RESEARCH ARTICLE Impact of grasshoppers and an invasive grass on establishment and initial growth of restoration plant species

Catherine Cumberland1,†, Jayne L. Jonas1, Mark W. Paschke1,2

Exotic plant invasion can have dramatic impacts on native plants making restoration of native vegetation at invaded sites challenging. Though invasives may be superior competitors, it is possible their dominance could be enhanced by herbivores if native plants are preferred food sources. Insect herbivory can regulate plant populations, but little is known of its effects in restoration settings. There is a need to better understand relationships between insect herbivores and invasive plants with regard to their combined potential for impacting native plant establishment and restoration success. The objective of this study was to assess impacts of grasshopper herbivory and the invasive grass Bromus tectorum (cheatgrass) on mortality and growth of 17 native plant species used in restoration of critical sagebrush steppe ecosystems. Field and greenhouse experiments were conducted using moderate densities of a common, generalist pest grasshopper ( bivittatus). Grasshoppers had stronger and more consistent impacts on native restoration plants in field and greenhouse studies than cheatgrass. After 6 weeks in the greenhouse, grasshoppers were associated with 36% mortality over all native restoration species compared to 2% when grasshoppers were absent. Herbivory was also associated with an approximately 50% decrease in native plant biomass. However, effects varied among species. Artemisia tridentata, Chrysothamnus viscidiflorus,andCoreopsis tinctoria were among the most negatively impacted, while Oenothera pallida, Pascopyrum smithii,andLeymus cinerus were unaffected. These findings suggest restoration species could be selected to more effectively establish and persist within cheatgrass infestations, particularly when grasshopper populations are forecasted to be high. Key words: Bromus tectorum, exotic plant, indirect effects, Melanoplus bivittatus, revegetation, sagebrush

invasion by the Eurasian winter annual Bromus tectorum Implications for Practice L. (cheatgrass) (Noss et al. 1995; Knapp 1996). Cheatgrass • Given a choice, early instar grasshoppers prefer to grows more quickly and efficiently than most native plant eat cheatgrass rather than many native plants used in species early in the growing season (Harris 1967), produces the restoration of western U.S. rangelands. However, self-facilitating alterations to fire regime and soil conditions grasshopper feeding has little impact on cheatgrass (Whisenant 1990), and increases the risk of extirpation for while even minimal feeding affects restoration species sagebrush-associated plant and species (Knapp 1996; negatively. Blank & Morgan 2010; Davies et al. 2011). Due to ongoing eco- • Immature grasshoppers can inflict severe damage on logical and economic consequences of cheatgrass invasion and restoration plant seedlings; restoration projects should limited success of restoration efforts, there is a need to better consider potential impacts and plan accordingly. understand mechanisms inhibiting native plant establishment • Certain restoration plants are either highly preferred or in cheatgrass-dominated areas. In particular, the question of highly intolerant of grasshopper herbivory, including the how native insect herbivores may be interacting with cheatgrass ecologically important shrub Artemisia tridentata (big sagebrush). In general, grasshopper-induced mortality on native restoration species was greatest in forbs and shrubs. Author contributions: CC, JJ, MP conceived and designed the study; CC, JJ performed the experiments; CC, JJ analyzed the data; CC, JJ, MP wrote and edited This information can be used to plan more successful the manuscript. restoration projects during periods of projected grasshop- 1Department of Forest and Rangeland Stewardship, Colorado State University, Fort per abundance. Collins, CO 80523-1472, U.S.A. 2Address correspondence to M. W. Paschke, email [email protected]

† Present address: Department of Biology, University of New Mexico, Albuquerque, Introduction NM 87131, U.S.A. Rangeland ecosystems of western North America have been © 2016 Society for Ecological Restoration doi: 10.1111/rec.12430 dramatically altered through disturbances such as livestock Supporting information at: overgrazing, agriculture, and roads, all of which facilitated http://onlinelibrary.wiley.com/doi/10.1111/rec.12430/suppinfo

