Rhinanthus minor population genetic structure and subspecies: Potential seed sources of a keystone species in grassland restoration projects

In the last few decades unimproved semi-natural grasslands have been affected by intensification of land use and habitat fragmentation. Because of their biodiversity these species-rich grasslands are of high conservation importance and efforts are under way to restore such habitats. Detailed knowledge of within species diversity will aid deciding on the optimal seed source for such restoration projects, e.g. local genotypes or ecotypes. Rhinanthus minor is a species that is typically found in semi-natural grasslands and is commonly used in grassland restoration projects. This is because R. minor is a hemiparasitic plant that takes minerals and nutrients from its host, which in turn decreases the host's biomass and leads to opportunities for less competitive species in the vegetation. Here, we investigate genetic diversity within and between R. minor populations. This allowed us to test whether the six different subspecies of R. minor that have been described in the UK, based on their morphology, flowering time, and habitat, can be differentiated using molecular markers. We identified moderate levels of genetic differentiation between R. minor populations within the UK. In addition, R. minor individuals from the UK appear to be distinct from R. minor and Rhinanthus angustifolius individuals from other European countries based on microsatellite genotyping and DNA sequencing of cpDNA and rDNA ITS. The molecular markers used in the current study did not separate populations of R. minor based on either their subspecies or habitat. The implication for the use of R. minor in grassland restoration projects seems to be that it is not necessary to use local seeds or seeds from the same subspecies.     

The role of the hemiparasitic annual Rhinanthus minor in determining grassland community structure

Summary Rhinanthus minor (yellow-rattle) is a widespread hemiparasitic plant of grassland habitats throughout Great Britain. It is usually considered to be indicative of species-rich grassland, but in a survey of 14 habitats throughout Britain it was found that R. minor at the time of flowering normally occupied relatively low-diversity patches within areas of high diversity as determined by the number of species, Simpson's Index and the Shannon-Wiener Index. Following the death of adult plants of R. minor in the summer it was shown that the pattern of species diversity changed such that by the time R. minor germinated in the following spring the differences between the areas containing and not containing R. minor were much less distinct. A perturbation experiment in which R. minor was removed from four sites indicated that the effect of the removal of R. minor on the development of community structure over the next year was to increase species diversity on three of the sites and decrease it on the fourth. Those species which responded to the removal of R. minor by an increase in abundance were shown to be preferred hosts. All three lines of evidence point to the fact R. minor has a significant effect on the species diversity of the communities in which it grows by selectively parasitizing components of the flora and modifying the competitive relationships between plants. However, as the communities generally responded to the removal of R. minor by an increase in diversity and as the general survey indicated that R. minor is generally associated with areas of low diversity it would appear that the plants which are selectively parasitized are generally not the competitive dominants in the community.     

Incorporating patterns of disperser behaviour into models of seed dispersal and its effects on estimated dispersal curves

The processes determining where seeds fall relative to their parent plant influence the spatial structure and dynamics of plant populations and communities. For animal dispersed species the factors influencing seed shadows are poorly understood. In this paper we test the hypothesis that the daily temporal distribution of disperser behaviours, for example, foraging and movement, influences dispersal outcomes, in particular the shape and scale of dispersal curves. To do this, we describe frugivory and the dispersal curves produced by the southern cassowary, Casuarius casuarius, the only large-bodied disperser in Australia’s rainforests. We found C. casuarius consumed fruits of 238 species and of all fleshy-fruit types. In feeding trials, seeds of 11 species were retained on average for 309 min (±256 SD). Sampling radio-telemetry data randomly, that is, assuming foraging occurs at random times during the day, gives an estimated average dispersal distance of 239 m (±207 SD) for seeds consumed by C. casuarius. Approximately 4% of seeds were dispersed further than 1,000 m. However, observation of wild birds indicated that foraging and movement occur more frequently early and late in the day. Seeds consumed early in the day were estimated to receive dispersal distances 1.4 times the ‘random’ average estimate, while afternoon consumed seeds received estimated mean dispersal distances of 0.46 times the ‘random’ estimate. Sampling movement data according to the daily distribution of C. casuarius foraging gives an estimated mean dispersal distance of 337 m (±194 SD). Most animals’ behaviour has a non-random temporal distribution. Consequently such effects should be common and need to be incorporated into seed shadow estimation. Our results point to dispersal curves being an emergent property of the plant–disperser interaction rather than being a property of a plant or species.     

