Timing of cotyledon damage affects growth and flowering in mature plants

Although the effects of herbivory on plant fitness are strongly linked to age, we understand little about how the timing of herbivory at the seedling stage affects growth and reproduction for plants that survive attack. In this study, we subjected six north-western European, dicotyledonous grassland species (Leontodon autumnalis, Leontodon hispidus, Plantago lanceolata, Plantago major, Trifolium pratense and Trifolium repens) to cotyledon removal at 7, 14 and 21 d old. We monitored subsequent growth and flowering (number of inflorescences recorded, and time taken for first flowers to open) over a 107 d period. Cotyledon removal reduced growth during establishment (35 d) for all species, and a further three exhibited reduced growth at maturity. Four species developed fewer inflorescences, or had delayed flowering after cotyledon removal. Although early damage (7 d old) had the greatest long-term effect on plant performance, responses varied according to the age at which the damage occurred and the species involved. Our results illustrate how growth and flowering into the mature phase is affected by cotyledon damage during different stages of seedling ontogeny, and we highlight the ways in which ontogenetic variation in seedling tolerance of tissue loss might impact upon plant fitness in mature plant communities.     

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.     

Interactive effects of introduced herbivores and post‐flowering die‐off of bamboos in Patagonian Nothofagus forests

Question: In November 2000, Chusquea culeou, a bamboo species dominating Andean forest understories in southern Argentina and Chile, massively flowered and died over a north‐south distance of ca. 120 km. Because bamboo is the major forage for large herbivores in these forests, we examined the interactive influences of the bamboo die‐off and herbivory by introduced cattle on understory and tree regeneration. Location: Lanín National Park, Argentina. Methods: Permanent plots, in and outside livestock exclosures, were installed in a Nothofagus dombeyi forest in patches of flowered and non‐flowered C. culeou. Plots were monitored over four years for changes in understory composition and tree seedling densities and heights. Results: After the C. culeou die‐off, new establishment of N. dombeyi was low, both with and without herbivory. Livestock alone directly increased N. dombeyi seedling mortality through physical damage. However, tree seedling browse ratings and height growth were interactively affected by bamboo flowering and herbivory; unfenced plots in flowered bamboo patches had the shortest seedlings, highest browse ratings, and lowest tree seedling annual growth rates. Understory cover was higher where livestock were excluded, and this effect was intensified in the patches of flowered bamboo. Neither herbivory nor bamboo flowering resulted in major changes in species composition, with the exception of Alstroemeria aurea. Conclusion: Effects of livestock on N. dombeyi regeneration were contingent on flowering of C. culeou. Prior to introduction of livestock, N. dombeyi regeneration was probably successful beneath canopy gaps during windows of opportunity following bamboo die‐off, but now livestock impede tree regeneration. Herbivory during bamboo withering periods also produces more open understories, particularly affecting palatable heliophyllous herb species such as Alstroemeria aurea. The results underscore the importance of assessing herbivore impacts on tree regeneration during relatively short periods of potential tree regeneration immediately following rare bamboo flowering and die‐off.     

Response of Faidherbia albida (Del.) A. Chev., Acacia nigrescens Oliver. and Acacia nilotica (L.) Willd ex Del. seedlings to simulated cotyledon and shoot herbivory in a semi‐arid savanna in Zimbabwe

