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Browsing intensity of herbaceous forbs across a semi-arid savanna catenal sequence
South African Journal of Botany 100 (2015) 69–74
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Browsing intensity of herbaceous forbs across a semi-arid savanna catenal sequence F. Siebert a,⁎, P. Scogings b a b
Unit for Environmental Sciences and Management, North-West University, Private Bag X6001, Potchefstroom, 2520, South Africa School of Life Sciences, University of KwaZulu-Natal, Private Bag X54001, Durban 4000, South Africa
a r t i c l e
i n f o
Article history: Received 20 March 2015 Received in revised form 5 May 2015 Accepted 7 May 2015 Available online xxxx Edited by RM Cowling Keywords: Kruger National Park Grazing lawn Exclosure Species richness Mesobrowser Herbaceous Herbivore diet
a b s t r a c t Ecological models to explain savanna heterogeneity and functioning weakly represent herbaceous forbs, which inevitably created knowledge gaps regarding the diversity and ecology of forbs. Forbs constitute over 70% of semi-arid savanna species richness. The aim of this study was therefore to (i) identify forb species that potentially form part of herbivore diet, and (ii) determine forb browsing intensity across a granitic savanna catenal sequence. Localized contrasts between nutrient-poor dystrophic uplands and nutrient-rich eutrophic bottomlands led us to predict that bottomlands would host forb assemblages dominated by browsed species. Forbs contributed to 78% of the total herbaceous layer species richness, of which 43% were browsed at varying intensities along the catenal sequence. Each topographic zone hosted a unique assemblage of browsed forbs, although browsing intensity was highest in the sodic bottomlands. Some browsed forbs formed prostrate, stoloniferous covers on the bottomlands, creating a lawn type dominated by forbs. Results presented here are the first to identify browsed forb species and to illustrate the turnover in browsing intensity of forbs across a semi-arid savanna catenal sequence. Our results add weight to the need to include herbaceous forbs in savanna management models to better understand savanna resource ecology and heterogeneity. © 2015 SAAB. Published by Elsevier B.V. All rights reserved.
1. Introduction African savannas are characterized by heterogeneous landscape types that provide a template upon which structural diversity and resource availability are shaped (Pickett et al., 2003). The general association of savanna types with soil fertility led to the concept of moist, nutrient-poor (i.e. dystrophic) savannas on highly leached, sandy soil versus arid, nutrient-rich (i.e. eutrophic) savannas on clayey substrates (Huntley, 1982). In arid and semi-arid savannas (b650 mm rainfall per annum), nutrient distribution can however be patchy. For instance, in a granitic savanna catenal sequence, there is a discernible turnover in nutrients and vegetation structure from uplands to bottomlands (Scholes, 1990), where uplands are associated with a nutrient-poor, broad-leaved savanna type (i.e. equivalent to dystrophic) and the clay-rich bottomlands with a nutrient-rich, fine-leaved savanna type (i.e. equivalent to eutrophic). This form of heterogeneity is however not attributed to abiotic variance in the landscape only, but is enhanced by the top-down effects of herbivory and fire, particularly so for the southern African savannas (Sankaran et al., 2005; Jacobs and Naiman, 2008; Smit et al., 2012). Despite of its variability, a defining feature of savannas is a continuous herbaceous layer and a discontinuous stratum of trees and shrubs within the same landscape (Knoop and Walker, 1985). ⁎ Corresponding author. Tel.: +27 182992374. E-mail address: [email protected] (F. Siebert).
http://dx.doi.org/10.1016/j.sajb.2015.05.007 0254-6299/© 2015 SAAB. Published by Elsevier B.V. All rights reserved.
Understanding this ecologically important coexistence of trees and grasses is extremely valuable, particularly for savanna ecosystem management (O’Connor et al., 2014). During the past two decades, savanna management has shifted its focus from causes of ecosystem change, habitat homogeneity, equilibrium and carrying capacity to responses to change, heterogeneity, dynamic equilibrium and ecosystem redundancy perspectives (Rogers, 2003; Grant et al., 2011). The understanding and application of these concepts to the herbaceous layer are however, largely based upon findings from rangeland science, a discipline driven by agriculture (i.e. herbivore productivity) rather than conservation in southern Africa (Tainton, 1999). For this reason, savanna management models exclusively used grass species, particularly due to their significant contribution to total standing biomass and their important role in forage for both ruminant and non-ruminant savanna grazers (Treydte et al., 2013). Herbaceous dicotyledonous species, non-graminoid monocots and geophytes (collectively termed ‘forbs’ hereafter) have been ignored or merely lumped into a ‘non-grassy, Increaser II’ category in management models (Scott-Shaw and Morris, 2014), although they constitute the largest component of herbaceous species richness in grasslands (Pokorny et al., 2004; Bond and Parr, 2010; Koerner et al., 2014; Scott-Shaw and Morris, 2014), temperate deciduous forests (Axmanová et al., 2012) and savanna ecosystems (Shackleton, 2000; Uys, 2006; Jacobs and Naiman, 2008; Pavlovic et al., 2011; Van Coller et al., 2013). In a study on savanna browser resource use, Du Toit
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(1988) reported that forbs constitute between 50% and 80% of the diet of three savanna mesoherbivores (measured in terms of feeding time allocation of kudu, impala and steenbok). Impala (Aepyceros melampus) feed mostly on palatable grass species and to a lesser extent on microphyllous woody species (e.g. Acacia spp. and Dichrostachys spp.), although forbs are also present in their diet and play an important role in the selection of feeding stations (Van der Merwe and Marshal, 2012). Forbs have also been recorded in the diet of two megaherbivores, i.e. African elephant (Loxodonta africana) and black rhinoceros (Diceros bicornis) (Malan et al., 2012; Landman et al., 2013). Further motivation for studies on forbs in diets of larger mammals was revealed through a DNA metabarcoding study of ancient DNA preserved in permafrost sediments (Willerslev et al., 2014). Contrary to earlier studies on Arctic vegetation, the study revealed that forbs, and not graminoids, dominated Arctic vegetation up until the Last Glacial Maximum (25–15 kyr before present), and that both graminoids and forbs featured in the diets of megafaunal mammals (Willerslev et al., 2014). The Kruger National Park (KNP) in South Africa is a well-studied savanna ecosystem in which heterogeneity and complexity are acknowledged and applied in management practices. Landscape heterogeneity in KNP influences vegetation patterns and hence community assemblages and densities of large herbivores at different spatial scales (Du Toit, 2003). At the smaller scale, savanna catenas represent gradual or sometimes abrupt turnover in soil moisture, nutrients, species assemblages and vegetation structure (Scholes, 1990). This study expands on work showing the value of savanna forbs (Du Toit, 1988) and is specifically aimed at testing whether differences exist in the distribution and browsing intensity of savanna forbs between dystrophic uplands and eutrophic bottomlands (Scholes, 1990). Knowledge of herbivore preference among forb species and differences in browsing intensities across the catenal sequence should improve our understanding of the resource value of savanna forbs.
