Functional Ecology 2009, 23, 1157–1166
doi: 10.1111/j.1365-2435.2009.01575.x
Phosphorus economics of tropical rainforest species and stands across soil contrasts in Queensland, Australia: understanding the effects of soil specialization and trait plasticity Sean M. Gleason*,1, Jenny Read1, Adrian Ares2 and Dan J. Metcalfe3 1
School of Biological Sciences, Monash University, Bld 18, Clayton, Victoria 3800, Australia; 2Department of Forest Ecosystems and Society, Oregon State University, 321 Richardson Hall, Corvallis, Oregon 97331, USA; and 3CSIRO Sustainable Ecosystems, Tropical Forest Research Centre, PO Box 780, Atherton, Queensland 4883, Australia
Summary 1. Edaphic specialization among species may lead to greater productivity and resource use efficiency across heterogenous landscapes than could be achieved in the absence of specialization. Although this idea has been tested conceptually and in garden experiments, it has rarely been examined in undisturbed forests. 2. To address this gap in our knowledge, we measured aboveground net primary productivity (aboveground biomass increment plus litterfall; ANPP) and phosphorus use efficiency (ANPP ⁄ P uptake) for stands on infertile schist soil and fertile basalt soil on the Atherton Tablelands, Australia. We also measured aboveground biomass production and estimated P use efficiency (PUE) for 52 tree species within these stands. Soil P fractions and radiation use efficiency (ANPP ⁄ percent intercepted radiation) were also measured. 3. Phosphorus use efficiency was markedly variable (CV = 44%) among species across soil types. Phosphorus use efficiency of obligate specialists on infertile soil was twice as high as species common on both soil types. Plastic responses within species were also significant, with trees on infertile soil having 45% greater PUE than trees on fertile soil. At the ecosystem level, genotypic and phenotypic traits accounted for 49% and 29% of the total PUE variance. Phosphorusefficient trees (PUE >8 kg biomass g)1 P uptake) on schist soils contributed more to stand-level species richness (schist = 73%, basalt = 20%), basal area (schist = 86%, basalt = 18%) and production (schist = 82%, basalt = 10%) than did P-efficient species on basalt soils. 4. Forest on schist soils achieved higher PUE than forest on basalt soils by partitioning more P to leaves rather than wood and by retaining P for longer periods of time before losing it via tissue senescence. These PUE traits enabled forest on schist to achieve similar ANPP and radiation use efficiency (i.e. PUE was not traded for radiation use efficiency). It is possible that opportunity costs of high PUE may exist among other life-history traits. 5. These results suggest that plasticity in traits that confer P conservation is significant, but limited, and that maximum P conservation at the landscape level must be achieved via genetic differences between species. Although this highlights the importance of genetic conservation in forests, it also demonstrates that high P conservation is possible with relatively few, but markedly plastic species. Key-words: phosphorus use efficiency, radiation use efficiency, species richness, forest productivity, soil phosphorus, trade-offs Introduction No species can maximize growth, reproduction and competitive ability in all environments (Funk & Vitousek 2007). As a *Correspondence author. E-mail:
[email protected]
result, plants trade fitness in one environment for fitness in another environment. Such trade-offs are likely to engender plant specialization (e.g. edaphic specialization and species– soil associations) and the coexistence of species (Tilman 2000). Species–soil associations in heterogeneous landscapes are common in temperate (Aerts 1999; Lusk & Matus 2000;
2009 The Authors. Journal compilation 2009 British Ecological Society
1158 S. M. Gleason et al. Read 2001) and tropical (Baltzer et al. 2005; Paoli et al. 2006; John et al. 2007) forests. Although species–soil associations are widespread, there appears to be no general mechanism driving the divergence of soil specialists. However, Aerts (1999) suggests that a trade-off between growth rate and nutrient retention may partially explain the divergence of species favouring sites of low fertility. This is because traits that lead to high nutrient retention, such as slow nutrient turnover and low tissue nutrient concentrations, can also contribute to low growth rate (Grime 1997; Aerts 1999). Thus, the trade-off between nutrient conservation and growth rate may be an important source of tree diversity (Reich et al. 1992; Aerts 1999) in forested ecosystems. Edaphic specialization can lead to higher ecosystem-level productivity (Tilman et al. 1997), but plasticity of nutrient use within species can result in similar effects on ecosystem productivity. For example, in a Metrosideros polymorpha Gaud forest along a nutrient gradient, plastic resource use efficiency increased productivity because resources were used more efficiently where they were more limiting (Herbert & Fownes 1999). In this study, we ask how much genotypic (intrinsic) and phenotypic differences in resource use contribute to ecosystem-level productivity in heterogeneous landscapes. This is an important question because the inability of species to adapt phenotypically to edaphic variation has an opportunity cost – reduced distribution on unsuitable substrates. Clearly, ranges of soil edaphic variation, phenotypic plasticity and intrinsic differences among species contribute to ecosystem-level functioning. We measured ANPP ([litterfall + biomass increment] ⁄ time) and P uptake for trees, species and stands across a P availability contrast in a tropical rainforest in Queensland, Australia. We asked the following questions. (i) Do P use traits differ between edaphic specialists and edaphic generalists on the same substrate? (ii) How plastic are P use traits among edaphic generalists growing on contrasting soils? (iii) How much of the total variance in P use traits among generalists is attributable to phenotypic plasticity or intrinsic differences between species? (iv) How do these differences in P use manifest at the ecosystem level?