Woody plant seedling establishment is constrained by herbivory in many semi‐arid savannas. We clipped shoots and cotyledons of three woody species 5‐day (=‘early’) or 28‐day (= ‘late’) post‐emergence to simulate herbivory. Seedlings had shoot apex, one or two cotyledon(s) removed, or were retained intact. Survival rates were ≥80%, ≥40% and ≥20% for Acacia nilotica, Acacia nigrescens and Faidherbia albida respectively. F. albida mobilized stored cotyledon reserves faster and consequently shed the cotyledons earlier than the two Acacia species. Cotyledons were shed off as late as 70 days post‐emergence with 5‐day shedding earlier than 28‐day and cotyledon life‐span decreasing with intensity of defoliation. Shoot apex removal 28‐day resulted in higher compensatory growth than 5‐day in all three species. Cotyledon removal had no effect on shoot length, while shoot apex removal reduced shoot length. In F. albida root growth was stimulated by shoot apex removal. We conclude that potential tolerance to herbivory in terms of seedling survival was of the order A. nilotica > A. nigrescens > F. albida, timing of shoot apex and cotyledon removal influenced seedling growth in terms of biomass and that shoot apex removal stimulated compensatory growth which is critical to seedling survival.     

Herbivory by hares as a threat to the native brooms

Adult mortality, seed production, and seedling establishment of two species of New Zealand broom (Carmichaelia juncea and C. vexillata) were studied in exclosure trials to determine the level of threat posed by herbivory by introduced mammals. While no effect on mortality was observed for either species, herbivory by hares drastically reduced seed production and subsequent seedling establishment in C. juncea. C. vexillata seemed less vulnerable to herbivore damage due to its plant architecture, as well as the timing and intensity of the herbivore impact. The results of this trial suggest that species characteristics and the dynamics of herbivore impacts need to be considered in planning targeted herbivore control.     

Additive and nonadditive effects of herbivory and competition on tree seedling mortality, growth, and allocation

The interaction between simulated cotyledon herbivory and interspecific competition was studied in a greenhouse experiment using two species of trees, Acer rubrum and Quercus palustris, which commonly invade abandoned agricultural fields. Herbivory treatments were applied as a gradient of cotyledon removal for A. rubrum with 0, 25, 50, 75, and 100% of cotyledon tissue removed. Cotyledons from Q. palustris were clipped and removed (control, early, and late removal) to create a gradient of seed reserve availability. The competition treatment consisted of plugs of old-field vegetation that filled the pots with perennial cover. Mortality of seedlings was higher with competition. There was a significant interaction between herbivory and competition with the highest mortality occurring with competition at the highest intensity of herbivory in both species. Herbivory reduced biomass for Q. palustris only, while competition reduced biomass in both species. Neither species showed an interaction between herbivory and competition for growth. There was a significant interaction between herbivory and competition on allocation patterns for both species, with greater allocation to roots with competition at the highest intensity of herbivory. This study demonstrates the potential for cotyledon herbivory and competition to interact, altering the invasion of tree seedlings into abandoned agricultural land.     

Impacts of seedling herbivory on plant competition and implications for species coexistence

Background and Aims

Although the causes and consequences of seedling herbivory for plant community composition are well understood, the mechanisms by which herbivores influence plant species recruitment to the established phase remain less clear. The aim was to examine how variation in the intensity of seedling herbivory interacts with growth-defence trade-offs and herbivore feeding preferences to affect plant community development.

Methods

Using 14-d-old seedlings of Trifolium pratense and T. repens, relative growth and susceptibility to herbivory by the snail Helix aspersa was quantified to elucidate putative growth-defence trade-offs for these species. Then mixed assemblages of 14-d-old Trifolium seedlings were exposed to herbivory by zero, two, five or ten snails and determined how variation in the intensity of herbivory affected competitive interactions into the mature phase (as measured by total plant biomass at 120 d old).

Key Results

In the absence of herbivory, communities were dominated by T. pratense; a result expected on the basis that it yielded larger and presumably more competitive seedlings. However, when seedlings were exposed to herbivory, the balance of competition shifted. At low levels of herbivory (two snails), both Trifolium species contributed equally to total plant biomass. More intense herbivory (five snails) resulted in almost total mortality of T. pratense and dominance of the mature community by T. repens. The most intense herbivory (ten snails) effectively removed all seedlings from the experimental community.