Long-term monitoring transects were located perpendicular to the perennial Sabie River. These transects, which crossed the catenal sequence consisted of 10 m × 20 m fixed plots (long side parallel to the river channel) with two nested 1 m2 plots in the eastern and western corners of each 200 m2 plot respectively in which all rooted forb and grass species were identified and counted for species richness and density analyses (see Van Coller and Siebert (2015) for a detailed account on the experimental design and layout of the transects). A total of 156 1 m2 plots provided data for calculating mean values per growth form. For browsing intensity, data were collected in 78 of the larger, fixed 200 m2 plots along the transects. Sampling was done during the rainy season (November/December 2013) when plant cover was at its maximum and most plant species were present. Half of the plots were located in a fire treatment, although no effect of fire was expected since the last fire occurred in 2007 (6 years prior to sampling).
2. Materials and methods
2.3. Browsing intensity
2.1. Study area
An index was designed to record the intensity of browsing signs on all individuals of potentially palatable forb species encountered in each 200 m2 plot. A forb species was considered ‘potentially palatable’ if it showed any signs of browsing. The index (Table 1) was broadly based upon Walker's Palatability Index (Walker, 1980). Although this index is referred to as a palatability index, it is based upon browsing intensities of forb species and individuals. Since insects contribute substantially to herbivory patterns in savanna ecosystems, browsing signs by insects were included in the index for an overall view of herbivore selection of forbs. Browsed forb species were grouped according to plant family (Germishuizen and Meyer, 2003) to determine whether these taxa (i.e. browsed forbs) represented similar plant families. Habitat preference (fidelity to a topographic zone) was used to differentiate between diagnostic (i.e. species dominant in one topographic zone), unique or character (i.e. restricted to one topographic zone) and common (i.e. common across all topographic zones) browsed species. The following were calculated for each plot: (i) the total number of browsed individuals for all species; (ii) the total number of browsed
The Nkuhlu study area (24°58′S, 31°46′E) is adjacent to the Sabie River in southern KNP. The climate is semi-arid subtropical with two broadly distinct seasons: a hot, occasionally wet, growing season and a warm, dry, dormant season (Williams et al., 2009). Mean annual rainfall at Skukuza, 30 km west of Nkuhlu, is ~550 mm (http://www.sanparks. org/parks/kruger/conservation/scientific/weather). Average daily temperatures at Skukuza are 15.7 °C in June and 26.6 °C in January. Average minimum temperature in June is 5.7 °C and average maximum temperature in January is 32.6 °C. The topography is an undulating landscape, 200–230 m above mean sea level, derived from granite and covering the sequence of terrain morphology from bottomlands to uplands. The uplands are characterized by shallow, sandy, coarse soil overlying rock, while the bottomlands (below the seepline) are characterized by deep, sodic, duplex soil, which is a typical pattern on catenas in granite-derived, semi-arid landscapes (Khomo and Rogers, 2005; Grant and Scholes, 2006). Sodic soils in the study area are composed of shallow (b15 cm) sand overlying impermeable clay and have high pH (N 8.5) and reduced hydraulic conductivity (Khomo and Rogers, 2005; Grant and Scholes, 2006; Tarasoff et al., 2007). Sodic soils are therefore regarded as potentially stressful environments for vegetation, which is sparse, but regarded as more attractive than upland vegetation to large herbivores, especially grazers and mixed feeders (Tarasoff et al., 2007; Levick and Rogers, 2008). The attractiveness of sodic patches to herbivores is because the vegetation is inherently more nutritious (Bailey and Scholes, 1997) and because it offers other attractions such as predator vigilance, water, dietary salts or anti-acidosis minerals (Khomo and Rogers, 2005). Nevertheless, trampling, excretion and defoliation are thought to maintain the vegetation in a nutritious vegetative state (Grant and Scholes, 2006). Directly adjacent to the Sabie
River, the bottomlands are composed of deep alluvial soils underlying riparian vegetation that is dense for the most part. Vegetation of the study area was described by Siebert and Eckhardt (2008). Common mammal herbivores included impala (Aepyceros melampus), African elephant (Loxodonta africana), hippo (Hippopotamus amphibius), black rhino (Diceros bicornis), white rhino (Ceratotherium simum), blue wildebeest (Connochaetes taurinus), Cape buffalo (Syncerus caffer), plains zebra (Equus quagga), greater kudu (Tragelaphus strepsiceros), steenbok (Raphicerus campestris), giraffe (Giraffa camelopardalis) and scrub hare (Lepus saxatilis). Elephant density fluctuated around 0.5–2.0 km− 2 (Grant et al., 2008). A breeding herd of 30–40 impala, several impala bachelors, two black rhino and an unknown number of steenbok were resident in the study area, while low numbers of giraffe and kudu were occasionally present. 2.2. Sampling design
Table 1 Index used to measure browsing intensity on herbaceous forbs (after Walker, 1980). Index % leaf area Description value removed 0 1 2 3 4
0 1–10% N10–50%
Not browsed. No signs of herbivory Few holes in leaves Lightly browsed. Few branches/branchlets/leaves removed. Most leaves remain on plant N50–80% Moderately browsed. Most branches/branchlets/leaves removed, leaving only a few leaves to remain on plant N80–100% Intensively browsed: Almost all branches/branchlets/leaves removed. Mostly only one or two leaves to remain on plant
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species; and (iii) an average plot index value based on each individual index value.
