OIKOS 80: 8-17. Copenhagen1997

Demographicevaluation of a herbivory-sensitiveperennial bunchgrass:does it possess an Achilles heel?

B. C. Hendon and D. D. Briske

Hendon,B. C. and Briske,D. D. 1997.Demographic evaluation of a herbivory-sen- sitive perennialbunchgrass: does it possess an Achillesheel? - Oikos 80: 8-17.

Plant and tiller demographyof a C4 perennialbunchgrass, sericea, were evaluatedto define specifictraits that contributeto its sensitivityto herbivoryby domesticgrazers. We tested threehypotheses: (1) defoliationadversely impacts tiller recruitmentto a greaterextent than mortality,(2) tiller recruitmentand/or mortality are particularlysensitive to defoliation at the time of culm elongation, and (3) synchronoustiller recruitmentcontributes to a meristematiclimitation which con- strains growth following defoliation. Demographicvariables were monitored on permanentlymarked and tillersthat weredefoliated at variousfrequencies and stages of phenologicaldevelopment for two successiveyears. Hypothesesone and threewere rejectedbecause defoliation adversely impacted per capita tillermortality to a greaterextent than per capita tiller recruitmentand tiller recruitmentoccurred throughoutthe spring and summer,rather than synchronously.Apical meristem elevationin vegetativetillers did not extendbeyond 5 mm above the soil surfaceand the proportionof reproductivetillers did not exceed 10%of the total numberof tillers. Low values for both morphologicalattributes indicate that they did not contributeto a meristematiclimitation constraining leaf growth.Hypothesis two was not rejectedbecause cumulative, but not per capita,tiller recruitment was reducedto a greaterextent by defoliationduring culm elongationthan duringthe pre-culmor post-culm stage. Plants that receivedmultiple defoliations exhibited the greatest declinein basal areaand tillernumber compared to undefoliatedplants, and only the undefoliatedplants and plants defoliated during the pre-culm stage recruiteda sufficientnumber of tillersto offset tillermortality. In spite of the adverseeffects of two of the four defoliationregimes, we were unable to identifya specifictrait (i.e., Achilles heel) within this species that contributedto a meristematiclimitation and herbivory-sensitivity.An alternativeinterpretation of herbivory-sensitivityis pro- posed which emphasizesthe involvementof more subtle extrinsic mechanisms, includingherbivore-mediated competitive interactions and drought-herbivoryinterac- tions. Assessmentof herbivoryresistance based on the 'specifictrait approach'fails to recognizeand address the importanceof extrinsicmechanisms associated with herbivore-inducedprocesses at higherecological scales.

B. C. Hendon and D. D. Briske (correspondence), Dept of Rangeland Ecology and Management, A&M Univ., College Station, TX 77843-2126, USA ([email protected]).

Grass-grazer interactions have been intensively investi- research activity, a thorough understanding of the gated since the 1970's and experimental evaluations of mechanisms and/or attributes that convey herbivory grass responses to defoliation have been conducted in sensitivity or tolerance have not been clearly estab- North America since the turn of the century (Briske lished. Consequently, herbivory tolerance is often ap- and Richards 1994, 1995). Yet, in spite of intensive plied on a comparative, rather than a mechanistic basis

Accepted8 January1997 Copyright? OIKOS 1997 ISSN 0030-1299 Printedin Ireland- all rightsreserved