Conclusions

The study illustrates a mechanism whereby spatio-temporal fluctuations in seedling herbivory, when coupled with species-specific variation in competitive ability and sensitivity to herbivore attack, can differentially influence plant recruitment into the mature phase. This mechanism may be a key element in our attempts to understand plant species coexistence, since fluctuations in plant recruitment are fundamental to the many theories that view coexistence as a consequence of a spatio-temporal lottery for dominance over regeneration micro-sites.Key words: Growth-defence trade-off, lottery models, plant–animal interactions, plant size variability, seedling acceptability, seedling defence, spatio-temporal niches, Trifolium pratense, Trifolium repens     

Fitness consequences of cotyledon and mature-leaf damage in the ivyleaf morning glory

To understand the evolutionary and ecological consequences of natural enemy damage to plants, it is essential to determine how the fitness effects of damage differ depending on the tissues damaged and the subsequent pattern of damage. In a field experiment with the ivyleaf morning glory, the direct and indirect effects on fitness of herbivore damage to cotyledons and mature leaves was evaluated. Damage to mature leaves had negligible direct effects on fitness and no indirect effects on fitness through other correlated traits. Damage to cotyledons also did not directly affect fitness, but did so indirectly through its effects on plant size. These findings suggest that increased resistance to cotyledon damage or increased compensatory growth following cotyledon damage could be effective strategies for plants of this species to counteract the negative effects of herbivory.     

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.     

A fungal endosymbiont affects host plant recruitment through seed- and litter-mediated mechanisms

1.  Many grass species are associated with maternally transmitted fungal endophytes. Increasing evidence shows that endophytes enhance host plant success under varied conditions, yet studies have rarely considered alternative mechanisms whereby these mutualistic symbionts may affect regeneration from seed.
2.  We performed a microcosm experiment to evaluate whether infection with Neotyphodium occultans affects recruitment in the annual grass Lolium multiflorum either directly, by infecting the seeds, or indirectly, by altering the suitability of recruitment microsites through the litter shed by host plants. Endophyte effects on establishment were tested for different litter depths and watering regimes under natural herbivory by leaf-cutting ants.
3.  Seed infection increased seedling emergence through the litter as well as final recruitment, irrespective of microsite conditions. However, litter produced by infected plants delayed emergence and decreased density of both infected and non-infected grass populations.
4.  Individual plant biomass did not change with seed infection but was increased under deep litter from endophyte-infected plants. Although seed infection did not protect establishing plants from leaf-cutting ants, herbivory was reduced in the presence of deep litter shed by infected plants.
5.  We conclude that fungal endophytes may affect host plant recruitment across subsequent generations not only by infecting the seeds but also through the host's dead remains. While the former effect entailed an advantage to infected plants, litter-mediated effects did not discriminate by infection status, and generally promoted the establishment of fewer and larger plants. Thus hidden foliar symbionts may play an underappreciated role in maintaining host species dominance through the litter produced by prior patch occupants.     

Seed size and chemical composition: the allocation of minerals to seeds and their use in early seedling growth

Summary

The seed size that is characteristic of each plant species is of central importance for their regeneration because of its effect on dispersability and seedling establishment. The chemical composition of the stored nutrients is also important in the early stages of growth. The factors that influence individual seed size and nutrient allocation during development on the parent plant are examined, and allocation strategies are compared in different plants. Experiments to determine the effective supply of different elements in seeds are reviewed. The apparent imbalance in the seed nutrient allocation is discussed. Mineral use in early seedling growth is described and the exhaustion of internal nutrient reserves is considered as a means of defining the end of seedling growth phase.     

