Next Article in Journal
Term and Preterm Birth Initiation Is Associated with the Macrophages Shifting to M1 Polarization in Gestational Tissues in Mice
Previous Article in Journal
Mycorrhizal Colonization Modulates the Essential Oil Profile and Enzymatic and Non-Enzymatic Antioxidants to Mitigate the Adverse Effects of Water Deficit in Salvia subg. Perovskia
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Biology
Volume 11
Issue 12
10.3390/biology11121758
biology-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Communication

Nitrogen and Carbon Mineralization from Green and Senesced Leaf Litter Differ between Cycad and Angiosperm Trees

by
Charles A. Paulino
1 and
Thomas E. Marler
2,*
1
Western Pacific Tropical Research Center, College of Natural and Applied Sciences, University of Guam, Mangilao, GU 96923, USA
2
Bagong Kaalaman Botanikal Institute, 15 Rizal Street, Barangay Malabañas, Angeles City 2009, Philippines
*
Author to whom correspondence should be addressed.
Biology 2022, 11(12), 1758; https://doi.org/10.3390/biology11121758
Submission received: 30 October 2022 / Revised: 24 November 2022 / Accepted: 1 December 2022 / Published: 3 December 2022
(This article belongs to the Section Ecology)
Browse Figures
Versions Notes

Abstract

:

Simple Summary

The addition of plant leaf litter to soils represents a critical component of the global carbon (C) and nitrogen (N) cycles. Tropical cyclones known at typhoons in the western Pacific islands transfer an enormous amount of green leaf litter from the forest canopy to the soil. We have shown on the island of Guam that this green litter releases carbon and nitrogen extremely rapidly compared with senesced leaf litter. Moreover, species such as Guam’s native cycad Cycas micronesica produce slowly decomposing litter, while other species such as Guam’s native angiosperm Morinda citrifolia produce rapidly decomposing litter. Soil priming is an important process in the global C cycle, and occurs when pre-existing organic matter releases more C as a result of new organic C additions. The green litter generated soil priming that was almost double that of the senesced litter. The release of N from the green litter into forms that are available to plants required only 14 d for the M. citrifolia litter but required more than 90 d for the C. micronesica litter. Scientists predict more frequent intense typhoons in the future, and we have shown one of the ecosystem-level processes that these typhoons will change.

Abstract

Plant leaf litter decomposition is directly influenced by the identity of the source plants and the leaf age. Defoliation of forests by tropical cyclones (TC) transfers copious amounts of high-quality green leaf litter to soils. We used a soil amendment approach with the incubated buried bag method to compare carbon (C) and nitrogen (N) mineralization dynamics of green and senesced leaf litter from cycad Cycas micronesica and angiosperm Morinda citrifolia trees on the island of Guam. Soil priming increased the decomposition of pre-existing organic C, and were greater for green leaf litter additions than senesced leaf litter additions. Available N content increased by day 14 and remained elevated for the entire 117-d incubation for soils amended with green M. citrifolia litter. In contrast, available N content increased above those in control soils by day 90 and above those in soils amended with senesced litter by day 117 for green C. micronesica litter. The net N mineralization rate was higher than control soils by 120% for the senesced litter treatments and 420% for the green litter treatments. The results reveal a complex but predictable interplay between TC defoliation and litter quality as defined by tree identity. We have illuminated one means by which increased frequency of intense TCs due to climate change may alter the global C and N cycles.

1. Introduction

Plant litter inputs to the soil system directly influence the dynamics of organic matter decomposition. Litter decomposition speed is partly resolved by litter chemistry which determines litter quality [1]. Therefore, plant species identity is a key modulator of litter decomposition [2]. Additionally, terrestrial ecosystems in the western Pacific are frequently influenced by tropical cyclone (TC) activity [3]. These large-scale disturbances often defoliate forests, adding copious amounts of high quality green leaf litter to the soil system [4,5]. Altogether, the identity of both species and the frequency of TCs interact in the insular habitats of the western Pacific to determine litter decomposition dynamics.
One of the disciplines in research on global carbon (C) and nitrogen (N) cycling is the soil priming effect. The priming effect occurs when the decomposition of native soil organic C increases in response to the input of fresh organic matter to the soil system [6,7,8,9]. A dominant factor controlling the mineralization during the decomposition of bulk soil organic matter during the priming effect is the chemistry of the new litter additions [10]. Soil priming has been discussed as a mediator in global-scale models of the C cycle [11], hence priming research is needed to understand all unique ecosystems, such as Oceania.
Among the 25 sympatric taxa that were influenced by a TC in a coastal Guam forest, the cycad Cycas micronesica K.D. Hill exhibited leaf chemistry with low quality litter, whereas the angiosperm Morinda citrifolia L. exhibited leaf chemistry with high quality litter [12]. To our knowledge, there have been no studies comparing actual litter decomposition or mineralization of these two sympatric indigenous tree species or addressing how TC defoliation influences these processes. Based on the fact that C. micronesica litter chemical traits have predicted recalcitrance and M. citrifolia litter chemical traits have predicted lability, we have hypothesized that the decomposition differences between soil amended with green versus senesced litter would be contrasting for C. micronesica and M. citrifolia leaves. We predicted that there would be differences between the decomposition of green and senesced leaves, which would become evident more rapidly for M. citrifolia and would become evident more slowly for C. micronesica.

