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Characteristics and Consequences of Invasion by Sweet Resin Bush into the Arid Southwestern United States

Elizabeth A. Pierson and Joseph R. McAuliffe1

Abstract.-Eutyops multifidus (sweet resin bush), a shrubby composite native to South Africa, was introduced to the arid southwestern United States in 1935 by the USDA Soil Conservation Service. The spread of this shrub represents one of the most serious threats to the ecological integrity and economic value of several ecosystems in the semiarid Southwest. In southern Arizona, this shrub readily invades vegetationally intact, semi-arid grasslands and eventually forms virtually uninterrupted monocultures from which native grasses, shrubs, and succulents are almost completely excluded. Study of plant responses at the advancing front of the areas occupied by sweet resin bush demonstrated that death of native species is linked to the spread of this exotic shrub. These dramatic vegetation alterations are persistent and lead to a variety of additional detrimental changes, including marked increases in soil erosion. We have identified the climatic, vegetation, elevation, and soil characteristics of sites that are susceptible to invasion by E. multifidus. In southern Arizona sweet resin bush can occur in vegetation ranging from Sonoran Desert at low elevation (ca. 850-1060 m) to grasslands, chaparral, and woodland at higher elevation (ca. 1300+ m). In grassland, this shrub can invade a wide variety of different soil types, ranging from loamy calcic soils typically occupied by stands of black grama (Bouteloua eriopoda) to heavy clay soils occupied by tobosa (Hilaria mutica) and curly mesquite (H. belangeri). A significant amount of public and private southwestern rangeland is within the range of this invasive species. Our results demonstrate the catastrophic consequences of invasion by sweet resin bush in the arid southwestern United States.

INTRODUCTION not been affected by invasions of exotic terrestrial plants, and purposeful or accidental introduction Invasion of natural plant communities by in­ combined with urbanization and land usage have troduced plants constitutes one of the most been a major causal factor in these invasions. serious threats to natural ecosystems worldwide. At a global scale, grasslands are among the The resulting transformations can permanently most vulnerable ecosystems to extensive vegeta­ decrease native diversity, and can produce perma­ tion change due to plant invasions. According to nent, self-perpetuating changes in ecosystem Mack (1989), in less than 300 years (and in most properties including hydrology, biogeochemical­ cases, little more than 100 years) much of the tem­ cycling, and disturbance regimes (especially fire). perate grassland outside Eurasia (a collective area 6 2 There are few ecosystems in the world that have of 2.0 x 10 km ) has been irreparably trans­ formed by human settlement and the concomitant introduction of alien plants. In contrast to temper­ ate grasslands, semi-arid grasslands have been 1U.S.Geological Survey, 1675 W. Anklam Rd., Tucson, Arizona, 85745, USA and Desert Botanical Garden, 1201 N. Galvin Parkway, viewed as less vulnerable to invasion. The percep­ Phoenix, Arizona, 85008, USA. tion is based on the notion that because of the

219 greater enyironmentallimitations placed on exist­ ence in arid and semi-arid climates, few species are assumed capable of invading and the few that are capable are unlikely to bring about extensive vegetation change. The paucity of information available on the consequences of plant invasions in semi-arid grasslands has perpetuated the no­ tion that these grasslands are less vulnerable to invasion. For the arid southwestern United States, this notion may prove to be dangerously inaccurate. The biseasonal rainfall and subtropical tempera­ tures characteristic of the Sonoran Desert and adjacent semi-arid grassland make them vulner­ able to invasive species tolerant of both Mediterranean and neotropical climate regimes (Burgess, et al. 1991). Species of exotic plants tol­ erant of both climatic regimes have already become naturalized in the semi-arid vegetation of the Southwest; many were deliberately intro­ duced by the United States Soil Conservation Service (SCS) for their climate tolerance (Table 1). The consequences of these invasions are just be­ ginning to be recognized and further vegetation change due to invasion is likely to be only a mat­ ter of time. Examination of the characteristics of success­ ful invading species and the consequences of their spread for the invaded ecosystem provides an ex­ Figure 1.-EuryOPS multifidus (Asteraceae), also known as sweet cellent opportunity to study the structure and resin bush, Is a perennial subshrub. It has ShOWY, yellow function of the native biological community and Inflorescences which bloom in Arizona from December to assess the vulnerability of these com-!punities to March. further invasion. In this paper we focus on E u- ryops multifidus (Asteraceae), commonly known as sweet resin bush (fig. 1). This woody subshrub Table 1.-Examples of exotic plant species that have become widely established in semi-arid and arid vegetation in was introduced into the arid southwestern United Arizona as a result of deliberate introduction for erosion States from South Africa in 1935 by the SCS. The control and range improvement prior to 1942. The table ecosystem-level changes that have occurred as a gives the family, genus, and species names, country of origin, and source of introduction. An asterisk (*) result of the range expansion of this species from Indicates those species that were either imported and experimental introductions by the SCS are among introduced for the first time by the USDA Soil the most dramatic examples of the consequences Conservation Service (SCS) or widely distributed by the SCS, having been initially introduced by other means. of plant invasions in the arid Southwest. Interest­ ingly, relatively little has been written previously Plant names Origin Source Asteraceae Euryops multifidus South Africa* about this serious ecological problem. In this pa­ Asteraceae Pentzia incana South Africa * per, we summarize what is presently known Chenopodiaceae Atrip/ex semibaccata Australia* about the A) taxonomy and B) ecology of E. multi­ Fabaceae Melilotus indicus Eurasia* fidus; C) describe the history of introduction of Fabaceae Melilotus officinalis Eurasia'" Geraniaceae Erodium cicutarium Europe* sweet resin bush and other exotic species by the Poaceae Agropyron cristatum Turkey* SCS to the southwestern United States, D) de­ Poaceae Andropogon ischaem Turkey* scribe some of the changes in the structure and Poaceae Avena fatua Europe function of vegetation communities that have Poaceae Bromus rubens Europe Poaceae Cynodon dactylon Old world* been invaded by sweet resin bush, E) describe the Poaceae Eragrostis curvula South Africa * potential mechanisms that can account for these Poaceae Eragrostis lehmanniana South Africa * changes, and F) delineate the geographic area in Poaceae Pennisetum ciliare South Africa * Poaceae Schismus barbatus Old World* North America at risk of future invasion by this invasive species.