2.4. Statistical analyses STATISTICA 11 (2012) was used to test the difference between density and richness of forbs compared to grasses. To test for the distribution of browsed species across the catena, non-metric multidimensional scaling (NMDS) analysis, along with the application of the Bray Curtis Dissimilarity Index, was applied in PRIMER version 6 (Clarke and Gorley, 2006) for a visual interpretation of species assemblages. Analysis of similarities (ANOSIM), a non-parametric test for significant differences, was performed to test for significant differences in forbs species composition and browsing between topographical zones in PAST (Hammer et al., 2001). ANOSIM uses rank dissimilarities based on the Bray–Curtis coefficient of similarity. The significance of the separation of two distinct groups in ordinal space is calculated using an R-statistic between one (groups are totally different) and zero (groups are indistinguishable) (Clarke, 1993). To assess which taxa were primarily responsible for the observed differences, the Similarity Percentage (SIMPER) method (Clarke, 1993) was applied to the data set in the PAST computer software package (Hammer et al., 2001). The homogeneity of variance assumption was tested using Levene's test (Levene, 1960). Since the data met these assumptions, a one-way analysis of variance (ANOVA) was applied to the data set in STATISTICA 11 (2012) to test the effect of catenal position on the browsing intensity (measured as the mean palatability index value per plot). To distinguish between significantly different zones with respect to browsing, pairwise Unequal N HSD (Tukey) tests were conducted. 3. Results 3.1. Forb species richness and density Of the 228 total species in the herbaceous layer that were recorded, 178 were forb species, which made up 78% of the total species richness of the herbaceous layer. Species richness of forbs was significantly (t = 17.81; n = 180; p ≤ 0.001) higher than for grasses (Fig. 1). Forb density, measured as the number of individuals per 1 m2, was not significantly (t = 1.46; n = 180; p = 0.144) higher than grass density (Fig. 1). A total of 76 herbaceous forb species were browsed at various levels of intensity, which makes up 43% of the total forb species richness in the study area. A summary of the most important browsed forb species (termed ‘key browsed species’ hereafter) is presented in Table 2. 3.2. Species composition A total of 2353 individuals of the 76 browsed forb species were recorded. Twenty-nine forb species each contributed more than 1% to the total number of browsed forb individuals across all topographic zones according to the SIMPER Analysis (Clarke, 1993). Eleven species (i.e. Pupalia lappacea, Justicia protracta, Hibiscus sabiensis, Indigofera tinctoria, Kyphocarpa angustifolia, Ruellia cordata, Acalypha indica, Chamaecrista mimosoides, Commelina benghalensis, Justicia flava and Amaranthus dinteri) comprised half of all browsed forb individuals across topographic zones, of which P. lappacea, J. protracta and Hibiscus sabiensis contributed to 20% of all browsed forb individuals across the catenal sequence. Unique assemblages of browsed forb species were observed for each topographic zone (Fig. 2). Differences in species composition between topographic zones were confirmed by Bray–Curtis similarity in ANOSIM (p ≤ 0.001, R = 0.385) (Clarke, 1993). A summary of the most important browsed forb species in the study area (Table 2) revealed unique browsed species assemblages for each topographic zone.
Fig. 1. Mean species richness (no. of species) (a) and density (no. of individuals) (b) of forbs vs. grasses per 1 m2 plot.
3.3. Browsing Data were normally distributed and equal variance assumptions were tested for in the Levene's procedure. Significant variation in browsing intensity measured as mean palatability index values per plot was revealed across the catena (F2,75 = 12.58; p b 0.001). Post hoc tests for significant difference in browsing intensity between different topographic zones revealed significantly more browsing in sodic bottomlands (Table 3). The least number of browsed forb individuals at the experimental site was recorded in the riparian zone (Table 3).
4. Discussion Forb species contributed significantly to total herbaceous species richness, which is consistent with the majority of phytodiversity studies in grassland and savanna ecosystems globally (e.g. Shackleton, 2000; Pokorny et al., 2004; Uys, 2006; Jacobs and Naiman, 2008; Bond and Parr, 2010; Pavlovic et al., 2011; Axmanová et al., 2012; Van Coller et al., 2013; Koerner et al., 2014; Scott-Shaw and Morris, 2014). Herbaceous species diversity studies along catenal zones suggest that disturbance and resource availability interact to shape diversity patterns in savanna ecosystems, although diversity is consistently higher in the eutrophic bottomlands (Shackleton, 2000; Stromberg, 2007). Forb species richness and density in this semi-arid savanna are therefore suggested
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Table 2 List of diagnostic (i.e. dominant in one topographic zone), unique (i.e. restricted to one topographic zone) and common (i.e. occur in all topographic zones) browsed forb species along the Sabie River. Numerical values reflect the frequency of a species (i.e. the number of records within a topographic zone) with 1 ≤ 10%, 2 = 10–50%, 3 ≥ 50%. Species with frequencies less than 10% were only included if they were unique species. Species groups Diagnostic species Triumfetta annua Sesbania bispinosa* Malvastrum coromandelianum* Amaranthus dinteri Achyropsis leptostachya Corbichonia decumbens Seddera suffruticosa Potulaca kermesina Talinum arnotii Gomphrena celosioides* Commelina benghalensis Blepharis integrifolia Aptosimum lineare Chamaecrista mimosoides Clerodendrum ternatum Indigofera daleoides Senna italica Polygala sphenoptera Ruellia patula Acalypha indica
Family
Riparian bottomlands
Sodic bottomlands
Tiliaceae Fabaceae Malvaceae
2 2 2
1 1 1
Amaranthaceae Amaranthaceae Molluginaceae Convolvulaceae Portulacaceae Portulacaceae Amaranthaceae Commelinaceae 1 Acanthaceae 1 Scrophulariaceae Fabaceae
2 2 2 2 2 2 2 2 2
Lamiaceae Fabaceae Fabaceae Polygalaceae Acanthaceae Euphorbiaceae
Common species Indigofera tinctoria Ruellia cordata Sida cordifolia Barleria elegans Rhinacanthus xerophyllus Pupalia lappacea Kyphocarpa angustifolia Hibiscus sabiensis Bidens bipinnata* Justicia protracta Justicia flava Hermannia glanduligera
1 1
2 2
1 2
Unique (character) species Ageratum conyzoides* Asteraceae 1 Ruellia otaviensis Acanthaceae 1 Amaranthus dinteri Amaranthaceae Achyropsis leptostachya Amaranthaceae Potulaca kermesina Portulacaceae Talinum arnotii Portulacaceae Gomphrena celosioides* Amaranthaceae Aizoon canariense Aizoaceae Ecbolium glabratum Acanthaceae Aptosimum lineare Scrophulariaceae Chamaecrista Fabaceae mimosoides Clerodendrum ternatum Lamiaceae Indigofera daleoides Fabaceae Senna italica Fabaceae Polygala sphenoptera Fabaceae Polygala uncinata Fabaceae Tephrosia purpurea Fabaceae
Uplands
2 2 2 2 2 3
2 2 2 2 2 1 1 2 2 2 2 2 2 1 1
Fabaceae Acanthaceae Malvaceae Acanthaceae Acanthaceae
3 2 2 2 1
3 3 2 2 2
1 1 1 1 1
Amaranthaceae Amaranthaceae Malvaceae Asteraceae Acanthaceae Acanthaceae Sterculiaceae
2 2 2 2 2 2 1
3 3 3 1 3 2 1
3 3 3 2 1 3 2
Species marked with an asterisk (*) are alien species.
to be driven by similar fine-scale fluctuations in soil fertility. Our results showed a contrast in the distribution of browsed forbs between dystrophic uplands and eutrophic bottomlands. Browsed forb species formed unique assemblages across the catenal sequence, suggesting that localized contrasts between nutrient-poor dystrophic uplands and nutrient-rich eutrophic bottomlands drive changes in the composition of browsed forbs. Turnover in species composition along the catenal sequence is well-known in savanna ecosystems (Scholes, 1990; Siebert and Eckhardt, 2008; Siebert et al., 2010; Scogings et al., 2012) as
Fig. 2. Two-dimensional non-metric multi-dimensional scaling (NMDS) ordination of 78 plots hosting browsed forb species.
