Impacts of secondary seed dispersal and herbivory on seedling survival in Aesculus turbinata

Abstract. Aesculus turbinata is a tree species with large seeds (6.2 g mean dry weight). We studied the demography of its seeds and seedlings in a temperate deciduous forest in northern Japan to elucidate the ecological significance of large seeds with special reference to herbivory and secondary dispersal. Both seed and seedling stages suffered greatly from herbivores. Seedling herbivory was important judged from experiments with shoot clipping and hypogeal cotyledon removal. However, some seedlings survived through re-sprouting after herbivory. Survival rate and percentage resprouting seedlings were lower than those with remaining cotyledons, though seedling size was not affected. This suggests that stored resources in hypogeal cotyledons are working as a kind of ‘risk hedge’ against severe aboveground shoot clipping experienced by A. turbinata. The spatial distribution of seedlings was expanded via seed scatter-hoarding by rodents. Seedling survival rate was higher within canopy gaps than under closed canopy, indicating that canopy gaps are safe sites for establishment, and was negatively correlated with seedling density. Therefore, secondary seed dispersal in this species seems to be effective in ‘finding’ safe sites and in ‘escaping’ density-dependent mortality. The large seeds and seedlings of A. turbinata are attractive to herbivores, but the high resistance of seedlings to herbivory due to large reserves and the effective secondary dispersal appear to mitigate these disadvantages.     

Restionaceae seedlings: Morphology,anatomy and systematic implications

Restionaceae differ from most monocot families in having both epigeal and hypogeal germination. The green cotyledons associated with epigeal germination have a central vascular strand as found in most epigeal monocotyledons. In some genera the cotyledon may have a hairpin‐like structure, also described for Anthericaceae. The cotyledon of the hypogeal seedlings is short, without green pigment and largely remains embedded in the seed coat. Hypogeal germination is correlated with large, woody, indehiscent, frequently myrmecochorous nuts, while epigeal germination is found in species with smaller indehiscent nutlets or seeds, dispersed in a variety of ways. The primitive condition is most likely epigeal germination. In hypogeal seedlings of some African and Australian taxa an epicotyledonary rhizome is found between the primary root and the first leaves. Seedlings of African Restionaceae frequently have elongated culm internodes, whereas in the Australian species studied, internodes are very short, resulting in a cluster of seedling leaves. The leaf blades, which in most species are only found on the seedlings, are very simple anatomically. However, they appear to be unifacial, similar to the leaf blades of Anarthria (Anarthriaceae). The anatomical specialisations in the blades mirror those recorded for the culm anatomy. These observations are consistent with the hypothesis that Centrolepidaceae may be neotonous Restionaceae. They also corroborate the morphology of the African Restionaceae, and the presently accepted phylogeny of the African genera of Restionaceae.     

Seedling functional types in a lowland rain forest in Mexico

Seedling morphology of 210 species (173 trees and 37 lianas) was studied from a community perspective to identify major patterns of seedling functional types in a Mexican rain forest. Five types of seedlings were distinguished: cryptocotylar with reserve storage or absorption cotyledons (epigeal [CER] and hypogeal [CHR]), phanerocotylar epigeal, either with photosynthetic cotyledons (PEF) or with reserve storage or absorption cotyledons (PER), and phanerocotylar hypogeal with reserve cotyledons (PHR). The most common seedling type was PEF (49.5%), followed by CHR (31.4%), PER (9.5%), PHR (7.2%), and CER (2.4%). Excepting the CER type, seedling type frequencies did not differ between trees and lianas. The PEF seedlings had the lightest seeds, whereas CHR seedlings had the heaviest ones. Pioneer trees showed lighter seeds than persistent trees or lianas in species with PEF but not in species with PER. Pioneer trees (38 species) showed three seedling types and the most common was PEF (82%). Persistent trees (135 species) showed the five seedling types but PEF (43%) and CHR (37%) were the most frequent. Seedling type frequencies differed among dispersal syndrome groups. The animal dispersal syndrome was significantly more frequent in species with CHR. Our results show an evolutionary convergence of seedling types at the community level worldwide and the existence of a phylogenetic inertia in the evolution of initial seedling morphology. A comparison among eight tropical communities indicated on average that PEF is the most frequent type and CER the least common, although the relative frequency of each seedling type differs among communities, particularly between Neotropical and Paleotropical sites.     

