The Ecology of the Earth's Grazing Ecosystems

Douglas A. Frank; Samuel J. McNaughton; Benjamin F. Tracy

BioScience, Vol. 48, No. 7. (Jul., 1998), pp. 513-521.

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http://www.jstor.org Mon Oct 29 19:30:32 2007 The Ecology of the Earth's brazing Ecosystems Profound functional similarities exist between the Serengeti and Yellowstone

Douglas A. Frank, Samuel J. McNaughton, and Benjamin F. Tracy

s recently as 150 years ago, the size, possesses almost four times most of Earth's grasslands The grazing ecosystem the ungulate species, and has ap- .supported large migratory proximately 52 times the number of populations of hoofed herbivores be- is among Earth's ungulates as YNP (Table 1). longing to the Artiodactyla, Perisso- There are several additional dif- dactyla, and Proboscidea-that is, most endangered ferences between the Serengeti and ungulates. These herbivores included YNP. First, the Serengeti is a slop- bison (Bison bison) on the North terrestrial habitats ing, broad plateau covered primarily ~meric'anplains, saiga antelope (Saiga by grassland and savanna, whereas tatarica) on the Eurasian steppe, YNP is a mountainous reserve occu- wildebeest (Connochaetes taurinus) be markedly different. We contend pied by coniferous forest (80%)and and zebra (Equus burchelli) on the that the Serengeti and YNP are ex- grassland (20%),the latter being the African savanna, and the ecologi- tant members of a once-widespread focus of this discussion. Serengeti cally equivalent kangaroos (Macro- ecosystem type that we refer to as a grass species all possess the C, pho- podidae) on the Australian savanna. "grazing ecosystem." This ecosys- tosynthetic pathway, whereas grasses As a result of the ~ost-industrial tem is distinguished from other habi- of YNP all have the C, pathway. global expansion of cropland and tats by its prominent herbivore-based Moreover, the Serengeti and YNP cattle ranching, most grasslands food web and by the extent to which support warm, tropical grasslands grazed by Pleistocene megaherbi- ecological processes are regulated by and cool, temperate grasslands, re- vores were eliminated. Today, they dynamics within that food web. spectively, which are about as dis- are restricted to the world's few large similar climatically as any two grass- grassland reserves that protect all Structural and land ecosystems on Earth (Figure 2). seasonal ranees of the animals. In Nevertheless, within the constraints this article, ke describe profound climatic differences imposed by some of these differ- functional similarities between two The Serengeti and YNP have been ences, the ecosystems exhibit a high of the most celebrated of these re- described as being dissimilar largely degree of functional similarity. maining habitats, the Serengeti eco- because of their structural, bound- system of east Africa and Yellowstone ary, and climatic characteristics Energy dynamics of National Park (YNP) of the North (Berger 1991). Annual movements grazing ecosystems American intermountain west, which of the major ungulate species delin- previously have been considered to eate the Serengeti ecosystem, of which Grazing ecosystems support more 85% is protected in the Serengeti herbivore biomass than any other Douglas A. Frank (e-mail: dafrank@ National Park, Masai Mara Game terrestrial habitat (Sinclair 1975, mailbox.syr.edu) is an assistant professor, Reserve, and numerous other, smaller Detling 1988, McNaughton et al. SamuelJ.McNaughton (e-mail: sjmcnaug@ game reserves. By contrast, the 1989, 1991, Huntly 1991).A func- mailbox.syr.edu) is a professor, and Ben- boundaries of YNP were originally tional consequence of this disparity jamin F. Tracy (e-mail: [email protected]) was drawn to protect the area's thermal in trophic structure emerges by com- a graduate student in the Department of features, with little regard to the paring the relationship between Biology, Syracuseuniversity, Syracuse, NY 13244-1220.They study the effects of large migratory patterns of animals. Con- aboveground production and herbi- herbivores on grassland processes in the sequently, ungulates regularly mi- vore consumption in the Serengeti Serengeti and Yellowstone National Park. grate across park boundaries to habi- and Yellowstone ecosystems with O 1998 American Institute of Biological tats that are not protected (Figure 1). that in other terrestrial ecosystems Sciences. The Serengeti is almost three times (Figure 3). For consumption measure-