2. Materials and Methods

Leaf litter was collected in northeast Guam from trees growing in coastal karst substrates that were formed in slope alluvium, loess, and residuum overlying limestone (Clayey-skeletal, gibbsitic, nonacid, isohyperthermic Lithic Ustorthents) [13]. The litter was collected in January 2018 from a single area of occupancy, in which, C. micronesica and M. citrifolia trees coexisted. Fresh senesced litter was collected as yellow leaves rather than brown leaves to ensure no nutrient leaching of the tissues had occurred following senescence. The youngest fully expanded green leaves were also collected from the same trees which provided the senesced litter. The leaf material was cut into 2 cm sections and then stored in paper bags in a laboratory at the University of Guam.
The speed of C and N mineralization from these sources of leaf litter was determined using a soil amendment approach by employing the buried bag method [14]. Fresh soil was collected from the surface (top 15 cm) in a forested portion of the University of Guam campus on 1 September 2018. The soil was the same karst soil series as the litter collection site, and there were numerous tree species that had contributed litter. We restricted the soil collection to locations where there was no prior exposure to C. micronesica or M. citrifolia litter to ensure there were no complications from home-field advantage effects [15]. Large rocks were extracted by hand and small rocks were filtered out with a sieve. After which, the bulk soil was thoroughly homogenized.
The initial nutrient content in each of the four categories of leaf litter was determined from three separate samples removed from the bulk dried leaf litter. Each sample was milled to pass through a 20-mesh screen. Total N and total C were determined by dry combustion (LECO CN Analyzer, LECO Corporation, St. Joseph, MI, USA).
The living soil was separated into 15 3-L samples for incubation. The air-dried litter for each species and leaf age was milled to pass through a 20-mesh screen, which was then separated into 100-g samples. Each 100-g sample was added to one of three 3-L samples of soil and homogenized to create three soil amendment replications per species–leaf age combination. This approach utilized 12 of the soil samples, and the remaining 3 3-L soil samples served as controls with no added leaf litter. Thus, there were 5 soil treatments with 3 replications. Control soils were not amended. Green litter M. citrifolia soils contained 100 g of green M. citrifolia litter, green C. micronesica soils contained 100 g of green C. micronesica litter, senesced M. citrifolia soils contained 100 g of senesced M. citrifolia litter, and senesced C. micronesica soils contained 100 g of senesced C. micronesica litter.
We had previously determined that the water holding capacity of this soil was 41%. We added water to each 3-L replication to approximate a 50% water holding capacity to ensure adequate moisture and aeration. An initial soil sample of 100 mL was extracted from each of the 15 bags to serve as day = 0 in the incubation study. Each sample that was collected was enclosed in a plastic bag and frozen at −20 °C. The remaining soil for each replication was enclosed in a 3.78-L resealable plastic bag for incubations.
The 15 bags were buried in an 80 cm × 420 cm mesocosm constructed in an open air laboratory setting on 2 September 2018. The mesocosm was filled with horticultural perlite, in which each bag was buried, and a randomized complete block design was employed using three blocks. Each bag was opened and the soil was thoroughly mixed every two weeks to ensure that the decomposing organic matter was redistributed throughout the mineral soil and that the carbon dioxide did not accumulate in the bags. Fresh weights were used to determine if there was water loss, and water was added to maintain a 50% water holding capacity whenever needed. Additionally, 100-g samples were removed at 14, 30, 60, 90, and 117 days and frozen at −20 °C. Therefore, there were 6 sampling periods, including the initial sampling period.
For chemical analyses, the soils were thawed to ambient temperature, then N and C components of the soil samples were determined as previously described [16]. Total N and total C were determined by dry combustion [17], and organic C was determined by dichromate consumption using the modified Walkley–Black protocol [18]. Nitrate N and ammonium N were determined colorimetrically following 2M potassium chloride extraction [19]. Available N was determined as the sum of the nitrate and ammonium content. Both the percentage of total N comprised of available N and the percentage of total C comprised of organic C were calculated. In addition to these analyses, which were conducted for every sampling date, we also determined the content of other characteristics for the unamended control soils by combining all sampling dates for each of the three replications. Extractable macronutrients other than phosphorus (P) were quantified following digestion with diethylenetriaminepentaacetic acid [20]. Analysis was completed using inductively coupled plasma optical emission spectrometry (Spectro Genesis; SPECTRO Analytical Instruments, Kleve, Germany). Available P was determined using the Olsen method [21]. Soil reaction was determined from saturated paste (Accumet AB200 meter, Thermo Fisher Scientific, Singapore).
The influence of the five soil treatments (control, green M. citrifolia, green C. micronesica, senesced M. citrifolia, and senesced C. micronesica) over 117 d of incubation on the C and N variables were assessed using factorial analysis with repeated measures according to the variance observed in five species–leaf age combinations, six sampling dates, and three replications treated as blocks (PROC MIXED, SAS Institute, Cary, NC, USA). The incubation time was designated as the repeated measure. Five different covariance structures were evaluated for each response variable according to Akaike information criterion. Compound symmetry was determined to be the best covariance structure for total N, total C, and percent organic C. Heterogeneous compound symmetry was determined to be the best structure for ammonium N, nitrate N, organic C, and percent available N. Finally, unstructured covariance structure was found to be the best covariance structure for available N. Mean separation for significant factors was conducted by Tukey’s honest significant difference.
In addition to the response variables that were determined for every sampling date, we calculated the efficiency of priming by subtracting the final organic C content of each primed soil bag in a block from the finalorganic C content in the corresponding control soil bag from each block. This metric represented the amount of organic C in the control soils that was mineralized by the activities of microorganisms stimulated by priming with the fresh organic matter additions. We used a one-way analysis of the variance to determine the influence of the four species–leaf age soil amendments on the efficiency of priming. Mean separation was conducted using Tukey’s honest significant difference.
We also calculated net N mineralization for each of the five soil treatments by subtracting the initial available N concentration from the final available N concentration, then dividing by the 117-d incubation duration. This metric is the sum of the net ammonification and net nitrification, and represents the release of inorganic N from soil organic matter. We used a one-way analysis of the variance to determine the influence of the five soil treatments on net N mineralization. Mean separation was conducted using Tukey’s honest significant difference.

