Does seed ingestion by bats enhance germination? A new meta‐analysis 15 years later

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Sensitivity of seed germination to water stress in high-altitude populations of a threatened palm species

• Divergence in seed germination patterns among populations of the same species is important for understanding plant responses to environmental gradients and potential plant sensitivity to climate change. In order to test responses to flooding and decreasing water potentials, over 3 years we germinated and grew seeds from three habitats of Euterpe edulis Mart. occurring along an altitudinal gradient.
• Seed germination and root growth were evaluated under different water availability treatments: control, flood, −0.4 MPa, −0.8 MPa, in the years 2012, 2013 and 2014, and in the final year of the experiment (2014) at −1.0 MPa and −1.5 MPa.
• Seeds from the montane habitat did not germinate in the flooding treatment. Seed germination of all three habitats decreased in the −1.5 MPa treatment and the montane habitat had lowest germination in this treatment. Time required for half of the seeds to germinate increased up to −0.8 MPa. Seeds from montane habitats germinated more slowly in all treatments. The only difference in seed germination synchrony was an increase in the submontane population under the flooding treatment. However, synchrony decreased at the lowest water potentials. Roots of the montane population were more vigorous in most treatments, except at −0.8 MPa.
• The unusual ability of these seeds to germinate at low water potentials might be related to early seed germination at the onset of the rainy season, which potentially decreases seed predation pressure. Seeds of the montane population were more sensitive to both types of water stress. A predicted increase in the frequency and intensity of extreme high rainfall or drought events may predispose early stages of this population to adverse factors that might negatively affect population viability with elevational in future climate change scenarios.

     

Small mammal herbivores mediate the effects of soil nitrogen and invertebrate herbivores on grassland diversity

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Plant‐driven changes in soil microbial communities influence seed germination through negative feedbacks

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Heteromorphic seeds of wheat wild relatives show germination niche differentiation

• Crop wild relatives are fundamental genetic resources for crop improvement. Wheat wild relatives often produce heteromorphic seeds that differ in morphological and physiological traits. Several Aegilops and Triticum species possess, within the same spikelet, a dimorphic seed pair, with one seed being larger than the other. A comprehensive analysis is needed to understand which traits are involved in seed dimorphism and if these aspects of variation in dimorphic pairs are functionally related.
• To this end, dispersal units of Triticum urartu and five Aegilops species were X‐rayed and the different seed morphs weighed. Germination tests were carried out on seeds, both dehulled and left in their dispersal units. Controlled ageing tests were performed to detect differences in seed longevity among seed morphs, and the antioxidant profile was assessed in terms of antioxidant compounds equipment and expression of selected antioxidant genes. We used PCA to group seed morphs sharing similar patterns of germination traits, longevity estimates and antioxidant profile.
• Different seed morphs differed significantly in terms of mass, final germination, germination timing, longevity estimates and antioxidant profile in most of the tested species. Small seeds germinated slower, had lower germination when left in their dispersal units, a higher antioxidant potential and were longer‐lived than large seeds. The antioxidant gene expression varied between morphs, with different patterns across species but not clearly reflecting the phenotypic observations.
• The results highlight different trait trade‐offs in dimorphic seeds of Aegilops and T. urartu, affecting their germination phenology and longevity, thereby resulting in recruitment niche differentiation.

     

Effect of seed passage through vertebrate frugivores'' guts on germination: a review

The capacity of seeds to germinate after ingestion by frugivores is important for the population dynamics of some plant species and significant for the evolution of plant-frugivore interactions. In this paper the effects of different vertebrates on seed germination of nearly 200 plant species are reviewed, searching for patterns that predict the circumstances in which germination of seeds is enhanced, inhibited, or unaffected by the passage through the digestive tract of a seed disperser. It was found that seed dispersers commonly have an effect on the germinability of seeds, or on the rate of germination, or both, in about 50% of the plants they consume, although the diversity of animal species tested so far is still rather low (42 bird species, 28 non-flying mammals, 10–15 bats, 12 reptiles, 2 fishes). Enhancement of germination occurred about twice as often as inhibition.

In spite of the morphological and physiological differences in their digestive tracts, the different animal groups tested have similar effects on seed germination, although non-flying mammals tend to influence germination slightly more often than the other groups. Data on fishes are still too scarce for any generalization. Seed retention time in the dispersers' digestive tract is one factor affecting germination, and helps to explain the variation in seed responses observed among plant species, and even within a species. However other factors are also important; for example, the type of food ingested along with the fruits may affect germination through its influence on chemical or mechanical abrasion of the seed coat. Seed traits such as coat structure or thickness may themselves be responsible for some of the variation in seed retention times. Seeds of different sizes, which usually have different transit times through frugivores, and seeds of either fleshy or dry fruits, show often similar germination response to gut passage.

