High abscission rates of damaged expanding leaves: field evidence from seedlings of a Bornean rain forest tree

Herbivore damage is known to cause the premature loss of mature leaves. However, the effects of herbivory on abscission during the early stages of leaf development remain unexplored, even though herbivores frequently prefer unlignified, immature leaves. In a field experiment, we removed 50% of the tissue from leaves at various stages of development on seedlings of Shorea hopeifolia (Dipterocarpaceae), a dominant rain forest tree in Indonesian Borneo. Four weeks following simulated herbivory, >88% of unlignified expanding leaves had been abscised, compared to only 20% of fully expanded, unlignified leaves and 0% of recently lignified, mature leaves. In a separate experiment over 9 wk, simulated herbivory did not increase abscission rates of mature leaves, even when 75% of leaf tissue was removed. Because most (58%) of S. hopeifolia seedlings under natural conditions had lost 1% or less of the tissue from their mature leaves, herbivore damage probably has little effect on the abscission of mature leaves. In contrast, the tendency for damaged expanding leaves to abscise may explain why 49% of S. hopeifolia seedlings had already lost their youngest leaf. If similar patterns occur in other species, herbivore attacks on developing leaves may contribute substantially to both leaf loss and the cumulative impact of herbivory on the growth and survival of whole plants.     

Demographic consequences of chromatic leaf defence in tropical tree communities: do red young leaves increase growth and survival?

Background

Many tropical forest tree species delay greening their leaves until full expansion. This strategy is thought to provide newly flushing leaves with protection against damage by herbivores by keeping young leaves devoid of nutritive value. Because young leaves suffer the greatest predation from invertebrate herbivores, delayed greening could prevent costly tissue loss. Many species that delay greening also produce anthocyanin pigments in their new leaves, giving them a reddish tint. These anthocyanins may be fungicidal, protect leaves against UV damage or make leaves cryptic to herbivores blind to the red part of the spectrum.

Methods

A comprehensive survey was undertaken of seedlings, saplings and mature trees in two diverse tropical forests: a rain forest in western Amazonia (Yasuní National Park, Ecuador) and a deciduous forest in Central America (Barro Colorado Island, Panamá). A test was made of whether individuals and species with delayed greening or red-coloured young leaves showed lower mortality or higher relative growth rates than species that did not.

Key results

At both Yasuní and Barro Colorado Island, species with delayed greening or red young leaves comprised significant proportions of the seedling and tree communities. At both sites, significantly lower mortality was found in seedlings and trees with delayed greening and red-coloured young leaves. While there was little effect of leaf colour on the production of new leaves of seedlings, diameter relative growth rates of small trees were lower in species with delayed greening and red-coloured young leaves than in species with regular green leaves, and this effect remained when the trade-off between mortality and growth was accounted for.

Conclusions

Herbivores exert strong selection pressure on seedlings for the expression of defence traits. A delayed greening or red-coloured young leaf strategy in seedlings appears to be associated with higher survival for a given growth rate, and may thus influence the species composition of later life stages.     

南京地区落叶栎林主要木本植物的展叶动态研究

 植物的展叶过程是由自身遗传因子决定的,同时又受到多种生态因子的调节,反映了植物的生活史对策和群落物种多样性的维持机制。在2001和2002年的3～6月间,不定期记录了南京地区三个落叶栎(Quercus spp.)林中主要木本植物的展叶情况,包括被标记标准枝的叶数、叶的长度、宽度、叶面积、叶干重等参数。结果表明在所调查的落叶栎林中,林冠层物种的成熟叶面积和单位叶面积干重都显著大于林下层物种;最早展叶的物种为林下层物种,但林冠层展叶顺序与林下层无显著差异。叶面积越大、单位叶面积干重越小的物种展叶越晚;林冠层物种展叶较林下层快,物种成熟叶面积越大,展叶速率越大。最后对展叶顺序和展叶速度的生态学意义作了讨论。     

