Assessment of sexual vs asexual reproduction in Prosopis cineraria in the United Arab Emirates using seed pod observationsDavid J. Gallacher1 and Ali El-Keblawy2
1Assistant Professor, Zayed University, PO Box 19282, Dubai, United Arab Emirates. E-mail: [email protected]; 2Associate Professor, Plant Ecology, Department of Applied Biology, University of Sharjah, Sharjah, UAE, e-mail: [email protected]
Distribution of Prosopis cineraria in the United Arab Emirates (UAE) varies from open forests in gravelly wadi beds to tight clusters in low sand dunes. Observations of pod production were used to test the hypothesis that clustering was due to asexual reproduction, while open forests were derived sexually. Flowers are self-incompatible and insect pollinated, thus requiring pollination from a genetically different tree to produce fruit. Observations of pod distributions on 591 trees in open, clustered, and mixed forests could all be explained by the hypothesis. Findings indicate that large clusters containing hundreds of genetically identical trees are common, and that asexual reproduction is far more frequent in the region than is sexual. Conservation efforts should facilitate both forms of reproduction within the species’ natural range. Food sources for native wildlife, and for livestock, could both be enhanced by increasing the rate of outcrossing during pollination in clonal forests.
Ghaf (Prosopis cineraria) is the dominant tree species across most of the northern United Arab Emirates (UAE). It has an important place in the cultural heritage and ecology of the region (Lemons et al. 2003). Under natural conditions, tree distribution of P. cineraria has been observed to occur either as an open forest (Jongbloed et al. 2003), typically in gravelly areas such as wadi beds, or in distinct clusters of variable size (Aspinall 2001; Gallacher and Hill 2005), typically on dunes covering a gravel substrate. These two distribution modes often overlap geographically, thus presenting as an open forest that contains, or is dominated by, tighter clusters. Within Oman, ghaf forests are associated with underlying aquifers, in which clusters can also be observed (Brown 1988). However, clustering has not been reported elsewhere in the species’ natural habitat, suggesting that it may be a feature specific to the Arabian Peninsula population.
P. cineraria has become a preferred species in the extensive afforestation projects within Abu Dhabi emirate, and for shelterbelts and roadside plantations throughout the UAE. As a native species, it is perceived to use water more efficiently than non-natives, and its extensive root system is useful for stabilizing sand dunes. Artificial forests comprised of P. cineraria were found to contain enhanced floral diversity and an improved soil fertility, when compared to un-forested rangeland, and artificial forests of Acacia tortilis and Ziziphus spp. (Ksiksi et al. 2006), and of the exotic P. juliflora and Euclayptus spp. (El-Keblawy and Ksiksi 2005)through the determination of the effect of forest trees on species diversity and abundance of perennial plants in six forests. The impact of artificial forests on physical and chemical characters of the soil was also evaluated.\n\nThe results showed insignificant variation in species richness and species diversity index among the six studied forests. The effects of type and size of trees grown in the forest trees were significant on all the studied community attributes. All the attributes were
significantly greater inside than outside forests cultivated with the native Prosopis cineraria (L.. The role of P. cineraria within the natural Arabian peninsula ecology has been well described (Brown 1988).
P. cineraria reproduces both sexually and asexually under natural conditions (Brown 1992). A tight cluster in Oman was shown to be clonally derived, by methods of root excavation and isoenzyme analysis (Brown 1988). Commercial propagators have reported that the species suckers easily, though cuttings do not readily produce roots (Sandison and Harris 1991; Puri and Kumar 1995). Asexual reproduction occurs through root suckers. In low dunes, these can be frequently observed at and near the base of mature trees. The lead author has observed trees to produce a lateral root, 3-4 cm diameter and extending up to 19m from the base of the parent tree, harboring root sprouts. Sightings of living lateral roots were extremely rare, even on apparently shifting sands, but discarded lateral roots rise to the surface in a declining forest.