Seeds of different plants species differ strongly in their germination response after ingestion, even by the same frugivore species. Congeneric plants often show little consistency in their response. Even within a species variation is found which can be related to factors such as the environmental conditions under which germination takes place, seed morphology, seed age, and the season when the seeds are produced.

The effect of gut passage on germination differs between tropical and temperate zones. Seed germination of both shrubs and trees (data on herbaceous species are still scarce) in the temperate zone is more frequently enhanced than in the tropics. This result supports the hypothesis that enhanced germination may be more advantageous in unpredictable or less constant environments. Significant differences in frugivore-mediated germination are also found among different life forms. In both tropical and temperate zones, trees appear to be consistently more affected than shrubs or herbs. This might be due to an overall higher thickness of the seed coats, or to a higher frequency of seed-coat dormancy in tree species.

The influence of frugivory upon the population dynamics of a species has to be evaluated relative to other factors that influence germination and seedling recruitment at a particular site. Whether seed ingestion by dispersers is really advantageous to a plant (as has commonly been assumed) can only be assessed if we also determine the fate of the ingested seeds under natural conditions, and compare it to the fate of seeds that have not been ingested.     

Is the loss of Australian digging mammals contributing to a deterioration in ecosystem function?

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Effects of warming on seed germination of woody species in temperate secondary forests

• Seed germination, a critical stage of the plant life cycle providing a link between seeds and seedlings, is commonly temperature-dependent. The global average surface temperature is expected to rise, but little is known about the responses of seed germination of woody plants in temperate forests to warming.
• In the present study, dried seeds of 23 common woody species in temperate secondary forests were incubated at three temperature sequences without cold stratification and after experiencing cold stratification. We calculated five seed germination indices and the comprehensive membership function value that summarized the above indicators.
• Compared to the control, +2 and +4 °C treatments without cold stratification shortened germination time by 14% and 16% and increased the germination index by 17% and 26%, respectively. For stratified seeds, +4 °C treatment increased germination percentage by 49%, and +4 and +2 °C treatments increased duration of germination and the germination index, and shortened mean germination time by 69%, 458%, 29% and 68%, 110%, 12%, respectively. The germination of Fraxinus rhynchophylla and Larix kaempferi were most sensitive to warming without and with cold stratification, respectively. Seed germination of shrubs was the least sensitive to warming among functional types.
• These findings indicate warming (especially extreme warming) will enhance the seedling recruitment of temperate woody species, primarily via shortening the germination time, particularly for seeds that have undergone cold stratification. In addition, shrubs might narrow their distribution range

     

Diaspore dispersal season influences root growth and seed traits,but not germination responses,of sympatric Piper species in a seasonal forest

• Seeds may differ in terms of dormancy, longevity, sensitivity to desiccation and dry mass, according to the timing (dry season/rainy season) of diaspore dispersal. In addition, seasonal variations in temperature and water availability can act as signals of the season during seed development, influencing germination responses and root growth. We evaluated the effects of temperature variations and water availability on germination parameters, root growth and seed traits of four coexisting Piper species in seasonal vegetation that differed in diaspore dispersal timing.
• Eight temperature treatments (15, 20, 23, 25, 28, 30, 35 °C, and alternate 30 °C–20 °C) and four induced water potentials (0, −0.3, −0.6 and −1.2 MPa) were used. The parameters germination onset, germination percentage (G%), mean germination time (MGT), root elongation, seed longevity during ex situ storage and dry mass of seeds were evaluated.
• Germination responses observed were independent of the diaspore dispersal timing, such as variations in germination onset, G% and MGT, both in temperature and water availability treatments. In contrast, root elongation, longevity and dry mass of seeds varied according to the time of diaspore dispersal.
• Our results corroborate the hypothesis that the timing of diaspore dispersal is an important factor in controlling the initial development of seedlings in seasonal vegetation, but not in germination responses. The predominance of negative effects of temperature increases and water deficit on root growth shows that the initial stages of plant development can be strongly impacted by these environmental factors.

