Ectomycorrhizas and mast fruiting in trees: linked by climate-driven tree resources?

Until recently, an almost entirely overlooked aspect of tree phenology has been the likely role of ectomycorrhizas (EM) in the mast fruiting. The positive association between EM and masting appears not to be strictly universal at the genus and family level (Alexander & Högberg, 1986; Newman & Reddell, 1987), but nevertheless it is certainly striking enough to raise the important questions: does mast fruiting depend on EM symbiosis and, if so, how does the link function, and under what conditions? Mast fruiting refers to a distinct supra-annual pattern in fruiting and seedling, evidenced in most cases by large peak years separated by no or very little activity (Herrera et al., 1998; Kelly & Sork, 2002). There are many well-documented examples of mast fruiting among strongly EM tree families, such as Pinaceae, Fagaceae and Betulaceae in the temperates, and likewise for certain prominent families in the tropics, such as Dipterocarpaceae in South-east Asia and Caesalpiniaceae (Leguminosae) in Central Africa and northern South America. The Rosaceae interestingly also contain many horticultural species which show alternate-bearing, a phenological pattern with the shortest possible between-fruiting interval of 1 yr. Mast fruiting can be generally viewed as an extension of this basic pattern with increasing and varying intervals between fruiting events. The EM–masting connection calls for interpetation in terms of a resource model for tree growth and reproduction, and for experimental and field observational testing. For the present, however, we have a rather small number of isolated yet telling cases that are pointing in an exciting direction. The paper by Henkel, Mayor & Woolley (pp. 543–556) in this issue makes a valuable contribution in this problem area, not only by highlighting a new example of masting in a tropical EM species but also by coupling this phenomenon to ideas about climate-driven tree resources.

‘The process of mast fruiting in trees has to be maintained by a tree physiological mechanism, and the search is now on to discover and understand this’

It has been commonly supposed since Büsgen and Münch (1929), but not unequivocally demonstrated, that large trees need to build up resources to a sufficiently high level in order to trigger flowering and to enable high fruit and seed production. The most well-known case in Europe is Fagus sylvatica L., for which there are several sets of long-term phenological observations (e.g. Piovesan & Adams, 2001). Large trees sustain considerable nonphotosynthesizing biomass in terms of primarily stem and branch wood, roots and mycorrhizas, and this creates a large respiratory load. Further, in a masting year, dry matter allocation can be upward of half of the annual leaf production (Green & Newbery, 2002), and this presumably creates a strong additional temporary sink for tree carbohydrates and nutrients. Accumulation of resources in the intermast interval, enhanced in years of raised radiation [due to El Niño/Southern Oscillation (ENSO) years, for example], will likely increase carbohydrate concentrations in the tree, but these need to be complemented by increased nutrient concentrations. EM may therefore play a role here and in contrast to vesicular–arbuscular mycorrhized trees they may be able to store nutrients, especially phosphorus (P), for later use in fruiting. It is widely agreed that the ultimate cause of masting in trees is avoidance of predators and pathogens: strong, even irregularly spaced pulses of seed and seedling input to the population lead to satiation and increased survival (Janzen, 1974, and the recent study of Curran & Leighton, 2000). However, this process has to be maintained by a tree physiological mechanism, and this is where the search is being renewed.

Physiological control and climatic variables

Henkel et al. report on masting in a large tropical ectomycorrhizal tree species in the Caesalpiniaceae, Dicymbe corymbosa Spruce ex Benth., which locally dominates stands of lowland rain forest on the Guianan Shield in South America. It is closely related taxonomically to other genera within the tribe Amherstieae in Central Africa and shares many characteristics with them by growing on low-P, well-drained soils (Malloch et al. 1980; Alexander, 1989a). D. corymbosa allocated 3.0 tonne ha⁻¹ to reproduction in the 2003 mast year (Henkel et al., 2005), a very high amount: Zagt (1997) showed that Dicymbe altsonii, also from Guyana, invested 2.0 tonne ha⁻¹ per event. Microberlinia bisulcata A. Chev. – another large caesalp – in Central Africa shows similar strong masting and the link to EM has been inferred too (Newbery et al. 1997; Newbery et al. 1998). There, with a shorter intermast interval compared with D. corymbosa (c. 3 vs 5 yr), investment was close to 1.0 tonne ha⁻¹ (Green & Newbery, 2002). Impressive examples are to be found in the Dipterocarpaceae, for which Curran (1994) has developed extensive arguments about how masting and EM-habit may have coevolved. The seminal work by Ashton et al. (1988) showed how dipterocarp mass flowering (often followed by mast fruiting) was linked to cool nights in ENSO years, and the hypothesis advanced was that low temperatures triggered floral initiation. The subset of interrelated climatic variables – low rainfall, high daytime radiation and low nighttime temperatures – may connect with resource level regulation, hormonal switches and floral initiation in woody plants.

Dominance and regeneration

The phenomenon of dominance in tropical rain forests has attracted more attention in recent years as we move away from the somewhat idealized picture of all rain forests being composed of very species-rich vegetation types. Richards (1996), in what is perhaps the cornerstone monograph for tropical ecologists, gave much thought to this aspect of local and regional dominance. Particularly clear are the forests on low-nutrient soils, especially those in Africa and South America where EM species frequently dominate (Alexander, 1989b). However, there is varying evidence as to whether regeneration at these sites is persistent or not. Connell & Lowman (1989) have argued for EM species being responsible for this dominance because the EM symbiosis aids recruitment. This appears to be the case for Dicymbe in the study of Henkel et al. (2005), but there are counter examples in Africa which accord closer to the Aubréville (1938) model of shifting mosaics, namely that regeneration is poor below adults and that new stands form away from present ones (Newbery et al., 1998), and there are monodominant forests of non-EM species, e.g. Mora spp. in South America (Torti & Coley, 1999). Henkel et al. (2005) show that predation was low in their 2003 mast year and that the rate of survival of seedlings to saplings was high. So we could predict that non-EM dominant species will not have a mast fruiting strategy and, correspondingly, that predator–pathogen pressure is low. In a similar vein, we have yet to explain why the EM caesalps in East African dry forests (Högberg, 1986) have no consistent reports of mast fruiting, and there is no clear case for Eucalyptus (EM Myrtaceae) in Australia (Smith & Read, 1997). Could the EM–masting association be restricted to moist temperate and tropical forests? This remains to be unravelled in the coming years.

Perspectives

The link between EM and mast fruiting opens up an exciting new area of research which involves not only the well-known traits of EM in P acquisition, interplant transfer and storage (Smith & Read, 1997) but also has implications for whole-tree physiology, phenology and population dynamics. High fitness not only requires efficacious morphological and physiological adaptations but a successful life-history strategy for a tree. How climate interacts with soil conditions, especially climatic events such as dry periods (owing to intensified dry seasons in seasonal temperate and tropical climates, or dry periods in otherwise normally aseasonal ones) is worth pursuing further. The answer will need phenological data from long-time series at several comparable sites – for example, continued observations on species like Dicymbe. This approach will hopefully take us closer to a better understanding of which factors determine mast fruiting, and, moreover, it will revive interest in the slumbering problem of what is the integrated control mechanism for flowering and fruiting in trees in general.