8 OIKOS 80:1 (1997) (Briske1996, Briske et al. 1996).Herbivory resistance is the time of culm elongation,just before inflorescence establishedby the qualitativeand/or quantitative expres- emergence,has been demonstratedto increase tiller sion of attributesconferring resistance (e.g., specifictrait initiationin severalperennial grasses (e.g., Jamesonand approach)and/or the extentof biomassremoval or dam- Huss 1959,Olson and Richards1988b), but suppressit age associatedwith herbivory(e.g., bioassayapproach) in others (Vogel and Bjugstad 1968, Culvenor 1994). (Simms 1992). Limited insight into the mechanisms Similarly,the periodicityof tiller initiation also may conferring herbivory-sensitivityto individual species influencethe capacityfor growthby affectingmeristem- populationsfurther constrains our abilityto extrapolate atic availability (Mott et al. 1992, Culvenor 1994). this importantconcept to higherecological scales (e.g., Synchronoustiller initiation may exhaust the pool of Brown and Allen 1989, Brown and Stuth 1993). axillarybuds to the extent that minimalmeristematic A current assessment of herbivory tolerance in potentialremains, if the currenttiller cohort experiences grassesindicates that demographicprocesses and archi- mortality in response to defoliation, drought, or a tecturalattributes are of greaterimportance than phys- combinationof stresses. iological processes. A thorough comparativeinvesti- We evaluatedthe C4 perennialgrass, Eriochloa sericea gation of a herbivory-tolerantand herbivory-sensitive (Scheele)Munro, because of its recognizedsensitivity to C3 perennial bunchgrass by Caldwell et al. (1981) herbivoryby domesticgrazers. This specieshas showna demonstratedthat the ability to replace leaf area by drasticdecrease in abundanceon the EdwardsPlateau rapid tiller initiation and developmentof leaves with of Texas since high concentrationsof domestic herbi- low specificmass were more importantthan compensa- vores (cattle, sheep and goats) were introducedin the tory photosynthesis(Nowak and Caldwell1984) or size 1870's(Youngblood and Cox 1922).Viable populations of reservecarbon pools (Richardsand Caldwell 1985). of E. sericeacurrently exist in communitieswhere grazing Similar conclusionshave been drawn from investiga- by domesticherbivores has been minimalor absentfor tions of species populationswith contrastinghistories long periods(>50 yr; Smeinset al. 1976).We reasoned of grazing (i.e., grazing morphs). Decumbentcanopy that an especially herbivory-sensitivespecies would architecturescomprised of a largernumber of smaller providean excellentopportunity to identifythe specific tillerswith lower leaf areasmake a greatercontribution trait(s)(i.e., Achillesheel) that contributedto the herbi- to herbivory resistance than physiological processes vore-induceddecline in and tillerpopulations. We includingphotosynthetic rate, transpirationrate or wa- emphasizeda demographicassessment because previous ter-use efficiency (Detling and Painter 1983; but see investigationshave indicatedthat tiller replacementis Polley and Detling 1988).Architectural attributes limit- among the most criticalprocesses associated with her- ing the amount and photosyntheticefficiency of re- bivory tolerancein bunchgrasses(Caldwell et al. 1981, mainingleaf area following defoliationalso have been Mott et al. 1992).Annual tiller replacement is necessary emphasizedas an explanationfor herbivory-sensitivity to offset mortalityassociated with short tiller longevity of Themedatriandra (Coughenour et al. 1985,Hodgkin- (<2 yr) to maintainboth plant and populationpersis- son et al. 1989, Mott et al. 1992). This information tence (Olson and Richards1988a, b, Briskeand Butler collectivelyidentifies meristematic availability, includ- 1989). ing leaf differentiationfrom apical meristemsand tiller Three specifichypotheses were tested:(1) defoliation initiationfrom axillarybuds, as a criticalvariable deter- adverselyimpacts tiller recruitmentto a greaterextent miningherbivory resistance in perennialgrasses. thantiller mortality, (2) tillerrecruitment and/or mortal- Although both initiation and longevity of tillers of ity are particularlysensitive to defoliationat the time of numerousbunchgrasses are known to be adverselyaf- culm elongation,and (3) synchronoustiller recruitment fected by defoliation,tiller initiation is frequentlythe contributesto a meristematiclimitation which constrains most sensitive (Butler and Briske 1988, Bullock et al. growth. Research protocol involved identificationof 1994; but see Olson and Richards 1988a).Differential establishedE. sericea plants in a communitythat had tiller initiationamong grassesfollowing defoliation ap- been protectedfrom domestic herbivoresfor approxi- pearsto be a functionof axillarybud activation,rather mately50 yr. Demographicvariables were monitored on thana reductionin the numberand/or viability of axillary permanentlymarked plants and tillersthat were defoli- buds (Muellerand Richards 1986, Busso et al. 1989). ated at various frequenciesand stages of phenological Unfortunately,variable axillary bud growthamong spe- developmentfor two successiveyears. cies followingdefoliation is difficultto interpretbecause our understandingof the physiologicalprocesses and environmental signals regulating tiller initiation is inconclusive(Cline 1991, Murphyand Briske 1992). Methods The magnitudeof tillerrecruitment can be influenced Study site by the phenologicalstage of plant developmentat the time of defoliation,but the documentedresponses are Researchwas conductedat the Texas A&M University inconsistent(Briske and Richards1995). Defoliation at AgriculturalExperiment Station located 56 km south of