220 TAXONOMY, PHYTOGEOGRAPHY, AND and several are toxic (Hegnaur, 1977). Almost all PHYTOCHEMISTRY OF EURYOPS members of the genus Euryops produce and se­ MULTIFIDUS crete resin. The nature of the distinctive phytochemistry of the entire tribe suggests that Euryops multifidus belongs to the tribe many of the chemicals produced serve a role in Senecioneae (Asteraceae), which includes the defense against herbivores and parasites, as prominent genera Senecio, Othonna, and Euryops chemical inhibitors involved in allelopathy, or (Nordenstam, 1968). Representatives of the tribe both. are most common in South Africa. There are 97 species of Euryops, all of which occur natively only on the African continent; 96 of them occur ECOLOGY OF EURYOPS MULTIFIDUS IN only in South Africa. Euryops multifidus has a ITS NATIVE RANGE western Cape distribution in South Africa, rang­ ing from the Malmesbury Flats in the south to E'uryops multifidus is listed in A Catalogue of Lake Namaqualand in the north (range includes Problem Plants in Southern Africa (Wells, et al.p the Cape Province, The Orange Free State, Basuto­ 1966), as a ruderal, agrestal, and pastoral weed. land, and Namaqualand States). It occurs in The undesirable characteristics of this weed in­ transitional communities between arid fynbos and clude a) its ability to replace "preferred karriod vegetation, in rhenosterveld and in succu­ vegetation" b) its unpalatability and c) its occur­ lent karroo. It often occurs on rocky outcrops rence as a contaminant of seed (Wells, et al., 1966). between sea level and 1500 m in elevation (Nor­ Sweet resin bush, like most members of the genus, denstam, 1969). The distribution of E. multifidus has showy, yellow flowers which bloom during strongly overlaps that of E. tenuissim us. Interest­ the winter and early spring. The 3-4 mm long, 1-2 ingly, the latter species has been introduced as an mm wide achenes are covered by a wooly in­ ornamental in the arid southwestern United dumentum of 3-7 mm long white or brown hairs States, but has not yet become invasive. and are easily transported on clothing or fur. The common name "resin bush" has been ap­ Three to seven achenes per inflorescence are com­ plied to all species of the genus Euryops (Smith, monly produced (fig. 2). 1966). The common name is a literal translation of Information on the range ecology of E multi­ the Dutch name Harpuis bosch, "hars" (resin) fidus in South Africa, particularly its palatability, "puisje" (a small pimple), referring to thel'esinous is both sparse and contradictory. The problem secretion exuded from the stem and branches in stems from its description in The Flowering Plants the form of small pimply drops on most Euryops of South Africa (Pole-Evans, 1928), one of the species. Apparently the resin which accumulates most prominent early floras of South Africa. Here, under the bushes of most species was noted in E. multifidus is described as being highly palat­ colonial South Africa for its alleged medicinal able to sheep, yet invasive of over-grazed and value and was easily collected (Smith, 1966). Sev­ over-stocked land. Another more recent source eral of the species are known locally by distinctive names. The names applied specifically to E. multi­ fidus include Soetharpuis ("soet" meaning "sweet"), Skaapbossie (meaning "sheep bush"), and Kapokbossie (meaning "chicken pox bush") (Smith, 1966; Nordenstam, 1968). All members of the Senecioneae tribe are known for their distinctive phytochemistry com­ pared to other Asteraceae and this has been used to taxonomically distinguish the genera of the tribe and species within each genera (Hegnaur, 1977). Known phytochemicals common to the three prominent genera of the tribe are diterpene derivatives, sesquiterpene lactones, furanoelemo­ philones, and acetophenones. The production of sesquiterpene lactones particularly is believed to Figure 2.-The fruits of sweet resin bush, 3-4 mm long, 1-2 mm wide a(~henes, are covered by a wooly Indumentum and are easily be involved in defense against herbivores and transported on clothing or fur. Three to seven fruits per parasites since most of them are intensely bitter Innorescence are commonly produced.