assemblages are commonly associated with the changing abiotic template. For example, dystrophic uplands in granitic Lowveld landscapes are typically characterized by broad-leaved vegetation (dominated by Combretum spp.) dominated by less palatable grasses, while eutrophic bottomlands are associated with fine-leaved, mostly Acacia spp. in the woody layer and more palatable grasses in the herbaceous layer (Gertenbach, 1983). Despite unique assemblages of browsed forbs, some were common across the catena (Table 2). Most of these generalist species formed the largest proportion of the key browsed forbs according to SIMPER analyses, although they were neither equally abundant nor equally browsed across the catena, supporting the effect of topographical position (i.e. moisture and nutrient availability) on forage patch selection (Grant and Scholes, 2006). Sodic bottomlands are particularly important for dry season survival of larger mammals of the savanna ecosystem through nutritional benefits (Grant and Scholes, 2006). Feedbacks between herbivores and the herbaceous layer are evident in sodic patches since herbaceous species richness drops substantially as standing above-ground biomass increases in the absence of herbivory (Van Coller et al., 2013; Van Coller and Siebert, 2015). Since sodic bottomlands are well-known for nutrient accumulation (Khomo and Rogers, 2005) and higher species richness than dystrophic uplands (Shackleton, 2000), higher richness of browsed species and increased browsing may be expected. Although our results revealed higher browsing in the sodic bottomlands, the density of browsed forb species was not higher than the crest zone. The dystrophic uplands hosted as many individuals of browsed forb species as the sodic bottomlands. One of the key browsed species, Chamaecrista mimosoides, as well as one third of all browsed forb species of the uplands belong to the Fabaceae, which are known for their nitrogen-fixing capacity in dystrophic conditions. Our results suggest that high richness of browsed forbs on the uplands may be possible because the high number of N-fixing species in the assemblage is not only an adaptation to the abiotic conditions, but may also facilitate the persistence of non-fixing species (Li et al., 2014). The key browsed forb species according to SIMPER analyses, belonged to fifteen families, of which species from the Acanthaceae, Table 3 Mean (± SD) browsing index values and number of browsed individuals per 200 m2 across the catena at the Nkuhlu site in Kruger National Park. Topographic zone
Mean browsing index value per 200 m2 Mean browsed individuals per 200 m2
Alluvial bottomland
Sodic bottomland
Upland
1.9 ± 0.63b
2.8 ± 0.74a
2.1 ± 0.66b
18.3 ± 12.29a
36.5 ± 16.63b
34.8 ± 16.64b
Means bearing the same letter are not significantly different (determined by Tukey's unequal NHSD test at p b 0.05).
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Amaranthaceae, Fabaceae and Malvaceae contributed to the group that is significantly more browsed. The dominant browsed forb species on the sodic soils of the bottomlands varied from small, succulent to large or prostrate plants. Increased browsing on the sodic bottomlands infers that forb palatability is enhanced by soil nutrients, which are in turn maintained by high herbivore concentrations on these nutrient hotspots (Grant and Scholes, 2006). Some browsed forb species were apparently browsed regardless of the obvious presence of putative antiherbivore defense mechanisms. For example, C. ternatum is glandulous and aromatic, and H. sabiensis, which comprised 20% of browsed forb individuals across the catenal sequence, is glandulous and hairy. Trichomes on Hibiscus species elsewhere apparently do not deter mammal herbivores and are thought to function as defenses against insects (Louthan et al., 2013). Blepharis integrifolia, a prostrate forb of up to 40 cm when not browsed (Germishuizen and Meyer, 2003) (Fig. 3a), formed patches of continuous ground cover in the sodic bottomlands (Fig. 3b). Under browsed conditions, B. integrifolia appears as lowgrowing plants that spread like stoloniferous grasses (e.g. Fig. 3b), which were similar in appearance to grazing lawns (McNaughton, 1984) despite its spiny bracts (Fig. 3c). This continuous forb ground cover was presumably also created and maintained by heavy browsing, although these observations require further investigation, such as quantifying differences in growth rate and nitrogen content under browsed and not-browsed conditions. Grazing lawns are recognized as important components in savanna ecosystems (Hempson et al., 2014) because they provide nutritious forage for grazers such as white rhino (Waldram et al., 2008). The function of forbs in these highly valuable forage patches therefore needs to be explored. Although the density and richness of non-native species along the Sabie River are very low when compared to native species (Foxcroft et al., 2008), three of the five most important browsed forbs in the riparian bottomlands were non-native species. Ecosystem functioning in protected areas such as Kruger National Park is therefore not only related to native species. Woody cover in KNP increased by 12% on granitic substrates since 1940 and may be expected to increase further (Eckhardt et al., 2000). Of the list of important browsed forb species, P. lappaceae, A. indica, C. benghalensis, J. flava and J. protracta are, however, all shade tolerant, which implies that these forage resources may become increasingly important in time. Forbs are highly dynamic in their response to small-scale environmental heterogeneity (Shackleton, 2000; Stromberg, 2007; Bond and Parr, 2010; Lettow et al., 2014) and therefore understanding their ecology remains a challenge. However, we anticipate that this study will further stimulate curiosity on this life form and its contribution to patterns and processes in savanna ecology. 5. Conclusions Forb species (i.e. herbaceous dicotyledonous species, non-graminoid monocots and geophytes) made up an important component of the herbaceous diversity of a semi-arid savanna ecosystem. Forb species made out the largest component of total herbaceous richness and made a potentially significant contribution to herbivore nutrition in this semi-arid savanna, of which a large proportion (i.e. 43%) was browsed. Consistent with patterns of water availability and nutrient turnover along a savanna toposequence, herbaceous forbs were more intensively browsed on nutrient-rich, eutrophic bottomlands and more specifically in the sodic zone. Our results therefore strongly support the need to consider herbaceous forbs in models to explain savanna resource ecology and heterogeneity. Since it remains a challenge to tease out the key factors in plants that influence their consumption by large herbivores, more research on the ecology of savanna forbs is anticipated to expand our current view on their functions in heterogeneous landscapes driven by local-scale variability in nutrients, water, herbivory and fire.
Fig. 3. Blepharis integrifolia is a forb species that grows upright when not browsed (a) but forms patches of prostrate ground cover or ‘browsing lawns’ on heavily utilized sodic bottomlands (b), where it is browsed despite its spiny bracts (c).