3. Results

The incubation soils without amendments exhibited characteristics that were similar to those reported for this series of karst soil. Total N was 3.4 ± 0.4 mg·g−1, total C was 72.3 ± 4.8 mg·g−1, Olsen phosphorus was 89.6 ± 8.8 µg·g−1, extractable potassium was 354.7 ± 34.6 µg·g−1, extractable calcium was 18.5 ± 1.6 mg·g−1, extractable magnesium was 1289 ± 78.2 µg·g−1, and soil pH was 7.5 ± 0.1.
The senesced M. citrifolia litter samples contained 13.6 ± 1.6 mg·g−1 N and the senesced C. micronesica litter samples contained 19.8 ± 2.8 mg·g−1 N. The senesced M. citrifolia litter samples contained 473.8 ± 11.9 mg·g−1 C and the senesced C. micronesica litter samples contained 509.8 ± 19.8 mg·g−1 C. The green M. citrifolia litter samples contained 25.1 ± 3.6 mg·g−1 N and the green C. micronesica litter samples contained 26.7 ± 3.8 mg·g−1 N. The green M. citrifolia litter samples contained 433.5 ± 14.9 mg·g−1 C and the green C. micronesica litter samples contained 496.7 ± 21.8 mg·g−1 C.

3.1. Carbon Changes with Duration of Incubation

The total C, organic C, and the percentage of total C comprised by organic C were all influenced by the type of soil treatment (Table 1). Additionally, the organic C and percentage of C that was organic were also influenced by the time of sampling. The interaction of these two main factors (S × T) was not significant for any of the C response variables, therefore the changes related to incubation time were similar for each of the soil treatments.
The total C of the primed soil treatments are separated into two overlapping groups (Figure 1a). The soils primed with either the green or senesced leaf age categories of M. citrifolia exhibited the greatest total C throughout the 117-d incubation period. Soils primed with either of the two leaf age categories of C. micronesica exhibited a total C that was not different from that in the control soils. The organic C content of the primed soil treatments are separated into three groups (Figure 1b). The soils primed with green M. citrifolia leaf litter exhibited the greatest organic C content, followed by the soils primed with senesced M. citrifolia or green C. micronesica leaf litter. Organic C content of soils primed with senesced C. micronesica leaf litter did not differ from that in the control soils. The percentage of total C that was comprised of organic C can be separated into three groups (Figure 1c). The two green leaf litter priming treatments exhibited the greatest percentages, the two senesced leaf litter priming treatments exhibited intermediate percentages, and the control soils contained the least percentages of organic C.
The total C content in the primed soils was not influenced by the main factor of time and exhibited an overall mean of 73.5 mg·g−1. In contrast, organic C content in the primed soils declined 38% from day 0 to day 117 (Figure 2). Similarly, the percentage of total C comprised of organic C declined as the incubation duration progressed. The initial organic C percentage was 1.23-fold greater than the final organic C percentage.

