Potential causes of root proliferation in old root channels
The mangrove trees at Twin Cays and throughout the Belize Barrier Reef Complex clearly exhibited root promiferation inside decaying roots and old root channels. Root channels may provide a path of least resistance through an impermeable matrix, as observed in some compacted soils (Heilman 1981; Dell et al. 1983; Sollins & Radulovich 1988). However, the peat soil in which the mangrove roots were growing was relatively soft, and corings did not reveal any compacted or impenetrable layers. In fact, the coring device was pushed by hand to a 2.5 m depth, well beyond the rooting zone. Furthermore, deeper corings indicate that the limestone bedrock lies 8–10 m below the soil surface (Macintyre et al. 1986).
Another possibility is that the root channels simply provide more space for growth, i.e. larger pores than the interstitial spaces in the peat, and therefore less growth restriction. However, the artificial root channels that were empty did not have more roots than the ones that were filled with sand, confirming that additional growing space did not generate greater root proliferation by mangroves (Fig. 4). Also, total pore space in surface mangrove peat at Twin Cays was high (Table 5).
The root channels could have also ameliorated some stress factor generally present in the soil at Twin Cays. Mangrove soils are often characterized by high salinity, low Eh (indicating a strong soil oxygen demand) and accumulation of sulphide, a known phytotoxin that affects mangrove growth (McKee et al. 1988; McKee 1993; McKae 1995; Table 1 this study). Although salinity was not measured directly in the root channels, it could not have been much lower than that measured in the surrounding peat (Table 1), which was similar to that of seawater (c. 36‰) that floods the soil twice daily (Fig. 1). Eh measurements also indicated no difference in redox status between unoccupied root channels and the soil, but this comparison does not completely eliminate the possibility. The selected channels may have been unoccupied because they did not provide more beneficial conditions than the bulk soil. However, even if occupied channels had been measured and found to have higher redox status and/or lower sulphide, a causal relationship could not be assumed because of the reciprocal effects of root oxygen leakage on these soil factors (McKee et al. 1988; McKee 1993). Furthermore, the fact that root production was increased in artificial channels containing muck, which was characterized by strongly reducing conditions and high sulphide (Fig. 4, Table 5), suggests that these factors do not always inhibit root proliferation. However, they may play a role in root morphology, as discussed below.
The most reasonable explanation is that the roots proliferated inside decaying roots upon contact with decomposing organic matter and nutrients. Plant root systems generally respond to soil heterogeneity by proliferation in the most nutrient- or water-rich zones (Fitter 1994), and numerous studies have experimentally demonstrated increased branching and fine root production in nutrient-enriched patches (Robinson 1994; Roy & Singh 1994; Hodge et al. 1998). Mangrove root proliferation in response to nutrient-rich organic matter, but not to greater space or a reduction in physical impedance to root growth in artificial channels (Fig. 4), is consistent with this explanation.
The mechanism whereby roots proliferate in decaying organic material or areas of increased nutrient concentrations is most likely through increased branching by a root randomly encountering the richer area, rather than by a locational mechanism (i.e. a tropic response to an environmental cue such as a nutrient gradient) (Fitter 1994). The pattern of mangrove root growth in natural channels agreed with this explanation. Many natural channels contained no in-grown roots, and in occupied channels the roots grew along the longitudinal axis until diverted by a rupture or collapse of the channel wall. Also, the muck-filled artificial channels contained primary roots with many lateral roots, suggesting that proliferation occurred as a consequence of increased branching when appropriate conditions were encountered.