Pod production in the UAE is highly variable. Fecundity is affected by access to water, such that trees in urban settings typically produce perhaps hundreds times the number of pods observed in trees with less reliable water sources. Under natural conditions, forests have been observed to produce pods annually, but some isolated clusters have been reported to not produce pods over many seasons. One possible hypothesis is that fecundity is affected by tree density and, therefore, competition for water. Hence, the number of pods in a remote cluster would be relative to water availability, rather than to the number of trees.
Prosopis species are typically self-incompatible (Pasiecznik et al. 2004; Barrera and Smith 2009), leading to a second hypothesis that isolated tree clusters are asexual clonal colonies, derived from a single tree, and flowers therefore reject pollen from other flowers within the same tree cluster. Pollination occurs via insect vectors, though birds and bats may contribute (Brown 1992). Only a few flowers within each inflorescence can develop into pods due to space, but the other flowers may contribute to reproductive success by attracting pollinators (Koptur 1984) or by rejection of self-incompatible pollen. Pollinators are likely to move among trees within a cluster more frequently than they will move among trees of different clusters. Hence, the frequency of pod production within a tree cluster would be inversely related to the frequency of asexual reproduction among trees. From this hypothesis, a highly isolated cluster of trees would produce many pods if each tree of the cluster had grown from seedlings, and few to potentially no pods if they are clonally derived from one original seedling.
The aim of this study was to determine if observation of seed pod production could be used as a novel method of identifying mode of tree reproduction over a large scale. Some clusters contain many hundreds of trees, but asexual reproduction has been proven only within small clusters of 3-4 trees. If the hypothesis that pod production is related to localized genetic variation is correct, then it would provide an easy method of assessing the genetic base of a forest. Implications for both conservation and agroforestry management will be discussed.
Material and methods
Three locations were identified for this study, termed ‘cluster’, ‘open’, and ‘mixed’. The ‘cluster’ location contains four isolated clusters (Fig 1a) within the Dubai Desert Conservation Reserve.
Clusters 1 and 2 are proximal, their borders separated by 260 m, but the next closest cluster of the species is six kilometers away. They are comprised of 247 and 456 trees respectively. Cluster 3 contains fewer, larger trees, while cluster 4 contains just four trees which might be a natural cluster, or might be an anthropogenically derived group. Structure of all four clusters are described in Gallacher and Hill (2005). The ‘mixed’ location was chosen through satellite imagery (Google Earth) because it appears to contain many clusters within a broader, possibly open forest (Fig 1b). The ‘open’ location is a wadi bed (Falaj Al Mualla) that contains trees in a clearly non-clustering distribution. Both the ‘open’ and ‘mixed’ locations are within Umm Al Quwain Emirate, and are close to the center of the ghaf population within the UAE.
Trees at each location were observed on 3 May 2012 for presence/absence of flowers, and then on 26 June (clusters) and 2 July 2012 (mixed and open) for presence/absence of seed pods. For the latter, a transect line was followed through the forest, and each observed tree was GPS tagged. Trees with many pods were easily detected by sight and, with a little practice, even trees with just a handful of pods could be detected quite readily. It is possible that some trees with just one or a few pods were overlooked.
Flowering was observed to be ubiquitous. Fecundity varied substantially among trees within sites, and appeared to be correlated with quantity of leaf matter, though the relationship was not tested in this study. Trees with extremely minimal vegetation were still observed to produce flowers.
Pod production, however, was strongly related to tree distribution (Table 1), such that trees in open forest always produced pods, while trees in clusters usually did not. No pods were observed in Clusters 1-3, indicating that pollen was incompatible within each of these clusters. In a previous season, authors have observed a single pod growing on a single tree in Cluster 3. This is consistent with the prediction that flowers will usually be pollinated from the same or neighboring trees, but will, on rare occasions, be pollinated from distant trees. Since Clusters 1 and 2 are separated by only 260 meters, pollination between these clusters should be more frequent.
Table 1: Number of trees observed with one or more seed pods, among different classifications of tree distribution.
