Effects of herbivore-induced disturbances on above- and belowground community heterogeneity within a semi-arid sodic African savanna

Abstract

Large mammalian herbivores (LMH) function as significant drivers of change within consumer-controlled grassy biomes, essentially maintaining Africa’s open ecosystems through numerous top-down and bottom-up feedbacks. These feedbacks fundamentally drive and maintain invaluable ecological processes and cycles, subsequently regulating system structure and functioning. Yet, heterogeneous savanna ecosystems are faced with anthropogenic-induced changes to native LMH communities with which these systems evolved. The most common change to herbivore communities includes the switch towards single-species pastoralism at the expense of a diverse suite of wild African herbivores. Such dramatic changes in native herbivore communities might affect several underlying structural and functional constituents of these herbivore-adapted systems through top-down trophic cascades. Numerous studies have reported on the compartmentalised effects of native LMH on vegetation structure and edaphic properties. Given the link between these structural constituents and associated soil microbes (bacteria and fungi), herbivory is potentially a major driver of belowground microbial community structure and activity, and subsequently, soil function. However, little is known about the long-term impact of herbivory, and particularly the loss thereof, on bacterial and fungal community composition and potential implications for microbially-mediated decomposition. Considering the close association between herbivory and preferentially foraged sodic vegetation, sodic patches are suggested to exhibit changes related to altered herbivory intensity over short time scales. The Nkuhlu research exclosures within the Kruger National Park (KNP), South Africa, provided an ideal setting to explore spatial and temporal heterogeneity patterns within intensively utilised herbivore-driven sodic patches, and how these patterns are affected by changes in native herbivore communities. This study was specifically designed to elucidate the effects of herbivory, or the loss thereof from a herbivore-adapted system, on belowground microbial community structure and associated soil-based decomposition of detrital plant material, and how these potential belowground changes are related to observed changes in vegetation structure and edaphic properties. Sampling was conducted within five sites, each comprising five experimental plots, located across three herbivore treatments of varying intensity within the Nkuhlu exclosures. Successful retrieval of tea bags after the application of the extended, site-specific version of the Tea Bag Index (TBI) highlighted the value of this approach to quantify decomposition in a disturbance-driven savanna ecosystem. Results revealed that decomposition rate (k) was

highest in the presence of all LMH, irrespective of incubation time (3-, 6-, 9- and 12-months) with significant variation occurring after a six- and nine-month period. Conversely, stabilisation factor (S) was highest under complete herbivore exclusion across all four incubation periods with significantly higher values attained after the three- and six-month periods. Global comparison of TBI-based decomposition data revealed substantial differences between varying sites, illustrating the importance of an improved understanding of the complex functioning of semi-arid African savannas and how natural disturbances, such as herbivory play a valuable role in maintaining ecological processes, including carbon cycling. Next- Generation Sequencing (NGS) of soil-based genomic material for combined dry and wet seasons revealed a positive association between bacterial α-diversity and herbivore-induced disturbances, with the highest values obtained in the presence of all LMH. Conversely, fungal richness was highest in the sites from which herbivores were excluded for ~18 years, whereas diversity was highest under intermediate levels of herbivore disturbances. With seasonality as an added variable, substantial variation in both bacterial and fungal α-diversity indices were revealed, including significantly higher fungal richness and diversity under complete herbivore exclusion for the dry season. Moreover, heat tree analysis revealed significant changes in relative abundance of both bacterial and fungal taxa across the three herbivore treatments. Local scale vegetation sampling consisted of herbaceous biomass and species composition in an attempt to link observed changes in microbial community composition and soil function with changes in vegetation structure. Linking aboveground and belowground results revealed that herbaceous- and bacterial α-diversity measures together with decomposition rate (k) were positively associated with herbivore-induced disturbances. Conversely, herbaceous biomass, fungal α-diversity measures and stabilisation factor (S) had a positive association with herbivore exclusion. In the face of increasing land-use change and subsequent disturbance to carbon cycling, this study emphasises the importance of effectively managing heterogeneous savanna herbivore communities as a major determinant of system heterogeneity (above- and belowground) and associated nutrient cycling. This study could potentially be used as a framework to advance holistic ecological research and to develop bottom-up management strategies, at least for sodic patches within the KNP.