|Contributing Authors:||Sonia Kéfi, Florian Schneider, Angeles G. Mayor, Alain Danet, Marina Rillo, Simon Benateau, Jacob Keizer, Ana Vasques, Susana Bautista, Paco Rodriguez, Alejandro Valdecantos, Jaime Baeza, Ramón Vallejo, Max Rietkerk, Mara Baudena, Mart Verwijmeren, Koen Siteur, Rubén Díaz-Sierra|
|Source document:||S. Kéfi, A. Vasques, F. Schneider, M. Rietkerk, A.G. Mayor, M. Verwijmeren, R. Diaz-Sierra and M. Baudena. 2016. Response of Mediterranean drylands to increasing pressures. CASCADE Project Deliverable 6.1, 54 pp
Facilitation between plants is known to be an important mechanism driving vegetation patchiness [12,102,110], but we lack understanding of how interactions between plants change in response to combined effects of drought and consumer pressure – the main stressors in many arid ecosystems.
In semi-arid ecosystems, shrubs, trees and annual plant species compete for water, which is considered the main growth-limiting resource. Shrubs, however, often also provide positive (i.e. facilitative) effects by relieving drought stress for less drought-tolerant neighbouring plants, for example by shading or by increasing water availability (via increased infiltration) within their direct vicinity . Shrubs can also lower grazing pressure by protecting neighbouring individuals against herbivore damage, a process known as associational resistance . The total net effect of one plant (nurse plant) on the other plant (protégée plant) is a trade-off between competitive and facilitative effects, and a crucial question to be answered is how a combination of different stressors (e.g. drought and grazing) influences the direction and strength of plant-plant interactions in dryland ecosystems  .
Early conceptual models of plant-plant interactions hypothesized that the net outcome of plant–plant interactions shifts from competition towards facilitation with increasing drought stress or grazing pressure [15,114]. Recent meta-analyses indeed showed that at the global scale a shift towards more facilitative plant–plant interactions is observed as stress levels increase [115,116]. However, recent studies question if positive species interactions can be expected under very severe drought stress , as competitive effects may become more intense during severe dry periods. In addition, studies from grazed ecosystems show that under severe grazing stress, plant-plant interaction wane from facilitation to neutral, as plants that provide benefits for neighbours lose their ability to do so under very high grazing pressure [118,119]. Very few studies have empirically tested the impact of combined effects of drought and grazing (but see [120,121]), and changes in plant-plant interactions along combined stress gradients are still not well understood .
Previous ecohydrological models investigated the balance between positive and negative interactions between two plant species [10,100], by modelling the competitive water uptake by plants in combination with an increased infiltration of water in the soil due to increased biomass. These studies assessed which factors tilt the balance between the facilitative and competitive effects along a drought gradient. However, it has not yet been studied with mechanistic models how the joint effects of grazing and drought - highly realistic in (semi-) arid ecosystems - shape the net interactions between plants.
1. Effect of rainfall intermittency and grazing on plant coexistence
To study how the combination of drought and grazing gradients affects plant-plant interactions, and thus community composition and stability, we extended the model previously described in »Dryland response to changes in rainfall intermittency , where two plant species differed in their water and drought functional traits. For the first time, a study of plant-plant interactions represented rainfall as highly intermittent, i.e. it catches the fact that rainfall in drylands occurs in pulses . In this model, the drought resistant species was also an unpalatable nurse species, which protected the palatable protégée species from grazing damage (facilitation via grazing protection). The protégée species had a higher optimal growth rate when soil water content was higher. The two species compete for water, but also one species facilitates the other via grazing protection. This modelling work was based on the plant-plant dynamics studied within a field experiment, located in the UA CASCADE site of Santomera, Spain  (in the same way as the study in »Dryland response to changes in rainfall intermittency). The experiment also provided part of the parameters for the model.