July 1998 513 w -- Montana ) Western Corridor

\

\ ) Forest

30 I 50 100 150 200 250 Mean Annual Precipitation (cm)

Figure 2. Approximate placement of the Serengeti and grassland habitat of Yel- lowstone National Park in Whittaker's (1975)climate-biome diagram. The area designated as grassland includes shrub- Figure 1. The locations of the Serengeti and Yellowstone National Park (YNP)in Africa grassland, savanna, and open woodland and North America, respectively. The boundaries of both ecosystems (dashed lines) are habitat. The Serengeti and Yellowstone are determined by the migratory patterns of ungulates. Isopleths of mean annual precipi- climatically disparate grassland ecosystems. tation are shown for the Serengeti, and isopleths of elevation are shown for YNP. These variables are the principal environmental factors controlling habitat variability and consumed increased as NFP increased seasonal migrations (denoted by arrows) in the two ecosystems. for both groups of habitats. The low level of dis~ersionof ments, we included plant material re- est, and small grassland sites lacking samples around the regression line moved by all important herbivores, large herbivores. The second includes characterizing plant productivity and both vertebrates and invertebrates. the Serengeti and Yellowstone, which consumption in the Serengeti and All values were energy equivalents exhibit high herbivory rates. On av- Yellowstone grasslands suggests that (kJ), converted from biomass mea- erage, herbivores removed 57% (SE the relationship describes a con- surements using standard conversion = 3.4, n = 40) of NFP in the Serengeti tinuum from cool, temperate to factors (Golley 1968). For produc- and Yellowstone, whereas they re- warm, tropical grazing ecosystems. tivity measurements, we considered moved only 9% (SE = 1.4, n = 40) of Primary production is greater in the only the nonwoody fraction of NFP in other terrestrial ecosystems. Serengeti (average = 11,118 kJ . m-2 aboveground productivity-that is, For example, only 10% (SE = 2.1, n yr-I, SE = 978, n = 28) than in net foliage production (NFP)-be- = 14) of the aboveground produc- Yellowstone (average = 3168 kJ . cause woody production is largely tion was consumed in temperate m-2 yr-', SE = 530, n = 12), most unavailable to herbivores. grasslands that lack large herbivores, likely because of a combination of Plotting plant production against showing that the removal of migra- several factors: solar radiation and consumption revealed that terrestrial tory grazers dramatically affects the temperature are higher in the tropi- ecosystems fall into two groups that energy dynamics of grasslands. cal system; some areas of the are distinguished by the intensity of Slopes of the relationships did not Serengeti receive more precipitation herbivory (F1,78= 88.2, P < 0.0001; differ statistically between the two (range= 40-100 cmlyr) than Yellow- Figure 3). The first group includes groups (P > 0.10) and were greater stone (range= 40-75 cmlyr); a greater low-herbivory habitats: desert, tun- than 1, indicating that the propor- proportion of precipitation results dra, temperate forest, tropical for- tion of available primary production in runoff in the Yellowstone ecosys- tem; and the C,photosynthetic path- Table 1.Properties of the Serengeti ecosystem and Yellowstone National Park (YNP). way of the Serengeti vegetation con- fers greater water-use efficiency than Property Serengeti YNP the C, photosynthetic pathway of Size (km2) 26,000 9018 Yellowstone plants. Consumption Ungulate species 31 8 also is higher in the Serengeti (aver- Ungulate number 2,137,000 40,600 age = 7737 kJ . m-2. yr-', SE = 911) Vegetation structure Savanna and grassland Coniferous forest and than in Yellowstone (average = 1332 shrub-grassland kJ . m-2 yr-l, SE = 406), as is the Photosynthetic pathway of grass species C, C3 percentage of production consumed,