常绿阔叶林中栲树展叶期叶片的虫食格局

叶片的虫食主要发生在展叶期。虽然展叶期短暂, 它却可能是了解植食性昆虫和植物之间相互关系的关键。为了解栲树(Castanopsis fargesii)在展叶期叶片的虫食格局和展叶方式对叶片虫食的影响, 研究了栲树展叶期内的虫食动态变化, 结果表明: 栲树展叶的两个阶段(折叠期和打开期), 虫食叶片的格局存在较大的差异, 打开阶段的日虫食频度和日虫食率显著高于折叠阶段(F_{1, 32}=8.97, p=0.005 4; F_{1, 32}=12.38, p=0.001 4), 展叶期最终叶片虫食频度为50.72%, 叶片虫食率为8.25%。折叠期叶片主要受到低强度的虫食, 打开期叶片虫食则以较大强度的虫食为主。展叶期叶片的虫食主要发生在夜间, 夜间虫食率显著高于日间虫食率(t=2.51, p=0.017), 变化趋势与日虫食率一致。栲树叶片在展叶的两个阶段可能采用了不同的防御对策。     

The consequences of delayed greening during leaf development for light absorption and light use efficiency

Many species of rainforest plants have an unusual form of leaf development such that leaves delay greening until after full leaf expansion. Chlorophyll accumulation was measured during leaf development in five woody rainforest species, three with white young leaves, and two with ‘normal’ greening. In the three species with white leaves, the chlorophyll content of the expanding leaves was about 0.4mg dm^?2, whereas in the two species with green young leaves, chlorophyll content was about 2.1 mg dm^?2. Chlorophyll accumulation in greenhouse and field experiments was independent of light level. During leaf expansion, species with delayed chloroplast development only absorb 18–25% of the maximum possible light, compared with 80% for species with normal greening. Furthermore, species with delayed greening have low chlorophyll contents and reduced absorption for at least 30 d after full expansion. At a PPFD typical of the forest under story, the photosynthetic light use efficiency based upon incident radiation was 0.030–0.036 for species with delayed chloroplast development and 0.068–0.085 for the two species with normal greening. The lower light use efficiency of white species was primarily due to decreased light absorption. However, they also had a slightly lower light use efficiency based upon absorbed radiation, suggesting that development of other components of the photo-synthetic apparatus also may be delayed. Despite the fact that delayed greening decreases light absorption and light use efficiency during leaf development, it is extremely common in shade-tolerant species. We suggest that an advantage of delayed greening is that resources are not invested in the leaf until it is fully expanded and better defended from herbivores.     

The influence of Salix leaf abscission on leaf-miner survival and life history

Abstract. 1. Early abscission of mined leaves was an important mortality factor of a Phyllonorycter species (Lepidoptera: Gracillariidae) on Salix lasiolepis Benth. (Salicaceae). A larger percentage of mined leaves abscised early (34.4% in 1990; 24.5% in 1991), and Phyllonorycter survival was greatly reduced in these abscised leaves.
2. Leaf-mining by Phyllonorycter was associated with increased early leaf abscission. An egg removal experiment demonstrated that leaf mining induced this increase in leaf abscission.
3. The induction of early leaf abscission was dependent upon the timing of herbivory and simulated herbivory (mechanical damage). Early mechanical damage induced leaf abscission, late mechanical damage did not. Mines which expanded early were more likely to induce leaf abscission than mines which expanded more slowly.     

Deciduous leaf drop reduces insect herbivory

Deciduous leaf fall is thought to be an adaptation that allows plants living in seasonal environments to reduce water loss and damage during unfavorable periods while increasing photosynthetic rates during favorable periods. Observations of natural variation in leaf shedding suggest that deciduous leaf fall may also allow plants to reduce herbivory. I tested this hypothesis by experimentally manipulating leaf retention for Quercus lobata and observing natural rates of herbivory. Quercus lobata is primarily deciduous although individuals show considerable natural variation in leaf retention. Oak saplings with no leaves through winter experienced reduced attack by cynipid gall makers the following spring. This pattern was consistent with the positive correlation between natural leaf persistence and gall numbers. These cynipids do not overwinter on the leaves that trees retain through winter, although they appear to use persistent leaves as oviposition cues. If these results are general for woody plants in continental temperate habitats, they suggest that an important and unrecognized consequence of deciduous leaf shedding may be a reduction in herbivore damage, and that this effect should be included in models of deciduous and evergreen behavior.     

