Response of water-bound fluxes of potassium, calcium, magnesium and sodium to nutrient additions in an Ecuadorian tropical montane forest
Introduction
It is usually assumed that nutrient constraints limit vegetation development and primary production of tropical forests, which are mainly regulated by the supply of the key nutrients N and P (Vitousek, 1984, Vitousek and Howarth, 1991, Vitousek et al., 1993, Tanner et al., 1998, LeBauer and Treseder, 2008, Fisher et al., 2013). This was confirmed by a number of nutrient manipulation experiments focusing on N and P amendments to ecosystems (Tanner et al., 1990, Tanner et al., 1992, Elser et al., 2007, Bobbink et al., 2010, Ceulemans et al., 2014).
In the humid tropical montane forest of south Ecuador on the Amazon-exposed Andean slope, multiple effects of nutrient additions and indications of N and P co-limitation of the ecosystem have been found with respect to soil microorganisms (Krashevska et al., 2010), short-term N, P and Ca cycling (Wullaert et al., 2010, Wullaert et al., 2013), aboveground and belowground biomass (Homeier et al., 2012), nitrous oxide fluxes (Martinson et al., 2013; Müller et al., 2015), N cycling in organic material of canopy soils (Matson et al., 2014), performance of tree seedlings and tree seedlings traits (Cárate-Tandalla et al., 2015, Cárate-Tandalla et al., 2018), phosphatase activity (Dietrich et al., 2016), dissolved organic matter cycling and N leaching (Velescu et al., 2016), wood anatomical traits (Spannl et al., 2016) and tree growth (Báez and Homeier, 2018).
In addition, an increasing number of studies revealed the importance of other elements as well as of co-limitations by multiple nutrients in tropical ecosystems (Chapin et al., 1986, Kaspari et al., 2008, Vitousek et al., 2010, Harpole et al., 2011, Kaspari and Powers, 2016). There is evidence that also the alkali and alkaline earth metals potassium (K), calcium (Ca), magnesium (Mg) and sodium (Na), which are commonly called base cations, are able to constrain biological functioning in tropical forests (Wright et al., 2011, Baribault et al., 2012, Wullaert et al., 2013, Kaspari et al., 2014). These are essential nutrients, life supporting elements in all ecosystems worldwide and their supply is mainly governed by weathering of primary minerals from the parent rocks, atmospheric deposition and internal cycling (Jobbagy and Jackson, 2001, Jobbágy and Jackson, 2004). Terrestrial plants require K for phloem transport, osmotic balance and photosynthesis (Tripler et al., 2006), while Ca is essential as a structural component of cell walls and membranes, for enzyme activation, stomatal regulation and cell division (White and Broadley, 2003), and Mg is a central atom of chlorophyll molecules (Gransee and Führs, 2013). Investigations in a tropical lowland forest in Panama revealed that K, P and N can limit allocation of assimilates to roots, tree growth, or litter production (Wright et al., 2011), while multiple nutrients limited productivity (Turner and Wright, 2014). The response of extractable nutrients to climate seasonality and long-term fertilizer amendments varied depending on the nature of their biogeochemical cycling (Turner et al., 2013). Multiple co-limitations of primary production by N, P and K were shown to co-exist in grassland ecosystems (Fay et al. 2015). Further studies showed that Ca or K alone may limit plant growth, or co-limit in addition to N and P (Cuevas and Medina, 1988). Although required in smaller amounts, Mg is essential for plant growth, but its availability to plants is strongly affected by the availability of other cations like NH4+, Ca2+ and K+ (Fageria, 2001, Gransee and Führs, 2013). In a catchment under tropical montane forest in south Ecuador, Wilcke et al. (2017) quantified all major Ca, K and Mg fluxes from 1998 to 2013 and showed that the size of their aboveground fluxes was much larger than the fluxes related with sorption to soil and weathering.