OIKOS 80:1 (1997) 9 Sonora,Texas, USA. The station lies in the southwest- development to assess plant and tiller responses. A ern portion of the Edwards Plateau Land Resource portionof the plantswere defoliatedin the (1) pre-culm Area (30 18'N, 100 28'W;735 m a.s.l.). Stony, clay soils elongationstage (mid-April),(2) culm elongationstage of the Tarrantseries (Lithic Haplustolls)dominate the (mid-May),(3) post-culmelongation stage (mid-June), area. Soil depth typicallyranges between 15 and 30 cm and (4) at all threephenological stages. Defoliation was and slopes are generally less than 5%. Soils contain implementedby hand clipping plants to a height of 6 limestonefragments, stones and gravel and are under- cm above the soil surface which removed approxi- lain by a limestonesubstratum (Wiedenfeld and McAn- mately 75%of the canopy volume. Neighboringplants is a drew 1968).The area potentially midgrassgrassland within a 30-cm radius of the permanentlymarked with individualand clusteredtrees including Quercus plants also were defoliated,in the same manneras the var. Ju- virginiana Mill, Q. pungens vaseyana Buckl., targetplants within a treatment,to a height of 6 cm to ashei Buckl. and J. Sudw. Late-seral niperus pinchotii minimizeconfounding influences of neighborhoodcom- have decreasedin abundancein to midgrasses response 1972, intensivelivestock but in areas excludedfrom petition (e.g. Mueggler Belsky 1986). Neighbor- grazing, hoods were of three or four E. sericea and Bouteloua comprised conspecific grazing curtipendula (Michx.) of size to the Torr have retained or increased their relative abun- neighbors comparable target plants. Plant variablesmonitored were basal live tiller dance and Merrill Median annual area, (Smeins 1988). pre- and the of culmed and is 439 mm, but seasonal and annual number, proportion vegetative cipitation tillers. If showed of droughts,as well as above normal rainfallevents, are plants signs fragmentation(i.e, of the basal common. Annual precipitationwas 98 and 93%of the separation plant circumference),separate basal area measurementswere made for each long-termmean duringthe first and second year of the fragment. were as the absolute at investigation,respectively. However, a distinct dry pe- Plant variables analyzed change riod occurred between June and August 1994 when each census from the initial census (April 1994).Plants precipitationwas 56%less than the long-termmean for that died duringthe investigationwere includedin the that interval. The study site was located in a 16-ha analysisto representan absoluteloss of basal area and pastureexcluded from livestockherbivory since 1948. tiller number. Four tillers with three or four leaves and no visible juveniletillers were permanentlymarked on the periph- ery of each plant with wire loops to monitor tiller Species description demography.Tiller variables were juvenile tiller recruit- ment, of meristem, Eriochloasericea (Scheele) Munro, Texas cupgrass,is a height apical phenology(vegetative and those with culms) and sur- C4 perennialbunchgrass (Shaw and Smeins 1983). E. reproductiveincluding cohort. Tillers between succes- sericeais classifiedin the tribe Paniceaeand subfamily vivorshipby emerging sive census intervals were as individual Panicoideaewithin the family . It has erect to analyzed cohorts. Cumulativetiller recruitmentand ascendingculms that can attain heights of 50-90 cm. mortality Growthfrequently begins in Februaryand reproductive were calculated as the summation of tillers that developmentoccurs in May; however, flowering can emergedor died from the initially marked tillers. Per occur as early as April and continue until November capita tiller recruitmentand mortalitywere calculated when environmentalconditions are favorable.The geo- for each intervalas the numberof tillers emergingor graphicdistribution of this species is limited to Texas, dying duringa censusinterval relative to the numberof Oklahomaand Coahuila, Mexico. E. sericea has been live markedtillers plant-' at the previouscensus (Bul- describedas a late-seraldominant for severalgrasslands lock et al. 1994). Per capita tiller dynamicswere ana- in Texas (Dyksterhuis1946, Allred 1956, Collins et al. lyzed as mean tiller tiller- plant- month- . Response 1975).This specieshas declinedin abundancethrough- variablesfor both plant and tillers were monitoredin out its range following long-term intensive livestock mid-April,mid-May, mid-June and in mid-Octoberof grazingand land conversion(Shaw and Smeins 1983). both years. The experimentwas arrangedas a split-plot design with defoliation the main plot factor and time the subplot factor. Data were analyzedusing GLM proce- Experimental design dures (SAS InstituteInc. 1988). Means were separated Sixty E. sericeaplants with a mean basal area of 20.2 using BonferroniT-tests when a factor was significant. (s.e. 3.3) cm2 and mean tiller numberof 53 (s.e. 7.4) Significancewas determinedat P < 0.05 unless other- were identifiedin April 1994. Twelve plants were ran- wise indicated. A LIFETESTlogrank procedurewas domly assignedto each of four defoliationtreatments used to determineif defoliationtreatment altered tiller and a control group along four line transects.Defolia- survivorship within individual cohorts (Pyke and tion was imposedat three phenologicalstages of plant Thompson 1986, SAS InstituteInc. 1988).

