Natural variation of nickel,zinc and cadmium (hyper)accumulation in facultative serpentinophytes Noccaea kovatsii and N. praecox

Aims

Data on the variability of hyperaccumulation potential of the facultative serpentinophytes Noccaea kovatsii and N. praecox on different geological substrates are scarce. The aim of this study was to assess the accumulation potential of these two species from ultramafic and non-ultramafic substrates, with special emphasis on the hyperaccumulation of Ni, Zn and Cd.

Methods

Samples of plants and corresponding soils were collected from 16 sites covering a wide range of geochemistry. Elemental concentrations were determined in the roots, shoots and the rhizosphere soils. The pH, particle size distribution and content of organic matter were also determined in the soil samples.

Results

All ultramafic accessions of both species hyperaccumulated Ni with high intraspecific variability. Only one accession of N. kovatsii from a schist soil hyperaccumulated Zn, with also a high Cd accumulation. Accumulation and translocation of Ni in both species were much higher in the ultramafic accessions, whereas Zn accumulation and translocation was found in both ultramafic and non-ultramafic accessions.

Conclusions

Ni accumulation and translocation was restricted to ultramafic populations of both species, whereas it is a species-wide trait for Zn. This study provides new and comprehensive information on the natural variation of hyperaccumulation of Ni, Zn and Cd in N. kovatsii and N. praecox.

     

Differential Responses of Herbivores and Herbivory to Management in Temperate European Beech

Forest management not only affects biodiversity but also might alter ecosystem processes mediated by the organisms, i.e. herbivory the removal of plant biomass by plant-eating insects and other arthropod groups. Aiming at revealing general relationships between forest management and herbivory we investigated aboveground arthropod herbivory in 105 plots dominated by European beech in three different regions in Germany in the sun-exposed canopy of mature beech trees and on beech saplings in the understorey. We separately assessed damage by different guilds of herbivores, i.e. chewing, sucking and scraping herbivores, gall-forming insects and mites, and leaf-mining insects. We asked whether herbivory differs among different forest management regimes (unmanaged, uneven-aged managed, even-aged managed) and among age-classes within even-aged forests. We further tested for consistency of relationships between regions, strata and herbivore guilds. On average, almost 80% of beech leaves showed herbivory damage, and about 6% of leaf area was consumed. Chewing damage was most common, whereas leaf sucking and scraping damage were very rare. Damage was generally greater in the canopy than in the understorey, in particular for chewing and scraping damage, and the occurrence of mines. There was little difference in herbivory among differently managed forests and the effects of management on damage differed among regions, strata and damage types. Covariates such as wood volume, tree density and plant diversity weakly influenced herbivory, and effects differed between herbivory types. We conclude that despite of the relatively low number of species attacking beech; arthropod herbivory on beech is generally high. We further conclude that responses of herbivory to forest management are multifaceted and environmental factors such as forest structure variables affecting in particular microclimatic conditions are more likely to explain the variability in herbivory among beech forest plots.     

Herbivory on Temperate Rainforest Seedlings in Sun and Shade: Resistance,Tolerance and Habitat Distribution

Differential herbivory and/or differential plant resistance or tolerance in sun and shade environments may influence plant distribution along the light gradient. Embothrium coccineum is one of the few light-demanding tree species in the temperate rainforest of southern South America, and seedlings are frequently attacked by insects and snails. Herbivory may contribute to the exclusion of E. coccineum from the shade if 1) herbivory pressure is greater in the shade, which in turn can result from shade plants being less resistant or from habitat preferences of herbivores, and/or 2) consequences of damage are more detrimental in the shade, i.e., shade plants are less tolerant. We tested this in a field study with naturally established seedlings in treefall gaps (sun) and forest understory (shade) in a temperate rainforest of southern Chile. Seedlings growing in the sun sustained nearly 40% more herbivore damage and displayed half of the specific leaf area than those growing in the shade. A palatability test showed that a generalist snail consumed ten times more leaf area when fed on shade leaves compared to sun leaves, i.e., plant resistance was greater in sun-grown seedlings. Herbivore abundance (total biomass) was two-fold greater in treefall gaps compared to the forest understory. Undamaged seedlings survived better and showed a slightly higher growth rate in the sun. Whereas simulated herbivory in the shade decreased seedling survival and growth by 34% and 19%, respectively, damaged and undamaged seedlings showed similar survival and growth in the sun. Leaf tissue lost to herbivores in the shade appears to be too expensive to replace under the limiting light conditions of forest understory. Following evaluations of herbivore abundance and plant resistance and tolerance in contrasting light environments, we have shown how herbivory on a light-demanding tree species may contribute to its exclusion from shade sites. Thus, in the shaded forest understory, where the seedlings of some tree species are close to their physiological tolerance limit, herbivory could play an important role in plant establishment.     

