Low availability of functional seed trait data from the tropics could negatively affect global macroecological studies, predictive models and plant conservation.

BACKGROUND: Plant seeds have many traits that influence ecological functions, ex situ conservation, restoration success and their sustainable use. Several seed traits are known to vary significantly between tropical and temperate regions. Here we present three additional traits for which existing data indicate differences between geographical zones. We discuss evidence for geographical bias in availability of data for these traits, as well as the negative consequences of this bias. SCOPE: We reviewed the literature on seed desiccation sensitivity studies that compare predictive models to experimental data and show how a lack of data on populations and species from tropical regions could reduce the predictive power of global models. In addition, we compiled existing data on relative embryo size and post-dispersal embryo growth and found that relative embryo size was significantly larger, and embryo growth limited, in tropical species. The available data showed strong biases towards non-tropical species and certain families, indicating that these biases need to be corrected to perform truly global analyses. Furthermore, we argue that the low number of seed germination studies on tropical high-mountain species makes it difficult to compare across geographical regions and predict the effects of climate change in these highly specialized tropical ecosystems. In particular, we show that seed traits of geographically restricted páramo species have been studied less than those of more widely distributed species, with most publications unavailable in English or in the peer-reviewed literature. CONCLUSIONS: The low availability of functional seed trait data from populations and species in the tropics can have negative consequences for macroecological studies, predictive models and their application to plant conservation. We propose that global analyses of seed traits with evidence for geographical variation prioritize generation of new data from tropical regions as well as multi-lingual searches of both the grey- and peer-reviewed literature in order to fill geographical and taxonomic gaps.

Emerging infectious disease triggered a trophic cascade and enhanced recruitment of a masting tree.

There are several mechanisms that allow plants to temporarily escape from top-down control. One of them is trophic cascades triggered by top predators or pathogens. Another is satiation of consumers by mast seeding. These two mechanisms have traditionally been studied in separation. However, their combined action may have a greater effect on plant release than either process alone. In 2015, an outbreak of a disease (African swine fever, ASF) caused a crash in wild boar (Sus scrofa) abundance in Bialowieza Primeval Forest. Wild boar are important consumers of acorns and are difficult to satiate relative to less mobile granivores. We hypothesized that the joint action of the ASF outbreak and masting would enhance regeneration of oaks (Quercus robur). Data from ungulate exclosures demonstrated that ASF led to reduction in acorn predation. Tree seedling data indicated that oak recruitment increased twofold relative to pre-epidemic period. Our results showed that perturbations caused by wildlife disease travel through food webs and influence forest dynamics. The outbreak of ASF acted synergistically with masting and removed herbivore top-down control of oaks by mobile consumers. This illustrates that the ASF epidemic that currently occurs across Europe can have broad effects on forest dynamics.

Seed type, habitat and time of day influence post-dispersal seed removal in temperate ecosystems.

Seed survival is of great importance for the performance of plant species and it is strongly affected by post-dispersal seed removal by either different animals such as granivorous species and secondary dispersers or abiotic conditions such as wind or water. The success of post-dispersal seed removal depends on seed specific traits including seed size, the presence of coats or elaiosomes, the mode of seed dispersion, and on the habitat in which seeds happen to arrive. In the present study we asked how seed traits (dehulled vs. intact; size; dispersal mode), habitat (forest vs. grassland), and time of day (night vs. day) influence post-dispersal seed removal of the four plant species Chelidonium majus, Lotus corniculatus, Tragopogon pratensis and Helianthus annuus. Seed removal experiments were performed in three regions in Hesse, Germany. The results showed different, inconsistent influences of time of day, depending on habitat and region, but consistent variation across seed types. C. majus and dehulled H. annuus seeds had the fastest removal rates. The impact of the habitat on post-dispersal seed removal was very low, only intact H. annuus seeds were removed at significantly higher rates in grasslands than in forests. Our study demonstrates consistent differences across seed types across different habitats and time: smaller seeds and those dispersed by animals had a faster removal rate. It further highlights that experimental studies need to consider seeds in their natural form to be most realistic.

Are all patches worth exploring? Foraging desert birds do not rely on environmental indicators of seed abundance at small scales.

