Extremely long-distance seed dispersal by an overfished Amazonian frugivore

Throughout Amazonia, overfishing has decimated populations of fruit-eating fishes, especially the large-bodied characid, Colossoma macropomum. During lengthy annual floods, frugivorous fishes enter vast Amazonian floodplains, consume massive quantities of fallen fruits and egest viable seeds. Many tree and liana species are clearly specialized for icthyochory, and seed dispersal by fish may be crucial for the maintenance of Amazonian wetland forests. Unlike frugivorous mammals and birds, little is known about seed dispersal effectiveness of fishes. Extensive mobility of frugivorous fish could result in extremely effective, multi-directional, long-distance seed dispersal. Over three annual flood seasons, we tracked fine-scale movement patterns and habitat use of wild Colossoma, and seed retention in the digestive tracts of captive individuals. Our mechanistic model predicts that Colossoma disperses seeds extremely long distances to favourable habitats. Modelled mean dispersal distances of 337-552 m and maximum of 5495 m are among the longest ever reported. At least 5 per cent of seeds are predicted to disperse 1700-2110 m, farther than dispersal by almost all other frugivores reported in the literature. Additionally, seed dispersal distances increased with fish size, but overfishing has biased Colossoma populations to smaller individuals. Thus, overexploitation probably disrupts an ancient coevolutionary relationship between Colossoma and Amazonian plants.     

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.     

Fishing‐down within populations harms seed dispersal mutualism

Large fish are often the most effective seed dispersers, but they are also the preferred target for fisheries. We recently started to comprehend the detrimental impacts of the extirpation of large frugivorous fish species on natural forest regeneration, but we lack a general understanding of how intraspecific size‐selective harvest affects fish–fruit mutualism. Our literature review demonstrated that large individuals within populations positively affect diverse aspects of seed dispersal, from consuming a higher diversity of seeds to enhancing germination. Furthermore, we filled a research gap by studying how individual size variations within two small frugivorous fish species (<16 cm) affect seed dispersal in flooded savannas. Even within small‐bodied species, large individuals swallow a higher number of intact seeds, but not necessarily a higher proportion. Overall, our results demonstrate the disproportional role of large‐bodied individuals as key seed dispersers in flooded habitats. Consequently, fishing‐down within both large‐ and small‐bodied species can negatively affect seed dispersal and natural regeneration in overfished wetlands.     

Within Flood Season Variation in Fruit Consumption and Seed Dispersal by Two Characin Fishes of the Amazon

Many Amazon River fishes consume fruits and seeds from floodplain forests during the annual flood season, potentially serving as important seed dispersers and predators. Using a participatory approach, this study investigated how within-season variation in flood level relates to fruit consumption and seed dispersal by two important frugivorous fish, Colossoma macropomum and Piaractus brachypomus , in two Lower Amazon River fishing communities in Brazil. Diets of both fish species were comprised of 78–98 percent fruits, largely dominated by a few species. Diets included fruits of 27 woody angiosperms and four herbaceous species from 26 families, indicating the importance of forest and Montrichardia arborescens habitat during peak flood. A correspondence between peak fruit species richness and peak flood level was observed in one of two communities, which may reflect higher forest diversity and/or differences in selection of fishing habitat. Both fishes are seed dispersers and predators, the relative role of which did not vary by flood level, seed size, or fish size, but may vary with seed hardness. Interspecific differences in diet volume and intact seeds suggest P. brachypomus are more effective seed dispersers than C. macropomum . Overall, the spatial and temporal variation in fruit species composition and richness demonstrate plasticity in fruit consumption in relation to flood level and locally available fruits. While such diets are adaptive to the dynamic changes of Amazon floodplain habitats, the high consumption of forest fruits and seeds from mid- and late-successional species suggests that floodplain forest degradation could disrupt seed dispersal and threaten local and regional fisheries.     

Big Fish are the Best: Seed Dispersal of Bactris glaucescens by the Pacu Fish (Piaractus mesopotamicus) in the Pantanal, Brazil

We studied the potential role as seed disperser of the pacu fish (Piaractus mesopotamicus, Characidae) in the Pantanal of Brazil. The most important food item in the diet of the pacu in the wet season was fruits of the palm Bactris glaucescens found in the guts of 73 percent of all fishes collected (N= 70). We found a positive relationship between fish length, weight, and gape size and the number of intact seeds in their gut. Therefore, large pacus are especially important in dispersing B. glaucescens seeds within the studied system. Since the best seed dispersers are the largest fishes, which are preferred by commercial fisheries, we predict that the ongoing over fishing in freshwater ecosystems will have major impacts on the dispersal system of fish‐dependent plants. We suggest that it is paramount to change the attitudes in fisheries management of fruit‐eating fishes and urgent to evaluate the impact of fishing on forest regeneration.     

