Systematic reduction of natural enemies and competition across variable precipitation approximates buffelgrass invasiveness (Cenchrus ciliaris) in its native range.

Invasive grasses cause devastating losses to biodiversity and ecosystem function directly and indirectly by altering ecosystem processes. Escape from natural enemies, plant-plant competition, and variable resource availability provide frameworks for understanding invasion. However, we lack a clear understanding of how natural stressors interact in their native range to regulate invasiveness. In this study, we reduced diverse guilds of natural enemies and plant competitors of the highly invasive buffelgrass across a precipitation gradient throughout major climatic shifts in Laikipia, Kenya. To do this, we used a long-term ungulate exclosure experiment design across a precipitation gradient with nested treatments that (1) reduced plant competition through clipping, (2) reduced insects through systemic insecticide, and (3) reduced fungal associates through fungicide application. Additionally, we measured the interaction of ungulates on two stem-boring insect species feeding on buffelgrass. Finally, we measured a multiyear smut fungus outbreak. Our findings suggest that buffelgrass exhibits invasive qualities when released from a diverse group of natural stressors in its native range. We show natural enemies interact with precipitation to alter buffelgrass productivity patterns. In addition, interspecific plant competition decreased the basal area of buffelgrass, suggesting that biotic resistance mediates buffelgrass dominance in the home range. Surprisingly, systemic insecticides and fungicides did not impact buffelgrass production or reproduction, perhaps because other guilds filled the niche space in these highly diverse systems. For example, in the absence of ungulates, we showed an increase in host-specific stem-galling insects, where these insects compensated for reduced ungulate use. Finally, we documented a smut outbreak in 2020 and 2021, corresponding to highly variable precipitation patterns caused by a shifting Indian Ocean Dipole. In conclusion, we observed how reducing natural enemies and competitors and certain interactions increased properties related to buffelgrass invasiveness.

Human altered disturbance patterns and forest succession: impacts of competition and ungulate herbivory.

Human activities are altering patterns of ungulate herbivory and wildfire regimes globally with large potential impacts on plant community succession and ecosystem resilience. Aspen (Populus tremuloides) is a keystone species which co-exists with conifer species across temperate forests in North America. Aspen sucker regeneration which is the foundation of aspen-conifer forests succession is often a targeted food source by multiple ungulate species. Using a region-wide exclosure network across a broad gradient of aspen-conifer overstory abundance, we empirically tested the effects of ungulate herbivory and conifer competition (that increases with fire suppression), on the regeneration and recruitment of aspen forests over a 4-year period. The study results indicate that ungulate herbivory and increasing abundance of overstory conifers dramatically reduced aspen regeneration and recruitment success. The average height of aspen suckers exposed to ungulate herbivory was 72% shorter than aspen suckers in fenced plots and resulted in 24% less recruitment. There was a 9% decrease in aspen recruitment and 12% decrease in average aspen height with every 20% increase in overstory conifer density. Aspen suckers were most vulnerable to herbivory at 70 cm height, with the probability of herbivory decreasing under 50 cm or above 90 cm. Steep slope angles and higher winter precipitation increased aspen regeneration and recruitment success. Reduction in aspen recruitment in response to ungulate herbivory and competition by conifers may result in loss of biodiversity, altered forest function and loss of key ecosystem services because of the important role that aspen plays in facilitating forest succession and biodiversity.

Temporal patterns of ungulate herbivory and phenology of aspen regeneration and defense.

