The phenology of growth and reproduction in plants

The study of phenological aspects of plants involves the observation, recording and interpretation of the timing of their life history events. This review considers the phenology of leafing, flowering and fruit production in a range of species and communities. The selective forces (both abiotic and biotic) that influence the timing of these events are discussed. Within the limits imposed by phylogenetic constraints, the phenological patterns (timing, frequency, duration, degree of synchrony, etc.) of each phase are probably the result of a compromise between a variety of selective pressures, such as seasonal climatic changes, resource availability, and the presence of pollinators, predators and seed dispersers. Many studies on flowering times stress the role of interactions between plant species which share pollinators or predators. The timing of fruiting plays a key role in controlling the abundance and variety of obligate frugivores in many tropical communities. The importance of long-term recording is stressed, particularly in species which fruit irregularly. An understanding of the phenology of plants is crucial to the understanding of community function and diversity.     

Consumer pressure and seed set in a salt marsh perennial plant community

Summary Seed predation can be an important determinant of plant success, but has received little attention in wetland plant communities. Here, we examine the role of flower and seed predators in limiting the seed production of the dominant perennial plants in a salt marsh plant community. Of the four perennial investigated, direct ovule loss to consumers ranged from 51 to 80%, resulting in seed set reductions ranging from 50% to over 20-fold. Most losses were due to generalist grazing by the grasshopper, Conocephalus spartinae. More species-specific losses were inflicted by planthoppers, and microlepidopteran and dipteran larval seed parasites.Insect abundance and consumer pressure on flowers and seeds increased over the early summer, peaked in the middle of July, and declined through August, and this temporal pattern was reflected in the natural consumer damage incurred by each of the marsh perennials. Juncus gerardi flowers earlier than other marsh perennials and largely escapes heavy consumer losses. Spartina patens and Distichlis spicata flower in the middle of the summer during the peak consumer activity and incur extremely heavy seed losses. Spartina alterniflora flowers late in the summer as consumer pressure is subsiding, which appears to minimize its seed loss. In addition to destroying seeds directly, consumers also markedly reduce the frequency and affect the timing of sexual expression in these plants. In particular, predation drastically reduces the frequency of male flowers, which could lead to pollen limitation of seed set.Intense flower and seed predation on these marsh perennials may be an important determinant of the success of marsh plant populations as well as a potent selective force on their flowering phenologies and reproductive effort.     

Latitude, seed predation and seed mass

Aim We set out to test the hypothesis that rates of pre‐ and post‐dispersal seed predation would be higher towards the tropics, across a broad range of species from around the world. We also aimed to quantify the slope and predictive power of the relationship between seed mass and latitude both within and across species. Methods Seed mass, pre‐dispersal seed predation and post‐dispersal seed removal data were compiled from the literature. Wherever possible, these data were combined with information regarding the latitude at which the data were collected. Analyses were performed using both cross‐species and phylogenetic regressions. Results Contrary to expectations, we found no significant relationship between seed predation and latitude (log₁₀ proportion of seeds surviving predispersal seed predation vs. latitude, P = 0.63; R² = 0.02; n = 122 species: log₁₀ proportion of seeds remaining after postdispersal seed removal vs. latitude, P = 0.54; R² = 0.02; n = 205 species). These relationships remained non‐significant after variation because of seed mass was accounted for. We also found a very substantial (R² = 0.21) relationship between seed mass and latitude across 2706 species, with seed mass being significantly higher towards the tropics. Within‐species seed mass decline with latitude was significant, but only about two‐sevenths, as rapid as the cross‐species decline with latitude. Results of phylogenetic analyses were very similar to cross‐species analyses. We also demonstrated a positive relationship between seed mass and development time across ten species from dry sclerophyll woodland in Sydney (P < 0.001; R² = 0.77; Standardized Major Axis slope = 0.14). These data lend support to the hypothesis that growing period might affect the maximum attainable seed mass in a given environment. Main conclusions There was no evidence that seed predation is higher towards the tropics. The strong relationship between seed mass and latitude shown here had been observed in previous studies, but had not previously been quantified at a global scale. There was a tenfold reduction in mean seed mass for every c. 23° moved towards the poles, despite a wide range of seed mass within each latitude.     