Sodium is an omnipresent element which is essential especially for animals (Hill et al., 2016). Although the effects of Na on biota are mainly discussed in view of salinity in arid ecosystems (Munns and Tester, 2008, Keisham et al., 2018), recent studies in tropical forests found that Na also affected decomposition of organic matter and, therefore, the carbon cycle (Kaspari et al., 2014), when Na supply from soils and atmospheric deposition was low and the demand of soil fauna was not sufficiently covered. Furthermore, several beneficial effects of Na on plant nutrition were reported (Kronzucker et al., 2013). In a long-term ecosystem study in the tropical montane forest of south Ecuador, Na was retained in the aboveground, biotic part of the studied micro-catchment (Wilcke et al., 2017). This retention was related with a general scarcity of Na in the ecosystem.
Base cation cycling may be influenced by N deposition from the atmosphere, availability of mineral N species, as well as by leaching and retention (Matzner et al., 2004; Lucas et al., 2011). Increasing N supply can stimulate biomass production in N-limited systems and lead to increased uptake of base cations from the soils (Vitousek and Howarth, 1991). However, nitrate (NO3−) leaching can affect base cation availability more than soil parent material (Perakis et al., 2006). If available N cannot be efficiently used because of the scarcity of other co-limiting elements like P, or if N inputs exceed the uptake by plant roots, N could be ultimately leached as NO3− from the root zone (Velescu et al., 2016), which may be accompanied by base cations for charge equilibrium reasons (Currie et al., 1999, Cusack et al., 2016). Thus, when N inputs are elevated and N leaching occurs, this may lead to sustained cation losses and to a depletion of alkali and alkaline earth metals from the topsoils (Lucas et al., 2011). Calcium amendments either as carbonates or as neutral salts are a common management approach in forest soils depleted of base cations resulting from acidic deposition. Additions of Ca are known to improve available Ca stocks, cation exchange capacity and mitigate Al toxicity (Johnson et al., 2014). However, added Ca may increase leaching of K and Mg and have antagonistic effects on K and Mg uptake at high Ca concentrations in soil solution (Fageria, 2009). Similar to N, an improvement of the P supply may affect base cations fluxes in P-limited tropical forests. In the short term, alleviation of P limitation may increase exchangeable K+, Ca2+, and Mg2+ pools as a consequence of the stimulation of microbial biomass, litterfall production and nutrient return with litterfall by phosphorus (Zhu et al., 2015). In a N-rich tropical forest, beneficial effects of P additions on base cation availability were, however, reported to disappear after six years of P amendments (Mao et al., 2017).
It has been shown that forest ecosystems in south Ecuador receive considerable, but highly variable Ca and Mg inputs via episodic Sahara dust deposition transported by the northeasterly trade winds from North Africa over the Atlantic and the Amazon basin and that these elements accumulate in the topsoils and organic layers (Boy and Wilcke, 2008, Wilcke et al., 2013, Wilcke et al., 2017). Furthermore, high Ca retention observed during periods with elevated atmospheric Ca deposition suggested deficiencies in Ca supply to the plants (Boy and Wilcke, 2008), but not all plant species benefited from improved Ca availability (Wullaert et al., 2013). Low, but constant amounts of phosphorus were also reported to reach these remote ecosystems (Wilcke et al., 2019).
However, between Sahara dust deposition periods, which are mainly associated with variable La Niña events, increasing nitric acid and ammonium inputs reach the forests on the east Andean cordillera (Wilcke et al., 2013), which are buffered by the release of base cations from the forest canopy and the soils. Considering the multiple interactions among all nutrients, understanding the effects of globally increasing N availability (Galloway et al., 2008) on base cation fluxes is of great importance when predicting the response of tropical forest ecosystems to environmental change. Although it could have been expected that increasing N deposition would favor acidification (Malhi et al., 1998; Larssen et al., 2011, Mao et al., 2017), this was not supported by field observations in the tropical montane forest of South Ecuador (Wilcke et al., 2017, Wilcke et al., 2020). Experimental nutrient additions did not affect pH values of throughfall and litter leachate (Velescu et al., 2016), while Ca amendments accelerated Ca cycling, but leaching and ecosystem fluxes of other nutrients were not significantly affected in the short term (Wullaert et al., 2013). However, if N deposition from the atmosphere further increases and climatic conditions for nitrification are additionally improved by rising temperatures and longer dry spells reducing soil waterlogging periods (Peters et al., 2013, Rollenbeck et al., 2015, Wilcke et al., 2020), a future risk of net depletion of K, Ca, Mg and Na from the root zone cannot be excluded, if element losses exceed the inputs by atmospheric deposition.