Acknowledgments We thank Judith Botha, Rheinhardt Scholtz, Patricia Khoza and Adolf Manganyi from SANParks for their logistical support during data collection, Stefan Siebert from the AP Goossens herbarium, NorthWest University and Guin Zambatis from the Skukuza Herbarium, SANParks for providing assistance during plant identification, and all students and colleagues for field work assistance. Funding was provided
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South African Journal of Botany journal homepage: www.elsevier.com/locate/sajb
Browsing intensity of herbaceous forbs across a semi-arid savanna catenal sequence F. Siebert a,⁎, P. Scogings b a b
Unit for Environmental Sciences and Management, North-West University, Private Bag X6001, Potchefstroom, 2520, South Africa School of Life Sciences, University of KwaZulu-Natal, Private Bag X54001, Durban 4000, South Africa
a r t i c l e
i n f o
Article history: Received 20 March 2015 Received in revised form 5 May 2015 Accepted 7 May 2015 Available online xxxx Edited by RM Cowling Keywords: Kruger National Park Grazing lawn Exclosure Species richness Mesobrowser Herbaceous Herbivore diet
a b s t r a c t Ecological models to explain savanna heterogeneity and functioning weakly represent herbaceous forbs, which inevitably created knowledge gaps regarding the diversity and ecology of forbs. Forbs constitute over 70% of semi-arid savanna species richness. The aim of this study was therefore to (i) identify forb species that potentially form part of herbivore diet, and (ii) determine forb browsing intensity across a granitic savanna catenal sequence. Localized contrasts between nutrient-poor dystrophic uplands and nutrient-rich eutrophic bottomlands led us to predict that bottomlands would host forb assemblages dominated by browsed species. Forbs contributed to 78% of the total herbaceous layer species richness, of which 43% were browsed at varying intensities along the catenal sequence. Each topographic zone hosted a unique assemblage of browsed forbs, although browsing intensity was highest in the sodic bottomlands. Some browsed forbs formed prostrate, stoloniferous covers on the bottomlands, creating a lawn type dominated by forbs. Results presented here are the first to identify browsed forb species and to illustrate the turnover in browsing intensity of forbs across a semi-arid savanna catenal sequence. Our results add weight to the need to include herbaceous forbs in savanna management models to better understand savanna resource ecology and heterogeneity. © 2015 SAAB. Published by Elsevier B.V. All rights reserved.
1. Introduction African savannas are characterized by heterogeneous landscape types that provide a template upon which structural diversity and resource availability are shaped (Pickett et al., 2003). The general association of savanna types with soil fertility led to the concept of moist, nutrient-poor (i.e. dystrophic) savannas on highly leached, sandy soil versus arid, nutrient-rich (i.e. eutrophic) savannas on clayey substrates (Huntley, 1982). In arid and semi-arid savannas (b650 mm rainfall per annum), nutrient distribution can however be patchy. For instance, in a granitic savanna catenal sequence, there is a discernible turnover in nutrients and vegetation structure from uplands to bottomlands (Scholes, 1990), where uplands are associated with a nutrient-poor, broad-leaved savanna type (i.e. equivalent to dystrophic) and the clay-rich bottomlands with a nutrient-rich, fine-leaved savanna type (i.e. equivalent to eutrophic). This form of heterogeneity is however not attributed to abiotic variance in the landscape only, but is enhanced by the top-down effects of herbivory and fire, particularly so for the southern African savannas (Sankaran et al., 2005; Jacobs and Naiman, 2008; Smit et al., 2012). Despite of its variability, a defining feature of savannas is a continuous herbaceous layer and a discontinuous stratum of trees and shrubs within the same landscape (Knoop and Walker, 1985). ⁎ Corresponding author. Tel.: +27 182992374. E-mail address: [email protected] (F. Siebert).
http://dx.doi.org/10.1016/j.sajb.2015.05.007 0254-6299/© 2015 SAAB. Published by Elsevier B.V. All rights reserved.
Understanding this ecologically important coexistence of trees and grasses is extremely valuable, particularly for savanna ecosystem management (O’Connor et al., 2014). During the past two decades, savanna management has shifted its focus from causes of ecosystem change, habitat homogeneity, equilibrium and carrying capacity to responses to change, heterogeneity, dynamic equilibrium and ecosystem redundancy perspectives (Rogers, 2003; Grant et al., 2011). The understanding and application of these concepts to the herbaceous layer are however, largely based upon findings from rangeland science, a discipline driven by agriculture (i.e. herbivore productivity) rather than conservation in southern Africa (Tainton, 1999). For this reason, savanna management models exclusively used grass species, particularly due to their significant contribution to total standing biomass and their important role in forage for both ruminant and non-ruminant savanna grazers (Treydte et al., 2013). Herbaceous dicotyledonous species, non-graminoid monocots and geophytes (collectively termed ‘forbs’ hereafter) have been ignored or merely lumped into a ‘non-grassy, Increaser II’ category in management models (Scott-Shaw and Morris, 2014), although they constitute the largest component of herbaceous species richness in grasslands (Pokorny et al., 2004; Bond and Parr, 2010; Koerner et al., 2014; Scott-Shaw and Morris, 2014), temperate deciduous forests (Axmanová et al., 2012) and savanna ecosystems (Shackleton, 2000; Uys, 2006; Jacobs and Naiman, 2008; Pavlovic et al., 2011; Van Coller et al., 2013). In a study on savanna browser resource use, Du Toit
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(1988) reported that forbs constitute between 50% and 80% of the diet of three savanna mesoherbivores (measured in terms of feeding time allocation of kudu, impala and steenbok). Impala (Aepyceros melampus) feed mostly on palatable grass species and to a lesser extent on microphyllous woody species (e.g. Acacia spp. and Dichrostachys spp.), although forbs are also present in their diet and play an important role in the selection of feeding stations (Van der Merwe and Marshal, 2012). Forbs have also been recorded in the diet of two megaherbivores, i.e. African elephant (Loxodonta africana) and black rhinoceros (Diceros bicornis) (Malan et al., 2012; Landman et al., 2013). Further motivation for studies on forbs in diets of larger mammals was revealed through a DNA metabarcoding study of ancient DNA preserved in permafrost sediments (Willerslev et al., 2014). Contrary to earlier studies on Arctic vegetation, the study revealed that forbs, and not graminoids, dominated Arctic vegetation up until the Last Glacial Maximum (25–15 kyr before present), and that both graminoids and forbs featured in the diets of megafaunal mammals (Willerslev et al., 2014). The Kruger National Park (KNP) in South Africa is a well-studied savanna ecosystem in which heterogeneity and complexity are acknowledged and applied in management practices. Landscape heterogeneity in KNP influences vegetation patterns and hence community assemblages and densities of large herbivores at different spatial scales (Du Toit, 2003). At the smaller scale, savanna catenas represent gradual or sometimes abrupt turnover in soil moisture, nutrients, species assemblages and vegetation structure (Scholes, 1990). This study expands on work showing the value of savanna forbs (Du Toit, 1988) and is specifically aimed at testing whether differences exist in the distribution and browsing intensity of savanna forbs between dystrophic uplands and eutrophic bottomlands (Scholes, 1990). Knowledge of herbivore preference among forb species and differences in browsing intensities across the catenal sequence should improve our understanding of the resource value of savanna forbs.