221 (Wells, et al., 1966) describes the palatability of Plant: Introduction Offices were closed or moved. sweet resin bush as uncertain. The early reference One site of introduction at Frye Mesa, Arizona has by Pole-Evans may have contributed to the selec­ been identified from the caption of a 1935 SCS tion of E multifidus by the SCS in the. 1~~O' s for photograph of a test planting. Few other specific introduction to the southwest on the basis of its records of test plantings and revegetation projects forage value. The unresolved question of the plan­ have been identified, although SCS Annual Re­ t's palatability in its native range is further ports indicate that they occurred. complicated by the distinctive phytochemistry of In order to determine the current distribution the genus described previously. of E. multifidus in the arid Southwest, we have compiled a list of sightings recorded in local floras and on specimens from herbarium collections in Arizona, California, New Mexico and Texas. We HISTORY OF INTRODUCTION OF SWEET have found no records of the presence of sweet RESIN BUSH BY THE SCS IN THE resin bush outside of Arizona. We have recently SOUTHWESTERN UNITED STATES visited every documented report of sweet resin bush to determine whether it is still present, the According to SCS Annual Reports, Euryops extent of vegetation change that has taken place, multifidus was among the first species collected and, if possible, the source of the introduction. We by Regional Director F. J. Crider in 1934 for intro­ have determined that the current distribution of d uction to the arid Southwest. The main requisites sweet resin bush is localized around four epicen­ for the species selected by the SCS for introduc­ ters where sweet resin bush was apparently tion into Arizona and New Mexico, were a) deliberately introduced in the late 1930's: Frye general climatic adaptation especially drought re­ Mesa, Marijilda Canyon, Upper Verde Valley, and sistance, b) suitability for erosion control and Sabino Canyon (fig. 3). Below we describe what is other economic uses, and c) ease of propagation" known about the introduction of sweet resin bush (Crider, 1935). It should not be surprising given at each of these locations. these criteria that E. multifidus and other species introduced by the SCS have become invasive and now constitute serious threats to native vegetation Frye Mesa (Table 1). Each of the species was selected from vegetation native to semiarid regions such as Sweet resin bush was introduced in 1935 onto western Asia, South Africa, and Australia. Eu­ Frye Mesa, 18.1 km southwest of Thatcher, Ari­ ryops multifidus was selected for introduction zona, as part of an SCS experimental planting into the arid southwest because it was believed to program (fig. 4). Sweet resin bush has spread from be extremely drought resistant; have good forage the abandoned 27 x 27 m fenced enclosure and has value, especially for sheep; and to propagate read­ become established on the mesa top, on deposi­ ily from seed" (Crider, 1935). tional slopes and along washes below the mesa, Each species selected by the SCS for introduc­ and at the base of the mesa. It occurs in vegetation tion to the arid southwest was observed and ranging from the creosote bush-dominated flats at increased for distribution in the Tucson Regional the base of the mesa (elev. 1060) to semi-arid Conservation Nursery and then distributed to grassland and surrounding chaparral and wood­ Area Nurseries in Safford, Arizona, and Shiprock land on the mesa top (elev. 1300+ m). At the foot and Albuquerque, New Mexico. Test plantings of of the mesa, E. multifidus occurs on relatively exotics on public and private lands outside the deep, loamy, and calcic soils that are occupied by nurseries were carried out by each area nursery. black grama (BouteJoua eriopoda) and a variety of The Civilian Conservation Corps (CCC) was ulti­ native shrubs. On terraces of relatively young al­ mately provided with stock from the nurseries luvium along washes, it has displaced stands of and this was used in range restoration projects mesquite (Prosopis velutina)· and catclaw acacia throughout the arid Southwest. Based on the rec­ (Acacia greggii). On the mesa top, it occurs on ommendations of the SCS, seeds and young plants extremely clayey soils that support grasslands were also made available to anyone wishing to dominated by curly mesquite (H belangeri). use them for range improvement. Unfortunately, Vegetation dominated by E. multifidus on the the SCS kept few records describing the exact lo­ mesa. top is centered approximately on the aban­ cations, dates, and fates of test plantings, and doned planting site and is spreading on the mesa those that were kept have been lost as the SCS top from the point of introduction primarily as an 222 advancing front (Le., enlarging circle), radiating out in all directions from the point of introduction but advancing more quickly downslope and along drainages. This pattern of spread has produced an almost uninterrupted monoculture of E. m ulti­ fidus over one ~uarter of the mesa top (ca. 1.3 km2 of the ca. 4 km area covered by semi-arid grass­ land). Interspersed within the semi-arid grassland vegetation on the mesa top there exists a mosaic of disj unct patches of vegetation dominated by E. multifidus ranging in size from 2000 m2 to less 2 than 1 m . These patches serve as invasion foci (Mack, 1985) expanding in the same way as the main population and eventually coalescing with other patches or merging with the main popula­ tion, The result is a patchwork of vegetation that is clearly visible from the valley floor at most sea­ sons because of the contrasting phenology of the

ARIZONA

Colorado Plateau

o Flagstaff

Figure 4.-Repeat photographs of the Soil Conservation Service (SCS) test planting at Frye Mesa, Arizona: top, taken In 1935 by the SCS; and bottom, taken In 1991 by R. M. Turner. Sweet resin bush was Introduced Into the 27 x 27 m exe/osure pictured in the 1935 photograph. Almost 60 years later, sweet resin bush forms an almost unlnterupted monoeulture over one quarter of the mesa top. dominant grassland species and E. multifidus. Sweet resin bush is a brilliant green throughout the much of the year with showy yellow flowers from late December to March, when much grass­ 100 land vegetation is dormant. The situation is o reversed in summer. km

Reglon· con t"alnlng fW arm, Marijilda Canyon Semi-arid Grasslands E'. multifidus was apparently introduced along Figure 3.-The current distribution of sweet resin bush Is localized FSR 57 approximately 2.4 kilometers from its in­ around four epicenters in Arizona where this exotic was deliberately Introduced. The locations of these epicenters are tersection with Swift Trail Road (State Route 366), represented by solid triangles on this map of Arizona: A. Frye although no record of this introduction was found Mesa, B. Marijilda Canyon, C. UpperYerde Yalley, and D. Sabino in the SCS documentation available in Tucson, Canyon. At risk of future Invasion are the warm, semi-arid grassland and Sonoran desertscrub vegetation of Arizona. The Arizona. Circumstantial evidence for the role of geographic range of these vegetation types Is Indicated on the the SCS include the presence of a Civil Conserva­ map. tion Corp (CCC) work camp in Marijilda Canyon

