Oecologia DOI 10.1007/s00442-013-2864-8
Concepts, Reviews and Syntheses
Generalities in grazing and browsing ecology: using across‑guild comparisons to control contingencies Johan T. du Toit · Han Olff
Received: 11 June 2013 / Accepted: 11 December 2013 © Springer-Verlag Berlin Heidelberg 2014
Abstract In community ecology, broad-scale spatial replication can accommodate contingencies in patterns within species groups, but contingencies in processes across species groups remain problematic. Here, based on a focused review of grazing and browsing by large mammals, we use one trophic guild as a “control” for the other to identify generalities that are not contingent upon specific consumerresource interactions. An example of such a generality is the Jarman–Bell principle, which explains how allometries of metabolism and digestion influence dietary tolerance and thereby enable resource partitioning within both guilds at multiple scales. By comparing the grazing succession with browsing stratification we show how competition from smaller herbivores, rather than facilitation from larger ones, is the underlying process structuring ungulate assemblages when shared resources become limiting. Also, grazing lawns and browsing hedges are functionally similar. In each case, plants expressing tolerance traits can withstand chronic grazing or browsing in sites where the nutritive value of the local food resource is enhanced in positive feedback to the actions of its consumers. The debate over whether ungulates accelerate or decelerate nutrient cycling can be resolved by comparing grazing and browsing effects in the same ecosystem type. Evidence from
Communicated by Jörg U. Ganzhorn. J. T. du Toit (*) Department of Wildland Resources, Utah State University, Logan, UT 84322‑5230, USA e-mail: [email protected] H. Olff Center for Ecological and Evolutionary Studies, University of Groningen, Nijenborgh 7, 9747 AG Groningen, The Netherlands
African savannas points to the rate of nutrient cycling being controlled by the mix of tolerance and resistance traits in plants; not the relative dominance of grazing or browsing by local herbivores. We recommend this across-guild comparative approach as a novel solution with widespread utility for resolving contingencies in community processes. Keywords Community ecology · Ungulate · Competition · Facilitation · Lawn · Nutrient cycling
Introduction Finding generalities at the community level is a special challenge to ecologists because communities are both complex and idiosyncratic. Any patterns or processes that might be identified within them are contingent upon the conditions that define them (Lawton 1999). Therefore, in the context of community ecology, a contingency is a constraint on a generality and is caused by the observed pattern or process being applicable only within a subset of potential conditions. Controlling such contingencies can require large-scale replication using global research networks to standardize multiple local studies for testing postulated generalities in community-level patterns (Adler et al. 2011). Another approach is to make comparisons across similar ecosystem types on different continents (Knapp et al. 2004) or even across marine and terrestrial ecosystems (Webb 2012), with the one ecosystem serving as the “control” for the other. For example, it has been found helpful to compare marine and terrestrial predator– prey systems to identify universal behavioral responses by which prey animals reduce their risk of predation (Wirsing and Ripple 2011). Here we propose that contingencies can also be controlled within ecosystems by making
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Variation in body size
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Fig. 1 A conceptual framework for identifying generalities applicable to vertebrates at the community level. Variation in resource use allows for the functional classification of species into two or more guilds, within each of which there is variation in body size. Ecological or evolutionary patterns or processes identified within one guild might be contingent upon the subset of resources defining that guild. Across-guild comparisons enable the emergence of patterns or processes that apply across all variations in resource use and body size within the assemblage of interest, and the identification of contingencies in those that do not. A community-level generality is free of contingencies across guilds
comparisons at the community level, between functionally differentiated species groups. As a conceptual framework for vertebrates (Fig. 1), body size and resource use are ecologically important sources of variation that provide the basis for a functional classification of species within a community of interest. Empirical patterns within separate functional groups (trophic guilds) are contingent upon separate resource classes and such patterns are blurred, or “noisy,” if the functional groupings are ignored. If, however, an ecological or evolutionary process is explored in each guild and analogous patterns are found, even despite certain differences (in slope, intercept, scatter, etc.), then a generality has emerged across guilds. For example, the scaling of space use by individual animals has long been debated by authors using global meta-analyses in which the data are grouped by taxonomic class and trophic level. In mammals the groupings were initially as coarse as “hunters” and “croppers” (McNab 1963) and over the next 40 years were only minimally refined to carnivores, omnivores, and herbivores (Jetz et al. 2004). But now a focused meta-analysis of space use by terrestrial and arboreal primates—essentially an across-guild comparison—has at least clarified the general determinants of home range overlap, even if not the individual use of space (Pearce et al. 2013). Conversely, across-guild comparisons are also useful for identifying contingencies. The island rule, for instance, predicts gigantism for small terrestrial vertebrate species and dwarfism for large ones when insular types are compared with their mainland ancestors (Lomolino 2005). In their recent meta-analysis Lomolino et al. (2013) found the island effect to be strongest in palaeo-insular species
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(extant species excluded) dependent on terrestrial food resources (species using aquatic food resources excluded). Hence, the effect emerges through prolonged isolation and is contingent upon a relatively restricted resource base; identifying the contingency delimits the generality of the rule. Such examples fit within the conceptual framework of across-guild comparisons (Fig. 1) yet that general approach has not previously been formalized for controlling the contingency problem in community ecology. Here we demonstrate the utility of the framework for clarifying generalities in grazing and browsing ecology. Our focus is on animal– plant and animal–animal interactions in terrestrial communities that include large herbivorous mammals (>5 kg). Grazers and browsers Grazers mainly eat the foliage of monocotyledons (such as grasses and sedges) whereas browsers mainly eat the foliage of dicotyledons (forbs and woody plants). Browsing is evolutionarily older than grazing, which mostly coevolved with the radiation of grasses over the past 15 million years (Janis et al. 2000). Therefore, because the two guilds result from evolutionary radiation in different episodes with different contingencies, they can be considered a “repeated experiment” in evolutionary time. Browsers have always been in a coevolutionary arms race with their woody food plants, which have a plethora of physical and chemical defenses against herbivory, towards which grasses are comparatively tolerant (Gordon and Prins 2008). Some mammalian taxa such as bovids, cervids and rhinos are represented in both guilds, and some such as equids (grazers) and giraffids (browsers) are exclusive to either one. Some species known as “mixed feeders” switch back and forth between guilds, mainly grazing when green grass is available and browsing when the grass turns brown or disappears in the winter or dry season. Among species of similar size and gut morphology, the digestive systems of grazers and browsers are essentially the same (Gordon and Illius 1994). Nevertheless, the numerous large herbivore species that are specialized for either grazing or browsing represent two species groups recognized as being behaviorally and functionally distinct within their ecosystems (Gordon and Prins 2008). The resource base of grazers is distributed across the landscape in an essentially continuous two-dimensional grassy carpet while the shrubs and trees fed on by browsers occur as discrete food sources each with its own threedimensional architecture. The economically most important free-ranging livestock species (cattle, sheep, horses) are grazers, which stay in herds on open plains or pastures from which excess food can be harvested and stored as hay, making them generally easier to manage than browsers. As a result there is a research bias towards grazers and therein
Oecologia
lies an unresolved contingency—grazers use only a subset (mainly grass) of all the plant types constituting the food resources of large herbivores. Here we propose, and aim to demonstrate with examples, that browsing ecology is now sufficiently developed for us to assume that a meaningful generality in large herbivore ecology is one that applies to grazing and browsing guilds alike. Our conceptual framework (Fig. 1) entails the comparison of guilds in which member species display substantial variation in body size, which suits large mammalian herbivores because their body masses span three orders of magnitude. However, the megafaunal extinctions of the late Quarternary period have, for a variety of possible reasons of which some are anthropogenic (Brook and Bowman 2004), depauperated the larger mammalian size classes on all continents other than Africa (Johnson 2002). We thus draw heavily from the literature on grazing and browsing ecology in African savannas, where both guilds are represented in the fauna with the highest diversity of extant ungulate species in the widest body-size range (du Toit and Cumming 1999).