514 BioScience Vol. 48 NO. 7 65% (SE = 4) versus 40% (SE = 5). Figure 3. Rela- There are two caveats to our in- tionship between herbivore con- Yellowstone terpretation of these findings. The 7 Tundra - 0 first is that tropical forest habitat sumption (C)and 10.000- - Desert net foliage pro- ' 0 Small temperate cannot be confidently classified with grassland reserve duction (NFP)for Tamparate a sinale sam~le. he second is that looo - old field - terrestrial ecosys- - Temperate forest our analysis does not include com- tems. The solid B v Tropical forest bined production-consumption data line shows the re- - for tundra grazed by herds of cari- lationship for the $ bou or reindeer (Rangifer tarandus). Serengeti and g - The two high-consumption tundra Yellowstone eco- lo samples in Figure 3 were from sites systems (log.C = .I . experiencing rodent outbreaks, indi- cating that tundra can support high episodic rates of herbivory. How- = 38;'~<0.0001); Net Foliage Production (k~/m~/~r) the dashed line ever, whether ungulate-grazed tun- shows the rela- dra supports the chronic high levels tionship for other terrestrial ecosystems (log C = 1.62(logNFP) -3.55; r2= 0.47; df = 39; of herbivory characteristic of graz- P < 0.0001).Serengeti and Yellowstone measurements were determined by the authors ing ecosystems is unknown. (McNaughton 1985, Frank and McNaughton 1992, Tracy 1996),and data from the Because of their higher rates of other ecosystems were compiled from the literature (seeMcNaughton et al. 1989,1991 primary productivity and greater for references). proportions of this production flow- ing to consumers, tropical grazing energy and nutritional requirements coincides with a "green wave" of ecosystems support greater ungulate in grasslands, in which the quantity plant production that is initiated in biomass than temperate grazing eco- and quality of forage varies dramati- the western corridor (Figure 1)at the systems per unit area. Using the most cally in space and time. Ungulates beginning of the wet season and recent estimates of animal popula- solve this dietary problem with a sweeps eastward to the Serengeti tions for the Serengeti ecosystem and series of hierarchical foraging deci- plains as the season progresses. YNP (Houston 1979, Singer and sions that include which plant part In addition to the general pattern Mack 1993, Dublin 1995, YNP or species to bite each second, which of green biomass spreading across 1997) and mean adult biomass val- sward in a landscape to graze each the ecosystem through time, plant ues for each of the ungulate species hour, and which region to migrate to production is randomly distributed (Houston 1979, 1982), and assum- each season (Senft et al. 1987, throughout the western corridor and ing that elk (Cervus elaphus),bison, McNaughton 1989). the Serengeti plains early in the wet and pronghorn (Antilocarpa ameri- season because of stochastic rainfall cana)are the predominant grazers of Green waves and nutrition-rich di- events; grazers exhibit an uncanny YNP grassland, we calculated that 1 ets. In the Serengeti, spatiotemporal ability to locate patches of plant ha of grassland supports 94 kg of variation in forage at the regional growth (McNaughton 1979, 1985). ungulate biomass in the Serengeti (spatial) and seasonal (temporal) At the end of the wet season. animals and 37 kg of ungulate biomass in scales is determined primarily by the reverse their movements, eventually YNP. The finding that the 5.8-fold pattern of precipitation across that arriving in the northwest corner by greater rate of consumption in the ecosystem (Figure 1).Each year at the end of the drv season. which is Serengeti., results in onlv a 2.5-fold the beginning of the wet season, mil- often the only area supporting plant greater ungulate biomass indicates lions of wildebeest (Figure 4), zebra, biomass at that time of year that conversion of plant material to and eland (Taurotragusoryx)set out (McNaughton 1979, 1985). ungulate biomass is more efficient in on a long-distance migration from The wet season migration to the Yellowstone (360,000 kJ foragelkg the northwest corner of the Serengeti Serengeti plains has bien attributed grazer)than in the Serengeti (823,085 ecosystem, where they graze tall to avoidance of sticky, muddy soil kJ foragelkg grazer).This difference grasses of open woodlands during and ~redatorsrather than to the mav, in LDart reflect the smaller aver- the drv season. to the southeast sec- sear& for food because during the age size of grazers in the Serengeti tion, &here they graze shortgrass migration much of the Serengeti sup- (116 kg) than in Yellowstone (255 plains in the wet season (Grzimek ports abundant forage biomass kg),which results in a higher specific and Grzimek 1960, Talbot and Tal- (Sinclair 1995).However, an analy- metabolic rate per unit of grazer bio- bot 1963, McNaughton 1979).This sis of 16 minerals required by graz- mass in the Serengeti (Peters 1983). migration represents movement ers, and of two elemental ratios that against a gradient of mean annual affect mineral availability, in young Seasonal migrations rainfall and from heavily weathered, grass leaves collected during the wet infertile (dystrophic)grassland in the season from several locations repre- Animal biomass in grazing ecosys- drv season to volcanic. fertile senting wet, dry, and transitional tems is dominated by migratory her- (eutrophic)grassland in the wet sea- season ranges, respectively-the bivores (Fryxell et al. 1988). These son. Aerial surveys (McNaughton Serengeti plains (where most of the animals face the problem of meeting 1979) indicate that this migration animals were located), the north-