Establishment and growth of seedlings of Eucalyptus obliqua: Interactive effects of litter,water, and pathogens

We studied how leaf litter, water and fungal pathogens affect the establishment, survivorship, and growth of Eucalyptus obliqua using glasshouse and field experiments. In a glasshouse experiment, the presence of leaf litter of E. obliqua increased the establishment of seedlings when the seeds were placed beneath the litter, but dense litter layers reduced seedling emergence when seeds were placed on top. Results from a complementary experiment suggest that the effect of litter may be mediated by the high humidity microenvironment it creates, which may enhance imbibition of unburied seeds. In another glasshouse experiment, litter in combination with excessive water applications reduced seedling emergence and increased seedling mortality, but the addition of fungicide reverted these effects. Litter with lower water application or fungicide added increased seedling emergence. In all cases higher biomass in seedlings growing in litter treatments was associated with earlier emergence. In two recently burnt sites, the density of seedlings of E. obliqua was positively correlated to the presence of litter. Experimental addition of litter in the field reduced soil temperature during the summer, and together with watering, increased soil water content, and the water potential of established seedlings. However, neither treatment had any positive effect on their growth or survivorship. On the contrary, litter addition reduced the height and number of leaves, probably as a result of increased herbivory. We conclude that in Mediterranean-type systems litter may produce various effects on seedling establishment depending on their developmental stage, and the season.     

Herbivory, serotiny and seedling defence in Western Australian Proteaceae

We examined how acceptability characteristics displayed by 28-day-old seedlings of 12 species of Western Australian Proteaceae affect the likelihood of seedling herbivory in the field. The seedling attributes quantified were cotyledon phenolic, cyanide and nitrogen concentrations, and cotyledon area, thickness and specific leaf area. Only phenolic content was significantly correlated (negatively) with field rates of herbivore attack. This finding shows that the phenomenon of selective herbivore attack on seedlings may be influenced by a specific plant life-history trait, (in this case cotyledon phenolic concentration). In addition, we also studied the interaction between fire, serotiny and herbivory in matched burned and unburned plots. Although herbivore activity was greater in unburned plots, weakly serotinous species were as prone to defoliation as congeneric, strongly serotinous species, even though their seedlings recruit successfully in the absence of fire. This result suggests that seedlings of species able to establish between fires are not better defended against the higher levels of herbivory normally associated with unburned vegetation.     

Induced responses in three tropical dry forest plant species – direct and indirect effects on herbivory

Induced changes in plant quality are hypothesized to reduce herbivore numbers and subsequent damage to the plant. The resultant decrease in herbivory may be due to direct negative impacts on herbivores, through the reduction in foliage quality as food, or due to indirect effects of plant-induced traits interacting with the third trophic level, increasing predation and parasitism rates on herbivores. The relative importance of induced responses as direct and/or indirect defenses has not been evaluated in natural systems. Moreover, few studies have evaluated the influence of early-season damage on late-season herbivory in natural systems, particularly in the tropics. The presence of induced responses and subsequent impact on folivory as a consequence of early-season damage were evaluated in three plant species ( Croton pseudoniveus , Bursera instabilis and Piper stipulaceum ) in a tropical dry forest in Mexico. A two-factorial experiment was applied to determine if induced responses influenced subsequent herbivory directly, by reducing foliage quality, or indirectly, through their interaction with parasitoids and predatory arthropods. Plants from all three species with reduced early-season damage had higher herbivory rates through the rest of the growing season, compared to plants that were damaged during leaf expansion. Chemical analyses showed that early-season damage induced the production of total phenolics and condensed tannins for C. pseudoniveus and B. instabilis , respectively. The mechanism by which these compounds affected subsequent herbivory was most likely by directly reducing foliage quality as food for herbivores, given that predatory arthropods and parasitoids had no effects on herbivory in this study. I conclude that early-season damage in these three species influenced later-season herbivory through the induction of plant responses that may act to reduce plant quality as food for herbivores.     

