This chapter evaluates the role of endozoochory on seed germination and reviews the information gathered on germination patterns in experiments aimed at examining the effect of a seed's passage through a frugivore's gut, and gives further directions on methods for future studies. Most data demonstrating the different mechanisms by which frugivores can affect seed fate are from studies performed with birds and mammals, which are the numerically dominant dispersers in many systems.
Animal movement and behaviour is fundamental for ecosystem functioning. The process of seed dispersal by frugivorous animals is a showcase for this paradigm since their behaviour shapes the spatial patterns of the earliest stage of plant regeneration. However, we still lack a general understanding of how intrinsic (frugivore and plant species traits) and extrinsic (landscape features) factors interact to determine how seeds of a given species are more likely to be deposited in some places more than in others. We develop a multi-species mechanistic model of seed dispersal based on frugivore behavioural responses to landscape heterogeneity. The model was fitted to data from three-years of spatially-explicit field observations on the behaviour of six frugivorous thrushes and the fruiting patterns of three fleshy-fruited trees in a secondary forest of the Cantabrian range (N Spain). With such model we explore how seed rain patterns arise from the interaction between animal behaviour and landscape heterogeneity. We show that different species of thrushes respond differently to landscape heterogeneity even though they belong to the same genus, and that provide complementary seed dispersal functions. Simulated seed rain patterns are only realistic when at least some landscape heterogeneity (forest cover and fruit abundance) is taken into account. The common and simple approach of re-sampling movement data to quantify seed dispersal produces biases in both the distance and the habitat at which seeds arrive. Movement behaviour not only affects dispersal distance and seed rain patterns but also can affect frugivore diet composition even if there is no built-in preference for fruiting species. In summary, the fate of seeds produced by a given plant species is strongly affected by both the composition of the frugivore assemblage and the landscape-scale context of the plant location, including the presence of fruits from other plants (from the same or different species).
The effectiveness of a frugivore as a disperser of a plant is greatly determined by how fruits and seeds are handled in its mouth and its digestive tract. Although a number of studies have investigated the effect of avian ingestion on germination, we still know very little about the modifications to seeds during ingestion and the specific consequences on plant fitness. Here we investigate for the first time the different mechanisms by which germination patterns of seeds are modified following ingestion by frugivores. Specifically, we examine changes in seed mass, water content, permeability, seed coat thickness, texture, and resistance in two common Mediterranean fleshy-fruited plants, Phillyrea angustifolia and Myrtus communis, after ingestion by Eurasian Blackbirds, Turdus merula. We found a number of differences between the plant species: Phillyrea seeds lost mass, mainly due to water loss, and had thinner coats after gut passage, but Myrtus seeds did not. Seeds of both species showed increased permeability, while Myrtus seeds in particular became less resistant to breakage. No quantifiable changes in seed coat texture were detected in either species, although this trait was partly associated with differences in germination rate in Phillyrea. High intraspecific plant variation was found for most seed traits measured. Seed passage through birds' guts sped up germination in both species, especially in Myrtus. Increased permeability in seeds of both species following ingestion resulted in a higher germination rate. Moreover, seeds with thick coats (and in the case of Phillyrea, harder coats) germinated at a slower rate and produced seedlings that also grew more slowly, indicating a cost of coat thickness and/or hardness for seedling emergence. Results obtained here contribute to explaining the great heterogeneity in germination responses among and within plant species and the large variety of factors, both intrinsic and extrinsic to the plants, that influence such responses.
For plants dispersed by frugivores, spatial patterns of recruitment are primarily influenced by the spatial arrangement and characteristics of parent plants, the digestive characteristics, feeding behaviour and movement patterns of animal dispersers, and the structure of the habitat matrix. We used an individual-based, spatially-explicit framework to characterize seed dispersal and seedling fate in an endangered, insular plant-disperser system: the endemic shrub Daphne rodriguezii and its exclusive disperser, the endemic lizard Podarcis lilfordi. Plant recruitment kernels were chiefly determined by the disperser's patterns of space utilization (i.e. the lizard's displacement kernels), the position of the various plant individuals in relation to them, and habitat structure (vegetation cover vs. bare soil). In contrast to our expectations, seed gut-passage rate and its effects on germination, and lizard speed-of-movement, habitat choice and activity rhythm were of minor importance. Predicted plant recruitment kernels were strongly anisotropic and fine-grained, preventing their description using one-dimensional, frequency-distance curves. We found a general trade-off between recruitment probability and dispersal distance; however, optimal recruitment sites were not necessarily associated to sites of maximal adult-plant density. Conservation efforts aimed at enhancing the regeneration of endangered plant-disperser systems may gain in efficacy by manipulating the spatial distribution of dispersers (e.g. through the creation of refuges and feeding sites) to create areas favourable to plant recruitment.
