Effects of Nutrient Addition on the Productivity of Montane Forests and Implications for the Carbon Cycle
Both carbon storage and sequestration are major ecosystem services provided by forests. The NUMEX (Ecuadorian NUtrient Manipulation EXperiment) study aims to identify the underlying mechanisms for the variation of these services as affected by future changes in nutrient availability. The ongoing experiment is being conducted in southern Ecuador to improve our understanding of the effects of continuous moderate N and P addition to tropical montane forest ecosystems. This chapter summarizes the short-term effects of nutrient addition evident at the end of the experiment’s first year. The rapid responses of the studied Andean montane forests to N and P addition observed at this early stage of the experiment illustrate the vulnerability of the forests to higher nutrient deposition.
Nitrogen (N) and phosphorous (P) are key nutrient elements for plant growth. The ecological cycles of these elements that were previously free of anthropogenic disturbances have recently been severely affected by human activities. As a consequence, P and N in particular are often more readily available for plant growth than in “undisturbed” ecosystems, and a better understanding of how net primary production is affected by higher nutrient availability is urgently needed (Elser et al. 2007; Gruber and Galloway 2008; Xia and Wan 2008). The results of recent meta-analyses show that N is limiting for plant productivity in most terrestrial ecosystems of the world, but limitation by P can be equally important. Moreover, the addition of both N and P to ecosystems results in strongly positive synergistic reactions (Elser et al. 2007; LeBauer and Treseder 2008; Xia and Wan 2008).
Nutrient manipulation experiments (NUMEXs) carried out in tropical forests have in most cases shown that traits related to aboveground productivity such as litter production or stem growth are positively influenced by N and P addition (Tanner et al. 1998). In contrast, no clear picture has emerged with respect to the response of belowground processes to fertilization. Some studies found a slowing down of belowground carbon (C) turnover after N and P addition (e.g., Giardina et al. 2004), while others noted enhanced soil C sequestration (Cusack et al. 2010; Li et al. 2006). Further studies revealed large soil CO2 losses upon P addition (Cleveland and Townsend 2006), a slowing down of belowground C turnover upon N and P addition (Giardina et al. 2004) and an increase in soil carbon stocks upon N and P addition (Gamboa et al. 2010). Increased deposition of NH4+ may also increase soil acidification due to nitrification and nitrate leaching, which possibly could reduce forest productivity (Lewis et al. 2004).
These manifold effects point to complex interactions between soil nutrient availability and C turnover in tropical forests and highlight the incompleteness of our understanding of how the tropical C cycle will respond to changes in nutrient availability (Cleveland and Townsend 2006; Cleveland et al. 2006; Wright 2005). One scenario resulting from increasing N (and P) deposition in tropical forests is that the system is driven toward N saturation, as has been observed in a number of temperate forest ecosystems (e.g., Aber et al. 1998). Comprehensive multidiscipline studies on physiological and biogeochemical responses to continuous high N input have been conducted in several temperate and boreal forests (e.g., Högberg et al. 2006; Magill et al. 2004), but are virtually lacking for tropical forests. A recent study in a Panamanian lowland forest showed that N addition may increase soil N losses through both enhanced nitrate leaching and N-oxide emission where the soils are relatively fertile (Corre et al. 2010). However, the nutrients were added in high amounts in most of these experiments (≥100 kg N ha−1 and/ or 50 kg P ha−1). The reported responses accordingly allow no reliable prediction as to possible long-term effects of the increases in atmospheric N and P deposition expected for tropical forests, which would represent a more moderate input distributed over a longer time period.
This chapter presents initial results of the ongoing NUMEX experiment that is being conducted in southern Ecuador to improve our understanding of the effects of continuous moderate N and P addition to tropical montane forest ecosystems. Both carbon storage and sequestration are major ecosystem services provided by forests (regulating services; see Chap. 4), and the NUMEX study aims to identify the underlying mechanisms for the variation of these services as affected by future changes in nutrient availability.
23.2 Material and Methods
23.2.1 The Ecuadorian Nutrient Manipulation Experiment
The research area has a tropical humid climate, and the mean annual precipitation increases along the altitudinal gradient (see Chap. 1). Rainfall shows little seasonality, and there are no regularly occurring dry periods (Emck 2007).
