is there a ‘browse trap’? dynamics of herbivore impacts on trees and grasses in an african...

Is there a ‘browse trap’? Dynamics of herbivoreimpacts on trees and grasses in an African savannaAnn Carla Staver1* and William J. Bond2

1Department of Ecology, Evolution, and Environmental Biology, Columbia University, New York, NY 10027, USA; and2Botany Department, University of Cape Town, Private Bag X1, Rondebosch 7701, South Africa

Summary

1. Despite widespread acknowledgement that large mammal herbivory can strongly affect vegetationstructure in savanna, we still lack a theoretical and practical understanding of savanna dynamics inresponse to herbivory.2. Like fire, browsing may impose height-structured recruitment limitations on trees (i.e. a ‘browsetrap’), but the demographics of herbivore effects have rarely been considered explicitly. Evidencethat cohorts of trees in savannas may establish during herbivore population crashes and persist longterm in savanna landscapes is anecdotal.3. Here, we use an experimental approach in Hluhluwe iMfolozi Park in South Africa, examiningthe response of grass biomass and tree populations to 10 years of graduated herbivore exclusion,and their subsequent response when exclosures were removed.4. We found that grazer exclusion increased grass biomass and that, despite presumable increases infire intensity and grass competition, herbivore – especially mesoherbivore, including impala andnyala – exclusion resulted in increases in tree size. After herbivore reintroduction, grazers reducedgrass biomass over short time-scales, but tree release from browsing persisted, regardless of treesize.5. Synthesis. This work provides the first experimental evidence that release from browsing trumpsgrazer–grass–fire interactions to result in increases in tree size that persist even after browser reintro-duction. Escape from the ‘browse trap’ may be incremental and not strictly episodic, but, overlonger time-scales, reductions in browsing pressure may lead to tree establishment events in savannathat persist even during periods of intense browsing. Explicitly considering the temporal demo-graphic effects of browsing will be the key for a much-needed evaluation of the potential globalextent of herbivore impacts in savanna.

Key-words: browse trap, browsing, demographic variability, elephant, grass, herbivory, largemammal, plant–herbivore interactions, savanna, tree

Introduction

The dynamics of mammal herbivore impacts on trees in sav-annas remain the most poorly understood driver of savannavegetation structure, despite extensive localized evidence thatthe impacts of herbivores can be substantial (Prins & van derJeugd 1993; Barnes 2001; Augustine & McNaughton 2004;Cot�e et al. 2004; Sharam, Sinclair & Turkington 2006; Forn-ara & Du Toit 2007; Asner et al. 2009; Holdo et al. 2009;Staver et al. 2009; Moncrieff et al. 2011). Savannas areunderstood to be systems where top-down impacts can havemajor effects on both tree distributions and structure (Bond

2008). Impacts of fire have received extensive attention interms of underlying dynamics (Higgins, Bond & Trollope2000), demographics (Trollope & Tainton 1986; Hoffmann1999; Hanan et al. 2008; Hoffmann et al. 2009; Werner &Prior 2013) and global impact (Bond, Woodward & Midgley2005; Lehmann et al. 2011; Staver, Archibald & Levin2011a,b). As a result, a fundamental theoretical and practicalunderstanding of the role of fire in savanna systems is welladvanced. By contrast, an equivalent understanding of thedynamics and demographics of herbivore impacts in savannais mostly lacking.In many respects, a comprehensive understanding of her-

bivory presents challenges that fire does not. First, herbivoryis comprised of both grazing and browsing; grazing isexpected to increase tree growth rates, either because of*Correspondence author. E-mail: [email protected]

