Impacts of Treatment

The treatment categories we analyzed were Biocontrol; Fertilizer; Fire; Fire with Additional Treatments; Grazing; Herbicide Alone; Herbicide with Additional Treatments; Herbicide with Manual Removal Follow-Up; Manual Removal Alone or with Additional Treatments; and Seeding (Table 1). If a series of treatments occurred in a single study, the study was categorized by the first treatment to occur (e.g., fire and herbicide application would be categorized as Fire with Additional Treatments, but herbicide and then fire application would be categorized as Herbicide with Additional Treatments). Biocontrol included the application of insects and fungi. Fertilizer included the application of nitrogen and phosphorous. Fire included both prescribed burns and (accidental) wildfire. Fire with Additional Treatments included prescribed burns or wildfire followed by seeding, manual removal, livestock grazing, or herbicide treatment. Grazing was by cattle or manual defoliation by clipping. Herbicide Alone included several herbicide types (Table 2). Herbicide with Additional Treatments included herbicide followed by seeding, transplanting, mulching, and/or irrigating seeded or transplanted plants. Manual Removal was done in all instances by pulling the plant out using tools such as digging bars and picks. Manual Removal Alone and Manual Removal with Additional Treatments were lumped for the chi-square test due to low sample size and included manual removal followed by thatching (piling biomass) or fertilization. Seeding included different timing of seeding as well as seeding following shrub removal. Treatment details including timing, frequency, and description for each study are included in the Supplementary Table S1.

Fire significantly increased the abundance of P. ciliare and significantly decreased the abundance of native species (Table 1; Figure 1). Fire with Additional Treatments significantly reduced the abundance of P. ciliare (Table 1; Figure 1). Herbicide Alone, Herbicide with Additional Treatments, and Herbicide with Manual Removal Follow-Up significantly reduced P. ciliare abundance (Table 1; Figure 1). Herbicide with Additional Treatments significantly enhanced the abundance of native species (Table 1; Figure 1). Studies conducted in wildlands invaded with P. ciliare included all treatment categories except Biocontrol; studies conducted in pastures intentionally planted with P. ciliare included the treatment categories Biocontrol, Herbicide with Additional Treatments, Herbicide Alone, Fire with Additional Treatments, Grazing, Fertilizer, and Fire (Figure 2).

Figure 1. Mean ± SE of Pennisetum ciliare treatment efficacy based on 229 studies, each of which have been assigned “reduces” (−1), “neutral” (0), or “increases” (1) for how the treatment category impacts the abundance of P. ciliare (shown in gold) and native species (shown in grey). Mean abundances are shown by the vertical black bars; SE values are shown by the surrounding color. Treatment means to the right of zero (the blue dotted line) tend to increase the abundance of the indicated species; treatment means to the left of zero tend of decrease the abundance of the indicated species. Missing SE bars (i.e., “Herbicide with Manual Removal Follow-Up” and “Manual Removal Alone”) indicate no variation in response categories. The Biocontrol treatment category had no studies on native species.

Figure 2. Mean ± SE of Pennisetum ciliare treatment impacts the abundance of P. ciliare (shown in gold) and native species (shown in grey), separated by (A) studies conducted in wildlands invaded by P. ciliare (N = 88) and (B) studies conducted in pastures intentionally planted with P. ciliare (N = 61). Mean abundances are shown by the vertical black bars; SE values are shown by the colored bar. Treatment means to the right of zero (the blue dotted line) tend to increase the abundance of the indicated species; treatment means to the left of zero tend of reduce the abundance of the indicated species. Missing SE bars (i.e., “Herbicide with Additional Treatments” in Planted Pastures) indicate no variation in response categories. Only treatment categories with three or more studies are shown in order to show a measure of spread (Supplementary Table S5).

Impacts of Herbicides

Herbicide Alone was the most frequently studied treatment (Table 1). There were 10 unique sources on the use of herbicide treatment alone containing 239 studies when all herbicide rates studied were incorporated (Figure 3; Supplementary Table S1). Pennisetum ciliare life stage at which the herbicides were applied varied and included: pre-emergent herbicide application in a greenhouse setting (n = 32), seedling/immature herbicide application in a greenhouse setting (less than 150 d old; n = 131), and herbicide application aimed at mature and immature plants in a field setting (n = 76). Average herbicide application rate was 1.5 kg ha⁻¹. Data were collected an average of 7 mo after the last herbicide application. In 228 of the 239 studies, herbicide was applied once. Supplementary Table S4 details application methods, application rates, timing, system, and herbicide brand used.