223 11

during the period from 1934 to 1942 when E. mul­ Sabino Canyon tifidus was being used for revegetation work. CCC labor was used frequently to set up test plots At Sabino Canyon in the Coronado National and to revegetate eroded sites with plants recom­ Forest in Tucson, Arizona, E. multifidus was ap­ mended and provided by the SCS. The parently introduced at the Lowell Ranger Station. co-occurrence of Pentzia incana (a South African It is unknown whether this introduction was part composite which was also introduced by the SCS of a SCS test planting or whether it escaped from for revegetation during this period) and the pres­ a garden at the Ranger Station. Sweet resin bush ence of small spreader dams (used by the CCC for has become naturalized on the grounds surround­ erosion control) are also strong indications that E. ing the Station and has spread into surrounding multifidus was introduced by the SCS using CCC Sonoran Desert vegetation along washes and labor at this site. roadways. E. multifidus occurs in two adjacent, yet cur­ rently distinct patches, one approximately 100 x 200 m and the other approximately 60 x 60 m in CONSEQUENCES OF INVASION BY size. The populations occur along the gentle slope EURYOPS MULTIFIDUS IN THE next to the roadway and extend into the adjacent SOUTHWEST Marijilda Wash. Individuals can be found in Mari­ jilda Wash and along its banks as much as one We sampled the vegetation in the four sites quarter mile downstream from the introduction discussed above where sweet resin bush was in­ site. Both areas have relatively clayey soils and troduced and has become invasive (fig.3). The support a mixed species grassland in which sites represent an elevational and climatic contin­ sideoats grama (Bouteloua curtipendula) is the uum. The two sites at the upper elevational end dominant species. experience greater effective precipitation and are characterized by vegetationally intact semiarid grassland (Frye Mesa, elevation 1300 m; Marijilda Upper Verde Valley Canyon, elevation 1220 m). The intermediate site is a former semiarid grassland converted to a E. multifidus was also apparently introduced shrub-dominated community by a century of in­ southeast of Cottonwood, Arizona along Camino tense grazing (Upper Verde Valley, elevation 1065 Real near its junction with FSR 359. Similar to the m). The remaining site, characterized by Sonoran Marijilda Canyon site, we have found nt> record of desertscrub, occurs on the lower, drier end of the this introduction in the SCS documentation avail­ continuum (Sabino Canyon, elevation 850 m). able in Tucson, Arizona, however sufficient circumstantial evidence exists to suggest this was also an SCS site where E. multifidus was planted Vegetation Change Resulting From 0 for erosion control. The population occurs on a 1 / 0 Invasion By Sweet Resin Bush slope and perpendicular to this slope are a series of berms built for erosion control. E. multifidus At each of the four sites, we sampled vegeta­ appears to have been planted in association with tion within areas lacking sweet resin bush and berm construction in an effort to control erosion. adjacent areas invaded by sweet resin bush in or­ The native vegetation appears to have been der to characterize differences in the number and heavily disturbed and is currently dominated by coverage of species occurring in each type of Gutierrezia sarothrae, Prosopis velutina, and vegetation. At each site, the areas used in these Bromus rubens, although it probably previously comparisons were matched for slope, aspect, and supported a grassland dominated by tobosa soils. At Marijilda Canyon, Upper Verde Valley, (Hilaria mutica). E. multifidus occurs on both and Sabino Canyon the coverage in each vegeta­ sides of Camino Real. It appears to have been in­ tion type was estimated in a total of fifty, 0.25 m2 troduced only on the uphill side of the road and square plots spaced at 1 m intervals along two currently occupies an area of approximately 250 x parallel, 25 m transects. At Frye Mesa, where the 175 m. Downslope and north of the road E multi­ area invaded by sweet resin bush is much more fidus occurs in a series of disjunct patches in extensive, the plots were spaced at 6 m intervals approximately the same size area; however, indi­ along two parallel, 150 m transects. The coverage viduals can be found as far as 300 m downslope of grasses and forbs was estimated from basal from the edge of the patch. area, the coverage of shrubs and succulents was