Effects of above- and belowground herbivory on growth,pollination, and reproduction in cucumber

Plants experience unique challenges due to simultaneous life in two spheres, above- and belowground. Interactions with other organisms on one side of the soil surface may have impacts that extend across this boundary. Although our understanding of plant–herbivore interactions is derived largely from studies of leaf herbivory, belowground root herbivores may affect plant fitness directly or by altering interactions with other organisms, such as pollinators. In this study, we investigated the effects of leaf herbivory, root herbivory, and pollination on plant growth, subsequent leaf herbivory, flower production, pollinator attraction, and reproduction in cucumber (Cucumis sativus). We manipulated leaf and root herbivory with striped cucumber beetle (Acalymma vittatum) adults and larvae, respectively, and manipulated pollination with supplemental pollen. Both enhanced leaf and root herbivory reduced plant growth, and leaf herbivory reduced subsequent leaf damage. Plants with enhanced root herbivory produced 35% fewer female flowers, while leaf herbivory had no effect on flower production. While leaf herbivory reduced the time that honey bees spent probing flowers by 29%, probing times on root-damaged plants were over twice as long as those on control plants. Root herbivory increased pollen limitation for seed production in spite of increased honey bee preference for plants with root damage. Leaf damage and hand-pollination treatments had no effect on fruit production, but plants with enhanced root damage produced 38% fewer fruits that were 25% lighter than those on control plants. Despite the positive effect of belowground damage on honey bee visitation, root herbivory had a stronger negative effect on plant reproduction than leaf herbivory. These results demonstrate that the often-overlooked effects of belowground herbivores may have profound effects on plant performance.     

Seed size, seedling morphology, and response to deep shade and damage in neotropical rain forest trees

To investigate the existence of coordinated sets of seedling traits adapted to contrasting establishment conditions, we examined evolutionary convergence in seedling traits for 299 French Guianan woody plant species and the stress response in a shadehouse of species representing seed size gradients within five major cotyledon morphology types. The French Guianan woody plant community has larger seeds than other tropical forest communities and the largest proportion of hypogeal cotyledon type (59.2%) reported for tropical forests. Yet the community includes many species with intermediate size seeds that produce seedlings with different cotyledonal morphologies. A split-plot factorial design with two light levels (0.8% and 16.1% PAR) and four damage treatments (control, seed damage, leaf damage, stem damage) was used in the shadehouse experiment. Although larger-seeded species had higher survival and slower growth, these patterns were better explained by cotyledon type than by seed mass. Even larger-seeded species with foliar cotyledons grew faster than species with reserve-type cotyledons, and survival after stem grazing was five times higher in seedlings with hypogeal cotyledons than with epigeal cotyledons. Thus, to predict seedling performance using seed size, seedling morphology must also be considered.     

Herbivory and competition slow down invasion of a tall grass along a productivity gradient

Competition models including competition for light predict that small plant species preferred by herbivores will be outshaded by taller unpreferred plant species with increasing productivity. When the tall plant species is little grazed by the herbivores, it can easily invade and dominate short vegetation. The tall-growing grass Elymus athericus dominates the highly productive stages of a salt-marsh succession in Schiermonnikoog and is not preferred by the herbivores which occur there, hares and geese. We studied how interspecific competition and herbivory affected performance during early establishment of this species with increasing productivity. Seedlings were planted in the field in a full factorial design, manipulating both interspecific competition and herbivory. The experiment was replicated along a natural productivity gradient. Competition reduced aboveground biomass production and decreased the number of ramets that were produced but did not affect survival of seedlings. The negative effects of competition on seedling performance increased with increasing productivity. In contrast to our expectations, herbivory strongly reduced seedling survival, especially at the unproductive sites and had only small effects on seedling growth. The present study shows that unpreferred tall-growing species cannot easily invade vegetation composed of short preferred species. Grazing by (intermediate-sized) herbivores can prevent establishment at unproductive sites, and increased competition can prevent a rapid invasion of highly productive sites. Herbivores can have a long-lasting impact on vegetation succession by preventing the establishment of tall-growing species, such as E. athericus, in a window of opportunity at young unproductive successional stages.Plant nomenclature follows Van der Meijden et al. (1990)     