Generality 1: variations in body size and trophic morphology underlie resource partitioning at multiple scales The across-guild comparative approach was used, apparently inadvertently, by Geist (1974) in his formulation of the strongest generality in ungulate ecology, the Jarman– Bell principle. It was based on two independent studies: one of behavioral ecology in grazing and browsing antelopes (Jarman 1974); the other on feeding ecology in a grazing guild (Bell 1971). The essential principle, that larger herbivores can survive on lower quality food that is more abundant, has been found to rest solidly on allometric scaling laws and empirical evidence (Demment and Van Soest 1985; Illius and Gordon 1987, 1992). Differences in body size among sympatric guild members therefore imply interspecific differences in tolerance for less-digestible (fibrous) foods during periods of nutritional limitation, signaling evolutionary pressure for resource partitioning (du Toit 2011; Kleynhans et al. 2011). Scaling up from bites of food to the spatial arrangement of herbaceous plants in a pasture or branches on a tree, allometries of dietary tolerance and other size-dependent features (e.g. stride length, bite volume) predict that herbivores of different body size should perceive food patches at coarser or finer scales of spatial resolution (Cromsigt and Olff 2006; Laca et al. 2010). Indeed, recent field experiments and simulation models confirm that grazers (sheep, cattle) and browsers (moose Alces alces) are predictably sensitive to variation in the fractal dimensions of their
immediate foraging environments (Laca et al. 2010; Pastor and De Jager 2013). Also, at the habitat scale, the wider dietary tolerances of larger herbivore species should enable them to occupy a wider range of habitat types. Conversely, smaller species should each be more specialized for specific habitats that provide higher quality food year-round. This theoretical prediction has been empirically confirmed for grazing and browsing guilds (du Toit and Owen-Smith 1989; Redfern et al. 2006) despite differences in digestive morphology (ruminant vs. non-ruminant) complicating the pattern among grazers (Cromsigt et al. 2009). Overall, across multiple scales, body size emerges as the primary axis along which resources are partitioned among coexisting species in both guilds. Being a contingency-free rule, the Jarman–Bell principle is of immense heuristic value to the ecology and management of communities that include large herbivores. It also reaffirms the importance of metabolic theory as a conceptual pillar of ecology (Brown et al. 2004).
Generality 2: competition exerts a stronger influence than facilitation on the structure of large herbivore assemblages when food resources are limiting Originally described from field observations in East Africa (Vesey-Fitzgerald 1960), “the grazing succession” refers to waves of different ungulate species grazing patches of grassland in a predictable sequence. In his classic analysis of the phenomenon, Bell (1971) surmised that the “earlier members of the succession prepare the structure of the vegetation for the following members,” implying facilitation as the primary interspecific interaction. The particular grazing succession studied by Bell involved zebra Equus quagga, wildebeest Connochaetes taurinus, and Thomson’s gazelle Eudorcas thomsonii feeding from the same sward but with their peak densities separated by intervals of about 2 months (Fig. 2). With zebras being non-ruminants and larger (approximate adult female mass = 219 kg) than wildebeest (163 kg) and gazelles (16 kg), the order of succession corresponds with the order of narrowing dietary tolerances; zebras can tolerate ingesting the highest fraction of fibrous stem from the mix of grass stem, sheath and leaf tissues available in the sward. Bell’s grazing succession, with partitioned grazing niches and facilitation of the smaller members by the voluntary actions of the larger members, is a compelling concept but has become widely questioned (Illius and Gordon 1987; Arsenault and Owen-Smith 2002, 2008; Kleynhans et al. 2011). We suggest some clarity can be gained by resolving the contingency inherent in community-level studies that focus on grazers. If communities that include large herbivorous mammals are primarily structured either by facilitation or competition, then a common
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underlying process should be evident in both grazing and browsing guilds. The disproportionately long necks of some terrestrial herbivores such as giraffes Giraffa camelopardalis, tortoises (e.g. Chelonoidis spp.), and perhaps sauropod dinosaurs, are parsimoniously explained by selection for high browsing (Wilkinson and Ruxton 2012). Giraffes can feed up and down a wide height range, but by feeding above reach of other browsers they derive an advantage in leaf mass gained per bite from the canopy (Woolnough and du Toit 2001). An experiment involving fenced and unfenced trees in the wild showed reduced leaf availability per shoot in the lower canopies of unfenced trees, caused by selective browsing by various ungulate species shorter than giraffes (Cameron and du Toit 2007). Those smaller-bodied guild members, having narrower dietary tolerances, narrower muzzles, and lower intake requirements enabling more time for selective feeding, pick out the most palatable leaves and shoots from the foliage within their reach. Giraffes therefore benefit by browsing on leafier shoots higher in the canopy. The result is browsing stratification, which, we argue, is driven by the same process as the grazing succession but in a vertical instead of horizontal plane (Fig. 3). The patterns obviously differ in that the grazing succession involves herbivores of different size feeding in the same sward at different times, whereas in browsing stratification the different-sized herbivores feed at different heights at the same time. Nevertheless,
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Month after peak rain Fig. 2 Grazing succession in which different ungulate population densities peak on the same patch of grassland in a sequence through time. Counts of each herbivore species were made by Bell (1971) in standardized transects in each month over 3 successive years in the Serengeti ecosystem of East Africa. Here, the counts over all 3 years are combined for each month following peak rain and expressed as relative density with 1.0 being the highest population density for that species. Zebras graze down the tall grass during and soon after the rainfall peak. They become replaced by wildebeest, which, when the abundance of the grass resource is declining some 3–4 months after the rainfall peak, are replaced by Thomson’s gazelles
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Fig. 3a, b Browsing stratification in which ungulate species differ in the heights above ground at which they allocate time to browsing. Measured in the Kruger ecosystem of South Africa (Cameron and du Toit 2007), leaf biomass (dry) per standardized Acacia nigrescens shoot is reduced in the lower canopies of trees exposed to a complete guild of browsing ungulates (filled symbols; mean ± SE), when compared to neighboring trees excluded by fences 2.2 m high (open sym-
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bols), but not above ~3 m where only giraffes have access (a). In the same ecosystem, the allocation of feeding time across heights from the ground (du Toit 1990) shows that giraffes avoid competing with other guild members, here represented by kudu Tragelaphus strepsiceros and steenbok Raphicerus campestris, that selectively reduce leaf biomass per shoot at the lower levels of the canopy (b)
Oecologia
the underlying process—smaller species directionally displacing larger species from feeding sites—is the same and is supported by modeled and observed interactions within both guilds (Illius and Gordon 1987; Gordon and Illius 1989; Van de Koppel and Prins 1998; Cameron and du Toit 2007). The emerging generality is that competition has a stronger influence than facilitation in structuring large herbivore assemblages under conditions of resource limitation. When the food resource is abundant, facilitation can explain the movement of smaller grazers onto swards that have been coarsely grazed and trampled by larger species (Van de Koppel and Prins 1998). Facilitation can also explain wet season weight gains in cattle grazing together with zebras (Odadi et al. 2011), and impala Aepyceros melampus population growth in areas where browsing elephants Loxodonta africana have converted woodland to shrubland (Rutina et al. 2005; Moe et al. 2009). Nevertheless, reduced patch residence time and/ or locally depressed feeding efficiency are to be expected for the facilitating species when the abundance of shared resources declines (Arsenault and Owen-Smith 2002). That expectation is consistent with Bell’s original data from the Serengeti grazing succession in which, about 3 months after the rainfall peak in 3 successive years, wildebeest moved forward each time Thomson’s gazelles began moving in from behind (Fig. 2). Exceptions apply, of course, to those large species that are anatomically specialized for lawn grazing, such as hippos Hippopotamus amphibius and white rhinos Ceratotherium simum that pluck short grass with their wide lips (Arsenault and Owen-Smith 2008). The particular niches into which those species have evolved appear to be virtually immune from interspecific competition.