Evolutionary and ecological correlates of early seedling morphology in East African trees and shrubs

Seed size and cotyledon morphology are two key juvenile traits that have evolved in response to changes in plant species life-history strategies and habitat associations. Correlations of these traits with each other and with other juvenile traits were examined for 70 species of trees and shrubs in Kibale National Park, Uganda. Although species with photosynthetic cotyledons were more abundant than in other tropical floras, both univariate and multivariate analyses supported trait associations expected from the literature. Trait values varied continuously across species, yet mean trait values differed significantly among habitat association types. Species with large seeds, large seedlings, thick storage cotyledons, slow germination, large-stature adults, and dispersal by large animals were common in forest and gap habitats. An opposite suite of traits was common in open habitats (grassland and edge). Analyses incorporating phylogeny (independent contrasts and omnibus tests) confirmed that these suites of traits showed correlated evolution. Cotyledon functional morphology yielded a strong phylogenetic signal, while seed mass was labile. Nevertheless, contingent change tests found that evolutionary change from photosynthetic to reserve cotyledons was more likely when disperser and perhaps seed size of ancestral species were already large, suggesting a strong interdependency among these traits.     

The effects of seed size, cotyledon reserves, and herbivory on seedling survival and growth in Quercus rugosa and Q. laurina (Fagaceae)

In a greenhouse experiment, seedling survival of two oak species (Quercus rugosa and Q. laurina) was greatly affected by the excision of cotyledons 1 mo after germination, with a greater impact on Q. laurina. The effect of seed size was also significant for both species, with a positive correlation between seed mass and survival and growth. The effect of cotyledon excision on seedling growth persisted throughout the first growing season in Q. rugosa and was not analyzed for Q. laurina due to the low number of seedlings that survived cotyledon excision. Seed size significantly affected seedling height, diameter, leaf area, and biomass at 6 mo. Seed size and cotyledon retention affected the ability of Q. rugosa to recover from herbivory, as both factors had a significant effect on relative growth rates after aerial biomass removal. The results show that seedlings originating from large seeds can better endure loss of cotyledons and aerial biomass and thus are better equipped to confront stress early in their lives.     

Seedling tolerance to cotyledon removal varies with seed size: A case of five legume species

It is generally accepted that seedlings from large seeds are more tolerant to defoliation than those from small seeds due to the additional metabolic reserves present in the large seeds. However, information on the effects of amount of seed reserves (cotyledon removal) from seedlings resulting from large vs. small seeds on seedling growth and long‐term survival in the field is limited. Five legume species with different sizes of seeds were sown in the field and none, one, or both cotyledons removed 7 days after seedling emergence. Seedling biomass, relative growth rate (RGR) and survival were determined at different time. Cotyledon removal, species, and their interaction had significant effects on seedling growth and survival. During the period between 33 and 70 days, seedlings from large seeds had a significantly lower RGR than those from small seeds. Biomass, RGR, and survival of seedlings from large seeds were significantly reduced by removal one or both cotyledons, whereas those of seedlings from small seeds were not affected. Seed energy reserves are more important for the early growth of seedlings from large seeds than for those from small seeds. The overall effect of cotyledon removal on growth and survival varies with seed size (i.e., energy reserves) with seedlings from small seeds being less sensitive than those from large seeds under field conditions.     