The effect of conspecific density,herbivory, and bamboo on seedling dynamics of a dominant oak in a Neotropical highland forest

Conspecific negative density dependence (CNDD) is one of the main mechanisms influencing diversity maintenance in tropical forests. Tropical highland forests, in contrast to most lowland forests, are commonly dominated by a few tree species, and testing the importance of density dependence effects on seedling establishment of dominant trees may provide insights on the mechanisms regulating population dynamics and forest composition of tropical highlands. We tested the effect of CNDD regulation on seedling survival and recruitment of Quercus costaricensis, a monodominant oak in the Talamanca highland forests of Costa Rica. We used Ripley's K and generalized linear mixed models to test the effects of conspecific density, distance to the nearest adult, density of Chusquea bamboo shoots, and herbivory on the annual survival probability of 3579 seedlings between 2014 and 2017. We did not find a significant effect of CNDD on seedling survival. However, bamboo density and herbivory both significantly decreased oak seedling survival. All seedlings had signs of herbivory and predator satiation may explain the lack of density dependent regulation in seedlings of this species. We argue that the lack of intraspecific density regulation at the seedling stage may contribute to explain the dominance of Q. costaricensis in the highland forests of Costa Rica. Local seedling dynamics of this endemic oak are instead regulated by herbivory and the density of Chusquea. Abstract in Spanish is available with online material.     

The confounding effects of logging on tree seedling growth and herbivory in Central Amazon

Light availability is an important modulator of seedling growth and plant–herbivore dynamics. Logging increases light levels in forests, potentially altering herbivore–plant interactions that drive seedling establishment. We conducted a transplant experiment to evaluate how logging and herbivory affect seedling growth and survival in three shade‐tolerant tree species, at paired canopy gap and understory sites in logged forest and an adjacent unlogged area in central Amazonia (Brazil). Seedlings were either left exposed to naturally occurring insect herbivores or protected from insects by a fine netting structure. We measured the herbivore damage and growth rate of seedlings after 18 mo. In general, logged areas received more light than unlogged sites. Growth and herbivory rates were positively influenced by light, and herbivory was also influenced positively by logging. In gaps, increased growth mitigated foliar damage. Logging resulted in a loss of foliar tissue due to increased herbivory. Herbivory rates were higher in the understory of logged sites than in that of unlogged understory sites, but growth was similar in these areas. Thus, the understory of logged areas provided the least favorable sites for shade‐tolerant tree regeneration, due to higher herbivory rates. The effect of logging on biotic interactions can extend beyond the gaps it creates into untouched understory sites. To our knowledge, this is the first time such a pattern has been observed, highlighting the importance of evaluating the impact of logging on biotic interactions.     

Seedling herbivory, community composition and plant life history traits

Despite the voluminous literature documenting plant-animal interactions, it is only recently that ecologists have begun to focus upon the importance of seedling herbivory in plant communities. This review aims to synthesize our current understanding of the effect that selective seedling removal by herbivores has in shaping post-disturbance plant community structure. In order to do this I describe how individual seedling and plant community characteristics influence the likelihood of seedling herbivory. I argue that seedling palatability, size and morphology, together with the frequency, distribution and timing of seedling emergence all play a significant role in determining seedling regeneration success in the face of herbivore attack. I also outline how current plant defence theories can be related to recent field observations concerning seedling acceptability and removal. In addition, I suggest that those seedling characteristics which provide the emerging plant with some degree of resistance against herbivory should be viewed as one component of a suite of plant life history traits affecting seedling regeneration success or failure. In view of the increasing importance of comparative methods in plant ecology, I propose that future research should integrate seedling acceptability with other plant life history traits thought to affect seedling regeneration. Recent work suggests that seed size may be paramount in determining regeneration success. I explore the possibility that seed size and seedling acceptability may be linked and discuss how these two factors may interact along successional gradients in plant communities.