Our overall results suggest that the direction and intensity of interactions among annual plants depend not only on habitat productivity but even more so on the life stage at which a plant is observed. In general, the interaction type shifted from facilitation or neutral net interactions towards intensive competition with increasing productivity and time.
competition dominates in high-productive habitats, independent of the plants’life stage
Most previous discussions about the importance of accounting for life-history stages in competition experiments have been motivated by the so-called Grime-Tilman (Newman) debate. This debate stems from the unresolved question of whether competition intensity increases with increasing habitat productivity (Grime 1973, 1979; Huston 1979; Keddy 1990) or stays constant (Newman 1973; Tilman et al. 1982). As empirical work has supported both views equally, many efforts have been made to explain the contradictory findings. One such explanatory hypothesis claims that the use of different response variables may lead to opposing results, e.g. the response of mortality to the presence of neighbours might change with productivity while the response of growth stays constant (Goldberg & Novoplansky 1997). We can now evaluate whether our experiment would have yielded differential support to either of Grime's or Tilman's views, depending on the life stage under consideration.
On average, our findings indicate facilitative or neutral interactions at the drier end of the gradient and increasingly negative interactions with increasing rainfall. With one exception (juvenile weight of B. didyma), competition was more intense in the two wetter sites (Matta and Ein Ya’acov) compared with the semi-arid site (Lahav), for both species in all life stages (Fig. 2). As productivity at our sites increases strongly with rainfall, this pattern corroborates the model of Bertness & Callaway (1994) and between-site differences for RII values were similar for all response variables, irrespective of life-history stage. Therefore, the time at which interactions among plants are studied does not necessarily affect the qualitative outcome of experiments designed to test for the effect of interaction with the environment on relationships.
interaction intensity shifted from slightly positive to strongly negative over time
Our overall results show clearly that there were differences between life stages in direction and intensity of interactions. Intriguingly, these differences did not vary randomly across the plants’ life cycle but exhibited a consistent trend through time: RII shifted from positive or neutral at early life stages towards extremely negative values at the time of seed production.
Several reasons for the shift from facilitation to competition have been discussed before. For example, Goldberg et al. (2001) observed in a study on desert annuals that negative density dependence was most intense at the germination stage. Seedling density and total standing crop were therefore low, resulting in less frequent negative interactions at early stages of the growth of the vegetation. However, in our case, density-dependent germination is unlikely to explain the positive neighbour effects at the seedling stage, as seed germination of B. didyma is markedly accelerated in the presence of seeds of other species (K. Tielbörger, unpublished results), suggesting that facilitation is critical even at the earliest life stages.
Other hypotheses concerning changes in interaction type and strength with time suggest that seedlings might be more sensitive to harsh conditions than to competition. Therefore, at this stage, both importance and intensity of competition (Brooker et al. 2005) may be low and the effect of neighbours predominantly positive. For example, bigger plants may facilitate seedlings by non-trophic effects, such as reduction of temperature and evapotranspiration (Callaway et al. 1995; Holmgren et al. 1997), particularly in water-limited systems such as ours. As there is no apparent reason why positive interactions (e.g. via shading) should become less intense at later life stages, the increasingly negative RII values during development can only be explained by more intense competition. The most straightforward explanation may be that increasing standing crop (i.e. growth of the plants) leads to an elevated demand for resources and thus greater competition. This idea is consistent with the hypothesis that exploitation competition is the primary mechanism underlying growth patterns (Goldberg et al. 2001).
Despite the general trend of increasingly negative density dependence along the gradient and across life stages, plant survival always responded either positively or not at all to the presence of neighbours. As with other variables, survival was more positively affected by neighbours in seedlings than in adults, but both showed markedly different values from those for juvenile weight, number of seeds and adult weight.
For two reasons, interpretation of our findings should explicitly take into account the fact that both species we used are annuals. First, such ‘within life-form’ interactions may be more likely to be negative than, for example, the effect of shrubs on annual vegetation (Callaway 1995; Holmgren et al. 1997), as plants interact at similar life stages. This may be an explanation for why we detected facilitative effects rather rarely. However, our main hypothesis, i.e. a directional shift in interaction intensity through time, can be tested irrespective of the presence of positive interactions.
A more important limitation of our study system may be that annual plants follow strategies that are different from those of perennial plants. For instance, their short life cycles, and the variable environment of sites such as ours, mean that annuals invest much more into reproduction than into growth (Petrůet al. 2006) and clonal growth or retrogression does not occur at all. Another important difference is that annuals survive the most stressful periods (summer drought at our site) in the form of seeds and we cannot therefore observe neighbour effects in the season where positive interactions are most likely to occur. In coexisting perennial species, such facilitative interactions may repeatedly occur throughout the life cycle. Therefore, while annual plants are a simple and useful system to investigate directional shifts in plant–plant interactions throughout a complete life cycle, future studies with perennial plants are needed to test the generality of our findings.