Journal of Applied Ecology 2009, 46 , 223���230 doi: 10.1111/j.1365-2664.2008.01595.x �� 2008 The Authors. Journal compilation �� 2008 British Ecological Society Blackwell Publishing Ltd What controls woodland regeneration after elephants have killed the big trees? Stein R. Moe 1 *, Lucas P. Rutina 1,2 , H��kan Hytteborn 3 and Johan T. du Toit 4,5 1 Department of Ecology and Natural Resource Management, Norwegian University of Life Sciences, PO Box 5003, NO-1432, ��s, Norway 2 Department of Wildlife and National Parks, PO 131, Gaborone, Botswana 3 Department of Biology, Norwegian University of Science and Technology, NO-7491 Trondheim, Norway 4 Department of Wildland Resources, Utah State University, 5230 Old Main Hill, Logan, Utah 84322-5230, USA and 5 Mammal Research Institute, Department of Zoology and Entomology, University of Pretoria, Pretoria, South Africa Summary 1. Top-down regulation of ecosystems by large herbivores is a topic of active debate between scientists and managers, and a prime example is the interaction between elephants Loxodonta africana and trees in African savannas. A common assumption among wildlife managers is that a local reduction in elephant numbers will ultimately allow woodland to self-restore to a desired former state. Such regeneration is, however, dependent on the survival of seedlings of impacted tree species. We conducted a field experiment to investigate seedling predation in the elephant- transformed Chobe riparian woodland of northern Botswana. 2. We planted seedling gardens in (i) complete exclosures that excluded all herbivores except small rodents and invertebrates, (ii) semi-permeable exclosures that excluded ungulates but included primates, lagomorphs, all rodents, gallinaceous birds, etc, and (iii) completely open plots. Seedlings were of two tree species decreasing in the area ( Faidherbia albida and Garcinia livingstonei ) and two that are increasing ( Combretum mossambicense and Croton megalobotrys ). 3. After 9 months, seedling survival ranged from 75% for all species in the complete exclosure to 20% for Faidherbia albida in the open plots. Survival of all seedlings except C. megalobotrys declined precipitously in open plots during the dry season when invertebrates are largely dormant but when impalas Aepyceros melampus (locally abundant ungulates) increase the browse components of their diets. 4. Seedling survival in the open plots was negatively related to local impala density but unrelated to that of any other browser. 5. Synthesis and applications . Our findings relate to the current debate about managing elephants to restore southern African savanna landscapes to desired historical states. Various seedling predators, including the ubiquitous impala Aepyceros melampus , regulate the regeneration of trees from seedlings, and our experiments support the hypothesis that tall closed-canopy woodlands originate during episodic windows of opportunity for seedling survival. To artificially recreate such a window would require the decimation of seedling predators as well as elephants, which is impractical at the landscape scale. Key-words: African savanna, browsing, impala, forest dynamics, seedling predation Introduction Savanna systems are characterized by a mixture of trees and grasses where the relative dominance of woody cover is determined by abiotic factors like water (Amundson, Ali & Belsky 1995), nutrients (Walker & Langridge 1997) and fire (Trollope 1984), and biotic factors like herbivory (Scholes & Archer 1996). However, when high densities of ungulates consume large proportions of the biomass, fire becomes less important in determining the balance between wood- land and grassland (McNaughton, Ruess & Seagle 1988). African elephants Loxodonta africana Blumenbach are usually regarded as the main factor determining savanna woody cover, because of its very large body size enabling *Correspondence author. E-mail: stein.moe@umb.no

224 S. R. Moe et al. �� 2008 The Authors. Journal compilation �� 2008 British Ecological Society, Journal of Applied Ecology , 46 , 223���230 elephants to kill mature trees (Owen-Smith 1988 Dublin 1995). However, the local persistence of woody species is not only dependent on the survival of mature individuals, but also on recruitment from germinating seedlings. A recent study from East Africa has shown that elephants exert minimal browsing damage to acacias in smaller size classes ( 2��5 m) (Augustine & McNaughton 2004), yet low recruitment of the seedlings of certain woody species is a major factor affecting the structure and composition of African savanna woodlands (e.g. Laws 1970 Pellew 1984 Dublin, Sinclair & McGlade 1990 Ruess and Halter 1990). While elephants generally browse on trees, ungulates commonly select seedlings (Hobbs 1996 Augustine & McNaughton 1998) because they are more palatable than older plants (Crawley 1983), and browsing by medium-sized ungulates has been suggested as the controller of woodland regeneration in East African savannas (e.g. Belsky 1984 Mwalyosi 1990 Prins and van der Jeugd 1993 Sinclair 1995). In Serengeti National Park, Tanzania, Belsky (1984) found that browsing antelopes such as impala Aepyceros melampus Lichtenstein, Grant���s gazelle Gazella granti Brooke, Thomson���s gazelle G. thomsoni G��nther, eland Taurotragus oryx Pallas and dikdik Madoqua kirkii G��nther controlled woody plants 1 m in height. Prins & van der Jeugd (1993) showed that even-aged stands of acacia woodland observed in Lake Manyara National Park, Tanzania, were established during years of low impala populations. While previous studies have debated the effects of elephants and smaller ungulates on woody cover, recent experimental studies have pointed to invertebrates (Shaw, Keesing & Ostfeld 2002) and rodents (Goheen et al . 