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.     

Diversity of seeds captured by interception exceeds diversity of seeds deposited in traps

Seed dispersal, a key process in terrestrial landscapes, is increasingly important in the face of habitat fragmentation and global climate change. Seed dispersal is also notoriously difficult to characterize, especially in species rich and spatially complex tropical forests. We contrasted assemblages of biotically dispersed seeds collected from four sites using two methods: deposition into seed traps and interception by the capture of frugivorous birds. We also compared seed deposition and interception with local fruit production. Species accumulation curves for seeds deposited in seed traps began to level off sooner than curves for seeds collected from birds captured in mist nets, and extrapolation showed significantly greater estimated species richness for seeds collected from birds than for those deposited in traps. Assemblages from birds and from traps at each site were quite different, with an abundance‐based similarity index of 0.64; this dissimilarity increases if bat‐dispersed seeds are included in the analysis. Common bird‐dispersed species were retrieved from both mist‐netted birds and from seed traps, but numerous locally fruiting understory species were recovered only from birds. We conclude that the sampling of seeds carried by birds provides a valuable complement to other methods of studying seed dispersal in species‐rich tropical forests by revealing relationships between specific dispersers and their seed plants and by creating a more complete account of species diversity of seeds being transported at a given site.     

Seed dispersal potential by wild mallard duck as estimated from digestive tract analysis

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

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The Role of Arboreal Seed Dispersal Groups on the Seed Rain of a Lowland Tropical Forest1

Most tropical plants produce fleshy fruits that are dispersed primarily by vertebrate frugivores. Behavioral disparities among vertebrate seed dispersers could influence patterns of seed distribution and thus forest structure. This study investigated the relative importance of arboreal seed dispersers and seed predators on the initial stage of forest organization–seed deposition. We asked the following questions: (1) To what degree do arboreal seed dispersers influence the species richness and abundance of the seed rain? and (2) Based on the plant species and strata of the forest for which they provide dispersal services, do arboreal seed dispersers represent similar or distinct functional groups? To answer these questions, seed rain was sampled for 12 months in the Dja Reserve, Cameroon. Seed traps representing five percent of the crown area were erected below the canopies of 90 trees belonging to nine focal tree species: 3 dispersed by monkeys, 3 dispersed by large frugivorous birds, and 3 wind‐dispersed species. Seeds disseminated by arboreal seed dispersers accounted for ca 12 percent of the seeds and 68 percent of the seed species identified in seed traps. Monkeys dispersed more than twice the number of seed species than large frugivorous birds, but birds dispersed more individual seeds. We identified two distinct functional dispersal groups, one composed of large frugivorous birds and one composed of monkeys, drop dispersers, and seed predators. These groups dispersed plants found in different canopy strata and exhibited low overlap in the seed species they disseminated. We conclude it is unlikely that seed dispersal services provided by monkeys could be compensated for by frugivorous birds in the event of their extirpation from Afrotropical forests.     

黄檗的更新特点及食果实鸟类对其种子的传播

在帽儿山实验林场和哈尔滨实验林场 ,黄檗母树下没有幼苗分布 ,不能进行天然更新 ,需要靠食果实鸟类等将果实和种子传播至远离母树的其他林下。捕食黄檗果实的食果实鸟类有 9种。其中 6种是食果肉鸟类 ,吞入果实后 ,消化果肉 ,而种子完整地随粪便排出而得以传播。其余 3种是食种子鸟类 ,没有传播作用。果实在鸟类消化道内的滞留时间达 2 0～ 30min ,具有很长的潜在传播距离。将鸟类消化后的种子与完整果实和人为去果肉种子进行萌发对比实验 ,消化后种子的累计萌发率与其余二者之间均没有显著性差异 ,说明食果实鸟类的消化 (道 )过程对种子萌发没有明显影响 ,同时证明果肉对种子萌发率没有显著影响 ,果肉中不含萌发抑制物质。黄檗提供多种鸟类以食物 ,而鸟类也同时以多种肉质果植物为食物。因此食果实鸟类和肉质果植物 (包括黄檗 )之间形成了松散的互利共生关系     

Intra-specific downsizing of frugivores affects seed germination of fleshy-fruited plant species

