Considered together, our results indicate rapid competitive exclusion and displacement of the endemic Cyperus atlanticus by the pantropical Guilandina bonduc and suggests that competition for water might be a preeminent mechanism. First, over time Guilandina patches expanded simultaneously with bare soil zones that surround the patches, while Cyperus surrounding the halos contracted. These rapid changes in distributions corresponded with large roots of Guilandina extending into bare soil zones and under Cyperus, and the presence of Guilandina fine roots beneath bare soil zones and living Cyperus stands. In turn, soil water potentials were much lower in bare soils than in soils under Guilandina or Cyperus, and the water potentials of individual Cyperus plants were much lower when co-occurring with Guilandina than when alone. Finally, when aboveground biomass of Guilandina was removed experimentally, bare soil zones contracted and were replaced to a large degree by Cyperus. As Guilandina grew back, the cover of both bare soils and Cyperus zones decreased. We propose a scenario in which Guilandina establishes, expands its roots systems beyond its canopies, these roots dry soils beneath Cyperus which kills it, and then Guilandina expands and repeats the process.
Our evidence for competition for water is somewhat unusual in a tropical environment, and perhaps more so when the lowest water potentials measured for Cyperus leaves in competition were roughly − 1.2 MPa, levels which would not create stress for most plant species. First, it is important to note that our measurement of leaf and soil water potential were taken during an exceptionally wet time, and it is likely that in drier periods Guilandina may have decreased Cyperus water potentials much more than we measured. However, Cyperus species also appear to require unusually wet substrates and even small decreases in water potential might damage them. Most species in the genus are aquatic, and Rodiyati et al. (2005) found that Cyperus brevifolius and Cyperus kyllingia grew better in soils that were either maintained at 37% (field capacity) or 69% (flooded) water than soils at 14% water. Jones and Murthuri (1984) found diurnal patterns of Cyperus papyrus water potential reached a mid-day minimum of -1.5 MPa. If C. atlanticus requires exceptionally wet conditions, such as other Cyperus species, the water potentials we recorded for Cyperus when growing with Guilandina could be inhibitory.
The strongest evidence for competition for water, in general, is the removal of competitors from around targets in the field, and then a response by the target that includes both improved water relations and metrics that relate to fitness (e.g., Ehleringer 1984, Callaway et al. 1996). We used removal experiments to show that Guilandina excluded Cyperus, but our evidence for exclusion via competition for water is based on correlations between the presence of roots, spatial variation in soil water potentials, and a correlation between reduced Cyperus water potential in the presence of Guilandina.
Previous reports raised the possibility that the displacement of Cyperus by Guilandina could result from an allelopathic interaction (Carvalho-Silva et al 2013). Indeed, the striking halos of bare soil around Guilandina shrubs and halos of dead and dying Cyperus are similar or even starker than patterns described for other species connected to allelopathy (Hierro and Callaway 2021). Much like in our case, Polygonella myriophylla is a shrubby perennial endemic to Florida with distinct bare zones surrounding aboveground patches (Weidenhamer and Romeo 1989). They conducted bioassays with soils collected from beneath Polygonella, bare zones, and surrounding vegetated areas and found that germination and seedling growth of grasses were suppressed in Polygonella and bare zone soil relative to soil from beneath other more distant species. However, in contrast with this study, our bioassays showed that soil from directly beneath the canopies of Guilandina had strongly positive effects on Cyperus biomass, relative to soil from the bare and Cyperus zones.
Plants with nitrogen-fixing microbial mutualists commonly improve available soil nitrogen (Callaway 2007), and it might be that effects of soil directly beneath the canopies of the nitrogen-fixing Guilandina canopies, once removed from the complex effects of living roots, were unmasked in the controlled bioassays (see Callaway et al. 1991). Also, bulk effects of soil in bioassays might not reflect the effects of Guilandina roots on Cyperus roots in situ (see Schenk 2006). In other words, Guilandina roots might have had contact-based inhibitory effects on Cyperus that are not detectable in bulk soil (Mahall and Callaway 1991). As potentially allelopathic chemicals can rapidly attenuate in natural soil and in the time between soil collection and the bioassay (Inderjit et al. 2011), the allelopathic effects of Guilandina is still a possible mechanism. However, considering that both species coexist side by side at Site 1 with no noticeable effect on each other, this could hold only for Sites 2, 3 and 4. Overall, considering that the soil beneath Guilandina patches were stimulatory to Cyperus, potential allelopathic interaction behind the exclusion of Cyperus by Guilandina (Carvalho-Silva et al. 2013), was not supported by our studies.