224 estimated from canopy area, and the coverage of dramatic increase in exposure of bare soil (Figs. bare soil was estimated to be the area of the plot 5A, 5B) and increased soil erosion. In the intact not covered by plant basal area or rocks. Coverage grassland vegetation, interdigitating bunches of is expressed as a percentage of the plot area and native perennial grasses, particularly Hilaria be­ was recorded in six classes (0-5, 5-12, 12-25, 25-50, langeri, form soil dikes which capture and hold 50-75, 75-100 %). soil. Where the sweet resin bush has rep laced the Additionally, at Frye Mesa, we quantified the native species, not only is more bare soil exposed, effect of sweet resin bush on the vigor of the small but the soil is more easily removed. Exposed roots tree Prosopis velutina which is not excluded by E. and soil pedestals around the bases of the remain­ multifidus, but exhibits significantly greater mor­ ing native grasses caused by soil erosion are tality of major branches in areas dominated by E. clearly evident in the transition zone and in vege­ multifidus than in intact grassland. Stem mortal­ tation dominated by sweet resin bush. This ity was expressed as the percentage of the total situation is ironic since one of the goals of the SCS canopy composed of persistent, dead branches Plant Introduction Program was to introduce spe­ and was recorded in one of six mortality classes cies which would reduce soil erosion. (0-5, 5-25, 25-50, 50-75, 75-95, 95-100%). We esti­ mated the stem mortality for all trees in 5, 1000 m2 circular plots spaced 40 m apart. Upper Verde Valley, Altered Semi-arid Grassland Frye Mesa and Marijilda Canyon, Semi-arid Grasslands In the upper Verde Valley, where the grass­ lands have been altered by heavy grazing, the Invasion by sweet resin bush has produced native perennial grasses (Hilaria m utica, H be­ dramatic and apparently persistent changes in the langeri, and Panicum obtusum) have been structure and function of the semi-arid grasslands excluded and replaced by woody plants (Gutier­ sites we sampled. Sweet resin bush has spread ex­ rezia sarothrae and Prosopis velutina). Inspite of tensively, forming near monocultures within both this transition to vegetation dominated by indige­ of these semi-arid grassland sites. All native nous disturbance tolerators, we found that the grasses and most woody perennials including the coverage and diversity of these species are signifi­ prevalent subshrubs Calliandra eriophylla, Erio­ cantly reduced in the presence of sweet resin bush gonum wrightii, and Gutierrezia' sarothrae are (Fig 5C). Coverage of the annual forb Plantago completely excluded from areas now dominated insularis was also found to be dramatically differ­ by sweet resin bush (Figs. 5A, 5B). The decrease in ent in invaded and uninvaded vegetation during the species richness of perennial plants on areas the spring of 1993. In the uninvaded vegetation, occupied by sweet resin bush is dramatic (19 ver­ this annual formed a nearly continuous carpet in sus 2 species at Frye Mesa and 23 versus 6 species 100% of the plots sampled (average density 3700 2 at Marijilda Canyon). Most striking is the elimina­ plants/m , average biomass 48 g/m2), whereas in tion of Gutierrezia sarothrae, a weedy native vegetation dominated by sweet resin bush, P. in­ which increases rapidly with disturbance. The sularis occurred in 90% of the plots sampled 2 small tree Prosopis velutina is not excluded by E. (average density 1100 plants/m , average biomass multifidus, but at Frye Mesa exhibits significantly 12 g/m2). greater mortality of major branches in areas domi­ In this altered grassland, more than 50% of the nated by E. multifidus than in intact grassland (59 soil surface is bare even in the absence of sweet versus 15% of major branches, respectively). The resin bush (as compared to less than 10% in vege­ only woody perennial that is apparently unaf­ tationally intact grassland). However, the fected by sweet resin" bush is the sub shrub exposure of bare soil does not increase further fol­

Krameria parvifolia I which is equally prevalent lowing sweet resin bush establishment (fig. 5C). and vigorous in intact and invaded areas at Mari­ jilda Canyon (fig. 5B). Interestingly, K parvifolia is a facultative root parasite (MacDougal and Can­ Sabino Canyon, Sonoran Desertscrub non, 1910). The significance of this exception is discussed in the next section. In contrast to the grassland sites, the species In both grassland sites, elimination of native richness of the desertscrub vegetation is not sig­ species, especially grasses, leads to significant and nificantly reduced in the presence of E. multifidus

225 60 FRYE MESA 60 MARIJILDA CANYON

50 50 ~ Intact Grassland cu Intact Grassland i; > 40 0 <10 ~ U u 1: 30 30 c:cu 20 cu~ 20 Q.~ Q. 10 10

0 0 ! E . .. .. "!! ;:::- 0 e .; "N "N c s l i e i ., :=. ~ .. ~ ~ t: i ~ I: I It ! :I .! U ! ~ ;; .. u.I i ;; 1! 8: "~ ! .2 ~ CD '" III u :I u -; .. " "" tlJ j ~ tlJ } & 0 tlJ 0

60 60 Intact Grassland Intact Grassland so 50 Invaded by Euryops Invaded by Euryops '-cu ~ 40 > 8 8 40 +Jc::: 30 ....c::: 30 20 20 Q.~ Q.~ 10 10

0 0 l! E .. .. It .. § ! "~ :I "N e 0 -6 "N € I c c u l e c; u 1 ~ ~ ~ :I ".. t: E 8: :: 8. U 8: f :I ~ 8: !! w 1ft 1ft ~ ~ .. 1ft 1i -8 CD.. Ii ".. ::i 10.. u w ~ "" tI u :I tlJ J! tlJ j <5 & 1 Cover Type Cover Type

60 UPPER VERDE VALLEY 60 SABINO CANYON

50 so Altered Grassland Intact Sonoran '- '-cu ~ 40 ~ 40 Desertscrub 8 U +J c: 30 +-'c: 30 20 cu~ 20 Q.e Q. 10 10

0 0 ri) ..Q. .. .!! '6 0 "N Q. ~ CII § 0 ~ ~ ~ ~ u ! w:I ~ w 2 i .. III ~ Q. 10 i tlJ ~ 5" 60 60 Intact Sonoran Desertscrub Altered Grassland 50 so '- Invaded by Euryops '- Invaded by Euryops ~ 40 ~ 40 8 8 +-'c::: 30 +Jc: 30 cu cu~ 20 ~ 20 ':L Q. 10 10 0 0 .. 1ft '! "N "a § CII 0 l!! ~ .. ! ~ 10.. 2 l IV ! A. 10 :I .! tlJ j 0 0 Cover Type Cover Type Figure 5.-Mean percent cover of Euryops multifidus and native species in vagetationally intact and adjacent invaded areas. Coverage is given for perennial grasses, prominent woody species, and all other perennial species combined at: upper lett. Frye Mesa, upper right, Marlillda Canyon. lower lett. Uppw Verde Valley, lower right, Sabino Canyon. Coverage of bare soli, the area of the plot not covered by plant basal area or rocks, Is also given.

