A significant challenge of global change is the human-mediated movement of pasture grasses and their subsequent impact on ecosystem processes when they become invasive. We must understand invasive grass ecology and their natural enemies in native and introduced ranges to mitigate these impacts. Guinea grass (Megathyrsus maximus) is a pantropically introduced pasture grass that escapes intended areas and invades native ecosystems – threatening biodiversity and ecosystem function. The success of invasive plants has often been attributed to ecological release from stressors, including natural enemies and resource availability. Our objective was to assess Guinea grass functional traits across three different habitat types in native and invaded ranges by documenting ungulate and arthropod abundance, diversity, and feeding guilds. Guinea grass functional traits were assessed in three habitat types: grassland, riparian, and woody thickets around nitrogen-fixing Prosopis glandulosa in its introduced range in Texas, USA, and Senegalia mellifera in its native range in Kenya. We characterized Guinea grass functional traits by measuring plant height, cover, biomass, root-to-shoot ratios, and reproductive traits. We then examined the phytophagous arthropod and ungulate abundance and feeding guild diversity across the three habitat types. We hypothesized that functional trait expression related to invasiveness would be associated with Guinea grass in its introduced range. Also, we hypothesized that the abundance and diversity of phytophagous arthropods and ungulates would be lower in the invaded range. Finally, we hypothesized that Guinea grass functional traits would differ between the three habitat types, given the habitat types’ innate differences in resource availability. We found that Guinea grass was 2.5 times taller and 3.3 times more productive and covered 2.5 times more area in its invaded versus native ranges. Introduced Guinea grass had higher reproduction rates with 2.5 times more reproductive tillers, while habitat type drove vegetative reproduction with 15 times more stoloniferous establishment in wooded and riparian sites than grasslands. Texan ungulate communities were less species-rich, less functionally diverse, and less abundant than the Kenyan ungulate community. The phytophagous arthropod diversity on plants was twice as high on Kenyan Guinea grass than on Texan Guinea grass. Total arthropod family richness was nearly double, with 15 families represented in Kenya and 8 in Texas. These results suggest that Guinea grass has escaped a rich assemblage of arthropods and ungulates and likely explains some of its spread in introduced ranges. This study demonstrates how the invasive success of Guinea grass can be understood in terms of its competitive ability and interaction with natural enemies in the introduced and native ranges and may inform future biological control.

arthropod diversity, biological control, ecological stressor release, function, invasion, natural enemy, ungulate

Introducing perennial grasses for rangeland improvement has led to the pantropical distribution of highly invasive grasses (Marshall et al. 2012; Rhodes et al. 2021). Alarmingly, the traits beneficial to higher livestock yields are associated with invasiveness (Jank et al. 2014) and lead to human-mediated dispersal (Parsons 1972; Pyšek and Richardson 2007). Dozens of hypotheses have successfully explained biological invasions, each with its level of support and interconnectedness (Catford et al. 2009; Jeschke et al. 2012). Two prevalent hypotheses relevant to invasive grasses are the Enemy Release Hypothesis (Keane and Crawley 2002) and the Evolution of Increased Competitive Ability (Blossey and Notzold 1995). The mechanisms underlying these hypotheses are likely not mutually exclusive (Jeschke et al. 2012), and each mechanism leads to the expansion of realized niche spaces in invaded ranges. When released from biotic and abiotic factors that limit their productivity and reproductivity, nonnative species may become invasive (Cox and Ricklefs 1977; Torchin et al. 2003; Canavan et al. 2019). For example, the Enemy Release Hypothesis posits that specialist enemies will be absent from the new system and that generalists will prefer native plants (Keane and Crawley 2002). However, these hypotheses are often context-dependent, and generalities may not apply to particular species (Pyšek and Richardson 2007). Therefore, describing the mechanisms leading to invasion by focal organisms of management or agricultural interest is critical for understanding the invasion process and mitigating the negative consequences.