The loss of largest-bodied individuals within species of frugivorous animals is one of the major consequences of defaunation. The gradual disappearance of large-bodied frugivores is expected to entail a parallel deterioration in seed dispersal functionality if the remaining smaller-sized individuals are not so effective as seed dispersers. While the multiple impacts of the extinction of large bodied species have been relatively well studied, the impact of intraspecific downsizing (i.e. the extinction of large individuals within species) on seed dispersal has rarely been evaluated. Here we experimentally assessed the impact of body-size reduction in the frugivorous lizard Gallotia galloti (Lacertidae), an endemic species of the Canary Islands, on the seed germination patterns of two fleshy-fruited plant species (Rubia fruticosa and Withania aristata). Seed germination curves and the proportions of germinated seeds were compared for both plant species after being defecated by large-sized individuals and small-sized individuals. The data show that seeds of W. aristata defecated by larger-sized lizards germinated faster and in a higher percentage than those defecated by small-sized lizards, while no differences were found for R. fruticosa seeds. Our results suggest that disappearance of the largest individuals of frugivorous species may impair recruitment of some plant species by worsening seed germination. They also warn us of a potential cryptic loss of seed dispersal functionality on defaunated ecosystems, even when frugivorous species remain abundant.     

渤海鱼类食物关系的初步研究

本文材料取自1982年4月—1983年5月在渤海逐月进行的拖网探捕调查。共分析了54种鱼的1,863个胃。用3个指标确定各种饵料在鱼类食谱中的重要性:(1)重量百分比(W);(2)尾数百分比(N);(3)出现频率(F)。根据3个指标计算每种饵料的相对重要性指标:IRI=(N+W)·F。按照IRI的大小,渤海的鱼类大体上可分成5个类群:(1)浮游动物食性;(2)浮游和底栖动物食性;(3)底栖动物食性;(4)底栖和游泳动物食性;(5)游泳动物食性。这些龟类按Odum和Heald的方法可分成3个营养级:(1)低级肉食性鱼类;(2)中级肉食性鱼类;(3)高级肉食性鱼类。 在渤海饵料生物中,起主要作用的是浮游动物、鼓虾、短尾类、尖尾鰕虎鱼、钝尖尾鰕虎鱼和(鱼是)鱼.根据主耍饵料,渤海鱼类可以分成5个类群:(1)以黄盖鲽为代表,它们主食腔肠动物、多毛类和棘皮动物;(2)以鳎类为代表,主食鼓虾和短尾类;(3)以鳐类、石首鱼类为代表,主食鼓虾和钝尖尾锻虎鱼;(4)以(鱼是)鱼为代表,主食浮游动物;(5)以牙鲆为代表,主食鱼类。5个类群之间,仅第2、3两个类群在鼓虾上有食物竞争。 在除掉渤海湾、辽东湾及5米以内浅水区外的调查海区内的54种鱼1863个消化道中,仅发现8尾对虾,它表明对虾几乎没有被其它鱼类捕食。对近岸及各湾的幼体和仔、幼虾来说,可能并非如此,需要进行专门的调查后才能弄清。     

Studies on food organisms of pelagic fishes as revealed by the 1979 North Atlantic Eel Expedition

The extent to which pelagic fishes occurring in the Sargasso Sea and adjacent parts of the Atlantic prey on leptocephali (Anguilliformes) was investigated. Most of the fishes examined (c. 95%) were collected using a commercial pelagical trawl. The stomach contents of about 1000 fishes (25 species of 10 families), mostly belonging to the suborders Myctophoidei, Stomiatoidei and the order Anguilliformes, were examined. The remains of invertebrates, mainly crustaceans, molluscs, tunicates, chaetognaths, and siphonophores were found in 28.8 % of the stomachs. Fishes, mostly myctophids or fish remains, were observed in 11.2 % of the stomachs; 18.7 % contained unidentified items and 40.6 % were empty. Leptocephali (Ariosoma spp. andGnathophis sp.) were found in the alimentary tract of 0.5 % of the fishes examined, exclusively represented by the myctophid,Ceratoscopelus warmingii. This report indicates that the Sargasso Sea population ofAnguilla leptocephali, economically the most important eel, is not seriously affected by predation of oceanic fish species considered in this study.     

