to colonize new habitats. Successful endozoochorous dispersal implies that seeds not only get consumed and survive the digestive tract but are also able to develop into viable seedlings in a dung environment.
• We experimentally assessed the germination probability and timing of 15 annual and perennial temperate European grassland species in cattle and horse dung and in different climatic conditions (greenhouse and outdoor conditions).
• Interspecific variation in germinability and germination timing are found, while life strategy had only an effect on germination timing. We found adverse effects of both cattle and horse dung on the germination characteristics of all tested grassland species, but the effects of cattle dung were more pronounced. In comparison with the control treatment, fewer seeds emerged in dung and more time was needed to germinate. Also, germination metrics clearly differed between the artificial greenhouse and outdoor conditions, with generally a lower germinability in outdoor conditions.
• According to our results, a large cost seems to be associated with endozoochorous dispersal in this stage of the life cycle, as seed dispersal effectiveness strongly depends on the quality of the deposition site with a lowered survival and germination probability when seeds are deposited in dung.

     

A non‐destructive sampling protocol for field studies of seed dispersal by fishes

This paper presents a standardized protocol for the non‐lethal capture of fishes, sampling of stomach contents and quantification of seed dispersal efficiency by frugivorous fishes. Neotropical pacu Piaractus mesopotamicus individuals were collected with fruit‐baited hooks. The diets of 110 fish were sampled using a lavage method, which retrieved >90% of stomach contents of both juveniles and adults and allowed individuals to recover within 5 min of treatment. The proportional volume of six food categories was similar for stomachs and whole digestive tracts retrieved by dissection. Fruit pulp was proportionally lower in the stomach. The abundance and species richness of intact seeds increased with fish size independent of whether only stomachs or whole digestive tracts were analysed. The analysis of stomach contents accounted for 62·5% of the total species richness of seeds dispersed by P. mesopotamicus and 96% of common seeds (seed species retrieved from more than one fish). Germination trials revealed that seed viability was similar for seeds collected from the stomach via lavage and seeds that passed through the entire digestive tract. Therefore, stomach contents provide an unbiased representation of the dietary patterns and seed dispersal of frugivorous fishes.     

A reassessment of the role of simple seed traits in mortality following herbivore ingestion

Grazing mammals are regarded as major vectors in seed dispersal of grassland plants, through seed ingestion and subsequent excretion (endozoochory). The (evolutionary) ecology underlying this dispersal mode is relatively poorly understood because there are limited data, among others, on how seed attributes perform in this process (and could thus be selected for). For seed mortality following ingestion, contrasting patterns described for the role of simple seed traits seem partly due to inadequate comparative analytical methods. We conducted a feeding experiment in which controlled seed quantities from 48 grassland herb and grass species were fed to cattle. Seed mass, length and shape measurements were related to seed mortality rate using phylogenetically independent contrasts, which account for taxonomic interdependence. The proportion of seeds surviving the digestive tract was generally low, but it reached 100%, with increased germination for some species. Neither seed size nor shape correlated significantly with mortality. Structural traits are likely to overrule these simple seed traits, as illustrated by high survival of species having water-impermeable seeds. As this trait has interesting properties with respect to intraspecific variation and genetics, it could provide opportunities for inference on evolutionary consequences for this type of dispersal.     

粪种子库的理论基础、影响因素和生态意义

成熟种子被动物采食和排泄后,沉积在粪便中的有活力的种子称为粪种子库。种子经动物消化道携带而实现传播的过程称为消化道传播,粪种子库是种子消化道传播的必经阶段和关键节点。粪种子库和种子消化道传播一直以来都是生态学家关注的热点。介绍了粪种子库的形成原因和理论基础,指出粪种子库是动-植物互作的结果;讨论了影响粪种子库结构和组成的因素,包括种子形态、动物种类和外界环境对粪种子库生态功能的调控作用;阐述了粪种子库的生态意义,主要表现为种子远距离传播、粪便物质返还以及促进植物群落更新和发展;最后指出将来关于粪种子库的研究需要重点关注的几个方面问题,以期为合理、全面认识粪种子库提供理论参考,并为深刻理解动-植物互作机制提供科学依据。     

Seed traits and bird species influence the dispersal parameters of wetland plants

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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.     