Biological and environmental effects on fine-scale seed dispersal of an invasive tree in a secondary subtropical forest

Dispersal abilities of invading species emerge from the interaction between the species and some features of the target community. Ligustrum lucidum is a tree species invading different ecosystems. Major spatial patterns of Ligustrum invasions and their ecological consequences have been analyzed, but no study addressed the dispersal process at a fine scale, assessing the effects of different biological and environmental factors. Ligustrum lucidum is an ornithochoric species. The structure of the environment determines bird movements and thus affects seed dispersal. We used inverse modeling to analyze bird-mediated dispersal of L. lucidum seeds in a secondary Yungas forest and surrounding crop-fields. We assessed the effects of egestion mode (regurgitation and defecation) and tree density (as an environment character) on seed dispersal. Seed dispersal presented different spatial patterns depending on the egestion mode. Tree density was positively associated with the number of regurgitated dispersed seeds and negatively associated with the number of defecated dispersed seeds. In both cases, dispersal distance increased in open areas, but absence of perches inhibited seed arrival. Thus, spread of L. lucidum is facilitated in open areas with some trees; inside the native forest, short distance dispersal facilitates the gradual invasion by this exotic species. Our results suggest that processes like crop abandonment and forest succession, which are active in subtropical montane systems, may facilitate L. lucidum invasion. Our seed dispersal models should be combined with actual distribution maps of L. lucidum to identify areas vulnerable to new invasions.     

Modelling the effects of genetics and habitat on the demography of a grassland herb

There is growing evidence that genetic and ecological factors interact in determining population persistence. The demographic effects of inbreeding depression can largely depend on the ecological milieu. We used demographic data of the perennial herb Succisa pratensis from six populations in grazed and ungrazed sites with different soil moisture. We built an individual-based model assessing the demographic consequences of inbreeding depression in populations with different management and habitat. Today this plant has to cope with severe landscape fragmentation, deteriorating habitat conditions in terms of decreasing grazing intensity, and the effects of inbreeding depression. For each population we performed simulations testing two inbreeding depression hypotheses (partial dominance and overdominance) and three epistatic functions among loci. The results indicated stronger inbreeding depression effects for populations in unfavourable sites without grazing or in xeric habitats compared to populations in favourable mesic sites with grazing. Overall, we found stronger effects with overdominance, a result that emphasizes the importance of understanding the genetic mechanisms of inbreeding depression. Hence, management practices can interact with the genetic consequences of inbreeding depression in population dynamics, which may have important implications for plant population ecology and evolutionary dynamics of inbreeding depression.     

Disentangling facilitation and seed dispersal from environmental heterogeneity as mechanisms generating associations between savanna plants

Question: How can we disentangle facilitation and seed dispersal from environmental heterogeneity as mechanisms causing spatial associations of plant species? Location: Semi‐arid savanna in the Kimberley Thorn Bushveld, South Africa. Methods: We developed a two‐step protocol for the statistical differentiation of association‐promoting mechanisms in plants based on the Acacia erioloba–Grewia flava association. Individuals of the savanna shrub G. flava and the tree A. erioloba were mapped on four study plots. Disentangling the mechanism causing the association of G. flava and A. erioloba involved tests of three spatial and one non‐spatial null model. The spatial null models include homogeneous and heterogeneous Poisson processes for spatial randomness based on the bivariate spatial point patterns of the four plots. With the non‐spatial analysis, we determined the relationship between the canopy diameter of A. erioloba trees and presence or absence of G. flava shrubs in the tree understorey to find whether shrub presence requires a minimum tree canopy diameter. Results: We first showed a significant positive spatial association of the two species. Thereafter, the non‐spatial analysis supported an exclusion of environmental heterogeneity as the sole cause of this positive association. We found a minimum tree size under which no G. flava shrubs occurred. Conclusions: Our two‐step analysis showed that it is unlikely that heterogeneous environmental conditions caused the spatial association of A. erioloba and G. flava. Instead, this association may have been caused by seed dispersal and/or facilitation (e.g. caused by hydraulic lift and/or nitrogen fixation by the host tree).     

Microsite and litter cover effects on seed banks vary with seed size and dispersal mechanisms: implications for revegetation of degraded saline land

