The invasion of ecosystems by non-native species is recognized as one of the most significant global challenges, particularly in semiarid regions where native biodiversity is already under stress from drought and land degradation. The implicit assumption is that invaders are strong competitors, but a greenhouse pairwise experiment conducted to examine intraspecific and interspecific competition effects of Opuntia ficus-indica, a widespread invader in semiarid ecosystems, with two species native to the highlands of Eritrea, Ricinus communis and Solanum marginatum, revealed that O. ficus-indica is a weak competitor. In direct interaction, the competition in aboveground productivity measured by the logarithmic response ratio for O. ficus-indica was 3.4-fold and 5.9-fold higher than for R. communis and S. marginatum, respectively. Belowground, the native R. communis was facilitated (-1.00±0.69) by O. ficus-indica which itself suffered from high competition. This pattern became even stronger under water shortage, where aboveground competition for S. marginatum decreased 5.7-fold, and for O. ficus-indica, it increased 1.4-fold. Despite being a poor competitor, O. ficus-indica outperformed R. communis and S. marginatum in both aboveground (4.3 and 3.8 times more) and belowground (27 and 2.8 times more) biomass production, respectively. The findings of this study challenge the common interpretation that invasive species are strong competitors and highlight the importance of considering other factors, such as productivity and tolerance limits, when assessing the potential impacts of invasive species on semiarid ecosystems.
Research Article
How can an inferior competitor be a successful invader?
https://doi.org/10.21203/rs.3.rs-2715432/v2
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plant competition
non-native plant species
plant invasion
semiarid ecosystem
pairwise greenhouse experiment
Opuntia ficus-indica
It is generally concluded that invasive plants outcompete native species during their successful invasions of many ecosystems1. Thereby, invasive species can endanger populations of native species2–4, reduce spatial diversity5, or negatively affect crop yields6. All these processes are commonly explained by the superior competitive abilities of the invasive species7. It is argued that only highly competitive species can spread in a new environment8 after successfully overcoming biotic and abiotic barriers9.
Field observations show that invasive species outcompete and limit the abundance of native species7,10,11 and direct paired competition experiments generally support this finding7. Exceptions with highly competitive native species limiting the exotic invaders mainly stem from temperate grasslands7. Here, competition by native species has been shown to reduce invasive plant growth considerably and even stronger than herbivory. Accordingly, the high competitive abilities of native species can effectively reduce invasion12–14. However, little is known about the competitive balance between invaders and native species in subtropical semiarid shrublands7, where unpredictable precipitation can cause strong abiotic stress as well as temporarily abundant free resources.
Free resources due to fluctuating environments in time or disturbance in space generally make communities more susceptible to invasion15,16. Consequently, ecosystems in unpredictable climates where a limiting resource, here water, create chronic stress but intermittent rainfall events cause unlimited conditions at hardly predictable points in time, can be expected to offer little resistance to invasions. Subtropical semiarid drylands are such ecosystems, but little is known about invasion processes and competitive balances between invaders and native species in these ecosystems7. Stress tolerance could further affect competitive balances, particularly in resource-limited ecosystems such as the water-limited semi-arid subtropical shrublands.
Opuntia ficus-indica (prickly pear) is a cactus native to Mexico that is exceptionally successful in invading arid and semi-arid ecosystems, e.g., in Australia, South Africa, Kenya, Tanzania, Ethiopia, Eritrea, Somalia, Yemen North America and Hawaii17–19. Moreover, it is reported that O. ficus-indica is the most widespread invasive cactus, found nowadays in 22 different countries on all continents except Antarctica outside its native range20. It acts as an ecosystem engineer, modifying the habitat of the indigenous plant and animal species 21 and reducing spatial diversity5. Its invasion has economic effects by impeding the movement of livestock and humans as it forms impenetrable thickets and thereby threatens large-scale cattle ranching18.
Based on its invasion success, O. ficus-indica is assumed to outcompete the neighbouring native species22 and, due to its strong drought tolerance23,24, can be assumed to become even more competitive when water availability is low. Coincidentally, vast parts of the areas invaded by O. ficus-indica will face increasing water scarcity with ongoing climate change25. The competitive abilities of O. ficus-indica, however, have not yet been tested experimentally, neither under water-limited nor under wetter conditions.