     

Role of Brycinus lateralis (Teleostei: Alestidae) in dispersal and germination of Nymphaea nouchali (Angiospermae: Nymphaeaceae) seeds on a seasonal floodplain of the Okavango Delta,Botswana

Seed passage through the gut of vertebrates can be important for seed dispersal, but might influence seed viability. The ability of seeds to germinate after ingestion by seed-eating fish is important for the population dynamics of some plant species, and significant in the evolution of plant–fish interactions. Certain fish in the Okavango Delta, Botswana, are fruit- and seed-eaters and could act as seed dispersers. We sampled 14 fish species in 2013, finding Nymphaea nouchali var. caerulea seeds in the digestive tracts of eight, most commonly in the striped robber Brycinus lateralis. Seeds extracted from the gut of this species had an overall mean germination success of 11.7%. This fish species might well be a legitimate seed disperser, having a positive effect on seed dispersal from parent plants in the Okavango Delta. The current study represents one of the first investigations of the likelihood of seed dispersal by fish on the African continent.     

Effects of season and population size on pollination and reproductive output in a Mediterranean shrub

• Pollinator guilds may change throughout extended flowering periods, affecting plant reproductive output, especially in seasonal climates. We hypothesised a seasonal shift in pollinator guild and an autumn reduction in pollinator abundance, especially in small and sparse populations.
• We recorded pollinator identity, abundance and behaviour in relation to flower density from plant to population throughout the extended flowering of Ononis tridentata. We evaluated female reproductive output by recording pollination success and pre‐dispersal seed predation in eight populations of contrasting size and density. Offspring quality was also characterised through seed weight and germination.
• A diverse guild of insects visited O. tridentata in spring, while only Apis mellifera was observed in autumn. Visitation frequency did not vary seasonally, but the number of flowers per foraging bout was lower, and seeds were heavier and had a higher germination rate in autumn. Plant and neighbourhood flowering display were not related to pollinator visitation frequency or behaviour. However, the rate of fertilised ovules, seed set and autumn flowering display size were positively related to population density.
• The maintenance of pollination in autumn enhances the reproductive performance of O. tridentata due to higher quality of autumn seed, and to a large reduction in seed predator pressure. We also suggest that observed changes in pollinator behaviour could be one of the processes behind seasonal variation in seed performance, since geitonogamous crosses were less likely to occur in autumn.

     

Does fire drive fatty acid composition in seed coats of physically dormant species?

• Seed dormancy is the key driver regulating seed germination, hence is fundamental to the seedling recruitment life-history stage and population persistence. However, despite the importance of physical dormancy (PY) in timing post-fire germination, the mechanism driving dormancy-break within seed coats remains surprisingly unclear. We suggest that seed coat chemistry may play an important role in controlling dormancy in species with PY. In particular, seed coat fatty acids (FAs) are hydrophobic, and have melting points within the range of seed dormancy-breaking temperatures. Furthermore, melting points of saturated FAs increase with increasing carbon chain length. We investigated whether fire could influence seed coat FA profiles and discuss their potential influence on dormancy mechanisms.
• Seed coat FAs of 25 species within the Faboideae, from fire-prone and fire-free ecosystems, were identified and quantified through GC–MS. Fatty acid profiles were interpreted in the context of species habitat and interspecific variation.
• Fatty acid compositions were distinct between species from fire-prone and fire-free habitats. Fire-prone species tended to have longer saturated FA chains, a lower ratio of saturated to unsaturated FA, and a slightly higher relative amount of FAs compared to fire-free species.
• The specific FA composition of seed coats of fire-prone species indicated a potential role of FAs in dormancy mechanisms. Overall, the distinct FA composition between fire-prone and fire-free species suggests that chemistry of the seed coat may be under selection pressure in fire-prone ecosystems.

     

Global effort allocation in marine mammal research indicates geographical,taxonomic and extinction risk‐related biases

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Germination of Prosopis juliflora (Sw) DC seeds after scarification treatments

Invasive plant species are the second most important threat to global biodiversity loss after land‐use change. Invasive species can modify native community composition, deplete species diversity and affect ecosystem processes. The Caatinga is one of the most human‐affected Brazilian ecosystems owing to non‐sustainable use of its natural resources. Prosopis juliflora is an important invasive plant species in the Caatinga ecosystem. Seed germination is a critical stage in plant life cycles and is a major factor in the establishment and success of invasive plant species. Among the factors that affect seed germination and dormancy, coat‐imposed seems to be the most important for P. juliflora. In Prosopis species, the ingestion of fruits by wild and domestic animals may promote and accelerate germination, enhancing the dispersal of seeds and fruits of these species. We investigated the germination capacity of P. juliflora seeds after artificial mechanical and chemical scarification and analyzed the changes in seedling vigor caused by the scarification treatments. Germination rate, germination time (TMG) and germination synchrony (E) differed significantly with the length of the scarification treatments in H₂SO₄ for both seeds with endocarps and seeds without endocarps (non‐endocarp seeds). Sulfuric acid affected plant survival more strongly than germination rate, particularly in non‐endocarp seeds.     

