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Journal of the Torrey Botanical Society 133(4), 2006, pp. 626–647

Evolution and origin of the Central of : , fire, and mammalian grazers1 Roger C. Anderson2 Behavior, Ecology, Evolution and Systematics Section, 4120 Department of Biological Sciences, State University, Normal, Illinois 61790

ANDERSON, R.C. (Behavior, Ecology, Evolution and Systematics Section, 4120 Department of Biological Sciences, Illinois State University, Normal, IL 61790). Evolution and origin of the Central Grassland of North America: climate, fire, and mammalian grazers. J. Torrey Bot. Soc. 133: 626–647. 2006.— are a widespread type that once comprised 42% of the cover on ’s surface. Features commonly shared among grasslands are with periodic , that are level to gently rolling, high abundances of animals, and frequent fires. World-wide expansion of grasslands occurred 8 to 6 MaBP and was associated with increasing abundance of grasses using the C4 photosynthetic pathway, a decline in , and coevolution of adapted to grazing and open . Beginning with Transeau’s seminal paper on the peninsula in 1935, North American ecologists debated the relative importance of fire and climate in determining the distribution of grasslands. In the 1960’s, a major research interest was the response of to fire, especially the productivity of burned and unburned grasslands. Understanding mechanisms for increased productivity on burned prairies began in the late 1960’s and continued into the middle 1980’s. During the past 20 to 25 years, grassland research has focused on the coevolution of grasses and mammalian grazers and fire-grazing interactions that affect heterogeneity and diversity across trophic levels. While this paper does not follow a chronological development of our understanding of grasslands, all of these major research interests are considered. Key words: , C4 grasses, Central Grassland, fire, grasslands, keystone species, mammalian grazers, prairie peninsula.

General Features of Grasslands. DISTRIBU- et al. 2000). This seemingly high estimate for TION AND STATUS. Grasslands occurred on all extant grasslands, however, results from in- continents, comprised almost 42% of the cluding not only ‘‘non-woody grasslands’’ but world’s plant cover, and once covered approx- also , woodlands, , and imately 46 million km2 of the earth’s surface. in the definition of grasslands. This Grasslands contain few or shrubs, are estimate of existing grassland is potentially dominated by grasses (members of the family misleading, because most ecologists would not ), and have a mixture of non-grami- include woodlands, shrublands, and tundra in noid herbaceous species called . Plant a definition of grasslands. In addition, while families most abundant as forbs are the this source recognizes that temperate grass- sunflower (Asteraceae) and pea (Fabaceae) have experienced heavy conversion to families (Curtis 1971, Risser et al. 1981). , it states that at least five percent of Extensive grasslands have been greatly altered grasslands world-wide are ‘‘strongly to ex- by human activity especially those associated tremely denuded.’’ This relatively low percent- with their conversion to agricultural - age possibly results from the inclusion of non- scapes for growing crops or grazing livestock. traditional landscapes in the definition of Nevertheless, a recent estimate is that about 40 ‘‘grasslands.’’ Applying a more widely used percent of the global land surface is grassland definition of grasslands, many of the world’s (excluding Greenland and ) (White temperate grassland have been essentially destroyed by human activities. For the , Noss et al. 1995) lists 1 A substantial portion of this manuscript is grasslands as being critically endangered (i.e. reproduced with permission from a book on fuel have declined by more than 98 ). For management being published by the USDA % Service, entitled ‘‘Cumulative Watershed Effects of example, 99% of the lying Fuel Management in the Eastern United States.’’ east and north of the River has been 2 I thank M. Rebecca Anderson for reviewing and completely destroyed (Chapman et al. 1990). commenting on this manuscript. E-mail: rcander@ In Illinois, of the 8,502,024 ha of original ilstu.edu Received for publication November 13, 2006, and prairie (60% of the state), only 931 ha or 0.01 in revised form December 5, 2006. percent of high quality remnant prairie re-