Summary1. The ingestion of fruits by vertebrate frugivores produces great variation on seed germination responses which depend on (1) the frugivorous species; (2) several factors intrinsic to the plant species; and (3) the conditions under which germination tests are conducted. Most studies on this topic have used only one or a few disperser species, and have been performed under controlled conditions. 2. The main goals of this study were to determine (1) the effect that birds ( Turdus merula ) and lizards ( Podarcis pityusensis ) have on seed emergence patterns of a group of common mediterranean plants; and (2) whether such patterns differ between field and common garden conditions. Over 2 years we compared seed emergence times with those of controls (pulp-removed seeds). 3. Emergence patterns were inconsistent for most plant species when comparing field vs. common-garden conditions. In some cases results were even contradictory: for instance lizards accelerated the emergence time of Rubus seeds in the field, but delayed it in the experimental garden; likewise Rubia seeds ingested by Blackbirds emerged more slowly than controls in the field, but faster than those in the garden. The two frugivorous species had also inconsistent effects on the same plant species. 4. Significant changes in seed weight after passage through the animals' digestive tracts were observed in most species. However, seed weight did not explain differences in seed emergence patterns between ingested and non-ingested seeds. 5. This study demonstrates the great heterogeneity in seed-emergence responses of the different plant species to ingestion by different types of frugivore, and to the different experimental conditions. Thus, caution is needed when making generalizations from studies that aim to evaluate the influence of frugivores on seed dispersal quality.
Mutualistic disruptions, such as those promoted by the loss of seed dispersers, can have negative effects on the plant regeneration of those species that strongly depend upon them. In order to adequately assess how plant communities are affected by such disruptions, we need to know the importance of the dispersal phase, both in its quantitative and qualitative components. We examined this in the narrow interaction between the shrub Daphne rodriguezii and its (only) disperser, the lizard Podarcis lilfordi. We quantified fruit removal and the effect of fruit/seed-size selection, seed treatment in the disperser's guts and seed deposition patterns on seedling emergence and survival. In the only locality in which lizards persist, they removed most fruits and showed preference for larger ones in one of the two study years. Seed treatment in lizard's guts had no effect on germination, although it tended to reduce the effect of seed size on germination (differences between large vs. small seeds in seed germination were higher for non-ingested seeds). Probability of seedling emergence, but not survival, was higher in the locality with lizards. Dispersed seeds under heterospecific shrubs showed higher seedling survival than those under conspecifics in all localities, especially the year with higher rainfall. Our findings support that the movement of seeds to nurse shrubs by lizards is the most important component of the seed dispersal process in the only remaining locality where both species coexist.
Since the success of an invasive species depends not only upon its intrinsic traits but also on particular characteristics of the recipient habitat, assessing the performance of an invader across habitats provides a more realistic analysis of risk. Such an analysis will not only provide insights into the traits related to invasiveness, but also the habitat characteristics that underpin vulnerability to invasion that, taken together, will facilitate the selection of management strategies to mitigate the invader's effect. In the present study, we considered the Mediterranean basin islands as an excellent study region to test how the same invasive species perform in different habitats within a single island, and to scale up differences among islands with similar climate. We tested how the performance of three widespread plant invaders with clonal growth but contrasting life-history traits, a deciduous tree Ailanthus altissima, a succulent subshrub Carpobrotus spp., and an annual geophyte Oxalis pes-caprae, varied depending upon the species identity, habitat, and invaded island. The environmental parameters considered were habitat type, elevation, species diversity in the invaded plot, and several soil traits (% C, % N, C/N, pH, and relative humidity). The study documents that the performance of these three important and widespread plant invaders is dependent mainly on species identity, and less upon the invaded island's general features. Likewise, differences in performance among habitats were only significant in the case of Ailanthus, whereas Carpobrotus and Oxalis appear to perform equally well in different environments. Ailanthus thus appears to have a broader spectrum of invasiveness, being able to invade a larger number of habitat types. On the contrary, Carpobrotus spp. have not yet invaded habitats different from those where the species have been originally introduced and where they are still commonly spread by humans. Oxalis distribution is mainly related to agricultural activities and disturbed sites, and the total area infested by this geophyte may be more reflection of the extent of suitable habitats than of invasiveness or ecological impact. Our results confirm the potential for these species to significantly alter the functioning of ecosystems in the Mediterranean islands and highlight the risk to other islands not yet invaded.
The spatial distribution of plants (and other primarily sessile organisms) depends on the interplay between their ecological requirements and the spatial template set before, during, and after the dispersal process. In the case of animal‐dispersed plants, the spatial characteristics of animal behaviour during the seed dispersal process are likely to leave a lasting imprint on plant distribution. Here, we hypothesize that the activity patterns of the frugivorous lizard Podarcis lilfordi directly influence the spatial distribution of the fleshy‐fruited shrub Daphne rodriguezii. To evaluate this hypothesis, we first analysed lizard activity, following radio‐tracked lizards during the plant's fruiting period, and identified its main determinants at several spatial scales of habitat aggregation (from 12.5 to 150 m). We hypothesised that lizard activity depends on differential habitat features explaining its territory use plus habitat preferences associated with each movement bout. In a second step, the most important determinants of lizard activity plus the variables describing habitat structure were used to predict the presence of adult and juvenile plants. Predictability of lizard activity (based on AUC and Pearson regression coefficients) was higher at broad spatial‐scales of habitat aggregation (75 m). The two best predictors of lizard activity were the habitat features of and the distance to the core area (defined as the area enclosing the 0.50 cumulative probability of lizard locations). Plant presence was best predicted by models based on a combination of lizard activity and habitat features at local spatial scales (1.5 m). Best models included habitat features and lizard activity for adult plants, and local‐scale habitat features, the proximity of adult plants and lizard activity for juveniles. In both cases, most plants (50–60%) were located at ‘optimal sites’ (both favourable for lizards and with adequate habitat features), whereas a small fraction of them (3–10%) were located at dispersal‐limited sites (i.e. with adequate habitat features but suboptimal for lizards). Our results thus suggest that the interplay between lizard activity and local habitat features determines the spatial patterns of juvenile‐plant presence and leaves a lasting signature on adult‐plant distribution.
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