Atlantica Trees Research Articles

UV-B-absorbing compounds in modern Cedrus atlantica pollen: The potential for a summer UV-B proxy for Northwest Africa

Sporopollenin is a complex biopolymer which is the main component of the pollen grain exine and is partly composed of the aromatic compounds para-coumaric acid ( pCA) and ferulic acid (FA). These compounds absorb ultraviolet-B radiation (UV-B, 280–315 nm), and their abundance in pollen and spores has been shown to increase in response to increased UV-B flux. Here, we show that the relative abundance of UV-B-absorbing compounds (UACs) measured using Fourier Transform Infrared Spectrometry (FTIR) in modern pollen of autumn-pollinating Cedrus atlantica trees increases in response to summer UV-B flux. This relationship was observed in native Moroccan samples ( r2 = 0.84, p < 0.0001), but not across a larger environmental gradient including non-Moroccan samples ( r2 = 0.00, p = 0.99). For non-Moroccan samples of known provenance, the abundance of UACs is similar to the abundance of UACs found in samples from their place of origin. The FTIR spectra of these samples also closely resemble the FTIR spectra of samples from their place of origin. This unexpected finding suggests there could be a heritable component to UAC production possibly associated with epigenetic memory, an important adaptive mechanism in conifers. Our results indicate that the relative abundance of UACs in Cedrus atlantica pollen could be used as a proxy to reconstruct historic summer UV-B flux in Northwest Africa during at least the Holocene and Late Glacial period while also highlighting how UV-B proxies should be established using pollen samples from specimens growing in their native range or environment.

Effect of the Galling Aphid of Baizongia pistaciae L. on Composition and Biological Activities of Essential Oils of Pistacia atlantica Desf. Growing Wild in Jordan

Aqueous extract of Pistacia atlantica leaves is widely used in Jordanian traditional medicine for management of diabetes. The genus Pistaciae serves as obligate host for a group of specialized gall-forming aphids. The present study aimed to identify the aphid attacking P. atlantica trees growing wild in Jordan, to determine the composition of the essential oils from leaves and galls (fresh and dry) and to investigate the antiproliferative activities of the traditionally used dry plant on colon and breast cancers. Hydro-distillation of the essential constituents of P. atlantica leaves was performed and their composition determined. The antiproliferative activity of leaf and galls oils, doxorubicin, and six pure components (sabinene, limonene, α-pinene, β-pinene, α-terpinene, and γ-terpinene) were investigated against two colon (Caco-2 and HCT116) and two breast cancer cell lines (MCF7 and T47D) by MTT assay. Fresh leaf showed the greatest variation in the constituents’ composition. Low molecular weight monoterpene hydrocarbons were the major constituents of both tested organs. The highest percentage of sesquiterpenes was observed in fresh leaf oil, with γ-muurolene as the major component. Tested components exhibited differences in their toxicity against the cell lines under experiments. Cytotoxic effect of doxorubicin was enhanced by the addition of P. atlantica leaf oil but not galls oil. Our findings demonstrated qualitative and quantitative diversity in the composition of the P. atlantica oils. The oils exhibited differences in the antiproliferative activity against colon and breast cancer cell lines. Further molecular experiments are needed to explain such differences.

Are microbial symbionts involved in the speciation of the gall-inducing aphid, Slavum wertheimae?

Microbial symbionts have come to be recognized as agents in the speciation of their eukaryote hosts. In this study, we asked if bacterial symbionts are, or were in the past, involved in the speciation of the gall-inducing aphid Slavum wertheimae (Hemiptera: Aphididae). This aphid is specific to the tree Pistacia atlantica, which has a fragmented distribution among mesic and xeric habitats, leading to corresponding fragmentation of the aphid population. Previous studies revealed genetic differentiation among populations of the gall-inducing aphid, suggesting cryptic allopatric speciation. Pistacia atlantica trees show no such variation. By means of diagnostic PCR, we screened several populations of S. wertheimae from mesic and xeric sites in Israel for the presence of nine known aphid symbionts: Arsenophonus, Hamiltonella, Regiella, Rickettsia, Rickettsiella, Serratia, Spiroplasma, Wolbachia, and X-type, as well as Cardinium, known to be a reproductive manipulator. Only one symbiont, Wolbachia, was detected in S. wertheimae. Wolbachia was found in all the aphids of the mesic populations, compared to 26% in the aphids from the xeric populations. Multilocus Sequence typing of Wolbachia revealed new haplotypes in the fbpA and coxA genes in both the mesic and xeric populations. Phylogenetic analysis showed that Wolbachia of S. wertheimae is closely related to Wolbachia strains from assorted hosts, mostly lepidopterans, but only distantly related to Wolbachia strains from other aphid species. We conclude that the cryptic speciation of mesic and xeric populations of S. wertheimae was likely driven by geographical isolation rather than by Wolbachia.