626 2006] ANDERSON: EVOLUTION AND ORIGIN OF GRASSLANDS 627 mains (Robertson et al. 1997). In this review, I of periodic droughts, frequent burning, and summarize the results of more than fifty years grazing animals and are adapted to all three of research studies of grassland ecosystems (Gleason 1922, Anderson 1990). This adapta- with a focus on the Central Grassland of tion for grasses is manifested in their ability to North America. While these studies were die down to underground organs and only conducted in a highly fragmented , expose dead tops above ground (Gleason some on prairies that are ten hectares or less in 1922). Grasses can escape by having size, they provide an overview of the structure growing tips beneath that are not exposed and function of the historic grassland ecosys- to desiccation. Prairie fires have a narrow tem, which none of the researchers experi- flame width and move relatively rapidly and, enced, and provide insight into how they because the soil is a good insulator, there is might be restored. little penetration of heat into the soil beyond a few mm below the surface (Anderson 1982). One of the most marvelous sights of my Consequently, the growing points of prairie whole life, unsurpassed in my travels in below the ground surface are protected nearly all parts of the world, was that of the from the heat of the fire and also from grazing. prairie in spring. Unfading are my memo- Grazers can remove aboveground tissues, but ries of that waving rippling sea of lavender, new shoots can emerge from belowground when the wild sweet william, a species of once the grazing pressure is removed (Tainton phlox two or three feet in height was in full and Mentis 1984). flower. It stretched away in the distance The adaptation of grasses to fire, drought, farther than the eye could reach…As the and grazing animals may represent a preadap- sea of phlox faded it was succeeded by tation of grasses to one or more of these another marvelous flower bed of nature’s factors; however, grasses and likely planting, and this in turn by others until co-evolved based on other features of grasses. mid-summer was reached…(Herre 1940). The post- expansion of grasslands and savannas worldwide was associated with CLIMATE. No single climate characterizes the adaptive radiation of large mammals grasslands and they occur in areas of the earth adapted to grazing (Stebbins 1981, Anderson that receive as little as 200 mm of precipitation 1982, 1990; Axelrod 1985, McNaughton 1993, annually to areas that receive 1300 mm annu- Oesterheld et al. 1999). Adaptive responses of ally, and in areas where mean annual tempera- grasses to herbivores that reflect a coevolution- tures vary from 0–30uC (Sauer 1950, Risser et ary relationship between grazers and grasses al. 1981, Oesterheld et al. 1999). Grasslands are includes the presence of silica in epidermal not necessarily treeless and they are transition- cells of grasses, perennating organs below al to savannas that are characterized by higher ground level, and aboveground production in densities of drought-tolerant, fire-resistant excess of that which decomposes in a single trees than grasslands. The ratio of trees/grass year (Stebbins 1981, Anderson 1982, 1990). increases as precipitation increases (Curtis The widespread expansion of grassland is 1971, Anderson and Bowles 1999, Oesterheld associated with the appearance of the C4 et al. 1999) and in landscapes receiving more photosynthetic pathway. The C4 photosyn- than 650 mm of precipitation there is a trend thetic pathway provides an advantage over the for increasing cover of woody species with more common C3 pathway because it provides ‘‘long-term fire exclusion’’ (Sankaran et al. higher quantum yields for carbon dioxide 2004). In areas of low precipitation, grasslands uptake under conditions of high irradiance grade into communities. Common and temperature. The C4 photosynthesis is features found among grasslands include: also favored over C3 photosynthesis when the climates with periodic droughts, frequent fires, concentration of atmospheric carbon dioxide occurrence on landscapes that are level to is below 500 ppmV (Cerling et al. 1997, gently rolling, and an abundance of grazing Ehleringer et al. 1997, 2002). During the animals (Saur 1950, Risser et al. 1981, Ander- Mesozoic, carbon dioxide concentrations were son 1982, Anderson 1990). thought to be greater than 1000 ppmV. However, in the early Miocene or late DROUGHT,FIRE, AND GRAZING ANIMALS. (Kellogg 1999), perhaps 20–25 Grassland plants evolved under the influence MaBP, decline in atmospheric carbon dioxide 628 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL.133 favored evolution of C4 plants in moist describe the extensive grasslands of North tropical and subtropical regions (Ehleringer America (Curtis 1971, Risser et al. 1981). et al. 1997). This photosynthetic pathway is Along a north-south gradient, grasslands found in less than 2% of all flowering plants extended from desert grasslands of southwest- but approximately one-half of the 10,000 ern United States and northern and central species of grasses and sedges use this pathway. to mixedgrass prairies of the Canadian While C4 plants are a small percentage of Provinces of , , and flowering plants, they contribute 25% of total (Risser et al. 1981). Across this global productivity, largely due to monocots gradient mean annual temperatures vary from in grasslands (Eherlinger et al. 2002). 2.8uC at Regina, in the northern Accelerated development of C4 grasslands mixedgrass prairie to 22.6uC in Monterrey, world-wide occurred during the Miocene- Mexico at the edge of Chihuahuan Desert transition (8-6 MaBP) when aridity grasslands. From south to north along the increased world-wide associated with the eastern edge of grasslands lying east of the expansion of the Antarctic Ice Sheet and , precipitation varies from atmospheric carbon dioxide was below about 250 mm in southeast to 750– 500 ppmV. During this period of time, the 1000 mm in (Risser et al. 1981). area occupied by forest and woodlands de- clined and there was an explosive evolution of Central Grassland of North America. grasses and forbs (Cerling et al. 1997, Ehler- GEOGRAPHIC VARIATION. This papers focuses inger et al. 1997, 2002). However, Keeley and on the Central Grassland of North American, Rundel (2005) posit that the conversion of which was a large triangular shaped grassland forest to C4 grassland four to seven MaBP whose base extended from the Canadian was not directly due to a decline in atmo- provinces of Alberta and Saskatchewan south- spheric carbon dioxide or increased aridity, ward along the eastern of the Rocky but rather to a climate change that encouraged Mountains and then to southeastern Texas fire. Under the new climatic conditions a warm (Outlined in Figure 1). The point of the moist growing resulted in high triangle extended well into the Midwest in production that was converted into combusti- southwestern , Illinois, and western ble fuels by a pronounced dry season. This Indiana, with scattered outliers in Michigan, monsoon climate likely would be accompanied , and Kentucky. This area includes the by frequent lightning strikes at the end of the grasslands of the twelve Great states, dry season. In the Keeley-Rundel (2005) and those grasslands described above lying model, fire would have been a primary driver, east of the River. Precipitation as it is today, in the conversion of forest to increases from west to east in this grassland grasslands and the maintenance of grasslands. from 260–1200 mm and across a north-south Expansion of open grassland and gradient annual temperature ranges from 3– habitats was associated with increased fossil- 22uC (Sala et al. 1988). ized silica bodies in the epidermis of grasses, Ecologists traditionally have divided the which provide protection against grazing. grassland into three sectors based on height Concomitantly, there was an increase in of the native grasses, which is a function of mammalian fossils with high-crowned teeth annual precipitation: a western shortgrass (hypsodonty) adapted to grazing (Stebbins prairie (260–375 mm precipitation), the east- 1981, Axelrod 1985) and evolution of animals ern tallgrass prairie or ‘‘True Prairie,’’ (625– with more cursorial (running) and saltational 1200 mm precipitation), and between the two (jumping) body forms. the mid- or mixedgrass prairie (375–625 mm precipitation) (Fig. 1). oc- The North American Grassland. Grasslands cupies an area dominated by grasses that are of North America constitute a diverse assem- 0.3–0.5 m tall, which includes buffalo grass blage of vegetation types that occur under (Buchloe dactyloides), blue grama (Bouteloua a wide range of climatic conditions and gracilis), and side oats (B. curtipendula)and covered about 15% of the continent (Fig. 1). hairy (B. hirsuta) grama grasses. Big bluestem These grasslands are referred to as prairies, (Andropogon gerardii), Indian grass (Sorghas- a French word meaning or , trum nutans), switchgrass (), which was used by early French explorers to and little bluestem (Schzachyrium scoparium) 2006] ANDERSON: EVOLUTION AND ORIGIN OF GRASSLANDS 629

FIG. 1. The distribution of the major grasslands of North America and the air masses that influence the climate of the Central Grassland. The location of the Central Grassland is outlined. Adapted from Risser et al. 1981 and Anderson 1990. Reprinted from Anderson 1990 with permission of the University of Press. are dominant species in the tallgrass prairie divisions between these arbitrarily designated and reach heights of 1.8–2.4 m. The mixed- grassland regions. grass or midgrass prairie is dominated by species that are 0.8–1.2 m tall and includes VARIATION WITHIN A GEOGRAPHICAL REGION. little bluestem, western wheatgrass (Pasco- Within each of the major regions of the pyrum smithii), and green needle grass (Nas- Central Grassland there are different types of sella viridula). In the mixedgrass prairie, prairie as a function of soil, aspect, slope tallgrass prairie species occur in depressed position and other factors. A primary factor areas that are moister than upland sites causing these varied vegetation patterns is resulting in a mixture of tall- and midgrass availability of soil moisture as a function of prairie species, which gives the midgrass variation in and topographic features prairie region its alternate designation of (Curtis 1971, Nelson and Anderson 1983, mixedgrass prairie. Across the Central Grass- Umbanhowar 1992, Corbett and Anderson land, species composition and abundance 2006). For example, there are approximately varies continuously and there are no sharp 930 hectares of high quality remnant prairie in 630 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL.133

Table 1. Leading species in six community types for species with mean (6 SE) quadrat frequency at least 2.0%. Letters after species names indicate its modal community in Wisconsin (Curtis 1971), PD5 dry prairie, PDM 5 dry mesic prairie, PM 5 mesic prairie, PWM 5 wet mesic prairie, PW 5 wet prairie, DUN 5 dune, OB 5 barren, CG 5 cedar glade, SB 5 sand barren, FN 5 , SS 5 southern sedge meadow, ND 5 Northern Dry Forest (Modified from Corbett and Anderson 2001, 2006).

