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Ecological Impacts and Phenotypic Plasticity of a Global Invasive Cactus, Opuntia ficus-indica
(2023)
Biological invasions by non-native species pose one of the major threats to biodiversity, the way ecosystems function, and the well-being of humans. These invasions can occur through various means, including accidental or intentional introductions by humans, natural dispersal, and climate change. Non-native species can harm the native species and ecosystems, by homogenizing plant communities, competing for resources, changing how the ecosystem operates, and eventually causing native species to go extinct. Even though not all non-native species become invasive, changes in climate and ecosystems can cause the successful establishment and spread of non-native species. Despite the advancements in our understanding of biological invasions in recent years, research has been biased towards temperate regions, whereas arid and semi-arid regions that are highly impacted by climate change are underrepresented. Thus, particularly focusing on the impacts of biological invasions in subtropical arid and semi-arid regions, the goal of this PhD project was to explore the effects of an invasive cactus on the local native communities and investigate the mechanisms of its successful invasion. Certain species are found to take advantage of the ever-drying climates in the arid/ semi-arid regions of the world. Opuntia ficus-indica, native to Mexico, is an exceptionally successful drought-tolerant invasive cactus that successfully grows in these regions. O. ficus-indica, a most widespread invasive cactus, is considered an ecosystem engineer as it modifies the habitats of indigenous plant species and dependent animals. This project aimed to identify the ecological impacts of O. ficus-indica in the highlands of Eritrea, the competitive potential of O. ficus-indica and the plastic changes that enabled its spread and invasion (Chapters I-III). For this purpose, field observations and common garden experiments were carried out throughout the project.
We investigated the effects of Opuntia ficus-indica on the spatial diversity of native plant communities (Chapter I), its competitive ability against native species (Chapter II) and the phenotypic plasticity of O. ficus-indica (Chapter III). To investigate the main ecological effects of O. ficus-indica on the native community, field data was collected from the highlands of Eritrea and comparisons were made between O. ficus-indica invaded and noninvaded areas (Chapter I). The study aimed to understand the effects of O. ficus-indica by examining species composition, richness, and diversity across vegetation layers and revealed that O. ficus-indica homogenises the species composition of the native ecosystem. This provides evidence that the presence of O. ficus-indica reduces landscape-level heterogeneity or spatial diversity. However, O. ficus-indica did not influence the species richness and diversity of the local communities. The mechanisms of the successful homogenisation of the local communities by O. ficus-indica were attributed to the potential competitive abilities of O. ficus-indica against the native species, and the plastic and adaptive traits it developed in the non-native ranges. The first assumption was tested by setting up a common garden competition experiment between two native Eritrean species, Ricinus communis and Solanum marginatum (Chapter II). The experiment used two water availability treatments, wet and dry, and categorized plants into intraspecific (native or invasive only) and interspecific (native and invasive) competition. The study evaluated the impacts by comparing the growth of O. ficus-indica alone to the growth alongside native species which revealed the weak competitive potential of O. ficus-indica. However, O. ficus-indica was observed to outgrow the native species in several folds which can be attributed to its successful invasion. The second assumption of the successful spread of O. ficus-indica was attributed to the phenotypic plastic traits adapted by O. ficus-indica in the non-native ranges (Chapter III). The phenotypic plasticity of O. ficus-indica was assessed by exposing it to water stress across dry and wet environments. The species were cultivated from a diverse set of 12 populations, encompassing its native range in Mexico with three cultivars and nonnative ranges in Africa (Algeria, Eritrea, Ethiopia), the island of Madeira off the coast of Africa, and in Europe, Italy with two cultivars and in Portugal from three sites. In Mexico and Italy, we collected various cultivars to ensure a wide representation of genotypes. We found that the species originating from the native range of O. ficus-indica exhibited lower plasticity to conditions of elevated water availability. Furthermore, a trial gradient experiment on O. ficus-indica was conducted to determine the appropriate watering levels for the species and the experiment revealed not only the species' capacity to endure a lack of water for nine months but also its ability to withstand prolonged waterlogged conditions.
This thesis illustrates the fact that invasive species are a major threat to biodiversity and ecosystem functioning worldwide, especially in rarely studied regions with dry climates and limited resources. How can invasive plants spread and cause negative impacts on native ecosystems (Chapter I), despite their weak competitive abilities (Chapter II)? This thesis explored these questions by examining the case of O. ficus-indica, an invasive species in arid/ semi-arid climates (Chapter I). It showed that O. ficus-indica has a high growth potential that allows it to overcome resource limitations, that its growth is not affected by competition from native species (Chapter II), and that it exhibits adaptive plasticity that enhances its invasion success in different environments (Chapter III). This thesis revealed the complex mechanisms and consequences of biological invasions in dry climates and contributes to the understanding of invasive species. It also suggests that more research is needed in understudied regions to assess the impacts of O. ficus-indica or invasive species in general on native biodiversity and ecosystem services and to identify the factors that influence the competitive and adaptive potentials.