Life histories and functional traits are important indicators of plant success and often correlate with their invasiveness and dominance in a community (Cornwell and Ackerly 2010). Invasive species outcompete native plants for resources (Blossey and Notzold 1995; Davis et al. 2000) and win apparent competition by losing natural enemies (Mlynarek et al. 2017). Several traits are associated with invasiveness: high reproductive output, reproductive mode (sexual vs. asexual), tolerance to herbivory, and height. Plant height often predicts invasiveness (Pyšek and Richardson 2007) through its impact on resource competition, correlation with biomass, and higher competitive ability to exploit resources (Canavan et al. 2019). Traits correlated to plant size are indicators of plant competition through their ability to disproportionately acquire resources such as light, water, and soil nutrients, which drive increased competitive ability and subsequent plant community composition (Lavorel et al. 2007; Dirks et al. 2017). Reproductive traits like clonality, increased flowering quantity, and increased flowering duration are indicators of invasiveness (Cadotte et al. 2006). Resource availability can drive interspecific differences in plant responses to herbivores (Coley et al. 1985). Likewise, intraspecific susceptibility to herbivores varies across resource availability (Fine et al. 2004). While a perennial grass in both its native and invaded range may have similar strategies, the release from natural enemies could alter these functional traits.

Guinea grass (Megathyrsus maximus syn. Panicum maximum (Jacq.) B.K. Simon & S.W.L. Jacobs) is consistently ranked among the most ecologically damaging invasive plant species globally (Best 2005; Randall 2017; CABI 2022). Guinea grass was first introduced to South Texas in the 1950s and has spread rapidly since the 1970s across a semi-tropical savanna dominated by the nitrogen-fixing trees honey mesquite Prosopis glandulosa Torr (Zitzer et al. 1996; Best 2005). Tree-grass interactions in these savannas include facilitation and competition for water and nutrient resources (Scholes and Archer 1997), and these primary associations mediate invasion at local scales (Colautti et al. 2006). Nitrogen-fixing trees promote improved nutrient availability, shade, and soil moisture (Zitzer et al. 1996; Scholes and Archer 1997) and facilitate Guinea grass invasion (Rhodes et al. 2022). Guinea grass is a tall-statured grass, often apomictic and polyploid, and is highly invasive pantropically (Kaushal et al. 2015; Canavan et al. 2019; Lambertini 2019). Tall-statured invasive grasses generally produce culms over 1.5 m in height and are noted for associating with invasiveness. They are commonly invasive outside their range (Lambert et al. 2010) and characterized by monodominance, high productivity, and reproductive rates (Canavan et al. 2019). Clonality, high flower count, and flowering throughout the season offer flexible life-history traits for invading Guinea grass (Rhodes et al. 2022). Comparing functional traits between naturally occurring invasive and native Guinea grass populations would improve our understanding of its invasion.

This dichotomy of Guinea grass is its economic success and ecological damage, which can be attributed to several core traits; its ability to grow in variable precipitation (400 mm – 1700 mm), high tolerance to herbivory (Sukhchain 2010), high reproductive rates (Rhodes et al. 2022) and strong competitive ability in its invaded range (Ho et al. 2016). Much of our current understanding of Guinea grass reproduction, production, and function is through its development as a pasture grass (Jank et al. 2014; Euclides et al. 2018; Maciel et al. 2018) or as a noxious weed (Alves and Xavier 1986; Best 2005; Ammondt and Litton 2012). However, few studies leverage an understanding of Guinea grass characteristics and interactions with natural enemies and stressors to understand the success of Guinea grass as an invasive species. Given that resource availability is a driver of invasion processes (Davis et al. 2000; Hui et al. 2016), understanding how resources alter Guinea grass production, reproduction, and interaction with the herbivore community is essential for mitigating Guinea grass invasion and evaluating prospective biological control programs.

Invasive plants alter the structure and function of arthropod communities (Van der Colff et al. 2015). Generally, invasive plants reduce arthropod diversity and abundance, leading to the collapse of trophic links (Herrera and Dudley 2003). However, the response of arthropod functional groups to invasive plants is mixed. Litt et al. (2014) found that abundance and taxonomic richness decreased in around half of the 87 studies reviewed, with the most significant increases in detritivores in 67% of the studies and herbivorous arthropods reduced by 48%. Plant community phylogenetic, phytochemical, and species richness can all impact an insect’s ability to feed on plants (Salazar and Marquis 2022). Therefore, many phytophagous arthropods may fail when plant communities change to invasive dominants, which may promote invasion.