Epiphytic lichen is associated with species richness of gall-inducing aphids but not with niche differentiation among them

The presence of epiphytic foliose lichen amplifies the heterogeneity of habitat by creating shelters for insects living on tree bark. It thus should enhance species number and spatial niche segregation among these canopy insects. We studied this hypothesis in a field experiment using four aphid species that induce galls on Pistacia atlantica trees covered with Xanthoria parietina lichen. In autumn 2008, 3 months after aphid fundatrices were oviposited, we marked six branches on each of 29 trees. Two served as a control, whereas the other four were isolated with insect glue; two of them were scraped with sandpaper to remove epiphytic foliose lichens. We therefore obtained three treatments comprising control branches, isolated branches with lichen, and isolated branches without lichen. In summer 2009, we counted all the galls developing on five new annual shoots on each of 174 branches. We observed more cecidogenic aphid species on all the branches with lichens than without, but each species at different proportions. The different frequencies of utilization of the lichen did not lead to habitat partitioning between species. In conclusion, although habitat heterogeneity itself was associated with species richness and population abundance, it did not induce spatial niche segregation. Considering that many economically important insect species, pests and natural enemies, oviposit or spend some portion of their lives in bark cracks, it is possible that some can use lichens too for protection or/and oviposition sites. As a consequence, lichens may affect management of agrosystems and their impacts should be investigated more deeply in such contexts.

Structure and spatio-temporal dynamics of cedar forests along a management gradient in the Middle Atlas, Morocco

Diameter distribution and temporal and spatial patterns of a Cedrus atlantica forest were studied across a management gradient (undisturbed, logged and highly disturbed) in Ifrane National Park, Morocco. Forest structure and regeneration dynamics showed significant differences among management levels. The diameter distribution in undisturbed and logged stands indicated the presence of few young individuals, and a poor regeneration status in highly disturbed stands. Variance in diameter was larger in natural stands compared to managed ones. There was a seedling establishment pulse during the time period between 1910 and 1990 at three sites, but a lack of sapling and juveniles occurred at undisturbed and logged forests in the last century, which might be attributed to competition between C. atlantica and Quercus ilex. Nevertheless, cedar trees persistently recruited to all forests during the last 50years, but cedar density was significantly higher in the highly disturbed forest areas. Spatial analysis shows a general trend toward aggregation for all species involved. This pattern was observed among C. atlantica trees in undisturbed and highly disturbed stands but was not significant in logged stands. Differences in management may promote variation in stand structure and regeneration dynamics of the subalpine cedar forests along the management gradient in the Middle Atlas, Morocco.

Genetic structure of a galling aphid Slavum wertheimae and its host tree Pistacia atlantica across an Irano-Turanian distribution: from fragmentation to speciation?

The Irano-Turanian distribution zone in the Levant crossroad is fragmented along different phyto- and zoogeographic and climatic regions, a relict of wider distribution in moister conditions during the Pleistocene and the Holocene. We examined the effect of the disjunct Irano-Turanian distribution among distinct mesic and xeric habitats on the genetic structure of the gall-forming aphid Slavum wertheimae and its obligate host tree Pistacia atlantica in Israel and Jordan. The genetic study included amplified fragment length polymorphism analysis of the trees and aphids and sequence analysis of fragments of the mitochondrial genes cytochrome oxidase I and II (COI and COII) of the aphids. P. atlantica trees did not show any differentiation or genetic structure among climatic regions. S. wertheimae aphids in Israel exhibited two distinct phylogenetic groups, one occupying the mesic region in the north and the other inhabiting the xeric south. The Jordanian aphids clustered within the Israeli northern populations. The results suggest that while the fragmented Irano-Turanian distribution in the Levant does not affect the genetic structure of P. atlantica trees, it promotes genetic differentiation among the aphids’ populations and may initiate an allopatric speciation.

Distinct antimicrobial activities in aphid galls on Pistacia atlantica

Gall-formers are parasitic organisms that manipulate plant traits for their own benefit. Galls have been shown to protect their inhabitants from natural enemies such as predators and parasitoids by various chemical and mechanical means. Much less attention, however, has been given to the possibility of defense against microbial pathogens in the humid and nutrient-rich gall environment. We found that the large, cauliflower-shaped, galls induced by the aphid Slavum wertheimae on buds of Pistacia atlantica trees express antibacterial and antifungal activities distinct from those found in leaves. Antibacterial activity was especially profound against Bacillus spp (a genus of many known insect pathogen) and against Pseudomonas aeruginosa (a known plant pathogen). Antifungal activity was also demonstrated against multiple filamentous fungi. Our results provide evidence for the protective antimicrobial role of galls. This remarkable antibacterial and antifungal activity in the galls of S. wertheimae may be of agricultural and pharmaceutical value.