Generality 3: plant‑herbivore feedbacks maintain grazing lawns and browsing hedges Lawns form where grazing is chronically concentrated on localized sites occurring within a lightly grazed matrix of grassy vegetation (Fig. 4a). They are dominated by grazing-tolerant stoloniferous grasses maintained in early growth stages within close-cropped patches surrounded by taller bunchgrasses (McNaughton 1984; Archibald 2008; Cromsigt and Olff 2008). Typically linked with aggregations of grazers such as herds of ungulates or flocks of geese, grazing lawns can also be created and maintained by small groups, or even individuals, of very large grazers such as white rhinos (Waldram et al. 2008). Although grazing lawns are, by definition, phenomena of the grazing guild, we are interested in whether the underlying herbivore-plant interactions are contingent upon grazing or can be generalized across guilds. Indeed, recent comparisons of grazing lawns and browsing hedges (Fornara and du Toit 2007; Cromsigt and Kuijper 2011) confirm that similar interactions do occur in both guilds, allowing a generality to emerge. There are numerous examples from tropical, temperate, and boreal ecosystems of increased browsing intensity on woody plants that respond with tolerance traits (Fornoni 2011) associated with increased palatability, attracting further browsing (Cromsigt and Kuijper 2011). Compensatory growth can be of enhanced nutritional value to browsers (du Toit et al. 1990; Danell et al. 1994) but is produced by chronically pruned plants at the expense of sexual reproduction. Long-term population studies are needed on the comparative life histories of woody plants that support browsing hedges and those that do not, yet some patterns are apparent. For example, in the
Fig. 4a, b A typical grazing lawn (a) maintained by cattle on the island of Schiermonnikoog, the Netherlands, and an A. nigrescens tree pruned into a characteristically conical browsing hedge (b) by giraffes in the Kruger National Park, South Africa. Photographs: J. T. du Toit
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taiga vegetation of northern Scandinavia, winter browsing by moose on willows (Salix phylicifolia) results in fewer catkins on browsed compared to unbrowsed twigs within individual plants in the following spring (Stolter 2008). Across gradients of browsing intensity in African savannas, Acacia stands at the high ends have a lower proportion of trees carrying pods and fewer pods per tree in comparison with stands at the low ends (Fornara and du Toit 2007; Goheen et al. 2007). Saplings at the high ends of browsing gradients also build disproportionately large root systems, perhaps as “storage” that can be mobilized for rapid growth in sporadic windows of opportunity when browser densities are low (Fornara and du Toit 2008a). Also, in temperate European floodplains where Prunus spinosa is chronically browsed by large herbivores, this spinescent shrub propagates through rhizomes to form thickets in a strategy similar to that of lawn grasses (Bakker et al. 2004). At the plant community level, grazing lawns are distinct in both structure and composition, being densely packed assemblages dominated by prostrate, grazing-tolerant grass species. Browsing hedges, however, can vary from heavily browsed individual shrubs or trees (Fig. 4b) within mixed stands that include lightly browsed plants (Bakker et al. 2004; Fornara and du Toit 2007) to dense multi-species patches of saplings “captured” by browsers in forest gaps (Cromsigt and Kuijper 2011). The latter case has the community-level characteristics of a grazing lawn, but is the lawn analogy being stretched too far when applied to hedged individual trees and shrubs? We suggest not. When a patch within a bunchgrass community becomes converted into a grazing lawn by local interactions of grazing, rainfall and fire (Archibald 2008), some plants grow horizontally by sending out stolons that establish multiple new tufts within a dense lawn. If all tufts within a grazing lawn were grouped by their vegetative origins, and each resulting genet classified as one plant, then the numerical dominance of the community would change dramatically. Viewed in this way, each genet of stoloniferous tufts in a grazing lawn is the prostrate equivalent of a clonal Prunus thicket (Bakker et al. 2004) or a hedged Acacia tree (Fornara and du Toit 2007). As a generality, spatial variations in grazing and browsing intensity are associated with variations in the morphophysiological traits of each guild’s food plants. Grazing lawns and browsing hedges are characterized by herbaceous and woody plants (respectively) with tolerance traits that allow survival in physiologically young growth stages under chronic herbivory regimes. In each case, the nutritive value and productivity of the local food resource is enhanced by plants maintaining younger tissues that are replaced in positive feedback to the actions of their consumers.
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Generality 4: nutrient cycling through large herbivores is controlled by plant defensive traits Resistance is any plant trait that reduces the preference or performance of herbivores, whereas tolerance is the relative degree to which a plant’s fitness is affected by herbivores (Strauss and Agrawal 1999). Both traits influence the effects of herbivores on nutrient cycling and in terrestrial ecosystems these effects can be either accelerating or decelerating (Ritchie et al. 1998). First described in the savanna of East Africa’s Serengeti (McNaughton 1976, 1985), the accelerating effect occurs where grasses with tolerance traits compensate for grazing by replacing nutrient-rich above-ground tissues through increased rates of nutrient uptake and growth. The decelerating effect is best known from the boreal forest of North America’s Isle Royale (Pastor and Naiman 1992) where long-term selective browsing by moose exposes the competitive advantages of woody plants with resistance traits. Such traits include chemically defended leaves with low nitrogen and high lignin contents, which decompose slowly. Serengeti and Isle Royale represent ecosystem types with extreme differences in multiple dimensions yet from them a generality has emerged in the literature: accelerating effects are attributed to grazing systems; decelerating effects to browsing systems (Pastor et al. 2006). Here we apply the across-guild comparative approach to question the generality of this grazer-browser dichotomy in nutrient cycling. Chronically intense herbivory by ungulates contributes to the encroachment of woody plants in rangelands worldwide and even targeted browsing by goats is usually inadequate to reverse the process (Archer 2010). In African savannas, the encroaching woody plants are commonly shrubs and trees such as various Acacia species and Dichrostachys cinerea (Roques et al. 2001). These fastgrowing, herbivore-tolerant legumes are physiologically adapted for fertile soils, with foliage that is highly palatable to browsing ungulates (Bryant et al. 1989). Plant tolerance to herbivory can be expressed together with resistance (Fornoni 2011) and in the cases of African Acacia species and D. cinerea the main resistance trait is spinescence. Uncommon among boreal forest plants, spinescence in African savanna plants restricts tissue loss sufficiently to allow palatable species to persist in sites of chronically intense browsing without any apparent deceleration of nutrient cycling (Fornara and du Toit 2007, 2008b, c). Furthermore, post-browsing regrowth on such species is typically characterized by reduced leaf concentrations of carbon-based secondary metabolites (du Toit et al. 1990; Fornara and du Toit 2007) and this even applies to some non-spinescent species (Rooke and Bergström 2007; Scogings et al. 2011). With accelerated decomposition of the resulting litter, browsing can have a positive effect on nutrient cycling in ecosystems
Oecologia Fig. 5a, b Simplified pathways of flow among nutrient pools and the controls exerted upon them by plant defensive traits in terrestrial ecosystems. In boreal forests (a) biomass is dominated by woody plants that express strong resistance to herbivory through plant chemical defense. Chronic selective browsing drives a long-term shift in plant community composition leading to an accumulation of nutrients in plants and litter, with decelerated “brown” nutrient cycling. In African savannas (b) plants with tolerance traits, such as compensatory growth, can withstand chronic grazing and browsing. Tolerance can be expressed together with resistance such as spinescence, which is common in these ecosystems among woody plants that are fast growing and produce highly palatable leaves that decompose quickly. Here nutrients flow through an accelerated “green” cycle (color figure online)
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as different as Acacia savannas in South Africa (Fornara and du Toit 2008c) and mountain birch (Betula pubescens ssp. czerepanovii) forests in northernmost Finland (Stark et al. 2007). Accelerating and decelerating effects of herbivores on nutrient cycling, as postulated by Ritchie et al. (1998), were not originally ascribed to grazing and browsing guilds, respectively. Despite compelling evidence linking browsing and decelerated nutrient cycling in the boreal forest of Isle Royale (Pastor and Naiman 1992), results from exclosure studies in other North American ecosystems remain equivocal (Singer and Schoenecker 2003; Bressette et al. 2012). Further research is needed on the rates and pathways of nutrient cycling associated with browsing hedges in multiple ecosystems (Cromsigt and Kuijper 2011) but we question the generality of the grazer-browser dichotomy as a controller of nutrient cycling. Rather, we point to factors controlling whether nutrients taken up by plants are recycled through herbivores (accelerated “green” cycle) or detritivores (decelerated “brown” cycle), which can also partly explain “why the ground is more brown than the world is green” (Allison 2006). In some plant communities, such as in boreal forests where resistance (chemical defense) is the dominant defensive trait, browsing drives a long-term shift in woody plant species composition that
results in accumulations of recalcitrant litter decomposing slowly in the brown cycle (Fig. 5a). In other plant communities, such as in African savannas where tolerance (compensatory growth) and resistance (spinescence) are both commonly expressed, grazing and browsing together provide a major conduit for nutrients to pass comparatively rapidly through the green cycle (Fig. 5b). We consequently propose, as a broad generality, that the influence of large herbivores—grazers and browsers alike—on the rate of nutrient cycling is controlled by the mix of tolerance and resistance traits in the plant community.
