Waterbirds as endozoochorous dispersers of aquatic organisms: a review of experimental evidence

It is commonly assumed that waterbirds act as dispersal vectors of aquatic organisms. In this paper we review experimental work focusing on the endozoochorous transport of propagules by waterbirds with the aim to determine what aspects of this mechanism have been investigated. We discuss (i) the main issues addressed in propagule feeding experiments, (ii) aspects of the gut structure that affect the retrieval, retention time and viability of propagules, and (iii) the importance of assessing propagule retention time in the gut. A total of 26 experimental studies exist, which represent a very low number when compared to studies of seed dispersal in terrestrial systems. The diversity of questions dealt with in these articles was low, with the majority focusing exclusively on whether propagules survive gut passage. More comparative studies involving batches of disperser and dispersed species should be carried out, also to establish whether they possess characteristics that favour endozoochorous transport. It is important to assess the effect of intra- and inter-specific variation in the different sections of the waterbird gut on the fate of propagules. Additionally, experimental work dealing with the mechanism of endozoochorous dispersal can be separated into a sequence of events. Each event is characterised by its own probability of occurrence. In most studies, complete data sets relating to every step of the process have not been collected. In order to quantify dispersal probabilities of propagules such data are necessary.     

Recent advances in the study of long-distance dispersal of aquatic invertebrates via birds

Although Darwin pioneered the study of long‐distance dispersal (LDD) of aquatic invertebrates via waterbirds, it remains in its infancy as a modern discipline. A handful of recent studies have quantified internal or external transport in the field, confirming that a variety of long‐distance migrants carry invertebrates both internally and externally. These studies show that variation in the morphology of vectors influences the frequency and size of propagules transported, and suggest that more invertebrate groups disperse via birds than was previously thought. Dispersal limitation has mainly been investigated for zooplankton in small experimental systems from which waterbirds were effectively excluded, and the extent of such limitation for invertebrate populations in wetlands interconnected by waterbird movements remains unclear. We expect that the spatial and temporal scales at which dispersal limitation constrains geographical ranges, species richness and genetic structure of invertebrates depends partly on the density of migratory birds using the area. Birds may have a major role in the expansion of exotic species. We propose several avenues for future research. There is a particular need for more quantitative studies of LDD by birds that will enable modellers to assess its role in maintaining invertebrate biodiversity among increasingly fragmented wetlands and in the face of climate change, as well as in the spread of invasive species.     

Passive internal transport of aquatic organisms by waterfowl in Doñana, south-west Spain

Aim Waterbirds may play an important role in the maintenance of aquatic ecosystem biodiversity by transporting plants and invertebrate propagules between different wetlands. The aim of this study is to provide the first quantitative analysis of the transport of plant and animal propagules by a community of waterbirds. Location Doñana marshes in south‐west Spain. Methods We quantified the number of intact seeds and invertebrate eggs in 386 faecal samples from 11 migratory waterfowl species (10 ducks and coot), collected from 3 November to 3 December 1998 (when birds were arriving from further north), and 22–25 February 1999 (when birds were leaving Doñana). Results Intact seeds of at least 7 plant genera, and invertebrate eggs (ephippia of at least 2 crustacea, statoblasts of at least 2 bryozoans and eggs of Corixidae) occurred in 65.6% of the faecal samples in early winter and 67.8% in late winter. Main conclusions The abundance of different propagule types varied between waterfowl species in a seasonal and species specific manner, probably owing to differences in foraging strategies, bill and gut morphology, and seasonal shifts in propagule availability or distribution. Lamellar density was positively correlated with the abundance of intact propagules. Our results confirm that waterfowl play an important role in the dispersal of organisms in aquatic environments by internal transport. Wherever there is a propagule bank accessible to waterbirds, transport can occur even when propagule production and waterfowl movements do not overlap in time.     

Do birds of a feather disperse plants together?