Figure 3. Mean ± SE of impact of herbicide active ingredients on Pennisetum ciliare abundance. Figure shows herbicides with sample sizes >4. Each study was assigned “reduces” (−1), “neutral” (0), or “increases” (1) for how the herbicide impacts P. ciliare abundance. Mean herbicide impacts closer to 0 (blue dotted line) indicate the impact was neutral and thus the herbicide is ineffective at treating P. ciliare; mean impacts closer to −1 indicate the herbicide is effective at reducing the abundance of P. ciliare. Sample size was inadequate to test the impact of herbicides on native species.

Active ingredients of herbicides used in the herbicide treatment category were: 2,4,5-T (n = 20), 2,4-D (n = 21), 3,6-DPA (n = 20), clethodim (n = 2), dicamba (n = 21), dimethenamid-P (n = 4), fluazifop (n = 7), glyphosate (n = 26), hexazinone (n = 20), imazapic (n = 3), imazapyr (n = 6), imazethapyr (n = 4), nicosulfuron (n = 2), picloram (n = 22), quizalofop-ethyl (n = 4), tebuthiuron (n = 4), triclopyr (n = 20), and some combination of herbicide active ingredients (n = 13) (Table 2). Of the eleven active ingredients that had an adequate sample size to test, three active ingredients significantly reduced P. ciliare (glyphosate, hexazinone, and imazapyr) and three active ingredients were significantly neutral (no effects) (Table 2; Figure 3).

Land Management Implications

This review highlights the value of integrating multiple P. ciliare control treatments for greater efficacy. All treatments performed in isolation (e.g., Herbicide Alone) were less effective than those applied in tandem with additional treatments (Figure 1). The utility of an integrated pest management approach in which several mutually supportive treatments are used to target invasives has been shown to be particularly effective in many studies (Davies and Sheley Reference Davies and Sheley2011; DiTomaso Reference DiTomaso2000; James et al. Reference James, Gornish, DiTomaso, Davy, Doran, Becchetti, Lile, Brownsey and Laca2015). Treatments performed in isolation often occur as a single treatment over a time period, whereas multiple treatment types across time allow a manager to eradicate several generations and different cohorts with multiple treatments (e.g., fire destroys all adult individuals but follow-up manual removal could be used to eradicate new seedlings coming up over the next 2 years; Gornish et al. Reference Gornish, Case, Valle, Bean and Moore-O’Leary2018). We found that that fire followed by additional treatments such as follow-up herbicide application, manual removal, or seeding resulted in much greater P. ciliare control while enhancing native species establishment compared with fire without additional restoration (Figure 1; Daehler and Goergen Reference Daehler and Goergen2005; Mayeux and Hamilton Reference Mayeux and Hamilton1983; Rutman and Dickson Reference Rutman, Dickson and Tellman2002). Additionally, herbicide treatment followed by seeding or transplanting native plants has been shown to result in both highly effective P. ciliare treatment and successfully reestablished natives (Figure 1; e.g., Daehler and Goergen Reference Daehler and Goergen2005; Dixon et al. Reference Dixon, Dixon and Barrett2002; James et al. Reference James, Gornish, DiTomaso, Davy, Doran, Becchetti, Lile, Brownsey and Laca2015; Tjelmeland et al. Reference Tjelmeland, Fulbright and Lloyd-Reilley2008).