An Advantage of Large Seed Size: Tolerating Rather than Succumbing to Seed Predators1

Although large seeds might be more attractive and apparent to seed predators, large seed size could enable tolerance of seed predators. If seeds are large enough to sustain damage that would kill smaller seeds yet still produce viable seedlings, investment above the minimum by the maternal plant could be advantageous. I tested this hypothesis by removing 0–80 percent of the cotyledons of four large-seeded (4–180 g) tree species from Papua New Guinea and monitoring germination and seedling growth for eight months. All species showed little negative effect on seedling size with up to 50 percent removal of cotyledons and the larger species showed a less serious effect on growth than smaller-seeded species above 50 percent removal. Large-seeded species clearly have more than the minimum-required cotyledonary reserves. Observations of viable seedlings with heavily damaged cotyledons suggest that these species withstand attack by rodents and beetles by virtue of their large size.     

Limited evolutionary divergence of seedlings after the domestication of plant species

The most vulnerable stage in the life of plants is the seedling. The transition from wild to agricultural land that plants experienced during and after domestication implied a noticeable change in the seedlings′ environment. Building on current knowledge of seedling ecology, and on previous studies of cassava, we hypothesise that cultivation should have promoted epigeal germination of seedlings, and more exposed and photosynthetic cotyledons. To test this hypothesis, we phenotyped seedling morpho‐functional traits in a set of domesticated and wild progenitor accessions of 20 Eudicot herbaceous crop species. Qualitative traits like epi‐ versus hypogeal germination, leafy versus storage type of cotyledons, or crypto‐ versus phanerocotyledonar germination, remained conserved during the domestication of all 20 species. Lengths of hypocotyls and epicotyls, of cotyledon petioles, and indices of cotyledon exposure to the aboveground environment changed during evolution under cultivation. However, those changes occurred in diverse directions, depending on the crop species. No common seedling phenotypic convergence in response to domestication was thus detected among the group of species studied here. Also, none of the 20 crops evolved in accordance with our initial hypothesis. Our results reject the idea that strong selective filters exerted unconsciously by artificial selection should have resulted in generalised channelling of seedling morphology towards more productive and more herbivore risky phenotypes. This result opens up unexplored opportunities for directional breeding of seedling traits.     

Impact of Cotyledon and Leaf Removal on Seedling Survival in Three Tree Species with Contrasting Cotyledon Functions1

The relative importance of cotyledons and leaves for seedling survival was evaluated using a factorial field experiment on three neotropical tree species with contrasting cotyledon functional morphologies (photosynthetic, epigeal reserve vs. hypogeal reserve). In all species, cotyledon and leaf removal shortly after leaf expansion had additive negative effects on seedling survival over 7 weeks. Carbon supplies from cotyledons and other carbohydrate reserves apparently enhanced ability of seedlings to cope with herbivory and disease.     

Seed reserve translocation and early seedling growth of eight tree species in a tropical deciduous forest in Mexico

Seed reserves play an essential role during germination and seedling establishment and are particularly important for species that grow in seasonal ecosystems with a short growing season. In this study, we examined (a) how and when the seedlings change their dependence from seed resources to external resources, (b) the lipid, nitrogen, and non-structural carbohydrate reserve translocation from seeds to seedlings over time, and (c) whether reserve translocation may be correlated to cotyledon and leaf lifespan of seedlings for eight tree species in a tropical deciduous forest in north-western Mexico. Our results showed that the cotyledon lifespan was not related to the cotyledon type (photosynthetic or reserve) and that the cotyledon biomass did not decrease significantly until germination. In six of the eight studied species, biomass allocation to the leaves was favored; lipids were the first reserve exhausted before the first leaves were totally expanded in seven of the eight study species. Species with the highest N concentration had expanded leaves and lost their cotyledons faster than species with a low N concentration. Our results suggest that tropical deciduous forest species employ different strategies to survive the dry season and re-sprout in the next growing season mediated by seed reserve concentrations, translocation patterns and subsequent biomass allocation.     

