Comparative morphology of the leaf epidermis in the genera Codonanthe (Martius) Hanstein and Nematanthus Schrader (Gesneriaceae)*

The leaf epidermis of 14 species ofCodonanthe and 10 species of Nematanthus has been examined. Species of Codonanthe section Codonanthe are geographically restricted to south-eastern Brazil, and are diploid. They possess multicellular-uniseriate nonglandular trichomes, glandular trichomes with a four-celled head and a short body, anisocytic stomata and lack extrafloral nectaries. Species of Codonanthe section Spathuliformae and Codonanthe subgenus Codonanthella are distributed from southern Mexico through Central America to north-western South America and are tetraploid. They possess unicellular non-glandular trichomes (except C. caribaea), glandular trichomes with a two-celled head (except C. caribaea) and a short body, anisocytic stomata and extrafloral nectaries (except C. caribaea). All Nematanthus species are distributed in south-eastern Brazil and are diploid (N=8). Six species of Nematanthus consistently have multicellular-uniseriate nonglandular trichomes, glandular trichomes with a four-celled head and a short (unicellular) or long (multicellular) body, anisocytic stomata and lack extrafloral nectaries. Four species of Nematanthus have multicellular-uniseriate non-glandular trichomes, glandular trichomes with a head of more than four cells and a short body, anisocytic and helicocytic stomata and lack extrafloral nectaries.     

Allometric analysis of the induced flavonols on the leaf surface of wild tobacco (Nicotiana attenuata)

Trichomes excrete secondary metabolites that may alter the chemical composition of the leaf surface, reducing damage caused by herbivores, pathogens and abiotic stresses. We examined the surface exudates produced by Nicotiana attenuata Torr. Ex Wats., a plant known to contain and secrete a number of secondary metabolites that are toxic or a deterrent to herbivorous insects. Extractions specific to the leaf surface, the trichomes, and the laminar components demonstrated the localization of particular compounds. Diterpene glycosides occurred exclusively in leaf mesophyll, whereas nicotine was found in both the trichomes and mesophyll. Neither rutin nor nicotine was found on the leaf surface. Quercetin and 7 methylated derivatives were found in the glandular trichomes and appeared to be excreted onto the leaf surface. We examined the elicitation of these flavonols on the leaf surface with a surface-area allometric analysis, which measures changes in metabolites independent of the effects of leaf expansion. The flavonols responded differently to wounding, methyl jasmonate (MeJA), herbivore attack and UV-C radiation, and the response patterns corresponded to their compound-specific allometries. Finding greater amounts of quercetin on younger leaves and reduced amounts after herbivore feeding and MeJA treatment, we hypothesized that quercetin may function as an attractant, helping the insects locate a preferred feeding site. Consistent with this hypothesis, mirids (Tupiocoris notatus) were found more often on mature leaves sprayed with quercetin at a concentration typical of young leaves than on unsupplemented mature leaves. The composition of metabolites on the leaf surface of N. attenuata changes throughout leaf development and in response to herbivore attack or environmental stress, and these changes are mediated in part by responses of the glandular trichomes.     

HETEROPHYLLY IN POPULUS GRANDIDENTATA (SALICACEAE) WITH EMPHASIS ON RESIN GLANDS AND EXTRAFLORAL NECTARIES

Big-tooth aspen displays heterophylly on twigs of saplings and on upper, vigorously growing twigs of larger trees. Early leaves, those present in overwintering buds which expand in spring, differ from late leaves, those that are mostly initiated and developed during the late spring and summer of the same year. The two sets of leaves differ in size, shape, number of teeth, number of marginal resin glands, and number and size of basilaminar extrafloral nectaries. Secretory structures are generally more prominent and active on late leaves. Marginal resin glands, resin-secreting stipules, and basilaminar nectaries of both early and late leaves are similar anatomically, having a secretory epidermis of cytoplasmically dense palisade-like cells separated from vascular bundle endings by several layers of isodiametric parenchyma. These secretory structures, and the dense mat of trichomes which cover the leaf until it fully expands, may help to protect the young leaves from insect damage. The basilaminar nectaries seem especially effective because they attract ants that probably discourage visits by other insects.     