3.2. Nitrogen Changes with Duration of Incubation

Total N content in the incubation soils was not influenced by the main effect of soil treatment or incubation time (Table 2). In contrast, the interaction of the treatment–incubation time (S × T) exerted a significant influence on the total N content. Ammonium N, nitrate N, available N, and the percentage of total N comprised of the available N were influenced by the main effect of soil treatment, the main effect of incubation time, and the interaction of the treatment–incubation time (Table 2).
Total N was limited in the incubation substrate and changed minimally throughout the 117-d incubation period. The means separated into two overlapping significantly different groups on days 14 and 60, but were not different among the other sampling dates (Figure 3a). Nitrate N did not differ among the soil treatments until day 60 when the nitrate N of green M. citrifolia soils was triple that of the other soil treatments (Figure 3b). This pattern persisted until day 90, but by day 117 the soils primed with green C. micronesica leaf litter exhibited nitrate N that was not different from that in the soils primed with green M. citrifolia, and the soils primed with the senesced litter of both species exhibited nitrate N that was intermediate. All four primed soil treatments contained more nitrate N than the control soil treatment on day 117. Ammonium N increased rapidly in the soils primed with green M. citrifolia leaf litter and reached a peak on day 30 (Figure 3c). By day 60 these M. citrifolia soils still contained ammonium N that was more than triple that of the ammonium N in the other four soil treatments. The five soil treatments did not differ in ammonium N content on days 90 and 117. The percentage of total N comprised of available N was greater in the soils primed with green M. citrifolia leaf litter than for the other soil treatments on day 14 through day 90 (Figure 3d). On day 117, the means of this metric separated into three groups, with the soils primed with green litter from both species exhibiting the highest values, the control soils exhibiting the smallest value, and the soils primed with senesced litter from both species exhibiting intermediate values. The trends in available N content (Figure 3e) were similar to those of the percentage of available N (Figure 3d). The early surge in ammonium N content in the soils primed with green M. citrifolia leaf litter combined with the later surge in nitrate N content in these soils to generate elevated available N from day 14 to day 90. The rapid increase in nitrate N content from day 90 to day 117 in the soils primed with green C. micronesica leaf litter caused the available N content to converge for the two green leaf litter soil treatments.

3.3. Soil Priming Effect and Net N Mineralization

The efficiency of the priming effect differed among the four primed soil treatments (f3,8 = 115.9; p < 0.001). Soils primed with the green leaf litter of both species contained about 0.45 mg·g−1 less organic C than the control soils at the end of the incubation period (Figure 4a). Soils primed with the senesced leaf litter of both species were not as efficient, and contained about 0.25 mg·g−1 less organic C than the control soils. These values suggest that the amount of organic C in the control soils was mineralized as a result of the priming effect.
Net mineralization differed among the five soil treatments (f4,10 = 690.9; p < 0.001). Soils primed with the senesced leaf litter of both species exhibited a daily production of available N that was 2.2-fold greater than that in the control soils (Figure 4b). Soils primed with the green leaf litter of both species exhibited a daily production of available N that was 5.1-fold greater than that in the control soils.

