Factors Influencing Recruitment of Forage Plants in Arid Karoo Shrublands, Suzanne J. Milton W. R. J. Dean

Abstract—We recorded mortality and natality in populations of 800 m above sea level) in the arid shrublands of the south- long-lived shrubs over five in arid rangelands of the south- ern Karoo, South Africa (Milton and others 1992). The area ern Karoo, South Africa and studied natural regeneration and sur- receives a variable rainfall (167 mm p.a., range 50-400 mm vival of sown seeds in cleared plots protected or exposed to grazing. over 92 years) that peaks in autumn (March-April). Soils Very little recruitment occurred in undisturbed shrub populations. are fine and alkaline and the vegetation is low growing Germination was a function of seed availability and of autumn (<0.8 m) and clumped with a projected canopy cover <25% rainfall, whereas recruitment was influenced by proximity of seed- (Figs 1a & 1b). lings to established shrubs and by follow-up rainfall in spring and Rangeland at TKRC was in good condition (20,900 forage summer. On the basis of these observations, we propose a simple plants/ha). Adjoining ranch 1 was in good condition and model to predict the circumstances under which rangeland forage moderately grazed (about 6 ha/sheep). Ranch 2 was in poor plants may be restored by resting, reseeding, clearing or combina- condition, and although moderately stocked during the tions of these procedures. study period (7.5 ha/sheep), was still carrying too many

There is a perceived need to increase the productivity and species diversity of overgrazed arid shrublands in the Karoo region of South Africa. Experience has shown that this goal cannot be achieved simply by resting or intensive browsing of range, because overgrazed shrublands are often dominated by long-lived shrubs that are distasteful to do- mestic livestock. Overgrazed shrubland may remain un- suitable for ranching for many years because the component species are long-lived and do not necessarily facilitate suc- cession to alternative states (Westoby and others 1989). Partial clearing of existing vegetation to alter water and nutrient availability (Luken 1990), or re-seeding to establish indigenous forage species, could possibly increase carrying capacity or nature conservation value of such shrublands. This paper reports on the demography of shrub popula- tions of the arid Karoo and on effects of weather, neighbor- ing plants, microsites and grazing animals on the survival of seedlings. These preliminary observations provide a basis for assessing the feasibility of rehabilitating Karoo rangeland.

Study Site and Methods

The study was carried out at Tierberg Karoo Research Center (TKRC), from which domestic livestock were ex- cluded, and on adjacent sheep ranches (33°10'S, 22°17'E,

In: Roundy, Bruce A.; McArthur, E. Durant; Haley, Jennifer S.; Mann, David K., comps. 1994. Proceedings: wildland shrub and arid land resto- ration symposium; 1993 October 19-21; Las Vegas, NV. Gen. Tech. Rep. INT-GTR-315. Ogden, UT: U.S. Department of Agriculture, Forest Service, Figure 1—(a) Arid shrubland at Tierberg Karoo Re- Intermountain Research Station. search Centre in the southern Karoo, South Africa. Sue Milton and Richard Dean are Senior Research Officers with the (b) Mixed species clumps of dwarf shrubs sur- Percy FitzPatrick Institute of African Ornithology, University of Cape rounded by bare ground. Town, Rondebosch 7700, South Africa.