© 2014 The Authors. Journal of Ecology © 2014 British Ecological Society

Journal of Ecology 2014, 102, 595–602 doi: 10.1111/1365-2745.12230

decreased grass competition or decreased fire frequency(Knapp et al. 1999; Archibald et al. 2005; Holdo et al.2009), while browsing is expected to directly decrease treegrowth (Barnes 2001; Sharam, Sinclair & Turkington 2006;Staver et al. 2009). In addition, herbivore communities arevaried and often diverse (Olff, Ritchie & Prins 2002), anddominant herbivore impacts may depend on what herbivoresare present (Prins & van der Jeugd 1993; Barnes 2001; Wil-son & Kerley 2003; Augustine & McNaughton 2004; Cot�eet al. 2004; Sharam, Sinclair & Turkington 2006; Fornara &Du Toit 2007; Asner et al. 2009; Holdo et al. 2009; Staveret al. 2009; Midgley, Lawes & Chamaill�e-Jammes 2010;Moncrieff et al. 2011). A focus on elephant impacts in themodelling literature especially (Dublin, Sinclair & McGlade1990; Baxter & Getz 2005; Bond 2008) may not be relevantto understanding the effects of a diverse browser communityin Africa and especially elsewhere. However, a predictivesynthesis should be possible.Here, we focus especially on the demographic structure of

herbivore impacts on the tree layer in an African savanna. Inthe case of fire, height structure – partly mediated by stemdiameter and bark thickness – is fundamentally important indetermining how trees respond to persistent disturbances(Trollope & Tainton 1986; Hoffmann 1999; Higgins, Bond &Trollope 2000; Prior, Williams & Bowman 2010; Wakeling,Cramer & Bond 2010); the vertical zone of influence ofsavanna fires is known as the ‘fire trap’, above which fireminimally affects trees (Bell 1984). Two lines of evidencesuggest that a similar model – a ‘browse trap’ – may be use-ful in conceptualizing browsing effects as well. First of all,the frequent occurrence of browse lines in areas with highbrowser density suggests that herbivore effects are heightstructured and that trees below some threshold size are sup-pressed by herbivores (Trollope & Tainton 1986; Hoffmann1999; Bond & Loffell 2001; Palmer & Truscott 2003; Hoff-mann et al. 2009; Moncrieff et al. 2011). Secondly, historicalanalyses, including pollen analyses and long-term tree ringstudies, have suggested that cohorts of trees in savannas mayarise after historical herbivore populations crashes (Prins &van der Jeugd 1993; Bond, Woodward & Midgley 2005; Gill-son 2006; Holdo et al. 2009; Lehmann et al. 2011; Staver,Archibald & Levin 2011a,b; Staver, Bond & February 2011);the strong implication of these apparent release episodes isthat trees reach some size at which they become substantiallyless vulnerable to the negative effects of browsing.Here, we take advantage of a series of graduated herbivore

exclosures in Hluhluwe iMfolozi Park in South Africa (Knappet al. 1999; Archibald et al. 2005; Holdo et al. 2009; Staveret al. 2009), which ran for 10 years and were subsequentlyremoved, to examine (i) the effects of a diverse assemblageof browsers on tree population structure and growth withinsavanna and (ii) the extent to which the effects of herbivoreremoval – and, by proxy, herbivore population crashes – arereversible or can result in long-term, persistent changes insavanna vegetation structure. These perspectives provide adirect experimental evaluation – albeit over shorter, experi-mental time-scales – of whether browsing impacts on trees in

savanna follow a ‘browse trap’ model. The data provide abasis for developing a theoretical framework for analysing theeffects of browsing in particular and, more broadly, mammalherbivory effects on the structure of savanna ecosystems.

Materials and methods

STUDY SITE

Hluhluwe iMfolozi Park (900 km2; 28o000–28o260 S; 31o430–32o090

E), in KwaZulu Natal, South Africa, spans a diversity of savannas –

from mesic systems at the boundary with forest to semi-arid ones.Rainfall is linked to elevation, resulting in a gradient between higherelevation Hluhluwe Game Reserve (975 mm mean annual rainfall)and lower elevation iMfolozi GR (<600 mm MAR). Fire frequencyin the park increases with rainfall; areas of high fire frequency haveburned more than 10 times between 1956 and 1996, while areas oflow fire frequency burned as little as once during the same period(Barnes 2001; Balfour & Howison 2002; Sharam, Sinclair & Tur-kington 2006; Staver et al. 2009). The park is home to a full com-plement of large mammals indigenous to south-eastern Africa. Largemammal herbivore densities within and between reserves varydepending on herbivore habitat preferences. Based on 2004 censusdata, impala (Aepyceros melampus) are the most numerous herbivorein the park, occurring with higher densities in semi-arid iMfolozi(36 km�2) than in mesic Hluhluwe (24 km�2); white rhino (Cerato-therium simum) make up the largest biomass in the park, occurringwith higher densities in iMfolozi (2.5 km�2) than Hluhluwe(1.8 km�2). Elephants move freely between parks and have biomassroughly equivalent to impala (0.36 km�2; 10.9 kg ha�1). Herbivoredensities have fluctuated substantially during the past century inHluhluwe iMfolozi Park, largely due to hunting, the rinderpest epi-demic and culling campaigns during the early part of the 20th cen-tury associated with efforts to eradicate the nagana livestock disease.Herbivore densities have been more stable in the last two decadeswith high herbivore biomass (~12 500 kg km�2 in 2004) [seeCromsigt, Prins & Olff (2009) and Staver et al. (2009) for moreinformation on herbivore populations].