10 OIKOS 80:1 (1997) Results 14 Plant variables 12

64 '+. 10 The generalized pattern of plant response to defoliation *n' over the was characterized an 8 2-yr investigation by 3 *^ increase in mean basal area plant-1, with the exception 1-1 s 6 CS . of plants receiving multiple defoliations, and a decrease 4 in mean tiller number plant-1 (Fig. la and b). Defolia- u Vz 2 tion was significant for both variables; a significant defoliation x time interaction was not observed. Time 0 was significant for mean tiller number plant- 1, but not for mean basal area plant-'. Tiller number plant-' 0 after October 1994 was lower to -2 significantly compared -4-i tiller number before October 1994 which 0 plant-1 may _s -4 have been a result of below average precipitation (56% Q) 04td -6 less than the long-term mean) during July and August -8 1994. 3 Multiple defoliation was the only treatment that in- -10 duced a significant decrease in mean basal area plant-1 -12 Undefoliated and defoliated at (Fig. la). plants plants -14 the pre-culm stage exhibited 55 and 24% increases in 5/94 10 4/95 10 basal area plant-', respectively. Plants defoliated dur- Census date ing the pre-culm stage showed a significantly greater 2. Mean cumulativetiller recruitment and (P <0.10) increase in basal area plant-1 compared to Fig. ( s.e.) (a) cumulativetiller mortality (b) for Eriochloasericea plants to defoliationto a of 6 cm at culm, subjected- I 1 1 , 'I' .r - height- r, 1 -. pre-culm,I I - 1 -- I post-culm and at all three stages ot phenological development a compared to undefoliatedplants on the Edwards Plateau, N 50 Texas. Cumulativevalues representthe accumulatedsum of tillersthroughout the 2-yr investigation.Different letters indi- O cate significant (P < 0.05) differences between defoliation - 40 treatments.Census dates were pooled for analysis.

30 a IC8 plants defoliated during the culm stage or post-culm stage (-5 and + 17% change, respectively). t 20 Plants receiving multiple defoliations showed the C,cn greatest decline (-77% relative to the initial census) in cg 10 b uip d lb mean tiller number plant-' and significantly differed 0 from all other treatments (Fig. lb). Plants defoliated b+ defoliation Multiple the culm exhibited an intermediate re- * *" Undefoliated during stage 70 * ' Pre-culmstage sponse (-47%) to plants receiving multiple defoliations !.f .i tc- Culmstage and undefoliated and those defo- 60 ~ -pCU plants (-13%) plants Post-culmstage liated during the pre-culm (-25.6%) and post-culm 50 stages (-28.5%). a occurred in the ,-rn 40 Plant fragmentation and mortality

