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.     

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.     

The role of Rhytidoponera metallica (Hymenoptera,Formicidae) in facilitating post‐fire seed germination of three ant‐dispersed legume species

The fire avoidance hypothesis proposes that a benefit of seed dispersal by ants (myrmecochory) is to protect seeds from being killed during fire and to facilitate post‐fire germination of seeds that require heat shock to break their physical dormancy. The aim of this study was to quantify the effect of fire and seed burial by a predominant seed‐dispersing ant, Rhytidoponera metallica (subfamily: Ectatomminae) on germination levels of three ant‐dispersed legume species (Pultenaea daphnoides, Acacia myrtifolia and Acacia pycnantha). Experimental burial of seeds within aluminium cans at a site prior to being burnt and at an adjacent unburnt site showed that fire increased germination levels, particularly for seeds buried at 1‐ and 2‐cm deep and that overall, germination levels differed among the three plant species. To quantify seed burial depths and post‐fire germination levels facilitated by R. metallica ants, seeds were fed to colonies prior to fire at the burnt and unburnt sites. Of the seeds buried within nests that were recovered, between 45% and 75% occurred within the upper 6 cm of the soil profile, although unexpectedly, greater percentages of seeds were recovered from the upper 0–2 cm of nests in the unburnt site compared with nests in the burnt site. Germination levels of buried seeds associated with R. metallica nests ranged from 21.2% to 29.5% in the burnt site compared with 3.1–14.8% in the unburnt site. While increased seed germination levels were associated with R. metallica nests following fire, most seeds were buried at depths below those where optimal temperatures for breaking seed dormancy occurred during the fire. We suggest that R. metallica ants may provide fire avoidance benefits to myrmecochorous seeds by burying them at a range of depths within a potential germination zone defined by intra‐ and inter‐fire variation in levels of soil heating.     

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.     

Mammal Abundances and Seed Traits Control the Seed Dispersal and Predation Roles of Terrestrial Mammals in a Costa Rican Forest

In Neotropical forests, mammals act as seed dispersers and predators. To prevent seed predation and promote dispersal, seeds exhibit physical or chemical defenses. Collared peccaries (Pecari tajacu) cannot eat some hard seeds, but can digest chemically defended seeds. Central American agoutis (Dasyprocta punctata) gnaw through hard‐walled seeds, but cannot consume chemically defended seeds. The objectives of this study were to determine relative peccary and agouti abundances within a lowland forest in Costa Rica and to assess how these two mammals affect the survival of large seeds that have no defenses (Iriartea deltoidea, Socratea exorrhiza), physical defenses (Astrocaryum alatum, Dipteryx panamensis), or chemical defenses (Mucuna holtonii) against seed predators. Mammal abundances were determined over 3 yrs from open‐access motion‐detecting camera trap photos. Using semi‐permeable mammal exclosures and thread‐marked seeds, predation and dispersal by mammals for each seed species were quantified. Abundances of peccaries were up to six times higher than those of agoutis over 3 yrs, but neither peccary nor agouti abundances differed across years. Seeds of A. alatum were predominantly dispersed by peccaries, which did not eat A. alatum seeds, whereas non‐defended and chemically defended seeds suffered high levels of predation, mostly by peccaries. Agoutis did not eat M. holtonii seeds. Peccaries and agoutis did not differ in the distances they dispersed seeds. This study shows that seed fates are contingent upon many factors such as seed defenses, frugivore–granivore abundances, and seed‐handling capabilities. Mammal–seed interactions are complex; the outcomes of these interactions depend on the inherent characteristics of seeds and their potential dispersers.     