216 sheep for the available forage (4,200 forage plants/ha). In- left on the remainder of the plots. All seedlings on these digenous steenbok (Raphicerus campestris: Bovidae) and plots were counted in April 1991, 1992 and 1993. hares (Lepus capensis: Leporidae) were present at all three sites at low densities (total biomass of mammalian herbi- Sowing Experiments vores 135 kg/km2). A total of 700 seeds of each of the 3 shrub species Flowering, Natality and Mortality and 700 seeds of a winter annual (Tetragonia echinata: Aizoaceae) were sown in March 1990 in the 50 vegetated Three common species of dwarf shrubs (all ) monitoring plots and in the 20 cleared plots. Treatments were selected for study: deciduous broad-leaved Osteosper- were replicated as shown in Fig. 2. Germination and sur- mum sinuatum preferred by sheep, evergreen microphyllous vival of seedlings emerging from the planted seeds were Pteronia empetrifolia palatable to sheep, and evergreen made 5 days after every rain event, and once monthly in microphyllous P. pallens which is toxic to sheep. All indi- the absence of rain. It was assumed that seedlings emerg- viduals in 50 permanent 5 x 5 m quadrats were measured ing in demarcated rows originated from sown seed. (height, canopy diameter, basal stem diameter) and labelled A further trial, using only O. sinuatum seeds, was initi- in November 1988. They were subsequently monitored an- ated in April 1991. Approximately 100 seeds (1 g) were nually until December 1991. Throughout this time the plots planted in and adjacent to each of 6 cleared plots on the were subjected to one of four different grazing treatments heavily grazed sheep ranch. Three of these plots were in as shown in Fig. 2. Despite the partly pseudo-replicated exclosures and three were in the surrounding area that sampling design, inferential statistics were used to test for was grazed by sheep. site and treatment effects on growth, survival and natality. Weather Records and Soil Moisture Seedling Emergence and Survival in Natural Vegetation Rainfall, mean daily temperature maxima and minima, relative humidity and soil moisture data were collected by Emergence and survival of seedlings in natural vegeta- a data logger at TKRC. Relative soil moisture was meas- tion was monitored in 100 wire hoops (160 mm diameter), ured using calibrated nylon sensors buried at 50 and 150 mm two in each of 50 plots used for demographic monitoring. below the soil surface in one vegetated and one cleared plot. All seedlings in the hoops were recorded five days after each major rain event (>10 mm) and in dry periods, at 4-6 weekly intervals. Results

Seedling Survival in Cleared Plots Flowering, Natality and Mortality

Twenty plots in TKRC, 10 in exclosures and 10 open to First flowering occurred at 2-3 years (5 mm b.d.) in O. grazing by indigenous mammals, were cleared of all veg- sinuatum and at 3-5 years (>10 mm b.d.) in Pteronia spp. etation in July 1989 by cutting plants at soil level. Cut Sheep reduced flower production by 63% in O. sinuatum plants were removed from 5 plots in each treatment and and by 68% in P. empetrifolia but had no effect on toxic P. pallens. The numbers of seedlings of a given species that emerged in a plot were related to the numbers of flow- ers (or seeds) of that species in the plot (Fig. 3). There was therefore little regeneration of palatable species where sheep removed most of the flowers. Over the 3 yr period (1988-1991) the annual turnover was <6% in all three spe- cies. Grazing had no effect on the natality : mortality ratio, and 88% of the 104 recorded fatalities were among seedlings.

Background Seedling Emergence and Survival

Seedlings emerged in early winter (April-June) when relative humidity was high and temperatures were low (Figs 4a & 4b). Although the emergence density of seed- lings was related to pre-emergence rain, their survival was correlated (P < 0.001) with post-emergence rainfall (July-October). More seedlings emerged on the overgrazed ranch than Figure 2—Layout of exclosures, grazing and clear- ing treatments at Tierberg Karoo Research Centre elsewhere (P < 0.001) but the percentage that survived (TKRC) and on adjacent sheep ranches. Exclo– did not differ between sites or treatments (Fig. 4b). Sur- sures on Argentina ranch were used only in the vival averaged (mean ± SD) 3.0 ± 2.5% in 1989, 3.3 ± 2.0 second seeding trial. in 1990 and 26.1 ± 5.2 in 1991. Most seedlings (86%) were of small (<0.5 mm) seeded Aizoaceae, the seeds of which

217 were dispersed from hygroscopic capsules during rain showers. However, on littered or vegetated microsites, 19% (247/1320) of emergent seedlings were species with large (>2 mm) wind dispersed seeds, compared with 7% (78/1056) of seedlings that emerged on bare soil.