Genetic variation in flowering phenology and avoidance of seed predation in native populations of Ulex europaeus

The genetic variation in flowering phenology may be an important component of a species’ capacity to colonize new environments. In native populations of the invasive species Ulex europaeus, flowering phenology has been shown to be bimodal and related to seed predation. The aim of the present study was to determine if this bimodality has a genetic basis, and to investigate whether the polymorphism in flowering phenology is genetically linked to seed predation, pod production and growth patterns. We set up an experiment raising maternal families in a common garden. Based on mixed analyses of variance and correlations among maternal family means, we found genetic differences between the two main flowering types and confirmed that they reduced seed predation in two different ways: escape in time or predator satiation. We suggest that this polymorphism in strategy may facilitate maintain high genetic diversity for flowering phenology and related life‐history traits in native populations of this species, hence providing high evolutionary potential for these traits in invaded areas.     

The effect of samara wing presence on predation of Acer pseudoplatanus (Sapindaceae) seeds on the ground

The key selective pressure shaping the morphology of samaras is seen as enhancing primary wind-borne dispersal from the parent plant to the ground. However, the consequences of the samara wing of primarily wind-dispersed tree species for post-dispersal processes has not been well studied. We explored whether the presence of this wing in Acer pseudoplatanus either deters or promotes predation after dispersal, either by increasing the time and energy required to predate the seed or by increasing the seed's visibility to predators. We found that wing-removed fruits were preferred, suggesting that the presence of samaras makes seed handling more expensive for granivores. Further, we found that fewer seeds were consumed from treatments that contained the most winged seeds, thus there was no evidence of the samaras making seed finding easier for granivores. We conclude that the presence of the wing may offer an anti-predatory benefit as well as aiding primary dispersal.     

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.     

Seed dynamics of resprouting shrubs in grassy woodlands: Seed rain,predators and seed loss constrain recruitment potential

Abstract Measuring the fate of seeds between seed production and seedling establishment is critical in understanding mechanisms of recruitment limitation of plants. We examined seed fates to better understand the recruitment dynamics of four resprouting shrubs from two families (Fabaceae and Epacridaceae) in temperate grassy woodlands. We tested whether: (i) pre‐dispersal seed predation affected seed rain; (ii) post‐dispersal seed predation limited seed bank accumulation; (iii) the size of the seed bank was related to seed size; and (iv) viable seeds accumulated in the soil after seed rain. There was a distinct difference in seed production per plant between plant families with the legumes producing significantly more seeds per individual than the epacrids. Seed viability ranged from 43% to 81% and all viable had seed or fruit coat dormancy broken by heat or scarification. Pre‐dispersal predation by Lepidopteran larvae removed a large proportion of seed from the legume seed rain but not the epacrids. Four species of ants (Notoncus ectatomoides, Pheidole sp., Rhytidoponera tasmaniensis and Iridomyrmex purpureus) were major post‐dispersal seed removers. Overall, a greater percentage of Hardenbergia (38%) and Pultenaea (59%) seeds were removed than the fleshy fruits of Lissanthe (14%) or Melichrus (0%). Seed bank sizes were small (<15 seeds m^?2) relative to the seed rain and no significant accumulation of seed in the soil was detected. Lack of accumulation was attributed to seed predation as seed decay was considered unlikely and no seed germination was observed in our study sites. Our study suggests that seed predation is a key factor contributing to seed‐limited recruitment in grassy woodland shrubs by reducing the number of seeds stored in the soil.     

The production, storage and viability of seeds of Acacia karroo and A. nilotica in a grassy savanna in KwaZulu-Natal, South Africa

African Acacias are often major contributors to the progressive increase in the woody component of savannas, a phenomenon commonly referred to as bush encroachment. They produce large quantities of seed and may have large soil‐stored seed banks. In Hluhluwe–Umfolozi Park, the number of adult Acacia nilotica trees per hectare far exceed that of A. karroo adults. The relative dominance is reversed in the juvenile stage with A. karroo outnumbering A. nilotica threefold outside closed woodlands. Acacia karroo trees were smaller than A. nilotica trees on average, but produced more seeds for a given basal diameter size class. Acacia karroo showed less bruchid infestation than A. nilotica at all stages of pod development. Unlike A. nilotica, a proportion of A. karroo seeds was able to germinate after bruchid attack. We detected no difference between the two species in the soil‐stored seed bank or in the viability of seeds found in the seed bank.     