Differences in response to simulated herbivory between <Emphasis Type="Italic">Quercus crispula</Emphasis> and <Emphasis Type="Italic">Quercus dentata</Emphasis>

To evaluate the responses of Quercus crispula and Quercus dentata to herbivory, their leaves were subjected to simulated herbivory in early spring and examined for the subsequent changes in leaf traits and attacks by chewing herbivores in mid summer. In Quercus crispula, nitrogen content per area was higher in artificially damaged leaves than in control leaves. This species is assumed to increase the photosynthetic rate per area by increasing nitrogen content per area to compensate leaf area loss. In Quercus dentata, nitrogen content per area did not differ between artificially damaged and control leaves, while nitrogen content per mass was slightly lower in artificially damaged leaves. The difference in their responses can be attributable to the difference in the architecture of their leaves and/or the severeness of herbivory. The development of leaf area from early spring to mid summer was larger in artificially damaged leaves than in control leaves in both species, suggesting the compensatory response to leaf area loss. Leaf dry mass per unit area was also larger in artificially damaged leaves in both species, but the adaptive significance of this change is not clear. In spite of such changes in leaf traits, no difference was detected in the degree of damage by chewing herbivores between artificially damaged and controlled leaves in both species.     

Simulated herbivory advances autumn phenology in Acer rubrum

To determine the degree to which herbivory contributes to phenotypic variation in autumn phenology for deciduous trees, red maple (Acer rubrum) branches were subjected to low and high levels of simulated herbivory and surveyed at the end of the season to assess abscission and degree of autumn coloration. Overall, branches with simulated herbivory abscised ～7 % more leaves at each autumn survey date than did control branches within trees. While branches subjected to high levels of damage showed advanced phenology, abscission rates did not differ from those of undamaged branches within trees because heavy damage induced earlier leaf loss on adjacent branch nodes in this treatment. Damaged branches had greater proportions of leaf area colored than undamaged branches within trees, having twice the amount of leaf area colored at the onset of autumn and having ～16 % greater leaf area colored in late October when nearly all leaves were colored. When senescence was scored as the percent of all leaves abscised and/or colored, branches in both treatments reached peak senescence earlier than did control branches within trees: dates of 50 % senescence occurred 2.5 days earlier for low herbivory branches and 9.7 days earlier for branches with high levels of simulated damage. These advanced rates are of the same time length as reported delays in autumn senescence and advances in spring onset due to climate warming. Thus, results suggest that should insect damage increase as a consequence of climate change, it may offset a lengthening of leaf life spans in some tree species.     

西双版纳热带季节雨林林窗内幼树叶生长与虫食动态

 研究了西双版纳热带季节雨林6种乔木幼树在林窗中的叶生长与叶虫食动态。6种幼树叶生长主要在雨季(5～10月),在旱季雾凉期(11～2月)叶停止生长。阳性树种旱季干热期(3～4月)开始叶生长,顶极树种至5月雨季初才开始叶生长。表明雾凉期低温抑制两类树种叶生长,干热期水分不足抑制顶极树种叶生长。叶生长同步性(每两个月的叶生长量变异系数C．V．)顺序为：望天树(Shorea chinensis,1.42)>金钩花(Pseuduvaria indochinensis,1.41)>八宝树(Duabanga grandiflora, 1.02)>云南石梓(Gmelina arborea,0.98)>团花树(Anthocephalus chinensis,0.84)和铁刀木(Cassia siamea,0.84)。旱季造成一些种类幼树出现落叶高峰,严重叶虫食也导致云南石梓在7～8月出现落叶高峰。叶虫食主要出现在雨季,团花树和云南石梓在干热期叶生长能减少昆虫取食,但此时铁刀木叶同步生长却不能降低食叶昆虫危害。6种幼树叶生长量年进程与叶虫食量年进程间存在正相关,其中望天树、金钩花、八宝树和团花树分别达到显著(p<0.05)或极显著(p<0.01)水平。望天树和金钩花在雨季初叶同步生长能减轻叶虫食。食叶昆虫偏爱取食幼叶,6种幼树平均幼叶的虫食量占总虫食量的72.9％,幼叶虫食速率平均为成熟叶的4.3倍。     