To study the interacting effects of annual rainfall amount, rainfall intermittency and grazing on plant coexistence and on the competitive or facilitative effects of a nurse species on a protégée species, we developed a mechanistic two-species-model coupled to a hydrological model of a single soil layer. The model describes the coupled dynamics of vegetation and soil moisture, and it is a combination and extension of the models presented by Baudena et al. (2007), Laio et al. (2001) and Díaz-Sierra et al. (2010) [91,100,124]. We used a one-layer bucket model, because in our field site we observed relatively shallow soil depths (20-30 cm) accessible for the root systems of both plant types (personal observation). The system dynamics was modelled by using three coupled ordinary differential equations (ODEs), for the soil water (s) dynamics, and for the nurse (N) and the protégée (P) plant growth dynamics.
Water input in the model consisted of stochastic rainfall events based on statistics of historical data for the yearly amount and timing of rainfall. Rainfall was modelled as stochastic Poisson events, with exponential distributions for inter-arrival time (i.e. time in between rainfall events), and for mean daily rainfall intensity (calculated from the mean annual rainfall) . We also included a dry season without any rain, occurring once every year, to simulate the summer dry season that is characteristic for the climate of the field site. We calculated realistic values for mean annual rainfall, rainfall inter-arrival time and length of drought season, based on 72 years of rainfall records for the Alcantarilla weather station nearby our field site (Agencia Estatal de Meteorología, AEMET). We varied rainfall mean annual values and intermittency values in subsequent model runs, with a higher intermittency resulting in higher rainfall inter-arrival time and thus also increased mean daily rainfall intensity.
Based on previous models [97,100], plant growth was modelled as proportional to transpiration, a function of the soil water content, with a proportionality constant that would determine the maximum growth rate. The ‘nurse’ species (N) suffered a baseline mortality rate but did not suffer a grazing mortality. The second plant type, the ‘protégée’ species (P) also suffered a baseline mortality on top of which a grazing mortality was implemented. The biomass removal per year was proportional to its own biomass with grazing rate.
Grazing damage was reduced by a function depending on the ratio of nurse biomass over protégée biomass. The nurse species decreased the amount of grazing-induced mortality for the protégé species. We followed the approach by Gross , but while that model uses the grazing protection as a function of the neighboring species alone, we choose to model grazing protection as a function of the ratio of nurse biomass over protégé biomass to account for size dependence (a small nurse plant cannot protect a larger protégé plant). Grazing protection was modelled using a Holling type III function, where the ratio of the nurse biomass over the protégé biomass determined the amount of reduction in grazing mortality.
Our two distinct plant functional types, nurse (N) and protégée (P), are woody perennial species that were selected in a parallel experiment in which plant growth of protected and unprotected planted saplings of Anthyllis cytisoides was monitored . In line with this experiment, performed in the CASCADE site of Santomera (Spain) we used Artemisia herba-alba as nurse plant in this study and modelled its growth. Artemisia spp. is not preferred by goats and has been found to be spatially associated with A. cytisoides in previous studies . Also in line with field observations and parallel experiments, we used Anthyllis cytisoides as protégé species in our model. A. cytisoides is a drought-deciduous shrub from the Fabacaea family, and it is highly palatable for both goat and rabbits. A. cytisoides has been found to constitute 41 % of livestock goat diet and is thus considered as highly preferred food source for goats .
In the default parameter setting, the two species are characterised by a trade-off: although A. herba-alba has the benefit of being able to grow under lower soil moisture levels because of its lower wilting point, A. cytisoides has a higher growth rate under more benign moist conditions. A similar trade-off between drought tolerance and optimal growth rate has been reported in several studies in dryland ecosystems and has been proposed as a possible mechanisms promoting plant coexistence .