Fine‐scale genetic diversity and landscape‐scale genetic structuring in three foundational bulrush species: implications for wetland revegetation

The appropriate sourcing of seeds for restoration is critical for establishing foundational plant species that support ecosystem functions and services. Genetic analyses of such species can yield insights into patterns of genetic diversity and structuring to inform seed collections. Here we document, for three foundational bulrush species, distinct genetic patterns to guide restoration of wetlands along the iconic Great Salt Lake, the largest lake in western North America. Specifically, Schoenoplectus acutus and Schoenoplectus americanus had moderate levels of site‐scale genet richness and relatively low genet richness levels within 1‐m² plots. These patterns contrast with Bolboschoenus maritimus, which had higher levels of site‐ and plot‐level genet richness, and has therefore likely experienced more recent seedling establishment. At the landscape scale, we found some evidence for genetic isolation of individuals at more remote sites (namely Fish Springs National Wildlife Refuge in the West Desert of Utah), but all species are relatively well dispersed over hundreds of kilometers, a pattern most likely to occur via avian dispersal. In our mechanistic dispersal assessment, we found abundant bulrush seeds present in waterfowl gizzards and those seeds germinated readily despite (or because of) partial digestion. Migratory waterfowl likely facilitate the broad dispersal of all species and may aid in bulrush establishment by breaking seed dormancy. These findings suggest that seeds for restoration should be collected within and among seed source sites to ensure a diverse restoration seed lot that does not disrupt gene flow patterns.     

Frugivory by the fish Brycon hilarii (Characidae) in western Brazil

Frugivory and seed dispersal have been poorly studied in Neotropical freshwater fishes. We studied frugivory and seed dispersal by the piraputanga fish (Brycon hilarii, Characidae) in the Formoso River, Bonito, western Brazil. We examined the stomach contents of 87 fish and found the diet of piraputanga consisted of 24% animal prey (arthropods, snails, and vertebrates), 31% seeds/fruits and 45% other plant material (algae/macrophytes/leaves/flowers). The piraputangas fed on 12 fruit species, and were considered as seed dispersers of eight species. Fruits with soft seeds larger than 10 mm were triturated, but all species with small seeds (e.g. Ficus, Psidium) and one species with large hard seed (Chrysophyllum gonocarpum) were dispersed. Piraputangas eat more fruits in the dry season just before the migration, but not during the spawning season. Fish length had a positive relation with the presence of fruits in their guts. The gallery forest of the Formoso River apparently does not have any plant species that depend exclusively on B. hilarii for seed dispersal because all fruit species are also dispersed by birds and mammals. Based on seed size and husk hardness of the riparian plant community of Formoso River, however, the piraputangas may potentially disperse at least 50% of the riparian fleshy fruit species and may be particularly important for long-distance dispersal. Therefore, overfishing or other anthropogenic disturbances to the populations of piraputanga may have negative consequences for the riparian forests in this region.     

Coyote and porcupine spread Russian olive seeds through endozoochory

Russian olive (Elaeagnus angustifolia) is an invasive tree that has spread throughout much of the western United States. The mode of seed dispersal occurs by hydrochory and possibly by birds. Seed dispersal by frugivorous mammals has not been investigated. Between 15 October and 4 November 2020, we walked through Russian olive windbreaks in western North Dakota, USA, and surveyed for mammal scat, and found 10 coyote (Canis latrans) and 54 porcupine (Erethizon dorsatum) scats that contained intact Russian olive seeds. We subsequently evaluated the viability, germination frequency, and time to germination of seeds ingested by coyote and porcupine relative to un-ingested control seeds harvested from trees at sites where we collected scat. Overall, Russian olive seeds that passed through mammal intestinal tracts had similar viability and equivalent (porcupine) or higher (coyote) germination frequency compared to controls. Additionally, coyote-ingested seeds germinated earlier (time to germination was low) than controls, but porcupine-ingested seeds were similar to controls. Thus, our data supports the idea that mammals may be agents of regional Russian olive seed dispersal.     

Frugivoría por Aves en un Paisaje Fragmentado: Consecuencias en la Dispersión de Semillas1