Chemical and mechanical changes during leaf expansion of four woody species of dry Restinga woodland

Young leaves are preferential targets for herbivores, and plants have developed different strategies to protect them. This study aimed to evaluate different leaf attributes of presumed relevance in protection against herbivory in four woody species (Erythroxylum argentinum, Lithrea brasiliensis, Myrciaria cuspidata, and Myrsine umbellata), growing in a dry restinga woodland in southern Brazil. Evaluation of leaf parameters was made through single-point sampling of leaves (leaf mass per area and leaf contents of nitrogen, carbon, and pigments) at three developmental stages and through time-course sampling of expanding leaves (area and strength). Leaves of M. umbellata showed the highest leaf mass per area (LMA), the largest area, and the longest expansion period. On the other extreme, Myrc. cuspidata had the smallest LMA and leaf size, and the shortest expansion period. Similarly to L. brasiliensis, it displayed red young leaves. None of the species showed delayed-greening, which might be related to the high-irradiance growth conditions. Nitrogen contents reduced with leaf maturity and reached the highest values in the young leaves of E. argentinum and Myrc. cuspidata and the lowest in M. umbellata. Each species seems to present a different set of protective attributes during leaf expansion. Myrciaria cuspidata appears to rely mostly on chemical defences to protect its soft leaves, and anthocyanins might play this role at leaf youth, while M. umbellata seems to invest more on mechanical defences, even at early stages of leaf growth, as well as on a low allocation of nitrogen to the leaves. The other species display intermediate characteristics.     

Perfect is best: low leaf fluctuating asymmetry reduces herbivory by leaf miners

Fluctuating asymmetry (FA) represents small, random variation from symmetry and can be used as an indicator of plant susceptibility to herbivory. We investigated the effects of FA of two oak species, Quercus laevis and Q. geminata, and the responses of three herbivore guilds: leaf miners, gallers, and chewers. To examine differences in FA and herbivory between individuals, 40 leaves from each tree were collected, and FA indices were calculated. To examine differences in FA and herbivory within-individuals, we sampled pairs of mined and unmined leaves for asymmetry measurements. Differences in growth of leaf miners between leaf types were determined by tracing 50 mines of each species on symmetric leaves and asymmetric leaves. Asymmetric leaves contained significantly lower concentrations of tannins and higher concentrations of nitrogen than symmetric leaves for both plant species. Both frequency of asymmetric leaves on plants and levels of asymmetry positively influenced the abundance of Brachys, Stilbosis and other leaf miners, but no significant relationship between asymmetry and herbivory was observed for Acrocercops. Brachys and Stilbosis mines were smaller on asymmetric leaves, but differences in mine survivorship between symmetric and asymmetric leaves were observed only for Stilbosis mines. This study indicated that leaf miners might use leaf FA as a cue to plant quality, although differential survivorship among leaf types was not observed for all species studied. Reasons for the different results between guilds are discussed.     

Association of red coloration with senescence of sugar maple leaves in autumn

We evaluated the association of red coloration with senescence in sugar maple (Acer saccharum Marsh.) leaves by assessing differences in leaf retention strength and the progression of the abscission layer through the vascular bundle of green, yellow, and red leaves of 14 mature open-grown trees in October 2002. Computer image analysis confirmed visual categorization of leaves as predominantly green, yellow or red, and chemical quantification of leaf pigment concentrations verified that leaf color reflected underlying differences in leaf biochemistry. Significantly lower chlorophyll concentrations within red and yellow leaves indicated that senescence was more advanced in leaves from these color categories relative to green leaves. Among leaf types, only red leaves contained high concentrations of anthocyanins. There were significant differences in leaf retention capacity among color categories, with the petioles of green leaves being the most firmly attached to twigs, followed by red and then yellow leaves. Microscopic analysis indicated that yellow leaves had the most advanced extension of the abscission layer through the vasculature, with green and red leaves having significantly less abscission layer progression than yellow. A more limited progression of the abscission layer through vascular bundles may be evidence of delayed leaf senescence that could extend resorption of mobile leaf constituents. Together, results from this study suggest an association between leaf anthocyanin content and functional delays in senescence.     