Biomass of nurse and protégée species and the competitive outcome were heavily dependent on the rainfall intermittency, annual rainfall amount and grazing rate variations (Figure 1). We did not find any effects of varying the initial conditions of nurse or protégée biomass on the final biomass values, implying that the modeled system did not display any multistability. In other words, there is no possible catastrophic shift in this model, probably as a consequence of the fact that the model does not represent the spatial dynamic of plant growth and of grazing (as opposed to the model of Schneider et al.  presented in »Dryland responses to grazing and droughts).
We show that under increasing grazing pressure, species can coexist thanks to grazing protection under current rainfall amount and intermittency scenario. In the low intermittency scenario (Figure 1, left panel), the nurse species biomass is constant over the grazing gradient, as grazing does not affect it and the protégée is fully outcompeted. The protégée without a nurse can persist when being grazed, but only for high rainfall values or low grazing rates (see Figure 1, dashed line in the panels of the bottom row or the right end of each panel). The protégée without a nurse can only obtain biomass values higher than the nurse under ungrazed conditions. Under current rainfall conditions (300 mm/y and inter-arrival time between events IM=8, Figure 12, central panel), high grazing would lead to protégée extinction, but the protection of the nurse allows for the protégée species to survive.
Moreover, we show that grazing results in increased facilitation of the nurse on the protégée, but only under current or higher intermittency conditions, and with an increasing relevance of facilitation with rainfall (Figure 2). This means that an increase in rainfall intermittency (leading to longer drought periods) or in grazing pressure will result in more facilitative interactions between plants. We also found that competitive interactions may become prevalent with drought stress. To quantify plant interactions, and their positive and negative net effects, we use two new indices (NIntA and NImpA), which we mathematical formulated from the classical concept of intensity and importance, respectively  (see Table 1).
This model suggests that the relative importance of facilitative vs competitive plant-plant interactions varies along stress gradients, thus determining the possibility for species coexistence and may affect ecosystem functioning. This information is crucial to obtain a better insight into the long-term co-existence of species in semi-arid ecosystems in response to future climate change.
2. Effect of biotic and abiotic facilitation on plant coexistence along drought and grazing gradients
Following up on the results of the effect of rainfall intermittency and grazing on plant coexistence reported in Section1. above, obtained for a specific system and a given set of species, we explored the generality of these results, and included, besides grazing protection, facilitation due to the effect of plants on soil water content, which is a very relevant mechanism in drylands [8,102]. We therefore developed a model to study theoretically the role of plant interactions along drought and grazing gradients for the resilience of dryland ecosystems .
We modified an existing model including two plants, light and soil moisture , in a similar way as in the Section 1 (). In the present model, the nurse plant can have two separate positive effects on the protégée: i) increasing water infiltration (abiotic facilitation) and ii) protecting from grazing (biotic facilitation). Soil water and light availability are modelled explicitly, and so are water and light competition between the two plant types. In this model, the nurse species is not assumed to be limited by water, but instead we assume that it is limited by light availability , which provides a coexistence mechanism for the two species, and allows a simple comparison of the two positive effects. We also simplified the model in Section 1  to assure analytical tractability in two main ways: a) the rainfall is modelled as constant; b) plant transpiration functions are modelled as differential functions of the soil moisture content and light availability, respectively. We also modified the model to fully analyze the effect of positive interactions of the nurse on the protégée. First, we considered that the protégée may not have any positive effect on the soil water, i.e. it did not increase infiltration. This assumption allows us to study separately the effects of the two different types of facilitation included in this model. Second, we introduced a limit to the maximum grazing protection that the nurse can provide. In the previous model (), the nurse fully prevented grazing, when its biomass was a number of times higher than the one of the protégée. We decreased this values to simulate partial grazing protection even at large densities of the nurse.
For the parameters that are shared with the previous model () we used the values previously deduced, except for the maximum water uptake of the nurse, which was cut by half to satisfy the classical criteria for nurse and protégé coexistence even for small positive interactions (the nurse species should consume less of the resource that limits the growth of the protégée, i.e. water, [100,129]). For the parameters involved in the nurse light absorption growth we proposed a set of tentative values, which allowed species coexistence and the analysis of net facilitative and competitive effects along the same environmental gradients.
