What does diaspore morphology tell us about external animal dispersal? Evidence from standardized experiments measuring seed retention on animal-coats

It is generally assumed that morphological structures like awns, bristles, or hooks increase retention potential of plant diaspores to the coats of animals, but this basic assumption has rarely been tested.In this paper we introduce a lab-experiment in which detachment rates of diaspores from mechanically shaken animal coats are measured using a standardized protocol and compared with detachment rates measured under natural conditions.The lab-experiments were used to assess ‘retention potentials’ of diaspores for more than 100 plant species. ‘Retention potential’ is defined as the proportion of diaspores still attached to the animal coat after a certain time period. We assessed the effect of several diaspore traits on retention potential and found that a strong negative effect of diaspore mass overrides the expected positive effect of structures like awns, bristles or hooks. However, a positive effect of these structures was proven, when analysing the dataset separately for diaspores of different mass classes. Additionally, we found a negative effect of flat appendages.Coat type also affects retention potentials, with higher values in curly sheep wool compared to straight cattle hair. Species with diaspore mass <2 mg had a fair chance to be dispersed in curly wool as well as in straight hair over long distances, once they get attached to the animal-coat. However, some species with diaspore mass >2 mg might also be dispersed over long distances, at least by sheep.The frequency distribution of retention potentials clearly shows that a binary classification of species dispersed in animal hair vs. species not dispersed is artificial since differences are gradual.The relative importance of diaspore mass for determining retention potential was higher in straight hair, whereas diaspore morphology had a relatively higher impact in curly wool. Hence, different sets of plant species are dispersed by different animals.     

Epizoochorous dispersal by ungulates depends on fur,grooming and social interactions

The transport phase of the animal‐mediated plant dispersal process is critical to dispersal effectiveness as it determines the spatial distribution of the diaspores released and their chance for further recruitment. Assessing this specific phase of the dispersal process generally requires combining diaspore retention times with the associated distances covered. Here, we specifically tested the effect of grooming behavior, interindividual contacts and ungulate fur on diaspore retention times and associated dispersal distances for the hooked diaspores of Xanthium strumarium L. experimentally attached to tamed individuals of three ungulate species. We used a comparative approach based on differing fur quality on different body zones of these three ungulates. During 6‐hr sessions, we monitored for grooming and social interactions that may induce intended or inadvertent diaspore detachment. Additionally, we proposed innovative approaches to directly assessing diaspore dispersal distances by red deer in situ. Fat‐tailed functions fitted diaspore retention time, highlighting the potential for long‐distance dispersal events. The longer the hair, the higher the retention capacity of diaspores in the animal's fur. As predicted, donkey retained diaspores longer than red deer and dwarf goat; and we also confirmed that diaspores attached to the short hair of the head fell off more quickly than did those on the other body zones. Dwarf goat groomed more often than both red deer and donkey, but also when it carried diaspores. Up to 14% of the diaspores detached from animal fur after specific grooming behavior. We observed, in controlled conditions, for the first time and for each ungulate species, interindividual transfers of diaspores, representing 5% of the diaspores attached to animals’ fur. Our results militate for incorporating animal behavior into plant dispersal modeling approaches.     

Epizoochorous and post-dispersal processes in a rare plant species: Jurinea cyanoides (L.) Rchb. (Asteraceae)

We used Jurinea cyanoides as a model plant species to ask the question whether sheep play a dual role in enabling the establishment of a rare species (1) by epizoochorous transport of diaspores and (2) by influencing post-dispersal processes. We carried out two field experiments in sand grassland (Jurineo–Koelerietum glaucae) in the northern upper Rhine valley, Germany. In the first one, we attached diaspores to the fleeces of sheep and assessed retention time, seed shadow, seedling emergence and establishment. In the second one, diaspore displacement by sheep trampling was investigated.It could be shown that establishment of J. cyanoides is possible after sheep-epizoochorous dispersal, but is severely limited by several factors. First, retention time is mostly short (only 18% of the diaspores remained in the fleeces >2 h). Thus, the seed shadow is concentrated around the place of attachment (mostly <5 m distance, maximum 17 m). Second, seedling emergence of dispersed achenes is severely limited by above-ground granivory (99%). Third, establishment is limited by seedling mortality (68%) due to summer drought. The seedlings germinated from achenes that had been incorporated into the soil (or into deeper parts of the bryophyte layer). The second experiment showed that sheep trampling significantly enhanced the incorporation of achenes into the soil compared with controls. Our study gives evidence that sheep can play a dual role: diaspore transport and facilitation of establishment by trampling.     