Pennisetum ciliare clearly responds positively to disturbances such as fire, grazing, and soil movement (Figure 1; Brenner and Kanda Reference Brenner and Kanda2013; Burquez-Montijo et al. Reference Burquez-Montijo, Miller, Martinez-Yrizar and B2002; Butler and Fairfax Reference Butler and Fairfax2003; De La Barrera Reference De La Barrera2008; Fensham et al. Reference Fensham, Donald and Dwyer2013; Jackson Reference Jackson2004; Mayeux and Hamilton Reference Mayeux and Hamilton1983; McIvor Reference McIvor2003; Miller et al. Reference Miller, Friedel, Adam and Chewings2010; Van Devender and Dimmitt Reference Van Devender and Dimmitt2006). Despite this, manual removal through digging and manually pulling out P. ciliare remains a common treatment method in some regions. For example, in the Sonoran Desert of North America, volunteer groups in the Tucson metropolitan area report dedicating more than 7,000 h annually to P. ciliare eradication efforts within parks and government land, primarily employing manual removal (K Franklin, personal communication, 2017). To address unintended consequences following land management that disturbs the ground, such as manual removal, fire, or development, practitioners could include active restoration in their control tool kit. Our review indicates that disturbance could present an opportunity to enhance control by including additional management methods such as seeding with a suite of native species to suppress the expected regrowth of P. ciliare. Sites can be protected from invasion or reinvasion by selecting plant species to use for revegetation that will competitively exclude the invasives by filling all resource niches (e.g., how and when water is used by a plant). We therefore recommend selecting candidate restoration species that have similar functional traits (e.g., root depth or establishment timing as a proxy for plant access to water resources) as the invader as well as the use of a seed mix that has a wide diversity of functional traits (Funk et al. Reference Funk, Cleland, Suding and Zavaleta2008).

Daehler and Goergen (Reference Daehler and Goergen2005) found the most effective P. ciliare treatment combination (measured 4 yr after the final treatment) to be burning of P. ciliare monocultures followed first by herbicide or manual removal of resprouts and then by seeding native species with supplemental irrigation. This suite of strategies suggests that (1) P. ciliare requires multiple iterations of control, because its seeds remain viable in the soil for several years (Winkworth Reference Winkworth1971); and (2) when working with a P. ciliare monoculture, where the source of native seeds is limited, seeding is highly effective, because it allows the site to continue to provide ecosystem services (rather than bare ground) and helps to competitively exclude P. ciliare reestablishment. These conclusions are reflected in the literature: Pyke et al. (Reference Pyke, Wirth and Beyers2013) conducted a meta-analysis on the impacts of seeding after fire on rangelands in the western United States and found that seeding (particularly with species that tend to establish at high rates) reduced the abundance of invasive species.

The efficacy of invasive species treatment will depend on the extent to which the site is invaded and the time since invasion (Falk et al. Reference Falk, Palmer and Zedler2006; Zavaleta et al. Reference Zavaleta, Hobbs and Mooney2001). In sites with a comparatively intact suite of native desert scrub species, Abella et al. (Reference Abella, Chiquoine and Backer2013) found there to be adequate native seed source remaining the soil seedbank for natural revegetation, and Woods et al. (Reference Woods, Fehmi and Backer2012) found that active revegetation after herbicide treatment yielded no effect on P. ciliare control. This suggests that sites with low levels of P. ciliare invasion may not require active revegetation after treatment. Alternatively, a highly invaded site with few remnant native species may require active revegetation due to inadequate native seed sources, altered soil nutrients, and an altered water budget inhibiting natural revegetation of natives (Castellanos et al. Reference Castellanos, Celaya-Michel, Rodríguez and Wilcox2016; Eilts and Huxman Reference Eilts and Huxman2013; Fensham et al. Reference Fensham, Donald and Dwyer2013; Hinojo-Hinojo et al. Reference Hinojo-Hinojo, Castellanos, Rodriguez, Delgado-Balbuena, Romo-León, Celaya-Michel and Huxman2016). Although active restoration appears to be critical for effective P. ciliare control in many cases, it is not a silver bullet. Often, planted or seeded species do not persist in the long term (e.g., Drayton and Primack Reference Drayton and Primack2012), and this technique will likely need follow-up management for long-term success. Further, ongoing land-use and grazing management need to be considered at any treatment site. Lyons et al. (Reference Lyons, Maldonado-Leal and Owen2013) found that managed, moderate grazing allows native species to return after P. ciliare treatment, but that overgrazing results in depletion of native grasses and forbs.

