Endozoochorous Dispersal Research Articles

The dispersal of vascular plants in a forest mosaic by a guild of mammalian herbivores

Endozochorous seed dispersal by herbivores can affect plant spatial dynamics and macroecological patterns. We have investigated the number and species composition of viable seeds deposited in faeces of a full guild of macroherbivores (four deer and two lagomorph species) in a forest in eastern Britain. One hundred and one plant species germinated from faecal pellet material, 85 of which were among the 247 vascular plant species recorded in the forest. However, three species - Chenopodium album, Urtica dioica and Agrostis stolonifera - comprised 56% of the seedlings recorded. Of the species recorded in faecal samples, 36% had no recognised dispersal mechanism, while very few (7%) were adapted to endozoochorous dispersal (fleshy fruit or nut). The number of species dispersed by the herbivores was ranked Cervus elaphus and Dama dama (96) > Capreolus capreolus (40) > Muntiacus reevesi (31) > Oryctolagus cuniculus (21) > Lepus europaeus (19), with the other taxa dispersing subsets of those dispersed by C. elpahus and D. dama. The invasive M. reevesi deposited the fewest seeds per gram of faecal pellet material (0.4 g(-1)) and hence fewer seeds per unit area than other deer species despite their numerical dominance, while C. elaphus/D. dama deposited the most (0.43 seeds m(-2) year(-1)). Due to differences in faecal seed density among habitats combined with the ranging behaviour of animals, more seeds were deposited in younger stands, enhancing the potential contribution of macroherbivores to population persistence by dispersal and colonisation in a successional mosaic.

Consequences of intraspecific seed‐size variation in Sparganium emersum for dispersal by fish

Summary The potential for seed dispersal by fish (ichthyochory) is likely to vary within aquatic plant species, depending on intraspecific variation in phenotypic seed traits. We studied the effect of seed size variation within the unbranched burreed (Sparganium emersum) on the potential for internal dispersal by the common carp (Cyprinus carpio), by feeding them light (< 10 mg), medium (10–20 mg) and heavy ( > 20 mg) seeds, seed mass being positively related to seed size. We hypothesized: (i) that ingestion, retention time, survival during gut passage and viability after gut passage of S. emersum seeds would be affected by seed size; and (ii) that this would translate into intraspecific variation in dispersal probability and dispersal distance among seed size categories. Ingestion was negatively related to seed size, while survival during gut passage was positively related to seed size. Seed viability after gut passage was not affected by seed size. Since the negative effect of ingestion was counterbalanced by an equally strong but positive effect on seed survival, the probability of dispersal did not differ between the tested seed‐size categories. The time that seeds remained in the digestive tract of carp did not differ between seed sizes, suggesting equal potential dispersal distances for all seeds. Based on optimum swimming speeds of carp, ranging from 0·9 to 1·8 km h−1, maximum dispersal distances will most likely range from 13·5 to 27 km. This study highlights the importance of studying all stages of the endozoochorous dispersal process in order to estimate the effect of a phenotypic seed trait on plant dispersal.

Endozoochorous dispersal, seedling emergence and fruiting success in disturbed and undisturbed successional stages of sheep-grazed inland sand ecosystems

This study examines the seedling emergence and fruiting success of plant species endozoochorously dispersed by sheep in a field experiment in a Koelerion glaucae area. We designed a factorial experiment (faeces/soil disturbance/successional stage/year) that mimics sheep-mediated microsites and analysed all occurring vascular plant species from September 2002–December 2004. The faeces samples were collected in the same ecosystem and additionally analysed in a common-garden experiment (seedling emergence potential). According to the latter, 28 vascular plant taxa were identified (on average 124 seedlings per 100 g air-dry sheep faeces). In the field, 15 species emerged directly out of faeces, only five of which were able to set seeds (the threatened species Medicago minima, Phleum arenarium, Silene conica, Vicia lathyroides and the non-threatened Vulpia myuros). Graminoid competitors were not able to set seedlings in the field but did so in the common-garden experiment (mainly Carex hirta). The total numbers of seedlings emerging out of faeces (5% of the potential) and reaching fruit ripeness (0.4%) were very low. In the stage of seedling emergence, ten of 42 species were significantly influenced by faeces, 11 species by disturbance and two species by an interaction of the two treatment factors ( Bromus tectorum, Saxifraga tridactylites). In the fruiting stage, two species profited by faeces ( Bromus tectorum, Vulpia myuros) and two species by disturbance ( Erophila verna, Corynephorus canescens). Overall, the density and diversity of fruiting individuals were significantly influenced by both treatment factors. The faeces factor showed a strong dependence on year (increasing effect on both dependent variables in the first year, decreasing effect in the second year). The disturbance factor is dependent particularly on successional stage (increasing effect especially in the later successional stage). Our study revealed the paradox that threatened species with low nutrient demands are the most successful direct colonisers of sheep-faeces deposits. For them to reach the fruiting stage is rare but is of importance if new habitats are to be made accessible.

