Is the Fynbos Biome the product of extensive niche construction?

Niche construction refers to the modification of its environment by a species in such a way as to make it more suitable for that species.¹ This may include the construction of termite mounds and beaver dams, and has been referred to by Dawkins as the “extended phenotype” of the organism.² The study of niche construction is particularly relevant to the understanding of plant invasions, since, in order to become invasive, plants must be successful in an environment in which they did not evolve and to which they may be poorly adapted. If they are able to modify their habitat, e.g. by reducing the soil moisture, increasing the salinity, or altering the flux of nutrients through the system, they may outcompete the indigenous plants and come to dominate the community.

In the southwestern Cape, there exist three mutually exclusive vegetation types: forest, strandveld, and fynbos. Forest and strandveld communities are characterized by trees and relatively large shrubs with broad leaves, and a shade-tolerant understorey, occurring on relatively rich soils.^3,4 Fynbos, on the other hand, consists of finer-leaved, low-statured, sclerophyllous shrubs occurring on soils with much lower nutrient concentrations,⁵ thought to be especially phosphate-deficient.⁶ This vegetation is proposed to have evolved around the time of sudden aridification when the Cape became a winter-rainfall region in the Pliocene.⁷

The distinctness of these three vegetation types in terms of species composition, despite their close proximity, has led researchers to attempt to identify the factors that determine their distributions and maintain the biome boundaries. One hypothesis that has been proposed is that niche construction by fynbos plants has contributed to preventing the incursion of species from the other biomes.⁸ This essay aims to evaluate this hypothesis against the hypothesis that inherent soil resource limitations maintain the integrity of the fynbos.

Berendse 1994⁹ has proposed a competition model that can be applied to productive trees vs. sclerophyllous trees and shrubs, from which can be predicted the conditions under which forest trees could invade the fynbos.

When water or nutrients are not limiting, light becomes the limiting factor and species with higher potential productivity and growth rates (e.g. forest trees) can compensate for their greater loss of resources (by high leaf turnover and evapotranspiration rates) and outcompete the slower-growing species (e.g. sclerophylls) by overtopping and shading them out.

However, when resources such as soil N and P are limiting, species with lower requirements (by unit biomass) will outcompete those that have loss rates greater than the rate at which they can replace nutrients. Fynbos occurs on soils that are low in nutrients, especially phosphate, and that are dry during the summer. The sclerophylly of fynbos plants has been ascribed the adaptive functions of limiting nutrient and water loss, as the long-lived leaves require relatively low investments of N and P;¹⁰ they photosynthesize efficiently with regard to nutrients; and the resources in the leaves are resorbed before leaves are shed.¹¹

One objection that can be raised to this model is that plants that have high productivity above ground are able to support more growth below ground.¹² Large, fast-growing trees may, thus, be able to access deeper water and nutrient pools than smaller plants with shallow roots, which are reduced to drought tolerance during the summer. However, forest species will typically not have at their disposal the various phosphate-acquisition adaptations found among fynbos taxa, such as cluster roots.

A more pertinent reason why this model may be invalid is that it assumes that the species will be able to compete until a stable state is reached. However, the fynbos experiences frequent disturbances in the form of crown fires, which clear the playing field by killing off the above-ground biomass. This is the basis for Mutch’s niche construction hypothesis (Mutch 1970, cited in Bond & Midgley 1995⁸, Schwilk & Kerr 2002¹³): Since the nutrients that are locked up in biomass are released in fires,¹⁴ the seeds of serotinous species common in the fynbos are able to make use of these nutrients in the absence of competition from other species. Forest species are not adapted to surviving fires, either through serotiny or resprouting. Fires are, therefore, advantageous to fynbos species and if traits evolve in fynbos plants that increase their flammability, this will enhance their fitness by creating a niche in which they can thrive, from which potentially more productive species are excluded. These flammability traits include high concentrations of structural material relative to living cytoplasm (high C-to-N ratios) and the production of volatile compounds such as terpenes.¹⁵

An alternative mechanism of niche construction in the fynbos may be that indigenous plants reduce the level of nutrients in the soil (MD Cramer, pers. comm.), which makes the habitat less suitable to species with high water or nutrient requirements, thus potentially modifying the environment from one that could favour the fast-growing trees to one in which trees are maladapted, but that slow-growing low-statured plants can tolerate.⁹ This mechanism has been suggested to be important in promoting invasion by plants that retard the nitrogen cycle with long N residence times in long-lived leaves, as well as slow remineralization rates due to high C-to-N ratios in litter.¹⁶ This may be exacerbated by rapid use of soil moisture, leading to reduced microbial activity.

In the context of the Cape Floristic Region, however, low water use efficiency is characteristic of forest species,¹⁷ rather than fynbos, so reduction of soil moisture is unlikely to be adopted for fynbos niche construction. On the other hand, woody fynbos plants do tend to be evergreen and sclerophyllous,⁵ and thus retain their N and P over several years, resorbing it when the leaves senesce,¹¹ and the high C:N litter ensures slow nutrient cycling.¹⁶ In combination with specialized nutrient acquisition organs, this may result in much of the available nutrients being removed from the soil and stored in biomass (as leaves, litter, or underground storage organs), which will push the system further towards the nutrient-limited state and away from the light-limited state in which they face strong competition from taller plants.

An interesting exception to the impenetrability of the fynbos to trees is the case of the alien invasive plants that occur in the Cape, notably acacias, eucalypts, and pines. Their distribution may inform our understanding of the mechanisms that give the fynbos its integrity. The invasive Acacia species A. mearnsii and A. saligna are common throughout the fynbos biome, often close to anthropogenic disturbances such as roads.^18,17 They are legumes and are, therefore, not nitrogen-limited thanks to their N₂-fixing microbial endosymbionts.¹⁹ However, they are presumably just as phosphate-limited as local forest trees, having evolved in savanna soils that are not P-deficient. Their tall growth form and abundant leaf area enable them to grow roots deep into the soil,²⁰ a trait that should also be common to the forest trees. Since their establishment is not limited by the summer drought or low P status of the soil, water and P deficiency are unlikely to be the factors that exclude forest trees from fynbos areas.

The red river gum Eucalyptus camaldulensis is also invasive in the fynbos biome.¹⁸ This species does not fix atmospheric nitrogen and is, therefore, as N-limited as the forest species in the fynbos. Since this species occurs not only along river courses (with moist soils and high litter content) but also drier, litter-free areas, e.g., the east-facing slopes of Lion’s Head (pers. obs.), nitrogen may also be ruled out as the factor that limits tree establishment in the fynbos.

The distributions of alien tree species could provide a test of whether the fynbos biome is the result of niche construction due to the evolution of flammability. If these trees are only found in areas protected from fire, such as narrow ravines or near human settlements, this would indicate that it is fire that prevents the establishment of trees in fynbos. If, instead, they are found in areas that burn frequently, they would have to be adapted not only to surviving fire (e.g. by resprouting, in E. camaldulensis²¹), but also to accessing water or nutrients that indigenous forest species are unable to.