Although most of the invasive species control literature has focused on the efficacy of management for target weeds, impacts of treatment on native plants and ecosystem processes (e.g., soil stability, soil microbes, biogeochemical cycles) need to be addressed to facilitate long-term eradication and continued ecosystem services (Flory and Clay Reference Flory and Clay2009; Funk et al. Reference Funk, Matzek, Bernhardt and Johnson2013; Zabaloy et al. Reference Zabaloy, Garland and Gomez2008; Zavaleta et al. Reference Zavaleta, Hobbs and Mooney2001). The effect of a treatment on the native plant community is important, because it can drive the maintenance of ecosystem services such as soil stability and food web interactions (Diaz et al. Reference Díaz, Purvis, Cornelissen, Mace, Donoghue, Ewers, Jordano and Pearse2013, Zavaleta et al. Reference Zavaleta, Hobbs and Mooney2001) and it can also determine the ability of the site to resist reinvasion (Funk et al. Reference Funk, Cleland, Suding and Zavaleta2008). Invasive species treatment methods such as herbicide application have been shown to negatively impact native plant communities, resulting in available physical space and resources that can intensify the original invasion (Crone et al. Reference Crone, Marler and Pearson2009; Rinella et al. Reference Rinella, Maxwell, Fay, Weaver and Sheley2009; Sheley et al. Reference Sheley, Mangold and Anderson2006). Rinella et al. (Reference Rinella, Maxwell, Fay, Weaver and Sheley2009) suggest that herbicide application may be appropriate in situations with either small patches of invasives or monocultures of invasives, but when substantial populations of native species are interspersed among the invasive species, herbicide application may cause more harm than good. In our review, long- and short-term effects of herbicide treatments on native species were almost completely ignored (63/249 studies reported treatment impacts on native species, only 7 herbicide studies reported the impacts on native species; Supplementary Table S1). Lack of reported information on the impacts of herbicide treatments on native plant communities is common in the invasive species research literature (Kettenring and Adams Reference Kettenring and Adams2011).

This review highlights discrepancies between research priorities in the scientific community and what land managers and government agencies are experiencing on the ground, a common theme in invasive species research and management (Downey et al. Reference Downey, Peterson and Franz2017; Kettenring and Adams Reference Kettenring and Adams2011; Matzek et al. Reference Matzek, Covino, Funk and Saunders2014; Waldén and Lindborg Reference Waldén and Lindborg2018). Government and land manager reports were more likely to value the use of multiple strategies in tandem and to emphasize the need for repetitive and successive treatment seasons for successful eradication (Siegel et al. Reference Siegel, Malusa and Loudbeau2017; Hunter Reference Hunter2012; Scheuring Reference Scheuring2016; USDA Forest Service 2014; Tu et al. Reference Tu, Randall and Rice2002; Tix Reference Tix2000). Conversely, we found that most studies in the literature only conducted 1 to 2 treatments and that the average period reported between treatment and measurement was 15 mo, which is inadequate to measure long-term success of P. ciliare management. Many of the herbicide treatment studies were greenhouse based or were conducted in a planted P. ciliare field where measurements occurred 1 to 3 mo after herbicide application. While this approach demonstrates the effectiveness of herbicides’ active ingredients, it fails to incorporate the complexities land managers deal with, such as access to treatment sites and unintended effects on native species. An issue that remains unaddressed is that P. ciliare continues to be sold and planted as a rangeland improvement grass in Mexico, the United States, and Australia, providing a continued source of invasion (Burquez-Montijo et al. Reference Burquez-Montijo, Miller, Martinez-Yrizar and B2002; Franklin et al. Reference Franklin, Lyons, Nagler, Lampkin, Glenn, Molina-Freaner, Markow and Huete2006; Friedel et al. Reference Friedel, Grice, Marshall and Van Klinken2011; Marshall et al. Reference Marshall, Lewis and Ostendorf2012). Grechi et al. (Reference Grechi, Chadès, Buckley, Friedel, Grice, Possingham, Van Klinken and Martin2014) created a decision framework to help manage P. ciliare in areas where it is considered an economically valuable forage species and suggested that managers may have to prioritize either forage production or biodiversity to make decisions about treatment.