Identification and Quantitative Determination of Lignans in Cedrus atlantica Resins using 13C NMR Spectroscopy

Identification and quantitative determination of individual components of resin collected on the trunk of 28 Cedrus atlantica trees, grown in Corsica, has been carried out using 13C NMR spectroscopy. Eight resin acids bearing either the pimarane or abietane skeleton, two monoterpene hydrocarbons and four oxygenated neutral diterpenes have been identified, as well as three lignans, scarcely found in resins. Three groups could be distinguished within the 28 resin samples. The nine samples of Group I had their composition dominated by diterpene acids (33.7-45.8%), with abietic acid (6.2-18.7%) and isopimaric acid (5.1-12.6%) being the major components. The four samples of Group II contained resin acids (main components) and lignans in moderate amounts (up to 10.3%). Conversely, lignans (38.8-63.8%) were by far the major components of the 15 samples of Group III. Depending on the sample, the major component was pinoresinol (18.1-38.9%), lariciresinol (17.2-33.7%) or lariciresinol 9'-acetate (16.9-29.1%). Finally, due to the high biological interest in lignans, a rapid procedure, based on 1H NMR spectroscopy, was developed for quantification of lignans in resins of C. atlantica.

Population ecology of Forda riccobonii (Hemiptera: Pemphigidae) on Pistacia atlantica

This paper discusses research on the population ecology and biology of the galling aphid Forda riccobonii [Stefani] on Pistacia atlantica Desf. trees in natural habitats in the northern region of Israel. 427 trees were searched for the presence of secondary galls produced by the second (F2) generation. This species occurred on only 29 trees in 7 of the 12 research sites. In the galled trees, a mean of only 22. 7 galls ± 6. 30 (SE) was located in 20 randomly selected branches. Of the 658 galls found, 65% populated the periphery of the crown, while the remaining ones were within. None were found higher than 4 meters above ground level, and they were dispersed evenly in each of the four cardinal directions. The distribution of the galls among the leaves on the galled shoots was not random: the aphids attacked the leaves that developed in the midseason (July) more than the others. Gall size varied greatly, depending on the number of chambers they comprised, from one to ten. Ahigh correlation was found between the number of chambers in the galls and the reproductive success of the F2, as measured by the number of winged aphids in autumn: a mean of 62 ± 2. 5 offspring (range: 47–81). Compared with other galling aphids in Pistacia, relatively few galls (19%) were occupied by predators, parasites, or inquilines. Of these, parasitoid wasps comprised more than 50%. Even so, the colonies in the parasitized galls succeeded in producing the same mean number of offspring as those living in intact galls. Observations indicate that F. riccobonii is less common in natural habitats than previously presumed. The specific morphology of its secondary galls, which consist of relatively closed chambers, seems to provide suitable protection from large enemies. Their relatively wide shape enables the production of a larger number of offspring compared with other galling aphid species that create two different galls in P. atlantica trees during their life cycle.

Sampling Bias in Roadsides: The Case of Galling Aphids on Pistacia Trees

Sampling along roadsides is convenient and is widely practiced in insect population researches. Ecological conditions in road verges are very different than those prevailing in natural habitats and they affect the annual growth of plants in semi-arid and arid regions. This in turn may improve development, survival and abundance of insects feeding on plants growing in roadsides. These trends may bias the results of sampling. To verify this assertion, we quantified the effects of growing in roadside on annual growth of Pistacia atlantica trees and Pistacia palaestina shrubs and compare two demographic indexes of nine gall-inducing aphid species on trees growing along roads with trees in the open landscape, in Israel. The annual growth of the two host plants was significantly more vigorous in roadsides than away from roads. Tests of Combined Probabilities showed that the likelihood of P. atlantica and P. palaestina to be parasitized by more galls of Fordini species is higher in roadsides than away from roads. Moreover, in the semi-dry regions of Israel, three aphid species on P. atlantica and five species on P. palaestina induced more galls in plants growing along roads than away from roads, while in the rainy Northern region, the difference was not significant between the two habitats. These results indicate a biased evaluation of population size in roadside habitat, which has to be accounted in insect–plant relation researches.

Gene flow among different taxonomic units: evidence from nuclear and cytoplasmic markers in Cedrus plantation forests.