OIKOS 80:1 (1997) 11 of the growing season (Fig. 2a). Cumulativetiller re- Mean apical meristemheights for vegetative,culmed cruitmentand mortalityshowed significant responses to and reproductivetillers were 5.5 (s.e. 0.4), 64.5 (s.e. defoliation.Multiple defoliation and defoliationat the 8.3), and 197.4 (s.e. 16.9), mm, respectivelyin April culm stage significantlyreduced cumulative tiller re- 1995. The percentages of culmed and reproductive cruitmentcompared to the other treatments.Plants that tillers relative to vegetative tillers for undefoliated receivedmultiple defoliations exhibited slightly greater plants in 1995 were 1, 10 and 6% in April, May and (7%) recruitmentthan those plants defoliated during June, respectively. the culm stage. Plants defoliatedduring the post-culm stage showed the least reduction(-5%) in recruitment comparedto undefoliatedplants. Plants defoliated dur- ing the pre-culm stage exhibited significantlygreater Discussion recruitmentcompared to all treatments. Our evaluation of E. sericea failed to Plants defoliatedduring the pre-culmand post-culm demographic cumulativetiller identify a specific trait that contributedto herbivory- stages displayed significantlygreater but it did the of and to sensitivity, support interpretation a mortality (28% 11%, respectively)compared meristematicconstraint on defolia- undefoliated and and growth following plants (39% 21%, respectively) tion. Two of the initial three were to defoliationsdur- hypotheses rejected. compared plants receivingmultiple Defoliation tiller tiller-' the Plantsdefoliated the culm adverselyimpacted mortality ing year (Fig. 2b). during to a extent than tiller tiller-' recruitment showed an intermediate and did not greater (hy- stage response and tiller recruitmentwas not differ from other treatment.The ratio pothesis 1) synchronous significantly any but occurred the and of cumulative tiller recruitmentto cumulative tiller (hypothesis3), throughout spring summerwhen conditionswere most fa- within early growing mortality a treatmentcorresponded closely with vorable. Tiller recruitmentwas reduced to a the numberof live tillers greater plant-'. extent by defoliationduring culm elongationthan dur- Tiller tiller-' recruitmentshowed a time significant ing the pre-culmstage or post-culmstage of phenologi- responsebased on greatesttiller recruitmentduring the springand early summer.Although a significantdefoli- ation responsewas not observed,a significantdefolia- 1.2 tion x time interaction ^-SI'll occurredand was likely caused ._ by high variationin recruitmentin June 1995for plants 1.0 defoliated in the culm and pre-culmstages (Fig. 3a). 0.8 Tillertiller-' mortalityrates were similarin magnitude , to recruitmentrates; however, mortality rates did show 0.6 a significant defoliation response because of lower 0.4 treatmentvariability (Fig. 3b). Plants subjectedto mul- 0.2 tiple defoliations had a significantlyhigher mortality rate than did undefoliatedplants. The other threedefo- 0.0 liation treatmentsdid not differ significantlycompared to undefoliatedplants. 1.2 The majority of tillers within all cohorts survived ,-a 1.0 1 of defoliationtreatment. Undefoli- only yr regardless 0.8 O as? ated exhibited tiller . c plants greatest survivorshipwith 0 the of the October 1994 cohort 0.6 exception (Fig. 4). S . - Tillers in the October 1994 cohort had the greatest _/ 0.4 survivorshipin those treatmentsshowing the greatest ._ 0.2 decrease in tiller number and basal area plant-' which is indicative of a density-dependentresponse. U.U Defoliation treatmentssignificantly affected tiller sur- 5/94 10 4/95 10 vivorshipin the June 1994 and April 1995 cohorts. In Censusdate both of these cohorts, tiller survivorshipwas signifi- Fig. 3. Mean(+s.e.) tillertiller-' plant-' month-' recruit- cantly reduced by defoliation during the culm stage ment(a) and mortality(b) for Eriochloasericea plants sub- to defoliationto a of 6 compared to undefoliated plants. Tiller survivorship jected height cm at pre-culm,culm, post-culmand at all threestages of phenologicaldevelopment was significantlyreduced by post-culm and multiple comparedto undefoliatedplants on the EdwardsPlateau, defoliation treatmentsin only the June 1994 cohort. Texas. Rates calculatedas the numberof tillersrecruited/died Tiller survivorshipfor the May 1995 and June 1995 during a census intervalrelative to the numberof live tillers cohortswas presentat the beginningof that interval.Rates werepresented similarto the respective1994 cohorts (data on a monthlybasis to standardizefor unevencensus intervals. not shown). Censusdates were pooled for analysis.