EXPERIMENTAL SET-UP

Experimental herbivore exclosures were established at 10 sites,located throughout Hluhluwe iMfolozi Park in a range of savannatypes, from grazing lawns with high herbivore pressure and low firefrequency to bunchgrass savannas with low herbivore pressure andhigh fire frequency [see Staver et al. (2009) for additional detail]. Ateach site, three treatment plots of 40 m 9 40 m were established in1999: a control (all herbivores = ‘+ all’) allowed access to all herbi-vores, a cable set 70 cm above the ground excluded rhinos (rhinofence = ‘�rhino’) and a standard game fence 2.5 m high thatexcluded hares and all larger herbivores (total exclosure = ‘�all’).Two additional treatments were established at each of the five Hluh-luwe sites in 2000: double cables set at 70 and 120 cm above theground excluded zebras and larger herbivores (zebra fence =

‘�zebra’) and an inverted standard game fence (i.e. the small mesh atthe top, instead of the bottom) 2.5 m high that excluded impala andlarger herbivores (impala fence = ‘�impala’).

The effectiveness of herbivore exclusion treatments was validatedvia monthly dung counts over the full course of the experiment,showing that exclosures were largely effective (Table 1 and Fig. 1)and gradually excluded herbivore species. The rhino fence resulted in

© 2014 The Authors. Journal of Ecology © 2014 British Ecological Society, Journal of Ecology, 102, 595–602

596 A. C. Staver & W. J. Bond

major decreases in use by large (elephant, giraffe and buffalo) andless agile (zebra) herbivores; the zebra fence reduced use by slightlysmaller herbivores (wildebeest); the impala fence effectively reduceduse by medium-bodied browsers especially (impala and nyala but alsowarthog). Only the total exclosure (‘�all’) completely excluded herbi-vores of any type, however, and reduced herbivore visitation to zeroor nearly zero (see Fig. 1).

All sites were burned during the dry seasons after the 2000, 2002,2004 and 2008 censuses. To minimize the attraction of a small burntpatch to herbivores, burns were timed to coincide with managementburns in the blocks (500 ha+) containing sites. Sites and treatmentsthat sustained high grass biomass burnt readily, while heavily grazedareas often did not burn. At all sites, the complete exclosure treatmentgenerated sufficient grass biomass to burn the whole plot. Thus, com-plete herbivore exclusion was always associated with exposure of sap-lings to fire.

Experimental treatments remained in place from 1999/2000 throughto the end of 2009, when exclosures were removed (barring those atone site in Hluhluwe and one site in iMfolozi). Trees were mapped in2000 onto a permanent 2 m 9 2 m grid that covered half of eachplot (i.e. an area of 40 m 9 20 m) and their heights measured everyyear (except those in ‘�impala’ and ‘�zebra’ plots in 2000 and2005); new trees were recorded during each census and tracked there-after. Tree species and heights were re-recorded in 2012 3 years afterexclosure removal; because the permanent grid was removed with ex-closures, relocating individual trees was impossible, but plots wererelocated exactly and censused. Grass biomass was estimated at eachpoint on the permanent grid using a disc pasture meter with region-specific calibrations from grass biomass estimated from clipping

(Waldram, Bond & Stock 2008) from 2000 to 2009 and as nearly aspossible in 2012.

DATA ANALYSIS

All statistics were performed in R 2.15.1 using the base statisticalpackage and the package ‘nlme’ (Pinheiro et al. 2012). Because ex-closure treatments were nested within sites and each plot was sampledrepeatedly, we analysed data using mixed-effects modelling, withregion (i.e. Hluhluwe v. iMfolozi), exclosure treatment, exclosureremoval and fire presence/absence as fixed effects and year, site andplot within site as random effects.