昆虫种子捕食与蒙古栎种子产量和种子大小的关系

为了了解昆虫种子捕食者在栎类种群更新中的作用,于2006年秋季,在黑龙江省伊春市带岭区东方红林场研究了昆虫对蒙古栎Quercus mongolica在参园和东山两个种群的种子蛀食情况及其与蒙古栎种子产量和种子大小的关系。结果表明：(1)在参园和东山两个林分内,蒙古栎种子雨动态非常相似,种子雨成分中完好种子的平均密度仅为3.2±4.1个/m²（参园）和1.7±2.8个/m²（东山）,分别仅占种子产量的4.0％和3.2％,而虫蛀种子和败育种子的比例均在38%以上,以虫蛀种子的比例最高,分别为58.2％和57.7％;(2)柞栎象Curculio arakawai是蛀食蒙古栎种子的主要昆虫种类,在虫蛀种子中所占比例高达96.8％（参园）和97.1％（东山）,且象甲蛀食种子中所含虫卵数与种子大小有关,即种子越大,所含象甲的虫卵数就较多。本研究的结果说明2006年蒙古栎成熟种子多遭遇虫蛀,导致完好种子的数量极低,因而可能成为限制蒙古栎种群更新的重要因素。     

Preferences of pollinators and herbivores in gynodioecious Geranium sylvaticum

BACKGROUND AND AIMS: For the maintenance of gynodioecy (i.e. the coexistence of female and hermaphroditic plants), females need to compensate for the lack of pollen production through higher seed production or better progeny quality compared to hermaphrodites. In Geranium sylvaticum, females produce more seeds per flower than hermaphrodites. This difference in seed production might be modified by biological interactions with pollinators and herbivores that may favour one sex and thus affect the maintenance of gynodioecy. METHODS: Sexual dimorphism in flower size and flowering phenology, and in attractiveness to pollinators, pre-dispersal seed predators and floral herbivores were examined in natural populations of G. sylvaticum. KEY RESULTS: Pollinators preferred hermaphrodites 25 % more often than females in two of the three study populations, and floral herbivores attacked hermaphrodites 15 % more often than females in two of the six study populations. These preferences might be explained by the larger flower size of hermaphrodites. In contrast, seed predators did not prefer either sex. CONCLUSIONS: The data suggest that pollinator preference does not benefit females, whereas the higher floral herbivory of hermaphrodites might enhance the maintenance of females in G. sylvaticum. Thus, although the data support the view that ecological factors may contribute to the maintenance of gynodioecy, they also suggest that these contributions may vary across populations and that they may function in opposite directions.     

Soil seed bank dynamics in the rare obligate seeding shrub,Grevillea barklyana (Proteaceae)

Abstract Grevillea barklyana is a rare, obligate seeding shrub that occurs in fire-prone heath and woodland in southeastern Australia. The size and dynamics of the soil seed bank were investigated in populations 2–29 years after fire in order to identify fire frequencies that would threaten population survival. Plants began flowering 2 years after fire (16%), but maximum inflorescence and seed production did not occur until 15–16 years after fire when plants were full size. Seed production declined in older populations. Fruit:flower ratios were very low (0.1–5.3%). Most flowers (> 95%) failed to initiate fruits. Of the initiated fruits, about 60% aborted, 27% were attacked by parrots and 13% matured. An exclusion experiment showed that fruits attacked by parrots would have otherwise matured. Seeds were consumed on the soil surface by mammals, particularly rodents. Post-dispersal seed losses were consistently high in all months and in all populations (78–100%). Mortality of adult plants increased with time since fire. In the 29-year-old population, 30% of plants were dead and 33% were senescent. Recruitment was negligible in the absence of fire, but following fire the seedling to parent ratio was 20:1. Seedling survival was high (90%) following two years of above-average rainfall. The observed seed bank was small (3–16 seeds irr) and increased during the first 16 years after fire before declining in the 21- and 26-year-old populations. The size and dynamics of the seed bank may limit population numbers, especially if the intervals between fires are less than 10 years or greater than 25 years.     

Insects remove more seeds than mammals in first‐year prairie restorations

Seed sowing is a common early step in restoration, but seed consumers can impede plant establishment and alter community structure. Moreover, seed consumers vary in feeding behaviors and the relative importance of different seed consumer groups during restoration are not well understood. At 12 first‐year prairie restorations in Michigan, we studied seed predation using seed removal trays to ask: What is the relative magnitude of seed removal by insects and mammals? Do seed removal rates change over the growing season? Do habitat edges influence seed removal? At what rates are 10 prairie plant species' seeds removed by mammals and insects? Seed removal depended on consumer type, time of year, and seed species. Insects accounted for the majority of seed removal, contrary to previous research in similar systems. In May, insects removed 1.8 times more seeds than mammals, while in August, they removed 5.1 times more. There was greater seed removal in August. During May 28% of seeds were removed, compared to 54% of seeds removed during August, an increase driven by insects. Edge proximity did not influence seed removal. Certain seed species were removed more than others. For example, Lespedeza capitata (round‐headed bush clover) was always removed at high rates, whereas Coreopsis lanceolata (lance‐leaved coreopsis) and Andropogon gerardii (big bluestem) were always removed at low rates. Mammals and insects showed different preferences for several species. This research suggests a prominent role of seed predation, particularly by insects, for early prairie restoration dynamics, with influences varying temporally and among species.     