MORPHOLOGY AND DISTRIBUTION OF PETIOLAR NECTARIES IN IPOMOEA (CONVOLVULACEAE)

The distribution of petiolar nectaries in 24 species of Ipomoea was investigated. Petiolar nectaries were found on 12 species (8 new reports, 4 confirmations of previous reports) and quoted from the literature as being found on 3 other species; they were absent from 9 species investigated. The structure of petiolar nectaries in the genus ranges from simple beds of superficial nectar-secreting trichomes (1 species), to slightly recessed “basin nectaries” (8 species), to “crypt nectaries,” which are structurally the most complex extrafloral nectaries known (3 species). (Structures were not determined for 3 species.) Petiolar nectaries are present in all subgenera, but all crypt nectaries occur in the same section (Eriospermum). Species with extrafloral nectaries tend to be perennial; species lacking extrafloral nectaries tend to be annual. There is no relationship between temperate or tropical habitat and presence of nectaries.     

Two Mallotus species of different life histories adopt different defense strategies in relation to leaf age

Plants defend their leaves using multiple defense traits that change functions with leaf age. We examined the effects of leaf age on the development of multiple defense traits in two related Mallotus (Euphorbiaceae) species: young plants of the fast‐growing Mallotus japonicus (Spreng.) Müll. Arg. and the slow‐growing Mallotus philippensis (Lam.) Müll. Arg. Sequential leaves of the two species were measured for their leaf area, leaf mass/area, densities of trichomes and pellucid dots, extrafloral nectar volume, and the numbers of extrafloral nectaries and pearl bodies. Mallotus japonicus shifted its defense tactics from direct defense using trichomes and pellucid dots in young leaves to biotic defense using extrafloral nectar and pearl bodies in middle‐aged leaves. In contrast, M. philippensis used direct, chemical defense throughout all leaf ages, together with the shift from indirect, biotic defense using extrafloral nectar in young leaves to direct, physical defense using leaf toughness in middle‐aged leaves. These results strongly suggest that, in relation to life history, plants can alter optimal combinations of multiple defense traits with leaf age.     

城市绿化植物叶片表面特征对滞尘能力的影响

以西安市21种常见绿化植物为对象,采用人工降尘方法测定植物叶片的最大滞尘量,研究植物叶片表面绒毛、润湿性、表面自由能及其分量对滞尘能力的影响.结果表明： 21种供试植物叶片的最大滞尘量在0.8～38.6 g·m^-2,不同树种最大滞尘量差异显著,物种间相差40倍以上.叶片表面绒毛数量及其形态、分布特征对滞尘能力具有重要影响,可能与绒毛和颗粒物间的作用方式有关.除叶片表面着生绒毛的悬铃木、国槐、榆叶梅和毛梾4个物种外,其他植物叶片接触角与最大滞尘量均呈显著负相关.接触角较小、易润湿的植物叶片最大滞尘量在2.0～8.0 g·m^-2,而接触角较大的银杏、三叶草、紫叶小檗和鸡爪槭的最大滞尘量均＜2.0 g·m^-2.叶片表面自由能主要表现分子间色散力的作用,而极性分量对表面自由能的贡献低于20%,可能与叶片表面含有的非极性或弱极性物质有关.最大滞尘量与叶片表面自由能及其色散分量呈显著正相关,而与极性分量的相关关系不显著.     

Contrasting exotic Solenopsis invicta and native Forelius pruinosus ants as mutualists with Catalpa bignonioides, a native plant

Abstract. 1. The suitability of the red imported fire ant Solenopsis invicta Buren and a native ant Forelius pruinosus (Roger) as participants in a food-for-protection mutualism with a native nectaried tree Catalpa bignonioides Walter was compared.
2. The mean mortality of folivore larvae of Ceratomia catalpae Boisduval was similar for S. invicta and F. pruinosus although S. invicta attacked fewer caterpillar aggregations and was a devastating pupal predator. Solenopsis invicta also differed from the native ant in that it attacked the parasitoid Cotesia congregata Say, another plant mutualist, and visited extrafloral nectaries less frequently.
3. Habitats invaded by S. invicta are characterised by a scarcity of both herbivores and of beneficial insects that visit extrafloral nectaries. The plants do not require protection, and extrafloral nectaries are visited rarely. Although plants are defended incidentally by S. invicta , the insect-plant mutualism therein is greatly simplified or defunct.     