Comparison between two methods to measure herbivory. Is herbivory in the neotropics more severe than we thought?

The quantity of plant tissue consumed by herbivores can be recorded 1) by measuring herbivory in previously marked leaves or 2) by performing punctual measures. i.e. selecting leaves at random to measure the tissue absent in each leaf Punctual measurements are frequently used because they are a faster method to estimate herbivory. However, punctual measures do not include totally consumed leaves. therefore they underestimate the actual herbivory rates. In three species of understory shrubs (Palicourea sp. P. angustifolia and P. oralis: Rubiaccae) herbivory was measured using punctual measures and marking young leaves in order to determine the degree of herbivory underestimation by punctual measurements. Punctual measurements underestimated herbivory up to three times in the species with a high number of totally consumed leaves. In the species with a lower number of totally consumed leaves, herbivory rates recorded using both methods were similar. These results suggest that herbivory in neotropical forests could be more severe than what is currently suggested.     

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.     

Leaf-consumption levels in subtropical mangroves of Paranaguá Bay (SE Brazil)

The objective of this study was to measure leaf consumption levels, mainly by insect herbivores and the tree-dwelling crab Aratus pisonii (H. Milne Edwards, 1837), in mangrove forests of a large subtropical estuarine system in the South Atlantic Ocean, to determine if patterns of herbivory varied with forest structure, tree species and marked seasonal differences in rainfall and temperature. We analyzed three structurally different mangroves located in the euhaline high-energy sector of Paranaguá Bay, all of them with known values of annual litter fall. Consumption levels varied from 2.2–5.4% of total leaf area considering each site as a whole, and from 2.0–6.0% considering each tree species separately. No significant differences in consumption levels were found between summer and winter samples, but significant differences were found among sites and among tree species. Leaves from Laguncularia racemosa were most consumed. The site with lower consumption levels was the one covered with dwarf trees, a condition usually caused by low nutrient availability in the soil. Analysis of nitrogen and phosphorus levels revealed lower amounts of both nutrients in soils and of phosphorus in leaves from this site when compared to the ones containing more developed trees. This result suggests a relationship between herbivory and nutrient availability in the plants.     

Insect herbivory on mangrove leaves in North Queensland*

Estimates of leaf damage by insect herbivores are presented for 25 species of mangrove plants, comprising canopy and understorey species. Leaf area loss was highly variable among the species sampled, with means ranging from 0.3 to 35.0% of expanded leaf area. There was also great variability amongst leaves within species, and the mean coefficient of variation for leaf loss from the 25 species was 266%. Of the 12 species sampled at more than one site in North Queensland, eight exhibited small, but significant, between-site differences in herbivory. In general, it did not appear that height in the canopy influenced herbivory. For the dominant mangrove forest community type at Missionary Bay, an estimated mean of 2.1% of leaf production, or 11 g m^-2 per year, entered the direct grazing pathway. This very low figure is compared with estimates from other studies on mangrove forests and estimates from a variety of Australian terrestrial forests.     

Leaf Phenology and Leaf Damage of Saplings in the Luquillo Experimental Forest,Puerto Rico1

Changes in light or water availability can result in synchronous leaf production, concentrating food availability for herbivores of young leaves to only a few months. To determine the importance of food availability on herbivory, leaf phenology and leaf damage were studied in the Luquillo Experimental Forest (LEF) of Puerto Rico. We studied 20 individuals of eight species for two years. Every month, new leaves were marked; the following month, leaf area and area of damage were measured. Over two years, comparison of leaf production and percent herbivory were performed for each species, and for all species taken together. More than 30 percent of the annual leaf production occurred in May and June. Leaf production was associated with an increase in PFD (photon flux density) and was not related to the patterns of rainfall. Although leaf production was synchronous, there were no differences in herbivory between the peak and non‐peak periods of leaf production. Possible explanations for the constant levels of herbivory throughout the year are the presence of a generalist herbivore community, the ability of herbivores to track changes in food availability, or high densities of herbivore predators that control herbivore populations.     