Accordingly, this paper deals with pair-wise competition experiments in two different water availabilities between the invasive plant O. ficus-indica and two typical and common native plant species of invaded areas in Eritrea, Ricinus communis and Solanum marginatum. Considering its global invasion success in dry ecosystems, we hypothesized that O. ficus-indica has a high competitive power and outcompetes the native species irrespective of water availability. We furthermore expected that its competitive superiority increases under water stress.
The competition between species can be quantified experimentally using indices based on pairwise experiments which express competition intensity, effects and response4,26. Competition indices help to quantify the proportional decrease in native plant performance due to the competing effects of invasive species and compare the effects on different species or under different environmental conditions26–29. When interspecific competition is weaker than the intraspecific competition in an invaded ecosystem, each native species in that community limits its population growth more than it limits the population growth of the competitive invader30,31.
Study species
Vilà et al.6 and Vilà and Weiner7 criticise pairwise competition experiments between invasive and native species for selecting highly competitive and aggressive invaders and comparing them to rare and threatened native species, which, per se, are poor competitors. Here, we avoid this bias by comparing a globally successful invasive species to two common and widespread native species which generally resemble the invasive species in growth form and life strategy.
Opuntia ficus-indica (Cactaceae) is an evergreen perennial plant that can grow up to 5 m in height. The species has succulent stems that are formed as a sequence of flattened segments, the cladodes, which generally have an elliptical base that supports the greatly enlarged, flattened upper portion. O. ficus-indica has spines, morphologically corresponding to leaves. Its flowers (5-10 cm in diameter) are sessile and solitary, and the fruits are berries that are 4-8 cm in diameter32. Nieddu and Chessa33 found the germination of O. ficus-indica seeds reaching up to 90% in growth chambers with a day/night temperature of 30/200C, but only reaching 55% when seeds were kept at room temperature and 43% when seeds were placed outdoors. The seeds are usually dispersed after the consumption of the fruits by humans, birds, and other animals (endozoochory). Furthermore, vegetative propagation occurs through cladodes readily taking root upon falling to the ground and conspicuous patch formation is an important factor in the persistence of local populations of the plant, although seedling recruitment is essential for expanding the geographic range and establishment in new areas32.
Ricinus communis (Euphorbiaceae) is a fast-growing soft wooden shrub or small tree (up to 5 m tall) distributed throughout the tropics and warm temperate regions. R. communis is indigenous to eastern Africa, the south-eastern Mediterranean Basin, and India. It has developed various strategies, such as rapid growth, allelopathy, thriving in a wide range of soil conditions, and high seed production, to adapt to the conditions of disturbed areas 34. R. communis is also known as a poisonous plant due to the presence of toxic ricin and ricinine in its seeds and other parts, however, it is still commonly used as an ornamental plant and because of its antimicrobial features, it is used as a medicinal plant to treat several ailments35.
Solanum marginatum (Solanaceae), native to the highlands of Eritrea and Ethiopia, is a perennial shrub (up to 2 m tall) with leaves densely covered in white stellate hairs and armed on both the upper and lower surfaces with prickles36. In its native range, it usually occurs in disturbed areas between altitudes of 2000 m and 3000 m above sea level37,38. S. marginatum is usually unpalatable to herbivores mainly due to the presence of a poisonous alkaloid chemical compound39,40.
The invasive O. ficus-indica and the native species are generally found to grow together in the highlands of Eritrea5. These three species have all been referred to as weedy and thrive in disturbed areas34,37,41 and all possess chemical and/or physical defences against herbivory. They differ little in their potential plant heights, but in some morphological features, O. ficus-indica as a cactus is a succulent plant that can store water, unlike the other two native species. Sharing a similar life strategy and avoiding the common bias of choosing rare native species6,7 were the important considerations for choosing these two native species.
