Functional ecology of encroachers in African savannas with a focus on N₂-fixation

Abstract

Savanna ecosystems across Africa are undergoing rapid changes in vegetation structure, characterised by the increased number and density of native woody plants, termed encroachment. Encroachment leads to the hyper-dominance of woody species, and negatively impacts biodiversity, ecosystem functioning and poses significant challenges for management and conservation. Despite the extent and severity of encroachment across Africa, the exact number and identity of encroaching species remains unclear.

Previous research has focussed on the drivers and impacts of encroachment, and not on the ecology of encroacher species. The understanding of the macroecology, nitrogen (N) dynamics and rhizobial mutualisms of encroacher species is limited. My thesis aims to address these knowledge gaps by quantifying the environmental niche, geographic range size and functional traits of encroacher species in Africa, along with the N-dynamics of Senegalia and Vachellia species in response to environmental drivers, and the diversity of rhizobial associations of N₂-fixing Vachellia species. This research will particularly focus on the implications for understanding encroachment in African savannas.

Chapter 1 summarises the literature on savanna ecosystems, focusing on their global distribution and the woody composition of African savannas to emphasise the pivotal role of the Fabaceae family (commonly known as legumes) within these ecosystems. Further, the review examines the role and dynamics of N₂-fixation in savanna ecology and how N₂-fixation can be measured, with a view to discussing how these proxies can give new insights to understanding encroachment. By synthesising the empirical evidence and theoretical frameworks, Chapter 1 sets the scene to introduce the thesis aims examining the ecology and functional traits of species responsible for encroachment.

Chapter 2 synthesises data on the six genera: Dichrostachys, Prosopis, Senegalia, Vachellia (from the Fabaceae family), Combretum and Terminalia (from the Combretaceae family). Species from these genera are the dominant woody components of many savanna ecosystems in Africa and contain the species driving encroachment. Of the 1,045 species comprising these genera, 416 can be defined as open ecosystem species, and of these, 15% can be classified as encroachers. Parallels can be drawn between plant invasion and encroachment, informed by this comparison, I analysed the environmental niche, range size, and functional traits of open ecosystem species to determine whether encroachers share environmental characteristics and functional traits.

Of the 63 species that can be classified as encroachers, these species are unified by a broad climatic niche, large geographic range size, tall stature, spinescence, a flexible plant habit and within the Fabaceae, the ability to fix N₂. These results mirror findings in invasion ecology to support the niche breadth hypothesis. I suggest encroachment is driven by species that have evolved broad environmental tolerances supporting extensive geographic ranges that are facilitated by plasticity in ecologically important functional traits such as habit enabling responsiveness to a rapidly changing environment.

Via a two-year glasshouse experiment, Chapter 3 examines the N-dynamics of 12 species of Vachellia and Senegalia. Encroachment is driven by increases in atmospheric CO₂ and climate change, however, there remains a limited understanding of how these shifts affect the ecology of woody plants. Six encroacher species and six non-encroacher species were grown under a combination of elevated CO₂ levels and drought conditions to compare the N-dynamics of encroachers and non-encroachers. The 232 plants were grown in an open-top chamber CO₂ facility in South Africa in combinations of elevated versus ambient CO₂ and wet versus dry soils with four proxies of plant N-dynamics quantified in these 12 species. I found that encroacher species consistently had higher nodule biomass in wet soils and at elevated CO₂.

Crucially, leaf δ¹⁵N values varied between encroacher and non-encroacher species, indicating a reliance on N₂-fixation for photosynthesis, suggesting capacity for a rapid response to changing environments. Despite this, both groups exhibited comparable long-term strategies for N allocation across varying environmental conditions, which implies similar underlying mechanisms. Understanding common life-history traits among encroacher species provides valuable insights into ecosystem functioning and facilitates the prediction of responses from both encroacher and non-encroacher species to accelerating environmental change.

Moving to the microbial scale, Chapter 4 examines plant-rhizobia symbioses to determine interspecific variation in rhizobial symbionts to consider implications for encroachment dynamics. The legume-rhizobia relationship varies from specific, with hosts associating with a select number of rhizobia species, to promiscuous where hosts associate with a large diversity of rhizobia species. A diverse relationship with rhizobia provides several benefits for host legumes that increases plant ecological fitness, including increased availability in symbiotic rhizobial partners for N₂-fixation. The protocol developed in this Chapter for isolating rhizobia from wild-growing plants represents a pioneering effort in identifying rhizobial symbionts of woody plants outside of a controlled, sterile environment. Using nodules from two encroacher species (Vachellia karroo and V. sieberiana) and one non-encroacher species (V. robusta) grown in savanna soils as part of the Chapter 3 experiment, I analysed 425 nodules, sequencing over 457 isolates during protocol development to successfully identify 33 rhizobia species. In the three species examined, there was a correlation between encroacher status and symbiotic promiscuity. Comparing the symbiotic dynamics of encroachers and non-encroachers and their associated rhizobia offers insight into only a small number of N₂-fixers are driving encroachment.

Chapter 5 synthesises my key findings from the macroecological, individual plant and microbial scales to present a conceptual framework integrating research across scales to understand how plant traits related to plant growth and performance underpin a life history strategy rapidly responsive to environmental change. In savanna ecosystems, atmospheric CO₂ concentrations, drought, fire, and herbivory events act as growth constraints and where global change can diminish these growth constraints enabling asymmetric changes in the savanna plant population dynamics. I propose that woody species capable of exploiting global change-driven encroachment capitalise on responsive traits and symbiotic associations to increase their number and density in savannas. This, in turn, alters savanna structure, composition, and ecosystem functioning.