Herbivory,foliar survival and shoot growth in fragmented populations of Aristotelia chilensis

Habitat fragmentation may modify ecological interactions such as herbivory, and these changes can impinge upon plant fitness. Through a natural experiment, we evaluated if herbivory, foliar survival and shoot growth of the evergreen tree Aristotelia chilensis differ between a continuous forest (600 ha) and small fragments (∼3 ha) of the Maulino forest. From September 2002, we monthly recorded leaf emergence, area lost to herbivores and survival in four cohorts of leaves. Although herbivory of A. chilensis was low overall (foliar area loss <12%), herbivory was higher in the continuous forest than in small fragments. Nevertheless, differences in herbivory hold only for the first cohort of leaves, which were the largest ones. At the end of the growing season, herbivory rates in the continuous forest and fragments converge for all cohorts. Except for the first cohort of leaves, whose survival was higher in the fragments than in the continuous forest, foliar survival and shoot growth was similar in the continuous forest and fragments, and there was no correlation between herbivory and foliar survival or shoot growth. Although Maulino forest fragmentation negatively affects the intensity of herbivory, this effect is only transient, affecting only leaves that emerge early in the season, and might not affect the vegetative fitness of A. chilensis adults. The consequences of changes in ecological interactions triggered by forest fragmentation ought to be assessed rather than inferred from variations in patterns of resource use.     

Evidence of biotic resistance to exotic plant invasion in degraded Bornean forests

Intact tropical forests are generally considered to be resistant to invasions by exotic species, although the shrub Clidemia hirta (Melastomataceae) is highly invasive in tropical forests outside its native range. Release from natural enemies (e.g., herbivores and pathogens) contributes to C. hirta invasion success where native melastomes are absent, and here we examine the role of enemies when C. hirta co-occurs with native Melastomataceae species and associated herbivores and pathogens. We study 21 forest sites within agricultural landscapes in Sabah, Malaysian Borneo, recording herbivory rates in C. hirta and related native Melastoma spp. plants along two 100-m transects per site that varied in canopy cover. Overall, we found evidence of enemy release; C. hirta had significantly lower herbivory (median occurrence of herbivory per plant = 79% of leaves per plant; median intensity of herbivory per leaf = 6% of leaf area) than native melastomes (93% and 20%, respectively). Herbivory on C. hirta increased when closer to native Melastoma plants with high herbivory damage, and in more shaded locations, and was associated with fewer reproductive organs on C. hirta. This suggests host-sharing by specialist Melastomataceae herbivores is occurring and may explain why invasion success of C. hirta is lower on Borneo than at locations without related native species present. Thus, natural enemy populations may provide a “biological control service” to suppress invasions of exotic species (i.e., biotic resistance). However, lower herbivory pressures in more open canopy locations may make highly degraded forests within these landscapes more susceptible to invasion.     

Plant defense against leaf herbivory based on metal accumulation: examples from a tropical high altitude ecosystem

Species that evolved in high‐altitude grasslands, where soils are dystrophic and metal rich, developed adaptations for these extreme conditions, such as metal accumulation and sclerophyllous leaves, and these adaptations may secondarily affect insect herbivory activity. The present study investigates the hypothesis that costs related to accumulation of certain metals may be evolutionarily compensated for by decreasing leaf herbivory in some plant species from rupestrian fields. Studies were conducted in different locations at the Ferriferous Quadrangle, a metal‐rich region in south‐east Brazil, with four species adapted to high‐altitude grasslands: Eremanthus erythropappus, Eremanthus incanus, Lychnophora ericoides and Byrsonima variabilis. Sample design varied according to population sizes and spatial distribution of individuals. We found that concentrations of manganese (Mn) and iron (Fe) significantly reduced the herbivory in the leaves of E. erythroppapus and E. incanus, whereas aluminum (Al) reduced herbivory in L. ericoides, and Mn affected negatively the herbivory in B. variabilis. These results support the hypothesis that metal‐accumulating plants, as a response to the harsh environment in which they evolved, are protected against foliar damage caused by insect herbivores in rupestrian fields.     