Experimental design
The greenhouse competition experiment was carried out from February 2020 to May 2021 at Greifswald, Germany. Two species native to the highlands of Eritrea, Ricinus communis and Solanum marginatum were selected to test the competitive potential of the invasive cactus O. ficus-indica in a common-garden pair-wise competition experiment. Two different treatments were set up based on resource availability (water) depicting dry and wet environments. Each treatment was prepared with fifty pots of one-litre volume. The substrate was a mixture of 75% loamy forest soil and 25% quartz sand. All plants were raised from seeds. Since O. ficus-indica needed more time to germinate, it was sown in January 2019, eight months ahead of the other two plants, which were sown in August 2019. After being transplanted into their respective target pots on February 10th, 2020, all plants, regardless of the species, exhibited similar heights of approximately 15 cm. The plants were categorized in two stands: intraspecific competition (native only, invasive only) and interspecific competition (native and invasive). The intraspecific category had a pair of R. communis plants per pot (20 replicates), a pair of S. marginatum plants per pot (20 replicates) and a pair of O. ficus-indica plants per pot (20 replicates). The interspecific category had O. ficus-indica and R. communis plants per pot (20 replicates), and O. ficus-indica and S. marginatum plants per pot (20 replicates). Half of the pots from each category were distributed to each condition of the wet and dry environment. The pots in the wet environment were watered twice per week with 100ml of water simulating a wet condition. The other half of the pots were watered only once per week with 100ml. The watering regimes were based on pre-trials with all three species. The dry variant was set right above the limit at which the native species showed strongly increased mortality. The invader O. ficus-indica proved to be remarkably resilient, surviving for nine months without any watering. To assess the plant's water tolerance limits, we conducted a pot experiment, exposing 16 plants to a gradient of water availability ranging from no water up to 260 ml twice a week over a period of nine months. While the growth of the plants exposed to drought on the lower end of the gradient was impeded, all plants survived the experiment, even the one not receiving any water for 9 months. In a subsequent recovery experiment, the plants that were previously subjected to drought showed rapid recovery within five days. Additionally, the plant that received the highest amount of water was submerged in a bucket of water for three months and displayed no signs of stress; instead, its roots grew upward and out of the water (see Supplementary 1 online for details on the pretrial).
The effects of the invader in the main experiment were assessed by comparing the native species growing alone (intraspecific, i.e., the average of the two plants per pot) with those that were growing with the invader (interspecific) for the wet and dry treatment, respectively. The positions of the pots within the greenhouse were frequently interchanged to secure similar environmental conditions and reduce edge effects or the like. The plants were kept at an average of 40% humidity and in a 12-hour day and night cycle, at temperatures of 20 °C and 12 °C, respectively.
Response parameters
We quantified above- and belowground net primary production at the end of the experiment (after 15 months of growth in competition), hereafter ANPP and BNPP. Belowground biomass was gently washed free from the substrate by rinsing it into a coarse sieve so that the substrate was washed away, and the roots and rootlets could all be collected. The above- and belowground biomasses were dried for five days at 60 °C and 100% ventilation and weighed.
Statistical analyses
The growth parameters (ANPP and BNPP) were analysed using a two-factorial analysis of variance (ANOVA 42 ) with the explanatory factors being water regime (wet/dry) and competition (intraspecific/interspecific for both the native species and the invader, i.e., a factorial variable with four levels: native-native, native-invasive, invasive-native, invasive-invasive, with the biomass value of the first named in each pair in interspecific competition and the average biomass of both individuals per pot in case of intra-specific competition) including their interaction. Single models were run for each native species (S. marginatum and R. communis) and each response parameter (ANPP and BNPP) for a total of four ANOVA analyses. Tukey’s HSD post hoc tests43 were used to assess the significance of differences in pairwise comparisons for significant interaction terms.
Furthermore, two different competition indices were implemented; Logarithmic Response Ratio (lnRR) and Relative Neighbour Effect (RNE)4,44,45. As both indices yielded highly similar patterns, we present the results based on lnRR in the main text (Fig. 2) and based on RNE in the Supplementary 2 online.
The Logarithmic Response Ratio (lnRR) is computed by the natural log of the ratio between the mean value of the respective control treatment (intraspecific without a second species) and the value of each treatment growing in competition with a second species (interspecific). Smaller values indicate weaker competition with negative values showing facilitation, while larger values indicate intense competition between the species4,27. lnRR is expressed as:
The effect of the different water regimes on the competition index data was examined using a one-way analysis of variance with water regime (dry/wet) as explanatory factor. Single models were run for each native species (S. marginatum and R. communis) and each response parameter (ANPP and BNPP) for a total of four ANOVA analyses.
Parametric assumptions were checked for all ANOVA models by examining the diagnostic plots (residuals versus fitted plots for homoscedasticity of the residuals and normal qq-plots for normal distribution of residuals46. According to the diagnostic plots, the ANPP and BNPP for both the R. communis and the S. marginatum datasets were log(x+1)-transformed. The competition index datasets did not require transformations. For graphical visualizations, the function bar graph.CI in the R package sciplot47 was used. All statistical analyses were done in R version 4.248.