226 (fig. 5D). However, some common perennial sub­ ,hrubs (Encelia farinosa and Porophyllum gracile) Transition from Intact Grassland to \Tere significantly less frequent in vegetation in­ 60 Vegetation Dominated by Euryops vaded by E. multifidus (fig. 5D). At this site, 50 ""'-Euryops <',weet resin bush seems to be invading bare -e-Grasses )round, rather than displacing the existing mem- '- ~ 40 oers of the community (notice the reduction in 8 coverage of bare soil where sweet resin bush has ~c 30 nvaded, fig. 5D). Although the coverage of E. CD ~ CD 20 nultifidus at this site is comparable to the cover­ Co age found in semi-arid grassland vegetation, a ;ignificant number of plots contained large, re­ 10 :ently dead individuals of E. multifidus. The 0 inability of sweet resin bush to replace the native 0 s 10 's 20 25 species and the high turnover in the exotic popu­ iation suggests this site occurs near the lower, drier limits of the range of this plant. 20

ABRUPT TRANSITION FROM NATIVE -Gutierrezia 15 -e-Calliandra VEGETATION TO VEGETATION \.. ~ DOMINATED BY EURYOPS MULTIFIDUS 8 ~ 10 C One of the most striking features of the grass­ CD lands that have been invaded by sweet resin bush ~ ~ is the sharpness of the transition between native 5 vegetation and vegetation dominated by E. multi­ fidus. We characterized this transition at Frye 0 Mesa by sampling vegetation along transects from 0 5 10 lS 20 2S intact grassland to areas dominated by sweet resin Transect Position (' meter intervals) bush. The transects, 25 m in length, were oriented such that the 10m point was located at the edge of Figure 6.-Mean percent cover of E. multifidus, native perennial the area dominated by sweet resin bush, the start grasses, and the prominent subshrubs Gutierrezia sarothrae of the transect (0 m) within desert grassland vege­ and Call/andra erlophylla along five, 25 m transects from grassland to sweet resin bush dominated vegetation. The tation, and the end (25 m) within the area invaded transects were oriented such that the 10m point was located at by sweet resin bush. In this way, vegetation sam­ the edge of the area dominated by sweet resin bush, the origin pling from 0 to 25 m along the transect within grassland vegetation, and the 25 m endpoint within the area invaded by sweet resin bush. The Small Arrows Indicate characterized the spatial transition from desert the presence of dead remains of perennial grasses. grassland to zones dominated by E. multifidus. The canopy coverage of vegetation was measured from 12% to less than 4% and the frequency of as described above. dead clumps of this grass increased (fig. 6). The Our vegetation sampling demonstrates that coverage of the small shrubs Gutierrezia sarothrae the transition from native vegetation to E. multi­ and Calliandra eriophylla also declined as the fidus monoculture is extremely abrupt and is coverage of sweet resin bush increased. Isolated characterized by the death and loss of dominant patches of sweet resin bush representing more re­ native grasses and shrubs, concomitant with an cent foci of establishment and occurring up to increase in sweet resin bush (fig. 6). An extreme hundreds of meters away from the central popula­ consequence of the loss of perennial grass cover is tion exhibit the same sharp transition from an increase in the exposure of bare soil. Within 6 monoculture to grassland. m along transects from desert grassland to vegeta­ The sharpness of the transition is due in part tion invaded by E. multifidus the mean coverage to limited recruitment of sweet resin bush away of E. multifidus and of bare ground increased from mature individuals. Although the achenes % % from 0 to 36 and 9.5 to 25 , respectively; in the can be dispersed by attachment to fur or clothing same space the mean coverage of the dominant or by water, most accumulate near the base of the bunchgrass species, Hilaria belangeri, dropped adults where they germinate. The increase in bare

