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South African Journal of Botany 78 (2012) 276–280 www.elsevier.com/locate/sajb

Short communication Seed dispersal and seed banks in marlothii () ⁎ C.T. Symes

School of Animal, and Environmental Sciences, University of the Witwatersrand, Private Bag 3, WITS 2050, South Africa

Received 5 January 2011; received in revised form 1 June 2011; accepted 20 June 2011

Abstract

Aloe marlothii flowers during dry winter months (July–September) and produces large numbers of wind dispersed seeds. Fire disturbance in a population of several thousand A. marlothii at Suikerbosrand Nature Reserve, Gauteng, permitted a series of seed dispersal experiments to be conducted. Germination trials indicated that seedling emergence decreased with increased distance from a well defined aloe stand and burn area margin, with seeds dispersed up to 25 m. Flowering frequency and total seed production were positively correlated with plant height, with seed production estimated to range from 26,000 to 375,000 seeds/plant. Although a large number of seeds are produced by flowering plants the survival rate of seeds did not extend beyond the following flowering season. © 2011 SAAB. Published by Elsevier B.V. All rights reserved.

Keywords: Mega-herbivore; ; Succulent; Suikerbosrand; Xanthorrhoeaceae

1. Introduction Pollination is primarily by birds but little is known about the ecology and seed dispersal of this species (Symes et al., 2009). Aloe marlothii A. Berger (Asphodelaceae) is a winter Numerous studies have investigated pollination in other flowering succulent with a widespread distribution in the (Hoffman, 1988; Ratsirarson, 1995; Stokes and Yeaton, 1995; grassland and savanna biomes of South Africa (Reynolds, Pailler et al., 2002; Johnson et al., 2006; Hargreaves et al., 2008; 1969; Glen and Hardy, 2000; Van Wyk and Smith, 2005). Botes et al., 2008; Wilson et al., 2009; Botes et al., 2009; Symes Large populations often persist on rocky north-facing slopes and et al., 2009), although few have considered seed dispersal in this mountainous areas, where some populations appear to be succulent taxon with wind dispersed seeds (Kamstra, 1971; Smith confined to fire-protected islands (Bredenkamp and Van Vuuren, and Correia, 1992; Stokes and Yeaton, 1995). 1987). Additional protection against fire may also be enhanced by Important in the management of Suikerbosrand Nature a dry leaf skirt that persists on the main stem of mature plants Reserve, and other conservation areas, is the control and (Bond, 1983). These stands may number hundreds to thousands regulation of fire. However, fires are likely to occur because of of plants with individuals reaching heights of up to 6 m (Van Wyk unplanned events, e.g. arson and lightning strikes, such as in and Smith, 2005; Symes and Nicolson, 2008). Aloe marlothii is mid-September 2003 when a portion (~349 ha) of the western important for numerous opportunistic bird species that utilise its part of the reserve was burned as a possible result of arcing copious dilute nectar (concentration 12% w/w, volume 250 μl/ power lines (D. Koen pers. comm.). During the fire, a section of flower; Symes and Nicolson, 2008) as a source of energy and the aloe stand within the nature reserve was heavily burned water during dry winter periods (Symes et al., 2008; Symes, 2010; (hereafter referred to as the burn area), killing all aloes within an Symes et al., 2011; Oatley, 1964; Oatley and Skead, 1972). area of ~1 ha. In the burn area, dominated post-fire by grass cover and pioneer herbaceous weed growth, the dead stems of hundreds of large aloes (estimated height N4 m) remained. A natural experiment was created whereby dispersal of aloe seeds ⁎ Tel.: + 27 11 717 6423; fax: + 27 11 717 6494. and recolonisation by aloes, in this naturally disturbed burn E-mail address: [email protected]. area, could be monitored. Consequently, seed dispersal and

0254-6299/$ - see front matter © 2011 SAAB. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.sajb.2011.06.008 C.T. Symes / South African Journal of Botany 78 (2012) 276–280 277 germination in A. marlothii from the burn area–aloe stand 2008). During soil sample collection, and while walking margin was investigated by conducting a series of seed bank transects, the area near the sample site (~2 m radius) was germination trials. In addition, the persistence of seeds in the searched for aloe seedlings. seed bank 1 year after flowering was investigated. Each soil sample was then separated on two trays (30× 40×10 cm) with a vermiculite substrate and watered every 2. Materials and methods 2–5 days in a greenhouse (Department of Botany, University of Pretoria) under conditions that have proved successful in 2.1. Study site previous germination of A. marlothii seeds (A. Berger, pers. comm.). Seedlings were counted every 27–53 days in 2005 Field work was conducted in the western section of and in 2006 more routinely every 14 days. All other plants Suikerbosrand Nature Reserve (26°31′50″ S, 28°10′07″ E, were removed from the trays at regular intervals (7–14 days) ~1,600-1,700 m a.s.l.), where hundreds to thousands of to reduce competition with germinating aloe seeds. A. marlothii plants grow, predominantly on north facing slopes. Details of flowering phenology during the study period and 3. Results nectar production in A. marlothii are given in Symes and Nicolson (2008). 3.1. Fruit set and seed production