Nutrient competition could also be a possible mechanism behind the exclusion of Cyperus by Guilandina. However, our soil analysis showed that, in general, the sites showed similar soil nutrient contents. The most striking differences were found in organic matter and carbon content, higher at the Site 1 in comparison to the other three sites. The analysis also revealed a very high CEC values for all sites, and a high saturation of the bases H+ and Al+ 3 at the Site 1. At the Sites 2, 3 and 4, the samples revealed a soil less acidic and with a base saturation ranging from 78 to 92%, indicating a high availability of nutrients for plants. Overall, our analyses corroborate previous studies showing that soils occurring at both top hills and lower slopes of Trindade island are fertile (Clemente et al. 2009). Taking together, these results suggest that variations in soil characteristics as texture, nutrient content and pH would not be enough to explain the interaction between Guilandina and Cyperus, the rapid responses of Cyperus in the removal experiment, and the variation in their ranges associated to rainfall. These results indicate that the expansion/retraction dynamics of the halos at the lower slopes of the island might not be associated to soil nutrient variability and/or nutrient competition.
A puzzling pattern in our results is that the highest biomass of Guilandina roots occurred under Guilandina, where water potentials were relatively high. In contrast, water potentials were far lower in bare soil zones where Guilandina roots were 4–5 times less abundant than under Guilandina. If the spread of Guilandina roots into bare soil zones and Cyperus stands is important for extracting water from soils and ultimately eliminating Cyperus, then why were soils under Guilandina so wet? It is possible that the shrubby canopies of Guilandina shaded soils and decreased vapor pressure deficit (VPD) at the soil surface. Thus, the loss of vegetation cover exposed the bare soil to direct solar heating and excessive drying, but this would be inconsistent with competition for water being the cause of the exclusion of Cyperus. Soil water differences cannot be attributed to soil texture, as texture was very similar across zones in each site. It is also possible that hydraulic redistribution, which can occur in the wet tropics (Oliveira et al. 2005) and seasonal tropics (Scholz et al. 2002), moved water from deep soils to shallow subcanopy soils. However, why redistributed water would not flow through roots to soils with the lowest water potential, the bare zones, is not clear.
The climate of Trindade Island is tropical, is classified as wet, and without a true dry season, but there are several reasons why our results might not extend to typical wet tropical systems. First, precipitation can be much higher in other tropical regions and perhaps results such as ours could not be obtained in much wetter climates. Second, interactions in many, if not most, tropical communities involve far more species, and the very low diversity of our study system may have yielded results that are inherently different than those that would occur in more diverse assemblages. On the other hand, the simplicity of species-poor communities has allowed experimental investigation of competition for water in other biomes, thus simple communities may provide opportunities to understand interactions more clearly than in more complex communities (Fonteyn and Mahall 1978; Ehleringer 1984). Indeed, our studies might be extended to either tropical regions subjected to water seasonality, as savannas, or dry regions where water availability can limit plant growth.
The patterns of zones and soil water potentials we describe may provide the first empirical evidence, although incomplete, for the theoretically derived “root-augmentation feedback” mechanism for self-organized vegetation pattern formation, well represented in model studies (Meron 2012). In this scenario, a plant extends roots beyond its canopy, extracts water from these distal areas, and forms relatively mesic subcanopy soils and relatively xeric soil surrounding the canopy. Over time, such feedbacks polarize these mesic and xeric microhabitats further, which can lead to strong spatial heterogeneity in vegetation patterning. Interestingly, model studies have focused on arid ecosystems, thus if Guilandina is driving root-augmentation feedback, it is doing so at much higher precipitation levels than models predict (see Gilad et al. 2007), suggesting that it may not only be applied to arid systems, but also to relatively wet systems with temporary dry periods or water shortage.
So, taking into consideration the potential variation in microclimate over much of the Trindade territory, we found competitive exclusion in the tropics, apparently via competition for water. While we demonstrated competitive exclusion experimentally, our evidence for competition for water is circumstantial – based on field recordings as soil water availability, dynamics of the zones and on a physiological trait (leaf water potential). With that caveat our results suggest that competition for water might be important in other relatively wet tropical communities, especially if the stronger competitor can drive soil water potential below that tolerated by neighbors. This has been shown in semi-arid systems (Callaway et al. 1996) and suggests important avenues of study in wetter systems, where intense competition is theoretically important (Dobzhansky 1950, MacArthur 1969; Bertness and Callaway 1994) and empirically demonstrated among dominant plant species (Uriarte et al. 2018; Yang et al. 2021; Weng et al. 2022). However, this empirical evidence is predominantly based on demographic correlations, thus future experimentation holds a great deal of promise.