1Multiple regression analyses of population densities on habitat variables of nutrient status and altitude (northern Kruger National Park). http://koedoe.co.za/index.php/koedoe/article/downloadSuppFile/1047/883
2Spearman rank correlations of population performance trend ratings with climate variables for blue wildebeest/zebra, selectively feeding antelope species groups (Figure 6), buffalo and waterbuck. http://koedoe.co.za/index.php/koedoe/article/downloadSuppFile/1047/884
DiscussionLinking climate–vegetation responses with large herbivore population performance Initial assessments revealed the existence of three population performance response groups; that is, groups of large herbivore species which shared similar population performance trends over time (Figures 3 and 4: buffalo and waterbuck; blue wildebeest and zebra; sable antelope, roan antelope, tsessebe and eland). Member species of these groups also shared landscape-scale distribution patterns in relation to subregion on a north-to-south (rainfall) gradient, altitude and nutrient status based on the underlying geology. Perusal of relevant studies (herbivore species guilds of key nutritional requirements) further revealed that the species of the same population performance response groups had common key nutritional resource requirements (Seydack et al. 2012). This permitted the grouping of the eight species under study into congruent guilds: bulk feeders with tolerance to fibrous herbage (roughage bulk feeders: buffalo and waterbuck), bulk feeders with preference for high nitrogen quality forage (short-grass preference grazers: blue wildebeest and zebra) and selective feeders for which dietary items of high carbon-nutrient quality are of particular importance (selective grazers: sable antelope, roan antelope, tsessebe and eland). Accordingly, key nutritional requirements for these three population performance response groups related to the availability of forage quanity, nitrogen quality and carbon-nutrient quality, respectively. A climate–vegetation response model was developed, which defined the expected impact of climate on these key resources (Seydack et al. 2012). According to the climate-vegetation response model forage quality is determined by the position of plant functionality on the SMP–RMP metabolic performance mode gradient (spatially: metabolic mode settings: CVRM-1; temporally: temperature acclimation sequences: CVRM-2). The SMP mode permits plant functionality at relatively low temperature and water availability levels, which supports storage-based nutrient accumulation and growth-curbed metabolic activity, resulting in comparatively high-quality forage. Plants in the RMP mode perform under conditions of high water and temperature levels, which results in low-quality forage. With the climate–vegetation response model being central to an explanatory framework, we proceeded to apply an approach of pattern/process matching where we explored the extent of consistency with which climate impacts on key nutritional resources (process) could explain spatiotemporal correlations between climate and herbivore population trends (pattern). Whereas buffalo and waterbuck, grouped as roughage bulk feeders, seemed to be tracking forage quantity largely determined by rainfall (Table 2; Mills et al. 1995; Owen-Smith & Ogutu 2003), temperature and dry-season rainfall were identified as influential in determining the availability of quality forage in the landscape important for selective grazers and those that prefer short grasses. The importance of dry-season rainfall for these species has been identified in previous studies (Dunham et al. 2004; Owen-Smith & Ogutu 2003). However, the effectiveness of dry-season rainfall in determining the availability of quality forage in the landscape appears to be interdependent with the prevailing plant metabolic performance mode settings (spatial scale) and temperature acclimation responses (temporal scale), as controlled spatiotemporally by gradients of water availability and temperature effects. According to the climate–vegetation response model, prevalence of the SMP mode in the arid northern KNP results in pronounced SMP-to-RMP temperature acclimation sequences (CVRM-2.1) in response to pulses of temperature increases [Figure 7a; broadly synchronous with temperature trends of the southern hemisphere (Figure 1)], thereby inducing accentuated population cycles of short-grass preference grazers (Figures 3a, b and 6) and selective grazers (Figures 4 and 6). Such pronounced temperature responses are expected since SMP mode plant functionality is sensitive to the impact of nocturnal warming on respiration (metabolic performance trade-off relationships) and pronounced phase states of temperature acclimation are associated with disproportionately enhanced (in SMP-P phase state) or reduced (RMP-T phase state) SMP-tw efficiency in responding to dry-season rainfall and producing high-quality forage in general. In the central KNP, with intermediate RMP–SMP mode settings and higher actual dry-season rainfall, a postulated favourable product of SMP-tw efficiency and dry-season rainfall seems to support the relatively sustained population performance of blue wildebeest and zebra. The higher rainfall in the southern KNP underpinned relative RMP mode settings (CVRM-1), which are inherently associated with poorer forage quality (lower carbon-nutrient quality, due to reduced storage