Materials and methods SITE DESCRIPTION AND SPECIES
Research sites were established within Wooroonooran National Park (1722¢S and 14543¢E) at a location c. 32 km inland from the coast and between 700 and 800 m elevation. The evergreen rainforest in this area of the park is classified as complex mesophyll vine forest (Tracey 1982) and receives c. 3Æ5 m of annual rainfall, with c. 70% falling between the months of November and April. Species richness is high with >1000 tree species occurring within the regional area of northeast Queensland (Hyland et al. 2002) and c. 100 occurring within a 0Æ25-ha plot. The research sites are located in forest occurring across two soil types (schist and basalt), which are often directly adjacent to one another at the same elevation, slope and aspect. Soil fidelity among species in these forests has been compared using the procedure of Dufreˆne & Legendre (1997) (S.M. Gleason, J. Read, A. Ares &
D.J. Metcalfe, unpublished data). This method considers both the relative abundance and the relative frequency of species as they occur on each substrate type and is independent of the relative abundances of other species. All schist specialist (six species) favoured schist soil (P < 0Æ001). In this paper, we analyse two main groups of species arising from these analyses: (i) species occurring exclusively on schist soils (specialists) (n = 6) and (ii) species occurring on both schist and basalt soils (generalists) (n = 36). There are no obligate basalt specialists in the study area. Although species categorized as specialists are obligate schist specialists on our sites, they do occur on other Ppoor substrates (e.g. weathered granite) outside the study area.
PLOT ESTABLISHMENT AND FERTILIZATION
In September 2005, 24 forest production plots were located on two ridges (c. 300 m apart) that crossed the schist-basalt geological contrast described. Within each ridge, 12 circular 100-m2 plots were established, six plots on schist and six plots on basalt. Plots were placed c. 50 m apart, but distance varied somewhat as large gaps were avoided to homogenize basal area among the plots. The diameter at breast height (d.b.h.), species, height, and distance and azimuth from plot centre were recorded for every tree >5 cm d.b.h. (c. 25 trees ⁄ plot). Trees with a d.b.h. >10 cm were fitted with a stainless steel dendrometer band (Keeland & Young 2005). To determine whether forest productivity was limited by either N or P, half of the plots were fertilized with 100 kg ha)1 year)1 of P (as superphosphate) and N (as urea). Fifty percent of this fertilizer was applied at the start of the experiment (October 2005) and the remaining fertilizer was applied midway though the experiment (June 2006).
SOIL DESCRIPTION AND ANALYSIS
Soils are derived from basalt (Red Ferrosol – Maalan series) and schist parent materials (Red Dermosol – Galmara series) (Malcolm et al. 1999). Whereas both soils have low pH, high organic C, moderate cation exchange capacities and high Al saturation, basalt soils have markedly higher P contents (labile and occluded pools) than schist soils (Table 1). Phosphorus limitation of plant growth on the schist soil has been previously demonstrated in a glasshouse experiment (Kerridge et al. 1972), in planted stands (Keenan et al. 1998; Webb et al. 2000), and is supported by plant stoichiometry, nutrient use traits and the distribution of schist specialists in these forests (Gleason et al., unpublished data). Mineral soil was collected (0–25 cm depth) on four different occasions during both wet (two collections) and dry (two collections) seasons from five random locations within each plot and combined into one bulked plot sample for each collection period. Soil P was fractionated using methods modified from Tiessen & Moir (1993). Although the most labile P fraction (NaHCO3-extractable P) varied seasonally, seasonal variability was similar between soil types and we present only dry season data here (Table 1). Additional details of these methods are given in Appendix S1 (Supporting Information). Cation exchange capacity and Al saturation were determined using the ammonium acetate method (Malcolm et al. 1999). Total organic carbon and N were determined using an induction furnace and Kjeldahl methods, respectively (Laffan 1988). Soil pH was measured in a 1:2 soil to water (mass) mixture after allowing the solution to stand for 1 h.
CYCLONE LARRY
Tropical Cyclone Larry struck Wooroonooran National Park on 20 March 2006, c. 6 months after plot establishment. The cyclone was
2009 The Authors. Journal compilation 2009 British Ecological Society, Functional Ecology, 23, 1157–1166
Soil specialization in an Australian rainforest 1159 Table 1. Sequential soil P fractionations and other soil variables for basalt and schist substrates
Soil variable Soil P fraction (lg g)1) NaHCO3 (0Æ5 M)* NaOH (0Æ1 M)* HCl (1 M)* HCl (10 M)* Total inorganic P* Total organic P* Total P* Other soil characteristics pH Organic carbon (%) Total N (%) ECEC (cmol + kg)1) Al saturation (%) Bulk density (g cm)3)
Basalt
Schist
P
4Æ68 (0Æ56) 84Æ2 (16Æ3) 3Æ99 (0Æ87) 969 (77) 1062 (91) 453 (21) 1515 (111)
6Æ38 (1Æ88) 14Æ4 (2Æ6) 1Æ60 (0Æ59) 141 (69) 164 (69) 76 (10) 240 (77)
0Æ408 0Æ006 0Æ046