Seed movements and fates are important for restoration as these determine spatial patterns of recruitment and ultimately shape plant communities. This article examines litter cover and microsite effects on seed availability at a saline site revegetated with Eucalyptus sargentii tree rows interplanted with 5?C6 rows of saltbush (Atriplex spp.). As litter accumulation decreases with increasing distance from tree rows, soil seed banks were compared between paired bare and litter-covered zones within three microsites; tree row, saltbush row closest to tree row and saltbush mid-row (middle row of saltbush between tree rows). Germinable seed banks of the four most abundant species with contrasting seed sizes and dispersal mechanisms were assessed to test the hypotheses that: (i) microsites with litter cover contain higher seed densities than bare areas, but that (ii) microsite and litter effects will vary depending on seed size and dispersal mechanisms. Overall, litter cover increased seed densities, however, litter effects varied with seed size, with no effect on small-seeded species and litter increasing densities of large-seeded species. Seed bank composition also differed between tree and shrub microsites due to differences in seed morphology and dispersal mechanisms. Water-dispersed species were unaffected by microsite but densities of wind-dispersed species, including Atriplex spp., were higher in saltbush microsites. Densities of wind-dispersed species also differed between the two saltbush microsites despite similar litter cover. Future plantings should consider row spacing and orientation, as well as the dimensions of seeding mounds and associated neighbouring depressions, to maximize litter and seed-trapping by microsites.     

Contemporary pollen and seed dispersal in a Prunus mahaleb population: patterns in distance and direction

Pollination and seed dispersal determine the spatial pattern of gene flow in plant populations and, for those species relying on pollinators and frugivores as dispersal vectors, animal activity plays a key role in determining this spatial pattern. For these plant species, reported dispersal patterns are dominated by short-distance movements with a significant amount of immigration. However, the contribution of seed and pollen to the overall contemporary gene immigration is still poorly documented for most plant populations. In this study we investigated pollination and seed dispersal at two spatial scales in a local population of Prunus mahaleb (L.), a species pollinated by insects and dispersed by frugivorous vertebrates. First, we dissected the relative contribution of pollen and seed dispersal to gene immigration from other parts of the metapopulation. We found high levels of gene immigration (18.50%), due to frequent long distance seed dispersal events. Second, we assessed the distance and directionality for pollen and seed dispersal events within the local population. Pollen and seed movement patterns were non-random, with skewed distance distributions: pollen tended moved up to 548 m along an axis approaching the N-S direction, and seeds were dispersed up to 990 m, frequently along the SW and SE axes. Animal-mediated dispersal contributed significantly towards gene immigration into the local population and had a markedly nonrandom pattern within the local population. Our data suggest that animals can impose distinct spatial signatures in contemporary gene flow, with the potential to induce significant genetic structure at a local level.     

Frugivores and seed dispersal: mechanisms and consequences for biodiversity of a key ecological interaction

The 5th Symposium on Frugivores and Seed Dispersal, held in Montpellier (France), 13-18 June 2010, brought together more than 220 researchers exemplifying a wide diversity of approaches to the study of frugivory and dispersal of seeds. Following Ted Fleming and Alejandro Estrada's initiative in 1985, this event was a celebration of the 25th anniversary of the first meeting in Veracruz, Mexico. Frugivory and seed dispersal are active research areas that have diversified in multiple directions since 1985 to include evolution (e.g. phylogenetic diversity and dispersal adaptations), physiology (e.g. sensory cues and digestion), landscape ecology (movement patterns), molecular ecology (e.g. gene flow, genetic diversity and structure), community ecology (e.g. mutualistic interaction networks) and conservation biology (effects of hunting, fragmentation, invasion and extinction), among others. This meeting provided an opportunity to assess conceptual and methodological progress, to present ever more sophisticated insights into frugivory in animals and dispersal patterns in plants, and to report the advances made in examining the mechanisms and consequences of seed dispersal for plants and frugivores.     

A European phylogeography of Rhinanthus minor compared to Rhinanthus angustifolius: unexpected splits and signs of hybridization

Rhinanthus minor and Rhinanthus angustifolius (Orobanchaceae) are annual hemiparasites, which occur sympatrically in Europe and are known to hybridize. We studied chloroplast and nuclear (amplified fragment length polymorphism [AFLP]) diversity in R. minor and compared genetic structuring in this species with R. angustifolius by analyzing the AFLP data for both species simultaneously. The AFLP data revealed that populations in Italy, Greece, and southeast Russia initially identified as R. minor were so distant from the other R. minor populations that they probably belong to another, yet unidentified taxon, and we refer to them as Rhinanthus sp. R. minor s.s. showed a clear geographic genetic structure in both the chloroplast DNA (cpDNA) and nuclear genome. The simultaneous analysis of both species shed new light on the previously published findings for R. angustifolius, because some populations now turned out to belong to R. minor. The admixture analysis revealed very few individuals of mixed R. minor-R.angustifolius ancestry in the natural populations in the west of Europe, while admixture levels were higher in the east. The combined haplotype network showed that haplotype H1 was shared among all species and is likely to be ancestral. H2 was more abundant in R. angustifolius and H3 in R. minor, and the latter probably arose from H1 in this species in the east of Europe. The occurrence of H3 in R. angustifolius may be explained by introgression from R. minor, but without interspecific admixture, these are likely to have been old hybridization events. Our study underlines the importance of including related species in phylogeographic studies.     