allocation, and lowered nitrogen quality, due to dilution by structural carbon resulting from high TW growth priority). Here selective grazers, mainly sable antelope, were sustained only at the highest altitudes and because of reasonable amounts of dry-season rainfall and the availability of carbon-nutrient quality forage procurable from andropogonoid grass species. Extending the emerging pattern to near tropical conditions (RMP-TW metabolic mode settings), it follows that selective grazers can persist under such circumstances only if substantial dry-season rainfall occurs and suitable andropogonoid grass species are commonly available as forage plants. This seems to be the basis for the stable persistence of roan antelope in moist dystrophic West African savannas receiving 800 mm rainfall or more per year (De Bie 1991). Blue wildebeest and zebra do not occur under such conditions where extreme nitrogen dilution of forage items is encountered (RMP-TW functionality). Whereas blue wildebeest and zebra populations performed poorly at extremes of the rainfall gradient (low rainfall: nitrogen dilution by storage products associated with SMP functionality and nitrogen dilution by structural carbon at higher rainfall: RMP-TW functionality), selective grazer species may cope with such conditions. At the arid extreme, SMP modes of plant functionality support forage with carbon-nutrient quality (given sufficiently low ambient temperatures or high altitude) and browsing then seems to be particularly advantageous (eland; roan antelope in more arid parts of West Africa; De Bie 1991). At the mesic end of the gradient, sufficient amounts of dry-season rainfall and andropogonoid grass species form the basis of their persistence. Blue wildebeest and zebra populations perform well under intermediate SMP–RMP plant functionality (central KNP), where nitrogen quality of forage is favoured by relative SMP-tw efficiency of plants, reasonable amounts of dry-season rainfall, growth activity curbed through moisture stress (SMP-Tw functionality) and nutrient-rich substrates. However, over the long term, populations of selective grazers declined (Figure 2a) because of plants’ progressive acclimation to rising temperatures (since about 1910: Figure 1), which compromised storage-based carbon-nutrient quality of available forage (CVRM-2.2). In contrast, rising ambient temperature, by enhancing nitrogen productivity under conditions of SMP-Tw plant functionality, increased the availability of forage with adequate nitrogen quality, expectedly thereby favouring increased population densities of blue wildebeest and zebra (Figure 2b).Bottom-up and top-down impacts on large herbivore population dynamics Owen-Smith and Mills (2006) presented results of comprehensive analyses indicating that changes in population abundance within the multi-prey, general predator system in the KNP arose from a complex interplay between changing climatic conditions, variable food production, shifting habitat conditions, varying vulnerability to predation and spill-over effects on other species. Findings by Owen-Smith and Mason (2005) highlighted the importance of changes in adult survival rates in shaping population trends, implicating an interaction with nutritional shortfalls and the central involvement of predation by lions (Panthera leo), which prey largely on the adult segment of most of the larger herbivore species (Owen-Smith et al. 2005). Patterns of shifting prey selection depending on changing relative abundance and vulnerability of the three principal prey species (wildebeest, zebra and buffalo) further implicated predation as the main cause of the decline of alternative prey species such as waterbuck and the selectively feeding antelope species (Owen-Smith & Mills 2008a). However, Owen-Smith and Mills (2006) caution that attempting to separate the relative importance of top-down influences through predation from bottom-up processes operating through food resources is difficult, as susceptibility to predation depends on changing nutritional conditions and other habitat conditions (concealment), particularly as these factors also affect predator populations. The results of this study permit an interpretation of these complex interacting patterns, placing greater emphasis on bottom-up, climatically linked nutritional factors relative to predation impacts. Prey selection for both buffalo and waterbuck was inversely dependent on rainfall averaged over three preceding years (Owen-Smith & Mills 2008a). Both buffalo and waterbuck seemed more vulnerable to malnutrition, and thus to predation, during periods of low rainfall (Owen-Smith & Mills 2006; Owen-Smith 2008; Owen-Smith & Mills 2008a). Despite heavy predation by lions on waterbuck (Mills et al. 1995), the resultant mortality did not seem to be additive and more important than the negative effects of drought, and populations increased during normal years despite heavy predation on the species by lions and other predators (Pienaar 1969). This also appears to be the case for buffalo. As forage resources improved after the 1991–1992 drought, both species showed recovery in abundance (Figures 3c-d). Prey selection on these species is thus considered rather to be a consequence of malnutrition and not the ultimate cause of declines in abundance. Wildebeest and zebra were found to be more susceptible to predation under conditions of above-average rainfall. This