4. Discussion

On a global scale, soils contain more C than vegetation and the atmosphere [22,23], and plant litter inputs and decomposition represent a critical part of the role of soils in the C cycle [24]. Therefore, understanding the soil processes which promote soil C sequestration [25] and research into how tree species influence organic C in soils [26] are needed to mitigate climate change. We have shown that TC defoliation in the Mariana Islands of Guam is a consequential factor in understanding the C cycle of the region. As predicted by green and senesced leaf litter chemistry [12], mineralization of C in soils amended with green leaf litter was more rapid than in those soils amended with senesced leaf litter. Moreover, the priming effect of green leaf litter amendment was almost double that of the senesced leaf litter, representing the amount of native C that would have remained in soil organic matter if the litter additions had not occurred. We have also shown that the influence of species on litter quality exerted a direct influence on the early dynamics of N mineralization processes. The rate of increase in N mineralization for green litter was more rapid for the labile M. citrifolia litter than for the recalcitrant C. micronesica litter. In other words, the higher rate of litter decomposition of senesced M. citrifolia leaf litter was magnified by introducing green M. citrifolia litter to the soil system.
The components of available N were most contrasting during the early stages of decomposition. Net ammonium content increased almost 600% in only 30 d for soils amended with green M. citrifolia litter. In contrast, net ammonification of the soils amended with green C. micronesica litter kept pace with the nitrifying microbes, such that the ammonium content was never higher than that in the senesced leaf litter treatments. Similarly, net nitrification was evident earlier in the incubation for the soils primed with green M. citrifolia litter, which caused nitrate N to become elevated by day 30. This contrasted sharply with the green C. micronesica litter soils, which did not exhibit increased nitrate N until day 117.
The biodiversity of sympatric plant species enables heterogeneous litter components, and an additive effect of litter mixing has been heavily studied [27,28,29]. Our results illuminate how mixing different types of litter may also directly influence the availability of nutrients through the contrasting influence of initial mineralization processes. More research is needed to determine the influence of mixing these two litter sources. This is because the rapid accumulation of microbes responsible for ammonification caused by the green M. citrifolia litter additions may increase ammonification of the green C. micronesica litter and advance the mineralization process for the cycad litter. Our results provide an example of how spatiotemporal population levels of detritovore and decomposer soil microbe taxa may be dramatically influenced by litter identity.
Our methods did not quantify small organic molecules in the soils that may directly influence plant nutrition. For example, peptides and amino acids, which are sources of soil N, may be directly absorbed by some plant roots [30,31], mycorrhizal fungi [32,33,34,35], and non-mycorrhizal fungi and are known to partner with plant roots [36]. Leaf N resorption processes during senescence are primarily enabled by the hydrolysis of soluble proteins [37,38]. Therefore, a greater proportion of green leaf litter N may be contained in large organic N compounds because the hydrolysis of N-containing compounds to enable resorption of N is negated by TC defoliation prior to senescence. This larger pool of N macromolecules in green leaves than in senesced leaves may supply the soils with more peptides and amino acids, which may be absorbed by plant roots. These issues deserve further study.
The buried bag method was useful for understanding some of the dynamics of litter additions to this living soil in Guam. However, these methods disallowed the plant root uptake of newly available inorganic N and they disallowed the leaching losses of nitrate N. In situ mineralization studies need to be conducted to determine if the green and senesced leaf litter from these two indigenous tree species exert direct influences on N loss from the soils in a real ecological setting. The results predicted that the leaching losses from soils amended with green M. citrifolia litter may be less than the other soil treatments because much of the newly available inorganic N remained as ammonium N and was not readily nitrified. In contrast, the initial increases of inorganic N were primarily nitrate N for the green C. micronesica litter treatment and the senesced litter treatments for both species, and hence, nitrate is highly susceptible to leaching loss. These differences indicated that the nitrogen use efficiency may be greater for soils amended with green M. citrifolia litter because much of the available N was present in the root zone in a form that was less susceptible to leaching loss prior to plant root uptake.
The two model species we selected for this pilot study also illuminated an example of the cascading influences on ecosystem function caused by invasive species. Guam’s C. micronesica population has been decimated since the armored scale Aulacaspis yasumatsui Takagi invaded Guam in 2003 [39]. The C. micronesica population is the only native plant host for this invasive species. Moreover, herbivory of C. micronesica stems by feral pigs (Sus scrofa L.) increased after plant health was compromised by the armored scale herbivory [40]. In contrast, Guam’s M. citrifolia population has benefitted from endozoochory by feral pigs [41]. Guam forest inventories conducted in 2002 [42] and 2013 [43] corroborated these species-specific responses by documenting a 59% decrease and 26% increase in C. micronesica and M. citrifolia large trees, respectively, with a breast-height diameter greater than 12.7 cm. These invasive consumer species may indirectly exert profound influences on C and N cycling in Guam’s forests by continuing to reduce the recalcitrant C. micronesica litter inputs and increase the labile M. citrifolia litter inputs relative to other sympatric tree species.

5. Conclusions

Slowly decomposing leaf litter from trees such as C. micronesica provide an ecosystem service by enabling soil organic matter accumulation. Our results show that the green litter that is generated by TCs may mute the efficacy of that ecosystem service by increasing litter decomposition speed and increasing the C mineralization of pre-existing organic matter through the priming effect. The speed of N mineralization was influenced more by species than the speed of C mineralization, indicating localized shifts in C/N stoichiometry during the weeks following TCs. Our results revealed a complex but predictable interaction of TC defoliation and litter quality as defined by tree identity. We have illuminated one process by which increased frequency of intense TCs due to climate change may alter the C and N cycles in western Pacific islands.

Author Contributions

Conceptualization, T.E.M.; methodology, C.A.P. and T.E.M.; formal analysis, T.E.M.; resources, C.A.P.; data curation, T.E.M.; writing—original draft preparation, T.E.M.; writing—review and editing, C.A.P.; funding acquisition, T.E.M. All authors have read and agreed to the published version of the manuscript.

Funding

This research was partially funded by the United States Forest Service, Cooperative Agreement number 17-DG-11052021-217.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data available upon request.