May 2017 Restoration Ecology Vol. 25, No. 3, pp. 385–395 385 Grasshopper–cheatgrass interactions warrants closer examination, given the potential for herbivores host plants if (1) actively growing B. tectorum is only available to influence competitive interactions between cheatgrass and during the early stages of grasshopper development or (2) B. tec- native plants. torum is nutritionally inadequate for grasshoppers to complete Ecological invasion theory predicts that resident natural ene- their life cycle. mies may either inhibit or increase the rate of spread of an intro- Restoration of degraded western U.S. rangeland has been duced species, depending on whether the species is attractive identified as a management priority but has often been unsuc- prey (Crawley et al. 1986). For example, an exotic plant species cessful (Davies et al. 2011). Restoring native vegetation in these stands a better chance of becoming invasive if it is introduced rangelands is especially challenging when practitioners must into a community of plants that are preferred by native herbi- contend with continual B. tectorum reinvasion. Some native vores (Crawley et al. 1986). Introduced and native species can restoration plant species might have the potential to succeed thus interact indirectly via a common enemy (Castorani & Hovel in competition with B. tectorum for space and resources, but 2015), leading to a form of herbivore-mediated “apparent” com- this potential could be curtailed by grasshopper preference petition (Holt 1977). A central assumption of the apparent com- for native plants, particularly during the establishment phase. petition hypothesis is that a shared evolutionary history with Here, we investigate impacts of a native, generalist grasshop- their host plants contributes to native herbivores’ preference for per on B. tectorum and native plant species used in restora- native plant foods. tion, to assess whether B. tectorum affects interactions between In the context of ecological restoration, relatively little is grasshoppers and native plants in a manner consistent with known about how interactions between native and invasive plant herbivore-mediated apparent competition. We conducted lab- species may be influenced by insect herbivores. Although her- oratory, greenhouse, and field experiments to address four bivorous in western U.S. rangeland ecosystems include questions: a wide variety of taxa and employ diverse feeding strategies, 1 Does a generalist grasshopper show a preference for restora- grasshoppers (: ) are the dominant above- tion species as a food source over B. tectorum? ground insect herbivores in these systems (Branson et al. 2006). 2 Does a generalist grasshopper affect restoration species sur- Evidence suggests that effects of grasshopper herbivory on plant vival and growth? communities can be substantial. In some western U.S. range- 3 If a generalist grasshopper feeds on B. tectorum, does this lands, grasshopper consumption of vegetation can rival that of affect B. tectorum survival and growth? livestock (Belovsky & Slade 2000; Branson et al. 2006). In 4 Do generalist grasshoppers affect survival and growth of addition to the amount of plant material consumed, grasshop- restoration species when B. tectorum is present? pers’ feeding habits result in a potentially large amount of veg- etation falling to the ground uneaten (“greenfall”) (Mitchell Grasshopper preference for native seedlings over invasive B. 1975; Meyer et al. 2002). Even where they consume only a tectorum, moderate impacts of grasshoppers on B. tectorum sur- small portion of primary production, grasshoppers can exert vival or growth, and stronger negative impacts of grasshoppers ecosystem-level influence by affecting plant competitive out- on native plants in communities with versus without B. tecto- comes (Joern 1989; Han et al. 2008). Survivorship and growth rum would support herbivore-mediated apparent competition of preferred food plants can greatly increase when grasshoppers as a mechanism of B. tectorum invasion and would suggest are excluded (Parker & Salzman 1985). a mechanism for past restoration failures. We expected native Many western U.S. grasshopper species overwinter as eggs, restoration species to be preferred because many western U.S. hatch in mid- to late spring, and reach adulthood 4–6 weeks rangeland plants remain green and relatively nutritious after B. later (Pfadt 1994). The timing of their emergence thus can over- tectorum has bolted (Rogers & Uresk 1974; Beckstead et al. lap with the spring growth phase of B. tectorum, which remains 2008), though these factors vary among plant species. Alterna- green into early summer (Hulbert 1955). Grasshoppers have tively, grasshopper preference for B. tectorum over native plants been observed eating invasive B. tectorum, though not neces- coupled with a negative effect of grasshoppers on B. tectorum sarily in proportion to its availability (Rogers & Uresk 1974; survival or growth would suggest that grasshoppers may act to Sheldon & Rogers 1978). Where B. tectorum is utilized as a food inhibit invasion and would thus promote restoration efforts. source, phenological asynchrony (i.e. between winter annual B. Our objectives are to contribute to a broader mechanistic tectorum and warm-season native plants) may increase feeding understanding of B. tectorum invasion dynamics in western pressure on natives if B. tectorum promotes grasshopper survival U.S. rangelands and provide useful information for restoration to adult stage. Researchers have noted grasshoppers eating green practitioners. To this end, native plants tested in our study were B. tectorum in the spring, and then switching to native plants as (1) species commonly utilized in restoration projects in western B. tectorum senesces (Mulkern et al. 1969, Fielding & Brusven U.S. rangelands or (2) species that have shown potential, in 1992; Beckstead et al. 2008). This switch may be linked to nutri- experimental trials, to compete well with B. tectorum and are ent levels, which decline sharply in B. tectorum as the growing therefore plausible restoration candidates (Table 1). As a test season progresses (Cook & Harris 1952; Rickard 1985). In one species, we used the widespread mixed-feeding Melanoplus study, nymphs of a mixed-feeding grasshopper species given a bivittatus (two-stripe grasshopper; Acrididae: ). 100% brome grass diet (B. inermis) all died before fourth instar Although M. bivittatus is not uniformly distributed throughout (MacFarlane & Thorsteinson 1980). This suggests that an abun- western U.S. rangelands, it is ranked as a serious economic dance of B. tectorum may not make up for an absence of other pest in this region (Henderson 1944; Dysart 1996), is favored