Gravel/dry Mesic/dry Wet/wet Community type species Dry sand Gravel/sand Hill prairie dolomite mesic dolomite PD 16.9 6 1.5 17.3 6 2.9 15.4 6 0.7 11.6 6 1.4 3.6 6 0.4 Optunia humifusa CG 8.4 6 1.8 Ambrosia psilostachya SB 6.7 6 2.2 DUN 3.9 6 2.0 Panicum oligosanthes PDM 3.3 6 1.7 2.4 6 1.6 Tephrosia virginiana OB 3.3 6 1.7 Bouteloua hirsuta CG 2.3 6 1.5 Stipa spartea PDM 2.0 6 1.0 4.4 6 2.4 4.5 6 1.0 Euphorbia corollata OB 5.4 6 2.0 3.6 6 0.4 Echinacea pallida PM 3.1 6 2.0 3.4 6 0.6 Lithospermum caroliniense SB 2.7 6 2.2 Koeleria cristata SB 2.5 6 2.0 Callirhoe triangulata PDM 2.3 6 1.6 PD 9.1 6 0.8 3.8 6 0.8 PDM 4.5 6 0.7 4.4 6 0.4 DP 2.2 6 2.2 4.5 6 0.4 Euphorbia corollata OB 4.1 6 0.4 4.6 6 0.7 Solidago nemoralis DP 3.6 6 0.5 Psoralea tenuiflora 2.8 6 0.4 Aster azreus DMP 2.5 6 0.5 canescens DP 2.3 6 0.4 3.6 6 0.7 DP 3.0 6 0.6 3.0 6 0.4 Rosa caroliniana 2.5 6 0.6 2.4 6 0.3 Aster ericoides PDM 2.3 6 0.6 3.6 6 0.4 Andropogon gerardii PM 5.0 6 0.5 2.5 6 0.7 Fragaria virginiana ND 2.2 6 0.3 2.7 6 0.8 Carex sp. 6.3 6 1.8 Solidago gigantea PW 4.3 6 0.9 Pycnanthemum virginianum 3.7 6 0.8 PWM Calamagrostis canadensis FN 3.5 6 1.5 Spartina pectinata PW 3.2 6 0.8 Carex stricta SS 2.2 6 2.1 Helianthus grossesserrratus 2.7 6 1.1 PWM FN 2.7 6 0.9

Illinois representing diverse habitat types CLIMATE OF THE CENTRAL GRASSLAND. Major differing in topography and substrate. Dry Air Mass Systems. The climate of the Central prairies includes hill and bluff prairies that Grassland is influenced by three primary air often occupy west or southwest facing slopes mass systems (Fig. 1): Polar, Gulf, and Moun- overlooking rivers with or glacial drift tain Pacific (Borchert 1950, Bryson and Hare derived soils (Evers 1955). Dry prairies also 1974, Risser et al. 1981). The Polar Air Mass occur on deep sand deposits or on dolomitic or influence is reflected in part by the increased gravel substrates with shallow stony soils. snow cover and decreasing temperatures from Additionally, there are wet-mesic to wet south to north within the Central Grassland prairies on loess-derived, till-derived, or dolo- (Risser et al. 1981) and the resultant north- -containing substrates (Table 1). Histori- south variations in vegetation patterns (Risser cally, the most common prairie types were et al. 1982, Kebart and Anderson 1987, mesic and wet prairies covering as much as Diamond and Smeins 1988). Gulf and Moun- 55% of the state (Fehrenbacher et al. 1968), tain Pacific Air Masses are most important in although most of these prairies have been determining the east-west variation in the converted to agricultural or urban uses. Central Grassland. The Gulf Air Mass origi- 2006] ANDERSON: EVOLUTION AND ORIGIN OF GRASSLANDS 631 nates in the . As the Gulf Mass extension into the Midwest that was oak- moves northward into the eastern sector of the hickory forest (Delcourt and Delcourt 1981). Central Grassland it brings humid air and In the eastern tallgrass prairie, prairie and often is associated with precipitation when it savanna replaced oak-hickory forest during encounters cooler air or generates moisture for the warm, dry period of the Hypsithermal, convectional storms. The Mountain Pacific which was accompanied by an increase in fire Air Mass arrives on the west as a humid frequency, beginning about 8,000 YBP and air mass. However, as it progresses eastward ending 5,000–3,500 YBP depending upon the air mass passes over several western location (Delcourt and Delcourt 1981, King mountain ranges (Coastal, Sierra, and Rocky 1981, Winkler et al. 1986, Winkler 1995, 1997, mountains). As the air mass rises, it cools Baker et al. 1996, Anderson 1998). Using adiabatically, and gives up much of its Illinois to illustrate changes in climate and moisture as orographic precipitation. The air vegetation during the , the drying mass is compressed by an increasing volume of trend of the Hypsithermal began about 8,700– atmosphere as it descends to lower elevations 7,900 YBP. A few hundred years later prairie on the east side of the Rocky Mountains, was present in . At the same causing the air mass to become warmer and time as prairie influx into central Illinois, more arid as it spills out into the . mesic forest was replaced by oak-hickory Thus, the Central Grassland occurs in the forest in northern Illinois. At the peak of the shadow of the western mountains. Hypsithermal in Illinois (8,000–6,000 YBP) From west to east in the Central Grassland, prairies occupied most of the state (King the frequency of the Pacific Air Mass 1981). A similar pattern of vegetational change decreases and the frequency of the Gulf Air occurred in northeastern (Baker et al. Mass increases. Associated with the change in 1996) and southern Wisconsin (Winkler et al. air mass frequency, mean annual precipitation, 1986, Winkler 1995, 1997), but the timing was periodic droughts, and periods of low humid- somewhat different (Anderson 1998). ity during summer decrease from west to east According to Axelrod (1985) the recent in the grassland (Transeau 1935, Borchert origin of the Central Grassland is indicated 1950, Bryson and Hare 1974, Risser et al. by the occurrence of most of its species in 1981). This west-east climatic variation causes forest and woodlands, presence of few endem- the changes in vegetation from the foothills of ic plants (Wells 1970a) insects, (Ross 1970) or the Rocky Mountains to the Midwestern (Mengel 1970, Risser et al. 1981), the United States that results in the short-, mixed- relict occurrence of a variety of species and tallgrass prairies. Annual net primary throughout the region, and the current in- production is also affected by this climatic vasion of woody plants into the grassland. gradient and in years of average precipitation Benedict et al. (1996) indicate that, among varies from 150–600 g m22 from west to east mammals, true grassland species comprise in the Central Grassland (Sala et al. 1988). only 11.6% of those occurring on the central and northern plains and only 5.3% of North History. While grasslands may American species evolved on prairies have been present on the North American (Knopf 1996). Similarly, many of the grass continent for 20 million years (Weaver 1968, species that occur in the central grassland Risser et al. 1981, Axelrod 1985, Benedict et al. evolved in eastern forest openings, the south- 1996), the Central Grassland is of relatively west or in mountain (Glea- recent origin. During the Pleistocene, climate son 1922, Risser et al. 1981). change and the continental ice sheet caused destruction of the mid-continent grassland or The Prairie Peninsula. LOCATION AND ORIGIN. its replacement by other vegetation types. At Near the and eastward in the the peak of Wisconsin glaciation (18,000 Central Grassland the climate becomes in- YBP), most of the Central Grassland was creasingly favorable for trees. The wedge-like dominated by spruce and jack pine forest or extension of the grassland into the Midwestern covered with glacial ice. During the early United States is called the prairie peninsula, Holocene, 10,000 YRBP, grasslands or oak because it is a peninsula of grass extending savanna occurred in much of the current into a forested region (Fig. 2) (Transeau central grasslands, except for the eastern-most 1935). Annually, this region receives 750– 632 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL.133

FIG. 2. The prairie peninsula from Transeau 1935 with permission from the Ecological Society of America.