2.2. Fruit and seed set Mean height (± SD) of aloes measured in fruit and seed set experiments was 2.67±0.71 m (n=40; Short aloesb2.5 m, During September 2006, a single raceme was collected from 2.09±0.24 m; Tall aloesN2.5 m, 3.26±0.50). No flowering 40 separate successfully fruiting aloe plants growing outside of plants were observed with more than one inflorescence. Seed the burn area. Fruiting success was calculated by determining production was correlated with plant height, with taller plants the proportion of flowers on each raceme that developed into producing more seeds (Table 1). The mean number of seeds per fruit. Because flowers are compacted on each raceme and fruit ranged from 52 (in a 2.16 m plant) to 141 (in a 3.88 m difficult to accurately count, the number of flowers on each plant). Calculated seed production ranged from 26,159 (in a raceme was determined by counting the number of pedicel scars 2.16 m plant) to 374,707 (in a 3.56 m plant). The number of on the raceme (Symes et al., 2009). Although I cannot be sure racemes per plant ranged from 3 to 25, the number of flowers that all pedicel scars represented the number of mature flowers per raceme from 77 to 421, and the number of fruits per raceme the size of the pedicel and the compact arrangement of flowers from 51 to 290. The proportion of flowers that produced fruit on the raceme strongly suggest that this method is accurate ranged from 22.8% to 87.3 %. Differences between short aloes (Symes et al., 2009). Plants of various heights were sampled, and tall aloes with respect to flowering characteristics, that and measured with a measuring pole to the nearest cm. The highlight the relationship between plant height and reproductive number of seeds in five fruits on each raceme was counted as output, are shown in Table 1. well as the number of racemes per inflorescence. Seed production in each was then determined as a 3.2. Seed bank experiments product of the mean number of seeds per fruit (determined from the five fruit mentioned above), the mean number of fruit per The highest germination rate occurred in soil samples raceme (n =40) and the total number of racemes per collected closest to the burn area–aloe stand margin in both inflorescence for each plant. years, with a typical negative exponential curve representing seedling emergence in the seed shadow (2005, R²=0.807, 2.3. Seed bank experiments y =16.435e− 0.092x; 2006, R²=0.925, y =38.188e− 0.153x; Table 2). During 2005 and 2006 germination and seedling Soil samples were collected at the burn area during 2005 and emergence continued over a period of three months with more 2006 to investigate seedling emergence (as a measure of seeds germinating close to the burn area–aloe stand margin germination) of aloe seeds in the soil bank (Harper, 1977). In (Fig. 1). In both years combined only one seedling emerged in 2005 soil samples were collected along two transects, 25 m the soil samples collected prior to flowering (Table 2). apart, running from the burn area–aloe stand margin (0 m) into the burn area. At 0, 7 and 25 m, approximately 1–2 kg of the 4. Discussion surface layer (up to 3 cm depth) of loose soil and vegetation litter was collected. Samples were collected in a 1×1 m quadrat The emergence of seedling aloes was recorded in soil prior to seed set (25 September), and after seed dispersal samples collected 25 m from the burn area–aloe stand margin (22 October) in 2005. In 2006 soil samples were collected prior and the seed shadow conformed well to a negative exponential, to seed set (23 September), and after seed dispersal (29 as is assumed for many other plant species (Willson, 1993; November), along three transects, each 25 m apart, at 0, 3, 7, 15 Portnoy and Willson, 1993). In addition, emergence of and 25 m from the burn area–aloe stand margin. The timing of seedlings occurred up to 4 months after sowing. Given the soil sample collections was important because the flowering annual production of large numbers of seeds it was surprising period differed slightly between years (Symes and Nicolson, not to have found any seedling aloes in the burn area during the 278 C.T. Symes / South African Journal of Botany 78 (2012) 276–280

Table 1 Mean values (± SD) related to aloes from which seed set was determined, * showing significant differences in variables for different height classes (Mann– Whitney U-test, Pb0.05). # showing significant correlation of reproductive characteristic and height (Spearman's R, Pb0.05; n=40 flowering plants). Height class UP All aloes RP b2.5 m N2.5 m Percentage fruit set 49.4±15.6 49.8±9.8 188.0 0.745 49.6±12.8 0.406 0.009 # Racemes/inflorescence 8.7±4.6 11.8±4.0 101.5 0.008 * 10.3±4.6 0.307 0.054 Flowers/raceme 260±76 300±59 144.5 0.133 280±70 0.439 0.005 # Fruit/raceme 125±52 151±45 127.0 0.048 * 138±50 0.346 0.029 # Seeds/capsule 84±23 98±23 103.0 0.009 * 91±24 0.004 0.979 Seeds/plant 95,148±73,174 167,549±70,301 74.0 0.001 * 131,348±79,752 0.567 0.000 #