386 Restoration Ecology May 2017 Grasshopper–cheatgrass interactions by disturbance (Pfadt 1994), and has been targeted for control used for each trial and each individual was used only once. We efforts in several western states (Henderson 1944; Cranshaw & did not test individuals until at least 24 hours following ecdysis. Hammon 2008; USDA-APHIS 2013, 2015). Preference testing took place in a Percival® E-36HO growth chamber (Geneva Scientific, Fontana, WI, U.S.A.) ∘at 35 Cand 70% relative humidity to maintain leaf turgor. Grasshoppers Methods were starved 24–28 hours before each trial. For a given trial, each individual was presented with petri dishes containing sim- Experimental Insects ilar amounts of B. tectorum and native plant biomass. Since Melanoplus bivittatus (two-stripe grasshopper) (Orthoptera: grasshoppers may select food plants based on visual cues, leaves Acrididae), a widespread, mixed-feeding generalist, was used were cut into approximately 5- × 3-mm pieces. Although cut- in all experiments. Experiments were originally planned to ting plant leaves is generally assumed to increase and/or induce use a more common grasshopper species, M. sanguinipes changes in the volatile compounds released (which could affect (mixed-feeding generalist), to be collected in western Colorado preference), we chose to use cut material for the following (Rio Blanco county), but overall low grasshopper densities at the reasons: First, cutting the leaves allowed us to provide sim- site (0.66 ± 0.17 grasshoppers m−2) and scarcity of this species ilar amounts of biomass and volatile compounds from each led us to collect a similar grasshopper species, M. bivittatus, plant species. Second, grasshoppers may choose foods based near Fort Collins, CO, where grasshopper densities were much on visual cues, which cutting eliminates. Third, leaves were cut higher in 2011 and 2012 (J.L. Jonas 2011, personal observa- immediately before each trial and presented to insects for 15 tion). Additionally, M. bivittatus was the only species abundant minutes. Nearly all studies of herbivory-induced plant defenses enough in the region to harvest an adequate supply of eggs for indicate that defensive compounds are produced only after an use in these experiments. Because M. sanguinipes and M. bivit- initial time lag of hours or days between damage and response tatus are closely related species and have many similar traits (Karban & Baldwin 1997, Karban 2011). Finally, a study of a with regard to diet and host use (Mulkern 1967, 1980; Lambley closely related generalist species (M. sanguinipes) found that et al. 1972; Fielding & Brusven 1993), we decided that M. bivit- preference for cut leaf material was similar to those for intact tatus would be a reasonable surrogate for M. sanguinipes for leaves (Kang & Hopkins 2004). Plant material was clipped and testing our hypotheses regarding grasshopper herbivory effects weighed immediately before and after each trial. Trials lasted 15 on restoration plant species. minutes, the length of an average feeding bout for this species We collected adult M. bivittatus at Colorado State Univer- (Langford 1930). sity’s (CSU) Environmental Learning Center in the fall of 2011 After accounting for water loss and converting wet mass to and 2012. Grasshoppers were reared in the laboratory on a stan- dry mass, difference in dry plant mass before and after the trial dard diet and supplied with fresh egg-laying substrate (700-mL was recorded as the amount consumed (to the nearest 0.0001 g). plastic container filled with moist sterilized sand) every 3–5 We conducted paired t tests (TTEST procedure, SAS v9.3, SAS days until females ceased egg laying. Eggs were then main- Inc, Cary, NC, U.S.A.) to determine preference. A species was tained at room temperature for 6 weeks prior to being held in considered preferred if the amount consumed was significantly diapause at 4∘C (Fisher 1994) for 6 months. Hatchlings from greater than the amount consumed of the other species in the these eggs were used in all experiments to maintain genetics of trial (i.e. native consumed—B. tectorum consumed ≠ 0) at 𝛼 = field populations and minimize potential effects of laboratory 0.05. confinement on mate choice. Refer to Appendix S1, Supporting Information, for additional grasshopper-rearing details. Effect of B. tectorum and Grasshopper Herbivory on Native Species: Greenhouse Experiment Grasshopper Food Choice: Preference Trials We conducted two 2 × 2 factorial experiments (greenhouse We assessed grasshopper preferences for B. tectorum versus and field) to assess grasshopper herbivory (with and without) native plants using paired-choice preference trials. Bromus tec- on native plants growing in multispecies assemblages with and torum and 17 native plant species (Table 1) were established without B. tectorum present. Greenhouse mesocosms were con- in early spring (February 2012–April 2012) in a greenhouse. structed using SC-10 conetainers™ (164 mL; Stuewe & Sons, The 17 native plant species selected are commonly used or Medford, OR, U.S.A.) held in 98-tube trays. Each mesocosm may potentially be used in restoration of western U.S. range- included egg-laying substrate (as described above) in a corner lands and have the C3 photosynthetic pathway. Plants were of the tray, leaving space for up to 90 tubes. Each tube contained v grown in well-draining media (potting soil:sand, 2:1 /v) with asingleliveplant. no fertilization and no more than adequate water under a 16:8 Native plant species used in this experiment were a subset of day:night photoperiod with average day:night temperatures of those tested in preference trials (Table 1). Plants were grown in ∘ ∘ v 25.9 C:20.2 C. well-draining media (potting soil:sand, 2:1 /v) with no fertil- All insects were reared on the standard diet (Appendix S1) ization and no more than adequate water. In the western United until they were tested. We conducted tests at each of six life States, B. tectorum usually germinates in response to autumn stages (instars II through V, adult female, adult male) for each precipitation, but when fall moisture is limiting it can assume native plant versus B. tectorum pairing. Ten individuals were a spring-annual character and germinate after snowmelt; thus,

May 2017 Restoration Ecology 387 Grasshopper–cheatgrass interactions

Table 1. Plants used in experiments testing effects of Bromus tectorum and grasshoppers on native plants in western U.S. rangelands. Seventeen native species were tested in food preference trials, 15 in greenhouse mesocosms, 8 in field mesocosms. PLS, pure live seed.