ANPP of O. ficus-indica was 4.3-fold higher under intraspecific competition than when competing with R. communis (Fig. 1 a). In comparison, the native R. communis was 14-fold less productive aboveground than O. ficus-indica, but its ANPP was unaffected by the identity of its neighbour as its production did not differ between intra- and interspecific competition. O. ficus-indica was unaffected by the water regime in ANPP while the native R. communis produced 2.2-fold more aboveground biomass under wet conditions and intraspecific competition than under dry conditions and interspecific competition (Fig. 1 a).
BNPP of O. ficus-indica was 27-fold higher under intraspecific competition than when competing with R. communis (Fig. 1 c). In comparison, the native R. communis was 17-fold less productive belowground under intraspecific competition than O. ficus-indica, but its BNPP even increased 3.1-fold under interspecific as compared to intraspecific competition. O. ficus-indica doubled its BNPP under the dry as compared to the wet water regime when growing with itself but produced very little BNPP and showed no water effect when grown under interspecific competition. R. communis, in contrast, increased its BNPP in dry conditions 1.9-fold over wet conditions only when growing in interspecific competition with O. ficus-indica, but not when growing with itself (Fig. 1 c).
ANPP of O. ficus-indica was 3.8-fold higher under intraspecific competition than when competing with S. marginatum (Fig. 1 b). In comparison, the native S. marginatum was 11-fold less productive aboveground than O. ficus-indica, but its ANPP was unaffected by the identity of its neighbour as its production did not differ between intra- and interspecific competition. In interspecific competition with S. marginatum, O. ficus-indica increased its ANPP 1.7-fold under wet as compared to dry conditions, while it did not show an aboveground growth response to the water regime when growing with itself. The ANPP of the native S. marginatum was unaffected by the water regime, irrespective of competition (Fig. 1 b).
BNPP of O. ficus-indica was 2.8-fold higher under intraspecific competition than when competing with S. marginatum (Fig. 1 d). In comparison, the native S. marginatum was only half as productive belowground as O. ficus-indica under intraspecific competition but showed a similar pattern as the latter as its BNPP was 3.0-fold higher when grown with itself than under interspecific competition. O. ficus-indica doubled its BNPP under the dry as compared to the wet water regime when growing with itself but produced less BNPP and showed no water effect when grown under interspecific competition. S. marginatum showed no significant effect in its BNPP on the water treatment (Fig. 1 d).
Competition index
Ricinus communis and O. ficus-indica showed aboveground competition in their direct interaction, with the lnRR for ANPP being 3.4-fold higher for O. ficus-indica than for R. communis (1.51±0.31 mean ± SD versus 0.45±0.23, respectively; Fig. 2 a). This pattern of aboveground competition was unaffected by the water regime. Belowground, the native R. communis was facilitated (-1.00±0.69) by O. ficus-indica which itself suffered strongly from high competition by the native species (3.35±0.65; Fig. 2 c). This pattern was significantly stronger for both species under dry than under wet conditions.
Solanum marginatum and O. ficus-indica showed aboveground competition in their direct interaction, which was 5.9-fold higher for O. ficus-indica than for S. marginatum (1.45±0.44 versus 0.24±0.33, respectively; Fig. 2 b). This aboveground competition was 5.7-fold stronger for S. marginatum under wet as compared to dry conditions and 1.4-fold weaker for O. ficus-indica under wet as compared to dry conditions. Belowground, S. marginatum and O. ficus-indica showed about equal competition in their direct interaction (1.20±0.46 versus 1.04±0.52; Fig. 2 d). For S. marginatum, belowground competition was unaffected by the water regime while competition increased 1.9-fold under dry as compared to wet conditions for O. ficus-indica.
Opuntia ficus-indica, a highly successful invader of semiarid and arid ecosystems on all continents containing such conditions, was an inferior competitor to R. communis and S. marginatum, two species native to the highlands of Eritrea where O. ficus-indica is also spreading vigorously, in our pairwise competition experiment. O. ficus-indica dropped in ANPP and BNPP about 4-fold and three to 27-fold, respectively, when growing together with the two native species. Competition indices indicated high competition for O. ficus-indica irrespective of the competing native, while the natives experienced less competition or even facilitation by O. ficus-indica. These findings reject the hypothesis that the successful invader is a superior competitor to the native species 49,50 . The majority of pairwise competition trials between invasive and native species supported that hypothesis7. The notable exceptions in that meta-analysis stem mainly from temperate grasslands, which are known to harbour native species with high competitive abilities that can resist invasions 51. Based on this and the competitive abilities found in our study, our invasive species should face strong resistance and have little success in invading native communities containing the two competitively superior native target species. Surprisingly, that is not the case. O. ficus-indica spreads vigorously into areas containing those two native species5. So, the question arises, how an inferior competitor can be a successful invader?