was attributed to prey selection shifting towards these species owing to their susceptibility to predation being increased through the effect of higher vegetation cover facilitating hunting success of lions (Owen-Smith & Mills 2008a). Reduced exposure to predation was apparently associated with increasing abundance of these two species. Also, higher predation pressure on adult wildebeest than on zebra (Owen-Smith & Mills 2008b) was believed to have resulted in higher population numbers for zebra than for wildebeest in recent decades (Joubert 2007b). These patterns were interpreted to support the contention that wildebeest and zebra, the primary prey species selected by lions in the KNP (Owen-Smith & Mills 2008b), were held below the food ceiling through additive predation (Owen-Smith 2008). However, following from the results of this study, some of these patterns can be interpreted alternatively with reference to the dynamics of nitrogen quality of the forage selected by these two species. Accordingly, the reduced population performance during periods of above-average rainfall is attributed to reduced nitrogen quality due to nitrogen dilution associated with high grass productivity. Between 1955 and 1970 the abundance of zebra commenced to exceed that of wildebeest and stabilised at higher population levels. According to our study, this was interpreted as resulting from zebra being tolerant to relatively lower nitrogen quality forage than wildebeest, as such quality was expected to decline with increasing nitrogen productivity and the associated progressively increasing TW growth priority over this time span (climate–vegetation response model). The provision of numerous artificial water points has been implicated to have benefited common water-dependent species, resulting in the influx of blue wildebeest and zebra into the range of the less water-dependent selective grazer species (Gaylard, Owen-Smith & Redfern 2003). Population declines of selective grazer species were consequently attributed to increased predation owing to the associated build-up of lion numbers in their ranges (Harrington et al. 1999). However, in spite of extensive water provisioning, the populations of blue wildebeest and zebra continued to fluctuate and the prolonged period of relatively low population densities of these species since the early 1990s in the northern KNP (Figures 3a–b) did not result in the recovery of selective grazer populations. Evidence of a marked shift in prey selection by lions towards the selectively feeding antelope species around 1987 was reported by Owen-Smith and Mills (2008a). The 2–3-fold increase in relative prey selection for these species was considered adequate to explain a similar rise in adult mortality observed after 1986 (Owen-Smith & Mason 2005; Owen-Smith & Mills 2008a). This shift in predation towards the selectively feeding antelope species was apparently induced by (1) lowered abundance and hence lower availability of buffalo as prey following the 1982–1983 drought and (2) coupled with reduced susceptibility of wildebeest and zebra over the period of low rainfall that set in during 1987. With all three principal prey species less available, lions apparently turned towards alternative prey species, including the selectively feeding antelope species and waterbuck (Owen-Smith & Mills 2008a). However, although the involvement of predation in the decline of selectively feeding antelope species after 1986 is implicated, it is difficult to decouple the interactive predator–prey dynamics from the extrinsically driven context provided by changing food resource conditions (Owen-Smith et al. 2005; Owen-Smith & Mills 2006). The results of this study support an interpretation of the decline of these antelope species involving an interaction between compromised forage quality and a resulting increased vulnerability to predation as a consequence. As accelerated rising temperatures since about 1980 (Figures 1 and 7) increasingly compromised carbon-nutrient quality of forage selected by selectively feeding antelope species (climate–vegetation response model), their nutritionally linked condition apparently declined and had involved most adults of the populations by 1986/1987. Rapid population declines ensued, with no signs of recovery to date (Figures 4a-d). In contrast, as food resource conditions (rainfall-based forage quantity) improved for waterbuck – a species heavily predated on by lions – their population numbers progressively increased (Figure 3d), whilst the population numbers of the selectively feeding antelope species remained low. According to the interpretation of this study the absence of recovery of these antelope populations is the result of continued low levels of carbon-nutrient quality of available forage due to sustained elevated ambient temperatures (Figures 6 and 7). Although impacts of predation on the small remaining populations of selectively feeding antelope species cannot be ignored (Grant et al. 2002), we conclude that even though proximate impacts of predation are considered of significance, the ultimate cause of population performance trends of these species appears to be related to the climatically compromised carbon-nutrient quality of their forage. ConclusionFrom a situation apparently prevailing during the first two to three decades of the 1900s, during which the abundance of selective grazers (sable antelope, roan antelope