227 soil at the base of adult plants may also aid the creased seedling mortality due to charcoal parti­ seedlings of sweet resin bush in becoming estab­ cles adhering to and damaging cotyledons. Given lished there. Whether recruitment away from the the extensive mortality of native species that oc­ patch is limited by seed dispersal or the availabil­ curs in proximity to established sweet resin bush ity of suitable sites (Le., areas with exposed soil) is plants, we believe that this simple experiment was unknown. adeq uate to identify persistent soil alterations if they did exist. We now feel that persistent al­ lelopathic soil alteration is not the primary POTENTIAL MECHANISMS TO EXPLAIN mechanism by which sweet resin bush excludes THE CHANGES IN STRUCTURE AND native grassland species. However, there may be FUNCTION OF VEGETATION other types of interference between sweet resin COMMUNITIES INVADED BY EURYOPS bush and native species such as the root interac­ MULTIFIDUS tions that occur between Larrea tridenta and Ambrosia dumosa as described by Mahall and We have demonstrated that sweet resin bush is Callaway (1991). capable of changing the structure of semi-arid Other field observations suggest that competi­ grassland communities by forming sharply de­ tive exploitation of resources, especially water, fined areas characterized by the elimination of may be an important competitive mechanism. The almost all native species and the concomitant ex­ bright green appearance of sweet resin bush much posure of soil to erosion. The substantial mortality of the year, especially during the winter when of native species in the transition zone suggests many of the dominant native perennials are dor­ that this dieback is the result of the proximity of mant, suggests that sweet resin bush is capable of the older E. multifidus individuals. These changes effici~ntly acquiring and potentially exploiting may result from either direct interaction between most of the available moisture within its proxim­ exotic and native (such as interference or exploita­ ity up to two months before native species tion competition) or indirect interaction (such as become active. We hypothesize that this exploita­ the alteration of an ecosystem level property by tion of water is the mechanism responsible for the exotic which in turn affects the native vegeta­ partial dieback (rather than complete elimination) tion). We are currently testing hypotheses of some woody plants such as Prosopis velutina. consistent with the possibility of both direct and The only woody plant that thrives in both intact indirect interactions between exotics and natives grassland and monocultures of sweet resin bush is although much of our research is as yet prelimi­ Krameria parvifolia (fig. 5B) at Marijilda Canyon. nary. This shrub is a facultative root parasite which is The nearly complete exclusion of native flora capable of obtaining water from the xylem of by E. multifidus and the formation of a zone of other plants (MacDougal and Cannon, 1910). bare soil and dead plants at the advancing front of Since Krameria parvifolia can potentially obtain even small populations of sweet resin bush sug­ water parasitically from the roots of E, multifidus, gested that interference competition may be the it may be immune to the depletion of soil water primary mechanism of interaction.With a simple by E. multifidus. We will be investigating further germination experiment, we tested the hypothesis the potential competition between sweet resin that this interaction may be due to persistent al­ bush and native grassland species for soil mois­ lelopathic soil alteration. We collected soil from ture in our future research. intact grasslands and areas dominated by E. m ul­ A third category of mechanisms we are inves­ tifidus. Quick-germinating radish seeds were tigating involves indirect interactions between sown in both of these soils as well as in a mixture sweet resin bush and the native vegetation. In fu­ of each soil with 20% (by volume) finely ground, ture research, we will test the hypothesis that activated charcoal. The activated charcoal was changes in ecosystem level properties such as ac­ added to adsorb any potential allelopathic com­ celerated erosion or the elimination of members of pounds. A total of 96 seeds per treatment were the community that make up different trophic lev­ sown, 4 seeds per 5 x 5 x 7 cm pot, in a completely els (e.g., rhizosphere microorganisms) may in turn randomized design. Surprisingly, we found no accelerate the death of the native plant species. difference in germination (nearly 100% in all treat­ Although our investigations of the potential ments) and no difference in seedling height mechanisms to explain the success of sweet resin among soil treatments (data not shown). Both of bush in the Southwest are preliminary, they sug­ the charcoal amended treatments had slightly in- gest that pre-adaptation of sweet resin bush to the

228 climate of the arid Southwest has played a signifi­ (Era~Jrostis lehmanniana and E. curvula). All three cant role in its success. of these species have been introduced extensively in heavily grazed pastureland and, like sweet resin bush, are capable of maintaining virtual GEOGRAPHIC AREA IN NORTH AMERICA monocultures by competitively excluding native AT RISK OF FUTURE INVASION BY species where they have been introduced. In one EURYOPS MULTIFIDUS of the few studies which has attempted to docu­ ment the consequences of invasion by these exotic In southern Arizona, semi-arid grasslands oc­ grasses, Bock et al. (1986) demonstrated that the cupy an elevational range between 900 and 1520 native semi-arid grassland community in their m. The three grassland sites where sweet resin southeastern Arizona study site had a signifi­ bush has become invasive range from 1060 to 1460 cantly greater variety and abundance of m elevation. Sweet resin bush becomes dominant indigenous grasses, herbs, shrubs, grasshoppers, on many kinds of soil including 1) those with rodents and birds than the areas dominated by thick clay-enriched horizons (Haplargids, Palear­ African lovegrasses. Our preliminary observa­ gids, Argiustolls), 2) deep, loamy calcic soils tions suggest that monocultures of sweet resin (Calciorthids), and 3) young, sandy to gravelly bush may be equally biologically sterile with re­ soils of recently formed alluvial terraces (Torriflu­ gard to mammalian, avian, and insect species vents and Camborthids). These account for most (data not shown). of the soils of semi-arid grasslands in southern The consequences to the native ecosystem of Arizona. Consequently, we believe that most of invasion by exotic plants can extend beyond the the semi-arid grasslands of southern Arizona are loss of native diversity, resulting in ecosystem at risk (fig. 3). The considerably colder winter con­ level changes that perpetuate further reductions ditions of the temperate, semi-arid grasslands of in native diversity. For example, many of the ex­ the Colorado Plateau in northeastern Arizona are otic grasses which have established in the probably too severe for E. multifidus. Southwest, especially bufflegrass and red brome The occurrence of sweet resin bush in Sonoran (Bromus rubens), tolerate burning better than desertscrub at Sabino Canyon suggests that some most natives. Because they can alter the structure areas supporting this vegetation type may also be of vegetation communities by producing continu­ at risk (fig. 3). However, at Sabino Canyon, E. ous canopies of grass and can prod uce multifidus did not entirely exclude the,. native substantially more biomass than the natives dur­ vegetation. The abundance of dead E. multifidus ing favorable years, they seem to promote fires following a recent dry year suggests that habitats that have a more adverse affect on the long-lived supporting desertscrub may be at the drier limit native vegetation than the exotics. We do not of the potential range of E. multifidus. Detailed know whether sweet resin bush has altered dis­ future analyses of the distribution of E. multifidus turbance regimes in the vegetation communities it with respect to climate in South Africa may pro­ has invaded, but effects on hydrologic and bio­ vide a more detailed and predictive estimate of geochemical-cycling regimes are likely to have potential range of spread in North America. occurred. Further, we have observed substantially enhanced erosion rates where sweet resin bush has invaded semi-arid grassland. This ecosystem DISCUSSION level change is likely to have permanently altered sites that have been invaded by sweet resin bush, Between 1935 and 1942 the SCS introduced a even if the exotic is removed. number of exotic species in the arid southwestern The growing list of exotics which have become United States for the purpose of range improve­ natu14 alized in the Sonoran Desert and semi-arid ment and erosion control (Table 1). The grassland vegetation of the southwestern United introduction of many of these species has sub­ States suggests that these vegetation types are in­ sequently been encouraged by public and private deed highly vulnerable to invasion by exotic groups, the end result being that many of the ex­ plants, particularly to those pre-adapted to the lo­ otics introduced in the early days of the SCS have cal climate and grazing regimes. The dramatic become some of the Southwest's most serious eco­ consequences of invasion that have been docu­ logical problems. The most notorious examples mented for the few exotic species studied suggest are the drought-tolerant African grasses: buffle­ that these vegetation types are not only vulner­ grass (Pennisetum ciHare) and the lovegrasses able, but have little resilience to invasion once