1200 mm of precipitation, a climate capable of there was a loss of trees from upland sites supporting forest. Historically, ecologists have during the droughts of the 1930’s and their debated why this area had grasslands rather retreat to sheltered locations adjacent to than forest (Transeau 1935, Curtis 1971). streams. Seedlings are strongly affected by Several general hypotheses emerged to explain drought and competition from grasses directly this vegetational pattern. One hypothesis and indirectly through production of flamma- focused on the importance of climate as ble, finely divided fuels that encourage the a primary determinate of vegetation patterns. spread of fire (Anderson 1990, Sankaran et al. The other hypotheses posited that fires set by 2004). Native Americans or soil conditions were responsible for absence of trees. DROUGHT AND ROOTING DEPTH. The differ- ential effects of drought on prairie grasses and CLIMATE EFFECTS. Transeau (1935) reasoned trees have been explained by the growth that climatic extremes were more important forms of the two groups of plants. In tallgrass than averages in determining the distribution prairie in Missouri, 80% of the root mass of . He demonstrated that the occurred in the upper 25 cm of soil (Dahlman prairie peninsula has periodic droughts when and Kucera 1965), and similar results were there is essentially a shifting of the drier reported by other investigators (Zink and western climatic conditions eastward into the Weaver 1946, Old 1969, Bartos and Jameson prairie peninsula. These periodic droughts 1974, Risser et al. 1981). Although prairie would favor the prairie and set back the plants have most of their in the upper forest. Indeed, during the droughts of the layers of the soil, many prairie plants have 1930’s, trees experienced high rates of mortal- deep root penetration (Rooting Depth for 14 ity in the prairie peninsula (Albertson and grasses and 15 forbs, Range 5 0.5–7 m, mean Weaver 1945). Transeau (1935) noted that 6 SE 5 2.36 6 0.24 m, original data from 2006] ANDERSON: EVOLUTION AND ORIGIN OF GRASSLANDS 633

Weaver 1954, recalculated by Risser et al. under cool moist conditions and are known as 1981). Scholes and Archer (1997) suggest that ‘‘cool season grasses.’’ The C3 grasses have in habitats with grasses, available evidence lower water use efficiency, photosynthetic suggests maximum rooting depth of trees is rates, and photosynthetic temperature optima generally greater than that of grasses. They and saturation levels for solar radiation, but also note that trees and grasses have the higher rates of photorespiration and higher maximum amount of their root mass in the CO2 compensation points than C4 plants. upper soil layers. Nevertheless, grasses may be Seasonal separation of C3 and C4 grasses. less dependent upon deep soil moisture than In North America, the primary separation of are trees (Schimper 1903, Walter 1971). C4 and C3 grass is related to temperature Britton and Messenger (1969) suggested (Terri and Stowe 1976). Where daytime that droughts that do not permit recharge of growing season temperatures are below 22 C, deep soil moisture are more detrimental to u C3 plants should dominate and where growing trees than grasses. Grasses can take advantage season temperatures are above 30 C, with of light showers that recharge the soil surface u layers because of their diffuse root system that adequate soil moisture, C4 plants should is concentrated in the upper portions of the predominate (Ehleringer et al. 1997). On soil. In the prairie peninsula, recharge of deep a latitudinal gradient, C4 plants should have soil moisture usually occurs during the dor- a higher quantum yield for carbon dioxide mant season, because high rates of evapo- fixation than C3 plants at latitudes less than transpiration during the growing season re- about 45u and C3 plants should have higher duce the likelihood of deep soil moisture quantum yield above that latitude (Ehleringer recharge. In the Midwest, areas that did not 1978). Where the two groups of grasses grow experience deep soil moisture recharge during together in the Central Grassland, the C3 the winter period of 1933–34 corresponded to grasses, e.g. wild rye, (Elymus canadensis), the location of the prairie peninsula (Britton Western wheatgrass ( smithii), and Messenger 1969). This finding supports green needlegrass ( viridula), porcu- the hypothesis that drought is an important pine grass (), and prairie factor in determining the occurrence of the Junegrass (Koeleria macrantha), grow in the prairie peninsula. spring and early summer, whereas the C4 grasses (e.g., big bluestem, Indian grass, GRASS ADAPTATIONS TO DROUGHT. Morpho- switchgrass, little bluestem, hairy and sideoats logical and Physiological Features. There are grama grasses) begin growth later than the C3 many morphological and physiological fea- grasses and maximize growth in mid-summer. tures that allow grasses to tolerate high Even though the C4 grasses are more drought moisture stress including (1) the occurrence tolerant than C3 grasses, during the drought of bulliform cells in leaves that cause them to of the 1930’s western wheatgrass increased its enroll when they loose water, thereby reducing abundance more than many C4 grasses. leaf surface area for transpiration, (2) utiliza- During several years it was able to utilize tion of the C4 or Hatch photosynthetic moisture that was available in the early pathway that adapts plants to high tempera- spring that was then unavailable to the later tures, high levels of solar radiation, and growing C4 grasses (Weaver 1968, Monson periods of moisture stress. The C4 plants have et al. 1982). high water use efficiency, stomatal sensitivity to water loss, and photosynthetic rates, and FIRE AS A FACTOR. Climate and fire in the ability to grow under conditions of low the Holocene. Following the end of the soil-water potential (Ares 1976, Briske and Hypsithermal the prairie peninsula climate Wilson 1978). While many of the dominant became cooler and moister and more favor- grasses in the Central Grassland are C4 able for trees. Following this climatic change, grasses, including Indian grass, big bluestem, stabilization of the vegetation in the prairie switchgrass, little bluestem, sideoats and hairy peninsula is thought to be due to fires set by grama grasses, there are many species of C3 Native Americans and occasional lightning grasses that dominate some prairies. The C3 strikes in a climate that could support prairie, plants only use the Calvin Cycle in dark savanna, or forest (Curtis 1971, Anderson fixation of carbon dioxide, maximize growth 1990, 1991a, 1998). 634 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL.133

Again fire has killed the trees over After the first frost, in the autumn of 1835, wide areas on which grass was growing, had killed the millions of tons of grass west exhibiting before our eyes nature’s of us, we began at Pike River, to see the simple method of converting into rising smoke at a distance. The Indians prairie. The reverse process is just as probably had fired the prairies as early as simple. When prairies are no longer swept they could for hunting purposes. It was over by fire, timber springs up, reconvert- sometime in the latter part of September. ing prairie into woodland. Grass, with fire We began to see the advancing fire toward as its ally, can beat timber. Timber can evening on the prairie, three miles west of beat grass when it has no fire to fight us; and before twelve o’clock it became (Wight 1877). a serious affair. The wind was from the south-west, and pretty strong, and the fire Effect of fire on prairies and woody species. progressed rapidly… The roaring terror Prairie fires can reach temperatures of 83 to came through the woods with awful 680uC on the soil surface (Wright 1973, grandeur. Large trees, as well as all Wright and Bunting 1975, and Parenti smaller vegetation, quickly fell before the 1978). Gibson et al. (1990) reported that on ruthless invader. (Lothrop 1856). Konza Prairie in fire temperatures varied from 166 to 343uC as a function of Ignition by lightning and humans. Light- habitat, upland or lowland site, and time since ning as an ignition source was important in the last fire, all of which affected fuel loadings. As western portion of the Central Grassland and previously noted, prairie grasses are protected can cause prairie fires during the growing from fire because their growing points are season, if the vegetation is dry (Anderson located beneath the soil surface and there is 1982, Howe 1994a,b, Bragg 1995). In Ne- little penetration of heat below the soil surface braska, in the western portion of the tallgrass (Reichert and Reeder 1972, Anderson 1982). prairie, lightning fires averaged 138 per year Fire is detrimental to trees because their between 1971 and 1975 and the historic fire aboveground growing points, shoot apical season was from spring through fall. Grass- meristems and vascular cambium, are exposed lands in the Great Plains originated during the and vulnerable to fire. Woody species can be Holocene and Native Americans have been on killed by fire or their shoots destroyed. Even if the continent for the past 30,000 years (Bragg woody plants resprout, they lose several years 1995). They used fire as a vegetation manage- of growth, which reduces their competitiveness ment tool for a variety of reasons including against grasses. Anderson and Brown (1986) encouraging the growth of the prairie, pre- reported that after a single fire in a forest venting the encroachment of woody species adjacent to sand prairie in central Illinois, into grasslands, as a tool for hunting, control- 34.1% of blackjack oak (Quercus marilandica) ling insect, easing travel, and for other reasons and black hickory (Carya texana) trees greater (Stewart 1956, Curtis 1971, Pyne 1983, 1997, than 9.0 cm (dbh) suffered mortality during Anderson 1990, 1997). Consequently, light- the first year following the fire, and 4.9% and ning and Native Americans were both re- 8.5% in the second and third years after the sponsible for igniting grassland fires. There burn, respectively. Frequent fire and periodic may have been frequent summer fires in the droughts may have interacted to effectively Great Plains, because Native Americans and control woody plant invasion into grasslands, lightning set summer fires (Devoto 1963). In especially on sites supporting mesic species, the northern Great Plains, 85% of lighting such as sugar maple (Acer saccharum), ashes caused fires occurred in June, July and (Fraxinus spp.), elms (Ulmus spp.), and bass- August, whereas Native American set fires wood (Tilia americana) that are more suscep- occurred in almost every month, but a majority tible to fire and droughts than . Even if were set in autumn and late summer (Higgins the trees resprout, browsing by and 1986, Ewing and Engle 1988). Summer fires may have kept woody species from dominat- are smaller those set during the dormant ing grasslands (Anderson 1982). Sankaran et season and lightning set fires are often al. (2004) suggested that through fuel re- extinguished by associated with the duction grazers favor trees but browsers storm that generated the lightning strikes encourage grass. (Bragg 1995). 2006] ANDERSON: EVOLUTION AND ORIGIN OF GRASSLANDS 635