Hybridization and introgression are important natural evolutionary processes that can be successfully investigated using molecular markers and open- and controlled-pollinated progeny. In this study, we collected open-pollinated seeds from Cedrus atlantica, Cedrus libani and C. libani x C. atlantica hybrids from three French-plantation forests. We also used pollen from C. libani and Cedrus brevifolia to pollinate C. atlantica trees. The progeny were analyzed using three different types of molecular markers: RAPDs, AFLPs and cpSSRs. Chloroplast DNA was found to be paternally inherited in Cedrus from the progeny of controlled-crosses. Heteroplasmy, although possible, could not be undoubtedly detected. There was no indication of strong reproductive isolating barriers among the three Mediterranean Cedrus taxa. Gene flow between C. atlantica and C. libani accounted for 67 to 81% of viable open-pollinated seedlings in two plantation forests. We propose that Mediterranean Cedrus taxa should be considered as units of a single collective species comprising two regional groups, North Africa and the Middle East. We recommend the use of cpSSRs for monitoring gene flow between taxa in plantation forests, especially in areas where garden specimens of one species are planted in the vicinity of selected seed-stands and gene-conservation reserves of another species.

Differential response of trees and shrubs to browsing and pruning: the effects on Pistacia growth and gall-inducing aphids

The effects of long term browsing on growth and morphology of P. atlantica trees and P. palaestina shrubs, and on the colonization of these hosts by their respective gall-inducing aphid guilds, were studied in natural vegetation pastures in Israel. To simulate apical dominance release by browsing, trees and shrubs were pruned and observed one year later. P. atlantica responded strongly to browsing, producing a crown of dense and sharp dry branches and thorn-like shoots, and pruning, compensating or overcompensating for the lost biomass in the studied morphological variables. Morphological responses of P. palaestina were less evident: we found no compensation in most variables. Three species of aphids produced more galls on browsed than on control shoots of P. atlantica. Two species induced more galls on pruned shoots. The five aphid species on P. palaestina colonized browsed and unbrowsed shoots equally, and produced fewer galls on pruned shoots. The role of apical dominance in architectural responses of trees and shrubs to browsing and pruning, as related to resource availability and timing, is discussed.

DEVELOPING OF MONOECIOUS PISTACHIO (P.VERA L.) POPULATIONS AND THE SEX DETERMINATION MECHANISM IN PISTACIA BY CROSSBREEDING

All species from the Pistacia genus are dioecious. This character negatively affects yield and quality of pistachios. Monoecious P. atlantica genotypes have been found in the Yunt mountains of the Manisa province of Turkey. The monoecious P. atlantica genotypes are divided into two groups: (1) one of the trees is fully monoecious i.e., all branches bear a mixture of male and female inflorescences and (2) two trees have several branches with only staminate flowers, while the rest of the branches bear pistillate inflorescences. This study aims to improve monoecious P. vera cvs and to determine the sex determination mechanism and inheritance in Pistacia by crossbreeding. The monoecious P. atlantica genotypes and two female P. vera cultivars ('Siirt' and 'Uzun') with a dioecious P. atlantica tree grown in the Yunt mountains were used as female genotypes. Monoecious P. atlantica genotypes and dioecious male P. vera and P. atlantica trees were used as pollinators. In total, twenty different inter- and intra-specific crosses were performed: four of them will be used to develop monoecious P. vera populations and the rest of them will help in understanding the sex inheritance and determination mechanism in Pistacia.

The effect of habitat and erosion on the distribution and development of Pistacia atlantica trees in the central Negev highlands of Israel

Pistacia atlantica trees have a very limited distribution in wadis in the central Negev highlands, and erosive processes may have a negative impact on the recruitment and survival of the trees. We measured the sizes of the trunks of adult trees, the condition of their canopies, fruit density, insect herbivory, and soil parameters--both in eroded and noneroded habitats. This was to determine the habitat soil quality and how it relates to the demographic disposition and vitality of these trees. The results revealed irregular size/age distribution and possible poor recruitment. There were no differences in fruit density between trees in eroded and noneroded habitats. However, analysis on gall density per branch revealed that Slavum wertheimae prefer host plants in relatively uneroded habitats. Analysis of water-holding capacity, soil organic carbon content, and pH revealed significant differences, with better soil quality existing in noneroded areas.

Evaluation of monoterpenic biogenic volatile organic compounds in ambient air around Eucalyptus globulus, Pinus halepensis and Cedrus atlantica trees growing in Algiers city area by chiral and achiral capillary gas chromatography

The monoterpenic biogenic volatile organic compounds (BVOCs) in ambient air around either Eucalyptus globulus, Cedrus atlantica and Pinus halepensis trees from El- Hamma Botanical Garden (Algiers) or from Pinus halepensis trees field located in Bab-Ezzouar (suburb of Algiers) was qualitatively and semi-quantitatively evaluated. The sampling was carried out in ambient air by adsorption through an activated charcoal cartridge followed by the carbon disulfide extraction. The solution was subjected to high-resolution gas chromatography (HRGC) analysis in programmed temperature. The identification of the components was established by the means of retention Kovàts indexes. The use of a β-cyclodextrin chiral capillary column allowed a good separation of monoterpenic enantiomers released in the atmosphere. The enantiomeric ratio provided a good insight into the enantiomeric compound preferentially emitted by plants.