Spatial patterns of dispersal, seed predation and germination during colonization of abandoned grassland by Quercus petraea and Corylus avellana

Key processes during recruitment of Quercus petraea and Corylus avellana were investigated in abandoned calcareous grasslands and adjacent scrub using the following methods: (1) observation of hoarding animals during the main period of ripening of acorns and hazel nuts, (2) exposition of seeds on the soil surface and in 5–6 cm depth to test differences in predation and germination, and (3) mapping of seedlings in the grasslands. European jays (Garrulus glandarius) and mice were the main disperser of seeds. Jays preferred acorns, whereas the rodents were less selective, but probably more important for dispersal of nuts. The maximum dispersal distance was about 10–20 m for mice and was estimated several hundred metres for jays. Mice collected hoards of several seeds in about 2 cm depth in the soil, whereas jays stored single seeds. Seed predation and probably hoarding by mice were highest under scrub and in unmown grassland, while jays preferred mown sites for hoarding. However, hiding of seeds in the soil reduced losses in all sites. Predation of nuts was slightly less intensive than that of acorns. Seeds of Corylus were more sensitive to desiccation than Quercus, but in both species germination was lower for seeds exposed on the soil surface and in drier sites. Quercus and Corylus were the most abundant woody species in the fallow grasslands, probably due to the effective multi-staged dispersal by jays and mice, whereas wind-dispersed and fleshy-fruited species were less common; the latter restricted to margins of adjacent scrubland. The study provides several examples for discordance in suitability of patches for seeds and seedlings due to different habitat requirements of successive developmental stages. This result emphasizes the need for studies in the multiple stages during recruitment of vertebrate-dispersed plants.     

A new rain-operated seed dispersal mechanism in Bertolonia mosenii (Melastomataceae), a Neotropical rainforest herb

Although widespread among fungi, lichens, liverworts, and mosses, seed dispersal mechanisms operated by rain are unusual among flowering plants. Generally speaking, two mechanisms are involved in seed dispersal by rains: the splash-cup and the springboard. Here we describe a new seed dispersal mechanism operated by rain in a Neotropical rainforest herb Bertolonia mosenii Cogniaux (Melastomataceae). The study was carried out at the lowland Atlantic rainforest, southeastern Brazil. We experimentally demonstrate that rain is necessary to release the seeds from the capsules through what we call "squirt-corner" seed dispersal mechanism: when a raindrop strikes the mature fruit, the water droplet forces the seeds outward to the angles (corners) of the triangular capsule and the seeds are released. As far as we know squirt-corner represents a new rain-operated seed dispersal mechanism, and a novel seed dispersal mode both for Melastomataceae and for flowering plants from Neotropical forests.     

The host range and selectivity of a parasitic plant: Rhinanthus minor L.

Summary Rhinanthus minor (Yellow-rattle) is a widespread hemiparasitic plant of grassland habitats throughout Britain. Association analysis of the dune vegetation at Holme-next-the-Sea in eastern England revealed only two potential host plants through positive association. In contrast direct examination of the root systems revealed haustorial connections with 20 host species. The number of species parasitized by one plant ranged from one to seven. Data from another four sites in Britain and one in central Europe indicate that the natural host range of R. minor encompasses at least 50 species from 18 families with 22% in the Leguminosae and 30% in the Gramineae. Comparison of the number of haustorial connections made to each species with the abundance of roots in the soil shows that R. minor is a highly selective parasite, but that the selectivity is not consistent between populations or between plants from different parts of the same population. The reasons for host selectivity are discussed.     

Stochastic LTRE analysis of the effects of herbivory on the population dynamics of a perennial grassland herb