The Contribution of Endozoochory to the Colonization and Vegetation Composition of Recently Formed Sand Coastal Dunes

The objective of this study was to determine whether endozoochory contributes to the dispersal and colonization of plant species in recently formed coastal dunes. At least 5.7% of species present in the study area are being dispersed by wild rabbits (Oryctolagus cuniculusL.). Most dispersed species are perennial herbs with small seeds size. The continuous input of seeds through rabbit feces into newly created areas would ensure the constant arrival of seeds and would facilitate colonization. Therefore, endozoochorous dispersal may play a relevant role for the structure and composition of dune plant communities.

Survival and germination of Mediterranean grassland species after simulated sheep ingestion: ecological correlates with seed traits

Abstract Large amounts of viable seeds from Mediterranean grassland species have been found in herbivore dung; however which species produce seeds that can survive and germinate after ingestion by herbivores is still not well understood. This paper evaluates the importance of seed size, shape and coat impermeability in the endozoochorous dispersal process of 20 abundant species from central Iberian rangelands. Seed survival, germination percentages and germination speed were analysed in controlled experiments on the chewing and gut passage process by inserting seeds in the rumen of fistulated sheep, followed by simulated acid–pepsin digestion. Higher germination percentages in the control than the simulated sheep ingestion treatment were found in 75% of seeds. All species showed lower survival following the treatment, two species had a higher germination speed and five had a lower rate. Large-seeded species generally had higher survival percentages than small-seeded species. Species with impermeable seed coats had higher germination percentages following treatment although no significant differences were noted for either seed survival or germination speed.

Endozoochorous dispersal of aquatic plants: does seed gut passage affect plant performance?

The ingestion of seeds by vertebrates can affect the germinability and/or germination rate of seeds. It is, however, unclear if an earlier germination as a result of ingestion affects later plant performance. For sago pondweed, Potamogeton pectinatus, the effects of seed ingestion by ducks on both germinability and germination rate have been previously reported from laboratory experiments. We performed an experiment to determine the effects of seed ingestion by ducks on germination, seedling survival, plant growth and asexual multiplication. Both at the start and end of the winter, seeds were fed to three captive shovelers (Anas clypeata) and planted outdoors in water-filled containers. Plant biomass and its allocation to vegetative parts (shoot and roots), tubers, and seeds were determined in autumn. More duck-ingested seeds than control (uningested) seeds germinated in early winter, but this difference disappeared for seeds planted in late winter, when the treatments were first stratified for 3 mo. None of the variables for measuring seedling survival and plant performance varied between treatments. Under our experimental conditions (no herbivory or competition), ingestion by ducks in early winter resulted in increased performance for seeds surviving gut passage due to enhanced seed germinability, without other costs or benefits for the seedlings.

Dispersal of vascular plants by game in northern Germany. Part II: Red deer (Cervus elaphus)

The endozoochorous dispersal of vascular plant species by red deer (Cervus elaphus) was investigated in three forest areas of Schleswig-Holstein and Lower Saxony. The primary aim of this study was to determine of which plant species and in what numbers diaspores are dispersed by red deer, an animal with eminently large home ranges during a single day as well as over the year. A second aim was to examine the significance of endozoochory for plant species composition and diversity in forests. Special emphasis was placed on whether there are differences between the three study sites and in the course of the vegetation period. Freshly deposited faecal pellet groups were collected in the forests on five dates between May and November 2002 and viable seed content was determined by greenhouse germination (seedling emergence method). A total of 28,009 individuals representing 59 vascular plant species were detected in 220 dung samples. Red deer appears thus as an important vector for endozoochorous dispersal of plants. The number of seedlings found in the faecal pellets differs between plant species and research areas as well as in the course of the vegetation period. Dung seed content is largely dominated by one species, Urtica dioica. Grouping the species found in dung according to their habitat preference showed that mainly species that occur in forests as well as in open vegetation and non-forest species were dispersed endozoochorously, while species occurring mainly under a closed canopy were present in the excrements only in low numbers.