BACKGROUND: Consumers should show strong spatial preferences when foraging in environments where food availability is highly heterogeneous and predictable. Postdispersal granivores face this scenario in most arid areas, where soil seed bank abundance and composition associates persistently with vegetation structure at small scales (decimetres to metres). Those environmental features should be exploited as useful pre-harvest information, at least to avoid patches predicted to be poor. However, we did not find the expected spatial association in the algarrobal of the central Monte desert by observing foraging seed-eating birds, a field technique influenced by how much they exploit visited patches. In this work we tested if the first stage of foraging by granivorous birds (patch visit, encounter or exploration) is positively associated with environmental indicators of patch quality by recording the removal of single seeds from 300 scattered experimental devices during seasonal trials. Spatial selectivity was analysed by comparing the structural characteristics of used vs. available microhabitats, and evaluated against bottom-up and top-down hypotheses based on our previous knowledge on local seed bank abundance, composition and dynamics. Their foraging activity was also explored for spatial autocorrelation and environmental correlates at bigger scales. RESULTS: Postdispersal granivorous birds were less selective in their use of foraging space than expected if microhabitat appearance were providing them relevant information to guide their search for profitable foraging patches. No microhabitat type, as defined by their vegetation structure and soil cover, remained safe from bird exploration. Analyses at bigger temporal and spatial scales proved more important to describe heterogeneity in seed removal. CONCLUSIONS: Closeness to tall trees, probably related to bird territoriality and reproduction or to their perception of predation risk, seemed to determine a first level of habitat selection, constraining explorable space. Then, microhabitat openness (rather than seed abundance) exerted some positive influence on which patches were more frequently visited among those accessible. Selective patterns by birds at small scales were closer to our predictions of a top-down spatial effect, with seed consumption creating or strengthening (and not responding to) the spatial pattern and dynamics of the seed bank.

Seed supply limits seedling recruitment of Eucalyptus miniata: interactions between seed predation by ants and fire in the Australian seasonal tropics.

Seed predation can cause substantial seed losses and influence plant population dynamics, but the impact depends on the extent to which populations are limited by seed availability or favorable microsites for recruitment. Harvester ants are the dominant post-dispersal seed predators in Australia's tropical savannas, and their abundance and foraging efficiency, as well as the availability of seed and microsites, are affected by fire history. We undertook a predator-exclusion experiment to examine the interactive effects of fire history (no fire compared with annual burning over 5 years) and seed predation by ants on seedling establishment of the dominant savanna tree, Eucalyptus miniata, in northern Australia. Despite its large seed size, the rate of removal (~ 20-60%) was similar or higher than typically reported for eucalypts, although it was lower than that recorded for the smaller seeds of the co-occurring E. tetrodonta. Seed predation rates were twice as high in annually burnt compared to unburnt sites, but there was no significant difference in the proportion of seedlings that emerged from the initial seed available. Seedling emergence in both regimes was low, representing < 7% of seed available after harvesting. About one-third of emergent seedlings were still alive during the middle of the following dry season. Our results indicate that seedling recruitment in E. miniata is limited by both seed supply and microsite availability. However, seed predation by ants reduces the likelihood of seedling establishment from low to virtually zero, which suggests that it plays a potentially important role in the population dynamics of savanna eucalypts.

Seed preferences by rodents in the agri-environment and implications for biological weed control.

Post-dispersal seed predation and endozoochorous seed dispersal are two antagonistic processes in relation to plant recruitment, but rely on similar preconditions such as feeding behavior of seed consumers and seed traits. In agricultural landscapes, rodents are considered important seed predators, thereby potentially providing regulating ecosystem services in terms of biological weed control. However, their potential to disperse seeds endozoochorously is largely unknown. We exposed seeds of arable plant species with different seed traits (seed weight, nutrient content) and different Red List status in an experimental rye field and assessed seed removal by rodents. In a complementary laboratory experiment, consumption rates, feeding preferences, and potential endozoochory by two vole species (Microtus arvalis and Myodes glareolus) were tested. Seed consumption by rodents after 24 h was 35% in the field and 90% in the laboratory. Both vole species preferred nutrient-rich over nutrient-poor seeds and M. glareolus further preferred light over heavy seeds and seeds of common over those of endangered plants. Endozoochory by voles could be neglected for all tested plant species as no seeds germinated, and only few intact seeds could be retrieved from feces. Synthesis and applications. Our results suggest that voles can provide regulating services in agricultural landscapes by depleting the seed shadow of weeds, rather than facilitating plant recruitment by endozoochory. In the laboratory, endangered arable plants were less preferred by voles than noxious weeds, and thus, our results provide implications for seed choice in restoration approaches. However, other factors such as seed and predator densities need to be taken into account to reliably predict the impact of rodents on the seed fate of arable plants.

The ecophysiology of seed persistence: a mechanistic view of the journey to germination or demise.