The roots of other tropical tree species growing in low-nutrient habitats are often physically associated with decomposing organic matter (Jordan & Escalante 1980; St. John 1983; St. John et al. 1983; Roy & Singh 1994). Some tropical trees exhibit extensive root mats in the leaf litter layer on the soil surface (Jordan & Escalante 1980; St. John et al. 1983; Roy & Singh 1994). Mangroves may also produce roots within the leaf layer when present (K. McKee, personal observation), but some mangrove forests lack a litter layer due to physical removal by tides or consumption by detritivores (Robertson 1991). However, mangrove root proliferation into other microsites has been reported. Red mangrove trees growing along the shoreline of Belizean islands show root growth into sponges encrusting the subtidal portions of their prop roots (Ellison et al. 1996). Relative abundances of 15N (δ15N‰) and 13C (δ13C‰) suggest that these mangrove roots obtain dissolved inorganic nitrogen from sponges, and that sponges obtain carbon from mangrove roots. This facultative mutualism may enhance mangrove growth, but only trees positioned along the island periphery and edges of tidal creeks (where their roots extend into the subtidal zone) could potentially benefit from this relationship. The majority of mangrove trees on Belizean cays must derive nutrients from other sources. Because terrigenous inputs of sediment are negligible, an important external source of nutrients is seawater. However, concentrations of nitrogen and phosphorus in seawater are low (Davis 1986). The calcium carbonate sand derived from calcareous algae (e.g. Halimeda spp.) that accumulate along the leeward shorelines also contains little N and P (Table 5). The largest store of nutrients occurs below ground in the peat substrate, but much of this may be in refractory forms, as in other peat-forming wetlands (Richardson 1999) and therefore unavailable for plant uptake. Also, plant roots must compete with bacteria and algae for nutrients. The proliferation of roots inside decaying roots places absorbing structures in intimate contact with nutrients released during mineralization before they can be leached by tidal flushing or immobilized by chemical or biological reactions.
Do species occupying the same habitat exhibit similar nutrient foraging patterns and does root proliferation in nutrient-rich microsites result in similar growth benefits for species? Both R. mangle and A. germinans exhibited comparable root proliferation in channels, which suggested similar foraging strategies. Einsmann et al. (1999), however, found that root proliferation in nutrient-rich patches was highly variable among 10 co-occurring plant species (coastal plain of South Carolina) examined in terms of scale (root mass and root length densities), precision (preferential proliferation in nutrient-rich vs. less fertile patches) and sensitivity (growth benefits gained by proliferation in patches). They further found no relationship between sensitivity and precision when plants were grown under different nutrient distribution treatments in pots, indicating that proliferation of roots in fertile patches does not always result in growth benefits. However, there may be benefits of nutrient foraging in a natural setting, where several environmental stress factors interact to limit plant growth.
Trade-off between nutrient acquisition and flood tolerance strategies
The larger proportion of live roots inside natural channels in the scrub vs. fringe or mixed zones suggests an interaction between nutrient availability and some other soil condition associated with tidal flooding. The development of more reducing soil conditions in interior scrub sites (Table 1) may limit development of fine lateral roots due to internal aeration requirements. A common strategy exhibited by wetland plants, including mangroves, is internal aeration accomplished through the development of aerenchyma, which provides a continuous, intercellular pathway for the rapid flux of oxygen through tissues growing in an anaerobic soil (Armstrong et al. 1991). However, roots of mangroves and other wetland species readily leak oxygen to the surrounding soil (McKee et al. 1988; Armstrong et al. 1991; Sorrell 1994) and if this loss is excessive, internal oxygen deficiencies and reduced energy status may develop (McKee & Mendelssohn 1987; McKee 1996). As root surface area can affect the rate of oxygen leakage (Sorrell 1994), long, thin roots with many fine laterals would be disadvantageous in a waterlogged soil with a high external oxygen demand, especially where the potential gain of nutrients was low. The maintenance of high internal oxygen levels to support rapid root extension would promote a ‘foraging’ growth pattern in a reducing soil environment until the root encountered a relatively nutrient-rich microsite. Then, the switch to an ‘exploitation’ growth pattern would be worthwhile, even if accompanied by greater oxygen leakage.
Where tidal flushing aerates the soil and brings more nutrients into contact with roots, root branching and fine root production may be maximized, e.g. in the fringe zone (Fig. 1, Table 1). In contrast, the relatively stagnant conditions in the scrub forest probably limit mass flow of nutrients to root surfaces and simultaneously generate a high external oxygen demand. Such conditions would require a trade-off between morphologies supporting internal aeration, i.e. short, thick roots with few laterals, vs. nutrient acquisition, i.e. long, thin roots with many fine laterals. Thus, although an overall increase in root system surface area by lateral branching might improve nutrient acquisition by mangroves, proliferation of roots only where there is a greater potential for nutrient capture would minimize oxygen losses from the whole root system. Not only should total uptake be increased by this response, but uptake per unit of carbon partitioned to the root system should be higher. In contrast, production of an abundance of roots randomly distributed through the bulk soil might achieve a similar total uptake, but the carbon and energy required below ground may be much higher. This hypothesis requires further testing, but the significantly greater proportion of live roots in natural channels formed in the scrub zone is consistent with this explanation.