Category Location No. trees observed No. trees bearing seed pods
Observed trees with pods (%)
Cluster 1 N24.849 E55.700 43 0 0Cluster 2 N24.846 E55.704 62 0 0Cluster 3 N24.794 E55.611 23 0 0Cluster 4 N24.801 E55.623 4 3 75Mixed N25.360, E55.800 437 42 10Open N25.370, E55.850 22 22 100
The absence of any observed pods suggests not only that each cluster consists entirely of one clonal group of trees, but also that both clusters might be the same clonal group. Cluster 4 consists of just four trees, which might not be a natural cluster. Three of the trees produced pods that were unevenly distributed in clumps within the trees. Hence, by the hypothesis, at least one of these trees was genetically different from the others.
Figure 1a: Two of the four isolated Prosopis cineraria clusters observed, containing 247 (cluster 1) and 456 (cluster 2) trees (Gallacher and Hill 2005). All are located within the Dubai Desert Conservation Reserve, United Arab Emirates.
Figure 1b: Observation site for ‘Mixed’ Prosopis cineraria clusters within an open forest (N 25.360, E 55.800), and the ‘Open’ forest along a wadi bed (N 25.370, E 55.850). The town is Falaj Al Mualla in Umm Al Quwain emirate of the United Arab Emirates. Dark dots within the mixed group are mostly Prosopis cineraria, though some on the Eastern edge of the mixed group are Acacia tortilis.
Distribution of pods among trees in the ‘mixed’ forest indicates that the forest is comprised mostly of one clonal cluster, interspersed with smaller, genetically different clusters. Three different patterns of pod distribution were observed:
• A single pod was observed on three trees, each surrounded by many trees devoid of fruit (Fig 2a). This is consistent with the hypothesis that pollination from outside the cluster will occur, but only rarely.
• A single cluster of trees was observed in which approximately half the trees contained a large number of pods, some trees with no pods, and some trees of low fecundity (Fig 2b). This pattern suggests the presence of several genetically distinct individuals, some of which have also reproduced asexually.
• Five locations were observed with multiple pod-bearing trees, usually with a small number of pods but occasionally with many. This is explained by the presence of one genetically different tree or tree cluster. The distinct cluster in Fig 3 illustrates a cluster within the larger cluster. It has a diameter of 33 meters, and is 72 meters from its nearest neighbor. Three of its 19 trees contained a small number of pods, while the rest were barren; indicating that some outcrossing had occurred with neighboring clusters but that most pollination was incompatible.
Observed pod distributions in this study can be explained through floral self-incompatibility and asexual reproduction to produce clonal clusters. Sexual reproduction is dominant in open forests that do not exhibit clustering, but asexual reproduction is dominant in isolated clusters such as those of the Dubai Desert Conservation Reserve, in which a single genotype may produce hundreds of trees. The research indicates that asexual reproduction is far more common than previously supposed. It also indicates that the species switches almost completely from one mode of reproduction to the other, depending on the habitat. Forests in low dunes are characterized by clustering and a lack of pod production, while forests growing on a gravel substrate are pod-producing and distributed as open forest.
The authors postulate that P. cineraria seedlings only rarely, if ever, succeed to establish in a low dune habitat, and instead require a gravelly substrate. Conversely, the lateral roots that enable asexual reproduction occur only in sandy substrate, probably due to the mechanics of lateral growth in the looser medium. Hence, clusters 1-3 were each derived from a single seedling that succeeded to grow on inter-dune gravel substrate, but they then reproduced asexually to produce clonal clusters on sand substrate, containing hundreds of individual tree clones. In the mixed forest, many seedlings have become established on the sandy/gravel substrate (Fig 2, East) but only one or a few have spread asexually to become established in the low dunes to the West. Numerically, most of the eastern trees and all of the western trees have been produced asexually.
Concerns about natural population sustainability of ghaf in the Arabian peninsula have previously focused on minimal observed regeneration of the species (Brown 1992; Gallacher and Hill 2005; Abdel Bari et al. 2007). Low regeneration is usually attributed to heavy grazing, which impacts
Figure 2: Two patterns of pod distribution within the ‘Mixed’ group, showing trees that were observed with (yellow) and without (green) pods. Trees lying on the path between green circles were also observed to be without pods.