The invasive O. ficus-indica produced several folds more biomass than the natives, even under competition with the natives where it is doing much worse than on its own. Therefore, it ‘outproduces’ the competitively stronger natives in all cases except for BNPP with R. communis. To better understand the role of competition in plant invasion, the relative biomass production of an invasive species compared to the native species should therefore be taken into consideration. Based on a meta-analysis of interspecific and intraspecific competition trials, Vilà and Weiner7 found that mixtures of native and invasive species are less productive than native monocultures but not less productive than monocultures of the invasive plants. In our study, the interspecific mixtures produced, on average, 13.9 g aboveground biomass per pot, which is more than twice the production of the native species in monoculture (5.7 g) but nearly seven times less than the invasive species in monoculture (97.1 g). The numbers for BNPP followed a similar pattern, being 2.9 g for the mixture, 3.3 g for the native monocultures, and 14.1 g for the invasive monocultures, respectively. Comparing these numbers to the meta-analysis implies that our finding of a highly productive but weakly competitive invasive species might be an interesting exception rather than the rule.
The results of our experiment showed that competition by the native species generally increased for O. ficus-indica under the dry as compared to the wet treatment (Fig. 2). At first sight, this finding contradicts our second hypothesis which expected higher competitive power of O. ficus-indica under dry conditions. However, this weak competition should not be interpreted as a sign of reduced invasion pressure on the community. O. ficus-indica is known to be highly drought-tolerant52. We based the water regimes of our experiment on pretrials that tested the water tolerance limits of the target species and found increased mortality of the native species right below our dry water regime. It is probably very relevant to its invasion success in dry ecosystems that O. ficus-indica itself was able to survive well below this limit. Our pretrial showed that it even survived nine months without any water addition in our experimental setup (see Supplementary 1 online). This extreme drought tolerance is an important advantage for O. ficus-indica, as drought is frequent in the highlands of Eritrea53. The native species are expected to be adapted to what was the norm frequency and magnitude of drought, but climate change will result in stronger and more frequent drought events25, which will challenge their survival. Disturbance in the native vegetation due to drought might therefore create gaps with little to no interspecific competition in which the invasive species can spread even more rapidly16. Notably, O. ficus-indica was also able to survive very wet periods according to our pretrials. Even complete submergence of the pots for three months did not kill the plants but resulted in roots growing on the surface of the water, probably seeking oxygen access (see Supplementary 1 online). Besides ‘outproducing’ native species by high biomass production, these extreme tolerance limits are another potential explanation for the global invasion success of O. ficus-indica.
The two native species showed interesting differences in their response to competition by O. ficus-indica. R. communis increased its BNPP under interspecific competition with O. ficus-indica when stressed with water shortage (dry water regime). This is reflected in the competition index indicating facilitation for R. communis by O. ficus-indica (Fig. 2). Fighting against O. ficus-indica belowground, however, did not help its general case as it was still ‘outproduced’ by O. ficus-indica aboveground. The ANPP of O. ficus-indica in interspecific competition with R. communis is quite remarkable when taking the very low BNPP due to high interspecific competition into consideration. S. marginatum, on the other hand, appeared to give in to the interspecific competition by O. ficus-indica belowground, as it showed decreased BNPP compared to the intraspecific interaction. O. ficus-indica is able to produce about 10 times as much root biomass in the presence of S. marginatum than in the presence of R. communis. Still, S. marginatum was successful in competing with O. ficus-indica aboveground, where it showed low competition, especially under dry conditions. Fighting against O. ficus-indica aboveground, however, did not help its general case, as it was still ‘outproduced’ by O. ficus-indica aboveground. Potential explanations for the different behaviour of the native species in response to competition by O. ficus-indica might be that S. marginatum unlike R. communis is rather a drought-tolerant species that can better survive longer periods without water37. Anyhow, neither strategy appeared to be successful as both natives are clearly outperformed by O. ficus-indica in ANPP, irrespective of the water regime and despite them being superior competitors to O. ficus-indica.