study. This suggests that under natural conditions germination plants each year (Symes and Nicolson, 2008). However, as rates and the survival of seedlings in the long term are extremely mentioned above, no recruitment was observed in the disturbed low for A. marlothii. In the patchy landscape of A. marlothii, area, i.e. burn area. Aloe seeds are soft, with very little where particular conditions, e.g. optimal micro-habitats, may be protective coat (Kamstra, 1971) and may rely on optimal favored for the persistence of populations (Smith et al., 2008), climatic conditions during spring (e.g., rainfall volume and propagation of seeds in the tail of distribution may be rainfall duration) for germination. If they do not germinate particularly important for long distance dispersal beyond core because these conditions are not provided for, then they are populations, i.e. founder populations (Cain et al., 2000). Long unlikely to germinate the following season because of their distance seed dispersal is generally very difficult to directly limited longevity. Although our results suggest that the survival document (Cain et al., 2000). From this study some under- of seeds in the long term is low, in Aloe greatheadii var. standing of finer scale dispersal of seeds is obtained, where the davyana seeds are known to survive in the soil for longer than gradual growth and spread of A. marlothii populations may two seasons (Smith and Correia, 1992). The area where an result from the annual short-distance dispersal of seeds within individual plant grows and is susceptible to fire may have the immediate shadow. However, beyond these distances the implications on its long term survival. In the closely related dispersal of seeds is less clear. succulent Haworthia koelmaniorum (Asphodelaceae) a safe The seeds of A. marlothii are similar in structure to A. ferox germination site (e.g., a rock fissure) is required for the (Kamstra, 1971) and with wind speeds of 20 km h− 1 and a successful growth, recruitment and persistence of a plant mean aloe height of 3.07 m for flowering aloes (n=80; unpubl. (Witkowski and Liston, 1997). The same may apply to data), seed dispersal distance is calculated at ~30 m (Stokes and A. marlothii where recruitment is possibly limited by the Yeaton, 1995). For taller plants (~5 m) in stronger winds availability of optimal growing sites despite abundant seed (40 km h− 1) this may exceed 50 m (Stokes and Yeaton, 1995). production. In addition, there would need to be reduced Taller aloes produced more racemes per inflorescence, and predation (browsing pressure) to enable a slow growing more seeds per seed capsule, and hence had higher overall seed succulent to develop into a mature plant (Shackleton and production, than shorter aloes so reproductive fitness, through Gambiza, 2007). Fire, moisture and temperature have been cited the production of more seeds and dispersal over a greater distance, is enhanced in taller plants. In addition, taller plants flower more frequently allowing them to contribute more seeds for dispersal (Symes and Nicolson, 2008). The recruitment of new plants may therefore be ensured by the production of exceptionally large numbers of seeds from different flowering

Table 2 Total number of germinated Aloe marlothii plants in soil samples collected before seed set and after seed set (2005, n=2 and 2006, n=3 for each distance) at different distances from the burn area–aloe stand margin. Samples were not collected at 3 m and 15 m during 2005. Distance from Pre-dispersal Post-dispersal margin (m) 2005 2006 2005 2006 0 106021 Fig. 1. Accumulative number of Aloe marlothii seeds germinated in seedling 3 – 0 – 18 trays for soil samples collected 0, 3, 7, 15 and 25 m from the burn area–aloe 7 0074 stand margin at Suikerbosrand Nature Reserve. Soil samples were collected after 15 – 0 – 4 dehiscence of fruit capsules. Emerged seedlings were counted at 14-day 250012 intervals from 3 December 2006 (day 0). C.T. Symes / South African Journal of Botany 78 (2012) 276–280 279 as primary factors determining aloe distributions (Jordan, Glen, H.F., Hardy, D.S., 2000. Fascicle 1: Aloaceae (First part): Aloe. In: 1996). These factors, together with optimum micro-habitat Germishuizen, G. (Ed.), Flora of southern Africa, vol. 5. Part 1. National Botanical Institute, Pretoria, pp. 1–167. conditions may be important in regulating and defining the Hargreaves, A.L., Harder, L.D., Johnson, S.D., 2008. Aloe inconspicua: the first persistence of A. marlothii across its range. record of an exclusively insect-pollinated aloe. South African Journal of Most large aloes appear to grow in rocky areas that afford them Botany 74, 606–612. protection from fire (Reynolds, 1969). In the warmer areas of its Harper, J.L., 1977. Population Biology of Plants. Academic Press, London, – range A. marlothii is not necessarily confined to rocky refugia pp. 1 892. Hoffman, M.T., 1988. The pollination ecology of Mill. South African (Bredenkamp and Van Vuuren, 1987). Bond (1983) suggested Journal of Botany 54, 345–350. that the dry leaf skirts of aloes offer protection from fires. 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