July 1998 515 (McNaughton 1990). In Yellowstone, ungulates undergo a seasonal migration that is func- tionally similar to that of the Serengeti, although it is driven by radically different environmental fac- tors. Yellowstone ungulates migrate along an elevational gradient, between low-elevation winter habitat and high- elevation summer habitat (Figure 1; Meagher 1973, Houston 1982, Frank and McNaughton 1992). Elk and bison (Figure 5) migrating to their summer range track a wave of green biomass as it sweeps up the elevation gradient through the growing season (Frank and McNaughton 1992). These ungulates intensively graze grassland sites for the first month or two after snowmelt, a period of high plant productivity, and then move Figure 4. The 1.5 million wildebeest of the Serengeti ecosystem, each weighing 125 progressively upslope to phenologi- kg, dominate animal biomass in the system, contributing over 60%. cally younger vegetation. They re- verse that movement during the fall, returning to valley bottoms, which accumulate low amounts of snow and support the greatest obtainable forage biomass in the ecosystem dur- ing the winter (Figure6; Meagher 1973, Houston 1982). To examine forage mineral con- tent during the migration to summer range and the effect of plant phenol- ogy on elemental levels of forages, we collected whole-plant samples of dominant grass species each month through the growing season from summer, transitional, and winter range sites. Forages were analyzed for the same essential minerals and elemental ratios as the Serengeti samples (Table 2). N, P, and Na content was highest during the first month of the growing season, and K was highest during the first two months. In addition, the Ca/P ratio increased through the growing sea- important regulators of grazing ecosystem processes. son, suggesting greater Ca interfer- ence of P absorption after the first west corner of the Serengeti, and the Mineralogical analysis of the top 10 month of plant growth. These results western corridor-showed that the cm of soil collected directly beneath indicate that ungulates in YNP track seasonal movements are associated sampled grasses revealed that for all mineral-rich forage as it sweeps up- with the mineral content of the elements except Mg, plant concen- slope through the growing season. grasses that different regions of the trations were significantly related to Together, the findings from both ecosystem support (McNaughton soil concentrations. Thus, patterns ecosystems indicate that one key 1990). Wet season forages were en- of forage quality across the Serengeti property of grazing ecosystems is the riched in nine minerals (ByCa, Co, are spatially linked to a gradient of high spatiotemporal variation in for- Cu, Fe, Mg, N, Na, and P) compared soil fertility that is defined at one ages; another is the close association with dry season forages, with tran- end by the heavily weathered soils between ungulates and the spatial sitional grasses displaying inter- of the dystrophic northwest corner pattern of high-quality forage, a pat- mediate concentrations of many and at the other by the volcanic soils tern that is determined by environ- elements (McNaughton 1990). of the eutrophic Serengeti plains mental factors specific to each graz-

BioScience Vol. 48 No. 7 ing ecosystem. Forage quality varies more among seasonal ranges in the Serengeti than over the growing sea- son in YNP, reflecting the fact that the edaphic effect on plant mineral content in the Serengeti is stronger than the phenological effect on plant mineral content in YNP.