Figure 3: A single cluster of 19 trees (N25.348 E55.789) located within the ‘mixed’ forest. Three of the trees contained a small number of pods, while the other 16 contained no pods. Note that the darker is shadow on sand substrate, while the lighter is tree canopy.
perennial seedlings more than annuals (Gallacher and Hill 2008). This study’s inference of widespread asexual reproduction has both positive and negative consequences for this discussion. Negative, because of low genetic diversity, and positive, because afforestation is relatively easily managed.
Natural genetic diversity is much smaller than the number of individual trees would imply, by perhaps two to three magnitudes. Nevertheless, the natural population in the UAE, is large, and probably still contains thousands of unique genotypes. Genetic diversity is substantial in Rajasthan , India (Rawat et al. 2007; Sharma et al. 2011)fodder, food and\nmedicinal uses. Some remarkable features are observed\nin the form of phenotypic variation in various populations\ninhabiting different regions of the Indian desert.\nTo asses these variations male meiotic studies
were conducted\nin ten different accessions collected from four\nproviences of Rajasthan, India. Analysis of data on chromosome\nassociations, chiasma frequency and their distributions\npattern concluded that the somatic chromosome\nnumber of P. cineraria is 2n = 2x = 28. The complete\nabsence of accessory chromosomes (B, suggestive of a species that is adaptive to a variety of conditions. It is difficult to imagine that significant genetic erosion is occurring in natural populations, unless specific habitats that facilitate specific genotypes are being eroded.
A realistic discussion of genetic diversity in Arabia must necessarily include the extensive artificial plantations of the species in afforestation projects and roadside plantations, dating mainly from the 1970s and 1980s (Kiriiwa et al. 2002). Most trees were planted in regions outside the natural range of the species, but most, particularly roadside plantings, have been sustained through groundwater irrigation. The number of artificially placed P. cineraria trees in the UAE far exceeds the natural population. The authors of this paper do not know the genetic origin of these trees, but due to the prevalence of Indian companies willing to provide seed, there is a good chance many are from the Thar Desert region. This raises two questions; are Arabian populations genetically differentiated, and if so, are Arabian populations being genetically eroded?
The high frequency of asexual generation in the species is encouraging for rehabilitation, since a highly degraded area might recover rapidly with appropriate herbivore protection. Rapid recovery from rootstock has been reported in other species of the same habitat (Gallacher and Hill 2006)2006. There is some indication that, even in natural systems, regeneration of the species occurs in waves, triggered perhaps by a series of high rainfall seasons, or a chance reprieve from grazing pressure. Hence, it should be possible to regulate the rate of asexual forest regeneration by providing a physical barrier to grazing during favorable seasons.
Seed pods have significant commercial and ecological significance. They are a food source for a wide variety of native herbivores (Brown 1988), and immature pods have been routinely fed to livestock (Pasiecznik et al. 2004) and, historically, the indigenous Bedu (Jongbloed et al. 2003). Thus, there is commercial, and possibly ecological, value in raising the frequency of cross-pollination among trees, by interspersing genetically different trees among an asexual cluster.
Asexual reproduction in Prosopis cineraria in the UAE appears to be very common in sandy substrate, and ubiquitous in low dunes, producing tight clusters ranging from two, to hundreds of individual trees. In contrast, sexual reproduction is ubiquitous on gravel substrates, where clusters are not observed. Asexual clustering distribution on this scale might be limited to the Arabian Peninsula, though available literature is insufficient on this issue. Conservation efforts should account for both forms of reproduction. Agroforestry could be enhanced through artificial cross-fertilization within asexual clusters to promote pod production.
Acknowledgments: The authors would like to thank the National Research Foundation of the United Arab Emirates for supporting this research, Zayed University for providing seed funding, and the Dubai Desert Conservation Reserve for continued in-kind support.
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