Results

Grass biomass increased strongly with herbivore exclusion inboth mesic Hluhluwe and semi-arid iMfolozi (Fig. 2 andTable 1). In Hluhluwe, the exclusion of rhinos and of impalaappeared to result in the biggest responses, while in iMfolozi,rhino exclusion had insignificant effects on grass biomass. Inneither reserve did fire have any significant effect on grassbiomass 1 year after the fire (Table 1), indicating that therecovery of grass biomass following a fire is rapid. Similarly,after reintroduction of herbivores with the removal of exclo-sures, the effects of exclusion were completely reversed; by2012, exclusion plots had grass biomass identical to that ofcontrols (Fig. 2 and Table 1). Thus, the grass layer appears to

Table 1. Results of linear mixed model analyses of the effects of herbivore exclusion, herbivore reintroduction, and fire on grass biomass, treeheight, and tree population structure across Hluhluwe and iMfolozi Game Reserves

Factor F d.f. P AIC

Dung abundance Region 1.51 8 0.231 4889Exclusion 10.5 26 <0.001Reintroduction* 2.9 376 0.1532Fire 20.9 376 <0.001

Grass biomass Region 2.14 8 0.181 5155Exclusion 16.86 26 <0.001Reintroduction 115.87 376 <0.001Fire 3.16 376 0.076

Plot-level mean tree height Region 4.87 8 0.058 3840Exclusion 8.29 26 <0.001Reintroduction 2.97 376 0.086Fire 32.12 376 <0.001

Proportion with height ≤ 1 m† Region 41.65 8 <0.001 �356Exclusion: +/� impala 32.36 29 <0.001Reintroduction 1.77 376 0.18Fire 35.88 376 <0.001

Proportion with 1 m < ht ≤ 2 m† Region 60.01 8 <0.001 �503Exclusion: +/� impala 40.74 29 <0.001Reintroduction 1.30 376 0.26Fire 38.70 376 <0.001

Proportion with height > 2 m†‡ Exclusion: +/� impala 6.39 29 0.017 �1418Reintroduction 1.61 376 0.21Fire 7.24 376 0.007

*Dung counts are not numerically comparable before and after herbivore reintroduction, because the temporal density of sampling differed sub-stantially.†Model did not converge when all exclusion treatments were included. On the basis of tree height analyses and Fig. 4, we reduced the treatmentlevels to two: either impala were present (in +all, �rhino and �zebra treatments) or they were absent (in �impala and �all treatments).‡Model did not converge even with fewer exclusion levels, probably because of insufficient replication, but did when the Hluhluwe v. iMfoloziGR contrast was excluded from the analysis.


Evaluating the ‘browse trap’ 597

respond reversibly and on short time-scales to the effects bothof fire and herbivory.Tree height (Fig. 3) and tree population structure (Fig. 4)

likewise responded strongly to herbivore exclusion (Table 1).In Hluhluwe, impala appeared to be the key herbivores whoseexclusion released trees; responses in iMfolozi were also con-sistent with the importance of impala, although the full rangeof treatments was not applied there. Fire clearly negativelyaffected tree height and tree population structure one yearafter the fire (Fig. 4 and Table 1), but the effects of fire didnot increase as grazer exclusion increased grass biomass. Bycontrast, mixed-effects models of tree density on exclosuretreatment, reintroduction and fire did not converge, suggestingthat tree density was not consistently affected either by herbi-vore exclusion or fire.The release of trees with herbivore exclusion was not

reversed when herbivores were reintroduced following exclo-sure removal (Figs 3 and 4; Table 1). However, mean treeheight did not continue to increase either, and tree size classdistributions were static (Fig. 4). This suggests that trees didnot experience ‘release’ from herbivory at some large size;had large trees escaped herbivory and continued to grow,mean tree height would have continued to increase or, atleast, continued growth of large trees would have been coun-tered by decreases in small tree size.Although elephant damage was visually very apparent, only

two plots – located at the same site, Nombali – experiencedany substantial degree of elephant damage after exclosures

were removed; the remainder of plots experienced elephantdamage ranging from mild to severe to 10% or fewer of trees(Fig. 5a). Even in the two plots that experienced substantialelephant damage, however, the release of trees into larger sizeclasses was not reversed when herbivores were reintroduced(Fig. 5b), suggesting that elephants, though certainly capableof reversing the effects of tree release from browsing pres-sures, do not necessarily do so, at least over short time-scalesand at the densities in which they occur in Hluhluwe iMfoloziPark [see also (Guldemond & Van Aarde 2008)].