Grassland structure and grazing effi- ciency. Foraging decisions influence not only diet quality but also con- sumption efficiency. This efficiency is important to migratory herbivores, which must balance time invested in energy and nutrient intake with nonfeeding activities, such as rest, reproduction, and travel (McNaugh- ton 1984, Spalinger and Hobbs 1992). Forage yield per bite for cattle (Ludlow et al. 1982) and African buffalo (Syncerus caffer; Prins 1996) Figure 6. Snow cover severely limits access to food for elk and other ungulates in is positively correlated with plant Yellowstone National Park during the winter. Photo: National Park Service. biomass per unit volume (i.e., with biomass concentration). When for- age biomass concentration is below only the green biomass, which repre- findings for the two ecosystems thus critical levels, herbivores may be sents relatively high-quality forage. indicate that the seasonal migrations unable to acquire sufficient energy Comparing maximum forage con- in grazing ecosystems allow animals and nutrients to maintain themselves centrations of up to 11 mg/cm3in the to simultaneously maximize diet (Chacon et al. 1978). Serengeti (see Figure 7a for the grazed mineral content and forage biomass To examine how grazer move- grassland values) with those of YNP obtained per bite. ments are associated with foraging (less than 1.5 mg/cm3; Figure 8) sug- efficiency, we measured plant bio- gests that foraging efficiencies are Positive feedback on grazing effi- mass concentration throughout the substantially greater in tropical than ciency. In addition to enhancing bio- seasonal ranges of migrating animals in temperate grazing ecosystems. Our mass yield per bite by responding to in both the Serengeti and YNP. In both ecosystems, forage biomass Table 2. Mean mineral concentrations (in pglg) and elemental ratios of grasses collected during different months after snowmelt at sites on the winter, transitional, concentration was determined by and summer ranges in Yellowstone National Park. dividing plant standing crop by canopy height, estimated as the rest- Month after snowmelt ing height of a Styrofoam sheet placed Element or ratio' 1 2 3 4 5 on top of the vegetation (McNaugh- Mineral ton 1985, Frank and McNaughton B 7.93abb 5.85a 7.20ab 8.79b 10.lb 1992). In the Serengeti, the maxi- Ca 3187a 3272a 3691ab 4267b 4562b mum biomass concentration during Co 0.43a 0.37a 0.12a 0.52a 0.35a the wet season was dramatically Cu 7.17~ 5.47ab 6.16bc 4.37a 5.68abc Fe 83.4a 8 1.3a 112.9a 100.la 61.9a higher on shortgrass plains (average K 22,380~ 20,033~ 14174b 10,446ab 7908a = 4.3 mg/cm3), where the animals Mg 1415a 1265a 1436a 1509a 1670a were concentrated at the time of sam- Mn 5 8.4a 64.6a 75.9a 83.3a 92.0a pling, than in midgrass (average = Mo 0.88a 0.82a 0.95a 0.89a 0.83a N 33,997d 22512c 17,866b 13,033a 9855a 1.2 mg/cm3) or tallgrass (average = Na 168c 123b 94a lOOab 82a 1.9 mg/cm3)areas (see Figure 7a for Ni 1.64ab 2.29bc 2.87~ 1.14a 1.28ab the grazed grassland values; P 2709d 1643c 1242b 885a 665a McNaughton 1984). Forage biomass Se 1.67b 0.46a 1.Slb 1.89b 2.29b concentration was similarly greatest V 0.93ab 0.72a 0.82ab 1.05b 1.03b Zn 35.6a 26.2a 29.2a 27.7a 35.la in YNP grassland early in the grow- Ratio ing season at precisely the time that Ca/P 1.19a 2.12ab 3.27b 5.54~ 7.96d herbivores were present (Figure 8). CdMo 8.33a 7.71a 7.49a 6.57a 8.29a Benefits conferred to herbivores 'B, boron; Ca, calcium; Co, cobalt; Cu, copper; Fe, iron; K, potassium; Mg, magnesium; Mn, by grazing highly concentrated, phe- manganese; Mo; molybdenum; N, nitrogen; Na, sodium; Ni, nickel; P, phosphorus; Se, nologically young vegetation in YNP selenium; V, vanadium; Zn, zinc. are even greater when considering bValues with different letters are statistically different from one another (a = 0.05).