Acknowledgments

We thank Dallas Johnson for the statistical analysis.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

References

  1. Aerts, R. Climate, leaf litter chemistry and leaf litter decomposition in terrestrial ecosystems: A triangular relationship. Oikos 1997, 79, 439–449. [Google Scholar] [CrossRef]
  2. Peng, Y.; Holmstrup, M.; Schmidt, I.K.; Bachega, L.R.; Schelfhout, S.; Zheng, H.; Heděnec, P.; Yue, K.; Vesterdal, L. Tree species identity is the predominant modulator of the effects of soil fauna on leaf litter decomposition. Forest Ecol. Manag. 2022, 520, 120396. [Google Scholar] [CrossRef]
  3. Marler, T.E. Pacific island tropical cyclones are more frequent and globally relevant, yet less studied. Front. Environ. Sci. 2014, 2, 42. [Google Scholar] [CrossRef] [Green Version]
  4. Wang, H.-C.; Wang, S.-F.; Lin, K.-C.; Lee Shaner, P.-J.; Lin, T.-C. Litterfall and element fluxes in a natural hardwood forest and a Chinese-fir plantation experiencing frequent typhoon disturbance in central Taiwan. Biotropica 2013, 45, 541–548. [Google Scholar] [CrossRef]
  5. Jaramillo, V.J.; Martínez-Yrízar, A.; Machado, L.I. Hurricane-induced massive nutrient return via tropical dry forest litterfall: Has forest biogeochemistry resilience changed? Ecosystems 2022, 25. [Google Scholar] [CrossRef]
  6. Kuzyakov, Y. Priming effects: Interactions between living and dead organic matter. Soil Biol. Biochem. 2010, 42, 1363–1371. [Google Scholar] [CrossRef]
  7. Bernard, L.; Basile-Doelsch, I.; Derrien, D.; Fanin, N.; Fontaine, S.; Guenet, B.; Karimi, B.; Marsden, C.; Maron, P.-A. Advancing the mechanistic understanding of the priming effect on soil organic matter mineralisation. Funct. Ecol. 2022, 36, 1355–1377. [Google Scholar] [CrossRef]
  8. Mo, F.; Ren, C.; Yu, K.; Zhou, Z.; Phillips, R.P.; Luo, Z.; Zhang, Y.; Dang, Y.; Han, J.; Ye, J.-S.; et al. Global pattern of soil priming effect intensity and its environmental drivers. Ecology 2022, 103, e3790. [Google Scholar] [CrossRef]
  9. Ren, C.; Mo, F.; Zhou, Z.; Bastida, F.; Delgado-Baquerizo, M.; Wang, J.; Zhang, X.; Luo, Y.; Griffis, T.J.; Han, X.; et al. The global biogeography of soil priming effect intensity. Glob. Ecol. Biogeogr. 2022, 31, 1679–1687. [Google Scholar] [CrossRef]
  10. Huys, R.; Poirier, V.; Bourget, M.Y.; Roumet, C.; Hättenschwiler, S.; Fromin, N.; Munson, A.D.; Freschet, G.T. Plant litter chemistry controls coarse-textured soil carbon dynamics. J. Ecol. 2022, in press. [Google Scholar] [CrossRef]
  11. Heimann, M.; Reichstein, M. Terrestrial ecosystem carbon dynamics and climate feedbacks. Nature 2008, 451, 289–292. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  12. Marler, T.E. Leaf elemental concentrations, stoichiometry, and resorption in Guam’s coastal karst forests. Diversity 2021, 13, 545. [Google Scholar] [CrossRef]
  13. Young, F.J. Soil Survey of Territory of Guam; U. S. Dept. of Agric. Soil Conservation Service: Washington, DC, USA, 1988. [Google Scholar]
  14. Eno, C.F. Nitrate production in the field by incubating the soil in polyethylene bags. Proc. Soil Sci. Soc. Am. 1960, 24, 277–279. [Google Scholar] [CrossRef]
  15. Palozzi, J.E.; Lindo, Z. Are leaf litter and microbes team players? Interpreting home-field advantage decomposition dynamics. Soil Biol. Biochem. 2018, 124, 189–198. [Google Scholar] [CrossRef]
  16. Marler, T.E. Perennial trees associating with nitrogen-fixing symbionts differ in leaf after-life nitrogen and carbon release. Nitrogen 2020, 1, 111–124. [Google Scholar] [CrossRef]
  17. Dumas, J.B.A. Procedes de L’analyse Organique. Ann. Chim. Phys. 1831, 47, 198–205. [Google Scholar]
  18. Nelson, D.W.; Sommers, L.E. Total carbon, organic carbon, and organic matter. In Methods of Soil Analysis. Part 3. Chemical Methods; SSSA Book Series No. 5; Sparks, D.L., Ed.; SSSA and ASA: Madison, WI, USA, 1996; pp. 961–1010. [Google Scholar]
  19. Cataldo, D.A.; Haroon, M.; Schrader, L.E.; Youngs, V.L. Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid. Commun. Soil Sci. Plant Anal. 1975, 6, 71–80. [Google Scholar] [CrossRef]
  20. Berghage, R.D.; Krauskopf, D.M.; Warncke, D.D.; Widders, I. Micronutrient testing of plant growth media extractant, identification and evaluation. Commun. Soil Sci. Plant Anal. 1987, 18, 1089–1109. [Google Scholar] [CrossRef]