12 OIKOS 80:1 (1997) 102

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101 I 8 '~ :CMultiple" defoliation 6 AF 4. ?p Und efo lia ted 5 Pre-culmstage 4x Cuimstage 3 m to3~ a height ofatpre-' 66 cm - Post-culm stage 2 October 1994 cohort April 1995 cohort 10 4/94 10 4/95 10 4/94 10 4/95 10 Censusdate Fig. 4. Survivorshipfor April, May, June, and October1994 tiller cohortsfor Eriochloasericea plants subjectedto defoliation to a heightof 6 cm at pre-culm,culm, post-culmand at all threestages of phenologicaldevelopment compared to undefoliated plants on the EdwardsPlateau, Texas. cal development (hypothesis 2). Plants receiving multi- Tiller recruitment is generally considered to be more ple defoliations during the growing season exhibited the responsive to defoliation than mortality in perennial greatest decline in basal area and tiller number com- grasses (Butler and Briske 1988, Bullock et al. 1994; but pared to undefoliated plants. Plant fragmentation and see Olson and Richards 1988a). However, per capita death became evident in these the end of the plants by tiller mortality increased significantly in plants sub- first season. Plants defoliated once a growing year jected to multiple defoliations compared to undefoli- during the culm exhibited elongation stage only slightly ated plants, while per capita tiller recruitment showed less adverse responses than plants receiving multiple greater variability and less response to defoliation. A defoliations. At the end of the 2-yr investigation, suffi- comparable response has been documented for A. cient tiller recruitment had occurred to compensate for desertorum, a herbivory-tolerant tiller mortality in only undefoliated plants and those perennial bunchgrass introduced into North America from Eurasia plants defoliated during the pre-culm stage. The ad- (Olson and Richards of tiller verse responses of E. sericea to defoliation were not 1988a). Responses per capita to proportionately greater than those observed for its re- recruitment and mortality defoliation significantly maining codominant, Bouteloua curtipendula, (Hen- modified both cumulative tiller recruitment and mortal- drickson and Briske unpubl.) and an extremely ity in E. sericea plants throughout the 2-yr investiga- herbivory-tolerant bunchgrass, Agropyron desertorum tion. However, live tiller number plant-1 appears to (Caldwell et al. 1981). have resulted primarily from differential per capita tiller