Plant and small mammal richness correlate positively in a biodiversity hotspot

Hotspots of biodiversity are important areas in facilitating an understanding of species richness and its maintenance. Herbivores can increase plant richness by reducing dominant plant species thus providing space for subdominant species. As small mammals are abundant in the Succulent Karoo and therefore might affect plant richness by means of herbivory, we tested if this mechanism might exist in the Succulent Karoo in southern Africa, a biodiversity hotspot due to its extraordinary plant richness. At ten ecologically different study sites we measured plant and small mammal richness and diversity and determined 11 abiotic factors including soil composition, altitude and rainfall. We found positive correlations between plant richness and the number of small mammal species. A general linear model revealed that the number of small mammal species was more important than abiotic factors in explaining variation in plant richness. To test whether small mammals might directly influence plant richness, we studied the influence of the bush-Karoo rat Otomys unisulcatus, a central place forager, on the plant community. The immediate surroundings of occupied O. unisulcatus nests showed significantly higher plant richness than control areas. We conclude that small mammals can have a positive effect on plant richness in the Succulent Karoo. While experimental data are needed to support these correlative results, the results of our study indicate that areas of high small mammal richness should be included in conservation programs of the Succulent Karoo.     

Mammals,agri‐environment schemes and set‐aside – what are the putative benefits?

• 1 The impacts of agricultural intensification on farmland wildlife have been the subject of increasing concern, particularly over the last two decades. Population declines have occurred for a number of mammalian species, sometimes drastically so, and changes in farming practice are believed to be significant contributory factors.
• 2 The major policy instruments for delivering environmental benefits on farmland are agri‐environment schemes. These encourage farmers to adopt more environmentally sensitive farming practices to promote farmland biodiversity. Additionally, compulsory set‐aside, which reduces agricultural surplus, could also have positive impacts on wildlife. In this paper we consider some of the putative benefits of agri‐environment schemes and set‐aside for mammals.
• 3 We review how establishment and management options within agri‐environment schemes and set‐aside might affect habitat resources for mammals. For example, conservation headlands increase plant and invertebrate resources within the crop edge for mammals such as wood mice. Grassy field margins can support communities of smaller mammals, and hedgerows may act as important commuting and hunting routes. Their potential will depend on factors such as seed mixtures used, timing and severity of cutting, and length of time they have been in place.
• 4 At a farm level, habitat heterogeneity may be increased through organic agriculture, which is supported by some agri‐environment schemes. Studies suggest significant benefits to mammals, including wood mice and bats. However, it is increasingly recognized that effective conservation of farmland mammals must seek solutions at the landscape scale, addressing such issues as habitat connectivity between farms. One approach may be the better targeting of scheme agreements.
• 5 We suggest that agri‐environment schemes and set‐aside can contribute to the conservation of mammals on farmland. Recent policy changes are likely to have further positive impacts on farmland wildlife but appropriate mammal monitoring programmes must be developed rigorously to assess their effects.

     

Masting behaviour in a Mediterranean pine tree alters seed predator selection on reproductive output

• Context‐dependency in species interactions is widespread and can produce concomitant patterns of context‐dependent selection. Masting (synchronous production of large seed crops at irregular intervals by a plant population) has been shown to reduce seed predation through satiation (reduction in rates of seed predation with increasing seed cone output) and thus represents an important source of context‐dependency in plant‐animal interactions. However, the evolutionary consequences of such dynamics are not well understood.
• Here we describe masting behaviour in a Mediterranean model pine species (Pinus pinaster) and present a test of the effects of masting on selection by seed predators on reproductive output. We predicted that masting, by enhancing seed predator satiation, could in turn strengthen positive selection by seed predators for larger cone output. For this we collected six‐year data (spanning one mast year and five non‐mast years) on seed cone production and seed cone predation rates in a forest genetic trial composed by 116 P. pinaster genotypes.
• Following our prediction, we found stronger seed predator satiation during the masting year, which in turn led to stronger seed predator selection for increased cone production relative to non‐masting years.
• These findings provide evidence that masting can alter the evolutionary outcome of plant‐seed predator interactions. More broadly, our findings highlight that changes in consumer responses to resource abundance represent a widespread mechanism for predicting and understanding context dependency in plant‐consumer evolutionary dynamics.