High-quality seed dispersal by fruit-eating fishes in Amazonian floodplain habitats

Seed dispersal is a critical stage in the life history of plants. It determines the initial pattern of juvenile distribution, and can influence community dynamics and the evolutionary trajectories of individual species. Vertebrate frugivores are the primary vector of seed dispersal in tropical forests; however, most studies of seed dispersal focus on birds, bats and monkeys. Nevertheless, South America harbors at least 200 species of frugivorous fishes, which move into temporarily flooded habitats during lengthy flood seasons and consume fruits that fall into the water; and yet, we know remarkably little about the quality of seed dispersal they effect. We investigated the seed dispersal activities of two species of large-bodied, commercially important fishes (Colossoma macropomum and Piaractus brachypomus, Characidae) over 3 years in Pacaya-Samiria National Reserve (Peru). We assessed the diet of these fishes during the flood season, conducted germination trials with seeds collected from digestive tracts, and quantified fruit availability. In the laboratory, we fed fruits to captive Colossoma, quantified the proportion of seeds defecated by adult and juvenile fish, and used these seeds in additional germination experiments. Our results indicate that Colossoma and Piaractus disperse large quantities of seeds from up to 35% of the trees and lianas that fruit during the flood season. Additionally, these seeds can germinate after floodwaters recede. Overexploitation has reduced the abundance of our focal fish species, as well as changed the age structure of populations. Moreover, older fish are more effective seed dispersers than smaller, juvenile fish. Overfishing, therefore, likely selects for the poorest seed dispersers, thus disrupting an ancient interaction between seeds and their dispersal agents. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

种壳厚度对鼠类种子扩散行为及种子命运的影响

种子扩散是植物更新和扩大分布区的一种重要途径。鼠类采取不同的种子扩散和贮藏策略,以应对食物短缺,同时也促进了植物种子扩散。为应对鼠类对植物种子的过度取食,种子进化出了一系列物理、化学等防御特征。其中种壳厚度作为一种物理防御策略,是影响鼠类贮藏行为和种子命运的关键因素。本研究拟通过去除天然栓皮栎（Quercus variabilis）种子的外壳,再在种仁外包被1、2、4、6不同层数的聚乙烯薄膜,模拟种壳厚度,准确控制种壳厚度。2020年10月—2021年1月,在四川都江堰森林生境中释放人工种壳包被的种子,研究人工种壳厚度对鼠类介导的种子扩散和命运的影响。结果表明：（1）鼠类优先扩散种壳较薄（1层薄膜包被）的人工种子;随着种壳厚度的增加,扩散速率逐渐降低,种壳最厚（6层薄膜包被）的种子扩散最慢（P < 0.001）;（2）鼠类喜好分散贮藏1层、2层薄膜包被的种子;当种壳厚度增加至包被4层、6层薄膜时,分散贮藏比例显著降低（P < 0.05）;（3）鼠类偏好集中贮藏4层薄膜包被的种子（P < 0.05）;（4）不同种壳厚度的种子扩散距离无显著差异（P > 0.05）;（5）种壳较薄（1层薄膜包被）的种子分散贮藏率在3 m范围内比例较高。采用聚乙烯薄膜包被是模拟种子外壳的可行方法,并可用于评估种壳厚度对鼠类种子贮藏行为和种子命运的影响等相关研究。     

Seed dispersal by red howling monkeys (Alouatta seniculus) in the tropical rain forest of French Guiana

A 2-year field study of the frugivorous diet of a howling monkey troop, in a tropical rain forest in French Guiana, shows that they disperse by endozoochory ≥95% of plant species from which they eat ripe fruit. Passage through the digestive tract of howlers does not significantly modify the germination success of most plant species samples. Their low digestion rate (X = 20 hr 40 min) is the ultimate cause of a bimodal defecation rhythm that results in the concentration of 60% of defecations being deposited under sleeping sites. The distance of seed dispersal can reach more than 550 m from parent trees,with a mean of 260 m. Although howling monkeys consume fruits differing in morphological characteristics, they are particularly able to disseminate seeds of species whose fruits have a hard and indehiscent external coat or large seeds or both. In French Guiana, they may be especially important dispersers of the Sapotaceae with fruits that simultaneously present both characteristics.     

Linking frugivore activity to early recruitment of a bird dispersed tree,Eugenia umbelliflora (Myrtaceae) in the Atlantic rainforest

Seed dispersal by animals is a complex process involving several distinct stages: fruit removal by frugivores, seed delivery in different microhabitats, seed germination, seedling establishment, and adult recruitment. Nevertheless, studies conducted until now have provided scarce information concerning the sequence of stages in a plant's life cycle in its entirety. The main objective of this study was to evaluate the immediate consequences of frugivore activity for Eugenia umbelliflora (Myrtaceae) early recruitment by measuring the relative importance of each fruit‐eating bird species on the establishment of new seedlings in scrub and low restinga vegetation in the Atlantic rainforest, Brazil. We conducted focal tree observations on E. umbelliflora trees recording birds' feeding behaviour and post‐feeding movements. We also recorded the fate of dispersed seeds in scrub and low restinga vegetation. We recorded 17 bird species interacting with fruits in 55 h of observation. Only 30% of the handled fruits were successfully removed. From 108 post flight movements of exit from the fruiting trees, 30.6% were to scrub and 69.4% to low restinga forest. Proportion of seed germination was higher in low restinga than in the scrub vegetation. Incorporating the probabilities of seeds' removal, deposition, and germination in both sites, we found that the relative importance of each frugivorous bird as seed dispersers varies largely among species. Turdus amaurochalinus and Turdus rufiventris were the best dispersers, together representing almost 12% probability of seed germination following removal. Our results show the importance of assessing the overall consequence of seed dispersal within the framework of disperser effectiveness, providing a more comprehensive and realistic evaluation of the relative importance of different seed dispersers on plant population dynamics.     