A species successfully invading semiarid to arid ecosystems across the globe, O. ficus-indica, is an inferior competitor to two common and widespread native species. One of the natives, R. communis, successfully competed with O. ficus-indica belowground, and the other native, S. marginatum, showed superior competition mainly aboveground. This finding contradicts the common implicit interpretation that successful invasive species have overall advantageous traits that make them stronger competitors than native species. Being vastly more productive, even under interspecific competition, and considerably more stress tolerant than the native species appears more important than competitive power, at least for invasions in semiarid to arid, open vegetation. Stronger and more frequent disturbance of the native vegetation by drought due to climate change will further accelerate the success of O. ficus-indica, as it is extremely drought tolerant and produces considerably more biomass in the absence of interspecific competition.
Data availability
The datasets generated during and/or analysed during the current study are available from the corresponding author upon reasonable request.
Funding: YT received a scholarship from the German Academic Exchange Service (DAAD).
Competing Interests: The authors have no relevant financial or non-financial interests to disclose.
Author Contributions: YT and JK contributed to the study conception and design. Material preparation, data collection and analysis were performed by YT. The pretrial experiment, design, data collection and analysis were performed by AB. The first draft of the manuscript was written by YT and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Acknowledgements
We thank Ilka Beil and Andrey Malyshev for their helpful input and greenhouse assistance. Yohannes B. Tesfay was supported by the DFG research training group RESPONSE (RTG 2010) and a scholarship from the German Academic Exchange Service (DAAD).
1. Gioria, M. & Osborne, B. A. Resource competition in plant invasions: emerging patterns and research needs. Frontiers in plant science 5, 501; 10.3389/fpls.2014.00501 (2014).
2. Maron, J. L. & Marler, M. Field-based competitive impacts between invaders and natives at varying resource supply. Journal of Ecology 96, 1187–1197; 10.1111/j.1365-2745.2008.01440.x (2008).
3. Parker, I. M. & Reichard, S. H. Critical Issues in Invasion Biology for Conservation Science. In Conservation Biology, edited by P. L. Fiedler & P. M. Kareiva (Springer US, Boston, MA, 1998), pp. 283–305.
4. Weigelt, A. & Jolliffe, P. Indices of plant competition. Journal of Ecology 91, 707–720; 10.1046/j.1365-2745.2003.00805.x (2003).
5. Tesfay, Y. B. & Kreyling, J. The invasive Opuntia ficus-indica homogenizes native plant species compositions in the highlands of Eritrea. Biol Invasions 23, 433–442; 10.1007/s10530-020-02373-8 (2021).
6. Vilà, M., Williamson, M. & Lonsdale, M. Competition Experiments on Alien Weeds with Crops: Lessons for Measuring Plant Invasion Impact? Biol. Invasions 6, 59–69; 10.1023/b:binv.0000010122.77024.8a (2004).
7. Vilà, M. & Weiner, J. Are invasive plant species better competitors than native plant species? - evidence from pair-wise experiments. Oikos 105, 229–238; 10.1111/j.0030-1299.2004.12682.x (2004).
8. Roy. Biological invasions in Europe and the Mediterranean basin (1990).
9. Wilson, J. R. U. et al. Residence time and potential range: crucial considerations in modelling plant invasions. Diversity and Distributions 13, 11–22; 10.1111/j.1366-9516.2006.00302.x (2007).
10. Levine, J. M. et al. Mechanisms underlying the impacts of exotic plant invasions. Proceedings. Biological sciences 270, 775–781; 10.1098/rspb.2003.2327 (2003).
11. MacDougall, A. S. & Turkington, R. ARE INVASIVE SPECIES THE DRIVERS OR PASSENGERS OF CHANGE IN DEGRADED ECOSYSTEMS? Ecology 86, 42–55; 10.1890/04-0669 (2005).
12. Lonsdale, W. M. & Farrell, G. S. Testing the Effects on Mimosa pigra of a Biological Control Agent Neurostrota gunniella (Lepidoptera: Gracillaridae), Plant Competition and Fungi Under Field Conditions. Biocontrol Science and Technology 8, 485–500; 10.1080/09583159830009 (1998).