How to predict attachment potential of seeds to sheep and cattle coat from simple morphological seed traits

Dispersal is a process that determines many aspects in the life-history of plants. Up to now, however, it is difficult to quantify. Many studies rather assess it as a categorical trait, i.e. assuming a species is dispersed by a certain vector or not. Gradual differences in the dispersal potential between species are rarely considered.
In this paper we focus on the key process of epizoochory: the attachment potential of species to animal coats. We present two simple models (GLMs) how to quantify and to predict attachment potentials to sheep wool and to cattle hair from easily measurable seed traits. To calibrate the models, we investigated the attachment potential of seeds of 130 plant species on mechanically shaken coats of sheep and cattle and measured traits describing the seeds. We found that seed mass and seed morphology were correlated with attachment potentials. For sheep wool, the combination of the logarithm of seed mass and a constant for the different seed morphology types explained 85% of the variation of attachment potentials. For cattle hair, 71% were explained. To validate the models, they were applied to 36 additional species. Predicted and experimentally measured attachment potentials were correlated with r=0.84 for sheep wool and r=0.61 for cattle wool. Thus, the attachment potential of seeds to sheep or cattle coat can be assessed for a large set of species using the described models if seed mass and seed morphology are known.     

Ants as diaspore removers of non-myrmecochorous plants: a meta-analysis

Diaspore (e.g. seeds, fruits) dispersal is pivotal for plant communities and often involves several steps and different dispersing agents. Most studies focusing on diaspore dispersal by animals have highlighted the role of vertebrates, neglecting the role of ants in the diaspore dispersal of non-myrmecochorous plants. Diaspore dispersal by ants is especially relevant in the current scenario of declining of vertebrate populations and, consequently, collapse of the dispersal system of large-seeded plants. Although ants can never compensate for the dispersal service provided by vertebrates, they can mitigate the impact of vertebrate decline via removal of diaspores deposited on the ground. We have used a meta-analytical approach to investigate the contribution of ants in the removal of non-myrmecochorous diaspores (through vertebrate exclusion experiments). We considered the number of diaspore removal as effect size and factors such as plant growth forms, diaspore and ant size, habitat type as moderators. In addition, we investigated the role of such factors on the diaspore removal distance by ants. Ants played complementary role to non-myrmecochorous diaspore removal services provided by vertebrates (mean Hedges’ g of −0.30). The ant diaspore removal was 69% higher for diaspores from shrubs than that of tree diaspores and removal of small-sized diaspores were 69% and 70% higher in comparison to medium- and large-sized diaspores, respectively. Regarding the diaspore removal distance by ants, those of tree species were removed 32% farther than those of shrub species, and diaspores were removed three- times farther in the savanna than in rainforest ecosystems. Our results highlight the shrubs and small-sized diaspores. Regarding the diaspore removal distance, the ants can be crucial for the dispersal of tree diaspores and in the savanna ecosystems. Finally, considering the biodiversity crisis, the ants may play an even more important role than appreciated in diaspores dispersal.     

Hair density in the Eurasian otter <Emphasis Type="Italic">Lutra lutra</Emphasis> and the Sea otter <Emphasis Type="Italic">Enhydra lutris</Emphasis>