DISTRIBUTION OF DEFENSE NECTARIES IN IPOMOEA (CONVOLVULACEAE)

The structure and distribution of defense nectaries in the genus Ipomoea (Convolvulaceae) were investigated. These nectaries do not reward pollinators and probably contribute to antiherbivore defense. Of 22 species sectioned, 15 had defense nectaries on the sepals. Of 12 other species observed, ten had sepal nectaries and two did not. Structurally, 14 of the species sectioned had crypt sepal nectaries and one had a basin nectary. Of the 14 species with crypt nectaries, two had invaginated spaces adding greatly to the internal area of these nectaries, and forming the most complex nectaries that have been reported. We term these labyrinthine crypt nectaries. All three types of nectaries are lined with secretory trichomes along the proximal surfaces of the crypts. Species with defense nectaries on the sepals tend to have petiolar defense nectaries as well, but the two locations may have different nectary types; e.g., basins on the petiole and crypts on the sepals. Since most reports of the function of these nectaries have shown antiherbivore defense by nectar feeders, the distributions of defense nectaries with respect to region and life history of the species were sought. Plants without sepal nectaries were found to have significantly smaller seeds than plants with sepal nectaries; they were also more frequently annuals. No significant relationship was found between region or breeding system and defense nectaries.     

Sucking herbivore assemblage composition on greenhouse <Emphasis Type="Italic">Ficus</Emphasis> correlates with host plant leaf architecture

Understanding arthropod herbivore selectivity trends towards host plant attributes is essential for predicting plant-associated herbivore assemblage structure. Little is known about such interactions between spontaneous herbivore species and cultivated plants under specific conditions of botanical garden greenhouses. In this study, the taxonomic and functional composition of sucking arthropod herbivore assemblages were correlated with leaf anatomical and surface features of 33 host species of Ficus L. (Moraceae) across four distantly located greenhouse complexes of botanical gardens. The analyses revealed that the species number and abundance of scale insects and their individual families, sessile phloem feeders, total phloem feeders and total herbivores were significantly positively correlated with the thickness of leaf lamina, epidermis and mesophyll, stomatal length and width, and the presence of abaxial multiple epidermis and weak ferruginous non-glandular trichomes. Significant negative correlations were revealed between the same herbivore parameters and the density of glandular trichomes. Heliomorphic leaves supported higher abundance and species richness of sessile phloem feeders compared to sciomorphic ones. The parameters of some phloem and mesophyll feeder taxa also correlated with non-glandular trichome length and density, type of trichomes and epicuticular wax layer, and the presence of calcium oxalate crystals in the epidermis. Results of the study suggest that the leaf architecture-related herbivory trends under greenhouse conditions are similar to those occurring in natural ecosystems when considering the functional significance of particular leaf traits, and remain relevant at the scale of particular plant taxa with disregard of spatial factor.     

Relationship between physical leaf characteristics and growth and survival of polyphagous grasshopper nymphs, <Emphasis Type="Italic">Parapodisma subastris</Emphasis> (Orthoptera: Catantopidae)

Common types of plant defense mechanisms are thought to affect the host ranges of polyphagous herbivorous insects, yet few studies have examined the relationship between host plant suitability for polyphagous insects and defense against them. We investigated the suitability of the 19 plant species growing in the habitat of the polyphagous grasshopper, Parapodisma subastris, to determine the relationship between the physical characteristics of leaves and the growth and survival of grasshopper nymphs. We examined leaf toughness, trichome density, and length. Nymph survival was greater on plants with characteristics ranging from soft leaves and dense trichomes to tough leaves and few trichomes than on plants with soft leaves and few trichomes. The exception was Rorippa indica, a plant with soft leaves and few trichomes that uses biotic defense, on which nymph survival was maximal. Higher-quality plants that share common physical characteristics over families may favor polyphagy by grasshoppers that possess ability to overcome the physical defense easily with their robust mandibles.An erratum to this article can be found at     

Within-plant distribution of phenolic glycosides and extrafloral nectaries in trembling aspen (Populus tremuloides; Salicaceae)

Expression of foliar secondary compounds and extrafloral nectaries (EFNs) within the same leaves may be incompatible if secondary compounds repel beneficial insects that might otherwise be attracted to EFNs. This study examined the within-plant distributions of phenolic glycosides and EFNs in trembling aspen, Populus tremuloides, and their relationships to herbivore damage. Populus tremuloides expresses extrafloral nectaries (EFNs) on a subset of its leaves. We studied short and tall naturally occurring aspen ramets across multiple sites in interior Alaska. Contrary to our expectations, foliar phenolic glycoside concentrations were approximately 30% greater on leaves bearing EFNs than on leaves without EFNs. The mean concentration of foliar phenolic glycosides in short ramets was nine times that in tall ramets. Phenolic glycoside concentration was negatively related to leaf mining damage by Phyllocnistis populiella (Lepidoptera; Gracilliadae) at concentrations greater than 27 mg/g, whereas the presence of EFNs was unrelated to mining damage. The positive association of chemical defensive compounds and EFNs in leaves suggests that, for species with variation in EFN expression, negative correlations between herbivory and EFN expression may arise indirectly from associated effects of other, correlated types of defense.     