Differences in endozoochorous dispersal between aquatic plant species, with reference to plant population persistence in rivers

Summary 1. In river ecosystems, populations are continuously subjected to unidirectional downstream currents resulting in a downstream movement of populations. To ensure long‐term population persistence in rivers, organisms must have a mechanism for upstream dispersal, which allows them to re‐colonise upstream areas.2. In this study we assessed differences in the potential for endozoochorous seed dispersal of Sparganium emersum and Sagittaria sagittifolia, two aquatic plant species with different seed morphologies, by mallard (Anas platyrhynchos) and teal (Anas crecca), two duck species with different body weights.3. We found no significant differences in seed retrieval (the proportion of ingested seeds retrieved after gut passage) and seed retention time (time between seed ingestion and retrieval), between mallard and teal, despite the difference in body weights. We did find a significantly higher germination (%) over retention time of S. emersum seeds retrieved from teal compared with mallard, most likely related to a more efficient removal of the seed coat during passage through the gut of teal.4. There were large differences between S. emersum versus S. sagittifolia in: (i) seed retrieval (22.65 ± 20.8% versus 1.60 ± 2.4%, respectively); (ii) seed retention time in duck gut, with a maximum of 60 h versus 12 h; (iii) the effect of gut passage on seed germination, with an increase of approximately 35% versus a decrease of 25%; and (iv) the effect of gut passage on seed germination rate, with an acceleration of 10 days versus a delay of 3 days on average. The results show that S. emersum has a higher potential for endozoochorous dispersal by ducks and postdispersal establishment than S. sagittifolia.5. We propose that, in rivers, bird‐mediated seed dispersal may promote re‐colonisation of upstream areas, enabling long‐term plant population persistence.

Gourmets or gourmands?—Diet selection by large ungulates in high-alpine plant communities and possible impacts on plant propagation

Summary Megaherbivores have a considerable impact on species composition and structure of natural plant assemblages at the alpine/nival ecotone of the Alps, but their role as dispersal vectors has scarcely been investigated. This study examined the diet selection of free-ranging ungulates on high-alpine swards with special focus on their potential for endozoochoric dispersal. Grazed areas and fenced control plots were investigated by a point-framing method. Results show that the foraging behaviour of ungulates in high-alpine swards is selective. Flowers and fruits are preferred to leaves. Accordingly, an increase in long-distance dispersal events of alpine vascular plants by grazing ungulates can be predicted. Preferential feeding on the conspicuous flowers of herbs rather than on graminoid inflorescences causes a more pronounced reduction of seed numbers in herbs. We therefore suppose the enhancement of long-distance dispersal to be higher for graminoids. The impact of herbivores on plant migration processes must therefore be considered when changes in alpine plant assemblages are to be assessed.

Endozoochory by ducks: influence of developmental stage of Bythotrephes diapause eggs on dispersal probability

Abstract. This paper evaluates whether the recent expansion of Bythotrephes longimanus Leydig (Crustacea: Onychopoda) may be a result of endozoochorous avian dispersal. In three experiments, we investigated the survival of diapause eggs in newly produced and end‐of‐winter developmental stages after their passage through the digestive tract of four species of ducks. Resistance of eggs to digestion was low for both developmental stages (< 12%). Most eggs (67–95%) were recovered by four hours after ingestion, with a longer maximum retention time for newly produced (22 h) than end‐of‐winter eggs (4–6 h). Ingestion had a detrimental effect on viability: only eggs retrieved one hour after ingestion hatched and the proportion of those ingested that produced viable neonates was low (0.5% for newly produced and 0.3–3% for end‐of‐winter eggs). We conclude that the probability of endozoochorous dispersal by individual ducks is low but becomes significant when considering the thousands of ducks moving among wetlands. Endozoochorous dispersal of B. longimanus would most likely involve the transport of newly produced diapause eggs from north to south, during the autumn migration of ducks. Based on flight speed estimates of ducks we estimate dispersal probability to drop sharply at distances over 60–80 km.

How far can the freshwater bryozoan Cristatella mucedo disperse in duck guts?

Statoblasts of Cristatella mucedo were fed to two duck species, pintail (Anas acuta) and shoveler ( A. clypeata), to assess whether endozoochorous dispersal is responsible for the metapopulation structure of this bryozoan. Eight individuals (four per duck species) were force-fed 500 statoblasts each. The number of intact sta- toblasts retrieved from the ducks faeces up to 48 hours after ingestion and their reten- tion times, i.e. the time spent in the gut from ingestion to defecation, were recorded. Retrieval of intact statoblasts did not differ significantly between duck species (37 ± 29% for pintail and 13 ± 21% for shoveler, average ± SE) and the pattern of retrieval over time was identical. Most statoblasts (79- 96% for pintail and 51- 96% for shove- ler) were recovered during the first four hours after ingestion. Maximum retention times were 44 hours for pintail and 32 hours for shoveler. A few statoblasts retrieved two hours following gut passage germinated, but none in the control group did. We provide evidence that the potential for waterfowl dispersal of C. mucedo statoblasts is higher for short distances up to 300 kilometres, but still possible over longer distances.