OIKOS 80:1 (1997) 13 mortality,rather than from differentialper capita tiller tolerant of herbivorythan is A. spicatum(Caldwell et recruitment.Cumulative tiller recruitmentvaried in re- al. 1981, Caldwell 1984). sponse to live tiller numberplant-1 as opposed to per The absence of a specific trait contributingto the capita tiller recruitmentwhich was not significantly defoliation-inducedmeristematic limitation in E. sericea influencedby defoliation. makes it difficultto explainthe significantreduction in Tiller recruitmentin E. sericea occurredthroughout cumulativetiller recruitmentand basal area and in- the spring and early summerregardless of the pheno- creased rate of tiller mortality in plants subjectedto logical stage at which defoliationwas imposed.Peren- multipledefoliations and defoliationat the culm stage nial forage grassesfrequently exhibit a markeddecline of phenologicaldevelopment. Perhaps these plants en- countereda in tiller recruitmentduring the culm elongation stage carbonlimitation imposed by minimalleaf area and low (e.g., Langeret al. 1964, Laude et al. 1968, Culvenor photosyntheticefficiency of the remaining defoliation as has been observedin 1994). However, this response is not consistentlyob- canopy following Themeda triandra et al. served in native perennialgrasses (Jamesonand Huss (Coughenour 1985,Hodgkinson et al. 1989,Mott et al. However,neither leaf area 1959, Olson and Richards1988b). Suppression of tiller 1992). nor photosyntheticrate was measuredin this initiation at this stage of phenologicaldevelopment is investiga- tion based on the evidence indicatingthat herbivory- often interpretedon the basis of hormonalregulation sensitivity in North American bunchgrasses is a (Jewiss1972, Murphy and Briske1992) and/or resource functionof meristematiclimitations, rather than physi- diversionfrom juvenile tillers to culm support elonga- ological constraints(e.g., Caldwellet al. 1981, tion at the time of and Powell Detling flowering(Ryle 1972, and Painter 1983, Busso et al. 1989). Smith and Leinweber et al. Resource 1973, Ong 1978). Why werewe unableto identifyan "Achillesheel" in diversionfrom tillers to culms is juvenile reproductive a bunchgrassspecies recognizedas being remarkably not a for reducedtiller initiation plausibleexplanation sensitiveto herbivory?The explanationmay lie beyond in E. sericeabecause of the low percentage(10% maxi- the inherentability of individualspecies to replaceleaf mum) of reproductivetillers observed. Tiller recruit- area following defoliation (i.e., intrinsic mechanisms; ment over a several month period demonstratesthat sensu McNaughton 1983). The specifictrait approach synchronoustiller recruitmentwas not an important (Simms 1992)for evaluatingand interpretingherbivory componentof herbivory-sensitivity. resistanceis based on the assumptionthat a relatively E. sericeadoes not possess morphologicalattributes small numberof traits, or even a singletrait, associated traditionallyassociated with herbivory-sensitivegrasses. with the developmentalmorphology or physiological The reproductive:vegetativetiller ratio did not exceed function of individual species is responsiblefor her- 10%and apical meristemelevation above the soil sur- bivory-sensitivity.An alternativeinterpretation of her- face did not exceed 5 mm in vegetativetillers. A high bivory-sensitivity,within comparable grass growth reproductive:vegetativetiller ratio determinesthat a forms, is based on the involvement of more subtle greaterportion of canopy replacementmust originate extrinsic mechanisms(sensu McNaughton 1983) and by tiller initiationfrom axillarybuds, ratherthan from their interactionwith intrinsicmechanisms, rather than leaf differentiationfrom existing apical meristems,be- on the exclusive contributionof intrinsicmechanisms cause apicalmeristems have been committedto inflores- (e.g., Barnes 1972, Brown and Stuth 1993). Extrinsic cence development(Branson 1953, Briske and Richards mechanismsinvolve both biotic and abiotic processes external to 1995).Elevation of apicalmeristems in vegetativetillers plants that potentially influencetheir re- to defoliation increasessusceptibility to removalby grazerswhich also sponse (McNaughton 1983). Important extrinsicmechanisms include selective determines that canopy replacementmust occur by herbivoryamong species (Brown and Stuth 1993, Andersonand Briske tiller growth from axillarybuds (Branson 1953, Booy- 1995), herbivore-mediated interactions sen et al. 1963).In both instances,canopy replacement competitive 1972, Caldwellet al. and by tillerinitiation from buds is a slower (Mueggler 1987) drought-her- axillary process interactions et al. O'Connor than continuation of leaf from bivory (Mott 1992, 1995). growth intercalary A decreasein tillernumber reduced meristemsor leaf differentiationfrom meristems significant plant- , apical survivorshipof the June 1994 tiller cohort, and the (Olsonand Richards1988b, Briske and Richards 1995). occurrenceof