The hair density of adult Eurasian otters Lutra lutra (Linnaeus, 1758) and sea otters Enhydra lutris (Linnaeus, 1758) was analysed using skin samples taken from frozen carcasses. Lutra lutra exhibited a mean hair density of about 70 000 hairs/cm² (whole body, appendages excepted), the mean individual density ranging from about 60 000 to 80 000 hairs/cm². The dominant hair type were secondary hairs (wool hairs), the hair coat comprising only 1.26% of primary hairs (PH). Secondary hair (SH) density remained constant over the body (appendages excepted), whereas a few variations in PH density were observed. Neither an influence of the sex, nor a seasonal variation of the hair coat was found, moulting seems to be continuous. Enhydra lutris had a hair density between 120 000 and 140 000 hairs/cm², the primary hairs representing less than 1% within the hair coat. Hair density remained quite constant over the regions of the trunk but was lower at the head (about 60 000 hairs/cm² on the cheek). The hair follicles were arranged in specific groups with different bundles of varying size, normally comprising dominant numbers of wool hair (SH) follicles. Invariably there was always a large central primary hair follicle and numerous sebaceous glands between the bundles and principally around the PH follicles. The results are discussed related to possible ecological influences on hair coat density.     

Importance of elaiosome size to removal of ant-dispersed seeds

Several studies relate removal of diaspores from different ant-dispersed plant species to the size of their claiosomes. This study is the first one to relate intraspecific variation in claiosome size to removal of diaspores by ants. This approach circumvents the problem posed by interspecific variation in chemistry and morphology of elaiosomes. We used the systemHepatica nobilis Mill. (Ranunculaceae) andMyrmica ruginodis Nyl. The elaiosome was the attractive part of the diaspore and its attractiveness decreased quickly after release from the fruit. In experimental runs where ants collected diaspores, the elaiosome size of accepted diaspores was larger than of those rejected and the largest diaspores were collected first. Since size of diaspore, elaiosome and achene were correlated, the diaspores that were removed first had both the largest elaiosome and achene. However, our experiments suggested that elaiosome size was more important to removal than achene size or the elaiosome:achene size ratio. If ant dispersal improves plant fitness, elaiosome size and hence diaspore size would be expected to increase over time. However, such directional selection mediated by the ants is probably counterbalanced by the plant. Seed predators and a negative trade-off between number and size of seeds would, among other factors, select for smaller diaspore size,i.e. counteract the effect of the ants' preference for larger elaiosomes.     

Epizoochory in a hedgerow habitat: seasonal variation and selective diaspore adhesion

Epizoochory has been less studied than other seed dispersal mechanisms, such as endozoochory, and generally only a small percentage of plant species show adaptations to this strategy. Nevertheless, epizoochorous seed dispersal can affect an appreciable number of herb species in forests and man-made habitats. Also, few studies have dealt with temporal variation in epizoochory. In this paper, medium-long distance epizoochory is analyzed in a hedgerow habitat for the first time, using a domestic dog in an area in northwest Spain. Special attention is paid to seasonal variation and differential traits of plant taxa involved. Approximately 30 % of available herb taxa were found attached to hair. The intermonthly difference in the frequency of the taxa involved in epizoochory was significant, and the overall peak was reached in June–October linked with diaspore ripening phenology. Ninety-three percent of the plant taxa adhered to hair had diaspores with traits facilitating epizoochory (hooks, spines, awns, rigid hairs), in comparison with 17 % for available plant taxa not adhered to hair. The taxa involved in epizoochory had larger diaspores than the rest of the available taxa, but ranged considerably in size. Numerous hooks covered the largest, heaviest diaspores, and allowed them to attach to hair. There was no significant difference in mean plant height between taxa involved in epizoochory and the rest of the available taxa. The difference in life span between taxa involved in epizoochory and the rest of available taxa was not significant, most of them being perennials in both cases. Seventy-three percent of all the available plant taxa were potential forest plants typically found in edges and gaps, and 64 % of the plant taxa involved in epizoochory were these kinds of potential forest plants. High or medium involuntary positive selection by the dog of diaspores of Taraxacum gr. officinale, Galium aparine, Geum urbanum, and Agrimonia eupatoria was observed. In conclusion, epizoochorous dispersal can be quantitatively and functionally important in hedgerow habitats during summer-autumn, affecting mainly herb taxa with specialized diaspores.     