Long-term monitoring transects were located perpendicular to the perennial Sabie River. These transects, which crossed the catenal sequence consisted of 10 m × 20 m fixed plots (long side parallel to the river channel) with two nested 1 m2 plots in the eastern and western corners of each 200 m2 plot respectively in which all rooted forb and grass species were identified and counted for species richness and density analyses (see Van Coller and Siebert (2015) for a detailed account on the experimental design and layout of the transects). A total of 156 1 m2 plots provided data for calculating mean values per growth form. For browsing intensity, data were collected in 78 of the larger, fixed 200 m2 plots along the transects. Sampling was done during the rainy season (November/December 2013) when plant cover was at its maximum and most plant species were present. Half of the plots were located in a fire treatment, although no effect of fire was expected since the last fire occurred in 2007 (6 years prior to sampling).
2. Materials and methods
2.3. Browsing intensity
2.1. Study area
An index was designed to record the intensity of browsing signs on all individuals of potentially palatable forb species encountered in each 200 m2 plot. A forb species was considered ‘potentially palatable’ if it showed any signs of browsing. The index (Table 1) was broadly based upon Walker's Palatability Index (Walker, 1980). Although this index is referred to as a palatability index, it is based upon browsing intensities of forb species and individuals. Since insects contribute substantially to herbivory patterns in savanna ecosystems, browsing signs by insects were included in the index for an overall view of herbivore selection of forbs. Browsed forb species were grouped according to plant family (Germishuizen and Meyer, 2003) to determine whether these taxa (i.e. browsed forbs) represented similar plant families. Habitat preference (fidelity to a topographic zone) was used to differentiate between diagnostic (i.e. species dominant in one topographic zone), unique or character (i.e. restricted to one topographic zone) and common (i.e. common across all topographic zones) browsed species. The following were calculated for each plot: (i) the total number of browsed individuals for all species; (ii) the total number of browsed
The Nkuhlu study area (24°58′S, 31°46′E) is adjacent to the Sabie River in southern KNP. The climate is semi-arid subtropical with two broadly distinct seasons: a hot, occasionally wet, growing season and a warm, dry, dormant season (Williams et al., 2009). Mean annual rainfall at Skukuza, 30 km west of Nkuhlu, is ~550 mm (http://www.sanparks. org/parks/kruger/conservation/scientific/weather). Average daily temperatures at Skukuza are 15.7 °C in June and 26.6 °C in January. Average minimum temperature in June is 5.7 °C and average maximum temperature in January is 32.6 °C. The topography is an undulating landscape, 200–230 m above mean sea level, derived from granite and covering the sequence of terrain morphology from bottomlands to uplands. The uplands are characterized by shallow, sandy, coarse soil overlying rock, while the bottomlands (below the seepline) are characterized by deep, sodic, duplex soil, which is a typical pattern on catenas in granite-derived, semi-arid landscapes (Khomo and Rogers, 2005; Grant and Scholes, 2006). Sodic soils in the study area are composed of shallow (b15 cm) sand overlying impermeable clay and have high pH (N 8.5) and reduced hydraulic conductivity (Khomo and Rogers, 2005; Grant and Scholes, 2006; Tarasoff et al., 2007). Sodic soils are therefore regarded as potentially stressful environments for vegetation, which is sparse, but regarded as more attractive than upland vegetation to large herbivores, especially grazers and mixed feeders (Tarasoff et al., 2007; Levick and Rogers, 2008). The attractiveness of sodic patches to herbivores is because the vegetation is inherently more nutritious (Bailey and Scholes, 1997) and because it offers other attractions such as predator vigilance, water, dietary salts or anti-acidosis minerals (Khomo and Rogers, 2005). Nevertheless, trampling, excretion and defoliation are thought to maintain the vegetation in a nutritious vegetative state (Grant and Scholes, 2006). Directly adjacent to the Sabie
River, the bottomlands are composed of deep alluvial soils underlying riparian vegetation that is dense for the most part. Vegetation of the study area was described by Siebert and Eckhardt (2008). Common mammal herbivores included impala (Aepyceros melampus), African elephant (Loxodonta africana), hippo (Hippopotamus amphibius), black rhino (Diceros bicornis), white rhino (Ceratotherium simum), blue wildebeest (Connochaetes taurinus), Cape buffalo (Syncerus caffer), plains zebra (Equus quagga), greater kudu (Tragelaphus strepsiceros), steenbok (Raphicerus campestris), giraffe (Giraffa camelopardalis) and scrub hare (Lepus saxatilis). Elephant density fluctuated around 0.5–2.0 km− 2 (Grant et al., 2008). A breeding herd of 30–40 impala, several impala bachelors, two black rhino and an unknown number of steenbok were resident in the study area, while low numbers of giraffe and kudu were occasionally present. 2.2. Sampling design
Table 1 Index used to measure browsing intensity on herbaceous forbs (after Walker, 1980). Index % leaf area Description value removed 0 1 2 3 4
0 1–10% N10–50%
Not browsed. No signs of herbivory Few holes in leaves Lightly browsed. Few branches/branchlets/leaves removed. Most leaves remain on plant N50–80% Moderately browsed. Most branches/branchlets/leaves removed, leaving only a few leaves to remain on plant N80–100% Intensively browsed: Almost all branches/branchlets/leaves removed. Mostly only one or two leaves to remain on plant
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species; and (iii) an average plot index value based on each individual index value.