Treatment Differences among Land-Use Categories

Although traditional reviews and meta-analyses couple all ecosystem types to synthesize overarching patterns (Gurevitch et al. Reference Gurevitch, Curtis and Jones2001), it is important to recognize that P. ciliare treatments conducted in different ecosystems and with different land-use histories will yield different results. For example, planted P. ciliare pastures will have historic and ongoing disturbances that fundamentally alter the conditions, including differences in native seedbank, native existing vegetation, soil/landscape conditions, grazing pressures, and the P. ciliare seed input. To help managers with decision making, we used the results of our analysis to examine differences in treatment impacts found in studies conducted in pastures intentionally planted with P. ciliare versus wildlands invaded by P. ciliare (Figure 3). Where there was overlap in treatments among land-use categories, many of the treatments resulted in similar impacts, though of different magnitude. One interesting exception is that Fire with Additional Treatments was more successful for treating P. ciliare–invaded systems than P. ciliare–planted pastures (Figure 3; Supplementary Table S5). Additional treatments for the invaded systems included seeding, follow-up herbicide application, and follow-up manual removal. Additional treatments for the planted pastures included grazing and follow-up herbicide. The differences between the two land-use categories could be more a function of different priorities in what is being studied/observed rather than differences due to the treatments themselves. Details on ecosystem type (e.g., desert scrub vs. semiarid grassland vs. woodland; annual precipitation) and specific treatments (e.g., number and timing of treatments) for each are found in Supplementary Table S1.

Competition Mechanisms and Restoration Opportunities

Our review found that the strategies most often studied by the scientific community and employed by land mangers tend to be top-down in nature (e.g., herbicide and manual removal; Table 1). To design an effective treatment strategy that is bottom-up in tandem with a top-down approach (e.g., seeding with native species after treatment), we should understand the traits and adaptations that make P. ciliare a successful invader (Stevens and Falk Reference Stevens and Falk2009). To address this need, we explored the literature for ways in which P. ciliare alters its environment to give itself a competitive advantage and suppress native species. We created a conceptual model to display the mechanisms that give P. ciliare a competitive advantage and suggest restoration opportunities based on P. ciliare traits and our treatment efficacy review results (Figure 4). Evidence (Supplementary Table S2) shows that P. ciliare impacts its environment by altering water availability, nutrient cycling, and disturbance regimes, creating a self-reinforcing feedback loop of invasion (Figure 4). Pennisetum ciliare is an example of a species that can tolerate low water conditions through water-conservation strategies better than native species, a trend that has been noted for invasive species in inherently low-resource environments such as drylands (Funk and Vitousek Reference Funk and Vitousek2007). For example, P. ciliare has lower water requirements for germination than native species (Ward et al. Reference Ward, Smith and McClaran2006), its growth responds to smaller precipitation events when native species remain dormant, reduces available soil water content, and causes dehydration symptoms in neighboring vegetation (Castellanos et al. Reference Castellanos, Celaya-Michel, Rodríguez and Wilcox2016; Eilts and Huxman Reference Eilts and Huxman2013; Stevens and Fehmi Reference Stevens and Fehmi2009), and it will establish into native vegetation that is weakened by drought (Cavaye Reference Cavaye1991), culminating in a self-reinforcing feedback loop of invasion through the mechanisms and traits of how P. ciliare uses water resources (Figure 4).

Figure 4. Conceptual model of Pennisetum ciliare traits and adaptations that result in altered water availability (blue), nutrient cycling (green), and disturbance regimes (orange), enabling it to outcompete native species. Opportunities for intervention and restoration are directly tied to the ways in which P. ciliare creates self-reinforcing feedback loops and inhibits the establishment and survival of native species. The information presented in this conceptual model is based on a literature review of how P. ciliare impacts its environment. A table of sources used to generate the material presented in this conceptual model can be found in Supplementary Table S4.