Evolution under domestication: contrasting functional morphology of seedlings in domesticated cassava and its closest wild relatives

Although cassava (Manihot esculenta ssp. esculenta) is asexually propagated, farmers incorporate plants from seedlings into planting stocks. These products of sex are exposed to selection, which in agricultural environments should favour rapid growth. To examine whether seedling morphology has evolved under domestication, we compared domesticated cassava, its wild progenitor (M. esculenta ssp. flabellifolia) and their sister species (M. pruinosa) under controlled conditions. Field observations complemented laboratory study. In both wild taxa, the hypocotyl did not elongate (hypogeal germination) and cotyledons remained enclosed in the testa. In domesticated cassava, the hypocotyl elongated (epigeal germination), and cotyledons emerged and became foliaceous. The difference in hypocotyl elongation was fixed, whereas cotyledon morphology varied with environmental conditions in M. pruinosa. Comparative analysis suggests that epigeal germination is primitive in Manihot, that the lineage including wild ancestors of cassava evolved hypogeal germination--which confers greater tolerance to risks in their savanna environment--and that with domestication, there was a reversion to epigeal germination and photosynthetic cotyledons, traits conferring high initial growth rates in agricultural habitats.     

The effect of seed mass and gap size on seed fate of tropical rain forest tree species in guyana

Abstract: For eleven tree species, differing in seed mass, germination success (emergence success for two small-seeded species) and the causes of failure to germinate were studied in the forest understorey and in logging gaps in the tropical rain forests of Guyana. In the forest understorey, germination success increased with seed mass. However, as gap size increased the difference between smaller and larger seeded species diminished because germination success of smaller-seeded species increased slightly, while that of larger-seeded species decreased dramatically. The negative effect of gap size on germination success of larger-seeded species was caused by an increased risk of desiccation with gap size, which was a far more important seed mortality agent for larger than for smaller-seeded species. Generally, seeds of smaller-seeded species suffered more from insect predation and were removed at higher rates than larger-seeded species. On the other hand, larger-seeded species were eaten more by mammals than smaller-seeded species. It is concluded that logging can result in shifts in the species composition in the tropical rain forests of Guyana which are dominated by species with large seeds, since germination success of larger-seeded species is dramatically reduced in large logging gaps.     

Life History Traits of Lianas During Tropical Forest Succession

Tropical secondary forests form an important part of the landscape. Understanding functional traits of species that colonize at different points in succession can provide insight into community assembly. Although studies on functional traits during forest succession have focused on trees, lianas (woody vines) also contribute strongly to forest biomass, species richness, and dynamics. We examined life history traits of lianas in a forest chronosequence in Costa Rica to determine which traits vary consistently over succession. We conducted 0.1 ha vegetation inventories in 30 sites. To examine the establishment of young individuals, we only included small lianas (0.5–1.5 cm diameter at 1.3 m height). For each species, we identified seed size, dispersal mode, climbing mode, and whether or not the seedling is self‐supporting. We found a strong axis of variation determined by seed size and seedling growth habit, with early successional communities dominated by small‐seeded species with abiotic dispersal and climbing seedlings, while large‐seeded, animal‐dispersed species with free‐standing seedlings increased in abundance with stand age. Contrary to previous research and theory, we found a decrease in the abundance of stem twiners and no decrease in the abundance of tendril‐climbers during succession. Seed size appears to be a better indicator of liana successional stage than climbing mode. Liana life history traits change predictably over succession, particularly traits related to seedling establishment. Identifying whether these trait differences persist into the growth strategies of mature lianas is an important research goal, with potential ramifications for understanding the impact of lianas during tropical forest succession.     

Positive relationship between fruit removal by animals and seedling recruitment in a tropical forest