Ungulates may be used to manage invasive plants, improving ecological restoration and maintenance outcomes with the added benefit of contributing to livestock yields (Frost and Launchbaugh 2003; Bailey et al. 2019). Grasses escaping from highly abundant and diverse ungulate communities will likely have higher productivity and reproductivity, competing well in invaded ranges. However, ungulates have differential impacts on plant species depending on their feeding guild and the physiology of the plant, such that the functional diversity of herbivores reduces plant establishment success (Rhodes et al. 2018). Targeted grazing of palatable grasses has shown promise for reducing the invasiveness of plants (Gaskin et al. 2021), but sustainable management is expected to entail arthropod associates. Thus, characterizing the arthropod and ungulate diversity in the native range of an invasive grass plays a critical role in understanding the ecological importance of those arthropods and developing efficient biological control programs.

The primary objective of this project was to evaluate Guinea grass functional traits across three habitat types in the native and invaded ranges and document the arthropod and ungulate herbivore community assemblages. To achieve this objective, we; first quantified Guinea grass functional traits and reproductive output across three habitat types. Second, we measured the richness and diversity of phytophagous arthropods and ungulate herbivores on Guinea grass in native ranges versus the invaded range. Third, we characterized these communities by their relative abundance and feeding guild diversity. Fourth, we developed a list of the arthropod community attached to Guinea grass to understand their impact. We hypothesized that functional trait expression related to invasiveness would be associated with Guinea grass in its introduced range. We hypothesized that functional traits would differ between the three habitat types, given the habitat types’ innate differences in resource availability. Finally, we hypothesized that the abundance and diversity of phytophagous arthropods and ungulates would be lower in the invaded range, consistent with the Enemy Release Hypothesiss.

We established field sites to examine Guinea grass occurring naturally in two savanna systems; 1) the native range in Laikipia Province, Kenya, and 2) the invaded range in South Texas, where Guinea grass is spreading rapidly. Ten locations were selected in both Kenya and Texas. Each location had three habitat types: woody mottes (thickets), open grassland, and riparian zones. Three 1 × 1 m subplots were randomly established within each habitat type for 180 subplots. Mottes were under woody legumes with higher soil moisture and soil nitrogen. We selected two major tree species, each native to the study area; Senegalia mellifera (Benth.) Seigler & Ebinger, common in the red soils of Laikipia, and P. glandulosa in Texas a common species. The grassland sites for each grouping were approximately halfway between the thicket (motte) and riparian habitat types. Riparian areas were defined as the upland portion of ephemeral creeks that fed into the main waterway (Los Olmos Creek in Texas and Ewaso Ng’iro River in Kenya).

In Kenya, field sites were selected along the Ewaso Ng’iro River. West of the river is Mpala Research Centre, an active cattle ranch with approximately 3000 livestock grazing at low to moderate stocking intensities on 19,500 hectares, including Zebu/Boran mix-breed of cattle, camel, goat, and sheep. Mottes were maintained naturally by large ungulate and fire disturbances. In Texas, the study was conducted at two ranches with active brush and cattle management activities in the semi-arid mesquite thorn tree savanna of the South Texas Plains ecoregion. A 1600-ha ranch pasture in Kenedy, Kleberg & Brooks Counties on Palobia loamy fine sand was brush-chained in the 1970s and then partly root-plowed in 1998 to form residual stands of P. glandulosa in a grassland matrix and a 1000-ha ranch pasture in Brooks County, on Padrones fine sand. Cattle regularly graze both sites and feed on Guinea grass. Stocking densities were generally low to moderate using resident longhorn cattle (Bos primigenius) and common stocker cattle (Bos taurus).

