Soil depth, plant rooting strategies and species’ niches

Abstract

What traits make plant rooting strategies adaptive for shallow or deep soils in water-limited environments? One is tempted to answer that effective shallow root systems should be best for shallow soils, while deep rooting would be best for deep soils. This is not what was found in a recent study by Poot & Lambers (this issue; pp. 371–381), who compared root developments and root system morphologies of two rare Hakea species (Proteaceae), which were endemic to shallow soils over ironstone, with four Hakea species commonly found on deeper soils in the same region of southwestern Australia. The shallow-soil endemics invested more in deep roots, less in cluster roots and showed considerably more lateral spread of their root systems at depth than their congeners from deep soils. ‘How do roots at the boundary between soil and bedrock locate rock fractures that are large enough for them to grow in?’ Not much is known about root system characteristics of plants that tend to grow on shallow soils over bedrock or massive hardpans, but the available data support the finding that such plants tend to be deeply rooted. According to a database containing root system information for plants from water-limited (arid to subhumid) environments (Schenk & Jackson, 2002b), shrubs and trees on deep soils have a geometric mean rooting depth of 2.2 m (standard error (SE) ± 0.1 m, n = 401), whereas shrubs and trees that grow on shallow soils over bedrock have a geometric mean rooting depth of 7.9 m (SE ± 1.7 m, n = 14). Given the difficulties of determining rooting depths in bedrock, it is probably safe to assume that this may be a conservative estimate. Roots of woody plants on shallow soils tend to grow along fractures deep into the underlying rocks (Fig. 1; Sternberg et al., 1996). Arbutus menziesii roots in fractured sandstone in the north Coast Range of California. Photograph courtesy of Robert C. Graham. The ingenious experimental design of the new Hakea study (Poot & Lambers) enables us to understand in greater detail the rooting strategy that allows plants to send roots down along the same pathways by which water infiltrates into the rock. Plants were grown in the center of containers that were 0.2 m long, 1.8 m wide and 0.15 m deep. Roots of the two shallow-soil endemics explored the bottom of their containers over the whole width much more thoroughly than roots of the other four species. On shallow soils, this root-foraging strategy should increase the chance of finding cracks that provide access to water and nutrients in rock fractures (Poot & Lambers, 2003) or even within the decomposed bedrock itself (Jones & Graham, 1993; Sternberg et al., 1996). Holding capacities for plant-available water of decomposed rock, gravel and petrocalcic horizons can be surprisingly high (0.03 to 0.3 m3 m−3) (Jones & Graham, 1993; Brouwer & Anderson, 2000; Duniway et al., 2007), but because they are typically lower than in soil, water infiltrates more deeply. Plant-rooting depths in water-limited environments are highly correlated with infiltration depth (Schenk & Jackson, 2002b; Laio et al., 2006; Schenk, 2008). Roots and their associated fungi can contribute to weathering and enlargement of rock fractures (Frazier & Graham, 2000; Landeweert et al., 2001), and mycorrhizal hyphae can grow into pores of the rock matrix that are not accessible to roots (Bornyasz et al., 2005). While it easy to understand why deep rooting may be an adaptive strategy on shallow soils, it is less obvious why so many rare species are restricted to such habitats (Baskin & Baskin, 1988). Why should high allocation to deep roots be a disadvantage on deep soils of water-limited environments? In fact, there are many factors that favor placing roots in the uppermost soil layers (Schenk & Jackson, 2002a), including (1) lower energy costs for construction, maintenance and resource uptake, (2) lower soil strength near the soil surface, (3) high water availability close to the surface, which is wetted even by small precipitation events, (4) high nutrient availability in the upper soil layers, (5) a lower probability of oxygen deficiency, and (6) because deep roots in dry soil could potentially be a drain for downwards hydraulic redistribution. Because of all these reasons, shallow roots generally have competitive advantages over deeper roots (Schenk, 2006). In fact, the competitive pressure favoring shallow root distributions appears to be so strong that the ‘shallowest possible root profiles’ is often a reasonable null-model to predict vertical root distributions at the plant community scale (Laio et al., 2006; Schenk, 2008). None of the many advantages of shallow rootedness listed above would restrict a deeply rooted plant species’ fundamental niche (sensu Hutchinson, 1957) to shallow soils. Allocating a high proportion of resources to deep roots is probably disadvantageous only if competitors take much more effective advantage of resources available in shallow soil layers, exclude the deep-rooted plants and thereby restrict the realized niche of such species. It is no surprise that the shallow-soil endemics survived well when transplanted to deep soils when competition was alleviated (Poot & Lambers). Even without strong competition, however, the common Hakea species had poor survival at the shallow ironstone sites, showing that their fundamental niche did not extend to these habitat conditions. Fundamental restrictions to a species’ ability to survive, such as intolerance to frost, shade or drought, are easy enough to understand, but the exact reasons that cause many rare species to be poor competitors outside their restricted ranges remain poorly understood (Poot & Lambers, 2003). Competitive ability is highly context-dependent and will vary depending on complex relationships with competitors and the environment. The hypothesis that deep rooting may be maladaptive in deep soils would have to be tested with a large number of species in many different environments, and the findings would probably vary widely. Causes of rarity in plant species may well be idiosyncratic if they reflect restrictions to realized rather than to fundamental niches. How do roots at the boundary between soil and bedrock locate rock fractures that are large enough for them to grow in? The research on Hakea (Poot & Lambers, 2003, this issue) suggests that these plants maximize their chance of encountering such fractures by spreading their roots along the rock surface. The main roots of the common Hakea species from deep soils reduced their growth when reaching the bottom of the containers (Poot & Lambers, 2003), which is a commonly observed pattern in roots that encounter physical barriers. The underlying mechanism may be self-inhibition of growth in response to an accumulation of root exudates close to a barrier (Falik et al., 2005). Plant species that possess such self-inhibition traits would be unable to forage for small clefts in a rocky substrate. Interestingly, roots of the shallow-soil-endemic Hakea species did not show growth inhibition at the physical barrier imposed by the bottom of containers (Poot & Lambers, 2003). This allows them to grow freely along physical barriers. Detection of crevices in the rock could be simply a result of gravitropism or hydrotropism, or a combination of both. Perhaps roots of these species could even be stimulated by gradients of root exudates that may follow along major pathways of water flow in rock crevices. Root foraging in fractures of rocks could be explored experimentally by offering roots choices between artificial crevices of different sizes, different inclinations, or different water and nutrient contents. To my knowledge, such foraging experiments, which would be the plant equivalent of the well-known rat maze experiments, have not been conducted with plants. In the case of Hakea, which forms cluster roots, it would be especially interesting to investigate whether cluster root formation could be stimulated in experimental crevices, which would indicate that roots in rock crevices play a role in nutrient supply as well as in water supply. Research on root behavior is sure to present us with many more surprises about the foraging abilities of plants.