Therefore, our objective was to elucidate the response of all major aqueous K, Ca, Mg and Na ecosystem fluxes in a tropical montane forest to N, P and Ca amendments in a nutrient manipulation experiment (NUMEX), in which N, P, N + P and Ca were fertilized at moderate levels considered as reflecting realistic future changes in nutrient availability. We hypothesized that (i) the combined addition of the limiting nutrients N and P increases the demand of K, Ca and Mg, tightening their cycling by reducing their leaching losses from the soil; (ii) the separate addition of N as urea enhances leaching of base cations together with NO3− resulting from nitrification; (iii) amendments of N + P and P alone as NaH2PO4·H2O generally increase Na leaching, but the Na included in the P fertilizer is only partly leached from the organic layer in spite of its high acidity; (iv) in the Ca-poor montane forest, the addition of Ca results in increased plant Ca uptake reflected by a faster Ca cycling between the forest canopy and the organic layer.
Section snippets
Study area
The study area is located in the province of Zamora-Chinchipe, on the Amazon-exposed slopes of the south Ecuadorian Andes (3.58° S, 79.08 W). The experimental plots were established in the Reserva Biológica San Francisco at an elevation of 2010–2128 m a.s.l. (Fig. 1).
The slope of the plots ranges between 15° and 40°, with an average of 28°. Precipitation is unimodally distributed over the year and reaches its maximum between April and July, yet without a marked dry season. Between 2007 and
Water fluxes
During the five years after the start of nutrient amendments, mean annual precipitation was 2070 ± 166 mm (SD). The water cycle of NUMEX was characterized by high annual interception of 819 ± 62 mm which corresponded to 40 ± 2% of the annual precipitation (Table 1). Annual ETr averaged 1479 ± 80 mm or 72 ± 9% of the mean annual precipitation, while transpiration averaged 660 ± 113 mm year−1 over the five years. Annual water fluxes with litter leachate percolating through the organic layer
Effects of N and P amendments on K, Ca and Mg fluxes
There was no significant effect of the N + P treatment on the mean response ratios of K, Ca and Mg fluxes with throughfall over five years (Fig. 2), although leaf litter production, specific leaf areas of the most common tree species and tree growth increased (Homeier et al., 2012, Báez and Homeier, 2018), revealing thus positive, synergistic effects of the combined N and P additions on forest development. This response to N + P amendments should have stimulated, in turn, the demand for K, Ca,
Conclusions
The combined amendment of the co-limiting nutrients N and P to the studied tropical montane forest ecosystem gradually increased Ca and Mg fluxes from the canopy with time. Because H+, Ca, and Mg deposition did not change during the observation period, the increasing Ca and Mg fluxes can be mainly attributed to leaching from the leaves, possibly indicating an increased uptake of these elements if N + P co-limitation is alleviated. Potassium cycling between canopy and organic layer became
CRediT authorship contribution statement
Andre Velescu: Conceptualization, Investigation, Formal analysis, Writing – original draft, Writing – review & editing. Jürgen Homeier: Conceptualization, Methodology, Writing – review & editing. Jörg Bendix: Conceptualization, Resources, Writing – review & editing. Carlos Valarezo: Conceptualization, Resources, Writing – review & editing. Wolfgang Wilcke: Conceptualization, Methodology, Writing – review & editing, Project administration, Funding acquisition.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
We thank Hans Wullaert for the initial establishment of NUMEX, Arthur Broadbent and Hannes Thomasch for their contribution to the field work in Ecuador and to the chemical analyses in Bern, Thorsten Peters and Rütger Rollenbeck for their support with the climate data and José Luis Peña Caivinagua for his help as a field technician. We thank the Deutsche Forschungsgemeinschaft (DFG) for funding our project within the research units FOR 402 and FOR 816. Furthermore, we thank Naturaleza y Cultura
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