However, in the more humid eastern por- frequency. Landscapes that are nearly level tion of the Central Grassland, where rainfall to slightly rolling can support the nearly usually accompanies lightning storms, most annuals fires that grasslands need for their fires were apparently set by Native Americans maintenance (Curtis 1971, Risser et al. 1981, (Curtis 1971, Pyne 2001). In the eastern Anderson 1982, 1990, 1991a). A regime of tallgrass prairie, fires occurred most frequently repeated fires might not be able to eliminate during the dormant season. Historical evi- fire resistant woody species from grasslands dence suggests that a large proportion of the but it can keep them in a reduced state and fires occurred in the autumn, during the period dependent upon recurring annual growth from known as ‘‘Indian summer’’ (McClain and roots for survival (Curtis 1971, Bragg and Elzinga 1994), a warm, dry period following Hulbert 1976, Heisler et al. 2003). In dissected killing frosts in the autumn, late October and landscapes fires move rapidly up slopes, as the early November. Howe (1995) suggested that fire is carried upward by rising convection North American grasslands evolved under currents. However, as the fire moves down a lightning caused summer fire regime since slope its movement is impeded by the upward grasslands were on the continent millions of flow of the convection currents. Steep slopes years before humans migrated to North and ravines function as fire breaks and provide American. He considers the dormant season sheltered locations where can survive fire regime that characterizes anthropogenic (Anderson 1998). Using a map of the historic set fires not to be typical of the fire regime that distribution of ‘‘timber’’ (forest/savanna) and shaped the North American Grasslands. prairie in Illinois (Anderson 1970) and distri- Nevertheless, the post-Pleistocene grasslands bution of average slope range in the state, of North America are of recent origin, as Anderson (1991a) examined the relationship previously noted, and do not predate the between topography and historic distribution arrival of humans on the continent and for of vegetation. About 60% of the state was the most part contain species that are not tallgrass prairie (Anderson 1991a,b, Robert- restricted to grassland (Gleason 1923, Axelrod son et al. 1997). Most of the prairie (82.3%) 1985). Prescribed summer fires have been occurred on landscapes with average slope proposed as a way of increasing plant diversity range of 2–4%, whereas only 23% of the forest in prairies because they set back the actively and savanna was associated with landscapes in growing dominant C4 (warm season) grasses this slope range category, mostly in flood so they are less competitive against C3 plants, plains. Seventy-seven percent of timber vege- which are not actively growing. Many of the tation occurred on landscapes with average forbs are C3 plants and they contribute most slope ranges greater than 4% (4–7% slope 5 of the species richness to the prairies (Ewing 35.2% and .7% 5 41.8%). Most of the and Engle 1988, Howe 1994 a,b, 1995, Cope- timbered areas were associated with glacial land et al. 2003). However, summer burns as , highly dissected portions of the a management practice are not widely applied older Illinoian glacial till , non-glaciated at the present time (Anderson 1997). landscapes, and waterways.