The annual bulk N deposition from precipitation ranged from 9.5 to 10 kg N ha−1 during the period of 1998–2003 (Boy et al. 2008), but recent data based on the monitoring of bulk and dry deposition between 1998 and 2010 (Wilcke et al. unpublished data) indicate higher annual depositions of 14–45 kg N ha−1, as well as 0.4–4.9 kg P ha−1.
Characteristics of the soil and the forest stands (including only trees of ≥10 cm dbh) at the three NUMEX sites. The figures quoted are means (±SE). Soil characteristics were determined in November 2007 prior to the first nutrient application
Bombuscaro (1,000 m)
San Francisco (2,000 m)
Cajanuma (3,000 m)
Org. layer depth [cm]
Mineral topsoil (0–5 cm)
Base saturation [%]
Total C [mg g−1]
Total N [mg g−1]
Total P [mg g−1]
Canopy height [m]
Tree density [trees ha−1]
Tree basal area [m2 ha−1]
The three study sites harbor three different forest types (Homeier et al. 2008). At 1,000 m, in the transition zone between the tropical lowland and the lower montane forest, an evergreen premontane forest reaches up to 40 m in height. Common tree families of this forest type are Fabaceae, Melastomataceae, Moraceae, Myristicaceae, Rubiaceae, and Sapotaceae. The evergreen lower montane forest at 2,000 m reaches a canopy height of 18–22 m. Characteristic tree families are Euphorbiaceae, Lauraceae, Melastomataceae, and Rubiaceae. The upper montane forest at 3,000 m reaches up to the tree line and canopy height is rarely higher than 8–10 m. Dominant tree families are Aquifoliaceae, Clusiaceae, Cunoniaceae, Lauraceae, and Melastomataceae. There is a complete tree species turnover from 1,000 m to 3,000 m, and less than five species are shared between the study plots at 2,000 m and either of the two other sites.
At each elevation level we established 16 plots of 400 m2 each (20 m × 20 m). These accommodated four treatments (N, P, N + P, control) in four replicates each. One replicate of each treatment was arranged randomly in one of four blocks (Fig. 23.1). The plots were installed in old-growth, closed-canopy stands that evidenced no visible signs of human or natural disturbance and were separated by a distance from each other of at least 10 m.
Most of the research was conducted within six subplots of 4 m2 each that were randomly placed along two perpendicular transects selected at random inside each of the 400 m2 plots.
N and P were added to the plots at an annual rate of 50 kg N ha−1 (as urea, CH4N2O) and 10 kg P ha−1 (as NaH2PO4). The nutrients were dispersed homogeneously within the plots on two application dates per year. NUMEX has been started in February 2008.
126.96.36.199 Soil Respiration
Soil respiration was measured using static vented chambers. Four permanent chamber bases with a base area of 0.04 m2 and a base height of 0.25 m each were randomly placed in four of the six subplots of each plot (16 per block; 48 per elevation). Gas samples were taken once every month from January 2008 until December 2008. Gas sampling is described in detail in Wolf et al. (2011). Gas fluxes were calculated from the linear increase in gas concentration multiplied by the density of the air and the volume of the chamber headspace. The value for the air density was adjusted for soil temperature and air pressure measured at the time of sampling.
188.8.131.52 Fine Root Biomass
For quantifying fine root biomass (roots < 2 mm in diameter), we took six root samples per plot to a depth of 20 cm using a soil corer of 3.5 cm diameter in January 2009. The soil samples were transferred to plastic bags and transported to the laboratory, where they were stored at 4 °C and processed within 6 weeks. The samples were soaked in water and freed from soil residues using a sieve with a mesh size of 0.25 mm. Only the fine roots of trees were considered for analysis. Live fine roots (biomass) were separated from dead rootlets (necromass) under the stereomicroscope. The fine root biomass was dried at 70 °C for 48 h, weighed, and expressed as g m−2 ground area.
184.108.40.206 Fine Litter Production
Six litter traps (surface area 0.36 m2 each, positioned 1 m aboveground) were installed per plot, one in each subplot. The fallen litter was collected every 2 (at 1,000 m) to 4 weeks (at 2,000 and 3,000 m). The samples were oven-dried at 60 °C and the dry weights were determined.