Clearing Experiments

Clearing of vegetation reduced the rate at which moisture was lost from the upper 15 cm of the soil (Fig. 5). The species composition of seedlings emerging from naturally dispersed seeds on cleared plots was correlated (P < 0.001) with the cover composition of the vegetation on the plots prior to clearing. The distance between a seedling and the perimeter of the cleared plot influenced its chances of survival. Seedlings emerging 2-3 m from established plants survived at higher densities (P < 0.001), and reproduced earlier (P < 0.05) than seedlings that Figure 3—Relationships between densities of emerged closer to neighbours (Fig. 6). emerging seedlings and the number of flowers or In the first sowing trial, more seedlings emerged on seeds of three non-succulent shrubs and of succu- cleared (7.0 ± SD 9.5%) than on vegetated plots (3.9 ± SD lent Mesembryanthema in the southern Karoo. 8.6%). Some of these shrub seedlings survived on cleared plots, but all shrub seedlings that emerged in vegetated plots died during their first summer (Fig. 7). No further shrub emergence occurred in the second autumn, but the winter annual (T. echinata) had many innately dormant seeds which emerged at higher densities in the second autumn (Fig. 7). The resultant plants set more seed in cleared than in vegetated plots (Table 1). In the second sowing trial, on the overgrazed ranch, 25 O. sinuatum seedlings emerged in vegetated plots and 92 emerged in cleared plots. Survival, after 2 years, was simi- lar in vegetated (24%) and cleared (23%) plots. In the first sowing trial, emergence and survival of shrub seedlings, but not winter annuals, was greater on over- grazed Ranch 2 than elsewhere (Fig. 7). In the second sow- ing trial on the overgrazed ranch, 59 O. sinuatum seedlings emerged in grazed areas and 58 emerged in exclosures. After 2 years, survival in grazed plots (10%) was lower

Figure 4—(a) Rainfall, temperature range and hu- midity at Tierberg Karoo Research Centre in the southern Karoo, and (b) seedling emergence over Figure 5—Soil moisture fluctuations at 150 mm be- four years in exclosures at TKRC (no sheep) and low soil surface in undisturbed and cleared vegeta- on adjoining sheep ranches. tion. Rain in millimeters per day.

218 Table 1—Numbers of seeds produced by a winter annual (Tetra- gonia echinata) grown in cleared and vegetated plots in exclosures and grazed rangeland in the southern Karoo. Means with shared superscripts do not differ significantly (ANOVA, P < 0.01).

Number Seeds per plant Treatment of plants Mean ± SD Exclosure cleared 11 6.36a 7.77 Rangeland cleared 24 4.00ab 6.83 Exclosure vegetated 24 0.95b 0.85 Rangeland vegetated 28 1.21b 1.19

(X2 = 9.7, 1 df, P < 0.01) than in exclosures (36%). Seed- lings in exclosures were larger (P < 0.001) than in plots grazed by sheep (Table 2).

Discussion Implications of Low Turnover Rates for Figure 6—Box and whisker plot showing median, upper and lower quartiles and ranges of seedling Management densities at three years in undisturbed vegetation Karoo shrublands, in common with those in arid parts of and in cleared plots at distances of 1, 2, and 3 m the United States (McAuliffe 1988) and Australia (Eldridge from neighboring plants. and others 1990), are dominated by plants that live for de- cades or centuries. Population turnover rates are low. For this reason, compositional losses caused by overgrazing or resting will be very slow. Restoration of productivity or diversity to over-exploited arid shrubland within a human lifetime may require re-seeding and active management of herbivory, competition and microsites.

Factors Influencing Forage Recruitment in Karoo Shrublands

Defoliation and florivory reduces seedling recruitment in many Karoo plants (Milton 1992; Milton and Dean 1988, 1990b, 1993; van Breda and Barnard 1991). Few species of Karoo succulents (Esler and others 1992) and long-lived shrubs have innately dormant seeds. Such species rely on regular seed production for population perpetuation, and are therefore lost from overgrazed rangeland (Milton 1992; O’Connor 1991). By altering the growth rates of forage

Table 2—Heights (mean ± one standard deviation) of one- and two--old Osteospermum sinuatum seedlings from seeds sown in Trial 2 on an overgrazed Karoo shrubland. Seeds were sown in cleared or vegetated exclosures and in cleared or vegetated rangeland grazed by sheep. Means with shared superscripts do not differ significantly (ANOVA, P < 0.01).

