Drought tolerant forb flora of a semi-arid protected savanna in the Lowveld of South Africa

Van Coller, H., Klem, J. & Siebert, F., 2021, ‘Drought tolerant forb flora of a semi-arid protected savanna in the Lowveld of South Africa’, Bothalia 51(1), a10. http://dx.doi. org/10.38201/btha.abc.v51. i1.10 Background: Increased frequency and intensity of droughts related to climate change are predicted to induce pressure on herbaceous communities. Considering that forbs contribute significantly to savanna ecosystem resilience, we investigated forb communities of a protected semi-arid savanna during an extensive drought.


Introduction
Predicted increasing drought intensity and frequency, combined with higher average temperatures due to global climate change, are threatening biodiversity, and therefore the stability, functioning and sustainability of terrestrial ecosystems (Barros et al. 2018). Drought is a common phenomenon in semi-arid rangelands (Vetter 2009) and has been shown to cause rapid and lasting effects on vegetation dynamics and ultimately ecosystem function and services (Barros et al. 2018;Ploughe et al. 2019).
Depending on intensity, droughts can cause shifts in plant species assemblages, leading to the establishment of different plant communities (Junk et al. 2018). In herbaceous layers of semi-arid savannas, these communities are composed mainly of annual grasses and both annual and perennial forbs (O'Connor 1998;Buitenwerf et al. 2011). In the savanna context, the term 'forb' is used to classify anything other than trees, shrubs and grasses, which has led to a poor functional definition of this life form. For the purpose of this study, we will define forbs as non-graminoid vascular plants with limited woody tissue and with perennating buds at or below soil surface. Drought episodes tend to favour forbs, since they possess a variety of drought-tolerant traits such as underground storage organs ) associated with persistent bud banks and viable seed banks (Siebert & Dreber 2019). Despite being associated with savanna land degradation and therefore perceived as being an undesirable functional group by land managers (Fynn & O'Connor 2000;Tessema et al. 2011), forbs are important through providing ecosystem functions (i.e. forage stability) during stressed conditions, and functional redundancy to absorb disturbances such as sustained grazing and droughts (Van Coller et al. 2018).
Forbs are an important source of nutritious forage and may constitute an important part of ungulate diets at certain times of the year (Du Toit 2003;Van Der Merwe & Marshal 2012). Moreover, forbs contribute significantly to the biodiversity of savanna and grassland systems (Buitenwerf et al. 2011;Siebert & Scogings 2015), which are functionally diverse, suggesting a stronger resilience to different environmental conditions (Turner & Knapp 1996;Van Coller et al. 2018). Forb ecology research in dry African savannas generally report on forb responses at the level of functional group rather than species level. Furthermore, variations in forb functional traits defining plant strategies for regeneration and survival in adaptation to climate extremes such as droughts, remain understudied (Siebert & Dreber 2019).
Below-average rainfall in the Central Lowveld of South Africa was recorded for two consecutive years (2015 and 2016) (Swemmer et al. 2018). Using data collected during this time, we sought to identify specific drought tolerant forb species and their respective functional traits in a semi-arid African savanna. In doing so, we aimed to enhance knowledge of the attributes that allow these forb species to persist during droughts and potential functions that they fulfil under such environmental conditions.

Materials and Methods
Forb communities were studied in the semi-arid savanna of the greater Kruger National Park (KNP). Protected areas are not exempt from natural disasters, such as drought. They therefore provide valuable natural experimental settings where spatial heterogeneity and ecological responses function under natural drivers (Pickett et al. 2003 Field surveys were undertaken at two sites of similar geology (i.e. granite and gneiss), but different soil nutrient statuses (i.e. nutrient-rich sodic soil versus nutrient-poor sandy soil). Floristic and functional trait data were collected from 48 plots of 1 m 2 (18 plots within the nutrient-rich site and 30 plots within the nutrient-poor site) during the usual rainy season (November-March) of the extensive drought of 2015/2016. In the KNP (i.e. nutrient-rich site), total annual rainfall was 200 mm below the mean annual rainfall for the area (Van Coller et al. 2018), while at the nutrient-poor site in Timbavati Private Nature Reserve (TPNR) it was ~330 mm below the long-term average (Kaschula et al. 2005). Within each plot, forbs were identified up to species level and all individuals counted. Frequency per species was calculated with respect to all recorded species in each respective site. Frequency is considered a stable variable for the abundance of an individual species (O'Connor 2015). Frequency measures (%) were used to identify forb species most commonly observed in the study sites. Only forb species with a frequency ≥ 1 are discussed. Functional traits were assigned to forb species (Cornelissen et al. 2003;Germishuizen & Meyer 2003) based on the potential contribution to the functioning of semi-arid protected areas (i.e. palatability, life history and nitrogen-fixing ability), as well as the ability to tolerate conditions related to drought and herbivory (growth form, life history, resprouting capacity and succulence).