This conceptual model is intended to be used by land managers to asses potential restoration opportunities based on the traits and adaptations of P. ciliare. Due to the ways in which P. ciliare inhibits native species, land managers may be more successful intervening with active restoration options to halt P. ciliare’s feedback loop of invasion and initiate permanent eradication and successful regeneration of native species. The ways in which P. ciliare impacts water availability, nutrient cycling, and disturbance could play out in management decisions through selection of restoration candidate species that are competitive with P. ciliare given the altered environmental factors. Traits of candidate restoration species that might prove to be competitive with P. ciliare include: species that establish in low water conditions (Ward et al. Reference Ward, Smith and McClaran2006), species that establish quickly after disturbance (Miller et al. Reference Miller, Friedel, Adam and Chewings2010; Tinoco-Ojanguren et al. Reference Tinoco-Ojanguren, Reyes-Ortega, Sánchez-Coronado, Molina-Freaner and Orozco-Segovia2016), species that can tolerate periods of drought (Cavaye Reference Cavaye1991; Eilts and Huxman Reference Eilts and Huxman2013; Halvorson Reference Halvorson2003), fire-tolerant species (Burquez-Montijo et al. Reference Burquez-Montijo, Miller, Martinez-Yrizar and B2002; De La Barrera Reference De La Barrera2008; McIvor Reference McIvor2003), and species that tolerate P. ciliare allelopathy (Fulbright and Fulbright Reference Fulbright and Fulbright1990) (Figure 3). This line of research could prove fruitful.

Future Directions

Considering that most of the studies in our review did not include a monitoring time that is ecologically relevant (average of 15 mo from last treatment), we see a need for extended studies that can show the long-term impacts of treatments on P. ciliare populations, native plant communities, and the above- and belowground ecosystems. Further, most studies in our review were examining treatments applied only once or twice, whereas the gray literature from government agencies and land managers emphasizes the need to apply multiple iterations of treatments over several years for P. ciliare control (e.g., Siegel et al. Reference Siegel, Malusa and Loudbeau2017; Hunter Reference Hunter2012; Scheuring Reference Scheuring2016; USDA Forest Service 2014; Tu et al. Reference Tu, Randall and Rice2002; Tix Reference Tix2000). This suggests the need for rigorous research that follows manager-driven treatment protocols wherein years of iterations of treatment occur.

Glaringly absent from both the scientific literature and land manager reports are the impacts of various treatments on native species (for herbicide treatments in particular). The effect the treatment has on the native species must be considered when planning an effective treatment protocol (Flory and Clay Reference Flory and Clay2009). Monitoring the change in invasive species populations and the results of treatment is critical to an effective invasive species management program (Kettenring and Adams Reference Kettenring and Adams2011; Lyons et al. Reference Lyons, Runge, Laskowski and Kendall2008; Maxwell et al. Reference Maxwell, Lehnhoff and Rew2009). When the site is highly invaded and few native species remain, reseeding the treated site with species that use space and resource niches typically occupied by P. ciliare may help keep the site free of P. ciliare without copious iterations of upkeep (Funk et al. Reference Funk, Cleland, Suding and Zavaleta2008). Research on candidate restoration species that can protect a site from invasion or reinvasion of P. ciliare as well as species that are fire resistant or regenerate well after fire may be a useful line of research.

Finally, we wish to acknowledge that P. ciliare treatment occurs within the context of the social, economic, and political environments, which vary over time and by geographic region. This is beyond the scope of our review; however, there are multiple excellent resources in the literature that discuss the human dimension and social challenges around controlling P. ciliare (please see: Brenner Reference Brenner2010, Reference Brenner2011; Brenner and Franklin Reference Brenner and Franklin2017; Franklin et al. Reference Franklin, Lyons, Nagler, Lampkin, Glenn, Molina-Freaner, Markow and Huete2006; Friedel et al. Reference Friedel, Grice, Marshall and Van Klinken2011; Grechi et al. Reference Grechi, Chadès, Buckley, Friedel, Grice, Possingham, Van Klinken and Martin2014; Lien and Baldwin Reference Lien and Baldwin2019; Marshall et al. Reference Marshall, Friedel, van Klinken and Grice2011, Reference Marshall, Lewis and Ostendorf2012). Additionally, we feel that a fruitful line of study would be to employ the tools of social science by distributing a survey eliciting land managers’ attitudes about P. ciliare introduction, knowledge of treatment options, willingness to pay for treatment, treatment priorities, and so on, and comparing the responses by region.