May 1992 August 1993 Treatment n height ± SD n height ± SD Exclosure cleared 12 11.6a 3.7 15 13.0a 3.2 Exclosure vegetated 16 4.6b 1.7 6 6.7b 3.4 Rangeland cleared 13 3.2b 1.3 6 4.5b 1.5 Figure 7—Emergence and survival of sown seeds Rangeland vegetated 3 4.0b 2.0 0 no survivors in exclosures, grazed vegetation, and cleared plots.

219 plant populations, herbivory can bring about changes in Non-succulent shrubs establish beneath low-growing, vegetation composition. succulent hosts which they later out-compete (Yeaton and Most shrubs and succulents germinate in autumn in the Esler 1990). The shrubs tolerate one another for decades, southern Karoo (van Breda and Barnard 1991). Large ger- forming mixed-species clumps. In this way Karoo vege- mination events were related to seed availability (dependent tation is arranged in a mosaic of plant islands and bare on vegetation composition, current herbivory and rainfall). ground, much like the vegetation of the Chihuahuan , Few seedlings reach reproductive maturity in undisturbed, Mexico (Montaña 1992). Grazing, and other factors that arid shrublands (Eldridge and others 1990; Milton 1993; increase the proportion of bare ground to vegetated and lit- Owens and Norton 1992). In the southern Karoo, seedling tered microsites, influence the composition of vegetation. survival was dependent on moisture availability in the six months after emergence. Seedlings survived where compe- Model for Change in Southern Karoo tition from established plants had been reduced, prolonging Shrublands water availability after rain events. Droughts (Danckwerts and Stuart-Hill 1988), hail storms On the basis of the foregoing discussion, improvement (Powrie 1993) and intensive trampling and grazing (Bosch in composition of Karoo rangeland could be achieved by: and Gauch 1991) also reduce competition and provide op- a) removing herbivores, b) adding seed of forage species, portunities for seedling establishment. Insects and mam- c) reducing competition from established plants, and d) mals that uproot plants, dig pits, or excavate nests ensure adding seed traps. In addition to this it may be necessary continual seedlings recruitment by creating establishment to restore ecosystem functioning (Milton and others 1994). sites in stable vegetation (Dean and Milton 1991; Milton This could involve soil amelioration (Dean 1992; Roux and and Dean 1990a; Dean and Yeaton 1992). Opperman 1986; Schlesinger and others 1990; Snyman and Seed traps influence the composition and arrangement of Fouché 1991), and reintroduction of animal or microbe spe- Karoo vegetation (Fig. 8). Small seeds (mostly produced by cies that move soil, facilitate nutrient uptake, pollination or low-growing succulent mesembryanthemaceae) are trapped dispersal, or alter competitive interactions between plant by fine soil particles so that their seedlings occur mainly species (Bond 1993; MacMahon 1987). in inter-shrub gaps. Winged or bristled seeds (Liliaceae, The model (Fig. 9) presents hypothetical mechanisms by Asteraceae, Aizoaceae) are tumbled by wind until trapped which an overgrazed arid shrubland (1), could be rehabili- in multi-stemmed plants, litter or mammal diggings (Dean tated to a more productive and diverse shrubland (2), or fur- and Milton 1991; Hoffman and Cowling 1987; Milton 1993). ther degraded to distasteful (3) or ephemeral vegetation (6).

Figure 8—Recruitment opportunities for plant species with small, smooth seed and large, winged seed.

220 There is little information on how transitions from ephem- erals to perennials may be facilitated, but our experiments suggest that seed traps should be provided, or small-seeded species that can establish in the open should be selected for initial re-seeding. An important aspect for future research is the effect of scale on vegetation rehabilitation. We have no information on the effects of the size of an area of transformed Karoo vegetation on its prospects for recovery, and annual disper- sal distances of the component plant species are unknown.