Phosphorus limitation and root proliferation
A final consideration is what nutrient element might be responsible for root proliferation in channels? Just because a root system is in contact with the nutrients in the soil solution does not mean that it has equal access to all nutrients. Strongly adsorbed anions such as phosphate have diffusion coefficients as low as 10−9 cm2 s−1 (Nye & Tinker 1977). By comparison, diffusion coefficients of nitrate and ammonium in dilute solution are c. 10−5 and 10−7 cm2 s−1, respectively. Robinson (1996), using data from a well-known study by Drew (1975), calculated that local proliferation of lateral roots would not necessarily achieve significantly greater capture of mobile nutrients such as nitrate, but would improve capture of less mobile phosphate. Fine roots with a large surface area per unit mass would thus substantially improve acquisition of relatively immobile phosphorus from the substrate. Additionally, root depletion zones would be narrow, and narrow depletion zones mean that roots can be closely packed without competing for a common phosphate pool (Nye & Tinker 1977). Thus, if phosphate concentrations are low, as they are on mangrove islands in Belize, prolific branching of the roots may increase a tree’s ability to capture this limited resource. The root proliferation in channels observed in this study, combined with the finding that red mangroves in the interior of Twin Cays are phosphorus-limited (Feller 1995; Feller et al. 1999), is consistent with these theoretical considerations.
Ecosystem-level consequences of nutrient conservation
Resorption of nutrients from senescing leaves is often cited as a major conservation mechanism in several types of low-nutrient ecosystems (Aerts 1996), including mangroves (Feller 1995; Feller et al. 1999). Dwarf R. mangle trees at Twin Cays reabsorb 73% of phosphorus and 47% of nitrogen during leaf senescence (Feller et al. 1999), indicating that these mangroves are extremely efficient at conserving nutrients, particularly phosphorus, at an individual plant level. Proliferation of roots inside decaying roots may have a similar effect by concentrating absorbing organs where they can recapture nutrients from below-ground tissues as they decompose. In a dynamic habitat such as the intertidal zone, the ability to alter root growth to take advantage of spatial heterogeneity or temporal pulses in nutrient availability would be particularly important. Work in other types of forests has shown that soil nutrient concentrations vary spatially and temporally and that localized nutrient-rich areas may be an important source of nutrients for plants growing in heterogeneous environments (Farley & Fitter 1999).
Although both R. mangle and A. germinans exhibited root proliferation in channels, the amount of fine root production (and consequently absorbing surface area per unit biomass) appears to be much greater for R. mangle (K. McKee unpublished data). The combination of root proliferation in decaying roots (this study), above-ground nutrient conservation strategies (Feller et al. 1999) and facultative mutualism with root-fouling sponges (Ellison et al. 1996), renders R. mangle particularly well-suited for growth in oligotrophic habitats. If root proliferation in enriched microsites improves nutrient capture, species such as R. mangle may be more competitive than other mangroves in low-nutrient systems, as demonstrated for some grassland species (Robinson et al. 1999).
Improved efficiency of nutrient acquisition as a consequence of selective exploitation of microsites at the individual plant level has implications for nutrient economy at the ecosystem level. If root growth and branching inside decaying roots improves nutrient acquisition, the need for allocation of biomass below ground may be reduced. The conserved carbon and nutrients could then be directed toward growth of shoots and aerial roots. Consequently, overall productivity of the ecosystem and its resilience to disturbance may be improved. Root proliferation in decaying roots (this study) and other nutrient-enriched microsites (e.g. epibionts; Ellison et al. 1996) may partially compensate for external nutrient limitations to mangrove growth as well as conserve nutrients within the mangrove ecosystem. Mangrove communities with tight nutrient cycles would tend to export smaller amounts of nutrients than those that are less conservative, and these differences would be expected to have an impact on secondary productivity in adjacent waters (Twilley 1988, 1995).