Are tortoises important seed dispersers in Amazonian forests?

According to most studies on seed dispersal in tropical forests, mammals and birds are considered the main dispersal agents and the role played by other animal groups remains poorly explored. We investigate qualitative and quantitative components of the role played by the tortoise Chelonoidis denticulata in seed dispersal in southeastern Amazon, and the influence of seasonal variation in tortoise movement patterns on resulting seed shadows. Seed shadows produced by this tortoise were estimated by combining information on seed passage times through their digestive tract, which varied from 3 to 17 days, with a robust dataset on movements obtained from 18 adult C. denticulata monitored with radio transmitters and spoon-and-line tracking devices. A total of 4,206 seeds were found in 94 collected feces, belonging to 50 seed morphotypes of, at least, 25 plant genera. Very low rates of damage to the external structure of the ingested seeds were observed. Additionally, results of germination trials suggested that passage of seeds through C. denticulata’s digestive tract does not seem to negatively affect seed germination. The estimated seed shadows are likely to contribute significantly to the dispersal of seeds away from parent plants. During the dry season seeds were dispersed, on average, 174.1 m away from the location of fruit ingestion; during the rainy season, this mean dispersal distance increased to 276.7 m. Our results suggest that C. denticulata plays an important role in seed dispersal in Amazonian forests and highlight the influence of seasonal changes in movements on the resulting seed shadows.     

Seed dispersal in the mycoheterotrophic orchid Yoania japonica: Further evidence for endozoochory by camel crickets

• Although orthopterans are rarely considered to be effective seed dispersal agents, the large flightless crickets known as ‘weta’ have been suggested to function as ecological replacements for small mammals in New Zealand, where such mammals are absent. In addition, a recent study reported that camel crickets mediate seed dispersal of several heterotrophic plants, including Yoania amagiensis in Japan.
• I investigated the seed dispersal mechanism of Yoania japonica because the fruit morphology is similar to Y. amagiensis. Specifically, I aimed to determine whether Y. japonica fruits are consumed by camel crickets and, if so, whether the seeds defecated by camel crickets remains intact, by checking seed viability with TTC staining, and whether germination rate is different between seeds collected directly from fruits and defecated seeds by comparing in situ seed germinability.
• The present study provides evidence that camel crickets function as seed dispersal agents of Y. japonica. Camel crickets were important consumers of Y. japonica fruits, and a substantial portion of the consumed seeds remained viable after passing through the digestive tract. In situ seed germination experiments revealed that the seeds defecated by camel crickets actually germinated in the field. In addition, the germination rate of defecated seeds was even higher than that of intact seeds, although the difference was not significant.
• Taken together with recent reports of insect‐mediated endozoochory, such a seed dispersal system may be common in plants with fleshy indehiscent fruits and small seeds, even in locations where other seed dispersal agents are present.

     

异子蓬二型种子的萌发与休眠特性及其生态适应

异子蓬为中亚荒漠的特有种,其果实为胞果,花被片在结果时宿存包被果实形成浆果状的散布单位.对异子蓬的散布单位、果实形态进行比较观察,并在5/15℃、5/25℃、15/25 ℃(暗/光=12h/12h)3个温变周期下进行种子萌发实验,结果表明:(1)异子蓬的散布单位绿色、浆果状,有大小两种形态;大小两种散布单位内包被的果实在形状、大小、颜色上存在着明显差异.(2)大的散布单位内包被的果实圆形,扁平,褐色,无光泽,直径(2.64±0.03) mm,重量(3.68±0.04) mg;小的散布单位内包被的果实双凸镜形,黑色,有光泽,直径(2.40±0.04) mm,重量(2.86±0.06) mg.(3)褐色种子在3个温变周期下的萌发率都在81%以上,萌发速度快,而黑色种子萌发率低,萌发慢,具有休眠现象.(4)划破种皮及低温层积处理可显著提高黑色种子在3个温变周期下的萌发率,延长储存时间也可有效地促进黑色种子的萌发,表明黑色种子处于非深度生理休眠状态.异子蓬产生的两种不同类型的种子及其在时间和空间上的萌发差异对荒漠异质环境具有重要的适应意义.     

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

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