Herbivores can have strong deleterious effects on vital rates (growth, reproduction, and survival) and thus negatively impact the population dynamics of plant species. In practice, however, these effects might be strongly correlated, for example as a result of tradeoffs between vital rates. To get better insights into the effects of herbivory on the population dynamics of the long‐lived grassland plant Primula veris population projection matrices were constructed from demographic data collected between 1999 and 2008 (nine annual transitions). Data were collected in two large grassland populations, each of which was subjected to two treatments (grazing by cattle versus a mowing treatment), yielding a total of 36 matrices. We applied a lower‐level vital rate life table response experiment (LTRE) using the small noise approximation (SNA) of the stochastic population growth rate to disentangle the contributions of changes in mean vital rates, variability in vital rates, correlations between vital rates and vital rate elasticities to the difference in the stochastic growth rate. Stochastic growth rates (a= log λ_S) were significantly lower in grazed than in mown plots (a= 0.0185 and 0.1019, respectively). SNA LTRE analysis showed that contributions of mean vital rates by far made the largest contribution to the observed difference in a between grazed and control plots. In particular, changes in sexual reproduction rates made the largest contributions to lower the stochastic growth rate in grazed plots: both adult flowering probabilities and flower and seed production were importantly lower in grazed populations, but these negative effects were largely buffered by increased establishment and seedling survival rates. Among the stochastic terms of the SNA decomposition, contributions of covariance and correlations between vital rates had the largest impact, whereas contributions of elasticities were smaller. The strongest correlation driver was the association between adult survival and seedling establishment, suggesting that environmental conditions favouring adult survival also are beneficial for seedling establishment. Overall, our results show that herbivory had a strong negative effect on the long‐term population growth rate of P. veris that was primarily mediated by differences in fecundity (flower and seed production) and germination.     

The influence of hygroscopic movement on seed dispersal in Daucus carota (Apiaceae)

Summary The influence of hygroscopic movement on seed dispersal in Daucus carota was examined. When relative humidity increases, umbels containing mature fruits close; when relative humidity drops, umbels open. Tests of the effectiveness of smalland large-angled umbels on dispersing seeds under various conditions demonstrate that umbels responding greatly to relative humidity (i.e. opening wide) lose seeds more quickly than do umbels responding little, and do not disperse them as far. As relative humidity increases, number of dispersing seeds drops to near zero. Response to changes in relative humidity within an umbel progressively increases from late August when dispersal begins. Umbels that slowly increase their response retain some seeds that may disperse over snow in winter. Individual variation in response to relative humidity is high among plants beginning dispersal at the same time. This variability is probably maintained by the variable consequences of dispersing seeds at different times.     

Uncoupling the effects of seed predation and seed dispersal by granivorous ants on plant population dynamics

Secondary seed dispersal is an important plant-animal interaction, which is central to understanding plant population and community dynamics. Very little information is still available on the effects of dispersal on plant demography and, particularly, for ant-seed dispersal interactions. As many other interactions, seed dispersal by animals involves costs (seed predation) and benefits (seed dispersal), the balance of which determines the outcome of the interaction. Separate quantification of each of them is essential in order to understand the effects of this interaction. To address this issue, we have successfully separated and analyzed the costs and benefits of seed dispersal by seed-harvesting ants on the plant population dynamics of three shrub species with different traits. To that aim a stochastic, spatially-explicit individually-based simulation model has been implemented based on actual data sets. The results from our simulation model agree with theoretical models of plant response dependent on seed dispersal, for one plant species, and ant-mediated seed predation, for another one. In these cases, model predictions were close to the observed values at field. Nonetheless, these ecological processes did not affect in anyway a third species, for which the model predictions were far from the observed values. This indicates that the balance between costs and benefits associated to secondary seed dispersal is clearly related to specific traits. This study is one of the first works that analyze tradeoffs of secondary seed dispersal on plant population dynamics, by disentangling the effects of related costs and benefits. We suggest analyzing the effects of interactions on population dynamics as opposed to merely analyzing the partners and their interaction strength.     

Two-phase seed dispersal: linking the effects of frugivorous birds and seed-caching rodents

Frugivorous birds disperse the seeds of many fruit-bearing plants, but the fate of seeds after defecation or regurgitation is often unknown. Some rodents gather and scatter hoard seeds, and some of these may be overlooked, germinate, and establish plants. We show that these two disparate modes of seed dispersal are linked in some plants. Rodents removed large (>25 mg) seeds from simulated bird feces (pseudofeces) at rates of 8–50%/day and scatter hoarded them in soil. Ants (Formica sibylla) also harvested some seeds and carried them to their nests. Rodents carried seeds 2.5±3.2 m to cache sites (maximum 12 m) and buried seeds at 8±7 mm depth. Enclosure studies suggest that yellow pine chipmunks (Tamias amoenus) and deer mice (Peromyscus maniculatus) made the caches. In spring, some seeds germinated from rodent caches and established seedlings, but no seedlings established directly from pseudofeces. This form of two-phase seed dispersal is important because each phase offers different benefits to plants. Frugivory by birds permits relatively long-range dispersal and potential colonization of new sites, whereas rodent caching moves seeds from exposed, low-quality sites (bird feces on the ground surface) to a soil environment that may help maintain seed viability and promote successful seedling establishment.