Our analysis shows that facilitative mechanisms affect coexistence (Figure 3-4 a, b). The more the nurse species either increases water infiltration (Figure 3 a, b) or protects the protégée from grazing (Figure 4 a, b), the larger the range of annual rainfall values or grazing pressure values, respectively, where coexistence of the two species is observed. In details, when rainfall decreases, the protégée equilibrium biomass decreases, and a nurse species that increases soil water infiltration can invade while previously excluded. Because the nurse species is drought tolerant (and provided they satisfy a classical criteria of water to light consumption, [100,129]), the two species will coexist (Figure 3 a,b). Along a grazing gradient, the less competitive nurse species can invade when grazing increases. Since the invading species can protect the established species from grazing, the two species coexist at equilibrium (Figure 4 a, b).
We also quantified the net effect of the facilitative and competitive interactions along the two stress gradients, showing that the type of shifts between competition and facilitation along a stress gradient depends on the specific interaction mechanisms and on their intensity (Figure 3 c, d, 4 c, d).
We conclude from this model analysis that it is not possible to find a unique trend in the facilitation/competition curves, as expected from the stress-gradient hypothesis, in its original or revised forms, which postulated that facilitation would be most relevant at high or intermediate level of stress. Our results show that the intensity and the net effect of the mechanisms leading to facilitation or competition can change depending on several factors.
3. Effect of biotic and abiotic facilitation on ecosystem resilience
The models presented in Sections 1. and 2. above studied the role of grazing protection from a nurse on species coexistence and on plant-plant interactions along stress gradients, but these models did not exhibit catastrophic shifts (in the parameter range analyzed). To follow up on these studies, we built on the model presented in »Dryland response to grazing and droughts which includes both grazing protection (i.e. biotic facilitation) and abiotic facilitation, but also exhibits catastrophic transitions to desertification .
Along a gradient of grazing intensity, the model shows that at low grazing intensity, only the protégée maintains itself in the system because it is more competitive than the nurse (Figure 5 left). Coexistence between both species is possible at intermediate grazing intensities. Above a threshold of grazing pressure, only the nurse can maintain itself because of its adaptation against grazing. This threshold of grazing pressure decreases as aridity increases, therefore favoring the nurse species at higher aridity levels. This succession of species along a grazing gradient matches field observations [131–133].
Moreover, studying the ecosystem response to increasing aridity shows that the system exhibits a high vegetation cover which decreases as aridity increases until a threshold is reaches at which the vegetation cover collapses to desert in catastrophic way (i.e. with hysteresis and bistability). Including the two species and the mechanism of indirect facilitation makes this schema more complex: before the extinction of the vegetation, there is a zone of coexistence which is tristable: desert is stable, the coexistence happens along a degradation path and the nurse alone maintains itself in case of regeneration.
This model with only two species shows how including different species and different strategies can affect the resilience of the ecosystems and more specifically transform the typical catastrophic shift curve into a more complex situation with practical implications of ecosystem restoration.
4. Effect of facilitation and climate shifts on plant coexistence
The previous sections have investigated how plant-plant interactions could contribute to coexistence of different plant species and functional groups along stress gradients in drylands. The studies, however, did not address the question of the origin of the different species and functional groups currently present in drylands.