Few data exist on seed dispersal by frugivorous birds in fragmented landscapes, originating from tropical dry forests, in contrast to more abundant data from tropical rain forests. In this study, we assessed the effect of frugivorous birds in a fragmented landscape of Veracruz, Mexico, now occupied by remnant fragments of tropical semi‐deciduous forest and dry deciduous forest, grassland, and shrubby patches on sand dunes. We determined four characteristics related to seed dispersal by birds: the interacting species of plants and birds, the characteristics of these species, spatio‐temporal variation in the dispersal system, and the outcome of the process. During one year, we recorded 54 frugivorous bird species and 33 ornithochorous plant species, which engaged in 176 different bird‐plant species interactions. Similarity (Sorensen index) of frugivorous bird communities using different vegetation types was high (>70%), suggesting that many bird species used all of the vegetation types. In contrast, the similarity of ornithochorous plant communities among vegetation types commonly was low (<37%), suggesting that most plant species were restricted to particular sites in this landscape. At the landscape level, as well as for tropical deciduous forest, we detected a significant positive relationship (Spearman's correlation of rank coefficient >0.65, P <0.05) among richness per month of frugivorous birds and plant species bearing fleshy fruits. Seeds of many plant species previously detected in studies of seed rain at the site were eaten by birds during this study. Most seeds of zoochorous species, which are deposited in the dry and decidous tropical forests patches, are produced within these vegetation types (i.e., they are autochthonous species), whereas bird‐dispersed seeds arriving in grassland and shrubby patches are produced outside (i.e., allochthonous) and are mostly woody species. Birds are important seed dispersers among vegetation types in this landscape but they have different effects in each one. The four characteristics studied, as well as the landscape approach of this research, allowed us to detect spatial and temporal patterns that otherwise would have remained undetected.     

Seed dispersal by changing frugivore assemblages: a mechanistic test of global change effects

In the face of global change it is important to understand how changes in species abundance and richness can affect ecosystem functions. Here we modelled seed dispersal by animals in a fragmented secondary forest of the Cantabrian Range (northwestern Iberian Peninsula), simulating the activity of six frugivorous bird species when dispersing three species of fleshy‐fruited trees. We calculated the density and richness of seeds deposited across a forested landscape, as well as the density of seeds arriving to open areas. We 1) study the complementarity of functional traits of each species with frugivore assemblages varying in species compositions (i.e. abundance and richness of bird assemblages), 2) identify those bird species whose functional roles are not redundant, and 3) explore the response of seed dispersal to random losses and to two non‐random bird loss scenarios (i.e. overhunting and fewer individuals from migrant species). We found that simulations with the avian composition observed in the field (i.e. with uneven abundances of six bird species) led to values of seed dispersal higher to those emerging from four bird species equally abundant. The selective removal of dominant bird species led to significant decays in seed dispersal, suggesting non‐redundant roles of abundant bird species. Seed dispersal decays were stronger under non‐random than random scenarios of bird loss. In terms of seed density, the functional decays also differed between the scenarios of overhunting and reduced arrival of migrant birds, notably beyond 50% changes in bird species composition. Our results illustrate the need to integrate species composition (controlling for bird abundance and richness) and their sensitivity to disturbances when predicting the impact of global change on ecosystem functions.     

Seed dispersal of a fleshy-fruited invasive shrub is affected by changes in the frugivorous bird assemblage along an elevational gradient

Seed dispersal by birds constitutes an essential mechanism for ornithochorous exotic plants to successfully invade a new system. New biotic associations with native birds might facilitate the upward spread of exotic plants from the foothills into the high mountains. However, environmental changes associated with elevation are known to drive changes in bird assemblages, and it is not clear how elevation changes impact the seed dispersal service of ornithochorous invaders. We evaluated changes in frugivorous bird assemblages of one of the exotic shrubs (Cotoneaster franchetii, Rosaceae) with the broadest elevation range among woody invaders in the Córdoba Mountains (Argentina). We quantified frugivory interactions (including absolute and proportional fruit consumption by seed dispersers, pulp consumers, and seed predators) using 4-h observations of focal C. franchetii shrubs distributed across low-elevation, mid-elevation, and high-elevation sites (700, 1100, and 1800 m a.s.l., respectively; 15 individuals per elevational band and one site per elevation). Seed disperser richness was highest at the low- and mid-elevation sites (three species vs. one at the high-elevation site), but proportional and absolute fruit consumption of C. franchetii was highest at the high-elevation site (39.1%, 88 seeds at high-elevation and 7.7%, 20 seeds at low-elevation). The Chiguanco Thrush (Turdus chiguanco, Turdidae) was the only seed disperser species found at the highest elevation site. Fruit consumption by seed dispersers was positively related to their abundance and elevation. In a high mountain system, a single abundant generalist seed disperser, rather than a high richness of seed disperser species, can uphold an effective dispersal service for an invasive ornithochorous shrub. This pattern may facilitate the spread of such plants across higher elevational ranges, thereby promoting the invasion of other exotic ornithochorous plants into upper elevations.