In South Texas, Guinea grass has pronounced functional and reproductive traits associated with invasiveness. Our results show that Guinea grass in South Texas was taller, dominated a larger area, produced more biomass (especially aboveground), and reproduced sexually at higher rates than in its native range. These differences likely have cascading impacts on Guinea grass’s competition with native species (Ammondt and Litton 2012; Ho et al. 2016; Espinosa-Garcia and Villasenor 2017; CABI 2022). Guinea grass’s release from ecological stressors and enemies has likely contributed to the highly successful expansion of Guinea grass in the three different habitat types in South Texas. In contrast, the three habitat types in Kenya corresponded to heterogeneous and lower productivity and reproduction capacity compared to the heterogeneity of its invaded range. Likewise, Guinea grass’s escape from abundant and functional diverse phytophagous arthropods and ungulates has likely contributed to its success across these variable environments. This study represents an essential step in describing differences in the breadth of Guinea grass’s natural enemies in its native and invaded ranges and the niches it can occupy, which improves our understanding of Guinea grass invasion.

The morphology and productivity of invasive plants are functional traits that can predict invasiveness (Pyšek and Richardson 2007). Greater height and biomass influence resource competition and invasiveness (Canavan et al. 2019), indicating faster growth rates, resource acquisition, and reproductive potential. Our results suggest that Guinea grass is becoming dominant in its invasive range by producing taller plants, higher biomass per plant, and higher foliar cover (Fig. 1) (Canavan et al. 2019). This productivity correlates to Guinea grass’s ability to compete for light and soil resources which have cascading effects on nutrient cycling and fire cycles (D’Antonio and Vitousek 1992). Tall-statured grasses disproportionately outcompete and become invasive compared to short-statured grasses (Canavan et al. 2019). Reproductive output and mode are associated with the invasiveness of plants (Pyšek 1997; Pyšek and Richardson 2007). In Guinea grass, seed-borne and vegetative reproduction likely leads to an effective invasion across different habitat types and resource availability (Rhodes et al. 2022).

Vegetative reproduction is associated with a higher competitive ability (Pyšek 1997), and the reproductive mode plays a critical role in sustaining local populations and dispersing propagules (Benson and Hartnett 2006; Simberloff 2009). Thus, reproductive traits play an important role in plant community assembly and subsequent invasion (Dirks et al. 2017). Guinea grass’s propagule pressure and reproductive plasticity are critical factors for its establishment in novel and resource-available habitat types in its expanding range (Rhodes et al. 2022). In an established perennial grass community, asexual reproduction can represent up to 99% of the population turnover, while sexually reproduced individuals can be near 1% (Benson and Hartnett 2006). The higher reproduction through seedheads in the invaded range and stoloniferous reproduction was important in mottes in the native and invaded range. Guinea grass will likely have more successful establishment events in the invaded range without significant herbivore pressure.

In savanna systems, woody vegetation and riparian patches integrate with a grassland matrix creating gradients of light environment, nutrient turnover, and water availability that have vital impacts on grass growth (Zitzer et al. 1996; Ludwig et al. 2004). The interaction between herbivores and resources significantly impacts community structure and plant production (Olff and Ritchie 1998; Fine et al. 2004; Wan et al. 2014). Plant species in different habitat types may express variable intraspecific traits (Pyšek 1997; Cadotte and Lovett-Doust 2001). Phenotypic plasticity may improve outcomes for invasiveness, and grasses invading multiple habitat types often achieve similar negative impacts on each habitat, despite their different resource availability (Richards et al. 2006). Our study found that in its native range, Guinea grass had different morphometrics and reproductive characteristics across habitat types. In Kenya, Guinea grass height in riparian areas was similar to the height in habitat types of Texas (Fig. 1A). These differences are partly due to increased water resources in riparian environments and nutrients and shade in mottes (Zitzer et al. 1996) that improve outcomes for germination and growth in the critical early stages of development (Rhodes et al. 2022).

Losing natural enemies can increase biomass compared to native populations (Torchin et al. 2003). Guinea grass’s escape from a comprehensive assemblage of natural enemies is correlated with these increases in primary production and reproductive capacity. Further, in this study, higher productivity translated into higher seedhead production, which could further accelerate the invasion of Guinea grass in South Texas savannas through enhanced dispersal and propagule pressure (Rhodes et al. 2022). The increase in productivity correlates to the lower number of arthropod herbivores in the invaded range, which is indicative of a reduction in natural enemies (Torchin et al. 2003; Lucero et al. 2020). Aggregated with this loss of phytophagous arthropods is the abundance and diversity of ungulate herbivores, which may contribute to lower productivity in the invaded range. The feeding guilds of both groups of organisms may differentially impact invasion success.