Conclusion In heed of Lawton’s (1999) warning that “community ecology is a mess, with so much contingency that useful generalizations are hard to find,” we encourage enquiry into methods to control the contingency problem rather than discourage the search for useful generalizations. For an approach that is at least applicable to terrestrial vertebrates, we recommend a conceptual framework in which the species of interest are organized into two or more trophic guilds. If a candidate generalization is found to hold across guilds then it is not contingent upon any particular subset
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of resources. It can thus be accepted as a generalized ecological or evolutionary pattern or process at the community level. We used large mammalian herbivores to illustrate this approach because they display wide variation in body size within two distinct trophic guilds. Each of those guilds has been extensively studied within the topics we sifted through for generalities, those being: interspecific competitive displacement from shared feeding sites when resources are limiting; plant-herbivore feedbacks; the involvement of large herbivores in nutrient cycling. We chose those wellstudied topics for the very reason that generalities can only be drawn from an adequate knowledge base. The acrossguild comparative approach, therefore, requires both an adequate distribution of species across guilds within the same ecosystem types and an adequate distribution of research across these guilds. Nevertheless, in addition to clarifying or rejecting generalities, across-guild comparisons should also be helpful for identifying knowledge gaps and stimulating new hypothesis-driven research in community ecology. Acknowledgments We are grateful to Jörg Ganzhorn and two anonymous reviewers for helpful comments on a previous draft. J. T. d. T. was supported by a visitor’s travel grant from the Nederlandse Organisatie voor Wetenschappelijk Onderzoek. We thank Dick Visser for help with the figures.
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Bryant JP, Kuropat PJ, Cooper SM, Frisby K, Owen-Smith N (1989) Resource availability hypothesis of plant antiherbivore defence tested in a South African savanna ecosystem. Nature 340:227–229 Cameron EZ, du Toit JT (2007) Winning by a neck: tall giraffes avoid competing with shorter browsers. Am Nat 169:130–135 Cromsigt JPGM, Olff H (2006) Resource partitioning among savanna grazers mediated by local heterogeneity: an experimental approach. Ecology 87:1532–1541 Cromsigt JPGM, Olff H (2008) Dynamics of grazing lawn formation: an experimental test of the role of scale-dependent processes. Oikos 117:1444–1452 Cromsigt JPGM, Prins HHT, Olff H (2009) Habitat heterogeneity as a driver of ungulate diversity and distribution patterns: interaction of body mass and digestive strategy. Divers Distrib 15: 513–522 Cromsigt JPGM, Kuijper DPJ (2011) Revisiting the browsing lawn concept: evolutionary interactions or pruning herbivores? Perspect Plant Ecol 13:207–215 Danell K, Bergström R, Edenius L (1994) Effects of large mammalian browsers on architecture, biomass, and nutrients of woody plants. J Mammal 75:833–844 Demment MW, van Soest PJ (1985) A nutritional explanation for body-size patterns of ruminant and nonruminant herbivores. Am Nat 125:641–672 du Toit JT, Owen-Smith N (1989) Body size, population metabolism, and habitat specialization among large African herbivores. Am Nat 133:736–740 du Toit JT (1990) Feeding-height stratification among African browsing ruminants. Afr J Ecol 28:55–61 du Toit JT, Bryant JP, Frisby K (1990) Regrowth and palatability of Acacia shoots following pruning by African savanna browsers. Ecology 71:140–154 du Toit JT, Cumming DHM (1999) Functional significance of ungulate diversity in African savannas and the ecological implications of the spread of pastoralism. Biodivers Conserv 8:1643–1661 du Toit JT (2011) Coexisting with cattle. Science 333:1710–1711 Fornara DA, du Toit JT (2007) Browsing lawns? responses of Acacia nigrescens to ungulate browsing in an African savanna. Ecology 88:200–209 Fornara DA, du Toit JT (2008a) Responses of woody saplings exposed to chronic mammalian herbivory in an African savanna. Ecoscience 15:129–135 Fornara DA, du Toit JT (2008b) Community-level interactions between ungulate browsers and woody plants in an African savanna dominated by palatable-spinescent Acacia trees. J Arid Environ 72:534–545 Fornara DA, du Toit JT (2008c) Browsing-induced effects on leaf litter quality and decomposition in a southern African savanna. Ecosystems 11:238–249 Fornoni J (2011) Ecological and evolutionary implications of plant tolerance to herbivory. Funct Ecol 25:399–407 Geist V (1974) On the relationship of social evolution and ecology in ungulates. Am Zool 14:205–220 Goheen JR, Young TP, Keesing F, Palmer TM (2007) Consequences of herbivory by native ungulates for the reproduction of a savanna tree. J Ecol 95:129–138 Gordon IJ, Illius AW (1989) Resource partitioning by ungulates on the Isle of Rhum. Oecologia 79:383–389 Gordon IJ, Illius AW (1994) The functional significance of the browser-grazer dichotomy in African ruminants. Oecologia 98:167–175 Gordon IJ, Prins HHT (2008) The ecology of grazing and browsing. Ecological studies 195. Springer, Berlin Illius AW, Gordon IJ (1987) The allometry of food intake in grazing ruminants. J Anim Ecol 56:989–999
Oecologia Illius AW, Gordon IJ (1992) Modelling the nutritional ecology of ungulate herbivores: evolution of body size and competitive interactions. Oecologia 89:428–434 Janis CM, Damuth J, Theodor JM (2000) Miocene ungulates and terrestrial primary productivity: where have all the browsers gone? PNAS 97:7899–7904 Jarman PJ (1974) The social organization of antelope in relation to their ecology. Behaviour 48:215–266 Jetz W, Carbone C, Fulford J, Brown JH (2004) The scaling of animal space use. Science 306:266–268 Johnson CN (2002) Determinants of loss of mammal species during the Late Quarternary ‘megafauna’ extinctions: life history and ecology, but not body size. Proc R Soc Lond B 269:2221–2227 Kleynhans EJ, Jolles AE, Bos MRE, Olff H (2011) Resource partitioning along multiple niche dimensions in differently sized African savanna grazers. Oikos 120:591–600 Knapp AK, Smith MD, Collins SL, Zambatis N, Peel M, Emery S, Wojdak J, Horner-Devine MC, Biggs H, Kruger J, Andelman SJ (2004) Generality in ecology: testing North American grassland rules in South African savannas. Front Ecol Environ 2:483–491 Laca EA, Sokolow S, Galli JR, Cangiano CA (2010) Allometry and spatial scales of foraging in mammalian herbivores. Ecol Lett 13:311–320 Lawton JH (1999) Are there general laws in ecology? Oikos 84:177–192 Lomolino MV (2005) Body size evolution in insular vertebrates: generality of the island rule. J Biogeogr 32:1683–1699 Lomolino MV, van der Geer AA, Lyras GA, Palombo MR, Sax DF, Rozzi R (2013) Of mice and mammoths: generality and antiquity of the island rule. J Biogeogr 40:1427–1439 McNab B (1963) Bioenergetics and the determination of home range size. Am Nat 97:133–140 McNaughton SJ (1976) Serengeti migratory wildebeest: facilitation of energy flow by grazing. Science 191:92–94 McNaughton SJ (1984) Grazing lawns: animals in herds, plant form, and coevolution. Am Nat 124:863–886 McNaughton SJ (1985) Ecology of a grazing ecosystem: the Serengeti. Ecol Monogr 53:291–320 Moe SR, Rutina LP, Hytteborn H, du Toit JT (2009) What controls woodland regeneration after elephants have killed the big trees? J Appl Ecol 46:223–230 Odadi WO, Karachi MK, Abdulrazak SA, Young TP (2011) African wild ungulates compete with or facilitate cattle depending on season. Science 333:1753–1755 Pastor J, Naiman RJ (1992) Selective foraging and ecosystem processes in boreal forests. Am Nat 139:690–705 Pastor J, Cohen Y, Hobbs NTH (2006) The roles of large herbivores in ecosystem nutrient cycles. In: Danell K, Bergström R, Duncan P, Pastor J (eds) Large herbivore ecology, ecosystem dynamics and conservation. Cambridge University Press, Cambridge, pp 289–325 Pastor J, De Jager NR (2013) Simulated responses of moose populations to browsing-induced changes in plant architecture and forage production. Oikos 122:575–582