植物锥形繁殖体结构及其适应

植物的锥形繁殖体是具有吸湿芒和锐利尖端的一种繁殖体类型。锥形繁殖体结构的功能几乎在植物生活史的各个阶段上都有体现,然而,其最基本的功能是通过繁殖体的打钻作用将自身埋入土壤。从植物繁殖体的形态结构出发,对锥形繁殖体的各项功能进行了综述,重点阐述植物繁殖体打钻作用及其机制方面的研究进展,面临的主要问题和未来的研究方向。     

Diaspore removal and potential dispersers of the rare and protected Paeonia officinalis L. (Paeoniaceae) in a changing landscape

Paeonia officinalis L., a rare and protected species, mostly occurs in open and semi‐open habitats and is often threatened by forest and shrubland spread. To explore the still undocumented dispersal features of this species, we address the following questions. What are the relative roles of ants, small rodents, and birds as diaspore removers in open habitat and woodland? Which animal groups constitute the potential disperser assemblage and how do they shape the spatial patterns of seed dispersal? Do diaspores fit the ornithochory syndrome or do they only mimic fleshy fruits? Two experiments were performed to quantify diaspore fall and diaspore removal by animal groups, above ground and on the ground. Ants did not contribute to dispersal. In open habitats, no seed removal was detected, either on follicles or once diaspores had fallen to the ground. In woodland, diaspores were weakly removed by vertebrates on follicles and were mainly removed by rodents on the ground. As a consequence, we suggest that long‐distance dispersal events are very rare, weakening the possible escape into space of populations subject to forest spread. Several traits indicate that diaspores fit the ornithochory syndrome, but other traits are strongly reminiscent of mimetic diaspores deceiving bird dispersers. © 2007 CNRS. Journal compilation © 2007 The Linnean Society of London, Botanical Journal of the Linnean Society, 2007, 154 , 13–25.     

Variation in dispersability among mainland and island populations of three wind dispersed plant species

Reduced dispersability of species living on islands relative to mainland has been documented in both plants and animals. One evolutionary scenario explains this trend by strong selection against dispersal, once the species has reached the island, to reduce dispersal out to sea. In this study, we compare the dispersal ability of three wind dispersed plant species (Cirsium arvense, Epilobium angustifolium, and E. hirsutum) from populations on mainland and three islands. Dispersal ability was estimated directly as drop time of diaspores, and indirectly using a morphological measure relating the weight of the diaspore to the size of the pappus (Cirsium) or seed hairs (Epilobium). Positive correlation between the morphological measure of dispersal ability and drop time of diaspores were found for all study species. Dispersal ability varied significantly among mainland and islands, and among species. C. arvense showed a significant reduction in dispersal ability on islands compared to mainland, whereas the reverse was found for the two Epilobium species. Overall Epilobium diaspores had a 2–4 times higher dispersability than C. arvense, indicating that degree of isolation of islands vary among study species. Significant differences in dispersability among plants within populations were detected in all species suggesting that this trait may have a genetic component.     