Discussion

These results suggest (i) that release from grazing can havestrong effects on grass biomass, but reduction in grass bio-mass following grazer reintroduction is rapid, (ii) that releasefrom browsing – especially by mesoherbivores, includingimpala and nyala – strongly promotes tree growth and (iii)that the effects of release from browsing on trees are stable,at least over relatively short time-scales following browserreintroduction. Large-bodied grazers did affect grass biomass,especially in mesic Hluhluwe, where the formation of grazinglawns is thought to be a direct result of megaherbivory (Wal-dram, Bond & Stock 2008) [see also (Knapp et al. 1999)].By contrast, suppression of tree growth occurred primarily asa result of browsing by small mesoherbivores such as impala

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Fig. 1. Dung abundance response (per year, log scale) to herbivoreexclusion, in mesic Hluhluwe and semi-arid iMfolozi GRs (a and b,respectively). Herbivore species denoted with solid shapes and lightgrey lines (warthog, zebra, wildebeest and buffalo) are predominantlygrazers, those with hollow shapes and black short dashes (nyala, gir-affe) are predominantly browsers, and those with hollow squares anddark grey long dashes (impala, elephant) are mixed feeders. Weadded one to all dung counts to facilitate plotting on a log scale.

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and nyala (Sharam, Sinclair & Turkington 2006; O’Kaneet al. 2012), but, at least over relatively short time-scales,these small-bodied browsers were not able to reverse gains intree height that resulted from a release from browsing pres-sure (Prins & van der Jeugd 1993; Barnes 2001; Holdo et al.2009); not even intensive effects of elephants could reversethe effects of a decade of release from smaller herbivores.Nonetheless, the reintroduction of herbivores did prevent fur-ther tree growth, suggesting that size-structured escape frombrowsing may not occur until trees are very large (in the pres-ence of giraffe (Moncrieff et al. 2011) documented releasefrom herbivory only above about 6–7 m in height), such thatescape from browser effects is a long time-scale process.

TREE LAYER DYNAMICS IN SAVANNA

The experimental response of tree growth to herbivory, herbi-vore exclusion and fire provides insights into how tree coveremerges in real savanna landscapes. First of all, the primaryeffect of herbivore exclusion on tree growth and populationstructure resulted from browser exclusion. Grazer exclusionclearly affected grass biomass, which should, in theory, inten-sify both tree–grass competition and fire effects on trees(Holdo et al. 2009; Riginos 2009; Cramer, van Cauter &

Bond 2010; February et al. 2013). However, even thoughfire–grazer interactions have been documented in the area(Archibald et al. 2005), the effects of browser release on treeperformance were far more substantial than the effects ofgrazers on tree–grass interactions. The potential for directbrowser impacts on tree emergence in savanna suggests thatthese deserve substantially more widespread attention.Results also provide some insights into the potential long-

term temporal dynamics of tree emergence in this savanna.Extant browsing regimes, either alone (in semi-arid iMfolozi)or in combination with extant fire regimes (in mesic Hluh-luwe), completely prevented large tree establishment. This isat odds with the fact that the park is characterized by savannawoodland and even thicket in some places. However, whenboth mesoherbivore browsing (in ‘−impala’ or ‘−all’ treat-ments) and fire were absent (from 2004 to 2008), recruitmentwas substantial (Staver et al. 2009). This suggests that, whenextant adult trees in the landscape established, the consumerenvironment was much different than it is now (Staver, Bond& February 2011), either because herbivore populations andfire management were historically radically different than now(Staver, Bond & February 2011) or because these vary natu-rally (Young 1994; Holdo et al. 2009), such that adult treeestablishment will continue to occur episodically. In theabsence of longer-term data, determining whether savannas intheir current form represent a historical anomaly, are subjectto continuous change or can be expected to persist into thefuture will be impossible.Although the combination of frequent fires and herbivory