Results and Discussion
Herbaceous productivity is strongly affected by rainfall, and generally reveals marked deterioration in response to drought conditions ( Figure 1) (Fynn & O'Connor 2000;O'Connor 2015). Despite this, frequency measures revealed a total of 31 forb species among the two study sites. A mean number of six and four forb species was recorded per plot (1 m 2 ) in the nutrient-rich and nutrient-poor sites respectively. The number of forb species per plot recorded in the nutrient-rich site ranged from one to 17, while a lower range (0-7) of forb species were recorded for plots in the nutrient-poor site.
Plant families that comprised most of the frequent taxa during the drought included Acanthaceae and Amaranthaceae in the nutrient-rich site, and Fabaceae and Boraginaceae in the nutrient-poor site ( Table  1). Prevalence of the Fabaceae is in accordance with Wagner et al. (2016) who reported that nitrogen-fixing herbaceous legumes from the Fabaceae may increase in abundance after disturbances in dry savanna rangelands, and also in disturbed grasslands (Muller et al. 2021). Nitrogen-fixing ability is a trait generally associated with ecosystems with low nutrient availability (Cornelissen et al. 2003), explaining the high frequency of Chamaecrista mimosoides (L.) Greene in the nutrient-poor site (Table 1). Over 50% of the most frequent forbs were annuals (  (Siebert & Scogings 2015), whilst the prostrate-growing annual Gisekia africana (Lour.) Kuntze revealed the highest frequency in the nutrient-poor site ( Table 1). Persistence of these species is therefore likely attributed to the positioning of perennating tissue at or close to the soil surface, since fewer species could have buds far above the soil surface during harsher climatic conditions such as drought (Cornelissen et al. 2003). Moreover, erect growing plant species with their perennating buds situated above the soil surface are especially susceptible to trampling, heavy grazing and exposure to extreme heat conditions, whereas prostrate-growing species are avoidant by retaining buds and leaf material close to the soil surface (Cornelissen et al. 2003). A prostrate growth form in forbs could therefore be considered an important resistance trait against drought and grazing in the protected Lowveld savannas of South Africa.
The presence of annual forb species with a pioneer character in seed banks (Tessema et al. 2016) allows for their initial colonisation of bare soil (Siebert & Dreber 2019). Therefore, some of the most frequently observed forb species during the drought (i.e. Portulaca kermesina N.E.Br. and P. hereroensis Schinz in the nutrient-rich site, and G. africana in the nutrient-poor site) were annuals (Table 1). Moreover, these species exhibited traits generally associated with grazing-and drought-tolerance (i.e. prostrate growth form and succulence) (Cornelissen et al. 2003). Although little is known about succulence as a drought-tolerant trait in forbs, the ability of these species to retain water in their leaves and stems during dry conditions, together with a prostrate growth form to avoid and tolerate herbivory, possibly favoured their survival when subjected to herbivore utilisation in dry, hot conditions. Annual forbs exhibiting this combination of traits therefore make up an important component of the forb flora of semi-arid protected areas, especially during a drought.
The majority of drought-tolerant perennial forbs in this study had the ability to resprout, either through buds located at or near the soil surface, or belowground. Such a disturbance-tolerant trait is well-known for trees and shrubs, but our understanding of regeneration from buds in forbs is unknown and requires further investigation (Siebert & Dreber 2019).
Over half of the frequent forb species recorded during the drought were palatable (

Conclusion
Despite anticipated deterioration of the herbaceous layer during droughts, forbs have the ability to withstand such disturbances through species-specific adaptions. Numerous forb species were able to persist amidst the abnormal hot and dry conditions, while providing the ecosystem with important functions and services, such as forage stability. Plant strategies for survival and regeneration during drought conditions are species-and family specific, which may vary across ecosystem types. Furthermore, drought-adaptations were also specific for life history groups, as annuals displayed strategies to survive after emergence (e.g. succulence and prostrate growth form), whilst the majority of perennial forbs had the ability to resprout from a persistent bud bank. As protected areas aim to conserve biodiversity, provide forage security for wildlife and to maintain ecosystem resilience, this study demonstrates that forbs contribute to these at plant taxonomic and functional trait levels.

Authors' contributions
HvC (North-West University) collected vegetation data from the Nkuhlu exclosures at the Kruger National Park (KNP), analyzed and reported data and wrote the manuscript, whilst JK (North-West University) collected data from Timbavati Private Nature Reserve (TPNR). FS (North-West University) was the project leader, promoter and supervisor to HvC and JK respectively, and was responsible for project design, data collection, reporting and the writing of the manuscript.

Disclaimer
The authors declare that the work presented, and views expressed in this submitted article is their own and is not an official position of the institution or funder. The authors furthermore declare that they have no financial or personal relationships that may have inappropriately influenced them in writing this article.

Source(s) of support
South African National Parks, National Research Foundation, North-West University.