Seed dispersal by neotropical waterfowl depends on bird species and seasonality

1. Waterbird‐mediated endozoochory is an essential mechanism for the dispersal of sessile organisms in freshwater ecosystems. However, in the neotropics there are no previous studies of how different waterbird species vary in the dispersal functions they perform, and how seasonality influences endozoochory. In this study, we identified plant diaspores dispersed in faeces of five South American waterfowl (Brazilian teal Amazonetta brasiliensis, yellow‐billed teal Anas flavirostris, ringed teal Callonetta leucophrys, coscoroba swan Coscoroba coscoroba, and white‐faced whistling‐duck Dendrocygna viduata).
2. We collected 165 faecal samples from five wetlands in southern Brazil surrounded by pasture and rice fields, then separated and measured intact seeds and other diaspores. Using generalised linear models, we tested how diaspore abundance and taxonomic richness differed among bird species and between cold (April–September) and warm (October–March) periods. We also analysed bird‐specific and seasonal variations in diaspore composition through principal coordinates analysis and permutational multivariate analysis of variance. We used indicator species analysis to determine which diaspore species discriminated between bird species and seasons. Finally, we measured diaspore length in order to analyse differences among waterfowl species in the size of diaspores dispersed.
3. We found 2,066 intact diaspores from 40 different plant taxa, including seeds of 37 angiosperms and diaspores of Lycophyta (Isoetes cf. maxima), Pteridophyta (Azolla filiculoides), and Charophyceae. There was at least one diaspore in 65% of all faecal samples. Diaspores of native amphibious and emergent plants were dominant. We found 1,835 diaspores (from 33 taxa) in the cold period but only 231 (23 taxa) in the warm period. Seeds of the grass Zizaniopsis bonariensis and of the sedge Rynchospora sp. were the most abundant taxa. A strong interaction between bird species and season was the most important predictor of variation in both taxonomic richness and abundance of diaspores. The taxonomic composition of diaspores differed among waterfowl species and season. Indicator species analysis identified 12 plant taxa associated with particular bird species and seasons. Coscoroba swan, the largest bodied species in our study dispersed a higher proportion (8.2%) of large (length >2 mm) seeds.
4. Despite considerable overlap, there are important differences in the plants dispersed by each species, and the smallest (ringed teal) and largest (coscoroba swan) birds are particularly different. All five waterfowl species are distributed over wide areas of South America and here we demonstrated that they are likely to be important plant vectors connecting wetland species at different geographical scales. Many of these plants have previously been assumed to lack mechanisms for long‐distance dispersal.

     

黄土丘陵沟壑区80种植物繁殖体形态特征及其物种分布

植物繁殖体的形态特征及其物种分布是植物长期适应环境的结果,对退化生态系统的更新与恢复具有重要的理论与实践指导意义。研究了80种植物的繁殖体形态特征及与其物种分布的关系,结果表明：1）繁殖体重量差别较大（0. 020—357.428 mg）,主要集中在1—9.999 mg（占52.5%）。2）繁殖体的形状指数FI变化范围较大（1.06—12.93）,61.3%的植物繁殖体的形状近圆球形。3）33种植物繁殖体具有明显的附属物,包括毛、翅、芒和刺等。4）87.5%的植物繁殖体表面具有各种纹饰（棱、被毛、纹和颗粒状等）;繁殖体颜色以褐色和黑色为主,少数繁殖体颜色鲜艳;6种植物繁殖体具有吸水分泌粘液的特性。5）黄土丘陵沟壑区繁殖体重量小或形状近圆球形的植物分布数量多、范围广。6）繁殖体具有毛、翅和芒附属物或吸湿分泌粘液的植物在黄土丘陵沟壑区较繁殖体无附属物的植物能够分布更多、更广。繁殖体这些有利于物种分布的形态特征对于植物适应该区干旱与土壤侵蚀干扰具有重要的生态学意义,而且可用于指导该区人工补播促进植被恢复的物种选择。     

Indirect effects of alternative food resources in an ant–plant interaction

The seeds of many plant species present a food body that is consumed by animal dispersers. In theory, if the animals are polyphagous, the availability of alternative food resource other than the diaspore itself may influence its dispersal and survival. We used the myrmecochore Helleborus foetidus L. (Ranunculaceae), the seeds of which are attached to a lipid-rich elaiosome that is attractive to ants, as a model system to investigate (1) whether alternative foods that are present along with the plant affect ant foraging behavior and diaspore removal and (2) whether food availability in an ant nest affects seed predation and germination. In a field experiment, artificial diaspore depots were offered together with either sugar, insect corpses, seed, or no food (control). Contrary to the prediction that ants would rather concentrate their foraging effort on the highly rewarding alternative foods only, many workers, attracted by the sugar, switched to the hellebore diaspores, which significantly enhanced removal rate. Results obtained in the laboratory further indicated that the larvae of Aphaenogaster iberica (a major seed disperser) predated more on the H. foetidus embryos when no alternative food was available. This, in turn, slightly reduced seed germination. Overall, these results shed light, for the first time, on the potential indirect effects of alternative resources on the fate of diaspores adapted for ant dispersal.     