THE VEGETATION MOSAIC. Topography and Waterways and vegetation distribution. The fire spread. In the eastern portion of the distribution of waterways has a pronounced Central Grassland the occurrence of the three effect on the occurrence of prairie vegetation. community types (prairie, savanna, and forest) Fires are generally swept from west to east so in the vegetation mosaic was the result of that areas to the west of bodies of water climate and fire frequency, which was strongly support prairie but the east side supports influenced by topographic features and distri- forest (Gleason 1913). Clear skies and dry bution of waterways (Gleason 1913, 1922, weather conditions favorable for fires are Wells 1970a,b, Anderson 1983, Grimm 1984). associated with high pressure systems. Highs In North American grasslands there can be have a clockwise flow of air and move from sharp transitions to distinctly different vege- west to east. As a high pressure system moves tation types that are associated with topo- into an area the leading edge of the front has graphic changes (Wells 1970a,b). The main wind in a westerly direction. Fire at this time affect of topography in determining vegetation would be carried to the west side of a body of patterns appears to be its control of fire water but vegetation on the east would be 636 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL.133 sheltered from the fire. As the high pressure 1948, Launchbaugh 1972, Wright 1969, 1972; system passes, the winds originate from the Heirman and Wright 1973, Anderson 1976, back side of the system and shift to an easterly Anderson 1982, Oesterheld et al. 1999). direction. Fires started under these conditions Time of the burn and productivity. In the could be carried to the east of waterways. of Kansas, at the western edge of However, as the high pressure system passes, the tallgrass prairie, the time of the burn low pressure replaces it bringing in high influences grass production on native grass humidity, an increased probability of pre- . Burned sites had lower production cipitation, and a reduced likelihood of fire. than unburned sites following winter or early- spring burns but late-spring burns and non- FIRE AFFECTS ON GRASSLANDS. Factors influencing fires. Golley and Golley (1972) burned areas had equal production. Decline of production on early burns compared to late- noted that grasslands can produce 20% more spring burns is due to litter being removed biomass than decomposes in a single growing from the site for a longer period of time on the season, and, if the excess biomass is not early burned than the late burned site, removed by fire or grazing, the productivity followed by early growth of the prairie on of the grasslands declines. However, the burned sites, which depletes soil moisture response of grasslands to burning can be (Knapp 1985). Absence of litter increases varied depending upon a variety of factors, runoff and evaporation of moisture from the including the amount of precipitation an area soil surface. The resulting decline in soil receives, grazing, which reduces fuel loading, moisture is the primary cause for a decline in fire frequency, timing of the burn, climatic production (McMurphy and Anderson 1965, conditions (especially rainfall and tempera- Owensby and Anderson 1967, Owensby and ture) before and after the burn, species Smith 1972, Bragg and Hurlbert 1976, Ander- composition, and fuel loading. son 1982, Knapp 1985, Svejcar 1990). Never- Climate and Fire Effects on Productivity. theless, grazing on forage on burned Oesterheld et al. (1999) summarized the effect sites make faster weight gains than cattle of fire on productivity, which were both grazing on unburned sites, because the forage positive and negative across a wide precipita- on burned sites is more palatable and higher in tion gradient (439–1129 mm annually) that protein than forage on unburned sites (An- included sites from North America, , derson 1976, Dyer et al. 1982, McNaughton et and the Mediterranean area. Fire enhanced al. 1982, Knapp et al. 1999). productivity by as much as 300% and reduced Litter Removal. The increased production it by as much as 80% of unburned control on burned eastern tallgrass prairie is related to sites. Positive effects of fire on productivity litter removal (Weaver and Roland 1952, were associated with sites receiving more than Ehrenreich 1959, Kucera and Ehrenreich about 700 mm of annual precipitation and 1962, Hadley and Kieckhefer 1963, Hulbert negative effects of fire on productivity oc- 1969, Peet et al. 1975, Knapp 1984). Old curred where precipitation was less than (1969) reported that litter removal increased 600 mm. In the eastern portion of the tallgrass production whether it was removed by fire or prairie, burning enhances productivity (e.g., by mechanical means. One of the mechanisms Hadley and Keickhefer 1963, Hulbert 1969, whereby litter removal enhances production is Kucera and Ehrenreich 1962, Old 1969, Vogl through the alteration of microclimatic condi- 1974, Peet et al. 1975, Rice and Parenti 1978). tions on the burned site to conditions more Exceptions to this generalization have been favorable for the growth of the dominant C4 reported for burning xeric sites (Dix and grasses than on unburned sites. Butler 1954, Zedler and Loucks 1969), al- Litter is a good insulating surface and it has though Dhillion and Anderson (1988) and high reflectance of solar radiation and low net Anderson et al. (1989) reported an increase in radiation, the difference between incident and production following burning on a deep sand reflected solar radiation. Consequently, the site in central Illinois. However, in the arid soil warms up slowly in the spring (Peet et al. western portions of the North American 1975). In contrast, on the burned surface the Grassland an increase in productivity does insulating and highly reflective litter layer and not always follow burning (Hopkins et al. standing dead biomass is removed by burning 2006] ANDERSON: EVOLUTION AND ORIGIN OF GRASSLANDS 637 and replaced by a darkened highly absorptive absence of standing dead biomass and higher surface. At the Curtis Prairie in University of wind speeds (57% lower than above the Wisconsin-Madison , during day- canopy). For example on June 10, leaf time, soil temperatures at 3 mm were warmer temperatures for big bluestem were 41.5uC on the burned site than the unburned site. (7.9u above air temperature) and 39.4uC (4.0u During the night, the burned prairie has a good above air temperature), for plants on un- radiating surface and cools rapidly, whereas burned and burned sites, respectively, on the unburned site has the insulating litter cover Konza Prairie. Because of active growth on that retains heat. Consequently, temperatures the burned site early in the spring that reduced were cooler in the upper layers of soil on the soil moisture, big bluestem plants on burned burned site than the unburned site. However, sites had greater water stress early in the at 25 cm depth in the soil the unburned site growing season than plants on the unburned was constantly cooler than burned site. The prairie (Knapp 1984). differences in microclimate between burned In summary, key microclimatic differences and unburned sites decreased as a grass between burned and unburned prairie that canopy developed on the unburned site affect productivity and result in higher pro- (Brown 1967, Anderson 1972, Peet et al. 1975). ductivity on burned prairies than unburned In the early spring, warmer soil tempera- prairies include: warmer spring temperatures tures during the day on the burned site on burned sites than unburned, greater avail- resulted in plants beginning growth earlier on ability of solar radiation and temperatures burned prairie than unburned prairie. Emer- more favorable for optimum photosynthesis gence of vegetation on the burned site can on burned sites than unburned sites (Peet et al, be 7–14 d or as much as 30 d later com- 1975, Knapp 1984). Differences in results pared to the burned site (Knapp 1984). Peet et between the Kansas and Wisconsin sites may al. (1975) reported that a burned site estab- be due to differences in standing dead bio- lished a larger standing crop of vegeta- mass, which stood 42 cm tall in Kansas and 22 tion (43.6 g m ) than the unburned site 10 cm in Wisconsin (Peet et al. 1975, Knapp 22 (1.24 g m ) by May 31 at the University of 1984).The more compacted litter on the Wisconsin-Madison Arboretum’s Curtis Prai- Wisconsin site may have slowed soil warming rie. They reported no difference in maximum more but reduced convectional cooling and photosynthetic rates between plants of big radiation less than on the Kansas site. bluestem on burned and unburned prairies. Higher production on burned prairies was Litter removal and inorganic . The attributed to the larger standing crop of green presence of a litter layer reduces the availabil- biomass earlier in the growing season on the ity of inorganic nutrients, especially nitrogen, burned prairie (Peet et al. 1975). which is thought to be the most limiting On the Konza Prairie, as leaves develop in grasslands. Annual burning of under standing dead biomass on unburned litter on prairies due to volatilization will prairie they are shaded and acquire character- reduce available nitrogen by about 1.0– istics of shade leaves and have low light 4.0 g m22 yr21. This represents about two saturation values and photosynthetic rates. times as much nitrogen as the amount input Standing dead litter reduces solar radiation by rainfall annually (Knapp and Seastedt and slows the wind speed (89% lower than 1986). Long-term there is a net loss of nitrogen above the canopy), which reduces convection- from grasslands that are burned annually al cooling. Leaf temperatures can rise above (Risser and Parton 1982, Ojima et al. 1990, the optimum for photosynthesis for C4 plants Blair 1997), despite biogeochemical pathways (30–35uC, Black 1973) and depress photosyn- to replenish nitrogen lost by burning. thesis (Knapp 1984). In contrast, on burned In prairies, both living tissue and detritus grasslands leaves develop in full sunlight as absorb annual rainfall, with each absorbing they emerge and have characteristics of sun about 20% of the annual deposition (Gilliam leaves with high light saturation values and et al. 1987). Inorganic nitrogen in rainfall photosynthetic rates. Additionally, leaf tem- provides nitrogen equal to about 25–50% of peratures on burned prairie are nearer the that required by living foliage (Risser et al. optimum for photosynthesis, because of great- 1981, Risser and Parton 1982). Nitrogen er convectional cooling as a result of the absorbed by microbes is converted to micro- 638 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL.133 bial protoplasm and is unavailable to plants. mass in excess of that which can be decom- As a consequence, more inorganic nitrogen in posed was a response to grazing. Grazing, like precipitation is available to plants on burned burning, accelerates the rates of mineralization prairies than unburned prairies because there of inorganic nutrients (Frank et al. 1998). For is no microbial sink for nitrogen in litter layers example, grazers like bison are effective in (Knapp and Seastedt 1986). Litter has high changing some recalcitrant species of nitrogen C/N and C/P ratios and microbes remove to that is easily converted to ammonia, nutrients from the soil to carry out decompo- a plant-useable form of nitrogen. The in- sition, which also reduces the availability of creased availability of inorganic nutrients can nitrogen to support plant growth (Seastedt enhance grassland productivity (Knapp et al. 1988). The input of nitrogen into prairies from 1999). Grazing removes the physiologically nitrogen fixation by free-living Cyanobacteria older, less productive leaf tissue and these is higher on burned prairies than unburned changes increase light and moisture for prairies because more light reaches the soil younger, more photosynthetically active tis- surface on burned prairies than unburned sue, which enhances aboveground production prairies (Eisele et al. 1989). In addition, (Frank et al. 1998). Some authors (McNaugh- ignition of the litter releases phosphorus and ton 1979, 1993, Owen 1981) have proposed an increase in available phosphorus enhances a symbiotic relationship between grasses and nitrogen fixation (Knapp and Seastedt 1986, grazers. Aboveground productivity of grass- Eisele et al. 1989). lands increases with moderate grazing (McNaughton 1979, Knapp et al. 1999), Grasslands and Grazers. HISTORY OF NORTH although other workers have questioned the AMERICAN GRAZERS. In North America, ex- beneficial effects of grazing (Belsky 1986, pansion of the grassland occurred in the Painter and Belsky 1993). Additionally, in- Miocene-Pliocene transition 7–5 MaBP and creased shoot production occurs at the ex- was associated with a concomitant increase in pense of belowground production and nitro- animals adapted to grazing , as in other areas gen and carbon are transferred from below in the world (Axelrod 1985). Through the ground to facilitate compensatory above- Pleistocene (1–3 Million MaBP) there was ground growth following grazing (Collins et a diverse grazing on the continent, al. 1998, Knapp et al. 1999) and excessive which included 32 genera and dozens of grazing will eventually cause a decline in species of mammals such as camels, horses, productivity (Anderson 1982). , antelopes, bison, and elephants. Near the end of the Pleistocene beginning ‘‘What a thousand acres of Silphiums about 25,000 YBP the number of grazing looked like when they tickled the bellies species sharply declined. This sharp decline of the buffalo is a question never again to has been attributed to the appearance of be answered, and perhaps not even asked.’’ efficient human hunters and/or climatic Aldo Leopold (1966) change (Flores 1996, Ehleringer et al. 2002). The peak of the American-evolved megafaunal BISON AS A KEYSTONE PRAIRIE SPECIES. Graz- crash occurred about 10,000 YRP leaving only ing patterns and preferences. Understanding about a half dozen browsing and grazing the role of bison in tallgrass prairie has forms. When Europeans entered the grass- occurred only in the last two decades when lands of North America the bison, elk, and reserve areas became available that were large other animals that characterized the grass- enough to support a reasonable number of lands were the remnants of the diverse bison and to allow them to graze in a way that that had been present prior to the massive simulated historic conditions. Knapp et al. extinction at the end of the Pleistocene (Flores (1999) delineated a keystone role for bison in 1996). maintaining diversity of tallgrass prairie. On Because of the long-term association of Konza Prairie bison fed primarily on grasses grazing animals and grasslands, it is not that constituted 90% of their diet and con- surprising that several lines of evidence suggest sumed only small quantities of forbs and that grazers strongly influence productivity essentially no woody vegetation (Fahnestock and diversity of grasslands. Golley and Golley and Knapp 1993, Vinton et al. 1993, Hartnet (1972) suggested that the production of bio- et al. 1996, Damhoureyeh and Hartnett 2006] ANDERSON: EVOLUTION AND ORIGIN OF GRASSLANDS 639