  21. Olsen, S.; Cole, C.; Watanabe, F.; Dean, L.A. Estimation of Available Phosphorus in Soils by Extraction with Sodium Bicarbonate; USDA Circular Nr 939, US Gov. Print Office: Washington DC, USA, 1954. [Google Scholar]
  22. Lehmann, J.; Kleber, M. The contentious nature of soil organic matter. Nature 2015, 528, 60–68. [Google Scholar] [CrossRef]
  23. Hengl, T.; de Jesus, J.M.; Heuvelink, G.B.M.; Gonzalez, M.R.; Kilibarda, M.; Blagotić, A.; Shangguan, W.; Wright, M.N.; Geng, X.; Bauer-Marschallinger, B.; et al. SoilGrids250m: Global gridded soil information based on machine learning. PLoS ONE 2017, 12, e0169748. [Google Scholar] [CrossRef] [Green Version]
  24. Chapin, I.F.S.; Matson, P.A.; Vitousek, P. Principles of Terrestrial Ecosystem Ecology; Springer Science & Business Media: Berlin, Germany, 2011. [Google Scholar]
  25. Rumpel, C.; Amiraslani, F.; Koutika, L.-S.; Smith, P.; Whitehead, D.; Wollenberg, E. Put more carbon in soils to meet Paris climate pledges. Nature 2018, 564, 32–34. [Google Scholar] [CrossRef] [PubMed]
  26. Jandl, R.; Lindner, M.; Vesterdal, L.; Bauwens, B.; Baritz, R.; Hagedorn, F.; Johnson, D.W.; Minkkinen, K.; Byrne, K.A. How strongly can forest management influence soil carbon sequestration? Geoderma 2007, 137, 253–268. [Google Scholar] [CrossRef]
  27. Cassart, B.; Basia, A.A.; Jonard, M.; Ponette, Q. Average leaf litter quality drives the decomposition of single-species, mixed-species and transplanted leaf litters for two contrasting tropical forest types in the Congo Basin (DRC). Ann. For. Sci. 2020, 77, 33. [Google Scholar] [CrossRef]
  28. Liu, J.; Liu, X.; Song, Q.; Compson, Z.G.; LeRoy, C.J.; Luan, F.; Wang, H.; Hu, Y.; Yang, Q. Synergistic effects: A common theme in mixed-species litter decomposition. New Phytol. 2020, 227, 757–765. [Google Scholar] [CrossRef] [PubMed]
  29. Zhou, S.; Butenschoen, O.; Barantal, S.; Handa, I.T.; Makkonen, M.; Vos, V.; Aerts, R.; Berg, M.P.; McKie, B.; Van Ruijven, J.; et al. Decomposition of leaf litter mixtures across biomes: The role of litter identity, diversity and soil fauna. J. Ecol. 2020, 108, 2283–2297. [Google Scholar] [CrossRef]
  30. Hill, P.W.; Quilliam, R.S.; DeLuca, T.H.; Farrar, J.; Farrell, M.; Roberts, P.; Newsham, K.K.; Hopkins, D.W.; Bardgett, R.D.; Jones, D.L. Acquisition and assimilation of nitrogen as peptide-bound and D-enantiomers of amino acids by wheat. PLoS ONE 2011, 6, e19220. [Google Scholar] [CrossRef] [Green Version]
  31. Vranova, V.; Zahradnickova, H.; Janous, D.; Skene, K.R.; Matharu, A.S.; Rejsek, K.; Formanek, P. The significance of D-amino acids in soil, fate and utilization by microbes and plants: Review and identification of knowledge gaps. Plant Soil 2012, 354, 21–39. [Google Scholar] [CrossRef]
  32. Hawkins, H.J.; Johansen, A.; George, E. Uptake and transport of organic and inorganic nitrogen by arbuscular mycorrhizal fungi. Plant Soil 2000, 226, 275–285. [Google Scholar] [CrossRef]
  33. Leigh, J.; Hodge, A.; Fitter, A.H. Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material. New Phytol. 2009, 181, 199–207. [Google Scholar] [CrossRef]
  34. Talbot, J.M.; Treseder, K.K. Controls over mycorrhizal uptake of organic nitrogen. Pedobiologia 2010, 53, 169–179. [Google Scholar] [CrossRef] [Green Version]
  35. Miransari, M. Arbuscular mycorrhizal fungi and nitrogen uptake. Arch. Microbiol. 2011, 193, 77–81. [Google Scholar] [CrossRef] [PubMed]
  36. Hill, P.W.; Broughton, R.; Bougoure, J.; Havelange, W.; Newsham, K.K.; Grant, H.; Murphy, D.V.; Clode, P.; Ramayah, S.; Marsden, K.A.; et al. Angiosperm symbioses with non-mycorrhizal fungal partners enhance N acquisition from ancient organic matter in a warming maritime Antarctic. Ecol. Lett. 2019, 22, 2111–2119. [Google Scholar] [CrossRef] [PubMed]
  37. Lim, P.O.; Kim, H.J.; Gil Nam, H. Leaf senescence. Annu. Rev. Plant Biol. 2007, 58, 115–136. [Google Scholar] [CrossRef] [Green Version]
  38. Diaz, C.; Lemaitre, T.; Christ, A.; Azzopardi, M.; Kato, Y.; Sato, F.; Morot-Gaudry, J.F.; Le Dily, F.; Masclaux-Daubresse, C. Nitrogen recycling and remobilization are differentially controlled by leaf senescence and development stage in Arabidopsis under low nitrogen nutrition. Plant Physiol. 2008, 147, 1437–1449. [Google Scholar] [CrossRef] [Green Version]