A Host Creates an Enemy‐free Space for Mistletoes by Reducing Seed Predation Caused by a Woodboring Beetle: A Hypothesis

Parasitic plants rely on host plants for nutrition. The number of host species varies largely between groups, from single species or genus to hundreds of species. Relative abundance of the host and evolutionary history are the main requisites for parasitic plants to develop specificity to abundant hosts. In the present study, we suggest a novel mechanism by which a hemiparasitic mistletoe can develop local specificity mediated by its host. First, we describe a novel interaction in which a woodboring beetle (Hypothenemus obscurus) preys on mistletoe seeds (Psittacanthus plagiophyllus) attached to tree branches. This beetle preys more frequently on seeds deposited on branches of non‐host species than on branches of its unique local host species (53 percent on average vs. 26 percent respectively). We hypothesize that local host specificity for this mistletoe could be partly mediated by beetle‐host incompatibility, since the host offers a predation‐free space in which mistletoes have better chances to grow. Furthermore, that the exceptional gum exudates produced by this unique host species minimize beetle attacks on branches, thus reducing predation of mistletoe seeds. This novel tritrophic interaction opens an avenue for research on macroscopic host‐specificity mechanisms that occur at the level of the host bark and that have been poorly studied by plant ecologists.     

A first step towards inferring levels of long-distance dispersal during past expansions

Improving the realism of spatially explicit demographic models is important for better inferring the history of past populations and for understanding the genetic bases of adaptation and speciation. One particular type of demographic event to take into account is long-distance dispersal (LDD). The goals of this study are to explore the impact of various levels of LDD on genetic diversity and to show to what extent LDD levels can be correctly inferred from multilocus data sets using an approximate Bayesian computation approach. We therefore incorporated LDD into a 2D stepping stone forward simulation framework coupled to a coalescent backward simulation step to generate genetic diversity at 100 microsatellite markers under various demographic conditions relevant to recent human evolution. Our results confirm that LDD considerably increases genetic diversity within demes and decreases levels of diversity between demes. By controlling the spatial occurrence of LDD, it appears that LDD events occurring during a phase of range expansion into new territories are more important in maintaining genetic diversity than those occurring in the wake of the expansion or when colonization is over. We also show that it is possible to infer whether LDD has occurred during a range expansion, but our results suggest that one can only approximately estimate the extent of LDD based on genetic summary statistics.     

浙江省典型天然次生林主要树种空间分布格局及其关联性

松阔混交林和常绿阔叶林是亚热带地区天然次生林代表性的森林类型,通过研究主要树种分布变动趋势,可以有效地指导森林经营措施。在该地区4个1hm~2典型样地,在0—30m尺度范围内综合分析了主要树种的空间分布格局及种间关联性,并对同一树种分发育阶段在不同森林群落中的种群空间分布格局进行了比较,以探讨亚热带地区天然次生林群落空间格局形成和种群维持机制。样地1和2为松阔混交林,其中样地1的马尾松密度较低,样地3和4为常绿阔叶林。研究结果表明:(1)以完全随机模型为零假设时,样地1的主要种群在小尺度(10 m)呈聚集分布,随尺度增加呈随机分布;样地2—4的主要种群在所有尺度呈聚集分布,随尺度增加聚集强度逐渐减弱;以异质泊松模型为零假设时,4个样地的主要种群在大部分尺度呈随机分布;(2)青冈和苦槠的小树(5.0 cm≤DBH10.0 cm)在4样地的所有尺度以聚集分布为主,大树(DBH≥10.0 cm)在松阔混交林样地呈随机分布趋势,但在常绿阔叶林样地青冈在0—20 m尺度、苦槠在所有尺度呈聚集分布;(3)松阔混交林中建群种马尾松和其他树种的种间关联性,在样地1的小尺度为负相关,随尺度增加为不相关,在样地2的所有尺度为负相关;常绿阔叶林中建群种青冈和其他树种的种间关联性在在样地3的小尺度为负相关,随尺度增加为不相关,在样地4的所有尺度为负相关;所有伴生树种的种间关联性以负相关为主。结果说明,种群空间分布格局及其关联性随群落结构和空间尺度的不同而出现变化,在松阔混交林和常绿阔叶林群落格局形成中除了扩散限制和生境异质性以外,密度制约机制在松阔混交林中发挥了重要作用,而在常绿阔叶林中其作用随着树木生活史阶段的提高而减弱。     