Experiment Field Scientific Name Common Name Abbreviation Life Cycle Pref. Trial Greenhouse (PLS m−2)

Forbs Amsinckia menziesii Menzies’ fiddleneck AMME A Y Y— Coreopsis tinctoria Golden tickseed COTI A/B/P Y Y 375 Helianthus annuus Common sunflower HEAN A Y Y 345 Machaeranthera tanacetifolia Tanseyleaf tansyaster MATA A/B Y Y 375 Oenothera pallida Pale evening primrose OEPA B/P Y Y — Grasses Elymus elymoides Squirreltail ELEL P Y Y — Leymus cinereus Basin wild rye LECI P Y Y — Pascopyrum smithii Western wheatgrass PASM P Y Y — Poa secunda Sandburg bluegrass POSE P Y Y 210 Pseudoroegneria spicata Bluebunch wheatgrass PSSP P Y Y — Shrubs Artemisia tridentata Big sagebrush ARTR P Y Y 600 Artemisia frigida Prairie sagewort ARFR P Y Y 420 Atriplex canescens Fourwing saltbush ATCA P Y — — Chrysothamnus viscidiflorus Yellow rabbitbrush CHVI P Y Y 300 Eriogonum umbellatum Sulfur flower buckwheat ERUM P Y — Krascheninnikovia lanata Winterfat KRLA P Y Y 375 Purshia tridentata Antelope bitterbrush PUTR P Y Y —

recruitment can occur at any time from early fall through late Effect of B. tectorum and Grasshopper Herbivory on Native spring (Stewart & Hull 1949; Mack & Pyke 1983). To mimic Species: Field Experiment this phenotypic plasticity, we established half the B. tectorum A2× 2 factorial field experiment with treatments similar to plants in winter (December 2011–January 2012) and held them those described above was conducted in a grassland area north outdoors until the beginning of the experiment. The other half of Fort Collins, CO (13T 0491505 4506630, elevation 1525 m) of B. tectorum plants and all native plants were sown in the owned by CSU. Over the course of this experiment (22 June–19 spring (February–April 2012) to mimic natural plant phenol- August, 2013), the site received 10.67 mm of precipitation ogy. Mesocosms without B. tectorum (“Native”) contained six and average daily temperature ranged from 16.72 to 23.55∘C individuals each of 15 native plant species (90 plants total). (Campbell® Scientific CR1000 Weather Data Logger, Campbell Treatments with B. tectorum (“Invaded”) had three individ- Scientific, Inc., Logan Utah, USA.). uals of each native species (3 individuals × 15 native plant We created a surface disturbance by mowing, scraping, and species = 45 native plants) and 22 fall-germinated and 22 rototilling a 400-m2 area and then established forty 1.25- × spring-germinated B. tectorum plants (89 plants total). There 2-m plots separated by a 1-m buffer (Appendix S1). Plots were were 20 replicates of each plant community (native; invaded). seeded in late February 2013 with either a native only mix (3,000 Conetainer trays were placed in cages (0.65 m L × 0.35 m W pure live seed/m2, Table 1) or the native mix plus 1,000 pure × 1 m H) made of aluminum screening on a plastic frame and live seed/m2 of B. tectorum. Seeding rates were high because watered weekly. we wanted to ensure establishment of native species and create Grasshoppers (+GH) were stocked in 10 replicates of each a dense stand of seedlings of each species during the short-term plant community. Initially, eight first-instar nymphs were added experiment. There is emerging evidence that such high seeding to each +GH cage, and then adjusted to five individuals at rates may be needed to overcome propagule pressure from inva- week two and finally to two individuals at week four to mimic sives such as cheatgrass (Schantz et al. 2015). We also wanted natural grasshopper mortality. Grasshoppers were not added to use high seeding rates because we anticipated high mortality to the other 10 replicates of each plant community (−GH). of seedlings in the presence of herbivores. Each grasshopper × The experiment ran for 6 weeks (11 May–22 June, 2012). We B. tectorum treatment (native+GH, native–GH, invaded+GH, harvested aboveground biomass by clipping plants at the soil invaded–GH) was randomly assigned to 10 replicate plots. As surface. Biomass from each conetainer was bagged individually, mentioned previously, B. tectorum can behave as either a spring oven-dried at 65∘C to constant mass, and weighed. Plants with annual or a facultative winter annual; we therefore assumed no visible aboveground biomass or with dry biomass less than that establishing B. tectorum in spring was a realistic growing 0.0001 g were recorded as mortalities. See Appendix S1 for regime. However, sowing all or some B. tectorum seeds in plots additional details. the prior fall might have given different results.

388 Restoration Ecology May 2017 Grasshopper–cheatgrass interactions

Grasshopper cages were constructed of Lumite® (Lumite, 0.0375 a Native Inc. Alto, Georgia, USA) insect screening attached to a PVC a Invaded frame (0.5 m L × 0.5 m W × 1 m H). Two first-instar grasshop- 0.0300 )