The differences between Kenya and Texas’s arthropod and ungulate communities were stark. Several arthropod species encountered in Kenya are from feeding guilds known to tend toward specialization, including stem borers and mites (Rhodes et al. 2021). While invasive species can acquire novel enemies in their invaded range (Torchin et al. 2003; Rhodes and St. Clair 2018), they do so to a lesser degree. Therefore, the acquisition of generalist herbivores in Texas has likely not replaced the top-down impact on Guinea grass dominance and height in its native range, similar to the general results of enemy release (Lucero et al. 2020). However, Kenyan Guinea grass was similar to Texas’s in resource-rich environments (riparian areas and mottes). This pattern may be due to increased tolerance to herbivory through resource availability (Coley et al. 1985) or growth-defense trade-offs (Lind et al. 2013). In addition, we documented that the phytophagous arthropod community varies drastically between the native and invaded ranges. In the case of invasive species that are important for forage and livestock yields, breeding programs select to heighten resistance to pathogens (Savidan et al. 1989; Maciel et al. 2018). Together, the arthropod and ungulate communities likely restrict Guinea grass to high-resource habitats and represent a barrier to its spread in Kenya. Yet, when released from these enemies, Guinea grass spreads well in a broader ecological niche in South Texas.

Utilizing natural enemies has formed the basis for classic biological control. The potential for classic biological control has been known for decades (Dodd 1940) as a self-sustaining management practice. However, invasive species management is also context-dependent, and a single organism may not be sufficient to contain an invasive organism. Therefore, more recent biological control programs often include a functionally diverse introduction of natural enemies, grasses such as Arundo donax (Goolsby et al. 2011; Goolsby et al. 2016), or control of invasive ants (Porter and Gilbert 2004). A renewed interest in controlling invasive grasses through biological control may lead to substantive improvements in the mitigation of grass invasion (Sutton et al. 2019).

This study represents an essential step in describing the productivity and reproduction of Guinea grass in three resource environments and its association with natural enemies in its native and invaded ranges. Guinea grass achieved high productivity and reproductivity across the range of habitat types in its invaded range when released from native enemies. However, in its native range, when subjected to natural enemies, the potential of Guinea grass was significantly reduced. In addition, the diversity of specialist and generalist arthropods in Kenya is high compared to the few generalist arthropods in Texas. This information improves our understanding of opportunities to develop impactful and sustainable biological control agents (Sutton et al. 2019). Further, since release from a single enemy may not drive increased invasiveness, using a suite of organisms across feeding guilds may be more appropriate in biological control (Porter and Gilbert 2004; Goolsby et al. 2011; Goolsby et al. 2016).

Grasses are a critical group of organisms that make up most food crops and are translocated for pasture development, yet are also among the most pervasive invaders (Linder et al. 2018; Sutton et al. 2019). Given these two competing interests, an important goal is to search for sustainable biological control specific to the problematic grass species (Rhodes et al. 2021). Understanding how Guinea grass’s ecology and biology differ in its native and introduced range may open opportunities for directed management. A troubling predicament is an enormous effort spent controlling Guinea grass as a weed and a similar effort developing Guinea grass as a pasture grass, encouraging invasive traits (Rhodes et al. 2021). Guinea grass represents an economically valuable forage species for livestock globally (Jank et al. 2014) yet often escapes to degrade ecosystem function and diversity. While traditional means of controlling invasive grasses may not be effective at landscape scales (Rhodes et al. 2021), a renewed focus on biological control for grasses could prove critical for controlling invasive grasses globally (Sutton et al. 2019).

We thank the skilled and knowledgeable technicians Godfrey Amoni, Kamukunji Katero from the Mpala Research Centre, and the Centre itself for its logistical support of this research. In Texas, Jason Lawson was our lead technician and was instrumental in assisting Texas’s collection and processing of materials. We also thank Kaitlyn Williams and Shellsea Miller for their molecular contributions. The authors have declared that no competing interests exist.

This research was funded by the Lee and Ramona Bass Foundation.