     

Genome‐wide identification and characterization of microRNAs responding to ABA and GA in maize embryos during seed germination

• MicroRNAs (miRNAs) are an important class of non‐coding small RNAs that regulate the expression of target genes through mRNA cleavage or translational inhibition. Previous studies have revealed their roles in regulating seed dormancy and germination in model plants such as Arabidopsis thaliana, rice (Oryza sativa) and maize (Zea mays). However, the miRNA response to exogenous gibberellic acid (GA) and abscisic acid (ABA) during seed germination in maize has yet to be explored.
• In this study, small RNA libraries were generated and sequenced from maize embryos treated with GA, ABA or double‐distilled water as control.
• A total of 247 miRNAs (104 known and 143 novel) were identified, of which 45 known and 53 novel miRNAs were differentially expressed in embryos in the different treatment groups. In total, 74 (37 up‐regulated and 37 down‐regulated) and 55 (23 up‐regulated and 32 down‐regulated) miRNAs were expressed in response to GA and to ABA, respectively, and a total of 18 known and 38 novel miRNAs displayed differential expression between the GA‐ and ABA‐treated groups. Using bioinformatics tools, we predicted the target genes of the differentially expressed miRNAs. Using GO enrichment and KEGG pathway analysis of these targets, we showed that miRNAs differentially expressed in our samples affect genes encoding proteins involved in the peroxisome, ribosome and plant hormonal signalling pathways.
• Our results indicate that miRNA‐mediated gene expression influences the GA and ABA signalling pathways during seed germination.

     

Linking seed germination and plant height: a case study of a wetland community on the eastern Tibet Plateau

• Seed germination is the earliest trait expressed in a plant's life history, and it can directly affect the expression of post‐germination traits. Plant height is central to plant ecological strategies, because it is a major determinant of the ability of a species to compete for light. Thus, linking seed germination and plant height at the community level is very important to understanding plant fitness and community structure.
• Here, we tested storage condition and temperature requirements for germination of 31 species from a wetland plant community on the eastern Tibet Plateau and analysed correlation of germination traits with plant height in relation to storage condition.
• Germination percentage was positively related to plant height, and this relationship disappeared when seeds were incubated at a low temperature (i.e. 5 °C) or after they were stored under wet‐cold conditions. The response of seeds to dry+wet–cold storage was negatively related to plant height. Based on the scores of each species on the first two principal components derived from PCA, species were classified into two categories by hierarchical clustering, and there was a significant difference between germination and plant height of species in these two categories.
• These results suggest that the requirements for seed germination together with seasonal change in environmental conditions determine the window for germination and, in turn, plant growth season and resource utilisation and ultimately plant height.

     

Small mammal controls on the climate‐driven range shift of woody plant species

Climate change is resulting in shifts in species’ ranges as species inhabit new climatically suitable areas. A key factor affecting range‐shifts is the interaction with predators. Small mammals, being primary seed predators and dispersers in forest ecosystems, may play a major role in determining which plant species will successfully expand and the rate at which range‐shifts will occur. Plants dispersing seeds beyond the species’ current range limits will encounter seed predators to which these seeds are novel; however, empirical studies of seed predator–novel seed interactions are lacking. The aims of our study were to: 1) quantify seed selection by small mammals presented with ‘novel’ seeds; 2) quantify the post‐selection fate of ‘novel’ seeds; and 3) identify seed traits that affect seed selection and post‐selection seed fate. We designed a field experiment exposing small mammal communities to novel seeds produced by plants expected to shift their ranges in response to climate change. We matched novel seeds with reference ‘familiar’ seeds and studied key steps defining interactions between small mammals and novel seeds. We found that the probability of selection of a novel seed varied among species and was, at times, higher than the selection probability of familiar seeds. Key traits that affected seed selection and the distance a seed was dispersed for caching were shell hardness and seed mass. We also found that 33% of dispersed seeds were cached in optimal germination sites (e.g. within fallen logs and buried under the leaf litter mat). Through seed emergence trials we found that emergence was higher for larger seeds, suggesting that the role of small mammals may be modulated by emergence rates. Our results suggest that the interaction between small mammals and novel seeds may have cascading effects on climate‐induced plant range shifts and community composition.