Edge Effects Act Differentially on Multiple Early Regeneration Stages of a Shade‐tolerant Tree Tapirira mexicana

Forest fragmentation is pervasive in tropical landscapes, and one pathway by which fragmentation may negatively impact populations is via edge effects. Early life‐stages are particularly important for species regeneration as they act as bottlenecks, but how edge effects may act differentially on different life‐stages is unknown. This study evaluated edge effects on multiple early life‐stages of a currently common animal‐dispersed, shade‐tolerant tree Tapirira mexicana (Anacardiaceae). The study was conducted in tropical premontane wet forest fragments in a highly deforested region of Costa Rica. The stages assessed were pre‐dispersal predation, primary dispersal, post‐dispersal predation, secondary dispersal, ex situ germination, in situ seed longevity, first and second year seedling abundance, second year seedling survivorship, and basal diameter growth. Results showed that impacts of edge effects were not equal across stages, but were limited to specific stages and times. One stage which may act as a bottleneck for species regeneration was pre‐dispersal predation. Over 60 percent of the seeds were predated by larvae, and predation was higher near the edge than interior habitat. Seeds lost viability within 10 d in the forest. Germination to first year seedling stage was also lower near edges, but such effect was eliminated within a year after that. Primary dispersal, seedling survivorship, and growth were not affected by proximity to edges, and both secondary dispersal and post‐dispersal predation were rare. This study demonstrates that current population abundance may not guarantee future species persistence and the importance of considering multiple life‐stages for a comprehensive assessment of forest fragmentation effects on species regeneration.     

Woody species tolerance to expansion of the perennial tussock grass Ampelodesmos mauritanica after fire

Abstract. In Mediterranean shrublands, post‐fire accumulation of above‐ground biomass of resprouters is faster than that of seeders. This suggests that resprouters may have a competitive advantage. To test this hypothesis, we used a removal experiment to study the effect of the presence of the dominant tussock‐grass Ampelodesmos mauritanica on the resprouting shrubs Erica multiflora and Globularia alypum and on the seeders Rosmarinus officinalis and Pinus halepensis three and four years after a wildfire. Water potential of target plants was also measured to see if Ampelodesmos removal increased water availability. Ampelodesmos marginally reduced growth of all target species but did not influence survival or water potential of any target species. Our results suggest that the effect of climatically influenced water stress was stronger than the effect of Ampelodesmos neighbours. Plant‐plant interactions in this Mediterranean community are weak after fire and the magnitude of the Ampelodesmos effect does not differ between seeders and resprouters.     

Distribution of myrmecochorous species over the landscape and their potential long-distance dispersal by emus and kangaroos

Topographical heterogeneity can create a mosaic of substrate types leading to the formation of isolated plant populations. Seed dispersal then becomes crucial for the colonization of such suitable but remote substrate types. We surveyed the distribution of seven elaiosome-bearing species (myrmecochores) over 5 km² of natural heathland in southwestern Australia. Ants are the standard means of dispersal of these species, which provide limited dispersal (usually of a few metres). Six species were associated with particular substrate types (dune or swale) and all occurred as discrete populations, on average 270–500 m apart, with closest dune edges 280 m apart. We evaluated the possible roles of emus and kangaroos as alternative agents of long-distance seed dispersal between substrate types. Their droppings contained viable seeds of three of the target species, as well as other myrmecochores, and were evenly distributed over the substrate types. While migration of these plant species between preferred substrate types seems unlikely when considering only their standard dispersal agents (ants), it is highly likely in the presence of emus (in particular) and kangaroos that act as non-standard dispersers. This may have important consequences for plant species conservation by increasing habitat connectivity and favouring regional persistence.     