and tsessebe) was of similar orders of magnitude to that of bulk feeding species (wildebeest, zebra and buffalo), the former declined progressively, whilst the latter increased over subsequent decades. These herbivore population trends were paralleled by progressively enhanced nitrogen productivity, increasing the availability of nitrogen quality forage and declining carbon-nutrient quality (storage-based plant metabolism), apparently linked to increasing temperature over time. Further analysis revealed that population numbers of buffalo and waterbuck, as roughage bulk feeders, tracked forage quantity largely determined by rainfall. Wildebeest and zebra, with their preference for grazing short grasses, were identified as nitrogen quality patch selectors. As such their population performance was favoured in habitats of high nutrient status with sustained nitrogen productivity and nitrogen quality, mainly found in the southern (central) KNP. Population performance of these species, as more clearly manifesting in the northern KNP, was negatively associated with reduced dry-season rainfall and elevated temperatures, a syndrome of climate effects expected to reduce forage nitrogen quality through nitrogen dilution. The population performance of antelope species selecting for carbon-nutrient quality plant parts (sable antelope, roan antelope, eland and tsessebe) was relatively enhanced at higher altitude sites and in northern KNP. Relatively lower temperatures associated with upper altitudes were expected to conserve carbon-nutrient quality of forage and the prevalence of the sustained metabolic performance mode of plants in the northern KNP to support relative plant carbon excess (climate–vegetation response model). Population performance of these antelope species was found to be spatiotemporally negatively associated with high temperature conditions, consistent with predictions of the climate–vegetation response model, according to which carbon-nutrient quality is compromised by elevated ambient temperature. Accordingly, the long-term population decline and the absence of population recovery of these species to date were attributed to progressively increasing and sustained elevated ambient temperature conditions as progressive SMP-to-RMP temperature acclimation reduced the scope for storage-based metabolism in favour of biomass productivity (growth). The results of pattern/process matching conducted in this study revealed remarkable consistency between herbivore population trends and key indices of forage quantity and quality, shaped in accordance with expectations of plant responses to climate (climate–vegetation response model). With regard to all eight species studied, their targeting by lion predation through shifting prey selection, as implicated by Owen-Smith and Mills (2008a), apparently coincided with time periods of compromised forage quantity or quality as predicted by climate–vegetation response processes in this study. Population trends of these species were found to be in apparent synchrony with features of a changing climate (rainfall, dry-season rainfall, and maximum and minimum ambient temperatures). Furthermore, some of the herbivore population trends, such as the lack of recovery of populations of the selectively feeding antelope species over recent years but population increases for waterbuck over the same period, cannot be readily explained with reference to predation, but conform to climatically driven forage availability as outlined in this study. We conclude that ultimate causality of the observed population trends of the species studied is linked to landscape-scale climate–vegetation responses controlling the availability of suitable forage (bottom-up regulation). Proximate impacts of predation additionally shaped the basic population dynamics in a complex and interactive manner (top-down impacts). Acknowledgements We acknowledge the effort of rangers, other field staff and scientists with regard to collecting diverse data sets (e.g. animal population censuses and grassland monitoring) over many decades, without which this study would not have been possible. Mss Judith Kruger, Sandra MacFadyen and Sharon Thomson of Scientific Services, KNP are acknowledged for providing data used in this study. We also thank Prof. Herbert Prins and Ignas Heitkönig for valuable discussions (both from Wageningen University). The South African Weather Service provided temperature and rainfall data. This study represents an output of the specialist scientist research programme in systems ecology conducted by members of the Conservation Services Division (Knysna and Skukuza) of South African National Parks. The main author, in his capacity as honorary research associate at the Botany Department, University of Cape Town thankfully acknowledges general support received from this institution. Competing interests The authors declare that they have no financial or personal relationship(s) which may have inappropriately influenced them in writing this paper. Authors’ contributions A.H.S. (Garden Route National Park) was responsible for the development of the climate-vegetation response model and the interpretation of large herbivore population performance patterns and trends in accordance with this model. C.C.G. (Kruger National Park), I.P.S. (Kruger National Park), W.J.V. (Garden Route National Park) and N.Z. 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