2004) as important acacia seedling predators in central Kenya. Indeed, Goheen et al . (2004) found that the net seedling survival was approximately twice as high in areas where large mammals were present compared to excluded areas in central Kenya, which is clearly contrary to the findings of other studies. These increases in seedling survival in areas with large mammals were attributed to the increase of rodents and invertebrates in plots excluding large mammals (Goheen et al . 2004). The riparian habitat of the Chobe riverfront (Chobe National Park, northern Botswana) has been gradually fragmented by elephants over the past half century. At present, only isolated remnants of the once continuous belt of tall mature trees remain (Mosugelo et al . 2002). The previously dominant riparian species are disappearing and being replaced by previously minor species (Simpson 1975 Moroka 1984 Rutina 2004). A well-developed continuous belt of tall mixed gallery woodland previously dominated by what are now ���decreasers��� ��� Faidherbia albida (Delile) A. Chev., Garcinia livingstonei T. Anderson, Diospyros mespiliformis Hochst. ex A.DC, Combretum imberbe Wawra, Acacia nigrescens Oliv., A. tortilis (Forssk.) Hayne and Philenoptera violacea (Klotze) Schrire (Child 1968) ��� has been replaced by shrubs and thickets dominated by what are now ���increasers��� ��� Croton megalobotrys Pax , Capparis tomentosa Lam., and Combretum mossambicense (Klotzsch) Engl. (Simpson 1975, 1978 Sommerlatte 1976 Moroka 1984 Addy 1993). Most of the decreasers show little signs of regeneration over the past 30���40 years (Sommerlatte 1976 Moroka 1984 Rutina 2004), suggesting either lack of germinable seeds or low seedling survival. The Chobe River represents the only permanent supply of drinking water for wildlife in 10 000 km 2 of dystrophic savanna, with the result that exceptionally high ungulate biomass densities occur in and around the Chobe floodplain in the dry season (Skarpe et al . 2004). With the locally high ungulate biomass, caused by the attraction of drinking water, there is a sparse herbaceous layer, and consequently, the fire frequency is low (Skarpe et al . 2004), which suggests the lack of regeneration by decreasers is not attributable to fire (cf. Dublin, Sinclair & McGlade 1990). Elephants have increased at 6% per annum in this area since 1987 (DWNP 1997 Gibson, Craig & Masogo 1998), and because it is well known that elephants can change mature woodland into shrubland and grassland (Caughley 1976 Dublin, Sinclair & McGlade 1990 Cumming et al . 1997), previous studies in Chobe have focused on elephants as the main agent of change (Child 1968 Simpson 1975, 1978 Sommerlatte 1976 Moroka 1984 Mosugelo et al . 2002). However, while elephants have probably been the main cause of mortality in mature trees, a high elephant population does not explain the virtual absence of seedlings of decreasers. This is supported by a previous study in Chobe that found elephants to browse predominantly in the 1���3 m height zone, which is well above the level of seedlings (Stokke and du Toit 2000). Apart from elephants, most other ungulate populations have been either declining or stable along the Chobe Riverfront during the past decades (DWNP 1997). One exception is the impala population that has increased substantially since the 1960s (Sheppe & Haas 1976 Rutina 2004), and some previous studies have either suggested (e.g. Prins & Van Der Jeugd 1993) or experimentally shown (Sharam, Sinclair & Turkington 2006) that browsing antelopes are important regulators of woodland regeneration. In view of the previously contradictory findings on the effects of large mammals on seedling survival, we aimed to investigate the impact of seedling predation on woody plant regeneration along the Chobe riverfront. In addition to identifying the main herbivores involved in seedling predation, we also tested whether seedling predation was higher on those woody species decreasing than on those increasing in abundance in woodlands heavily impacted by elephants. In essence, our study examined the reversibility of an elephant-driven shift in woody plant community structure in an ecosystem characterized by low fire frequency but high seedling predation. Materials and methods STUDY AREA The study was conducted within Chobe National Park in northern Botswana. The study area was a 20-km strip (~40���70 m wide) along the southern bank of the Chobe River. The study area is part of the vast (2��5 million ha) nutrient-poor Kalahari sand system extending