1. Dispersal of propagules by waterbirds is thought to be important for wetland plants because of the abundance of birds and their frequent movements among aquatic habitats. Differences in bird characteristics (size, movement, feeding ecology) were expected to lead to different outcomes for plant dispersal. 2. We investigated heterogeneity in plant dispersal by ducks (Anas superciliosa, Anas gracilis, Anas castanea). We calculated the probability of transport of viable seeds by germinating propagules retrieved from feathers and feet (epizoochory) and the contents of the oesophagus, gizzard and lower gut (endozoochory). 3. The abundance and richness of seeds carried internally and externally did not differ among sympatric bird species. We used estimates from the literature of movements of Anas species to approximate dispersal kernels for the transport of plant propagules. 4. Heterogeneity in the abundance and movement ecology of disperser species will result in differing patterns and degrees of connectivity for wetland plant metacommunities. Sedentary waterfowl are likely to have an important role in replenishing propagules and connecting aquatic metacommunities over small distances. Nomadic waterfowl may facilitate long‐distance dispersal. We discuss the implications of differences between duck species in movement patterns for connectivity of aquatic plant metacommunities across landscapes.     

Intercontinental long‐distance seed dispersal across the Mediterranean Basin explains population genetic structure of a bird‐dispersed shrub

Long‐distance dispersal (LDD) is a pivotal process for plants determining their range of distribution and promoting gene flow among distant populations. Most fleshy‐fruited species rely on frugivorous vertebrates to disperse their seeds across the landscape. While LDD events are difficult to record, a few ecological studies have shown that birds move a sizeable number of ingested seeds across geographic barriers, such as sea straits. The foraging movements of migrant frugivores across distant populations, including those separated by geographic barriers, creates a constant flow of propagules that in turn shapes the spatial distributions of the genetic variation in populations. Here, we have analysed the genetic diversity and structure of 74 populations of Pistacia lentiscus, a fleshy‐fruited shrub widely distributed in the Mediterranean Basin, to elucidate whether the Mediterranean Sea acts as a geographic barrier or alternatively whether migratory frugivorous birds promote gene flow among populations located on both sides of the sea. Our results show reduced genetic distances among populations, including intercontinental populations, and they show a significant genetic structure across an eastern‐western axis. These findings are consistent with known bird migratory routes that connect the European and African continents following a north‐southwards direction during the fruiting season of many fleshy‐fruited plants. Further, approximate Bayesian analysis failed to explain the observed patterns as a result of historical population migrations at the end of Last Glacial Maximum. Therefore, anthropic and/or climatic changes that would disrupt the migratory routes of frugivorous birds might have genetic consequences for the plant species they feed upon.     

Wind mediated dispersal of freshwater invertebrates in a rock pool metacommunity: differences in dispersal capacities and modes

Current evidence suggests regular overland transport of different freshwater invertebrates by wind, mainly over short distances. Yet, very little is known about the mechanism and scale of this process or about differences in wind dispersal dynamics and capacities among taxa and propagule types. We investigated wind dispersal of freshwater invertebrates in a cluster of temporary rock pools (spatial scale: 9,000 m²) in South Africa. Dispersing propagules and propagule bank fragments (i.e. aggregates of sediments and propagules) were intercepted during 1 month using a combination of windsocks (1.5 m above ground level) and sticky traps (ground level). The potential movement of propagule bank fragments (i.e. aggregates of propagules and sediments) was also simulated by tracking inter-pool movements of differently sized artificial substrate fragments similar to dry propagule bank fragments. We detected differences in the composition of dispersing communities intercepted at different altitudes (ground level and at 1.5 m). Comparison of dispersal distance distributions also revealed significant differences among taxa. Overall, larger propagule types (e.g. adult ostracods and oribatid mites) dominantly travelled near ground level while small resting eggs and cryptobiotic life stages of copepods were most frequently collected at higher altitudes (1.5 m) and dispersed over the longest distances. Finally, not only dispersal of single propagules but also ground level transport of propagule bank fragments was shown to contribute to local dispersal dynamics in temporary aquatic habitats.     