220.127.116.11 Leaf Area Index
The leaf area index (LAI) of the stands was estimated with the LAI-2000 Plant Canopy Analyzer (LI-COR Inc., Lincoln, NE, USA). The measurements were conducted with two instruments in the remote mode, i.e., by synchronous readings below the canopy at 2 m height above the forest floor and in a nearby open area (“above-canopy” reading). Six measurements were made directly above the litter traps in each plot in January 2008 (before the first fertilization with N and/or P: see Sect. 23.2.1) and again in January 2009 (1 year after the first fertilization).
18.104.22.168 Tree Diameter Growth and Plot Basal Area Increment
The stem diameter growth of all trees with a diameter at breast height (dbh) ≥ 10 cm present in a plot was monitored every 6 weeks in each of the 48 plots using permanently installed girth-increment tapes (D1 dendrometers, UMS, Munich). The annual increase in the cumulative basal area of a plot was calculated by adding the basal area increment of all of the trees of a plot during the period from February 2008 (after the first fertilization) to January 2009.
22.214.171.124 Drought Sensitivity of Tree Growth After Nutrient Addition
To investigate the short- and medium-term growth response of important tree species to drought, we conducted a preliminary study with electronic high-resolution dendrometers (Type DR, Ecomatic, Munich) on N-fertilized and non-fertilized trees of similar size of the species Podocarpus oleifolius D. Don ex Lamb., Graffenrieda emarginata (Ruiz & Pav.) Triana, Alchornea lojaensis Secco, and Prunus sp. These tree species were selected because of their appropriate wood anatomy.
Radial stem diameter variation was measured at 30-min intervals for each of one fertilized and one non-fertilized tree per species. Cumulative growth and daily stem radius change (dA) were calculated from these measurements (Deslauriers et al. 2007; Bräuning et al. 2009; Volland-Voigt et al. 2011). We defined drought spells as periods of at least four consecutive days without precipitation as registered at a nearby meteorological station. From July 2010, when the dendrometers were installed, to December 2010, nine dry spells occurred, the longest one of which showed no rainfall for 11 consecutive days (21.10.2010 to 31.10.2010). Altogether, tree data from 48 sampling days (sum of all days in drought spells) were subjected to analysis.
23.3 Results and Discussion: Rapid Effects of N and/or P Addition on Forest Productivity
23.3.1 Soil Respiration
Soil CO2 emissions did not differ between the control and nutrient-addition plots at the 1,000 m site. In contrast, N and N + P addition led to increased CO2 efflux at the 2,000 m site (p < 0.02; Tukey HSD test) as did N addition at the 3,000 m site (p < 0.01). The enhanced soil respiration with N addition at 3,000 m may be due to an increase in microbial biomass, as has been found by Corre et al. (2010) in thick soil organic layers of Panamanian tropical montane forests following N addition. But in our study at 2,000 m only after N + P addition an increase of microbial biomass C was recorded whereas N addition even reduced the microbial biomass (see Sect. 22.3). We were not able to distinguish between autotrophic and heterotrophic respiration and their responses to N addition, since we measured only gross soil CO2 emission rates.
23.3.2 Fine Root Biomass
This study found the highest fine root biomasses at the 2,000 m elevation. This was unexpected, since previous studies had recorded a continuous increase in fine root biomass along the transition from 1,000 m to 3,000 m (Röderstein et al. 2005; Moser et al. 2011). The present results show that the topographic position has a strong impact on root biomass in the study area. The high values at 2,000 m can be explained in terms of the location of the study plots on an upper slope, in contrast to the mid-slope position of the plots at the two other study sites. All three fertilization treatments at 1,000 m and 2,000 m resulted in a marked reduction in standing fine root biomass, with the effect being strongest after P addition (Fig. 23.2b). A decline of fine root biomass and a concurrent increase of dead root mass after nutrient addition have also been found in other montane forests when N was added (Cusack et al. 2011) or upon the addition of either N, P, or N + P (Gower and Vitousek 1989).
23.3.3 Fine Litter Production
A decrease in fine litter production with increasing elevation in tropical mountains is well documented (e.g., Moser et al. 2007) and may be explained by declines in tree leaf area and leaf production with increasing altitude coupled with higher mean leaf longevities. In our study the total amount of fine litter decreased after the first year of P addition at all elevations, whereas N and N + P addition had positive effects on litter production (Fig. 23.2c). An increase in litter production after N addition was also reported for other tropical montane forests by Adamek et al. (2009, Panama) and Tanner et al. (1992, Venezuela). Mirmanto et al. (1999) found that the addition of N, P, and the combination of N and P had positive effects on fine litter production in a lowland forest in Borneo.