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.

Long-distance endozoochorous dispersal of submerged macrophyte seeds by migratory waterbirds in northern Europe—a critical review of possibilities and limitations

We review whether migratory Anatidae, i.e., swans, geese and ducks, could be acting as vectors for dispersal of Zostera , Ruppia and Potamogeton propagules by endozoochory (carrying seeds in their guts). We list six prerequisites that must all be fulfilled, if successful dispersal should occur. Several Anatidae species feed on these macrophytes, and undertake rapid long-distance movements, making dispersal possible. We identify four problems, which in combination leads us to conclude that long-distance dispersal events are likely to be rare. (i) Most long-distance movements are out of phase with the reproductive efforts of the plants, and if birds arrive at sites when plants still bear seeds, they are likely to depart well after seed stocks have been depleted. (ii) Seed transport by birds will usually be uni-directional, from north to south on autumn migrations. (iii) Most of the gut contents of migratory birds are likely to have been discarded within 300 km of departure. (iv) In many cases, birds will arrive in habitats seriously different from those they departed, i.e., any seeds carried along will have low chances of surviving in their new site. We suggest that northbound dispersal by endozoochory can only occur during spring if waterbirds feed on seeds that have not been depleted and remained frozen down or buried in sediments, or during moult- or post-moult migrations. Moult migration takes place in summer in phase with the reproductive efforts of the plants. Also epizoochorous dispersal (external attachment) is subject to restrictions i, ii and iv.

The importance of seed dispersal in the Alexandria Coastal Dunefield, South Africa

The endozoochorous dispersal of seeds by mammals and birds between distinct vegetation communities was assessed to determine the importance of these processes in coastal dune field management. Isolated pockets of thicket vegetation (bush-pockets) within a large coastal dune field provided the opportunity to study vertebrate seed dispersal and its contribution to their origin and maintenance. Mammalian and avian faeces were collected for the quantification of seeds dispersed via endozoochory. Birds and mammals showed considerable overlap, dispersing intact seeds of 17 and 29 plant species, respectively, but mammals dispersed a greater diversity and size range than birds. Extrapolation of mammalian faecal data indicates an annual input of 23 million intact seeds to the dune field. Significantly more seeds are deposited by mammals and birds in the bush-pockets than on open sand, and birds deposited greater numbers of seeds nearer the seed source. Zoochory appears to be critical for the maintenance of the bush-pocket habitats through the dispersal of climax woody plant species into the dune field. Directional dispersal by birds and mammals to the bush-pockets is considered to be responsible for the maintenance and possible origin of these bush-pockets. The high number of exotic plant propagules dispersed by both avian and mammalian zoochory highlights the importance of management of the Alexandria Coastal Dunefield (ACD) beyond the reserve boundaries. In a dynamic system such as the ACD which is within a declared nature reserve, the continued existence of the bush-pockets may depend on the maintenance, beyond the reserve boundaries, of a reservoir of not only plant material but vertebrate dispersers as well.

RAPD variation and population genetic structure in Prunus mahaleb (Rosaceae), an animal-dispersed tree.

We examined the patterns of random amplified polymorphic DNA (RAPD) variation among seven Prunus mahaleb (Rosaceae) populations extending over approximately 100 km2 to examine local differentiation in relation to spatial isolation due to both geographical distance and differences in elevation. No less than 51. 4% of the RAPD loci were polymorphic, but very few were fixed and among-population variation accounted for 16.46% of variation in RAPD patterns. Mean gene diversity was 0.1441, with mean Nei's genetic diversity for individual populations ranging between 0.089 and 0.149. Mean GST value across loci was 0.1935 (range, 0.0162-0.4685), giving an average estimate for Nm of 1.191. These results suggest extensive gene flow among populations, but higher GST and lower Nm values relative to other outcrossing, woody species with endozoochorous dispersal, also suggest a process of isolation by distance. The combined effect of both geographical and elevation distances and nonoverlapping flowering and fruiting phenophases on the GST matrix was partially significant, revealing only marginal isolation of the P. mahaleb populations. The matrix correlation between estimated Nm values among populations and the geographical + elevation distance matrices (r = -0.4623, P = 0.07), suggests a marginal trend for more isolated populations to exchange less immigrants. Long-distance seed dispersal by efficient medium-sized frugivorous birds and mammals is most likely associated to the high levels of within-population genetic diversity. However, vicariance factors and demographic bottlenecks (high postdispersal seed and seedling mortality) explain comparatively high levels of local differentiation.