Pearce F, Carbone C, Cowlishaw G, Isaac NJB (2013) Space-use scaling and home range in primates. Proc R Soc B 280:20122122 Redfern JV, Ryan SJ, Getz WM (2006) Defining herbivore assemblages in the Kruger National Park: a correlative approach. Oecologia 146:632–640 Ritchie ME, Tilman D, Knops JMH (1998) Herbivore effects on plant and nitrogen dynamics in oak savanna. Ecology 79:165–177 Rooke T, Bergström R (2007) Growth, chemical responses and herbivory after simulated leaf browsing in Combretum apiculatum. Plant Ecol 189:201–212 Roques KG, O’Connor TG, Watkinson AR (2001) Dynamics of shrub encroachment in an African savanna: relative influences of fire, herbivory, rainfall and density dependence. J Appl Ecol 38:268–280 Rutina LP, Moe SR, Swenson JE (2005) Elephant Loxodonta africana driven woodland conversion to shrubland improves dry-season browse availability for impala Aepyceros melampus. Wildl Biol 11:207–213 Scogings PF, Hjältén J, Skarpe S (2011) Secondary metabolites and nutrients of woody plants in relation to browsing intensity in African savannas. Oecologia 167:1063–1073 Singer FJ, Schoenecker KA (2003) Do ungulates accelerate or decelerate nitrogen cycling? For Ecol Manage 181:189–204 Stark S, Julkunen-Tiitto R, Kumpula J (2007) Ecological role of reindeer summer browsing in the mountain birch (Betula pubescens ssp. czerepanovii) forests: effects of plant defense, litter decomposition, and soil nutrient cycling. Oecologia 151:486–498 Stolter C (2008) Intra-individual plant response to moose browsing: feedback loops and impacts on multiple consumers. Ecol Monogr 78:167–183 Strauss SY, Agrawal AA (1999) The ecology and evolution of plant tolerance to herbivory. Trends Ecol Evol 14:179–185 Van de Koppel J, Prins HHT (1998) The importance of herbivore interactions for the dynamics of African savanna woodlands: an hypothesis. J Trop Ecol 14:565–576 Vesey-Fitzgerald DF (1960) Grazing succession among East African game animals. J Mammal 41:161–172 Waldram MS, Bond WJ, Stock WD (2008) Ecological engineering by a mega-grazer: white rhino impacts on a South African savanna. Ecosystems 11:101–112 Webb TJ (2012) Marine and terrestrial ecology: unifying concepts, revealing differences. Trends Ecol Evol 27:535–541 Wilkinson DM, Ruxton GD (2012) Understanding the selection for long necks in different taxa. Biol Rev 87:616–630 Wirsing AJ, Ripple WJ (2011) A comparison of shark and wolf research reveals similar behavioral responses by prey. Front Ecol Environ 9:335–341 Woolnough AP, du Toit JT (2001) Vertical zonation of browse quality in tree canopies exposed to a size-structured guild of African browsing ungulates. Oecologia 129:585–590
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Concepts, Reviews and Syntheses
Generalities in grazing and browsing ecology: using across‑guild comparisons to control contingencies Johan T. du Toit · Han Olff
Received: 11 June 2013 / Accepted: 11 December 2013 © Springer-Verlag Berlin Heidelberg 2014
Abstract In community ecology, broad-scale spatial replication can accommodate contingencies in patterns within species groups, but contingencies in processes across species groups remain problematic. Here, based on a focused review of grazing and browsing by large mammals, we use one trophic guild as a “control” for the other to identify generalities that are not contingent upon specific consumerresource interactions. An example of such a generality is the Jarman–Bell principle, which explains how allometries of metabolism and digestion influence dietary tolerance and thereby enable resource partitioning within both guilds at multiple scales. By comparing the grazing succession with browsing stratification we show how competition from smaller herbivores, rather than facilitation from larger ones, is the underlying process structuring ungulate assemblages when shared resources become limiting. Also, grazing lawns and browsing hedges are functionally similar. In each case, plants expressing tolerance traits can withstand chronic grazing or browsing in sites where the nutritive value of the local food resource is enhanced in positive feedback to the actions of its consumers. The debate over whether ungulates accelerate or decelerate nutrient cycling can be resolved by comparing grazing and browsing effects in the same ecosystem type. Evidence from
Communicated by Jörg U. Ganzhorn. J. T. du Toit (*) Department of Wildland Resources, Utah State University, Logan, UT 84322‑5230, USA e-mail: [email protected] H. Olff Center for Ecological and Evolutionary Studies, University of Groningen, Nijenborgh 7, 9747 AG Groningen, The Netherlands
African savannas points to the rate of nutrient cycling being controlled by the mix of tolerance and resistance traits in plants; not the relative dominance of grazing or browsing by local herbivores. We recommend this across-guild comparative approach as a novel solution with widespread utility for resolving contingencies in community processes. Keywords Community ecology · Ungulate · Competition · Facilitation · Lawn · Nutrient cycling
Introduction Finding generalities at the community level is a special challenge to ecologists because communities are both complex and idiosyncratic. Any patterns or processes that might be identified within them are contingent upon the conditions that define them (Lawton 1999). Therefore, in the context of community ecology, a contingency is a constraint on a generality and is caused by the observed pattern or process being applicable only within a subset of potential conditions. Controlling such contingencies can require large-scale replication using global research networks to standardize multiple local studies for testing postulated generalities in community-level patterns (Adler et al. 2011). Another approach is to make comparisons across similar ecosystem types on different continents (Knapp et al. 2004) or even across marine and terrestrial ecosystems (Webb 2012), with the one ecosystem serving as the “control” for the other. For example, it has been found helpful to compare marine and terrestrial predator– prey systems to identify universal behavioral responses by which prey animals reduce their risk of predation (Wirsing and Ripple 2011). Here we propose that contingencies can also be controlled within ecosystems by making
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Variation in body size
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Fig. 1 A conceptual framework for identifying generalities applicable to vertebrates at the community level. Variation in resource use allows for the functional classification of species into two or more guilds, within each of which there is variation in body size. Ecological or evolutionary patterns or processes identified within one guild might be contingent upon the subset of resources defining that guild. Across-guild comparisons enable the emergence of patterns or processes that apply across all variations in resource use and body size within the assemblage of interest, and the identification of contingencies in those that do not. A community-level generality is free of contingencies across guilds