Response of an invasive liana to simulated herbivory: implications for its biological control

Pre-release evaluation of the efficacy of biological control agents is often not possible in the case of many invasive species targeted for biocontrol. In such circumstances simulating herbivory could yield significant insights into plant response to damage, thereby improving the efficiency of agent prioritisation, increasing the chances of regulating the performance of invasive plants through herbivory and minimising potential risks posed by release of multiple herbivores. We adopted this approach to understand the weaknesses herbivores could exploit, to manage the invasive liana, Macfadyena unguis-cati. We simulated herbivory by damaging the leaves, stem, root and tuber of the plant, in isolation and in combination. We also applied these treatments at multiple frequencies. Plant response in terms of biomass allocation showed that at least two severe defoliation treatments were required to diminish this liana's climbing habit and reduce its allocation to belowground tuber reserves. Belowground damage appears to have negligible effect on the plant's biomass production and tuber damage appears to trigger a compensatory response. Plant response to combinations of different types of damage did not differ significantly to that from leaf damage. This suggests that specialist herbivores in the leaf-feeding guild capable of removing over 50% of the leaf tissue may be desirable in the biological control of this invasive species.     

Tree seedling responses to leaf-cutting ants herbivory in Atlantic Forest restoration sites

Leaf-cutting ants (LCA) are generalist herbivores capable of causing severe plant damage. Negative impacts of ant herbivory vary according to the density of nests and availability of palatable plants; however, it is not yet clear how these herbivores affect tropical forest restoration sites. To investigate how LCA preference affects plant species performance, we evaluated the herbivory of Atta sexdens rubropilosa on native tree species seedlings in Atlantic Forest restoration sites. We expected pioneer species to suffer higher herbivory by LCA when compared with non-pioneer species and that species with higher damage will have poorer growth and higher mortality. The experiment was conducted in three restoration sites in northern Paraná state, southern Brazil, with 1,500 seedlings of 5 pioneer and 5 non-pioneer species. Sites share similar age, stand size, tree species composition, and LCA nest density. The number of attacks, degree of leaf damage, number of leaves, plant height, and survival were recorded. Specific leaf area, leaf polyphenols, flavonoids, tannins, and nitrogen content were analyzed for each species. Plant damage was similar between pioneer and non-pioneer plant species. This could be explained by trait variability among species in each group and by LCA generalist foraging. Preferred species suffered decreases in growth and survival. Less preferred species suffered fewer ant attacks and no change in performance. Results suggest that ant herbivory can influence plant species establishment and thus species composition in restoration sites by reducing performance and increasing mortality of some, but not all species, making LCA an important ecological filter.     

广东8种乡土绿化树种的叶结构型性状研究

为探讨乡土绿化树种对广东边缘热带和南亚热带气候的响应特征,在广州和湛江选取8种共有乡土绿化树种进行叶片结构型性状研究,分析两地间各性状的异同以及相关性状与叶比重(LMA)间的关系。结果表明,叶片鲜重(FW)、叶长、叶宽、平均宽度以及干重(DW)、叶面积和叶片含水率等在两地存在差异,但并未表现出一致的变化规律;尖叶杜英(Elaeocarpus apiculatus)、印度紫檀(Pterocarpus indicus)、大叶紫薇(Lagerstroemia speciosa)和非洲楝(Khaya senegalensis)两地间的比叶面积(SLA)差异极显著(P < 0.001);洋紫荆(Bauhinia variegata)的上、中部叶片厚度(TH),黄葛榕(Ficus virens var. sublanceolata)、大叶紫薇、白兰(Michelia alba)和人面子(Dracontomelon duperreanum)的上部叶片厚度均为广州大于湛江(P < 0.05)。LMA与FW和DW呈显著正相关,与叶片含水率呈显著负相关,而与叶面积、叶平均宽度和宽长比并无显著的线性相关关系。这可能是两地的气候条件相差不大,还不足以使乡土树种的结构型性状产生一致性的适应性变化特征。     