Ungulate herbivory can create strong top-down effects on forest recruitment, especially after fire. Defense strategies of tree species against ungulate herbivory include escape through vertical growth and resistance through the production of defense compounds. Using a four-way fence design and camera traps we characterized the differential impacts of ungulate herbivores (deer, elk, cattle) on aspen forest recruitment and plant defense responses and how they vary depending on the timing of herbivory. Aspen height growth was greatest between June and August and ungulate use of aspen was highest in July and August. Three years after fire, height of aspen differed among fence treatments with full ungulate exclusion > deer-only plots > native ungulate plots > fenceless plots: 108 ± 4 cm, 94 ± 4 cm, 89 ± 4 cm, and 65 ± 4 cm, respectively. Fenceless plots had the highest rates of removal of apical meristems by the end of 2014 and 2015 (61% and 53%, respectively). Native ungulate plots, and deer-only plots both had similar removal of apical meristems in 2014 (37% and 39%, respectively). The highest phenolic glycoside concentrations were associated with an 80% reduction in meristem removal and four-fold greater aspen height by the end of summer. Low nitrogen was associated with an 86% reduction in apical meristem removal and threefold greater aspen height. In conclusion, our study suggests that high ungulate abundance can have detrimental impacts on forest recruitment and that high aspen defense chemistry and lower leaf N deters ungulate herbivory, especially in the late summer.

Ungulate herbivory alters leaf functional traits and recruitment of regenerating aspen.

Herbivory by ungulates can affect forest regeneration success, but its long-term impacts on tree function and recruitment are less studied. We evaluated strategies of resistance, tolerance and vertical escape against ungulate herbivory by evaluating leaf traits (photosynthesis, morphology and chemistry) and growth rates of aspen in the presence and absence of ungulate herbivores 1, 2, 3 and 26 years after fires initiated aspen suckering. Over the initial 3-year period, ~60% of aspen stems in unfenced plots showed evidence of being browsed by ungulates. After 3 years, aspen in unfenced plots had smaller leaves, were 50% shorter, and had 33% lower nonstructural carbohydrate concentrations and 33% greater concentrations of condensed tannins, when compared with fenced aspen. Aspen exposed to ungulate herbivory over a 26-year period maintained smaller leaves, had lower annual radial growth rates and were still below the critical height threshold of 2 m required to escape ungulate herbivory for successful recruitment. In contrast, the average height of aspen protected from ungulates was approaching 6 m. Over the 26-year period leaves in unfenced plots had 41% lower nonstructural carbohydrate concentrations and greater expression of defense compounds-condensed tannins (63%) and phenolic glycosides (102%)-than leaves in fenced plots. Photosynthetic rates were slightly higher in aspen that experienced ungulate browsing, suggesting that changes in leaf anatomy and chemistry due to ungulate herbivory did not interfere with photosynthesis. Our data suggest that ungulate browsing increases investment in chemical defense, lowers nonstructural carbohydrate concentrations and reduces leaf area, which decreases the recruitment potential of regenerating aspen.

Stand Composition, Tree Proximity and Size Have Minimal Effects on Leaf Function of Coexisting Aspen and Subalpine Fir.

Forest structural heterogeneity due to species composition, spatial relationships and tree size are widely studied patterns in forest systems, but their impacts on tree function are not as well documented. The objective of this study was to examine how stand composition, tree proximity relationships and tree size influence the leaf functional traits of aspen, an early successional species, and subalpine fir, a climax species. We measured foliar nutrients, nonstructural carbohydrates (aspen only), defense chemistry and xylem water potential of aspen and subalpine fir trees in three size classes growing in close proximity or independently from other trees under three stand conditions: aspen dominant, aspen-conifer mixed, and conifer dominant stands. Close proximity of subalpine fir to aspen reduced aspen's storage of starch in foliar tissue by 17% suggesting that competition between these species may have small effects on carbon metabolism in aspen leaves. Simple sugar (glucose + sucrose) concentrations in aspen leaves were slightly higher in larger aspen trees than smaller trees. However, no differences were found in stem water potential, foliar concentrations of nitrogen, phosphorus, or secondary defense chemicals of aspen or subalpine fir across the gradients of stand composition, tree proximity or tree size. These results suggest that mechanisms of coexistence allow both aspen and subalpine fir to maintain leaf function across a wide range of stand structural characteristics. For aspen, resource sharing through its clonal root system and high resource storage capacity may partially contribute to its functional stability in mixed aspen-conifer stands.