Characterization of 24 microsatellite markers in 11 species of fire ants in the genus Solenopsis (Hymenoptera: Formicidae)

The social parasite ant Solenopsis daguerrei infests colonies of several mound-building fire ant species. Twenty-four microsatellite markers were isolated from a repeat-enriched genomic library of S. daguerrei. Eleven loci were polymorphic in this ant with two to six alleles per locus. Expected heterozygosity ranged from 0.0222 to 0.7940 among loci. Most microsatellites amplified successfully across the 11 Solenopsis species tested and will be useful for evolutionary genetic studies in this diverse ant group.     

Propagule pressure and colony social organization are associated with the successful invasion and rapid range expansion of fire ants in China

We characterized patterns of genetic variation in populations of the fire ant Solenopsis invicta in China using mitochondrial DNA sequences and nuclear microsatellite loci to test predictions as to how propagule pressure and subsequent dispersal following establishment jointly shape the invasion success of this ant in this recently invaded area. Fire ants in Wuchuan (Guangdong Province) are genetically differentiated from those found in other large infested areas of China. The immediate source of ants in Wuchuan appears to be somewhere near Texas, which ranks first among the southern USA infested states in the exportation of goods to China. Most colonies from spatially distant, outlying areas in China are genetically similar to one another and appear to share a common source (Wuchuan, Guangdong Province), suggesting that long‐distance jump dispersal has been a prevalent means of recent spread of fire ants in China. Furthermore, most colonies at outlier sites are of the polygyne social form (featuring multiple egg‐laying queens per nest), reinforcing the important role of this social form in the successful invasion of new areas and subsequent range expansion following invasion. Several analyses consistently revealed characteristic signatures of genetic bottlenecks for S. invicta populations in China. The results of this study highlight the invasive potential of this pest ant, suggest that the magnitude of international trade may serve as a predictor of propagule pressure and indicate that rates and patterns of subsequent range expansion are partly determined by the interplay between species traits and the trade and transportation networks.     

Seed longevity and fire: germination responses of an exotic perennial herb in NW Patagonian grasslands (Argentina)

Fire affects grassland composition by selectively influencing recruitment. Some exotic species can increase their abundance as a consequence of fire-stimulated seed germination, but response may depend on seed age. Rumex acetosella L. (Polygonaceae, sheep's sorrel) is a cosmopolitan herb that has invaded NW Patagonia's grasslands. This species forms persistent soil seed banks and increases after disturbances, particularly fire. We studied how fire and seed longevity influence R. acetosella germination. In 2008, we conducted laboratory experiments where we exposed different-aged seeds (up to 19 years old) to heat, smoke, charcoal, ash and control treatments. Total percentage germination and mean germination time depended on both seed age and fire treatment. Germination of younger seeds decreased with increasing temperature. There was no general pattern in germination responses of different-aged seeds to smoke, charcoal and ash. While smoke improved the germination of fresh seeds, charcoal decreased germination. Germination of untreated seeds was negatively correlated with seed age, and mean germination time increased with seed age. In most treatments, fresh seeds had lower germination than 1-5-year-old seeds, indicating an after-ripening requirement. Smoke stimulates R. acetosella germination, causing successful recruitment during post-fire conditions. Fresh seeds are particularly responsive to fire factors, possibly because they have not experienced physical degradation and are more receptive to environmental stimuli. Knowing the colonisation potential from the soil seed bank of this species during post-fire conditions will allow us to predict their impact on native communities.     

Role of small rodents in the seed dispersal process: Microcavia australis consuming Prosopis flexuosa fruits