1997, Steuter 1997, Knapp et al. 1999, Towne Collins 1990, Knapp et al. 1999). Dormant et al. 2005). While graminoids constituted season burns favors C4, warm season grasses the largest portion of the bison diet, the and late flowering forbs. Periodic fires are proportion of C3 and C4 grasses consumed necessary to maintain the species richness of varied seasonally. tallgrass prairies (Leach and Givnish 1996). Generally, mammalian herbivores prefer C3 Nevertheless, frequent fires, especially annual grasses over C4 grass. The reason for this burns, can encourage these grasses at the preference is not known, even though C3 expense of C3 plants, which include many grasses have higher digestibility and protein species of forbs (Kucera and Koelling 1964, content but lower C/N than C4 grasses Gibson and Collins 1990, Knapp et al. 1999). (Caswell 1973, Wilson and Hattersley 1989, Importantly, forbs contribute most of the Ehleringer et al. 2002). Nevertheless, while species richness to the prairie (Howe 1994a, some studies have reported that C4 grasses Hartnett and Fay 1998). Bison graze on the C4 have more fibers and higher silica concentra- grasses and reduce their abundance, which tion in their leaves than C3 grasses (Kepart favors unpalatable C3 forbs, which in turn and Baxton 1993, Kaiser 1998), other studies enhances the plant diversity of the prairie. found no difference in the two traits between Bison effects on animal diversity. Bison C3 and C4 grasses (Heidorn and Joern 1984, enhance spatial heterogeneity in the prairie Scheirs et al. 2001). In , C4 through their grazing patterns that results in grasses constituted 33–44% of the bison diet patches of lightly grazed to heavily grazed from early June through August and then areas that have sparse grass cover and little declined to 15% by September 30. Bison use of litter (Knapp et al. 1999, Fuhlendorf and C3 graminoids (sedges and grasses) increased Engle 2001). This spatial heterogeneity is from 52–58% in mid-June to mid-August to important for grassland bird diversity. In the greater than 80% after September 1 (Plumb eastern tallgrass prairie, some birds, such as and Dodd 1993). Similar patterns in seasonal the Killdeer and Upland Sand Piper require shifts in consumption of C3 and C4 grasses short vegetation across large areas. Other were found on the Konza Prairie (Vinton et al. species, such as Eastern Meadow Lark and 1993). Bobolink, utilize medium height vegetation Bison grazed in two patterns, which in- with moderate amounts of litter, whereas cluded creating distinctive grazing patches that species such as Henslow’s Sparrow and Marsh were 20–50 m2 in area and more extensive Wren occur where the vegetation is tall with grazing lawns that were greater than 400 m2. heavy amounts of litter (Herkert et al. 1993). During the growing season, bison revisited Endemic birds of western Great Plains also previously grazed sites in preference to un- have characteristic distributions related to grazed locations. The grass that grew after historic grassland types and grazing patterns grazing was higher in nitrogen, more palat- (Knopf 1996). able, and not intermixed with dead tissue compared to the ungrazed areas. Grazed areas Fire and bison grazing affect the diversity and density of . initially experienced short-lived increased pro- Joern (2005) found that upland or lowland topographic ductivity following grazing, but productivity position and fire frequency had no significant eventually declined as loss of aboveground affect on species richness or tissues was compensated for by movement of diversity (Shannon Index) on the Konza carbon reserves from belowground. By re- Prairie. However, bison grazing increased peatedly grazing the same areas, bison encour- species richness, diversity and evenness (J) of aged the growth of non-palatable species that grasshoppers. Grasshopper species richness are the forbs. This grazing pattern eventually was positively related to plant species richness encouraged shifting to other areas as forage and heterogeneity in plant height. Joern (2005) quality declined. On average 6–7% of the concluded that fire influences grazing patterns, grazing patches were abandoned annually which effects structure and plant species (Knapp et al. 1999). richness in grasslands (Vinton et al. 1993, Enhancing grassland plant diversity. Bison Pfeiffer and Stueter 1994, Pfeiffer and Hart- grazing can offset negative effects of frequent nett 1995, Hartnett et al. 1996, Knapp et al. burning on plant species diversity (Gibson and 1999, Fuhlendorf and Engle 2001). Conse- 640 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL.133 quentially, fire and large mammalian grazing ever, some grasshopper species increased after are crucial features for maintenance of grass- fire and/or showed rapid recovery following hopper diversity. burning (Evans 1988, Anderson et al. 1989). Thus, it is not possible to have a single Grassland small mammals. Microtine ro- burning regime that will be optimal for all dents also require a diversity of conditions insects, and an increasing number of entomol- with respect to vegetation and litter density. ogists are expressing concern that prairie Even though there are species of small insects are being harmed by current prescribed mammals that show positive (deer mice) and burning practices, that if continued, could negative (western harvest mice and prairie result in a substantial number of species being voles) responses to burning, those showing lost (Pyle 1997, Schlict and Orwig 1999, negative responses to burning recover in two Swengel 1996, Swengel and Swengel 2001). to three years after a burn (Schramm 1970, However, Panzer and Schwartz (2000) con- Schramm and Willcutts 1983, Kaufman et al. cluded that the current rotational plan (burn 1990, Matlack et al. 2001). Fires of varied about every 2–3 years) in Illinois has been intensity and completeness of fuel consump- compatible with ‘‘conservation of insect bio- tion should favor diversity of animals in diversity.…’’ grasslands. The mosaic of vegetation resulting Historically, some portions of extensive from grazing creates uneven patterns of fire grasslands likely remained unburned each year intensity as a result of having areas with fuel and provided refugia for fire sensitive insects. loadings that vary from sparsely grazed areas However, under current conditions that in- with heavy fuel loading to low fuel loading volve burning fragmented remnant prairies or where areas were subjected to intensive restorations nearly all or all of the area is grazing pressure. burned. Possible solutions to this management conundrum include burning only a portion of Invertebrate Species Response to Prairie each site on a rotational basis leaving 50–70% Fires. Even though grasshopper diversity is as unburned ‘‘refugia’’ for fire sensitive enhanced by a combination of bison grazing species, which can reinvade the burned site and burning, the response of invertebrates to after it regrows (Panzer 1988, Panzer and burning is varied. A number of factors de- Schwartz 2000, Panzer 2003, Andrew and termine the response of the invertebrate Leach 2006). Additionally, recommendations species to fire, including where individuals for burning practices to favor fire sensitive are located at the time of the fire (Macfadyen insects include leaving areas missed by the fire 1952, Reichert and Reeder 1972, Seastedt unburned, avoiding ‘‘hot fires’’ by burning 1984, Warren et al. 1987), microclimatic and early in the morning, and using spring burns vegetational structural changes after fire, and to preserve clumps of grasses that are used as the ability of the invertebrate species to adapt wintering sites for insects (Panzer 1988). to the changed environment following the burn (Anderson 1964, Evans 1984, 1988, White-Tailed Deer in Remnant Tallgrass Anderson et al. 1989). For example, species Prairie. Historically, in much of the tallgrass of spiders that were active on the soil surface prairie the bison was the most important large at the time of a burn were eliminated, whereas mammalian in nearly all of the other species survived in subsurface burrows, Central Grassland, although its abundance under rocks, or were protected in the bases of may have been substantially lower in the caespitose (clumped) grasses during a burn eastern than in the western portion of the that had surface temperatures of 200uC tallgrass prairies (Leach et al. 1999). However, (Riechert and Reeder 1972). Similarly, mixed currently the white-tailed deer is the large responses of species to fire were reported for native with the most impact on (Seastedt 1984), collembolans (Lussen- remnant and restored tallgrass prairies. While hop 1976, Amburg et al. 1981), grasshoppers bison graze almost entirely on grass, forbs, (Evans 1988), whereas butterflies (Swengel which are little used by bison, are selectively 1996, 1998, 2001), and leafhoppers decrease browsed upon by white-tailed deer. Anderson in abundance after fire (Panzer 1988). Grass- et al. (2001) reported that deer browse very hoppers that fed on forbs increased in little on grasses or sedges during the late spring frequency as fire frequency decreased; how- and summer. However, they browsed from 2006] ANDERSON: EVOLUTION AND ORIGIN OF GRASSLANDS 641