July 1998 12 - I I I I Figure 7. Forage con- tems, the positive relationship be- a Serengeti centration of grazed and tween forage mineral content and - ungrazedgrasslands. (a) forage biomass concentration averts Serengeti sites include the potential difficulty of simulta- shortgrass (circles),mid- neously optimizing forage quality grass (triangles), and ,- tallgrass (squares). Re- and foraging efficiency. Seasonal drawn from McNaugh- animal movements allow forage to - ton (1984).(b) Yellow- accumulate on ranges occupied by stone. Dotted lines herbivores during "bottleneck" sea- - denote equality (1:l). sons when low or no forage produc- Solid lines are least- tion occurs-that is, the dry season square fits; for the in the tropical Serengeti and winter - Serengeti, r2= 0.646, P in the temperate YNP. Furthermore, < 0.009; for YNP, r2 = ungulates in grazing ecosystems do 0.50, P < 0.03. not simply respond passively to eco- 0 2 4 6 8 system gradients of forage charac- Ungrazed forage concentration (rng/cm3) with teristics; they actually modify veg- age concentration of etation structure, with the result that 1.5 I I I the fenced controls, herbivores increase their own forag- b Yellowstone indicating that the ing efficiency. - densest ungrazed OE 1.2 - 0 vegetation had the Grazer regulation of plant \ greatest capacity to O aboveground production increase in concen- 2 2 - k 0.9 tration in response Grazers have important indirect ef- 2 .2 a to grazing. fects on grassland energy and nutri- Oo , 0 E! Herbivores make ent flows in addition to their direct 2 0.6 - - I forage more concen- consumption of plant biomass. For : ,, trated by reducing example, as described above, defo- 0 ,/, , canopy height more liation promotes shoot growth (Cald- 0.3 - ,, - ,, than aboveground well et al. 1981, McNaughton 1984, , biomass (McNaugh- Coughenour 1985).Grazing removes ,, 0.0 - ' I I I ton 1984). Grazing phenologically older, less produc- 0.0 0.3 0.6 0.9 stimulates regrowth tive tissue, which increases light ab- Ungrazed forage concentration (mg/cm3) from intercalary sorption by younger, more photo- meristems located at synthetically active tissue (Caldwell the base of defoli- et al. 1981, Wallace 1990) and im- spatiotemporal patterns of forage ated shoots and from new stems (i.e., proves both soil moisture status and concentration, ungulates in grazing tillers) that develop at the ground plant water-use efficiency (Mc- ecosystems also increase their con- surface, producing a short, uniform, Naughton 1985). Grazers enhance sumption efficiency by making veg- highly concentrated canopy (Mc- mineral availability by increasing etation more concentrated. In the Naughton 1984). This phenologi- nutrient cycling within patches of Serengeti, the forage biomass con- cally young plant tissue is relatively their waste (McNaughton et al. 1988, centration of grazed short-, mid-, nutritious, so grazers increase the Day and Detling 1990, Holland et and tallgrass plots was significantly nutrient content of their forage at al. 1992). In addition, grazing de- higher than that of paired ungrazed the same time as they stimulate in- creases microbial immobilization of (i.e., fenced) plots (Figure 7a). Across creased yield per bite (McNaughton nitrogen, resulting in greater rates of all sites, grazers increased biomass 1976, 1979, McNaughton et al. net nitrogen mineralization and ni- concentration by an average of 43%, 1982, Detling and Painter 1983). trogen availability to plants (Hol- with shortgrass sites exhibiting a We have already noted that ungu- land et al. 1992). Consequently, un- higher average increase (2.3 mg/cm3) lates in grazing ecosystems increase gulates stimulate allocation to shoot than midgrass (0.8 mg/cm3) or tall- nutrient intake by tracking spa- growth while simultaneously enhanc- grass (1.2 mg/cm3) sites (McNaugh- tiotemporal waves of highly nutri- ing light levels, soil moisture, and ton 1984). In Yellowstone, ungu- tious and concentrated forage sweep- nutrient availability. lates also increased forage biomass ing across vast landscapes. In the The effect of large herbivores on concentration; on average, forage Serengeti, spatiotemporal variation aboveground production in the concentration was 72% higher in in forage quality results from the Serengeti and Yellowstone was ex- grazed grassland than in paired interaction of precipitation and soil amined by comparing productivity ungrazed plots (Figure 7b). Further- fertility gradients. In YNP, forage of grazed grassland with that of more, in both ecosystems the propor- variation results from an elevation ungrazed grassland that had been tion by which grazers increased forage gradient that controls when sites fenced off for 1-2 years (McNaugh- biomass concentration was positively become snow free. In both ecosys- ton 1985, Frank and McNaughton