Dispersal of aquatic organisms by waterbirds: a review of past research and priorities for future studies

1. Inland wetlands constitute ecological islands of aquatic habitat often isolated by huge areas of non-suitable terrestrial habitats. Although most aquatic organisms lack the capacity to disperse by themselves to neighbouring catchments, many species present widespread distributions consistent with frequent dispersal by migratory waterbirds.
2. A literature review indicates that bird-mediated passive transport of propagules of aquatic invertebrates and plants is a frequent process in the field, at least at a local scale. Both endozoochory (internal transport) and ectozoochory (external transport) are important processes.
3. The characteristics of the dispersed and the disperser species that facilitate such transport remain largely uninvestigated, but a small propagule size tends to favour dispersal by both internal and external transport.
4. We review the information currently available on the processes of waterbird-mediated dispersal, establishing the limits of current knowledge and highlighting problems with research methods used in previous studies. We also identify studies required in the future to further our understanding of the role of such dispersal in aquatic ecology.     

Lichen colonization patterns show minor effects of dispersal distance at landscape scale

The role of dispersal in controlling the distribution of species at landscape scale (10²–10⁴ m) is still a matter of dispute. Here, we use the early colonization pattern of 23 epiphytic lichen species in a former tree‐less heathland landscape (170 km²) to test three hypotheses on how a landscape is colonized: A) mainly by long‐distance dispersal (LDD), B) by rare LDD events followed by limited local dispersal, and C) mainly by limited dispersal, resulting in a colonization front. The study system consisted of a chronosequence of 94 habitat patches constituting 0.4% of the landscape area, with a minimum inter‐site distance of 0.2 km. We used generalized linear mixed models with Bayesian inference to test predictions from the hypotheses. When age of sites and habitat area were accounted for, additional effects of geographical position of sites (distance from old sites, distance‐dependent relative propagule pressure, and distance from border of study area) on the probability of colonization by lichen species were small. Furthermore, species richness of sites did not depend on geographical position, either. Our results support a colonization process mainly governed by LDD at landscape scale, and that local stepwise colonization was not important. We argue that passively dispersed species with numerous small propagules tend to exhibit patchy populations with extensive dispersal at the landscape scale, rather than behaving like classical metapopulations.     

Retention time variability as a mechanism for animal mediated long-distance dispersal

Long-distance dispersal (LDD) events, although rare for most plant species, can strongly influence population and community dynamics. Animals function as a key biotic vector of seeds and thus, a mechanistic and quantitative understanding of how individual animal behaviors scale to dispersal patterns at different spatial scales is a question of critical importance from both basic and applied perspectives. Using a diffusion-theory based analytical approach for a wide range of animal movement and seed transportation patterns, we show that the scale (a measure of local dispersal) of the seed dispersal kernel increases with the organisms' rate of movement and mean seed retention time. We reveal that variations in seed retention time is a key determinant of various measures of LDD such as kurtosis (or shape) of the kernel, thinkness of tails and the absolute number of seeds falling beyond a threshold distance. Using empirical data sets of frugivores, we illustrate the importance of variability in retention times for predicting the key disperser species that influence LDD. Our study makes testable predictions linking animal movement behaviors and gut retention times to dispersal patterns and, more generally, highlights the potential importance of animal behavioral variability for the LDD of seeds.     

Biological Invasions Across Spatial Scales: Intercontinental, Regional, and Local Dispersal of Cladoceran Zooplankton

The frequency of dispersal of invertebrates among lakes depends upon perspective and spatial scale. Effective passive dispersal requires both the transport of propagules and the establishment of populations large enough to be detected. At a global scale, biogeographic patterns of cladoceran zooplankton species suggest that effective dispersal among continents was originally rare, but greatly increased in the past century with expanded commerce. Genetic analysis allows some reconstruction of past dispersal events. Allozyme and mitochondrial DNA comparisons among New World and Old-World populations of several exotic cladocerans have provided estimates for likely source populations of colonists, their dispersal corridors, and timing of earlier dispersal events. Detecting the Old-World tropical exotic Daphnia lumholtzi early in its invasion of North America has allowed detailed analysis of its spatial spread. Twelve years of collection records indicate a rapid invasion of reservoirs in the United States, by both regional spread and long-distance jumps to new regions. Combining landscape features with zooplankton surveys from south-central US reservoirs revealed higher colonization rates of D. lumholtzi at lower landscape positions, a result which can be explained by either greater propagule load or by higher susceptibility of these downstream reservoirs. Because invaded reservoirs provide a source of propagules for nearby floodplain ponds, the rarity of this species in ponds suggests limitation by local environments. Such analyses of invading species over multiple spatial scales allow a better understanding of ecological processes governing invasion dynamics.     