plant mortalityduring the summerof withoutthe occurrenceof elevated dry Herbivory-sensitivity 1994 indicate that a drought-defoliationinteraction apicalmeristems and a of high proportion reproductive contributedto the decline in tiller and plant popula- tillers the conclusionof Caldwell indi- supports (1984) tions of E. sericea. Extrinsicmechansims may be of that care must cating be taken to avoid unwarranted equal or greaterimportance than intrinsicmechanisms generalizationsconcerning herbivory tolerance in rela- in determiningspecies responses to herbivoryin grazed tion to architecture.For plant example,both A. deser- systems (Archer and Smeins 1991). Unfortunately, torumand A. spicatumdisplay early elevationof apical extrinsicmechanisms are often excludedfrom investiga- meristemsand possess a relativelyhigh proportionof tions designed to assess herbivory-sensitivityor toler- reproductivetillers, but A. desertorumis much more ance based on the specifictrait approach. 14 OIKOS 80:1 (1997) We speculate that herbivory-sensitivity of E. sericea contribute to species replacement. While we did not may partially result from the possession of a competitor investigate all potential intrinsic variables that may life-history strategy (Grime 1979: 9). This strategy is have contributed to the herbivory-sensitivity of E. characterized by early growth initiation, several weeks sericea, these results do represent a case where her- before that of associated C4 species, a high nitrogen bivory-sensitivity could not be explicitly attributed to a content and a low proportion of structural materials specific trait inherent to a species population. The (Shaw and Smeins 1983). These attributes are fre- alternative interpretation indicates that herbivory-sensi- quently associated with rapid growth rates as described tivity also can result from more subtle extrinsic mecha- in the resource availability hypothesis of plant defense nisms within a community. Assessment of herbivory (Coley et al. 1985). These attributes may have con- resistance based on the specific trait approach fails to tributed to the competitive ability of E. sericea by recognize and address the importance of extrinsic mech- effectively preempting resources early in the season in anisms associated with herbivore-induced processes at the absence of severe herbivory. However, early growth higher ecological scales. initiation and rapid growth may have predisposed this - Researchwas the USDA to selective which have in turn Acknowledgements supportedby species herbivory, may EcosystemsProgram (Grant #92-37101-7463)and the Texas compromised its competitive advantage relative to AgriculturalExperiment Station. We gratefullyacknowledge other perennial grasses within the community following the facilitationof field work by C. A. Taylor, superintendent of the Sonora station, and the constructiveevaluation of an the introduction of large numbers of domestic herbi- earlierdraft of the manuscriptby C. A. Busso,R. B. Shawand vores. Herbivory early in the growing season would F. E. Smeins. likely predispose this species to multiple defoliations which we have shown to adversely affect tiller popula- tions. References This species has historically been subjected to more - severe defoliation than imposed in this experiment Allred, B. W. 1956. Mixed prairiein Texas. In: Weaver,J. E. and F. E. Grasslandsof based on estimates of livestock numbers in the Albertson, (eds), the Great region Plains:their natureand use. JohnsenPubl., Lincoln,NE, during the late 1800's (Youngblood and Cox 1922). pp. 267-283. Sheep were the initial domestic herbivore introduced Anderson,V. J. and Briske, D. D. 1995. Herbivore-induced in is it driven into the region and are capable of grazing closer to the speciesreplacement grasslands: by herbivory toleranceor avoidance?- Ecol. Appl. 5: 1014-1024. soil surface than horses or cattle based on their prehen- Archer,S. and Smeins,F. E. 1991. Ecosystem-levelprocesses. sile abilities (Hofmann 1989). The herbivory tolerance - In: Heitschmidt,R. K. and Stuth, J. W. (eds), Grazing of even the most tolerant could have been management:an ecological perspective. Timber Press, species 109-139. this severe In Portland,OR, pp. suppressed by grazing regime. addition, Barnes,D. L. 1972. 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16 OIKOS 80:1 (1997) Smith,A. E. and Leinweber,C. L. 1973.Incorporation of 4C Wiedenfeld,C. C. and McAndrew,J. D. 1968. Soil surveyof by little bluestem tillers at two stages of phenological Sutton County, Texas. - Soil Conser. Serv., U.S.G.P.O., development.- Agron. J. 65: 908-910. Wash., DC. Vogel,W. G., and Bjugstad,A. J. 1968.Effects of clippingon Youngblood,B. and Cox, A. B. 1922. An economicstudy of yield and tillering of little bluestem, big bluestem, and a typicalranching area on the EdwardsPlateau at Texas.- Indiangrass.- J. Range Manage.21: 136-140. Tex. Agric. Exp. Stn. Bull. 297.

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