Small vertebrate granivores reduce seedling emergence in native tallgrass prairie restoration

High seed cost and low rates of establishment make tallgrass prairie restorations challenging and expensive endeavors. Typical seedling emergence rates in prairie restorations are approximately 10% and the causes of seed mortality are poorly understood. In this study, we examined the impact of small vertebrate granivores on prairie restoration by comparison of seedling emergence in open (sham) versus closed exclosures at three newly restored sites. To assess other causes of seed loss, we also tracked seed fates at one prairie restoration site. We coated seeds of four prairie species with fluorescent dye, placed them under closed exclosures, and monitored their fate (emerging seedling, partially germinated, nongerminated/viable, and nongerminated/nonviable) over a 5‐month period. On average, 9.6 more seedlings/m² emerged in the closed than the opened exclosures, suggesting that small vertebrate granivores reduce seedling emergence in prairie restoration. Granivores influenced the composition of the emerging community but did not preferentially consume large‐seeded species. In the seed‐tracking experiment, we found that greater than 70% of seeds were lost within 30 days of sowing, that seed recovery and viability both decreased with time in soil, and that seed fates differed between species. Collectively, our results indicate that small vertebrate granivores are an important cause of seed loss in prairie restoration, but unidentified belowground (e.g. fungal decomposition, invertebrate predation) and environmental (wind, rain) factors account for a greater proportion of total seed loss. Until these causes of seed loss are better understood, high seed costs will persist and continue to impede prairie restoration.     

Comparing methods of weed seed exposure to predators

Several methods of seed exposure are used in seed predation studies, but how these methods influence the results remains poorly studied. In this article, two commonly used methods of seed exposure – seed cards and plasticine trays – were compared in the field and in the laboratory using three species of weed seeds. In the field, cards or trays with seeds were exposed either with or without cages to keep vertebrates out and either with or without impermeable roofs to provide protection from the weather. The overall seed retrieval from the control stands varied significantly between the methods of seed exposure, roof treatment and the species of seeds, and the scatter in the seed retrieval increased or decreased monotonically with the temperature or precipitation for some species of seeds. This indicates that the controls were more or less relevant depending on the weather conditions and species. The seed removal from cards varied between the species of seeds. The effect of exclosure cages indicated that invertebrates were the dominant seed predators of Capsella bursa‐pastoris, while in Poa annua and Stellaria media both vertebrates and invertebrates were important. Higher seed removal from plasticine trays compared to seed cards was found for all three species of seeds, and placing roofs over the seeds affected seed removal in C. bursa‐pastoris and P. annua. In the laboratory, seed consumption varied with the method of exposure in 10 out of 12 combinations of seed species and predator (two species of carabids and two species of isopods). The overall tendency was the opposite of the field observations: seed consumption was higher for seeds on filter paper and cards compared to seeds on tin trays. We conclude that seed cards are more convenient for short term studies in the field, while tin trays are useful in laboratory multi‐choice experiments. To measure the realistic consumption of invertebrate predators in the laboratory, filter paper seems to be the best option as it does not present an obstacle to predators eating the seed. Using roofs introduced further bias regarding the estimates of seed removal in the field and thus should be avoided.     

Did fleshy fruit pulp evolve as a defence against seed loss rather than as a dispersal mechanism?

Relatively few studies have examined the evolution of the mutualism between endozoochorous plants and seed dispersers. Most seed dispersal studies are ecological and examine the role of fruit pulp in promoting seed dispersal. This interaction is often assumed to have originated due to selection stemming from seed dispersers. Here I suggest a "defence scenario" wherein fleshy fruits originated as mechanisms to defend seeds and secondarily became structures to promote seed dispersal. I suggest that frugivory followed from herbivores that specialized on consuming seed defensive tissues and that enhanced seed dispersal was initially a consequence of seed defence. The proposed defence scenario is not posited as an explanation for the sequence that led to all modern frugivores. However, it is suggested that seed predation was the initial source of selection that led to fleshy fruits; the necessary precursor to frugivory. Support is described from the fossil record and from modern structures and interactions. Testable predictions are made in hope that greater interest will be focused on the defensive role of fleshy fruit pulp both in modern interactions and historically.     