Palatability, decomposition and insect herbivory: patterns in a successional old-field plant community

We tested the hypothesis that selective feeding by insect herbivores in an old‐field plant community induces a shift of community structure towards less palatable plant species with lower leaf and litter tissue quality and may therefore affect nutrient cycling. Leaf palatability of 20 herbaceous plant species which are common during the early successional stages of an old‐field plant community was assayed using the generalist herbivores Deroceras reticulatum (Mollusca: Agriolomacidae) and Acheta domesticus (Ensifera: Gryllidae). Palatability was positively correlated with nitrogen content, specific leaf area and water content of leaves and negatively correlated with leaf carbon content and leaf C/N‐ratio. Specific decomposition rates were assessed in a litter bag experiment. Decomposition was positively correlated with nitrogen content of litter, specific leaf area and water content of living leaves and negatively correlated with leaf C/N‐ratio. When using phylogentically independent contrasts the correlations between palatability and decomposition versus leaf and litter traits remained significant (except for specific leaf area) and may therefore reflect functional relationships. As palatability and decomposition show similar correlations to leaf and litter traits, the correlation between leaf palatability and litter decomposition rate was also significant, and this held even in a phylogenetically controlled analysis. This correlation highlights the possible effects of invertebrate herbivory on resource dynamics. In a two‐year experiment we reduced the density of above‐ground and below‐ground insect herbivores in an early successional old‐field community in a two‐factorial design by insecticide application. The palatability ranking of plants showed no relationship with the specific change of cover abundance of plants due to the reduction of above‐ or below‐ground herbivory. Thus, changes in the dominance structure as well as potentially associated changes in the resource dynamics are not the result of differences in palatability between plant species. This highlights fundamental differences between the effects of insect herbivory on ecosystems and published results from vertebrate‐grazing systems.     

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.     

Seasonality of insect herbivory on the leaves of Neoboutonia macrocalyx in the Kibale National Park, Uganda

The seasonality of herbivory on the leaves of Neoboutonia macrocalyx Pax. in Kibale Forest National Park, Uganda, was studied. A total of 2929 fallen leaves was collected during 15 months under randomly-selected trees in three different habitats; natural forest and two selectively cut forest sites. The percentage of leaf area eaten and leaf size were estimated. Leaf herbivory was highly seasonal and correlated with rainfall in the previous 2 months, but less than 100 mm monthly rainfall had no effect. There was no correlation between leaf size and rainfall. Although Kibale Forest has two wet seasons, insect feeding on leaves had only one peak during the major rainy season from September to December. Three to four months after peak herbivory, leaves had very low rates of insect damage. Habitat had only a small effect on the amount of insect feeding. The sampling time accounted for 71% of variation in leaf herbivory. New leaves were formed continuously year-round. The constant leaf production by Neoboutonia trees may be an adaptation to escape generalist herbivorous insects which might be synchronized with the major wet season when the leaf flush of the most other deciduous species occurs. Thus, the availability of fresh leaves is not acting as a regulating factor in seasonality of Neoboutonia herbivory.     

Intraspecific variation in the status of ant symbiosis on a myrmecophyte,<Emphasis Type="Italic"> Macaranga bancana,</Emphasis> between primary and secondary forests in Borneo

A tree species, Macaranga bancana , distributed in South East Asian tropics has a mutualistic relationship with specific symbiotic ant species, which defend the plant from herbivores. To examine the intraspecific variation in the status of the ant-plant symbiosis among microhabitats of different light conditions, we investigated the species composition of nesting ants and the herbivory damage on M. bancana saplings by field observations and sampling in primary and secondary forests in Sarawak. In addition, the effectiveness of non-ant (physical and chemical) defenses were estimated by feeding the larvae of a polyphagous lepidopteran with M. bancana leaves from saplings in the two types of forests. All saplings in the primary forest were colonized by two Crematogaster ant species that had been known to be the obligate symbionts of M. bancana, while in the secondary forest, about half of the saplings were occupied by several ant species that were not obligate symbionts. There was little herbivory damage on saplings colonized by the two Crematogaster symbiont ants in both forest types, while the saplings colonized by the other ant species suffered a 10–60% loss of leaf area. Larval mortality of the polyphagous lepidopteran Spodoptera litura was significantly higher when larvae fed on leaves of M. bancana saplings in the secondary forest than when fed on leaves of M. bancana saplings in the primary forest. These results suggest that the symbiosis between ants and M. bancana is looser and the non-ant-defenses are stronger in secondary forests, where light is more intense, than in primary forests.     