per nymphs were placed in native+GH and invaded+GH meso- g ( cosms on 22 June, 2013. Grasshopper densities were increased ss a to five first-instar nymphs per cage (20 insects/m2)on26June, m 0.0225 b 2013. Grasshoppers were censused twice per month and main- b tained at uniform densities for the duration of the trial. Replace- 0.0150 e plant bio ment grasshoppers were reared in additional cages on separate v plots sown with the same seed combinations used in treatment Nati cages. Small mammals were excluded from the experimental 0.0075 area to prevent confounding effects of small mammal herbivory. After 8 weeks, the trial was ended (19 August, 2013). 0.0000 Plants were clipped at the soil surface and bagged by species. No grasshoppers Grasshoppers Biomass was oven-dried at 65∘C to constant mass prior to weighing. All species were weighed to the nearest 0.0001 g, Figure 1. Overall native plant biomass in greenhouse mesocosms except high-biomass species (Helianthus annuus and B. tecto- (g/individual) testing effects of grasshopper herbivory and Bromus rum) which were weighed to the nearest 0.01 g. See Appendix tectorum invasion. All-native mesocosms (“Native”) contained 15 native plant species commonly used in sagebrush steppe ecosystem restoration. S1 for additional details. Native-plus-B. tectorum mesocosms (“Invaded”) contained the same native species as all-native mesocosms, plus B. tectorum. Means with the same 𝛼 Statistical Analysis letter are not significantly different at = 0.05. Error bars are ± 1SE. To examine effects of herbivory and B. tectorum on plant biomass (greenhouse and field experiment) and mortality herbivory × B. tectorum interaction terms were not significant. (greenhouse experiment only), we used two-way analysis of Grasshoppers led to decreased biomass of most native restora- variance (GLIMMIX procedure, SAS v.9.3, SAS Inc) with tion species, but had no effect on biomass of Leymus cinereus, Tukey’s adjustment for multiple comparisons. Because the Oenothera pallida,andPascopyrum smithii (Table S2). Biomass number of individuals of each species differed among plant in Elymus elimoides and Machaeranthera tenacetifolia was assemblage treatments (native vs. invaded) at the outset of significantly greater when B. tectorum was present unless the greenhouse experiment, biomass values were scaled by grasshoppers were also present (Table S2); we speculate that this the number of individuals for each species or group in anal- facilitation was due to excess water captured by overhanging B. yses. Mortality data were arcsine square root transformed tectorum leaves. prior to analysis. To compare treatment effects on individual Grasshopper herbivory significantly increased mortality in species biomass, we used the nonparametric Kruskal–Wallis native restoration plants and B. tectorum (Fig. 2). Presence test (NPAR1WAY procedure) since transformations were not of B. tectorum had no effect on mortality in natives as a adequate to achieve normality. Where a significant difference in group and there was no herbivory × B. tectorum interaction. biomass was found, the simulation adjustment for least-squares Grasshoppers had no effect on mortality of Elymus elymoides, means in the GLIMMIX procedure was used to assess pairwise Leymus cinereus, Oenothera pallida, Pascopyrum smithii, and comparisons at 𝛼 = 0.05. Purshia tridentata (Table 2). Presence of B. tectorum signifi- cantly decreased grasshopper-induced mortality in Poa secunda (p = 0.002) (Table 2). Results Effect of B. tectorum and Grasshopper Herbivory on Native Grasshopper Food Choice: Preference Trials Plants: Field Experiment Grasshoppers showed no significant plant species preference in Helianthus annuus biomass was about 30 times greater than most (64%) comparisons (Table S1). Early-instar grasshoppers the biomass of all other native plants combined (Table S2). were more likely than adults to exhibit significant preference, Therefore, we analyzed H. annuus separately from all other more often for Bromus tectorum (20 of 31 times) than for native native species. The main effects of B. tectorum and grasshop- plants (11 of 31) (Table S1). Among adults, when preference pers on H. annuus biomass were not significant. However, the was detected, it was always for B. tectorum, but native species presence of both B. tectorum and grasshoppers significantly pairings in which B. tectorum preference was detected differed reduced H. annuus biomass compared to the three other treat- between males and females (Table S1). ments (Fig. 3A). For native plants (all species pooled except H. annuus), grasshoppers significantly decreased biomass Effect of B. tectorum and Grasshopper Herbivory on Native (Fig.3B).TherewasnoeffectofB. tectorum alone and no Species: Greenhouse Experiment significant grasshopper × B. tectorum interaction. Overall, grasshoppers significantly reduced total native restora- Both grasshopper and B. tectorum main effects were asso- tion plant biomass (Fig. 1). Bromus tectorum main effect and ciated with a significant reduction of Artemisia tridentata

May 2017 Restoration Ecology 389 Grasshopper–cheatgrass interactions

(A) (B) 50% 50% 45% b 45%

40%

y 40% y lit 35% lit a

a 35% ort 30% ort 30% m m 25% 25% 20% 20% Percent 15% Percent 15% 10% 10% a b 5% 5% a 0% 0% No Grasshoppers Grasshoppers No Grasshoppers Grasshoppers

Figure 2. Overall mortality in (A) native plants and (B) Bromus tectorum in greenhouse mesocosms testing effects of grasshopper herbivory and B. tectorum invasion. Means with the same letter are not significantly different at 𝛼 = 0.05. Error bars are ± 1SE.

Table 2. Percent mortality in native plants in greenhouse mesocosms testing effects of grasshopper herbivory and Bromus tectorum invasion. Plant biomass was collected from all-native (“Native”) versus native-plus-B. tectorum (“Invaded”) greenhouse mesocosms with and without grasshoppers. Plants with dry biomass <0.0001 g were recorded as mortalities. Species abbreviations are given in Table 1. Means with the same letter are not significantly different at 𝛼 = 0.05 for a given species.