中国独行菜族部分属种的叶表皮观察

利用光学显微镜对中国十字花科独行菜族部分广布属及相关属植物进行了叶表皮微形态学观察研究,结果表明:所研究的中国独行菜族植物叶表皮微形态具有多样性,可以划分为两种类型:第一类,叶上下表皮同形或近同形,叶表面被单毛或光滑无毛,包括独行菜属、群心菜属、菘蓝属和菥蓂属;第二类,叶上下表皮不同形,叶表面被分支毛和单毛,包括荠属和亚麻荠属;叶表皮微形态结果支持荠属应从独行菜族中移出,独行菜族是一多系类群,同时认为荠属与亚麻荠属植物具有较近的亲缘关系。     

Extrafloral nectaries in the genus Macaranga (Euphorbiaceae) in Malaysia: comparative studies of their possible significance as predispositions for myrmecophytism

Some species of the paleotropical tree genus Macaranga (Euphorbiaceae) live in close association with ants. The genus comprises the full range of species from those not regularly inhabited by ants to obligate myrmecophytes. In Malaysia (Peninsular and Borneo) 23 of the 52 species are known to be ant-associated (44%). The simplest structural adaptation of plants to attract ants are extrafloral nectaries. We studied the distribution of extrafloral nectaries in the genus Macaranga to assess the significance of this character as a possible predisposition for the evolution of obligate myrmecophytism. All species have marginal glands on the leaves. However, only the glands of non- myrmecophytic species function as nectaries, whereas liquids secreted by these glands in myrmecophytic species did not contain sugar. Some non-myrmecophytic Macaranga and transitional Macaranga species in addition have extrafloral nectaries on the leaf blade near the petiole insertion. All obligatorily myrmecophytic Macaranga species, however, lack additional glands on the lamina. The non-myrmecophytic species are visited by a variety of different ant species, whereas myrmecophytic Macaranga are associated only with one specific ant-partner. Since these ants keep scale insects in the hollow stems, reduction of nectary production in ant-inhabited Macaranga seems to be biologically significant. We interpret this as a means of (a) saving the assimilates and (b) stabilization of maintenance of the association's specificity. Competition with other ant species for food rewards is avoided and thereby danger of weakening the protective function of the obligate ant- partner for the plant is reduced. A comparison with other euphorb species living in the same habitats as Macaranga showed that in genera in which extrafloral nectaries are widespread, no myrmecophytes have evolved. Possession of extrafloral nectaries does not appear to be essential for the development of symbiotic ant-plant interactions. Other predispositions such as nesting space might have played a more important role.     

Morphology, development and homologies of the perianth and floral nectaries in Croton and Astraea (Euphorbiaceae-Malpighiales)

New observations are presented on the ontogeny, vasculature and morphology of both staminate and pistillate flowers of Croton and Astraea. These data support earlier hypotheses that the filamentous structures in pistillate flowers represent reduced and transformed petals. Staminate flowers of both genera possess five free nectaries, which are vascularised by divergences of the sepal traces in Croton and unvascularised in Astraea. In pistillate flowers, there are five separate non-vascularised nectaries in Astraea, but in Croton there is a single nectariferous disk that is vascularised by divergences of the sepal traces. The nectaries are initiated late in floral development, but their location indicates that they could represent the outer stamen whorl transformed into secretory staminodes. Other glandular structures occur in pistillate flowers of most Croton species, resulting in flowers with two secretory organ whorls. In these cases, the inner whorl is formed by modified staminodes. Our observations support the recent segregation of Astraea species from the larger genus Croton. Despite strong similarities between the two genera, there are clear structural differences, including the presence of colleters in Astraea (absent in Croton), moniliform trichomes on petals (rather than simple trichomes in Croton), non-vascularised nectaries (vascularised in Croton) and reduced, non-secretory filamentous structures (well developed and secretory in Croton).     