comparisons at the community level, between functionally differentiated species groups. As a conceptual framework for vertebrates (Fig. 1), body size and resource use are ecologically important sources of variation that provide the basis for a functional classification of species within a community of interest. Empirical patterns within separate functional groups (trophic guilds) are contingent upon separate resource classes and such patterns are blurred, or “noisy,” if the functional groupings are ignored. If, however, an ecological or evolutionary process is explored in each guild and analogous patterns are found, even despite certain differences (in slope, intercept, scatter, etc.), then a generality has emerged across guilds. For example, the scaling of space use by individual animals has long been debated by authors using global meta-analyses in which the data are grouped by taxonomic class and trophic level. In mammals the groupings were initially as coarse as “hunters” and “croppers” (McNab 1963) and over the next 40 years were only minimally refined to carnivores, omnivores, and herbivores (Jetz et al. 2004). But now a focused meta-analysis of space use by terrestrial and arboreal primates—essentially an across-guild comparison—has at least clarified the general determinants of home range overlap, even if not the individual use of space (Pearce et al. 2013). Conversely, across-guild comparisons are also useful for identifying contingencies. The island rule, for instance, predicts gigantism for small terrestrial vertebrate species and dwarfism for large ones when insular types are compared with their mainland ancestors (Lomolino 2005). In their recent meta-analysis Lomolino et al. (2013) found the island effect to be strongest in palaeo-insular species
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(extant species excluded) dependent on terrestrial food resources (species using aquatic food resources excluded). Hence, the effect emerges through prolonged isolation and is contingent upon a relatively restricted resource base; identifying the contingency delimits the generality of the rule. Such examples fit within the conceptual framework of across-guild comparisons (Fig. 1) yet that general approach has not previously been formalized for controlling the contingency problem in community ecology. Here we demonstrate the utility of the framework for clarifying generalities in grazing and browsing ecology. Our focus is on animal– plant and animal–animal interactions in terrestrial communities that include large herbivorous mammals (>5 kg). Grazers and browsers Grazers mainly eat the foliage of monocotyledons (such as grasses and sedges) whereas browsers mainly eat the foliage of dicotyledons (forbs and woody plants). Browsing is evolutionarily older than grazing, which mostly coevolved with the radiation of grasses over the past 15 million years (Janis et al. 2000). Therefore, because the two guilds result from evolutionary radiation in different episodes with different contingencies, they can be considered a “repeated experiment” in evolutionary time. Browsers have always been in a coevolutionary arms race with their woody food plants, which have a plethora of physical and chemical defenses against herbivory, towards which grasses are comparatively tolerant (Gordon and Prins 2008). Some mammalian taxa such as bovids, cervids and rhinos are represented in both guilds, and some such as equids (grazers) and giraffids (browsers) are exclusive to either one. Some species known as “mixed feeders” switch back and forth between guilds, mainly grazing when green grass is available and browsing when the grass turns brown or disappears in the winter or dry season. Among species of similar size and gut morphology, the digestive systems of grazers and browsers are essentially the same (Gordon and Illius 1994). Nevertheless, the numerous large herbivore species that are specialized for either grazing or browsing represent two species groups recognized as being behaviorally and functionally distinct within their ecosystems (Gordon and Prins 2008). The resource base of grazers is distributed across the landscape in an essentially continuous two-dimensional grassy carpet while the shrubs and trees fed on by browsers occur as discrete food sources each with its own threedimensional architecture. The economically most important free-ranging livestock species (cattle, sheep, horses) are grazers, which stay in herds on open plains or pastures from which excess food can be harvested and stored as hay, making them generally easier to manage than browsers. As a result there is a research bias towards grazers and therein
Oecologia
lies an unresolved contingency—grazers use only a subset (mainly grass) of all the plant types constituting the food resources of large herbivores. Here we propose, and aim to demonstrate with examples, that browsing ecology is now sufficiently developed for us to assume that a meaningful generality in large herbivore ecology is one that applies to grazing and browsing guilds alike. Our conceptual framework (Fig. 1) entails the comparison of guilds in which member species display substantial variation in body size, which suits large mammalian herbivores because their body masses span three orders of magnitude. However, the megafaunal extinctions of the late Quarternary period have, for a variety of possible reasons of which some are anthropogenic (Brook and Bowman 2004), depauperated the larger mammalian size classes on all continents other than Africa (Johnson 2002). We thus draw heavily from the literature on grazing and browsing ecology in African savannas, where both guilds are represented in the fauna with the highest diversity of extant ungulate species in the widest body-size range (du Toit and Cumming 1999).
Generality 1: variations in body size and trophic morphology underlie resource partitioning at multiple scales The across-guild comparative approach was used, apparently inadvertently, by Geist (1974) in his formulation of the strongest generality in ungulate ecology, the Jarman– Bell principle. It was based on two independent studies: one of behavioral ecology in grazing and browsing antelopes (Jarman 1974); the other on feeding ecology in a grazing guild (Bell 1971). The essential principle, that larger herbivores can survive on lower quality food that is more abundant, has been found to rest solidly on allometric scaling laws and empirical evidence (Demment and Van Soest 1985; Illius and Gordon 1987, 1992). Differences in body size among sympatric guild members therefore imply interspecific differences in tolerance for less-digestible (fibrous) foods during periods of nutritional limitation, signaling evolutionary pressure for resource partitioning (du Toit 2011; Kleynhans et al. 2011). Scaling up from bites of food to the spatial arrangement of herbaceous plants in a pasture or branches on a tree, allometries of dietary tolerance and other size-dependent features (e.g. stride length, bite volume) predict that herbivores of different body size should perceive food patches at coarser or finer scales of spatial resolution (Cromsigt and Olff 2006; Laca et al. 2010). Indeed, recent field experiments and simulation models confirm that grazers (sheep, cattle) and browsers (moose Alces alces) are predictably sensitive to variation in the fractal dimensions of their
immediate foraging environments (Laca et al. 2010; Pastor and De Jager 2013). Also, at the habitat scale, the wider dietary tolerances of larger herbivore species should enable them to occupy a wider range of habitat types. Conversely, smaller species should each be more specialized for specific habitats that provide higher quality food year-round. This theoretical prediction has been empirically confirmed for grazing and browsing guilds (du Toit and Owen-Smith 1989; Redfern et al. 2006) despite differences in digestive morphology (ruminant vs. non-ruminant) complicating the pattern among grazers (Cromsigt et al. 2009). Overall, across multiple scales, body size emerges as the primary axis along which resources are partitioned among coexisting species in both guilds. Being a contingency-free rule, the Jarman–Bell principle is of immense heuristic value to the ecology and management of communities that include large herbivores. It also reaffirms the importance of metabolic theory as a conceptual pillar of ecology (Brown et al. 2004).