Seed persistence is the survival of seeds in the environment once they have reached maturity. Seed persistence allows a species, population or genotype to survive long after the death of parent plants, thus distributing genetic diversity through time. The ability to predict seed persistence accurately is critical to inform long-term weed management and flora rehabilitation programs, as well as to allow a greater understanding of plant community dynamics. Indeed, each of the 420000 seed-bearing plant species has a unique set of seed characteristics that determine its propensity to develop a persistent soil seed bank. The duration of seed persistence varies among species and populations, and depends on the physical and physiological characteristics of seeds and how they are affected by the biotic and abiotic environment. An integrated understanding of the ecophysiological mechanisms of seed persistence is essential if we are to improve our ability to predict how long seeds can survive in soils, both now and under future climatic conditions. In this review we present an holistic overview of the seed, species, climate, soil, and other site factors that contribute mechanistically to seed persistence, incorporating physiological, biochemical and ecological perspectives. We focus on current knowledge of the seed and species traits that influence seed longevity under ex situ controlled storage conditions, and explore how this inherent longevity is moderated by changeable biotic and abiotic conditions in situ, both before and after seeds are dispersed. We argue that the persistence of a given seed population in any environment depends on its resistance to exiting the seed bank via germination or death, and on its exposure to environmental conditions that are conducive to those fates. By synthesising knowledge of how the environment affects seeds to determine when and how they leave the soil seed bank into a resistance-exposure model, we provide a new framework for developing experimental and modelling approaches to predict how long seeds will persist in a range of environments.

Seed predators exert selection on the subindividual variation of seed size.

Subindividual variation among repeated organs in plants constitutes an overlooked level of variation in phenotypic selection studies, despite being a major component of phenotypic variation. Animals that interact with plants could be selective agents on subindividual variation. This study examines selective pressures exerted during post-dispersal seed predation and germination on the subindividual variation of seed size in hawthorn (Crataegus monogyna). With a seed offering experiment and a germination test, we estimated phenotypic selection differentials for average and subindividual variation of seed size due to seed predation and germination. Seed size affects germination, growth rate and the probability of an individual seed of escaping predation. Longer seeds showed higher germination rates, but this did not result in significant selection on phenotypes of the maternal trees. On the other hand, seed predators avoided wider seeds, and by doing so exerted phenotypic selection on adult average and subindividual variation of seed size. The detected selection on subindividual variation suggests that the levels of phenotypic variation within individual plants may be, at least partly, the adaptive consequence of animal-mediated selection.

The action of post-dispersal beetles (Coleoptera: Scarabaeidae) and ants (Hymenoptera: Formicidae) on scats of Didelphis spp. (Mammalia: Didelphidae)

A two year study of dung beetles and ants acting on scats of two species of opossum (Didelphis spp.) was carried out. Scats were left in the field in order to detect post-dispersal agents. A portion of each scat (30 %) was examined for seeds in the laboratory. Beetles were recovered from burrows (51% of 84 faecal samples left in the field) where they either buried scats of opossums or were attracted, together with ants, to pitfalls (N = 10) baited with opossum scats. Dung beetles were the main post-dispersal agents of seeds found in scats of opossums, rolling the scats away or burying then on the site of deposition. They buried faeces at 4 to 15 cm in depth (N = 22 tunnels). The main dung beetles identified (medium to large size) were Eurysternus (28.7 % in pitfalls) and Dichotomius (13.7 %), Coprophanaeus (seen only directly on faeces), besides small-bodied beetles (< 10 mm; 57.6 %). The ant Acromirmex sp. transported some seeds from scats. This species was present in 25.5 % of all Formicidae samples (pitfall). These post-dispersal agents contribute to avert scat seed predators such as rodents, and to accelerate seed bank formation.

Por dos años estudiamos los escarabajos coprófagos y las hormigas que actúan en las heces de zarigüellas (Didelphis). Se dejaron excrementos en el campo para descubrir los agentes secundarios de dispersión. Una parte de cada excremento (30 %) fue analizada en laboratorio para estimar el número de semillas. Se recolectaron escarabajos del suelo (51 % de 84 excrementos dejados en el campo). También capturamos escarabajos y hormigas con trampas (N= 10). Los escarabajos coprófagos son los principales agentes secundarios de dispersión. Ruedan los excrementos o los entierran a 4-15 cm de profundidad (N= 22 túneles). Los escarabajos coprófagos de mayor tamaño fueron Eurysternus cyanescens (28.7 % en trampas), Dichotomius assifer (13.7 %) y Coprophanaeus saphirinus (sólo visto en madrigueras y directamente sobre los excrementos). Los escarabajos de menos de 10 mm fueron el 57.6 %. La hormiga Acromirmex sp. fue 25.5 % del total de hormigas capturadas en trampas. Hallamos varias especies de semillas en los excrementos, muchos de ellos enterrados por los escarabajos, y algunas fueron extraídas por las hormigas. Estos agentes secundarios ayudan a evitar los depredadores de semillas (eg. roedores) y aceleran la formación del banco de semillas, pues no las comen.

Post-dispersal predation on Pinus sylvestris seeds by Fringilla spp: ground substrate affects selection for seed color.