518 BioScience Vol. 48 No. 7 1993, McNaughton et al. 1996). Figure 8. Relationship Herbivores increased above~round between forage concen- production by an average ofvl02% tration and number of in Serengeti grasslands and 43% in days after snowmelt in Yellowstone grasslands (Figure 9); Yellowstone. Solid tri- angles, all forage; open thus, they dramatically promoted squares, green forage energy capture in both ecosystems. only; dashed line, least- Grazers had more variable effects on squares best fit for all production in the Serengeti, where forage (r2 = 0.27, P < the effects ranged from 8% inhibi- 0.0001); solid line, tion to 344% enhancement, than in least-squares best fit for YNP, where production was stimu- green forage (r2= 0.47, lated from 12% to 85%. Grassland P < 0.0001). sites in the Serengeti encompass broader climatic, edaphic, and con- foliated plants are sumption gradients than those in provided with both YNP, and this difference may ex- sufficient time and plain the greater variability of grazer suitable conditionsto effectsin the Serengeti. Thus, in con- regrow. Thus, the trast to most terrestrial habitats, spatiotemporal dy- Days after snowmelt where climate is the vreeminent namics of grazing factor determining primary pro- ecosystemspromote sustainability de- mineral nutrients, and feed. As a duction and ecosystem energy flow, spite the high chronic herbivory that result, domesticated ungulate bio- ungulates play a major role in regu- these habitats experience. mass on pasture and rangeland tends lating these processes in grazing eco- to be higher than wild ungulate bio- systems. Human transformation of mass in grazing ecosystems (Oester- grazing ecosystems held et al. 1992).Second, herding of The sustainability of domesticated ungulates by humans grazing ecosystems The grazing ecosystems of prehis- does not mirror the movements of tory have largely been converted to wild ungulates. The invention of the Grasslands and wild ungulates have food-producing regions for the windmill-driven water pump and coexisted for tens of millions of years. earth's human population. Cultiva- barbed-wire fencing transformed Their simultaneous emergence dur- tion has claimed approximately 20% grasslands throughout Earth, leading ing the Late Mesozoic (Stebbins of the earth's grasslands (Graetz to more sedentary and concentrated 1981, Gould and Shaw 1983, Archi- 1994), whereas much of the rest of animal use (McNaughton 1993). bald 1996) and concurrent adaptive the grassland habitat has been trans- Therefore, not only are the densi- radiations during the Miocene are formed into pasture and open range- ties of domesticated ungulates often among the most thoroughly docu- land supporting domesticated ungu- higher than those of wild ungulates, mented evolutionary patterns in the lates. These pastures and rangelands but also the spatiotemporal pattern fossil record (Love 1972, Morton differ from grasslands grazed by wild of grazing, which may play an im- 1972, Stebbins 1981, McNaughton ungulates in several important ways. portant role in the recovery of defo- 1991).The long coevolutionary his- First, the manage- tory between grasslands and ungu- ment intent of ani- % lates is testimony to the high ma1 husbandry is to ,\1600 I I I I I I sustainability of the grazing ecosys- maximize the pro- < tem. Key stabilizing elements of this duction of ungulate 31400 - • - habitat ire the large spatial and tem- biomass through vet- poral variation in mineral-rich for- erinary care, preda- 2 1200 - - age; the migratory behavior of ungu- tor control, and sup- . • • - lates, which track high-quality forage plemental water, 2 1000 - • . a . across a large region; and the inter- - - calary meristem of grasses, which Figure 9. Relationship $ '0° . . between rates of above- 0 0 . -.--- allows defoliated plants to regrow. - - ground production in $ 600 0 Because animals are continually :* :- on the move, grazing at any site, grazed and fenced areas b -.--& of the Serengeti (solid 2 400 - % ..o. - although often intense. never lasts 0 . -' - 0 . circles) and Yellowstone ; -$-. long. Furthermore, because ungu- -0 - . National Park (white 200 - • ,-. - lates tend to graze grasslands early -0-- circles).Grazers substan- $ -0-- in the growing season, when forage tially increase above- o .- I I I I I is the most rich in minerals, and then ground production in 0 100 200 300 400 500 600 700 migrate off sites while conditions are bothecosystems. Dotted Fenced aboveground production (g/m2/yr) still favorable for plant growth, de- line reflects equality.