Understanding the functional role of animal species in seed dispersal is central to determining how biotic interactions could be affected by anthropogenic drivers. In the Monte Desert, mammals play different functional roles in Prosopis flexuosa seed dispersal, acting as opportunistic frugivores (endozoochorous medium‐sized and large mammals) or seed hoarders (some small sigmodontine rodents). Our objective was assessing the functional role of Microcavia australis, a small hystricognathi rodent, in the fruit removal and seed deposition stages of P. flexuosa seed dispersal, compared to sympatric sigmodontine rodents. In situ, we quantified fruit removal by small rodents during non‐fruiting and fruiting periods, and determined the distance seeds were transported, particularly by M. australis. In laboratory experiments, we analysed how M. australis stores seeds (through scatter‐ or larder‐hoarding) and how many seeds are left in caches as living seeds, relative to previous data on sigmodontine rodents. To conduct field studies, we established sampling stations under randomly chosen P. flexuosa trees at the Ñacuñán Man and Biosphere Reserve. We analysed fruit removal by small rodents and seed dispersal distance by M. australis using camera traps focused on P. flexuosa fruits covered with wire screen, which only allowed entry of small animals. In laboratory trials, we provided animals with a known number of fruits and assessed seed conditions after removal. Small rodents removed 75.7% of fruit supplied during the non‐fruiting period and 53.2% during the fruiting period. Microcavia australis and Graomys griseoflavus were the main fruit removers. Microcavia australis transported seeds to a mean distance of 462 cm and cached seeds mainly in scatter‐hoards, similarly as Eligmodontia typus. All transported seeds were left in fruit segments or covered only by the endocarp, never as predated seeds. Microcavia australis disperses P. flexuosa seeds by carrying fruits away from a source to consume them and then by scatter‐hoarding fruits and seeds.     

Dispersal and predation of diaspores of Coula edulis Baill. in an evergreen forest of Gabon

The African walnut (Coula edulis) is a tree species of African evergreen forests, the seeds of which are collected and traded by African people. Many animal species consume African walnut diaspores; however, their roles as dispersers or predators have yet to be clarified. In this study, we present observations conducted in two different habitats of a Gabonese region over a 3‐year period. The originality of this research resides in the combination of three complementary approaches: (i) the use of camera‐traps (ii) the exploration of land rodent burrows and (iii) the examination of elephant dung. In total, 408 camera‐trap photographs have shown seven animal species involved in the dispersal/predation of C. edulis. Among these seven frugivorous species, the bush pig was found to be the main consumer and predator of seeds. Land rodents (Muridae) are potential predators, as they damaged the seeds and buried them deep in the soil. They may also play a role in the regeneration process as a result of the loss of seeds during transportation. Finally, no seeds appeared to emerge intact from elephant faeces. These results indicate that the natural regeneration rate of this tree species is low, unless other complex mechanisms are involved.     

Molecular evolutionary analyses of the odorant-binding protein gene Gp-9 in fire ants and other Solenopsis species

The fire ant Solenopsis invicta exists in two social forms, one with colonies headed by a single reproductive queen (monogyne form) and the other with colonies containing multiple queens (polygyne form). This variation in social organization is associated with variation at the gene Gp-9, with monogyne colonies harboring only the B allelic variant and polygyne colonies containing b-like variants as well. We generated new Gp-9 sequences from 15 Solenopsis species and combined these with previously published sequences to conduct a comprehensive, phylogenetically based study of the molecular evolution of this important gene. The exon/intron structure and the respective lengths of the five exons of Gp-9 are identical across all species examined, and we detected no evidence for intragenic recombination. These data conform to a previous suggestion that Gp-9 lies in a genomic region with low recombination, and they indicate that evolution of the coding region in Solenopsis has involved point substitutions only. Our results confirm a link between the presence of b-like alleles and the expression of polygyny in all South American fire ant species known to possess colonies of both social forms. Moreover, phylogenetic analyses show that b-like alleles comprise a derived clade of Gp-9 sequences within the socially polymorphic species, lending further support to the hypothesis that monogyny preceded polygyny in this group of fire ants. Site-specific maximum likelihood tests identified several amino acids that have experienced positive selection, two of which are adjacent to the inferred binding-pocket residues in the GP-9 protein. Four other binding-pocket residues are variable among fire ant species, although selection is not implicated in this variation. Branch-specific tests revealed strong positive selection on the stem lineage of the b-like allele clade, as expected if selection drove the amino acid replacements crucial to the expression of polygyne social organization. Such selection may have operated via the ligand-binding properties of GP-9, as one of the two amino acids uniquely shared by all b-like alleles is predicted to be a binding-pocket residue.