Comparison of Herbivores and Herbivory in the Canopy and Understory for Two Tropical Tree Species1

The Janzen–Connell model of tropical forest tree diversity predicts that seedlings and young trees growing close to conspecific adults should experience higher levels of damage and mortality from herbivorous insects, with the adult trees acting as either an attractant or source of the herbivores. Previous research in a seasonal forest showed that this pattern of distance‐dependent herbivory occurred in the early wet season during the peak of new leaf production. I hypothesized that distance‐dependent herbivory may occur at this time because the new foliage in the canopy attracts high numbers of herbivores that are limited to feeding on young leaves. As a consequence, seedlings and saplings growing close to these adults are more likely to be discovered and damaged by these herbivores. In the late wet season, when there is little leaf production in the canopy, leaf damage is spread more evenly throughout the forest and distance dependence disappears. I tested three predictions based on this hypothesis: (1) the same species of insect herbivores attack young and adult trees of a given plant species; (2) herbivore densities increase on adult trees during leaf production; and (3) herbivore densities in the understory rise during the course of the wet season. Censuses were conducted on adults and saplings of two tree species, raribea asterolepis and Alseis blackiana. Adults and saplings of both species had largely the same suite of chewing herbivore species. On adults of Q. asterolepis, the density of chewing herbivores increased 6–10 times during leaf production, but there was no increase in herbivore density on adults of A. blackiana. Herbivore densities increased 4.5 times on A. blackiana saplings and 8.9 times on Q. asterolepis saplings during the wet season, but there were no clear trends on the adults of either species. These results suggest that the potential of adult trees as a source of herbivores on saplings depends on the value of new leaves to a tree species' herbivores, which may differ across tree species.     

Patterns of leaf-pathogen infection in the understory of a Mexican rain forest: incidence, spatiotemporal variation, and mechanisms of infection

This study assessed the levels of damage by leaf pathogens and their variability in terms of host species, space (four mature forest sites) and season of the year (dry and rainy), and the mechanisms of infection in the understory of the Los Tuxtlas tropical rain forest. Sixty-five percent of the species surveyed in the dry season (N = 49) and 64.9% of those surveyed in the rainy season (N = 57) were damaged by fungi. Leaf area damaged per plant, on average, was <1% (range: 0.25-20.52%). There was considerable variation in the degree of infection among species, but not among sites and seasons. The survey showed that 43% of the leaves were damaged by herbivores and pathogens concurrently, 16% showed damage by insect herbivory alone, and only 1.4% of the sampled leaves showed damage by pathogens alone. Pathogenicity assays experimentally confirmed that the predominant mechanism of fungal establishment was wounding, such as that caused by herbivory (or other similar sources), and only rarely did infection occur through direct contact (without wounds). The results revealed the omnipresence of leaf fungal infection, although with low damage per plant, and the importance of herbivorous insects in the facilitation of fungal infection in tropical understory plants.     

Host-specificity of folivorous insects in a moist tropical forest

1. To assess the degree of herbivore host-specificity in the moist tropical forest on Barro Colourado Island, Panama, I conducted an extensive series of feeding trials on the common insect herbivores from 10 tree species.
2. The herbivores were offered leaves from both congeneric and confamilial plant species to their known host species, as well as leaves from the most abundant tree species in the forest.
3. The amount of damage caused by these herbivores to young, expanding leaves was also measured on nine of the tree species.
4. Of 46 herbivores species (seven Coleoptera, one Orthoptera, 38 Lepidoptera), 26% were specialized to a single plant species, 22% were limited to feeding on a single genus and 37% were able to feed on several genera within a single family. The remaining 15% were generalists, able to feed from several different plant families.
5. The causes of leaf damage varied extensively across the tree species. On average, specialist herbivores caused 58% of the damage to young leaves, generalists herbivores 8% and fungal pathogens 34%. For four of the tree species, pathogens were the most important cause of leaf damage.
6. In this forest, most chewing herbivores appear to have fairly narrow diets, and these specialists are responsible for most of the insect herbivory.     

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.