Acknowledgments

This report is a contribution to the Desertification Pro- gramme of the FitzPatrick Institute, University of Cape Figure 9—Rehabilitation model for Karoo shrubland. Town. The Programme is funded by the Foundation for Research Development, the Department of Environment Affairs and the Southern African Nature Foundation. At- The mechanisms for transitions between these states tendance at the Wildland Shrub and Arid Land Restoration of the vegetation include stock withdrawal, natural distur- Symposium was funded by the Foundation for Research bances (grazing, trampling, drought), and active manage- Development and the FitzPatrick Institute. We thank ment of either the vegetation (selective clearing, re-seeding) M.T. Hoffman, M.C. Rutherford, and W.R. Siegfried for or of the environment. Although oversimplified, the model comments and suggestions on a draft of this paper. provides a variety of testable hypotheses. Following Savory (1991), many livestock ranchers believe that short-duration, high-intensity grazing increases both productivity and References abundance of forage species. We have excluded this mecha- Bond, W.J. 1993. Keystone species. In: Schulze, E.D.; nism from our Karoo rehabilitation model because there Mooney, H.A. eds. Biodiversity and Ecosystem Function. is no evidence that it increases forage plant populations Springer, Berlin: 238-253. in arid Karoo shrubland (Hoffman 1988). Bosch, O.J.H.; Gauch, H.G. 1991. The use of defoliation gradients for the assessment and ecological interpreta- Hazards of Vegetation Manipulation tion of range condition. Journal of the Grassland Society As indicated in Fig. 9, reversal of changes involving the of 8: 138-146. replacement of one long-lived plant species by another may Danckwerts, J.E.; Marais, J.B. 1989 An evaluation of the require active intervention by the land manager. There is economic viability of commercial pastoralism in the no universally correct way to manage rangeland (Noy-Meir Smaldeel area of the . Journal of the Grass- 1993): all techniques should be critically evaluated by ex- land Society of southern Africa 6: 1-7. periment for each type of range. Reseeding, with or with- Danckwerts, J.E.; Stuart-Hill, G.C. 1988. The effect of se- out partial clearing, tilling or mulching have all been at- vere drought and management after drought on the mor- tempted in arid and semi-arid southern Africa (Roux and tality and recovery of semi-arid grassveld. Journal of the Vorster 1983). All are costly, none is infallible, and some Grassland Society of southern Africa 5: 218-222. may exacerbate existing rangeland problems. Dean, W.R.J. 1992. Effects of animal activity on the absorp- Seed addition could increase forage plant abundance but tion rate of soils in the southern Karoo, South Africa. is unlikely to succeed without some reduction of established Journal of the Grassland Society of southern Africa 9: plants and temporary protection from grazing. Clearing 178-180. should be approached with caution because it increases Dean, W.R.J.; Milton, S.J. 1991. Disturbances in semi-arid runoff (Snyman and Fouché 1991) and because the costs shrubland and arid grassland in the Karoo, South Africa: involved in vegetation manipulation are unlikely to be off- mammal diggings as germination sites. African Journal set by short-term benefits in arid rangelands (Danckwerts of 29: 11-16. and Marais 1989). Dean, W.R.J.; Yeaton, R 1992. The importance of harvester Droughts and hail storms that kill many established ant Messor capensis nest-mounds as germination sites plants may provide windows of reduced competition when in the southern Karoo. African Journal of Ecology 30: supplementary seeding of forage plants could lead to re- 335-345. cruitment. Walker and others (1986); and Westoby and Eldridge, D.J.; Westoby, M.; Stanley, R.J. 1990. Population others (1989); suggested that opportunistic management dynamics of the perennial rangeland shrubs Atriplex could capitalize on just such natural disturbances. Clear- vesicaria, Maireana astrotricha and M. pyramidata un- ing prior to re-seeding appears to be unnecessary where der grazing. Journal of Applied Ecology 27: 502-512. grazing has reduced above-ground perennial biomass be- Esler, K.J.; Cowling, R.M.; Ivey, P. 1992. Seed biology of low the normal range for the region. three species of Mesembryanthema in the southern Karoo. South African Journal of Botany 58: 343-349.

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