Fleshy-fruited plants rely on animal frugivores to disperse their seeds, and seed removal by frugivores may leave an imprint on seedling recruitment. However, to what extent plant–frugivore interactions are related to seedling recruitment has rarely been quantified at the community level, especially in species-rich tropical forests. In this study, we tested the effect of different plant traits on fruit removal by frugivores and tested the relative importance of fruit removal, plant traits and abiotic factors for seedling recruitment. We quantified plant–frugivore interactions of 22 fleshy-fruited plant species consumed by 56 diurnal frugivore species, and counted the number of seedlings that emerged along an elevational gradient in the Colombian Andes. We measured a set of plant traits (i.e., crop size; fruit size; seed load and mass; fruit nutritional contents), estimated the density of adult plants and recorded relevant abiotic factors (light, temperature and humidity). We found that fruit removal by frugivores was positively associated with crop size, but negatively associated with fruit length and unrelated to seed load and fruit nutritional content. Seedling densities were positively related to the density of adult plants, seed mass and fruit removal by animals. We found no relationship between abiotic factors and seedling recruitment. Our results indicate that fruit abundance and morphology are important determinants of fruit removal and that fruit removal is positively associated with seedling recruitment accounting for effects of species abundance and plant traits. We conclude that plant traits shape fruit removal and seedling recruitment at the community level, while these two crucial processes of forest regeneration are directly linked by seed dispersal of animals.     

Seed rain and advanced regeneration in a tropical rain forest

By comparing seed rain, seedling and sapling community structures we assessed the possible role played by vertebrate seed dispersal as a structuring factor in advanced regeneration of closed-canopied sites in the tropical rain forest of Los Tuxtlas, Mexico. Seed weight, initial morphology of seedlings and species abundance were also analyzed to determine if these traits influenced the probability of establishment in the shade.About half of the seed species falling in five closed forest sites (25×25 m) during one year came from fruiting trees growing within the sites (local seeds) and half from fruiting trees found outside the sites (immigrant seeds). Seeds of liana and upper-canopy species were over-represented among immigrant seeds compared with seeds of understory tree species. This probably reflects the activity of frugivorous arboreal mammals, bats, and birds. Species with immigrant seeds had both a lower abundance and a narrower spatial distribution than locally produced seeds. Therefore, immigrant seeds showed higher diversity values than locally produced seeds.Average seed size and the proportion of epigeous seedlings were similar in local and immigrant species. Under closed-canopied sites, factors affecting community organization seem to operate selectively, favoring the establishment of large-seeded, local abundant species in the advanced regeneration. However, the fact that some saplings of immigrant species were found in the plots suggest that a slow species infiltration may be occurring leading to a slow shift in the advanced regeneration species composition. We propose that the influence of seed dispersal on advanced regeneration structure depends on the disturbance history of the patches where seeds land.     

Adenosylhomocysteinase and adenosine nucleosidase activities in Lupinus luteus cotyledons during seed formation and germination

The activities of adenosylhomocysteinase (EC 3.3.1.1) and adenosine nucleosidase (EC 3.2.2.7) were assayed in extracts from yellow lupin (Lupinus luteus L.) cotyledons at different stages of seed formation and seedling development. Adenosylhomocysteinase activity was demonstrated in all the cotyledon extracts examined. Its lowest level was found in the dry seeds and the highest, in 4-day-old seedling cotyledons. Extracts from the cotyledons of maturating seeds, dry seeds, and seedlings up to the second day of growth exhibited no adenosine nucleosidase activity. Adenosine nucleosidase activity appeared in the cotyledons of 2-day-old seedlings and its highest level was reached in 4-to 5-day-old seedlings. There is no inhibitor of adenosine nucleosidase in the maturating and dry yellow lupin seeds. No activator of a possible zymogen form of adenosine nucleosidase from maturating or dry seeds occurs in the growing seedlings.     

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%)。     

Importance of animal and plant traits for fruit removal and seedling recruitment in a tropical forest