Variations in the dispersal curves of macroalgal propagules from a source

The process of dispersal is critical to marine benthic species (i.e. invertebrates and algae) as a fundamental element of population ecology and a crucial ecological process that maintains the diversity in communities. We simultaneously sampled the abundance of spores inhabiting the water column at different distances from known parent sources at 3 sites along the coast of central Chile. From these data we constructed 258 dispersal curves for common rocky intertidal macroalgae. Only 43.8% of these curves could be predicted by the expected model, which describes the spatial distribution of propagules to be dominated by a larger concentration near the parent individual or “source site”, followed by a marked decrease in abundance with increasing distance. The curves that departed from the expected model (56.2%) were grouped into three curve types, according to the number of propagule abundance maxima observed in space. This work suggests that macroalgal propagule dispersal patterns are more variable than previously thought. The existence of several alternative curves to the expected model, as well as the presence of one to several abundance maxima associated with the differential distribution of propagule patches in the water column, suggests the idea that propagules are released in pulses which can be transported variable distances from the source site.     

Propagule dispersal and the scales of marine community process

Benthic marine organisms are characterized by a bipartite life history in which populations of sedentary adults are connected by oceanic transport of planktonic propagules. In contrast with the terrestrial case, where ‘long distance dispersal’ (LDD) has traditionally been viewed as a process involving rare events, this creates the possibility for large numbers of offspring to travel far relative to the spatial scale of adult populations. As a result, the concept of LDD must be examined carefully when applied in a marine context. Any measure of LDD requires reference to an explicit ‘local’ scale, often defined in terms of adult population demography, habitat patchiness, or the average dispersal distance. Terms such as ‘open’ and ‘closed’ are relative, and should be used with caution, especially when compared across different taxa and systems. We use recently synthesized data on marine propagule dispersal potential and the spread of marine invasive species to draw inferences about average and maximum effective dispersal distances for marine taxa. Foremost, our results indicate that dispersal occurs at a wide range of scales in marine communities. The nonrandom distribution of these scales among community members has implications for marine community dynamics, and for the implementation of marine conservation efforts. Second, in agreement with theoretical results, our data illustrate that average and extreme dispersal scales do not necessarily covary. This further confounds simple classifications of ‘short’ and ‘long’ dispersers, because different ecological processes (e.g. range expansion vs. population replenishment) depend on different aspects of the dispersal pattern (e.g. extremes vs. average). Our findings argue for a more rigorous quantitative view of scale in the study of marine dispersal processes, where relative terms such as ‘short’ and ‘long’, ‘open’ and ‘closed’, ‘retained’ and ‘exported’ are defined only in conjunction with explicit definitions of the scale and process of interest. This shift in perspective represents an important step towards unifying theoretical and empirical studies of dispersal processes in marine and terrestrial systems.     

Propagule morphology and river characteristics shape secondary water dispersal in tree species

Plant migration is a multi-stage process often driven by multiple dispersal vector systems. Water-mediated dispersal (hydrochory) is known to move propagules of nonaquatic species over long distances, but whether propagule morphology affects floating processes is an open question. We used a multi-species approach to assess the role of propagule morphology in the dispersal of primarily wind-dispersed tree species in different urban rivers; the impact of hydraulic structures (locks, spillways) on floating was also considered. We released tagged propagules of eight tree species (Acer platanoides, Acer negundo, Acer saccharinum, Ailanthus altissima, Fraxinus excelsior, Robinia pseudoacacia, Tilia platyphyllos, Ulmus glabra) in the main lowland Spree River and in the small tributary Panke River (Berlin, Germany) and directly observed the fate of the floating propagules over river sections of 1,200 m. Our results demonstrate the following: (1) Water is an effective dispersal agent for wind-dispersed tree species, extending typical wind-related transport distances by several times. (2) Interspecific differences in transport distances reflect propagule characteristics (dry weight, maximum wing width) and river system. (3) Propagule morphology also affects deposition patterns as it was generally the large propagules that were trapped along semi-natural embankments in slow flow areas. (4) Hydraulic structures hampered but did not entirely stop water-mediated dispersal and diminished the effects of propagule morphology on floating processes. These results provide novel insights into the functioning of hydrochory as an important dispersal vector of tree species in river systems and as a driver of plant invasions.     