appeared sufficient to prevent tree growth in mesic areas, treesize class distributions were undoubtedly more dynamic inresponse to both fire and herbivory than they were in semi-arid areas. This is consistent with the observation that bushencroachment in South Africa, partly driven by increases in[CO2], appears to be proceeding more quickly in mesic thanin arid savannas (Buitenwerf et al. 2011). Even minimal vari-ation in interfire interval might be sufficient to allow trees torecruit in mesic Hluhluwe, especially in areas where suppres-sion of tree growth by browsing is mild. Indeed, although thistrend remains undocumented, bush encroachment appears tobe rampant in the mesic end of Hluhluwe iMfolozi Park inthe last decade, possibly tied in with changes in fire manage-ment and reductions in mesoherbivore populations.

THE ‘BROWSE TRAP ’

The idea of a disturbance ‘trap’ is one that is well-establishedin the case of fire, whose effects in savannas are highly lifestage specific (Bell 1984). Fire limits tree cover in savannaby preventing the recruitment of saplings into trees, butsavanna saplings are usually robust resprouters (Bond &Midgley 2001; Hoffmann et al. 2009). Trees >2–3 m inheight are rarely affected by fire (Hoffmann & Solbrig 2003;Prior, Williams & Bowman 2010), such that fire affects theestablishment, rather than the mortality, of savanna trees. Thisphenomenon is repeatable and shows up clearly in this studyin the fact that population structure under 2 m in height is

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Fig. 3. Plot-level mean tree height response to 10 years of herbivoreexclusion and 3 subsequent years of no fences, in mesic Hluhluweand semi-arid iMfolozi GRs (a and b, respectively).



much more sensitive to fire than population structure over2 m (although fires were sometimes intense and did affectlarge trees as well). This means that, from a theoretical per-spective, the effects of fire in savanna systems lend them-selves to stage-structured modelling: saplings are affected byfire, but trees are not (Higgins, Bond & Trollope 2000; Hananet al. 2008; Staver & Levin 2012).An analogous dynamic understanding of the effects of her-

bivory on savanna systems has so far been elusive, althoughherbivory and fire are in several respects analogous processes(Bond & Keeley 2005). Large tree recruitment may heavilydepend on episodic reductions in browsing pressure allowing

the release of large numbers of juvenile trees in savanna land-scapes (Prins & van der Jeugd 1993; Holdo et al. 2009; Sta-ver et al. 2009). In such circumstances, a ‘browse trap’ maybe a useful way of thinking about the effects of browsing insavannas. However, it is also clear that a dynamic model forthe ‘browse trap’ must be very different than that for the ‘firetrap.’ First, the temporal dynamics of the two are different, inthat fire constitutes an episodic – if chronic – disturbance insavannas, while herbivory is relatively continuous at the pop-ulation level; in the case of herbivory, it is likely release fromdisturbance, rather than the disturbance itself, that is episodic(Young 1994; Holdo et al. 2009).

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Fig. 4. Response of size class distribution to herbivore exclusion and subsequent reintroduction (fence removal is denoted by the vertical greyline). In mesic Hluhluwe and semi-arid iMfolozi GRs, respectively, the proportion of trees with height ≤1 m (a and d) generally decreasesthrough time, while the proportion of trees with height >1 m and ≤2 m (b and e) and with height >2 m (c and f) increases.

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Fig. 5. Rates of elephant damage after treatment removal (in 2012) across all sites and treatments (a), and the temporal response of tree size classdistributions in the two plots most heavily impacted by elephants (b). In (a), sites are listed in the same order for each treatment; the two mostheavily impacted come from the same site. Fences were removed in 2009, 3 years prior to sampling, and rates of damage represent totals acrossall 3 years.