Dendrochronology, the science of tree-rings is a tool which has been widely used for many years for understanding changes in the environment, as trees react to environmental changes over time. In the contemporary situation, where climate warming in the Arctic is unequivocal and its effects on the Alpine and tundra ecosystems are seen pronouncedly in the past decade, the role of dendro-studies and the use of trees and shrubs alike as proxies of change has become critical. Studies clearly indicate that warming in the Arctic and Alpine tundra has resulted in increased vegetation in recent years. Shrubs, in these sensitive ecosystems, have proven to be highly instrumental as they likely benefit from this warming and hence are good indicators and auditees of this change. Therefore, in this study, we investigate the potential of shrubs in the evolving field of dendro-ecology/climatology.
Studies from classical dendrochronology used annual rings from trees. Further, because of shrub sensitivity to contemporary change, shrub-based dendrochronological research has increased at a notable scale in the last decade and will likely continue. This is because shrubs grow even beyond the tree line and promise environmental records from areas where tree growth is very limited or absent. However, a common limitation noted by most shrub studies is the very hard cross-dating due to asynchronous growth patterns. This limitation poses a major hurdle in shrub-based dendrochronological studies, as it renders weak detection of common signals in growth patterns in population stands. This common signal is traced by using a ‘site-chronology’.
In this dissertation, I studied shrub growth through various resolutions, starting from understanding radial growth within individuals along the length of the stem, to comparison of radial growth responses among male and female shrubs, to comparing growth responses among trees and shrubs to investigation of biome-wide functional trait responses to current warming. Apart from Chapter 4 and Chapter 6, I largely used Juniperus communis sp. for investigations as it is the most widely distributed woody dioecious species often used in dendro-ecological investigations in the Northern Hemisphere.
Primarily, we investigated radial growth patterns within shrubs to better understand growth within individuals by comparing different stem-disks from different stem heights within individuals. We found significant differences in radial growth from different stem-disks with respect to stem heights from same individuals. Furthermore, we found that these differences depending on the choice of the stem-disk affect the resulting site-chronology and hence climate-sensitivity to a substantial extent and that the choice of a stem-disk is a crucial precursor which affects climate-growth relationships.
Secondly, we investigated if gender difference – often reported causing differential radial growth in dioecious trees – is an influential factor for heterogeneous growth. We found that at least in case of Juniperus communis. L and Juniperus communis ssp nana. WILLD there is no substantial gender biased difference in radial growth which might affect the site-chronology. We did find moderate differences between sexes in an overall analysis and attribute this to reproductive effort in females.
In our study to test the potential of shrubs for reconstruction, we used a test case of Alnus viridis ssp crispa. We found a strong correlation between ring-width indices and summer temperature. Initially, the model failed the stability tests when we tested the stability of this relation using a response function model. However, using wood-anatomical analysis we discovered that this was because of abnormal cell-wall formation resulting in very thin rings in the year 2004. Pointer year analysis revealed that the thin rings were caused because of a moth larval outbreak and when corrected for these rings the model passed all stability tests.
Furthermore, to see if trees and shrubs growing in same biomes react to environmental changes similarly, a network analysis with sites ranging from the Mediterranean biome to the Ural Mountains in Russia was carried out. We found that shrubs react better to the current climate warming and have a decoupled divergent temperature response as compared to coexisting trees. This outcome reiterated the importance of shrub studies in relation to contemporary climate change. Even though trees and shrubs are woody forms producing annual rings, they have very different growth patterns and need different methods for analysis and data treatment.
Finally, in a domain-wide network analysis from plant-community vegetation survey, we investigated functional relationships between plant traits (leaf area, plant height, leaf nitrogen content, specific leaf area (SLA), and leaf dry matter content (LDMC)) and abiotic factors viz. temperature and soil moisture. We found a strong relation between summer temperature and community height, SLA and LDMC on a spatial scale. Contrarily, the temporal-analysis revealed SLA and LDMC lagged and did not respond to temperature over the last decade. We realized that there are complex interactions between intra-specific and inter-specific plant traits which differ spatially and temporally impacting Arctic ecosystems in terms of carbon turn over, surface albedo, water balance and heat-energy fluxes. We found that ecosystem functions in the Arctic are closely linked with plant height and will be indicative of warming in the short term future becoming key factors in modelling ecosystem projections.