The present semi-arid Mediterranean climate arose about 3 Mya, when there was a climatic change from the wet Tertiary to the dry Quaternary period. Today, the Mediterranean basin vegetation can be grouped into two contrasting trait-syndromes, the old Tertiary trait-syndrome and the modern Quaternary trait-syndrome which have contrasting traits but coexist in the region . The tertiary trait-syndrome appeared in the region before the establishment of the more arid Mediterranean climate (3 Mya) and is known to be less drought-tolerant than the Quaternary trait-syndrome. In spite of this climatic change, most Tertiary species did not disappear from the region, but remained relatively abundant, coexisting with the more drought-tolerant Quaternary species. Empirical studies have shown that the Quaternary plants often serve as nurse plants which provide a suitable local environment for the Tertiary plants allowing them to persist in such an environment . A hypothesis is therefore that facilitation between plants can act as an evolutionary force, by creating dynamical spatial heterogeneity in the environment and therefore allowing divergent adaptation to happen.
This model is an interaction particle system, which is an extension of previous models [11,25,130], including those presented in »Dryland response to grazing and droughts and Section 3 above. In the model, individual plants improve their local neighboring environment, providing better conditions for seed germination and seedling survival (a.k.a. early survival) of other plants, thus mimicking the locally improved supply with water and organic matter observed in drylands (abiotic facilitation). We defined early survival of the plants as a function of local environmental quality, a simplified representation of soil quality and water availability at a particular location. Early survival here combines a number of morphological and physiological traits that lead to higher tolerance to drought and represents the different trait-syndromes. During a plant’s reproduction in the landscape, the offspring will either inherit its parental early survival trait or undergo a mutation that results in a random displacement from the parental phenotype. This way, individuals could adapt to drier environmental conditions at the cost of a shorter lifespan.
We ran numerical simulations of the model following the fate of mutants with different early survival rates in the plant population. We investigated the environmental conditions (arid vs. humid) that resulted in the evolution of either of the trait syndromes [136,137]. Finally, we investigated under which conditions the facilitative effects of the Quaternary plants enable ecological coexistence of the two functional groups.
We found that local facilitation increased the diversity of traits in the system along phenotypic evolution. It allowed the coexistence of drought-tolerant and drought-sensitive traits under dry environmental conditions such as the ones observed today in the Mediterranean region. This suggests that local facilitation can act as a selective pressure which favors non drought-adapted phenotypes, by promoting spatial environmental heterogeneity. After a period of climatic change from wet to dry conditions, facilitation was responsible for the maintenance of the Tertiary-like trait in the lattice (Figure 6); without facilitation only the Quaternary trait persisted, with no other coexisting ecotype. Thus facilitation could have been a mechanism by which the Tertiary plants persisted within the current Mediterranean climate, while adaptation to the semi-arid climate occurred.
Our work offers a new perspective on the importance of positive interactions for the maintenance of diversity through evolutionary time.
5. Effect of demographic noise on dryland response to stress
Model studies of drylands ecosystems often discard the individual nature and stochastic behavior of plants. These may give rise to demographic noise, which in certain cases can influence the qualitative dynamics of ecosystem models, such as the stability and resilience of the final states. To improve this aspect, we introduced a spatial stochastic hybrid model of a semi-arid ecosystem, in which plants are modeled as discrete entities subject to stochastic dynamical rules, while the dynamics of surface and soil water are described by continuous variables .
We show that demographic noise can have important effects on estimating the extinction and recovery dynamics of the ecosystem from models. In particular, we find that including the individual dynamics and its stochasticity, vegetation escapes extinction under a wide range of conditions for which the corresponding deterministic model predicts desert as the stable system state (See an example run in Figure 7). This is an important observation, given that semi-arid ecosystems are characterized by a rather scarce number of plants, scattered across regions of empty land. Intuitively, the demographic stochasticity is expected to promote extinction when the number of plants is small. It is therefore remarkable that we observed a relevant regime of parameters in which including the stochastic individual nature of the plants actually increased the likelihood of vegetation pattern emergence, and of escaping the desert state.
This investigation indicated that, in certain regimes, including demographic noise, and thus the individual nature of plants, could lead to a better (and larger) estimate of the resilience of semi-arid ecosystems. The study of semi-arid ecosystems might therefore benefit from the use of individual based models.
Note: For full references to papers quoted in this article see