3.5–18.9% of the standing crop of stems mitigated by large mammalian grazers. While depending upon time of sampling. Because burning separates fire-sensitive from fire-tol- forbs contribute most of the diversity to the erant or fire-dependent species, this separation prairie (Howe 1994a), excessive white-tailed provides a simplistic view of the varied deer browsing could reduce the diversity of the responses of grassland organisms to fire. For prairie. Anderson et al. (2005) demonstrated all major taxonomic groups of organisms, that diversity of prairie forbs was maximized there is a continuum of responses to fire. To at an intermediate level of deer browsing, maintain the biological diversity of grasslands supporting the intermediate hy- there must be areas large enough to support pothesis, which posits that diversity is maxi- varied fire regimes and include or simulate the mized at intermediate levels of disturbance functions provided by grazing, (Connell 1978, Collins et al. 1995). However, browsing, and burrowing animals (e.g., prairie the community quality of forbs, based on the dogs, pocket gophers, ground squirrels, and degree to which species were associated with invertebrates), which play critical roles in relatively undisturbed remnant prairies, de- developing and maintaining grasslands soils. clined as duration of intense deer browsing Most of our remaining grasslands in the (disturbance) increased. Forb quality was eastern portions of the Central Grassland are highest after eight years of protection from small remnant fragments, and in the mixed- browsing, suggesting a potential trade-off grass and shortgrass prairies excessive grazing between maximizing diversity and maintain- by cattle is an issue of concern. Maintaining or ing quality of forb communities that land improving the quality of our remaining grass- managers should consider (Anderson et al. lands can be achieved through sound range- 2006). land management, and restoration of prairies provides the means to ensure survival of Conclusions. Since the 1950’s, our under- prairie species. However, our efforts at prairie standing of grasslands has been greatly en- restoration are usually limited to establishing riched by widening the scope of our research prairie plants with little attention given to to include interactions among organisms in other prairie organisms. Invertebrates provide different trophic levels and examining the the greatest species diversity of any group of mechanisms that drive ecosystem processes. grassland organisms. They carry out many Fire has continued to be recognized as an important ecosystem functions such as polli- important factor that determines the distribu- nation, , and are critical links in tion and species composition of grasslands. food chains. Invertebrate biomass exceeds that For example, using simulation models Bond et of most vertebrate groups combined (Risser al. (2005) concluded that without fire world- 1996). Yet, it is rare for invertebrates to be wide current closed forest would increase from included in prairie restorations (Taron 1997). 27–56% of vegetated cells mostly as the result While we know a great deal about prairies of a reduction in cover of C4 plants. Without much of this information has not been fires 52.3 percent of the cells with C4 grasses adequately incorporated into our restoration present would be converted to angiosperm practices. Nevertheless, our success in manag- forest. This conversion would occur in large ing and preserving the remnant and restored areas of , Africa and smaller prairies should be enhanced because of our areas of , especially in humid areas realization that grasslands function because of that have climates with the potential to the interactions that have evolved among the support forests. In the Central Grasslands of organisms within the system North America, habitat fragmentation result- ing from agriculture and urban development If the land mechanism as a whole is good, has reduced the potential for fires to be carried then every part is good, whether we across landscapes and maintain the shifting understand it or not. If the biota, in the mosaic of grasslands, forest, and savanna course of eons, has built something we like vegetation that characterized the prairie pen- but do not understand, then who but a fool insula and the expansive area of mixed- and would discard seemingly useless parts? To shortgrass prairie (Anderson and Bowles keep every cog and wheel is the first 1999). The effect of fire on these grasslands precaution of intelligent tinkering (Aldo is complex, strongly influenced by climate, and Leopold 1966). 642 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL.133

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