Background matching might lower the risk of seeds being eaten by seed predators that search visually. In aviary experiments, we analyzed the selection of diff erent-colored seeds by ground-feeding finches (Fringillacoelebs and F.montifringilla) against four naturally occurring forest soil substrates. The substrates were fresh burn (black), 6-year-old burn (brown), mineral soil (pale yellow) and Pleuroziumschreberi feather moss (green). We used color-sorted seeds of Pinussylvestris, a species with a large natural variation in seed color, ranging from pale yellow to black. Although seeds were scattered on the substrates at a density of only 91 seeds m-2, birds removed seeds effectively. Both bird species found more pale than dark seeds on the fresh burn substrate. F. montifringilla also recovered more pale than dark seeds on the old burn, and more dark than pale seeds on mineral soil. In moss, the birds found very few seeds compared to the other substrates, and there was no color discrimination. P.sylvestris is frequently regenerating after fire, suggesting that dark seeds would be favored under selection from visually searching predators. Fire-adapted conifers with serotinous cones, e.g., Pinuscontorta ssp. latifolia, which spread their seeds primarily on freshly burnt surfaces, produce uniformly black or dark brown seeds. However, regeneration of the non-serotinous P.sylvestris is often extended for several years after a fire, during which substrate color and structure change. This may have helped to maintain variation in seed color. When regeneration of a plant species occurs on a substrate of uniform color, we believe that selection by visually searching seed predators will result in the evolution of cryptic seed color.

Post-dispersal predation and scatterhoarding of Dipteryx panamensis (Papilionaceae) seeds by rodents in Panama.

In tropical rain forests of Central America, the canopy tree Dipteryx panamensis (Papilionaceae) fruits when overall fruit biomass is low for mammals. Flying and arboreal consumers feed on D. panamensis and drop seeds under the parent or disperse them farther away. Seeds on the ground attract many vertebrate seed-eaters, some of them potential secondary seed dispersers. The fate of seeds artificially distributed to simulate bat dispersal was studied in relation to fruitfall periodicity and the visiting frequency of diurnal rodents at Barro Colorado Island (BCI), Panama. The frequency of visits by agoutis is very high at the beginning of fruitfall, but in the area close (<50 m) to fruiting trees (Dipteryx-rich area) it declines throughout fruiting, whereas it remains unchanged farther (>50 m) away (Dipteryx-poor and Gustavia-rich area). Squirrels were usually observed in the Dipteryx-rich area. Along with intense post-dispersal seed predation by rodents in the Dipteryx-rich area, a significant proportion of seeds were cached by rodents in the Dipteryx-poor area. Post-dispersal seed predation rate was inversely related to hoarding rate. A significantly greater proportion of seeds was cached in March, especially more than 100 m from the nearest fruiting tree. This correlates with the mid-fruiting period, i.e. during the height of D. panamensis fruiting, when rodents seem to be temporarily satiated with the food supply at parent trees. Hoarding remained high toward April, i.e. late in the fruiting season of D. panamensis. Low survival of scatterhoarded seeds suggests that the alternative food supply over the animal's home-ranges in May-June 1990 was too low to promote survival of cached seeds. Seedlings are assumed to establish in the less-used area of the rodents' home-range when overall food supply is sufficient to satiate post-dispersal predators.

Post-dispersal predation of Acacia farnesiana seeds by Stator vachelliae (Bruchidae) in Central America.

Post-dispersal seed predation by the bruchid beetle Stator vachelliae was investigated in Santa Rosa National Park, Costa Rica. This insect finds the seeds of the leguminous Acacia farnesiana in the feces of horses, deer, and ctenosaur lizards, the current major dispersers. Patterns of oviposition and pre-adult survival of beetles in the seeds were investigated in a series of experiments using fresh horse dung. S. vachelliae never minded into the dung balls, attacking only those seeds located on the surface. Fresh horse dung did not attract insects more readily than dry dung. The proportion of seeds attacked was not related to their density in a defecation, and was similar in three areas with different densities of the host plant. In a fourth area with no fruiting A. farnesiana shrubs all seeds survived insect predation. Bruchids attacked a greater proportion of seeds at 1 m than at 5 m from the edge of the shrub's crown. Seeds were mainly removed from horse dung by rodents with similar intensity in all areas and at both distances; this seed removal interfered with bruchid oviposition and probably with bruchid survival. S. vachelliae oviposited less frequently on seeds in dung fully exposed to sun. When oviposition on a dung pile was high, the distribution of eggs on the seeds was clumped, suggesting that some seeds were preferred to others. By the end of the dry season, bruchids stopped attacking the seeds. The results show that the fate of both seeds and bruchids is greatly influenced by the location and time of defecation.