The alkaloidal responses of wild tobacco to real and simulated herbivory

Summary I compared the induced alkaloidal response in undamaged leaves of plants subjected to herbivory by the larvae of Manduca sexta and to different simulations of this herbivory; all herbivory treatments removed similar amounts of leaf mass. Although larval feeding induced a significant increase (2.2x) in alkaloid concentrations compared to undamaged plants, the alkaloid responses to larval feeding were significantly lower than the responses to an herbivory simulation (4x controls) which involved removing the same amount of leaf area from the same positions on the leaf, over a similar time period. Moreover, another herbivory simulation, identical in amount of leaf mass removed and duration of damage to the larval feeding, but without regard to spatial array of leaf damage, resulted in an alkaloidal response (5.5x controls) higher still than the previous herbivory simulation. In a second experiment the importance of leaf vein damage on the induced alkaloidal response was examined. Here, leaf removal that involved cutting leaf tissues from between secondary veins before removing the midrib, resulted in alkaloidal responses that were significantly lower (1.7x controls) than responses from leaf removal that involved cutting both veins and midribs along with the intervein tissues (2.6x controls). Vein damage alone did not produce a significant response. These results indicate that herbivory is difficult to simulate: that how a leaf is damaged can be as important as the magnitude of leaf damage in determining a plant's response to damage.     

Herbivory in canopy gaps created by a typhoon varies by understory plant leaf phenology

1. Availabilities of light and soil nitrogen for understory plants vary by extent of canopy gap formation through typhoon disturbance. We predicted that variation in resource availability and herbivore abundance in canopy gaps would affect herbivory through variation in leaf traits among plant species. We studied six understory species that expand their leaves before or after canopy closure in deciduous forests. We measured the availabilities of light, soil nitrogen, soil water content, and herbivore abundance in 20 canopy gaps (28.3–607.6 m²) formed by a typhoon and in four undisturbed stands. We also measured leaf traits and herbivory on understory plants. 2. The availabilities of light and soil nitrogen increased with increasing gap size. However, soil water content did not. The abundance of herbivorous insects (such as Lepidoptera and Orthoptera) increased with increasing gap size. 3. Concentrations of condensed tannins, total phenolics, and nitrogen in leaves and the leaf mass per area increased in late leaf expansion species with increasing gap size, whereas none of the leaf traits varied by gap size in early leaf expansion species. 4. Herbivory increased on early leaf expansion species with increasing gap size, but decreased on late leaf expansion species. In these late leaf expansion species, total phenolics and C : N ratio had negative relationships with herbivory. 5. These results suggested that after typhoon disturbance, increased herbivory on early leaf expansion species can be explained by increased herbivore abundance, whereas decreased herbivory on late leaf expansion species can be explained by variation in leaf traits.     

The Herbivore Assemblage, Herbivory and Leaf Chemistry of the Mangrove Kandelia obovata in Two Contrasting Forests in Hong Kong

The herbivore assemblage, intensity of herbivory and factors determining herbivory levels on the mangrove Kandelia obovata (previously K. candel, Rhizophoraceae) were studied over a 13-month period at two forests with contrasting growing conditions in Hong Kong. Mai Po was part of an eutrophic embayment in the Pearl River estuary and generally offered more favourable conditions for mangrove growth, whereas Ting Kok had a rocky substratum and oceanic salinity. Twenty-four insect herbivore species were recorded on K. obovata, with lepidopteran larvae that consume leaf lamina being the dominant species. While leaf litter production was similar at the two forests, herbivory level at Mai Po (mean = 3.9% in terms of leaf area loss) was more severe than that at Ting Kok (mean = 2.3%). Peak herbivory levels were found in summer at both locations (6.5% for Mai Po and 3.8% for Ting Kok). Young leaves of K. obovata at both locations were generally preferred by the herbivores from the period of late spring to summer. Concentrations of most feeding deterrents (ash, crude fibre, and total soluble tannins) were significantly higher in both young and mature leaves at Ting Kok, whereas leaf nutrients (total nitrogen and water) were the same at the two sites. Young leaves at Ting Kok contained about 30% more tannins than their counterparts at Mai Po. Significant differences in leaf chemistry also existed between young and mature leaves at either site. The differences were concomitant with the observed patterns of leaf herbivory on K. obovata, and suggest a potential relationship between environmental quality and plant defence against herbivory.