Generality 2: competition exerts a stronger influence than facilitation on the structure of large herbivore assemblages when food resources are limiting Originally described from field observations in East Africa (Vesey-Fitzgerald 1960), “the grazing succession” refers to waves of different ungulate species grazing patches of grassland in a predictable sequence. In his classic analysis of the phenomenon, Bell (1971) surmised that the “earlier members of the succession prepare the structure of the vegetation for the following members,” implying facilitation as the primary interspecific interaction. The particular grazing succession studied by Bell involved zebra Equus quagga, wildebeest Connochaetes taurinus, and Thomson’s gazelle Eudorcas thomsonii feeding from the same sward but with their peak densities separated by intervals of about 2 months (Fig. 2). With zebras being non-ruminants and larger (approximate adult female mass = 219 kg) than wildebeest (163 kg) and gazelles (16 kg), the order of succession corresponds with the order of narrowing dietary tolerances; zebras can tolerate ingesting the highest fraction of fibrous stem from the mix of grass stem, sheath and leaf tissues available in the sward. Bell’s grazing succession, with partitioned grazing niches and facilitation of the smaller members by the voluntary actions of the larger members, is a compelling concept but has become widely questioned (Illius and Gordon 1987; Arsenault and Owen-Smith 2002, 2008; Kleynhans et al. 2011). We suggest some clarity can be gained by resolving the contingency inherent in community-level studies that focus on grazers. If communities that include large herbivorous mammals are primarily structured either by facilitation or competition, then a common
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underlying process should be evident in both grazing and browsing guilds. The disproportionately long necks of some terrestrial herbivores such as giraffes Giraffa camelopardalis, tortoises (e.g. Chelonoidis spp.), and perhaps sauropod dinosaurs, are parsimoniously explained by selection for high browsing (Wilkinson and Ruxton 2012). Giraffes can feed up and down a wide height range, but by feeding above reach of other browsers they derive an advantage in leaf mass gained per bite from the canopy (Woolnough and du Toit 2001). An experiment involving fenced and unfenced trees in the wild showed reduced leaf availability per shoot in the lower canopies of unfenced trees, caused by selective browsing by various ungulate species shorter than giraffes (Cameron and du Toit 2007). Those smaller-bodied guild members, having narrower dietary tolerances, narrower muzzles, and lower intake requirements enabling more time for selective feeding, pick out the most palatable leaves and shoots from the foliage within their reach. Giraffes therefore benefit by browsing on leafier shoots higher in the canopy. The result is browsing stratification, which, we argue, is driven by the same process as the grazing succession but in a vertical instead of horizontal plane (Fig. 3). The patterns obviously differ in that the grazing succession involves herbivores of different size feeding in the same sward at different times, whereas in browsing stratification the different-sized herbivores feed at different heights at the same time. Nevertheless,
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Month after peak rain Fig. 2 Grazing succession in which different ungulate population densities peak on the same patch of grassland in a sequence through time. Counts of each herbivore species were made by Bell (1971) in standardized transects in each month over 3 successive years in the Serengeti ecosystem of East Africa. Here, the counts over all 3 years are combined for each month following peak rain and expressed as relative density with 1.0 being the highest population density for that species. Zebras graze down the tall grass during and soon after the rainfall peak. They become replaced by wildebeest, which, when the abundance of the grass resource is declining some 3–4 months after the rainfall peak, are replaced by Thomson’s gazelles
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Fig. 3a, b Browsing stratification in which ungulate species differ in the heights above ground at which they allocate time to browsing. Measured in the Kruger ecosystem of South Africa (Cameron and du Toit 2007), leaf biomass (dry) per standardized Acacia nigrescens shoot is reduced in the lower canopies of trees exposed to a complete guild of browsing ungulates (filled symbols; mean ± SE), when compared to neighboring trees excluded by fences 2.2 m high (open sym-
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bols), but not above ~3 m where only giraffes have access (a). In the same ecosystem, the allocation of feeding time across heights from the ground (du Toit 1990) shows that giraffes avoid competing with other guild members, here represented by kudu Tragelaphus strepsiceros and steenbok Raphicerus campestris, that selectively reduce leaf biomass per shoot at the lower levels of the canopy (b)
Oecologia
the underlying process—smaller species directionally displacing larger species from feeding sites—is the same and is supported by modeled and observed interactions within both guilds (Illius and Gordon 1987; Gordon and Illius 1989; Van de Koppel and Prins 1998; Cameron and du Toit 2007). The emerging generality is that competition has a stronger influence than facilitation in structuring large herbivore assemblages under conditions of resource limitation. When the food resource is abundant, facilitation can explain the movement of smaller grazers onto swards that have been coarsely grazed and trampled by larger species (Van de Koppel and Prins 1998). Facilitation can also explain wet season weight gains in cattle grazing together with zebras (Odadi et al. 2011), and impala Aepyceros melampus population growth in areas where browsing elephants Loxodonta africana have converted woodland to shrubland (Rutina et al. 2005; Moe et al. 2009). Nevertheless, reduced patch residence time and/ or locally depressed feeding efficiency are to be expected for the facilitating species when the abundance of shared resources declines (Arsenault and Owen-Smith 2002). That expectation is consistent with Bell’s original data from the Serengeti grazing succession in which, about 3 months after the rainfall peak in 3 successive years, wildebeest moved forward each time Thomson’s gazelles began moving in from behind (Fig. 2). Exceptions apply, of course, to those large species that are anatomically specialized for lawn grazing, such as hippos Hippopotamus amphibius and white rhinos Ceratotherium simum that pluck short grass with their wide lips (Arsenault and Owen-Smith 2008). The particular niches into which those species have evolved appear to be virtually immune from interspecific competition.
Generality 3: plant‑herbivore feedbacks maintain grazing lawns and browsing hedges Lawns form where grazing is chronically concentrated on localized sites occurring within a lightly grazed matrix of grassy vegetation (Fig. 4a). They are dominated by grazing-tolerant stoloniferous grasses maintained in early growth stages within close-cropped patches surrounded by taller bunchgrasses (McNaughton 1984; Archibald 2008; Cromsigt and Olff 2008). Typically linked with aggregations of grazers such as herds of ungulates or flocks of geese, grazing lawns can also be created and maintained by small groups, or even individuals, of very large grazers such as white rhinos (Waldram et al. 2008). Although grazing lawns are, by definition, phenomena of the grazing guild, we are interested in whether the underlying herbivore-plant interactions are contingent upon grazing or can be generalized across guilds. Indeed, recent comparisons of grazing lawns and browsing hedges (Fornara and du Toit 2007; Cromsigt and Kuijper 2011) confirm that similar interactions do occur in both guilds, allowing a generality to emerge. There are numerous examples from tropical, temperate, and boreal ecosystems of increased browsing intensity on woody plants that respond with tolerance traits (Fornoni 2011) associated with increased palatability, attracting further browsing (Cromsigt and Kuijper 2011). Compensatory growth can be of enhanced nutritional value to browsers (du Toit et al. 1990; Danell et al. 1994) but is produced by chronically pruned plants at the expense of sexual reproduction. Long-term population studies are needed on the comparative life histories of woody plants that support browsing hedges and those that do not, yet some patterns are apparent. For example, in the
Fig. 4a, b A typical grazing lawn (a) maintained by cattle on the island of Schiermonnikoog, the Netherlands, and an A. nigrescens tree pruned into a characteristically conical browsing hedge (b) by giraffes in the Kruger National Park, South Africa. Photographs: J. T. du Toit
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taiga vegetation of northern Scandinavia, winter browsing by moose on willows (Salix phylicifolia) results in fewer catkins on browsed compared to unbrowsed twigs within individual plants in the following spring (Stolter 2008). Across gradients of browsing intensity in African savannas, Acacia stands at the high ends have a lower proportion of trees carrying pods and fewer pods per tree in comparison with stands at the low ends (Fornara and du Toit 2007; Goheen et al. 2007). Saplings at the high ends of browsing gradients also build disproportionately large root systems, perhaps as “storage” that can be mobilized for rapid growth in sporadic windows of opportunity when browser densities are low (Fornara and du Toit 2008a). Also, in temperate European floodplains where Prunus spinosa is chronically browsed by large herbivores, this spinescent shrub propagates through rhizomes to form thickets in a strategy similar to that of lawn grasses (Bakker et al. 2004). At the plant community level, grazing lawns are distinct in both structure and composition, being densely packed assemblages dominated by prostrate, grazing-tolerant grass species. Browsing hedges, however, can vary from heavily browsed individual shrubs or trees (Fig. 4b) within mixed stands that include lightly browsed plants (Bakker et al. 2004; Fornara and du Toit 2007) to dense multi-species patches of saplings “captured” by browsers in forest gaps (Cromsigt and Kuijper 2011). The latter case has the community-level characteristics of a grazing lawn, but is the lawn analogy being stretched too far when applied to hedged individual trees and shrubs? We suggest not. When a patch within a bunchgrass community becomes converted into a grazing lawn by local interactions of grazing, rainfall and fire (Archibald 2008), some plants grow horizontally by sending out stolons that establish multiple new tufts within a dense lawn. If all tufts within a grazing lawn were grouped by their vegetative origins, and each resulting genet classified as one plant, then the numerical dominance of the community would change dramatically. Viewed in this way, each genet of stoloniferous tufts in a grazing lawn is the prostrate equivalent of a clonal Prunus thicket (Bakker et al. 2004) or a hedged Acacia tree (Fornara and du Toit 2007). As a generality, spatial variations in grazing and browsing intensity are associated with variations in the morphophysiological traits of each guild’s food plants. Grazing lawns and browsing hedges are characterized by herbaceous and woody plants (respectively) with tolerance traits that allow survival in physiologically young growth stages under chronic herbivory regimes. In each case, the nutritive value and productivity of the local food resource is enhanced by plants maintaining younger tissues that are replaced in positive feedback to the actions of their consumers.