13. Müller-Schärer, H. The Impact of Root Herbivory as a Function of Plant Density and Competition: Survival, Growth and Fecundity of Centaurea maculosa in Field Plots. The Journal of Applied Ecology 28, 759; 10.2307/2404206 (1991).
14. Willis, A. J., Groves, R. H. & Ash, J. E. Interactions between Plant Competition and Herbivory on the Growth of Hypericum Species: a Comparison of Glasshouse and Field Results. Aust. J. Bot. 46, 707; 10.1071/BT97025 (1998).
15. Davis, M. A., Grime, J. P. & Thompson, K. Fluctuating resources in plant communities: a general theory of invasibility. Journal of Ecology 88, 528–534; 10.1046/j.1365-2745.2000.00473.x (2000).
16. Hughes, A. R., Byrnes, J. E., Kimbro, D. L. & Stachowicz, J. J. Reciprocal relationships and potential feedbacks between biodiversity and disturbance. Ecology Letters 10, 849–864; 10.1111/j.1461-0248.2007.01075.x (2007).
17. Brutsch, M. O. & Zimmermann, H. G. Control and utilization of wild opuntias. FAO Plant Production and Protection Paper, 155–166 (1995).
18. Obiri, J. F. Invasive plant species and their disaster-effects in dry tropical forests and rangelands of Kenya and Tanzania. Jàmbá: Journal of Disaster Risk Studies 3; 10.4102/jamba.v3i2.39 (2011).
19. Oduor, A. M. O., Long, H., Fandohan, A. B., Liu, J. & Yu, X. An invasive plant provides refuge to native plant species in an intensely grazed ecosystem. Biol Invasions 20, 2745–2751; 10.1007/s10530-018-1757-5 (2018).
20. Novoa, A., Le Roux, J. J., Robertson, M. P., Wilson, J. R. U. & Richardson, D. M. Introduced and invasive cactus species: a global review. AoB PLANTS 7; 10.1093/aobpla/plu078 (2015).
21. Jones, C. G., Lawton, J. H. & Shachak, M. Organisms as Ecosystem Engineers. Oikos 69, 373; 10.2307/3545850 (1994).
22. Shackleton, C. M. et al. Assessing the Effects of Invasive Alien Species on Rural Livelihoods: Case Examples and a Framework from South Africa. Hum Ecol 35, 113–127; 10.1007/s10745-006-9095-0 (2007).
23. Ali, N., Mounir, L. & Hichem, B. S. Cactus as a Tool to Mitigate Drought and to Combat Desertification. Journal of arid land studies 24, 121–124 (2014).
24. Luo, Y. & Nobel, P. S. Growth characteristics of newly initiated cladodes of Opuntia ficusindica as affected by shading, drought and elevated CO2. Physiol Plant 87, 467–474; 10.1111/j.1399-3054.1993.tb02495.x (1993).
25. IPCC. Climate Change 2022: Impacts, Adaptation, and Vulnerability. Contribution of Working Group II to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change ([H.-O. Pörtner, D.C. Roberts, M. Tignor, E.S. Poloczanska, K. Mintenbeck, A. Alegría, M. Craig, S. Langsdorf, S. Löschke, V. Möller, A. Okem, B. Rama (eds.)]. Cambridge University Press. Cambridge University Press, Cambridge, UK and New York, NY, USA, 3056 pp., doi:10.1017/9781009325844., 2022).
26. Goldberg, D. E. & Werner, P. A. Equivalence of competitors in plant communities: a null hypothesis and a field experimental approach. American Journal of Botany 70, 1098–1104; 10.1002/j.1537-2197.1983.tb07912.x (1983).
27. Goldberg, D. E., Rajaniemi, T., Gurevitch, J. & Stewart-Oaten, A. Equivalence of competitors in plant communities: a null hypothesis and a field experimental approach. Ecology 80, 1118–1131; 10.1890/0012-9658(1999)080[1118:EATQII]2.0.CO;2 (1999).
28. Grace, J. B. On the Measurement of Plant Competition Intensity. Ecology 76, 305–308; 10.2307/1940651 (1995).
29. Gurevitch, J., Morrow, L. L., Wallace, A. & Walsh, J. S. A Meta-Analysis of Competition in Field Experiments. The American Naturalist 140, 539–572; 10.1086/285428 (1992).
30. Adler, P. B. et al. Competition and coexistence in plant communities: intraspecific competition is stronger than interspecific competition. Ecology Letters 21, 1319–1329; 10.1111/ele.13098 (2018).