2.4. Statistical analyses STATISTICA 11 (2012) was used to test the difference between density and richness of forbs compared to grasses. To test for the distribution of browsed species across the catena, non-metric multidimensional scaling (NMDS) analysis, along with the application of the Bray Curtis Dissimilarity Index, was applied in PRIMER version 6 (Clarke and Gorley, 2006) for a visual interpretation of species assemblages. Analysis of similarities (ANOSIM), a non-parametric test for significant differences, was performed to test for significant differences in forbs species composition and browsing between topographical zones in PAST (Hammer et al., 2001). ANOSIM uses rank dissimilarities based on the Bray–Curtis coefficient of similarity. The significance of the separation of two distinct groups in ordinal space is calculated using an R-statistic between one (groups are totally different) and zero (groups are indistinguishable) (Clarke, 1993). To assess which taxa were primarily responsible for the observed differences, the Similarity Percentage (SIMPER) method (Clarke, 1993) was applied to the data set in the PAST computer software package (Hammer et al., 2001). The homogeneity of variance assumption was tested using Levene's test (Levene, 1960). Since the data met these assumptions, a one-way analysis of variance (ANOVA) was applied to the data set in STATISTICA 11 (2012) to test the effect of catenal position on the browsing intensity (measured as the mean palatability index value per plot). To distinguish between significantly different zones with respect to browsing, pairwise Unequal N HSD (Tukey) tests were conducted. 3. Results 3.1. Forb species richness and density Of the 228 total species in the herbaceous layer that were recorded, 178 were forb species, which made up 78% of the total species richness of the herbaceous layer. Species richness of forbs was significantly (t = 17.81; n = 180; p ≤ 0.001) higher than for grasses (Fig. 1). Forb density, measured as the number of individuals per 1 m2, was not significantly (t = 1.46; n = 180; p = 0.144) higher than grass density (Fig. 1). A total of 76 herbaceous forb species were browsed at various levels of intensity, which makes up 43% of the total forb species richness in the study area. A summary of the most important browsed forb species (termed ‘key browsed species’ hereafter) is presented in Table 2. 3.2. Species composition A total of 2353 individuals of the 76 browsed forb species were recorded. Twenty-nine forb species each contributed more than 1% to the total number of browsed forb individuals across all topographic zones according to the SIMPER Analysis (Clarke, 1993). Eleven species (i.e. Pupalia lappacea, Justicia protracta, Hibiscus sabiensis, Indigofera tinctoria, Kyphocarpa angustifolia, Ruellia cordata, Acalypha indica, Chamaecrista mimosoides, Commelina benghalensis, Justicia flava and Amaranthus dinteri) comprised half of all browsed forb individuals across topographic zones, of which P. lappacea, J. protracta and Hibiscus sabiensis contributed to 20% of all browsed forb individuals across the catenal sequence. Unique assemblages of browsed forb species were observed for each topographic zone (Fig. 2). Differences in species composition between topographic zones were confirmed by Bray–Curtis similarity in ANOSIM (p ≤ 0.001, R = 0.385) (Clarke, 1993). A summary of the most important browsed forb species in the study area (Table 2) revealed unique browsed species assemblages for each topographic zone.
Fig. 1. Mean species richness (no. of species) (a) and density (no. of individuals) (b) of forbs vs. grasses per 1 m2 plot.
3.3. Browsing Data were normally distributed and equal variance assumptions were tested for in the Levene's procedure. Significant variation in browsing intensity measured as mean palatability index values per plot was revealed across the catena (F2,75 = 12.58; p b 0.001). Post hoc tests for significant difference in browsing intensity between different topographic zones revealed significantly more browsing in sodic bottomlands (Table 3). The least number of browsed forb individuals at the experimental site was recorded in the riparian zone (Table 3).
4. Discussion Forb species contributed significantly to total herbaceous species richness, which is consistent with the majority of phytodiversity studies in grassland and savanna ecosystems globally (e.g. Shackleton, 2000; Pokorny et al., 2004; Uys, 2006; Jacobs and Naiman, 2008; Bond and Parr, 2010; Pavlovic et al., 2011; Axmanová et al., 2012; Van Coller et al., 2013; Koerner et al., 2014; Scott-Shaw and Morris, 2014). Herbaceous species diversity studies along catenal zones suggest that disturbance and resource availability interact to shape diversity patterns in savanna ecosystems, although diversity is consistently higher in the eutrophic bottomlands (Shackleton, 2000; Stromberg, 2007). Forb species richness and density in this semi-arid savanna are therefore suggested
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Table 2 List of diagnostic (i.e. dominant in one topographic zone), unique (i.e. restricted to one topographic zone) and common (i.e. occur in all topographic zones) browsed forb species along the Sabie River. Numerical values reflect the frequency of a species (i.e. the number of records within a topographic zone) with 1 ≤ 10%, 2 = 10–50%, 3 ≥ 50%. Species with frequencies less than 10% were only included if they were unique species. Species groups Diagnostic species Triumfetta annua Sesbania bispinosa* Malvastrum coromandelianum* Amaranthus dinteri Achyropsis leptostachya Corbichonia decumbens Seddera suffruticosa Potulaca kermesina Talinum arnotii Gomphrena celosioides* Commelina benghalensis Blepharis integrifolia Aptosimum lineare Chamaecrista mimosoides Clerodendrum ternatum Indigofera daleoides Senna italica Polygala sphenoptera Ruellia patula Acalypha indica
Family
Riparian bottomlands
Sodic bottomlands
Tiliaceae Fabaceae Malvaceae
2 2 2
1 1 1
Amaranthaceae Amaranthaceae Molluginaceae Convolvulaceae Portulacaceae Portulacaceae Amaranthaceae Commelinaceae 1 Acanthaceae 1 Scrophulariaceae Fabaceae
2 2 2 2 2 2 2 2 2
Lamiaceae Fabaceae Fabaceae Polygalaceae Acanthaceae Euphorbiaceae
Common species Indigofera tinctoria Ruellia cordata Sida cordifolia Barleria elegans Rhinacanthus xerophyllus Pupalia lappacea Kyphocarpa angustifolia Hibiscus sabiensis Bidens bipinnata* Justicia protracta Justicia flava Hermannia glanduligera
1 1
2 2
1 2
Unique (character) species Ageratum conyzoides* Asteraceae 1 Ruellia otaviensis Acanthaceae 1 Amaranthus dinteri Amaranthaceae Achyropsis leptostachya Amaranthaceae Potulaca kermesina Portulacaceae Talinum arnotii Portulacaceae Gomphrena celosioides* Amaranthaceae Aizoon canariense Aizoaceae Ecbolium glabratum Acanthaceae Aptosimum lineare Scrophulariaceae Chamaecrista Fabaceae mimosoides Clerodendrum ternatum Lamiaceae Indigofera daleoides Fabaceae Senna italica Fabaceae Polygala sphenoptera Fabaceae Polygala uncinata Fabaceae Tephrosia purpurea Fabaceae
Uplands
2 2 2 2 2 3
2 2 2 2 2 1 1 2 2 2 2 2 2 1 1
Fabaceae Acanthaceae Malvaceae Acanthaceae Acanthaceae
3 2 2 2 1
3 3 2 2 2
1 1 1 1 1
Amaranthaceae Amaranthaceae Malvaceae Asteraceae Acanthaceae Acanthaceae Sterculiaceae
2 2 2 2 2 2 1
3 3 3 1 3 2 1
3 3 3 2 1 3 2
Species marked with an asterisk (*) are alien species.
to be driven by similar fine-scale fluctuations in soil fertility. Our results showed a contrast in the distribution of browsed forbs between dystrophic uplands and eutrophic bottomlands. Browsed forb species formed unique assemblages across the catenal sequence, suggesting that localized contrasts between nutrient-poor dystrophic uplands and nutrient-rich eutrophic bottomlands drive changes in the composition of browsed forbs. Turnover in species composition along the catenal sequence is well-known in savanna ecosystems (Scholes, 1990; Siebert and Eckhardt, 2008; Siebert et al., 2010; Scogings et al., 2012) as
Fig. 2. Two-dimensional non-metric multi-dimensional scaling (NMDS) ordination of 78 plots hosting browsed forb species.