229 exotics become established and ecosystem critical review of the manuscript. Finally, we changes are initiated. thank R. M. Turner for providing negatives for the We suggest that the ecological danger posed repeat photographs of Frye Mesa. by sweet resin bush in the Southwest is signifi­ cant. We believe that by examining further the characteristics of successful invaders and the con­ REFERENCES sequences of their spread, we can continue to learn more about the structure and function of the Bock, C. E., J. H. Bock, K. L. Jepson, and J. C. Ortega. 1986 . native vegetation communities and their vulner­ Ecological effects of planting African Lovegrasses in ability to invasion. We suggest future research on Arizona. National Geographic Research 2(4):456-463. sweet resin bush be focused on a) the life history Burgess, T. L.,J. E. Bowers, and R. M. Turner. 1991. Exotic characteristics of sweet resin bush and the mecha­ plants at the Desert Laboratory, Tucson, Arizona. Ma­ nisms by which native species are excluded, b) the drono38(2):96-114. rate and mode of spread in different vegetation Crider, F. J. 1935. Annual Report of the Southwestern communities where it has been introduced c) the Nurseries of the Soil Conservation Service. Tucson, ecology of interactions between sweet resin bush Arizona. Reporting period: Fiscal Year 19341935. and other species in its native range, d) quantifica­ Hegnaur, R.1977. In: Heywood V. H.,]. B. Harborne, and tion of native ecosystem level changes as a B. L. Turner, eds. The Biology and Chemistry of the consequence of invasion by sweet resin bush (in­ Composi tae Vol I. Academic Press, London, U.K. cluding soil erosion and the biodiversity of MacDougal, D. T. and R. M. Cannon. 1910. Conditions of parasitism in plants. Carnegie Institution of Washing­ microorganisms in the soil), and e) assessment of ton, Publication No. 129. the necessity and feasibility of an eradication pro­ Mack, R. N. 1985. Invading plants: their potential contri­ gram based on our knowledge of the ecological bution to population biology. In: White, J., ed. Studies consequences of invasion by sweet resin bush. on Plant Demography: A Festschrift for John L.Harper. We hope this discussion of the dramatic conse­ Academic Press, London, U. K. quences that have occurred as a result of invasion Mack, R. N. 1989. Temperate Grasslands Vulnerable to by sweet resin bush and the other exotics men­ Plant Invasions: Characteristics and Consequences. In: tioned above demonstrates the severity of this Drake,J. A., ed. Biological Invasions: a Global Perspec­ ecological problem and illustrates the importance ti ve .1989 SCOPE .John Wiley and Sons, of implementing management practices that mini­ Mahall, B. E. and R. M. Callaway. 1991. Root communica­ mize the future consequences of i!lvasion by tion among desert shrubs. Proceedings of the National exotic species. Academy of Sciences (USA) 88:874-876. Nordenstam, B. 1968. The Genus Euryops, Part 1. Taxon­ omy. Opera Botanica, No. 20. C.W.K. Gleerup, Lund, ACKNOWLEDGMENTS Sweden.409 pp. Nordenstam, B. 1969. Phytogeography of the genus Eu­ We thank R. M. Turner for introducing E. A. ryops (Compositae) a contribution to the Pierson to the Frye Mesa site, M. St. John for intro­ phytogeography of Southern Africa. Opera Botanica, Ko. 23.C.W.K.Gleerup,Lund, Sweden. ducing J. R. McAuliffe to the same site, and T. L. Pole··Evans, I. B. 1928. The Flowering Plants of South Burgess for suggesting the collaboration. We also Africa. Vol. III. The Specialty Press of South Africa, thank B. Munda and M. Pater of the SCS Plant LTD.pp281-320. Materials Center, Tucson, Arizona and D. Kerby Smith, C. A. 1966. Common Names of South African of the SCS Plant Materials Center, Las Lunas, New Plants. Memoirs of the Botanical Survey of South Af­ Mexico for access to the archives of SCS Annual rica No. 35. Government Printer, Pretoria. p 244. Reports. We thank J. Ruyle, of the USDA Forest Wells, M.J., A.A. Balsinhas, H. Joffe, V.M. Engelbrecht, G. Service for facilitating research at Sabino Canyon. Harding, and C.H. Stirton.1986. A Catalogue ofProb­ We also acknowledge T. L. Burgess, P. Warshall, lem Plants in Southern Africa. Memoirs of the and M. P. McClaren for helpful discussions and J. Botanical Survey of South Africa No. 53. Government E. Bowers, R. M. Turner, and L. S. Pierson for their Printer, Pretoria.

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