31. Chesson, P. Mechanisms of Maintenance of Species Diversity. Annu. Rev. Ecol. Syst. 31, 343–366; 10.1146/annurev.ecolsys.31.1.343 (2000).
32. Gimeno, I. & Vilà, M. Recruitment of two Opuntia species invading abandoned olive groves. Acta Oecologica 23, 239–246; 10.1016/S1146-609X(02)01143-8 (2002).
33. Nieddu, G. & Chessa, I. DIstribution of phenotypic characters within a seedling population from Opuntia ficus-indica. Acta Hortic., 37–44; 10.17660/ActaHortic.1997.438.4 (1997).
34. Gordon, D. R., Tancig, K. J., Onderdonk, D. A. & Gantz, C. A. Assessing the invasive potential of biofuel species proposed for Florida and the United States using the Australian Weed Risk Assessment. Biomass and Bioenergy 35, 74–79; 10.1016/j.biombioe.2010.08.029 (2011).
35. Zarai, Z. et al. Essential oil of the leaves of Ricinus communis L.: in vitro cytotoxicity and antimicrobial properties. Lipids in health and disease 11, 102; 10.1186/1476-511X-11-102 (2012).
36. Hedberg, I. (ed.). Flora of Ethiopia (National Herbarium [etc.], Addis Ababa [etc.], 2006).
37. Asefa, A. & Gashe, G. Role of native herbivores in the increasing abundance of Solanum marginatum L.F. (Solanaceae) in the northern Bale mountains, Ethiopia. SINET - Ethiop. J. Sci., 40, 74–87 (2017).
38. Fichtl, R. & Adi, A. Honeybee flora of Ethiopia (Margraf, Weikersheim, Germany, 1994).
39. Abebe, D., Debella, A. & Urga, K. Illustrated checklist, medicinal plants and other useful plants of Ethiopia (Ethiopian Health and Nutrition Research Institute, Addis Ababa, Ethiopia, 2003).
40. Williams, S. Bale Mountains: A Guide Book. Ethiopian Wolf Conservation Programme, Addis Ababa. (2002).
41. Aynekulu, E. et al. Plant diversity and regeneration in a disturbed isolated dry Afromontane forest in northern Ethiopia. Folia Geobot 51, 115–127; 10.1007/s12224-016-9247-y (2016).
42. Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. lmerTest Package: Tests in Linear Mixed Effects Models. J. Stat. Soft. 82; 10.18637/jss.v082.i13 (2017).
43. Lenth, R. _emmeans: Estimated Marginal Means, aka Least-Squares Means_. (<https://CRAN.R-project.org/package=emmeans>., 2022).
44. Markham, J. H. & Chanway, C. P. Measuring plant neighbour effects. Functional Ecology 10, 548–549 (1996).
45. Oksanen, L., Sammul, M. & Mägi, M. On the indices of plant-plant competition and their pitfalls. Oikos 112, 149–155; 10.1111/j.0030-1299.2006.13379.x (2006).
46. Faraway, J. J. Linear Models with R (Chapman and Hall/CRC, 2004).
47. Morales, M. sciplot: Scientific Graphing Functions for Factorial Designs (<https://CRAN.R-project.org/package=sciplot>., 2020).
48. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. (URL https://www.R-project.org/, 2022).
49. D'Antonio, C. Impacts and extent of biotic invasions in terrestrial ecosystems. Trends in Ecology & Evolution 17, 202–204; 10.1016/s0169-5347(02)02454-0 (2002).
50. Zheng, Y. et al. Are invasive plants more competitive than native conspecifics? Patterns vary with competitors. Scientific reports 5, 15622; 10.1038/srep15622 (2015).
51. Thomsen, M. A. & D'Antonio, C. M. Mechanisms of resistance to invasion in a California grassland: the roles of competitor identity, resource availability, and environmental gradients. Oikos 116, 17–30; 10.1111/j.2006.0030-1299.14929.x (2007).
52. La Barrera, E. de & Nobel, P. S. Carbon and water relations for developing fruits of Opuntia ficus-indica (L.) Miller, including effects of drought and gibberellic acid. Journal of experimental botany 55, 719–729; 10.1093/jxb/erh084 (2004).
53. Funk, C. et al. The Centennial Trends Greater Horn of Africa precipitation dataset. Scientific data 2, 150050; 10.1038/sdata.2015.50 (2015).