However, the results of herbivore exclusion (release) fol-lowed by herbivore reintroduction in this study suggestanother major difference: browser reintroduction did not read-ily reverse gains in tree height that resulted from browsingrelease. Although the time-scale considered was relativelyshort, this does suggest that fire decreases the size of treeswithin the ‘fire trap’ much more readily than browsing doeswithin the ‘browse trap.’ We did not explicitly consider themechanism that might drive this response, but it is consistentwith browsing that removes buds, foliage and twigs up to amaximum size depending on type of browser (Wilson & Ker-ley 2003), thereby preventing tree growth but not reducingtree size (Midgley, Lawes & Chamaill�e-Jammes 2010). How-ever, regardless of whether increases in tree size from browserrelease are actually irreversible or are only relatively robust,tree establishment may thus proceed episodically – as in thecase of rinderpest or nagana outbreaks (Prins & van der Jeugd1993) – or even incrementally, since smaller release episodesmay accumulate if they occur repeatedly and are not readilyreversed. Theoretically, browsing by medium-sized herbivoresshould be formalized as affecting the establishment rate butnot the mortality of trees and/or as potentially reducing theirgrowth to zero but not less than zero.In considering adult tree establishment, including explicit

stage structure may be much less critical in browsing modelsthan it is in fire models. However, these data examine primar-ily trees that are much smaller than potential ‘escape height’from browsers; studies considering larger trees have suggestedthat the effects of browsing are stage structured (Bond & Lof-fell 2001; Moncrieff et al. 2011). Stage structure may alsononetheless be of critical importance in models that considerreproduction or even the effects of browsers on carbon stor-age in savanna systems (Holdo et al. 2009; Moncrieff et al.2011; Tanentzap & Coomes 2011).These key assumptions are not expected to hold true for

browsing that removes more than just buds and foliage, mostnotably for browsing by elephants, which can decrease treesize substantially when densities are high (Dublin, Sinclair &McGlade 1990; Barnes 2001; Baxter & Getz 2005). However,our results also suggest a note of caution in focusing soexclusively on the effects of elephants on the tree layer insavanna: in the continuous presence of high densities ofimpala and nyala, large trees simply do not establish. Theylimit large tree densities as much as or more than elephants,even if their effects are less visible. Here, elephants had littleeffect on tree growth during herbivore exclusion and (at leastin relatively open woodland and over short time-scales) couldnot reverse gains in tree size resulting from the exclusion ofsmaller browsers. A comprehensive analysis of the effects ofherbivores on savanna structure needs to move beyond ele-phants as the key browser.Herbivory – especially browsing – has clear local impacts

on the tree layer in savanna systems, especially in interactionwith fire. Fire has a demonstrable continental-scale impact onthe distribution of savanna (Bond, Woodward & Midgley2005; Lehmann et al. 2011; Staver, Archibald & Levin2011a,b), but the potentially comparable impact of herbivory

on savanna distributions has never been evaluated, in largepart because an appropriate global herbivory data set is lack-ing. At a minimum, browsing impacts on tree growth mayimpact the potential global role of fire (Wakeling, Staver &Bond 2011). However, browsing also plays a role indepen-dent of that of fire, especially in more arid systems, wherebrowsing is known to exert strong adaptive pressures on trees(Staver et al. 2012). These effects may be as fundamental asthose of fire; herbivory is thought to introduce bistability inecosystem structure (McNaughton 1984; Fornara & Du Toit2007) and radically affect ecosystem carbon stocks (Holdoet al. 2009; Tanentzap & Coomes 2011).The global extent of these impacts merits direct evaluation.

This analysis faces challenges: a diversity of herbivores thatshapes and is shaped by the environment (Olff, Ritchie &Prins 2002), impacts that depend on herbivore densities (Gul-demond & Van Aarde 2008) and the importance of temporalvariability in herbivore pressure (Prins & van der Jeugd 1993;Holdo et al. 2009). Here, we provide some key insights intothe demography and dynamics of herbivore impacts insavanna ecosystems that contribute to making such a synthe-sis possible.

Acknowledgements

We thank Hluhluwe iMfolozi Park and Ezemvelo KZN Wildlife for their sup-port and Phumlani Zwane, Sue Janse van Rensburg, An van Cauter, JuliaWakeling, Matt Waldram, Krissie Clarke, Zanele Chonco, Mendi Shelembe, Si-pho Zulu, Eric Khumalo, Vincent Mkhwanazi and Dumisani Mnomezulu forlogistical fieldwork support. This work forms a part of the Zululand Grass Pro-ject, the Zululand Tree Project and the Biome Boundaries Project. Funding wasprovided by the Andrew W. Mellon Foundation and the National ResearchFoundation of South Africa.

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Received 10 December 2013; accepted 17 February 2014Handling Editor: Amy Austin



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