23.3.4 Leaf Area Index
The LAI of the control plots decreased by 1.8 units upon an increase in altitude from 1,000 m to 3,000 m (Fig. 23.2d). This is well in accordance with the LAI decrease of about 1.1 units per km of elevation increase (from 500 to 2,000 m) reported by Unger et al. (2013) from northern Ecuador and with the average decrease of 1 unit per km of elevation increase reported in a pan-tropical review by Moser et al. (2007). We found LAI increases of 0.2–0.4 units after N, P, or N + P addition (except for the N-treatment at 3,000 m). In combination with the slightly higher foliar N concentrations after N addition (see Sect. 22.3) this should affect leaf photosynthetic capacity and ecosystem C sequestration positively (see Chap. 10, and Hyvönen et al. 2007). Since P addition increased the LAI but reduced fine litter production at all three elevations, mean leaf longevity must have been increased by the addition of 10 kg P ha−1 year−1.
23.3.5 Tree Growth
The annual stem diameter increment of montane forest trees is generally lower than that of tropical lowland trees. We accordingly found the highest mean radial growth rates and also the largest increases in the cumulative basal area of the plots at 1,000 m. At this altitude N addition as well as N + P addition resulted in a 20–30 % boost of the plot basal area increment in the first year after the start of the experiment (Fig. 23.2e). At 2,000 m and 3,000 m the addition of N or P led to only small positive or negative effects on basal area increment relative to the control. In contrast, the addition of both N and P had a marked positive effect, though less pronounced than that observed at 1,000 m.
A rapid increase in stem diameter growth of mature trees as a response to N addition has also been observed in other fertilization experiments, such as those in Jamaican montane forests (Tanner et al. 1990), in Hawaiian Metrosideros forests (Vitousek and Farrington 1997), and in Panamanian premontane forests (Adamek et al. 2009). However, Cavelier et al. (2000) found increased stem diameter growth in a Colombian elfin forest only when N and P were added together, and not when N or P was added alone.
23.3.6 Drought Sensitivity of Tree Growth After Nutrient Addition
Stem diameter characteristics and variation of N-fertilized (+N) and control (con) trees during dry spells over the period of July to December 2010 (n = 1 tree per species and treatment)
Dbh 2011 [cm]
Cum. growth [mm]
Mean dA [mm]
23.4 Conclusions: Implications for the Carbon Cycle in the Future
The rapid responses of the studied Andean montane forests to N and P addition observed at this early stage of the experiment illustrate the vulnerability of the forests to higher nutrient deposition. They also emphasize the urgent need for experimental studies on the effects of likely future alterations in the cycles of key elements in these forest ecosystems.
Since the forest canopy will become denser (increased LAI) upon fertilization and the trees will be relieved of growth constraints due to limited N and/or P availability, competition for light will increase among the trees with increasing input of nutrients. These changes may reduce the competitive ability of the seedlings and saplings of the currently abundant tree species in the understory and will in the long-term probably result in their eventual replacement by species adapted to more fertile soils. Changes in tree species composition (from slow-growing species adapted to nutrient-poor soils to faster growing species adapted to more fertile soils) will probably accelerate the projected shifts in the C cycle by increasing the biomass turnover rate.
The different tree species may respond in contrasting ways to elevated nutrient inputs. It is known for temperate forests that species which have a lower demand for N and are adapted to poorer soils are impacted more strongly by increases in N availability (Pardo et al. 2007). Drought sensitivity is another important tree trait that will shape future tree communities and is most likely to be affected by changes in nutrient availability.
Given the large stocks of carbon bound in the organic soil layers and also in the mineral soil (see Chap. 10), these forest ecosystems could represent significant sources of CO2 for the atmosphere in the future, since lower litter C/N ratios resulting from fertilization typically lead to faster decomposition rates. The large amounts of soil organic matter stored in these high-elevation forests make it likely that any change in the conditions controlling decomposition will result in large changes in the ecosystem C pool.
The results presented here summarize the short-term effects of nutrient addition evident at the end of the experiment’s first year. Given that these initial trends will persist, continued addition of substantial amounts of N and P will probably result in taller forests with a higher aboveground biomass but smaller belowground biomass. However, the belowground response of the system to nutrient addition is only poorly understood.
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