The traits of animals and plants influence their interaction networks, but the significance of species' traits for the resulting ecosystem functions is poorly understood. A crucial ecosystem function in the tropics is seed dispersal by animals. While the importance of species' traits for structuring plant–frugivore networks is supported by a number of studies, no study has so far identified the functional traits determining the subsequent processes of fruit removal and seedling recruitment. Here, we conducted a comprehensive field study on fruit removal by frugivorous birds and seedling recruitment along an elevational gradient in the Colombian Andes. We measured morphological traits of birds (body mass, bill width, Kipp's index) and plants (plant height, crop mass, fruit width and seed mass) which we expected to be related to fruit removal and seedling recruitment. We tested 1) which bird and plant traits influence fruit removal, and 2) whether network metrics at plant species level, functional identities of frugivores (community‐based mean trait values) and/or plant traits were the main determinants of seedling recruitment. We found that large‐bodied bird species contributed more to fruit removal than small‐bodied bird species and that small‐sized fruits were more frequently removed than large‐sized fruits. Small plant species and plants with heavy seeds recruited more seedlings than did large plants and plants with light seeds. Network metrics and functional identities of seed dispersers were unrelated to seedling recruitment. Our findings have two important implications. First, large birds are functionally more important than small birds in tropical seed‐removal networks. Second, the detected tradeoff between fruit size and seed mass in subsequent recruitment processes suggests that the adaptability of forest plant communities to a loss of large frugivores is limited by life‐history constraints. Hence, the protection of large‐bodied frugivores is of primary importance for the maintenance of diverse tropical plant communities.     

Seed mass and seedling dimensions in relation to seedling establishment

Several experiments have shown that seedlings from larger-seeded species are better able to survive various hazards during establishment. Previous work has suggested a general mechanism might underpin this outcome. Larger-seeded species might tend to mobilize their metabolic resources over a longer period into the autotrophically functioning structures of the seedling. Consequently relatively more resources would remain uncommitted at any given time during the early period of the seedling’s growth, and available to support respiration during carbon deficit. An important aspect of this larger-seed-later-commitment mechanism would be that at a given time, larger-seeded species would hold more resources uncommitted not just absolutely, but relative to the functional seedling structures that needed to be supported. Here we quantify, across a wide range of phanerocotylar species, an allometric pattern that supports the generality of a larger-seed-later-commitment mechanism as an explanation for superior performance by larger-seeded species in face of the hazards of seedling establishment. Larger-seeded species allocate relatively less to cotyledon area, reflecting the initial functional size of the seedling, and relatively more to dry mass per unit area of cotyledon, reflecting stored metabolic reserves. The shift in relative allocation is progressive, rather than seedlings falling into discrete morphological types. The allometry is similar whether considered as correlated evolutionary divergences (phylogenetically independent contrasts) or as correlation across present-day species. Received: 7 April 1999 / Accepted: 29 March 2000     

辽东栎幼苗生长对种子大小和子叶去除处理的响应

该文在温室内盆播条件下,设置不去除子叶(对照)、去除1/4子叶(轻度子叶去除)、1/2子叶(中度子叶去除)和3/4子叶(重度子叶去除) 4个处理,研究了种子大小和子叶去除处理对辽东栎幼苗生长及其形态学可塑性的影响。结果表明:(1)大种子幼苗株高、基茎、叶片数、单株叶面积、总干质量和根冠比在所有处理均大于小种子幼苗,除株高外,上述其他参数在轻度子叶去除处理的不同大小种子幼苗间均差异显著(P0.05),前者总干质量在中度子叶去除处理与后者差异也显著(P0.05)。大种子幼苗比叶面积和比根长在各处理均大于小种子幼苗,比枝长则相反。(2)随着子叶去除强度增大,大、小种子幼苗株高、基茎、叶片数、单株叶面积和总干质量等均呈减小趋势,株高、基径、叶片数和单株叶面积在重度子叶去除处理均显著小于对照和轻度子叶去除处理;小种子幼苗对子叶损失反应更为敏感,其株高、叶片数、单株叶面积和总干质量在中度子叶去除处理也显著小于对照(P0.05);小种子幼苗根冠比随子叶去除强度增大而增大,在中度和重度子叶去除处理显著大于对照和轻度子叶去除处理(P0.05)。(3)随着子叶去除强度增大,大小种子幼苗的比叶面积和比根长均逐渐增大,但大种子幼苗比枝长持续减小,轻度子叶去除处理的小种子幼苗比枝长最大。