assemblages are commonly associated with the changing abiotic template. For example, dystrophic uplands in granitic Lowveld landscapes are typically characterized by broad-leaved vegetation (dominated by Combretum spp.) dominated by less palatable grasses, while eutrophic bottomlands are associated with fine-leaved, mostly Acacia spp. in the woody layer and more palatable grasses in the herbaceous layer (Gertenbach, 1983). Despite unique assemblages of browsed forbs, some were common across the catena (Table 2). Most of these generalist species formed the largest proportion of the key browsed forbs according to SIMPER analyses, although they were neither equally abundant nor equally browsed across the catena, supporting the effect of topographical position (i.e. moisture and nutrient availability) on forage patch selection (Grant and Scholes, 2006). Sodic bottomlands are particularly important for dry season survival of larger mammals of the savanna ecosystem through nutritional benefits (Grant and Scholes, 2006). Feedbacks between herbivores and the herbaceous layer are evident in sodic patches since herbaceous species richness drops substantially as standing above-ground biomass increases in the absence of herbivory (Van Coller et al., 2013; Van Coller and Siebert, 2015). Since sodic bottomlands are well-known for nutrient accumulation (Khomo and Rogers, 2005) and higher species richness than dystrophic uplands (Shackleton, 2000), higher richness of browsed species and increased browsing may be expected. Although our results revealed higher browsing in the sodic bottomlands, the density of browsed forb species was not higher than the crest zone. The dystrophic uplands hosted as many individuals of browsed forb species as the sodic bottomlands. One of the key browsed species, Chamaecrista mimosoides, as well as one third of all browsed forb species of the uplands belong to the Fabaceae, which are known for their nitrogen-fixing capacity in dystrophic conditions. Our results suggest that high richness of browsed forbs on the uplands may be possible because the high number of N-fixing species in the assemblage is not only an adaptation to the abiotic conditions, but may also facilitate the persistence of non-fixing species (Li et al., 2014). The key browsed forb species according to SIMPER analyses, belonged to fifteen families, of which species from the Acanthaceae, Table 3 Mean (± SD) browsing index values and number of browsed individuals per 200 m2 across the catena at the Nkuhlu site in Kruger National Park. Topographic zone
Mean browsing index value per 200 m2 Mean browsed individuals per 200 m2
Alluvial bottomland
Sodic bottomland
Upland
1.9 ± 0.63b
2.8 ± 0.74a
2.1 ± 0.66b
18.3 ± 12.29a
36.5 ± 16.63b
34.8 ± 16.64b
Means bearing the same letter are not significantly different (determined by Tukey's unequal NHSD test at p b 0.05).
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Amaranthaceae, Fabaceae and Malvaceae contributed to the group that is significantly more browsed. The dominant browsed forb species on the sodic soils of the bottomlands varied from small, succulent to large or prostrate plants. Increased browsing on the sodic bottomlands infers that forb palatability is enhanced by soil nutrients, which are in turn maintained by high herbivore concentrations on these nutrient hotspots (Grant and Scholes, 2006). Some browsed forb species were apparently browsed regardless of the obvious presence of putative antiherbivore defense mechanisms. For example, C. ternatum is glandulous and aromatic, and H. sabiensis, which comprised 20% of browsed forb individuals across the catenal sequence, is glandulous and hairy. Trichomes on Hibiscus species elsewhere apparently do not deter mammal herbivores and are thought to function as defenses against insects (Louthan et al., 2013). Blepharis integrifolia, a prostrate forb of up to 40 cm when not browsed (Germishuizen and Meyer, 2003) (Fig. 3a), formed patches of continuous ground cover in the sodic bottomlands (Fig. 3b). Under browsed conditions, B. integrifolia appears as lowgrowing plants that spread like stoloniferous grasses (e.g. Fig. 3b), which were similar in appearance to grazing lawns (McNaughton, 1984) despite its spiny bracts (Fig. 3c). This continuous forb ground cover was presumably also created and maintained by heavy browsing, although these observations require further investigation, such as quantifying differences in growth rate and nitrogen content under browsed and not-browsed conditions. Grazing lawns are recognized as important components in savanna ecosystems (Hempson et al., 2014) because they provide nutritious forage for grazers such as white rhino (Waldram et al., 2008). The function of forbs in these highly valuable forage patches therefore needs to be explored. Although the density and richness of non-native species along the Sabie River are very low when compared to native species (Foxcroft et al., 2008), three of the five most important browsed forbs in the riparian bottomlands were non-native species. Ecosystem functioning in protected areas such as Kruger National Park is therefore not only related to native species. Woody cover in KNP increased by 12% on granitic substrates since 1940 and may be expected to increase further (Eckhardt et al., 2000). Of the list of important browsed forb species, P. lappaceae, A. indica, C. benghalensis, J. flava and J. protracta are, however, all shade tolerant, which implies that these forage resources may become increasingly important in time. Forbs are highly dynamic in their response to small-scale environmental heterogeneity (Shackleton, 2000; Stromberg, 2007; Bond and Parr, 2010; Lettow et al., 2014) and therefore understanding their ecology remains a challenge. However, we anticipate that this study will further stimulate curiosity on this life form and its contribution to patterns and processes in savanna ecology. 5. Conclusions Forb species (i.e. herbaceous dicotyledonous species, non-graminoid monocots and geophytes) made up an important component of the herbaceous diversity of a semi-arid savanna ecosystem. Forb species made out the largest component of total herbaceous richness and made a potentially significant contribution to herbivore nutrition in this semi-arid savanna, of which a large proportion (i.e. 43%) was browsed. Consistent with patterns of water availability and nutrient turnover along a savanna toposequence, herbaceous forbs were more intensively browsed on nutrient-rich, eutrophic bottomlands and more specifically in the sodic zone. Our results therefore strongly support the need to consider herbaceous forbs in models to explain savanna resource ecology and heterogeneity. Since it remains a challenge to tease out the key factors in plants that influence their consumption by large herbivores, more research on the ecology of savanna forbs is anticipated to expand our current view on their functions in heterogeneous landscapes driven by local-scale variability in nutrients, water, herbivory and fire.
Fig. 3. Blepharis integrifolia is a forb species that grows upright when not browsed (a) but forms patches of prostrate ground cover or ‘browsing lawns’ on heavily utilized sodic bottomlands (b), where it is browsed despite its spiny bracts (c).
Acknowledgments We thank Judith Botha, Rheinhardt Scholtz, Patricia Khoza and Adolf Manganyi from SANParks for their logistical support during data collection, Stefan Siebert from the AP Goossens herbarium, NorthWest University and Guin Zambatis from the Skukuza Herbarium, SANParks for providing assistance during plant identification, and all students and colleagues for field work assistance. Funding was provided
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