July 1998 519 liated grasses, has been disrupted on of high ungulate use outside of re- Instead, protection of the few graz- rangelands grazed by domesticated serves and by promoting incentives, ing ecosystems that remain is the herbivores. These differences be- such as ecotourism and indemnities, only feasible option for preserving tween systems grazed by wild and for landholders surrounding reserves this rare habitat. As threats to these domesticated ungulates help explain to preserve animal migration routes. ecosystems intensify, it becomes in- the discrepancy between the positive However, completely eliminating creasingly important to develop mea- feedbacks of wild ungulates on for- threats to the integrity of grazing sures for their preservation. age properties versus the neutral or ecosystems will be problematic so negative influences of domesticated long as human settlements occur within Acknowledgments herbivores on forage (Westoby 1985, the boundaries of the annual move- Oesterheld et al. 1992, Milchunas ments of migrating large herbivores. We thank James Coleman, Mary and Laurenroth 1993). Meagher, Myron Mitchell, and Paul Conclusions Schullery for comments on an early The conservation of draft of the paper. This work has grazing ecosystems Studies of the Serengeti ecosystem been supported by the National Sci- and the Yellowstone ecosystem docu- ence Foundation (grant nos. BSR- Wild ungulates are an inextricable ment many common ecological prop- 8505862, BSR-8817934, and DEB- component of the web of energy and erties of grazing ecosystems. Broad 9312435 to Samuel J. McNaughton nutrient flows in grazing ecosystems. abiotic gradients result in high spa- and DEB-9408771 to Douglas A. When ungulates are removed from tiotemporal heterogeneity of forages. Frank), the University of Wyoming grasslands, the functional character Migratory grazers track these spa- National Park Service Research Cen- of the system is altered, transform- tiotemporal patterns to increase their ter, and the Syracuse University ing a consumer-controlled, rapidly diet quality and grazing efficiency. Graduate School. cycling ecosystem into one that is Indeed, environmental gradients pro- detritivore based and slowly cycling. ducing spatial variability in forages References cited Recent evidence suggests that elimi- may be a necessary feature of graz- nating processes, such as fire, that ing ecosystems that contributes to Arcese P, Sinclair ARE. 1997. The role of occur at large spatial scales disrupts the characteristically high grazer bio- protected areas as ecological baselines. Jour- nal of Wildlife Management 61: 587-602. the long-term structural integrity and mass of these habitats (by increasing Archibald JD. 1996. Fossil evidence for a late biodiversity of grassland fragments the availability of high-quality for- Cretaceous origin of "hoofed" mammals. (Leach and Givnish 1996). Eliminat- age to mobile animals) as well as to Science 272: 1150-1 153. ing grazers that migrate over vast, ecosystem sustainability (by ensur- Berger J. 1991. Greater Yellowstone's native ungulates: Myths and realities. Conserva- spatially heterogeneous environments ing a natural rhythm of vegetation tion Biology 5: 353-363. by fragmenting grazing ecosystems defoliation-regrowth at any particu- Burrows R. 1995. Demographic changes and into grassland remnants similarly lar site). social consequences in wild dogs, 1964- alters the fundamental ecological char- A continuum exists among graz- 1992. Pages 400-420 in Sinclair ARE, acter of those fragmented habitats. ing ecosystems, from relatively less Arcese P, eds. Serengeti 11: Dynamics, Management, and Conservation of an The world's few extant grazing productive and moderately grazed Ecosystem. Chicago: University of Chi- ecosystems face large and growing temperate grassland (e.g., Yellow- cago Press. threats. As human populations con- stone) to highly productive and Caldwell MM, Richards JH, Johnson DA, tinue to increase around the bound- heavily grazed tropical grassland Nowak RS, Dzuree RS. 1981. Copingwith herbivory: Photosynthetic capacity and aries of these systems, animal move- (e.g., the Serengeti). Because of feed- resource allocation in two semiarid Agro- ments in and out of grassland reserves back mechanisms in which herbi- pyron bunchgrasses. Oecologia 50: 14-24. are becoming increasingly limited vores promote plant growth, grazers Chacon EA, Stobbs TH, Dale MB. 1978. (Western and Pearl 1989, Arcese and are important regulators of ecosys- Influence of sward characteristics on graz- Sinclair 1997).In addition, diseases tem processes in grazing ecosystems. ing behaviour and growth of Hereford steers grazing tropical grass pastures. transmitted from the outside threaten Stronger feedbacks in the Serengeti, Australian Journal of Agricultural Re- some wildlife populations in reserves, including larger ungulate effects on search 29: 89-102. such as that of the African wild doa- grazing efficiency and aboveground Coughenour MB. 1985. Graminoid responses (Lycaon pictus) in the Serengeti (Bur- primary production, suggest that to grazing by large herbivores: Adapta- tions, exaptations, and interacting pro- rows 1995). Fear of diseases being herbivores and other ecosystem com- cesses. Annals of the Missouri Botanical transmitted from ungulates migat- ponents are more tightly linked in Garden 72: 852-863. ing out of reserves to livestock has tropical grazing ecosystems than in Day TA, Detling JK. 1990. Grassland patch led to animals, such as bison in YNP, temperate grazing ecosystems. dynamics and herbivore grazing prefer- The grazing ecosystem is among ence following urine deposition. Ecology being slaughtered at the wilderness 71: 180-188. boundary (Meagher and Meyer Earth's most endangered terrestrial Detling JK. 1988. Grasslands and savannas: 1994). The fundamental problem habitats. The region-size reserves Regulation of energy flow and nutrient with resDect to the conservation of required to support the unique eco- cycling by herbivores. Pages 131-148 in grazing ecosystems is that these habi- logical processes of these systems Pomeroy LR, Alberts JJ, eds. Concepts of Ecosystem Ecology: A Comparative View. tats are incompletely protected. 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