A five-year study of mast seeding inPinus densiflora

I examined the annual pattern of seed production in three Korean populations ofPinus densiflora from 1998 to 2002. During the fall season, data were collected on the numbers of cones per tagged tree, as well as seed counts, their mass, and seed set following dehiscence. Dbh was measured for individual trees during each spring. Overall, 80.3% of the trees produced seed cones in even-numbered years compared with 51.6% in odd-numbered years. Moreover, trees that matured seed cones in even years produced 12 times more seeds per tree than those in odd years. Tree diameters generally increased significantly during the summers after odd-numbered years, although the trees at one site showed a consistent growth rate each year after 2000. Annual variations in individual seed mass, seed set, and the proportion of damaged seed cones occurred largely within odd or even years. Based on these results, the following conclusions were made: 1) seed-cone production ofP. densiflora is somewhat synchronized, but is not an all-or-nothing phenomenon, 2)P. densiflora tends to undergo mast seeding at two-year intervals, and 3) this alternate-year excess in seed crop may have evolved to increase fitness, though the exact evolutionary mechanism is unclear.     

A Study of Fruit–Frugivore Interactions in Two Species of Durian (Durio, Bombacaceae) in Sabah, Malaysia

We determined the fruit predators and seed dispersers of two species of durian ( Durio , Bombacaceae), D. graveolens and D. zibethinus , which have contrasting aril color and timing of dehiscence by observing fruiting trees in Deramakot forest reserve. In our observations in the wild, both species were extensively predated by orangutans before fruits matured. Durio graveolens was dispersed by black hornbills and D. zibethinus was dispersed by long-tailed macaques.     

六盘山区辽东栎的实生苗更新及其影响因子

研究了六盘山区辽东栎(Quercus liaotungensis)灌丛的种子产量、土壤种子库组成、湿沙和风干贮藏对种子寿命的影响以及动物取食子叶对种子萌发和幼苗建立的影响。结果表明, 辽东栎灌丛种子的完好率为27.51%, 被动物取食或搬运种子的比例(41.51%)显著高于其他类型种子(p < 0.01); 辽东栎次生林土壤种子库中萌发和虫蛀种子分别占35.16%和38.29%, 完好种子仅占13.65%, 捕食动物主要通过贮藏或搬运而影响土壤种子库中的种子密度。湿沙贮藏60天的辽东栎种子自动萌发率高达96.67%, 短期贮藏可加快种子的萌发进程, 提高萌发率和萌发指数, 但随着贮藏时间的延长, 种子萌发进程延迟, 萌发率、萌发指数和活力指数均不同程度地降低。排除动物取食处理的幼苗在林窗和林下生境的存活率分别为80%和83%, 而不排除动物取食幼苗在2种生境中分别仅有25%和31%能够存活, 表明子叶在幼苗建立中具有重要作用。林窗中幼苗子叶的动物取食率(85.00%)高于林下(71.00%), 子叶留存的幼苗在林窗中的存活率(6.00%)低于林下(15.50%), 而子叶被取食幼苗的存活率在两种环境中基本相等(分别为18.50%和18.00%)。     

Predator satiation and recruitment in a mast fruiting monocarpic forest herb

Background and Aims

Cross-pollination and satiation of seed predators are often invoked to explain synchronous mast reproduction in long-lived plants. However, explanations for the synchronous death of parent plants are elusive. The roles of synchronous seeding and post-reproductive mortality were investigated in a perennial monocarpic herb (Isoglossa woodii) in coastal dune forest in South Africa.

Methods

Pre-dispersal seed predation and seed production were assessed by measuring fruit and seed set of inflorescences sprayed with insecticide or water and with no spray treatments. Seed predation was measured at different densities of I. woodii plants by monitoring removal rates of seed from the forest floor. The influence of adult plants on establishment of I. woodii seedlings was assessed by monitoring growth and survivorship of seedlings in caged and uncaged 1 × 1 m plots in understorey gaps and thickets.

Key Results

Fruit and seed set were similar between spray treatments. An I. woodii stem produced 767·8 ± 160·8 seeds (mean ± s.e.) on dune crests and 1359·0 ± 234·4 seeds on the foredune. Seed rain was greater on the foredune than in other topographic locations. Seed predation rates were 32 and 54 % on dune crests and in dune slacks, respectively, and decreased with seed abundance, number of inflorescences per stem and plant height. Seedling recruitment was greater beneath synchronously dying adult plants than in natural understorey gaps (no I. woodii). However, seedling growth rate beneath I. woodii mid-way through its life-cycle was less than in gaps, although survivorship was similar.

Conclusions

The selective advantage of masting in I. woodii derives from satiation of both pre- and post-dispersal seed predators. In addition, post-seeding mortality of adult plants facilitates seedling establishment. Satiation of seed predators and the benefits of seedling establishment are strong drivers of the evolution of synchronous monocarpy in I. woodii.