No Grasshoppers Grasshoppers Species Native SE Invaded SE Native SE Invaded SE

AMME 10.00 4.44 a 6.67 4.44 a 66.67 6.80 b 56.67 11.17 b ARFR 0 0 a 0 0 a 51.85 12.25 b 46.67 12.37 b ARTR 5 2.55 a 6.67 4.44 a 83.33 5.56 b 76.67 7.11 b BRTE N/A 0.22 0.22 a N/A 2.67 0.93 b CHVI 11.67 8.26 a 0 0 a 69.68 5.96 b 68.97 8.90 b COTI 0 0 a 0 0 a 71.56 10.49 b 86.67 7.37 b ELEL 3.33 2.22 a 0 0 a 3.70 2.45 a 3.33 3.33 a HEAN 0 0 a 0 0 a 48.15 11.93 b 36.67 7.78 b KRLA 5.00 2.55 a 3.33 3.33 a 40.74 9.26 b 23.33 10.00 ab LECI 0 0 a 0 0 a 3.70 2.45 a 0 0 a OEPA 0 0 a 0 0 a 72.22 11.79 a 66.67 11.11 a MATA 0 0 a 0 0 a 0 0 b 0 0 b PASM 0 0 a 0 0 a 1.85 1.85 a 0 0 a POSE 0 0 a 0 0 a 57.41 11.15 b 16.67 5.56 a PSSP 1.67 1.67 a 0 0 a 14.81 3.34 b 10.00 5.09 ab PUTR 0 0 a 0 0 a 1.88 1.88 a 3.33 3.33 a

biomass, such that highest biomass occurred in plots with purposes, we have identified several native restoration species neither grasshoppers nor B. tectorum (Fig. 3C). Grasshop- that may be better performers where either B. tectorum or pers also significantly reduced Chrysothamnus viscidiflorus and mixed-feeding generalist grasshoppers are prevalent (most of Coreopsis tinctoria biomass; these species appeared almost western North America). However, results from our synthesized exclusively in plots lacking grasshoppers (Table S2). Grasshop- plant communities may not necessarily scale up to more com- pers had no effect on B. tectorum biomass (Table S2). plex field settings, where other invasive plant species (e.g. Sal- sola spp.) and multiple grasshopper species can interact across highly variable environments. Discussion We predicted native, generalist grasshoppers would prefer Our motivation for this research was to assist efforts to restore native restoration plants as food sources over exotic B. tectorum. western U.S. rangelands, where both grasshoppers and Bromus Our data did not support this hypothesis. First, grasshoppers tectorum are ubiquitous, by improving our understanding of showed no significant preference in most preference trial plant–insect relationships in the context of invasion. We found comparisons, indicating B. tectorum and native species were a generalist grasshopper species strongly impacts growth and equally acceptable foods. Second, where grasshoppers did survival of most restoration species, but our results provide show significant preference, it was more often for B. tectorum little support for the apparent competition hypothesis, since than natives. Nymphs exhibited significant preferences much these impacts were largely unaffected by B. tectorum pres- more often than adults, particularly for B. tectorum (20 of 31 ence in both greenhouse and field experiments. For restoration comparisons). Adults had wider feeding tolerances, especially

390 Restoration Ecology May 2017 Grasshopper–cheatgrass interactions

(A) Helianthus annuus (B) Native plants except H. annuus 10 Native 200 Native a 9 a Invaded 180 a Invaded 8 160 a

) 7

g a

) 140 ( g

( 6 120

b mass 5 mass 100 b b 80 nt bio 4 a nt bio Pl a 60 3 Pl 40 2 20 1 0 0 No Grasshoppers Grasshoppers No Grasshoppers Grasshoppers

(C) Artemisia tridentata 0.012 a Native 0.010 Invaded ) g 0.008 (

mass 0.006 nt bio a 0.004

Pl b b 0.002 b

0.000 No grasshoppers Grasshoppers

Figure 3. Biomass (g/0.25 m2 mesocosm) of (A) Helianthus annuus, (B) all native species except H. annuus,and(C)Artemisia tridentata from all-native field mesocosms (“Native”) compared to biomass in native-plus-B. tectorum mesocosms (“Invaded”) with and without grasshoppers. Note different y-axis scales. Means with the same letter are not significantly different at 𝛼 = 0.05. Error bars are ± 1SE. females, which showed significant preference in only 2 of 16 resistant to herbivory than forbs and shrubs because basal meri- comparisons. Nutritional content in the plants tested may have stems are less accessible to herbivores, which may explain why factored in this outcome. Grasshoppers were given a choice mortality was highest in forbs and shrubs, including the key- between green B. tectorum and seedling-stage natives; young stone species Artemisia tridentata (big sagebrush). Similarly, B. tectorum contains significantly higher nitrogen than many grasshoppers in field mesocosms significantly decreased native associated native species (Bishop et al. 2001; Beckstead et al. plant biomass overall, a result largely driven by effects on cer- 2008). Seasonal fluctuation in nutritional content may explain tain native species (particularly Helianthus annuus, which dom- why B. tectorum has been variously reportedly as either highly inated field plots and was highly preferred by grasshoppers). utilized by grasshoppers (this study; Beckstead & Augspurger It is also important to note that our laboratory studies differ 2004), or consumed at very low levels or not at all (Lambley from field situations in that cheatgrass typically completes its et al. 1972; Rogers & Uresk 1974; Sheldon & Rogers 1978). We life cycle early in the season whereas many native species may agree with others suggesting that life stage of both grasshop- continue activity and flower later (Beckstead et al. 2008). If pers and B. tectorum appears to factor in grasshopper feeding feeding on early season B. tectorum strengthens grasshopper choices (Fielding & Brusven 1992; Beckstead et al. 2008). populations, their impacts on native restoration plants could be However, even without significantly reducing biomass in all elevated. Grasshoppers in our greenhouse mesocosms signifi- native species individually, grasshoppers strongly affected over- cantly decreased B. tectorum biomass. Mortality in B. tectorum all native plant survival and growth. In greenhouse mesocosms, also increased significantly where grasshoppers were present grasshoppers doubled native species mortality as a whole, (but was approximately the same as background native plant which suggests it only takes a small amount of grasshopper her- mortality, i.e. mortality in natives with grasshoppers absent). bivory to produce negative impacts even for plants that are not This increase was very small compared to the impact on most highly preferred. Grasses (including B. tectorum) may be more natives. In the field, B. tectorum biomass was not significantly