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Generality 4: nutrient cycling through large herbivores is controlled by plant defensive traits Resistance is any plant trait that reduces the preference or performance of herbivores, whereas tolerance is the relative degree to which a plant’s fitness is affected by herbivores (Strauss and Agrawal 1999). Both traits influence the effects of herbivores on nutrient cycling and in terrestrial ecosystems these effects can be either accelerating or decelerating (Ritchie et al. 1998). First described in the savanna of East Africa’s Serengeti (McNaughton 1976, 1985), the accelerating effect occurs where grasses with tolerance traits compensate for grazing by replacing nutrient-rich above-ground tissues through increased rates of nutrient uptake and growth. The decelerating effect is best known from the boreal forest of North America’s Isle Royale (Pastor and Naiman 1992) where long-term selective browsing by moose exposes the competitive advantages of woody plants with resistance traits. Such traits include chemically defended leaves with low nitrogen and high lignin contents, which decompose slowly. Serengeti and Isle Royale represent ecosystem types with extreme differences in multiple dimensions yet from them a generality has emerged in the literature: accelerating effects are attributed to grazing systems; decelerating effects to browsing systems (Pastor et al. 2006). Here we apply the across-guild comparative approach to question the generality of this grazer-browser dichotomy in nutrient cycling. Chronically intense herbivory by ungulates contributes to the encroachment of woody plants in rangelands worldwide and even targeted browsing by goats is usually inadequate to reverse the process (Archer 2010). In African savannas, the encroaching woody plants are commonly shrubs and trees such as various Acacia species and Dichrostachys cinerea (Roques et al. 2001). These fastgrowing, herbivore-tolerant legumes are physiologically adapted for fertile soils, with foliage that is highly palatable to browsing ungulates (Bryant et al. 1989). Plant tolerance to herbivory can be expressed together with resistance (Fornoni 2011) and in the cases of African Acacia species and D. cinerea the main resistance trait is spinescence. Uncommon among boreal forest plants, spinescence in African savanna plants restricts tissue loss sufficiently to allow palatable species to persist in sites of chronically intense browsing without any apparent deceleration of nutrient cycling (Fornara and du Toit 2007, 2008b, c). Furthermore, post-browsing regrowth on such species is typically characterized by reduced leaf concentrations of carbon-based secondary metabolites (du Toit et al. 1990; Fornara and du Toit 2007) and this even applies to some non-spinescent species (Rooke and Bergström 2007; Scogings et al. 2011). With accelerated decomposition of the resulting litter, browsing can have a positive effect on nutrient cycling in ecosystems
Oecologia Fig. 5a, b Simplified pathways of flow among nutrient pools and the controls exerted upon them by plant defensive traits in terrestrial ecosystems. In boreal forests (a) biomass is dominated by woody plants that express strong resistance to herbivory through plant chemical defense. Chronic selective browsing drives a long-term shift in plant community composition leading to an accumulation of nutrients in plants and litter, with decelerated “brown” nutrient cycling. In African savannas (b) plants with tolerance traits, such as compensatory growth, can withstand chronic grazing and browsing. Tolerance can be expressed together with resistance such as spinescence, which is common in these ecosystems among woody plants that are fast growing and produce highly palatable leaves that decompose quickly. Here nutrients flow through an accelerated “green” cycle (color figure online)
Resistance
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as different as Acacia savannas in South Africa (Fornara and du Toit 2008c) and mountain birch (Betula pubescens ssp. czerepanovii) forests in northernmost Finland (Stark et al. 2007). Accelerating and decelerating effects of herbivores on nutrient cycling, as postulated by Ritchie et al. (1998), were not originally ascribed to grazing and browsing guilds, respectively. Despite compelling evidence linking browsing and decelerated nutrient cycling in the boreal forest of Isle Royale (Pastor and Naiman 1992), results from exclosure studies in other North American ecosystems remain equivocal (Singer and Schoenecker 2003; Bressette et al. 2012). Further research is needed on the rates and pathways of nutrient cycling associated with browsing hedges in multiple ecosystems (Cromsigt and Kuijper 2011) but we question the generality of the grazer-browser dichotomy as a controller of nutrient cycling. Rather, we point to factors controlling whether nutrients taken up by plants are recycled through herbivores (accelerated “green” cycle) or detritivores (decelerated “brown” cycle), which can also partly explain “why the ground is more brown than the world is green” (Allison 2006). In some plant communities, such as in boreal forests where resistance (chemical defense) is the dominant defensive trait, browsing drives a long-term shift in woody plant species composition that
results in accumulations of recalcitrant litter decomposing slowly in the brown cycle (Fig. 5a). In other plant communities, such as in African savannas where tolerance (compensatory growth) and resistance (spinescence) are both commonly expressed, grazing and browsing together provide a major conduit for nutrients to pass comparatively rapidly through the green cycle (Fig. 5b). We consequently propose, as a broad generality, that the influence of large herbivores—grazers and browsers alike—on the rate of nutrient cycling is controlled by the mix of tolerance and resistance traits in the plant community.
Conclusion In heed of Lawton’s (1999) warning that “community ecology is a mess, with so much contingency that useful generalizations are hard to find,” we encourage enquiry into methods to control the contingency problem rather than discourage the search for useful generalizations. For an approach that is at least applicable to terrestrial vertebrates, we recommend a conceptual framework in which the species of interest are organized into two or more trophic guilds. If a candidate generalization is found to hold across guilds then it is not contingent upon any particular subset
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of resources. It can thus be accepted as a generalized ecological or evolutionary pattern or process at the community level. We used large mammalian herbivores to illustrate this approach because they display wide variation in body size within two distinct trophic guilds. Each of those guilds has been extensively studied within the topics we sifted through for generalities, those being: interspecific competitive displacement from shared feeding sites when resources are limiting; plant-herbivore feedbacks; the involvement of large herbivores in nutrient cycling. We chose those wellstudied topics for the very reason that generalities can only be drawn from an adequate knowledge base. The acrossguild comparative approach, therefore, requires both an adequate distribution of species across guilds within the same ecosystem types and an adequate distribution of research across these guilds. Nevertheless, in addition to clarifying or rejecting generalities, across-guild comparisons should also be helpful for identifying knowledge gaps and stimulating new hypothesis-driven research in community ecology. Acknowledgments We are grateful to Jörg Ganzhorn and two anonymous reviewers for helpful comments on a previous draft. J. T. d. T. was supported by a visitor’s travel grant from the Nederlandse Organisatie voor Wetenschappelijk Onderzoek. We thank Dick Visser for help with the figures.
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