Simple Traits among Diaspore Weight/Number, Plant Height and Ability of Vegetative Propagation

Several expected correlations among followed internal plant traits were confirmed using the dataset of 492 herbaceous species from the temporal zone of Central Europe. Average diaspore weight (seed mass), reproductive capacity of population (number of produced diaspores), species height, and ability of lateral spread were the plant traits considered. The evident correlations were confirmed among all investigated traits: (i) The reproductive capacity of population negatively correlated with diaspore weight, plant height, and vegetative propagation. The diaspore weight and their number are closely correlated and co-adapted. (ii) Bigger plant species produce bigger diaspores. These trends are obvious at the inter- and intra-family levels. (iii) Larger plant species showed higher ability to vegetative propagation.     

Exploitation of Fallen Diaspores by Ants: Are there Ant–Plant Partner Choices?

Ants frequently interact with fleshy fallen diaspores (fruits or seeds) not adapted for ant‐dispersal. Such interactions are usually considered as opportunistic, but recent evidence has indicated that these ants may differ in their effects on diaspore survival and plant recruitment. We investigated if partner choices are recognizable among genera of ants and plants, and if ant and plant traits may influence such preferences in cerrado (savanna‐like vegetation) from southeast Brazil. During a 2‐yr period, 521 ant–diaspore interactions were recorded through various methods, yielding 71 ant species and 38 plant species. Exploitation of fallen diaspores was common among several ant genera, and included carnivorous, omnivorous, and fungivorous ants. Contrary to others areas around the world, where true myrmecochory (seed dispersal by ants) is common among shrubs, ants also exploited diaspores from several cerrado trees. Plant life form, diaspore size, and ant body size did not seem to explain the pattern of interactions observed. Two subsets of preferential interactions, however, segregated fungivorous ants from another group composed of carnivorous and omnivorous ants, probably influenced by the chemical composition of the plant diaspores. Omnivorous ants usually remove the fleshy portion of diaspores on spot and probably provide limited benefits to plants. Carnivorous and fungivorous ants usually remove the whole diaspore to the nest. As each of these ant groups may influence the fitness of diaspores in different ways, there are possible subtle pathways for the evolution of partner choices between ants and these non‐myrmecochorous diaspores.     

Estimating wind dispersal potential in Ailanthus altissima: The need to consider the three-dimensional structure of samaras

Plant dispersal is a very important ecological phenomenon, as it can enable species to move away from the parent plant. This contributes to shaping communities, determining patterns of distribution, landscape configuration, plant invasions and evolutionary processes. Measuring dispersal distance directly is difficult and thus, diaspore morphology can be used to make estimates. Previous research on the topic often resorts to analysing the diaspore’s morphology as if it was a bi-dimensional structure; when in many cases, diaspores have three-dimensional qualities. In this study, we show how estimates of wind dispersal potential of Ailanthus altissima can be considerably improved using morphological variables that succeed in describing the three-dimensional nature of samaras. We suggest that this reasoning could be extensively applied to research involving not only other species, but also multi-specific scenarios with a wide range of diaspore morphologies.     

DISPERSAL ECOLOGY OF CAREX PEDUNCULATA (CYPERACEAE), A NEW NORTH AMERICAN MYRMECOCHORE

Carex pedunculata is the first North American species of the Cyperaceae that is identified as a myrmecochore. Many morphological and phenological features of this species and its breeding system are interpreted as adaptive for seed dispersal by ants. In laboratory tests, workers of the ant species Aphaenogaster rudis carry the diaspores to the nest, eat the elaiosomes, carry larvae to the elaiosomes to feed, and deposit diaspores whose elaiosomes have been eaten with other nest debris. The achenes then germinate. Achenes will also germinate without any handling by ants. Workers will also transport diaspores with uneaten elaiosomes when the nest is disturbed. Greenhouse tests show that seedling growth is greatly inhibited if a diaspore remains near the parent plant and cohort seedlings. Field studies of natural populations identify rotting logs (the location of ant nests) as forest floor microsites for colonization of C. pedunculata and other myrmecochores. Ant nesting behavior may pattern much of the herb stratum. This species is self-compatible, and single seeds may start successful new populations. Three processes contribute to population growth: vegetative growth, germination of untransported diaspores, and germination of ant-transported diaspores.