May 2017 Restoration Ecology 391 Grasshopper–cheatgrass interactions affected when grasshoppers were present, whereas biomass Our intent was to determine whether native insect herbivores decreased significantly for native species (excluding H. annuus) may be contributing to B. tectorum dominance in western U.S. overall. rangelands through preferential feeding on native plants. We We expected grasshopper effects on native restoration found that a generalist grasshopper had substantial impacts on plants would change when B. tectorum was present. Despite natives, reducing biomass by approximately 50% and increas- Melanoplus bivittatus preference for B. tectorum, its presence ing mortality by more than 30% in both greenhouse and field. did not influence biomass or mortality in native plants inour Melanoplus bivittatus readily consume B. tectorum and in fact study. Other researchers have noted feeding damage on native prefer green B. tectorum to many native restoration plants, but plants increasing with increased invasive plant richness or not enough to offset their negative impacts on natives, and their density (Beckstead et al. 2008; Orrock & Witter 2010), so feeding did not increase B. tectorum mortality. Grasshoppers it is possible that the relative abundance of B. tectorum in may indeed be making native plants more vulnerable to B. tec- our experiments was not high enough to significantly alter torum competition, but they appear no more likely to consume grasshopper feeding pressure on native plants. In greenhouse native plants in moderately invaded than uninvaded contexts. mesocosms, grasshoppers significantly reduced biomass in Impacts of grasshopper herbivory may be especially critical at most native plants individually, but B. tectorum did not increase plant seedling stage, a factor in restoration applications because feeding pressure on natives and in fact relieved feeding pres- native seedling stage coincides with early instar stage for many sure on Poa secunda. This result is notable because of all grasshopper species. Early instar nymphs accounted for all the the native grass species tested, P. secunda is most similar in biomass reduction in the greenhouse and most of the feeding phenology to and has demonstrated some ability to compete in field mesocosms, where they inflicted severe damage despite with B. tectorum (Monsen 1992; Goergen et al. 2011). In field the huge amount of biomass available. Additional research is mesocosms, B. tectorum had little effect on natives (singly or as needed to determine the effects of cheatgrass on grasshopper a group, excluding H. annuus) relative to that of grasshoppers. populations. If grasshoppers are positively influenced by the However, the keystone shrub A. tridentata showed significantly presence of early-season cheatgrass, their effects on restoration reduced biomass where either grasshoppers or B. tectorum were species emerging or remaining active after cheatgrass senes- present, suggesting both factors have the potential to impact cence may be augmented. Over the course of development and A. tridentata. Heavy feeding by multiple grasshopper species with exposure to herbivory, plants may become more or less on A. tridentata has been documented previously (Sheldon & tolerant of or resistant to herbivory which may incur various Rogers 1978; Shiojiri & Karban 2008), including severe effects types of costs (Rosenthal & Kotanen 1994; Strauss & Agrawal on A. tridentata fecundity (Takahashi & Huntly 2010). 1999; Strauss et al. 2002). Such differences in tolerance and One result from our study supports the apparent competi- resistance among plant species and life stages may alter impacts tion hypothesis. Grasshoppers did not significantly decrease of insect herbivores as plant communities mature. H. annuus biomass except where B. tectorum was present. This Our study should be regarded as preliminary evidence of outcome is striking given H. annuus biomass in field mesocosms the potential effects of grasshoppers on restoration outcomes. was 30 times greater than biomass of all other native species Further testing is needed to demonstrate whether these results combined, likely related to the high seeding rate for this species. are generally applicable in restoration settings. Our results For other natives, direct competition with B. tectorum and/or have some generalizable implications for management and intolerance of herbivory may be more important factors limiting restoration of western U.S. rangelands. Several natives showed restoration success and sustaining B. tectorum dominance. potential to be useful restoration species where mixed-feeding In sites dominated by exotic annuals within the western grasshoppers are prevalent. Native grasses were strong perform- United States, grasshopper diversity is typically very low (1–3 ers, likely due to location of apical meristems at or below the species) and Melanoplus sanguinipes tends to be the dominant soil surface providing some protection from herbivory (Joern species (Parmenter et al. 1991; Fielding & Brusven 1993, 1994). 1989). Grasshoppers did not increase mortality in greenhouse We used M. bivittatus to assess potential effects of grasshop- mesososms for three of the five native grass species studied per herbivory in disturbed sites facing invasion by cheatgrass (Elymus elymoides, Leymus cinereus, Pascopyrum smithii). due to low M. sanguinipes abundance during the years of these A fourth grass, P. secunda, showed significantly decreased experiments. Despite similarities in the feeding ecology of M. mortality resulting from grasshoppers when B. tectorum was sanguinipes and M. bivittatus (Mulkern 1967, 1980; Lambley present. All instars exhibited significant preference for B. et al. 1972; Fielding & Brusven 1993), outcomes would likely tectorum compared to P. secunda in preference trials and differ with M. sanguinipes or a combination of grass-, forb-, grasshoppers did not reduce P. secunda biomass in the field, a and mixed-feeders more typical of intact western U.S. range- finding consistent with results from other studies (Beckstead lands. For example, M. sanguinipes feeding can be slightly et al. 2008; Goergen et al. 2011). more biased toward forbs over grasses and diet breadth and The shrubs Chrysothamnus viscidiflorus, Purshia tridentata, nutritional niches can vary from that of M. bivittatus (Mulk- and Krascheninnikovia lanata are valuable forage plants for ern et al. 1969; Lambley et al. 1972; Behmer & Joern 2008), wildlife and livestock in western U.S. rangelands (Vallentine so negative impacts on native forbs might be expected to be 1989). Our results suggest seedlings of C. viscidiflorus are more pronounced with M. sanguinipes feeding than found in our sensitive to grasshopper herbivory. Although it tended to be studies. less preferred than B. tectorum, C. visvidiflorus had 81% lower