Dormancy and endozoochorous dispersal ofOpuntia rastreraseeds in the southern Chihuahuan Desert

Seed dormancy and endozoochorous dispersal have important effects on population dynamics, i.e. seed bank formation, spatial and temporal bet-hedging, avoidance of crowding and decreased sib-competition. Seeds having primary dormancy do not germinate, even if adequate environmental and dispersal conditions are met, until an after-ripening period is completed. This study examined the effects on germination rates of seed dispersal by vertebrates and primary dormancy (i.e. how germination rates changed in time) in the prickly pearOpuntia rastrerafrom the southern Chihuahuan Desert. Ripe fruits, scats of coyote, mule deer, woodrat, common pig and pellets of the northern raven were collected in 1992 during the ripe fruit peak (August). A factorial design was used to assess the effect of disperser and seed age on germination rates using these seeds collected in 1992. In 1992, 1993 and 1994 (fresh, 1- and 2-year-old seeds, respectively) germination success after 3 months was determined for 100 seeds of each disperser, plus a control of uneaten seeds. We found differences in germination rates both between dispersers and years. All but one disperser (deer) decreased germination rates with respect to the control. Germination steadily increased with ageing of seeds, implying the presence of primary dormancy (embryo immaturity). Our results show that despite the large disperser coterie associated withOpuntia rastrera, seeds have an obligate primary dormancy which seems to result in seed bank formation. Seed germination and seedling establishment will depend on selection pressures caused mainly by environmental variability in deserts (unpredictable rainfall, extreme temperatures, safe-site availability). Nevertheless, endozoochorous dispersal provides some additional advantages (e.g. habitat colonization, genetic variability, avoidance of long-term local extinction) that needs further research.

New Insights Into Pasture Diversity: The Consequences of Seed Dispersal in Herbivore Dung

The dispersal of herbaceous species seeds through herbivorous mammal dung (endozoochory) has been known for some time, although its effect on the grazed communities has not been analyzed in depth. In a Mediterranean grassland, we have found that large quantities of seeds are dispersed in rabbit droppings (Oryctolagus cuniculus L.), with significant effects on the composition and structure of the soil seed reserves. Endozoochorous dispersal encourages the spread of species which lack morphological structures for dissemination, and favours the small-scale spatial diversification of the pasture through the spatial variability of dunging. On a larger scale, however, endozoochory plays a homogenizing role in the plant community through long-distance seed dissemination.

Establishment of pasture species on cattle dung: the role of endozoochorous seeds

Abstract. The process of colonization of cattle dung patches and its relation to endozoochorous dispersal is analysed in a Mediterranean pasture. Dung pats dropped in spring and winter were marked, and the vegetation developing on them during the first two years of colonization was followed. The influence of endozoochorous seeds on dung colonization is assessed through the study of: (1) the vegetation on spring and winter dung pats and the seed contents of both, which is abundant in the former and negligible in the latter; and (2) the vegetation on spring dung pats compared with that of the surrounding pasture. The origin of plants growing on dung (either seeds in the manure or in the soil seed bank) was traced by studying dung colonization under controlled conditions in pots with manure put on seed‐free sand, and on pasture turf. The results indicate that endozoochorous seeds germinate in manure; they are the main source of recovery in gaps generated by dung pats. The micro‐succession involved is independent of the type of pasture. A small‐scale spatial pattern results in which gaps of old dung are dominated by endozoochorous species. Thus, dung patches enhance the similarity between grazed communities, and the variation within communities.

Seed bank build‐up in small disturbances in a Mediterranean pasture: the contribution of endozoochorous dispersal by rabbits

The importance of endozoochorous dispersal in seed bank build‐up is analyzed in artificial 40 x 40 cm disturbances in a Mediterranean pasture The top 10 cm of soil in the disturbances was replaced by sterile soil, and the excrement laid m half of them was removed fortnightly The seed banks of the disturbances subjected to the two treatments was quantified by germination of soil samples (n = 44) gathered at the start of the following growth season Rabbit droppings were collected fortnightly to quantify their seed content and the pasture seed production was estimated Seed bank regeneration takes place early in the disturbances The main source of qualitative variation in seed banks is their position on the slope, while endozoochory lacks a characteristic qualitative effect However, endozoochorous dispersal is responsible for a significant increase in the number of germinable seeds, the richness and diversity of the seed bank samples with respect to those lacking it The importance of endozoochorous dispersal by rabbits in grassland dynamics is suggested to be its effect on the colonization of small disturbances, where species dispersed with dung are found to be favoured This aids the maintenance of grazing‐tolerant communities