Oviposition,larval survival and leaf damage by the willow leaf blotch miner,Micrurapteryx salicifoliella,in relation to leaf trichomes across 10 Salix species

1. Foliar trichomes clearly reduce chewing damage and efficiency of movement by some insect herbivores, but the effect of trichomes on insect oviposition is less well characterised. Trichomes are likely to have particularly strong, negative effects on species that require secure attachment of the egg to the leaf epidermis for successful transition to the feeding stage – a group that includes many leaf mining insects. 2. One such species, Micrurapteryx salicifoliella, must initially enter leaf cells directly from an egg adhered to the cuticle, but later instars can move between leaves and initiate new mines from the leaf exterior. 3. Natural patterns of occurrence by M. salicifoliella were quantified on 10 sympatric Salix species varying in trichome expression to test whether trichomes were associated with reduced oviposition, larval survival and leaf damage. 4. Mean egg density and leaf mining damage were negatively related to mean trichome density across Salix species. Survival of M. salicifoliella from egg to pupa was positively related to trichome density, suggesting that initiation of new mines by late‐instar larvae was not adversely affected by trichomes. There was no evidence that trichomes benefited leaf miner larvae indirectly by decreasing density‐dependent mortality; rather, the positive relationship between trichome density and larval survival may reflect less effective chemical defence by Salix species expressing high trichome density. 5. The results suggest that foliar trichomes serve as an effective defence against M. salicifoliella by deterring oviposition, but do not reduce the survivorship of those individuals that successfully transition from egg to larva.     

Functional interaction between leaf trichomes, leaf wettability and the optical properties of water droplets

Abstract. Because CO₂ diffuses 10000 times more slowly through water than air, there may be strong selective pressure for increased water repellency in terrestrial plant leaves. In the present study, leaf trichomes appeared to have a strong influence on leaf water repellency (i.e. degree of water droplet formation on the leaf surface) as well as the retention of droplets on the leaf. Based upon evaluation of 38 plant species from 21 families, we found that leaves with trichomes were more water repellent, especially where trichome density was greater than 25mm². However, droplet repellency and retention were both high in some species where trichomes entrapped droplets. Finally, the lensing effects of water droplets on leaf surfaces increased incident sunlight by over 20-fold directly beneath individual droplets. These results may have important implications for such processes as stomatal function, whole leaf photosynthesis, and transpiration for a large variety of plant species.     

Tibor Jermy (1917–2014)

Throughout the course of their evolution, plants have acquired a wide range of chemical and mechanical defenses to protect against herbivores. Ehrlich & Raven's coevolutionary theory suggests that this diversification of defensive traits is driven by the strong impact of novel traits on insect herbivores. However, the impact of plant defenses on insects is difficult to compare between related plant species due to variation in environmental and biotic conditions. We standardized these factors as far as possible by analyzing the effects of chemical and mechanical defensive traits on insects in a local community of 11 Salicaceae species growing in sympatry, and their leaf‐chewing herbivores. Defensive traits (salicylates, flavonoids, tannins, trichomes, and leaf toughness) were generally not inter‐correlated, with the exception of a negative correlation between salicylates and trichomes. The content of salicylates, a novel group of defensive metabolites in the Salicaceae, was correlated with low herbivore diversity and high host specificity. Despite these effects, the phylogeny of the studied species shows loss of salicylates in some Salix species instead of their further diversification. This could be due to salicylates not decreasing the overall abundance of herbivores, despite accounting for up to 22% of the dry leaf mass and therefore being costly. The defense of low‐salicylate willow species is thus probably maintained by other defensive traits, such as trichomes. Our study shows that the balance between costs and benefits of defensive traits is not necessarily in favor of novel compounds and illustrates a process, which may lead to the reduction in a defensive trait.     

Glandular trichomes as a barrier against atmospheric oxidative stress: Relationships with ozone uptake,leaf damage,and emission of LOX products across a diverse set of species

There is a spectacular variability in trichome types and densities and trichome metabolites across species, but the functional implications of this variability in protecting from atmospheric oxidative stresses remain poorly understood. The aim of this study was to evaluate the possible protective role of glandular and non‐glandular trichomes against ozone stress. We investigated the interspecific variation in types and density of trichomes and how these traits were associated with elevated ozone impacts on visible leaf damage, net assimilation rate, stomatal conductance, chlorophyll fluorescence, and emissions of lipoxygenase pathway products in 24 species with widely varying trichome characteristics and taxonomy. Both peltate and capitate glandular trichomes played a critical role in reducing leaf ozone uptake, but no impact of non‐glandular trichomes was observed. Across species, the visible ozone damage varied 10.1‐fold, reduction in net assimilation rate 3.3‐fold, and release of lipoxygenase compounds 14.4‐fold, and species with lower glandular trichome density were more sensitive to ozone stress and more vulnerable to ozone damage compared to species with high glandular trichome density. These results demonstrate that leaf surface glandular trichomes constitute a major factor in reducing ozone toxicity and function as a chemical barrier that neutralizes the ozone before it enters the leaf.