392 Restoration Ecology May 2017 Grasshopper–cheatgrass interactions biomass and 10 times higher mortality with grasshoppers than and B. tectorum was among them. Our results suggest gener- without in the greenhouse experiment. Results from the field alist grasshoppers have the capacity to influence restoration experiment were similar with C. viscidiflorus appearing in 75% success, especially during the seedling establishment phase. of the plots lacking grasshoppers but absent from plots with More detailed field studies regarding grasshopper impacts in grasshoppers. Sheldon and Rogers (1978) observed heavy use of disturbed western U.S. rangelands are needed to help promote C. viscidiflorus by several grasshopper species in mature sage- successful restoration of these ecosystems. brush steppe. Krascheninnikovia lanata was highly preferred to B. tectorum in preference trials, and mortality in greenhouse Acknowledgments mesocosms significantly increased when grasshoppers were This research was funded by an endowment from Shell Oil present. However, in the field K. lanata occurred with equal Company. We are grateful for the help of numerous student frequency and biomass across all treatments possibly owing employees in the Restoration Ecology Lab at CSU for help with to conditions that promoted regrowth following herbivory. field, greenhouse, and lab work. We also kindly thank Tony The shrub appearing to be most resistant to herbivory in these Joern and Angela Laws (Kansas State University) for use of experiments was P. tridentata. This species was less preferred field cages. than B. tectorum in preference trials; mortality was not affected and biomass only decreased 18% with grasshoppers in the greenhouse. Although not included in the field experiment seed LITERATURE CITED mix, this species should be further evaluated for performance Beckstead J, Augspurger CK (2004) An experimental test of resistance to against grasshoppers in restoration. cheatgrass invasion: limiting resources at different life stages. Biological Native annual forbs were tested with the expectation that Invasions 6:417–432 Beckstead J, Meyer SE, Augsperger CK (2008) The indirect effects of cheatgrass their rapid growth rates and tolerance of postdisturbance con- invasion: grasshopper herbivory on native grasses determined by neigh- ditions could make them better competitors with B. tectorum boring cheatgrass. In: Kitchen SG, Pendleton RL, Monaco TA, Vernon J than perennial forbs in the initial stages of restoration. Our (eds) Shrublands under fire: disturbance and recovery in a changing world. field results supported this prediction. Presence of B. tectorum USDA Forest Service Proceedings RMRS-P-52, Fort Collins, Colorado did not reduce biomass in any of the native forbs we tested. Behmer ST, Joern A (2008) Coexisting generalist herbivores occupy unique However, grasshoppers strongly preferred certain forbs over nutritional feeding niches. Proceedings of the National Academy of Sci- B. tectorum. Grasshoppers significantly reduced H. annuus ences 105:1977–1982 Belovsky GE, Slade JB (2000) Insect herbivory accelerates nutrient cycling biomass when B. tectorum was present. Coreopsis tincto- and increases plant production. Proceedings of the National Academy of ria was also preferred and negatively affected by herbivory Sciences 97:14412–14417 appearing in only one plot where grasshoppers were present Bishop CJ, Garton EO, Unsworth JW (2001) Bitterbrush and cheatgrass quality (vs. all except one plot where grasshoppers were absent). The on three southwest Idaho winter ranges. Journal of Range Management best-performing forb in the field was Machaeranthera tenaceti- 54:595–602 folia, which appeared with equal frequency with and without Blank RR, Morgan T (2010) Bromus tectorum (cheatgrass): monitoring an B. tectorum or grasshoppers, showing no difference in biomass invasion for 10 years. Soil Science Society of America. Paper No. 241-1. Branson DH, Joern A, Sword GA (2006) Sustainable management of insect her- across treatments. The resistance of M. tenacetifolia to both bivores in grassland ecosystems: new perspectives in grasshopper control. grasshopper herbivory and B. tectorum competition indicates BioScience 56:743–755 the species could be a valuable forb in restoration seed mixes. 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Supporting Information Table S2. Average biomass remaining in greenhouse (g/individual) and field meso- 2 The following information may be found in the online version of this article: cosms (g/0.25 m mesocosm), in studies testing effects of grasshopper herbivory in a context of Bromus tectorum invasion. Appendix S1. Complete materials and methods Table S1. Results from t tests of differences between Bromus tectorum and native plant consumption in paired-choice feeding preference trials.

Coordinating Editor: Stephen Murphy Received: 8 June, 2016; First decision: 24 July, 2016; Revised: 29 July, 2016; Accepted: 29 July, 2016; First published online: 9 September, 2016

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