Overseas seed dispersal by migratory birds

Long-distance dispersal (LDD) promotes the colonization of isolated and remote habitats, and thus it has been proposed as a mechanism for explaining the distributions of many species. Birds are key LDD vectors for many sessile organisms such as plants, yet LDD beyond local and regional scales has never been directly observed nor quantified. By sampling birds caught while in migratory flight by GPS-tracked wild falcons, we show that migratory birds transport seeds over hundreds of kilometres and mediate dispersal from mainland to oceanic islands. Up to 1.2% of birds that reached a small island of the Canary Archipelago (Alegranza) during their migration from Europe to Sub-Saharan Africa carried seeds in their guts. The billions of birds making seasonal migrations each year may then transport millions of seeds. None of the plant species transported by the birds occurs in Alegranza and most do not occur on nearby Canary Islands, providing a direct example of the importance of environmental filters in hampering successful colonization by immigrant species. The constant propagule pressure generated by these LDD events might, nevertheless, explain the colonization of some islands. Hence, migratory birds can mediate rapid range expansion or shifts of many plant taxa and determine their distribution.     

Vector activity and propagule size affect dispersal potential by vertebrates

Many small organisms in various life stages can be transported in the digestive system of larger vertebrates, a process known as endozoochory. Potential dispersal distances of these "propagules" are generally calculated after monitoring retrieval in experiments with resting vector animals. We argue that vectors in natural situations will be actively moving during effective transport rather than resting. We here test for the first time how physical activity of a vector animal might affect its dispersal efficiency. We compared digestive characteristics between swimming, wading (i.e. resting in water) and isolation (i.e. resting in a cage) mallards (Anas platyrhynchos). We fed plastic markers and aquatic gastropods, and monitored retrieval and survival of these propagules in the droppings over 24?h. Over a period of 5?h of swimming, mallards excreted 1.5 times more markers than when wading and 2.3 times more markers than isolation birds, the pattern being reversed over the subsequent period of monitoring where all birds were resting. Retention times of markers were shortened for approximately 1?h for swimming, and 0.5?h for wading birds. Shorter retention times imply higher survival of propagules at increased vector activity. However, digestive intensity measured directly by retrieval of snail shells was not a straightforward function of level of activity. Increased marker size had a negative effect on discharge rate. Our experiment indicates that previous estimates of propagule dispersal distances based on resting animals are overestimated, while propagule survival seems underestimated. These findings have implications for the dispersal of invasive species, meta-population structures and long distance colonization events.     

Not across the North Pole: plant migration in the Arctic

? The vascular plant flora of 66 arctic islands was studied to determine whether the islands have been occupied by random long-distance dispersal (LDD) or in a highly structured northward migration pattern via intervening islands as stepping-stones. ? A maximum parsimonious migration model minimizing dispersal distances of 1256 vascular plant taxa was calculated in the framework of network analysis. ? Plant dispersal is not stochastic in the Arctic at the global scale. Inferred mean dispersal distances of the plants occurring on arctic islands are c. 580 km (median 460 km). A LDD across the North Pole could not be inferred in the model and species may be recruited mainly from the nearest mainland or islands. At smaller scales, among adjacent islands, dispersal of vascular plants may be incomplete. Arctic islands do not yet appearto be saturated with species. ? The results suggest that changes in biodiversity in Arctic islands can be more easily predicted at the global scale than at the local scale. Because islands are not yet saturated with species, new colonizations may not necessarily be linked to climate change.     

A method for the direct detection of airborne dispersal in lichens

This study sets out a novel method to determine dispersal distances in lichens. Direct measurement of dispersal often remains difficult for lichens and other small inconspicuous species because of the need to track microscopic reproductive propagules, which even if they can be captured, cannot be identified using traditional morphological approaches. A low‐cost device (<£200) was developed to trap the reproductive propagules of lichens, capable of sampling around 0.1 m³ of air per minute. In parallel, molecular techniques were developed to enable species‐specific detection of propagules caught by the devices, with identification using novel species‐specific primers and optimization of a standard DNA extraction and nested PCR protocol. The methods were tested for both their sensitivity and specificity against a suite of lichen epiphytes, differing in their reproductive mechanisms, dispersal structures and rarity. Sensitivity tests showed that the molecular techniques could detect a single asexual propagule (soredium or isidium), or as few as 10 sexual spores. As proof of concept, propagule traps were deployed into a wooded landscape where the target epiphytes were present. Extractions from deployed propagule traps were sequenced, showing that the method was able to detect the presence of the target species in the atmosphere. As far as we are aware, this is the first attempt to use mechanized propagule traps in combination with DNA diagnostics to detect dispersal of lichens. The tests carried out here point the way for future dispersal studies of lichen epiphytes and other passively dispersed microscopic organisms including fungi or bryophytes.     

The importance of long-distance dispersal in biodiversity conservation

Dispersal is universally considered important for biodiversity conservation. However, the significance of long‐ as opposed to short‐distance dispersal is insufficiently recognized in the conservation context. Long‐distance dispersal (LDD) events, although typically rare, are crucial to population spread and to maintenance of genetic connectivity. The main threats to global biodiversity involve excessive LDD of elements alien to ecosystems and insufficient dispersal of native species, for example, because of habitat fragmentation. In this paper, we attempt to bridge the gap in the treatment of LDD by reviewing the conservation issues for which LDD is most important. We then demonstrate how taking LDD into consideration can improve conservation management decisions.     

Experiments on adhesive dispersal by wood mouse: seed shadows and dispersal distances of 13 plant species from cultivated areas in southern Sweden

This study on epizoochory offers experimental data on retention times and potential dispersal distances of propagules of 13 plant species that commonly inhabit cultivated areas in the south of Sweden. Wood mouse Apodemus flavicollis was used as dispersal vector. Seven of the investigated species produce fruits that carry obvious hooks, barbs or bristles and for comparison the remaining six species, lacking such features, were also included. Excised fruits that initially carried appendages were used in a complementary comparison. Propagules were applied by hand to the back of the animals, which were which released in enclosures to move about freely. Observations were made continually until the seeds were dropped. The distance covered by the animals while moving was measured and the potential dispersal distances calculated. Small fruits were in general found to be more efficiently transported than large ones, but large propagules carrying appendages sometimes remained in place for considerable periods. The potential dispersal distances ranged up to nearly 30 m. The retention time was significantly enhanced by the presence of dispersal attributes. The behavioural pattern of the animals (grooming, movements) plays a significant part in the successful transportation of propagules. By comparing the result with similar experiments using fallow deer Dama dama and domestic cattle Bos taurus as dispersal vectors it can be stated that mice are surprisingly effective as seed dispersers. Large mammals disperse propagules on a larger scale (<1 km) compared with small mammals, that affect plant distribution more locally (<100 m). We consider adhesive dispersal a most significant component in plant metapopulation dynamics, considerably enhancing the probability of occasional propagules reaching suitable sites in a fragmented landscape.     

The dispersal capacity of vegetative propagules of riparian fen species

Flowing water can disperse a high number of seeds and vegetative propagules over long distances and is therefore a very important dispersal vector in wetland habitats. Although the dispersal of seeds is relatively well studied, the dispersal of vegetative propagules has received less attention. However, in riparian and aquatic systems where many species have clonal growth forms, it can be very important. The relative importance of vegetative propagules in the dispersal of fen species was assessed first by determining their relative abundance in the field and second, by determining the buoyancy of plant fragments of ten fen species experimentally. On average, vegetative propagules made up 3.2–58.9% of the total propagule number (mainly Elodea nutallii). Buoyancy of the tested species ranged from 25 days to over 6 months. Surprisingly, the propagules of Stratiotes aloides and Hydrocharis morsus-ranae increased buoyancy when spring started (after ca. 100 days). The results demonstrate that vegetative propagules of riparian and aquatic fen species have a high capacity to disperse over long distances via water and are therefore likely to play an important role in the colonisation of new habitats. Especially because in nine out of the ten species tested, over 50% of the propagules were still viable after 6 months of floating.