  39. Marler, T.E.; Krishnapillai, M.V. Longitude, forest fragmentation, and plant size influence Cycas micronesica mortality following island insect invasions. Diversity 2020, 12, 194. [Google Scholar] [CrossRef]
  40. Deloso, B.E.; Terry, L.I.; Yudin, L.S.; Marler, T.E. Biotic threats to Cycas micronesica continue to expand to complicate conservation decisions. Insects 2020, 11, 888. [Google Scholar] [CrossRef] [PubMed]
  41. Gawel, A.M.; Rogers, H.S.; Miller, R.H.; Kerr, A.M. Contrasting ecological roles of non-native ungulates in a novel ecosystem. R. Soc. Open Sci. 2018, 5, 170151. [Google Scholar] [CrossRef]
  42. Donnegan, J.A.; Butler, S.L.; Grabowiecki, W.; Hiserote, B.A.; Limtiaco, D. Guam’s Forest Resources, 2002; Resource Bulletin PNW-RB-243; U.S. Department of Agriculture, Forest Service, Pacific Northwest Research Station: Portland, OR, USA, 2004. [Google Scholar]
  43. Lazaro, M.; Kuegler, O.; Stanton, S.; Lehman, A.; Mafnas, J.; Yatskov, M. Guam’s Forest Resources: Forest Inventory and Analysis, 2013; Resour. Bull. PNW-RB-270; U.S. Department of Agriculture, Forest Service, Pacific Northwest Research Station: Portland, OR, USA, 2020. [Google Scholar]
Biology 11 01758 g001 550
Figure 1. The influence of soil amendments with Cycas micronesica or Morinda citrifolia leaf litter on soil carbon traits. (a) Total C; (b) organic C; (c) percentage of total C comprised of organic C. Bars with same letter are not significantly different according to Tukey’s HSD. Mean ± standard error, n = 18.
Figure 1. The influence of soil amendments with Cycas micronesica or Morinda citrifolia leaf litter on soil carbon traits. (a) Total C; (b) organic C; (c) percentage of total C comprised of organic C. Bars with same letter are not significantly different according to Tukey’s HSD. Mean ± standard error, n = 18.
Biology 11 01758 g001
Biology 11 01758 g002 550
Figure 2. The influence of soil amendment with Cycas micronesica and Morinda citrifolia leaf litter on changes in carbon status over a 117-d incubation period. Means with the same letter are not statistically different according to Tukey’s HSD. Mean ± standard error, n = 18.
Figure 2. The influence of soil amendment with Cycas micronesica and Morinda citrifolia leaf litter on changes in carbon status over a 117-d incubation period. Means with the same letter are not statistically different according to Tukey’s HSD. Mean ± standard error, n = 18.
Biology 11 01758 g002
Biology 11 01758 g003 550
Figure 3. The influence of soil priming with Cycas micronesica or Morinda citrifolia leaf litter on changes in the nitrogen status over a 117-d incubation period. (a) Total N; (b) nitrate N; (c) ammonium N; (d) the percentage of total N comprised of available N; (e) available N. Means with same letter within each sampling date are not statistically different according to Tukey’s HSD. Dates with no letters indicate no differences among the soil treatment means.
Figure 3. The influence of soil priming with Cycas micronesica or Morinda citrifolia leaf litter on changes in the nitrogen status over a 117-d incubation period. (a) Total N; (b) nitrate N; (c) ammonium N; (d) the percentage of total N comprised of available N; (e) available N. Means with same letter within each sampling date are not statistically different according to Tukey’s HSD. Dates with no letters indicate no differences among the soil treatment means.
Biology 11 01758 g003
Biology 11 01758 g004 550
Figure 4. The influence of soil priming with Cycas micronesica or Morinda citrifolia leaf litter on changes in the nitrogen status during a 117-d incubation period. (a) efficiency of priming; (b) net mineralization. Bars with same letter are not statistically different according to Tukey’s HSD. Mean ± SE, n = 3.
Figure 4. The influence of soil priming with Cycas micronesica or Morinda citrifolia leaf litter on changes in the nitrogen status during a 117-d incubation period. (a) efficiency of priming; (b) net mineralization. Bars with same letter are not statistically different according to Tukey’s HSD. Mean ± SE, n = 3.
Biology 11 01758 g004
Table
Table 1. Results from 5 soil treatment × 6 incubation time factorial ANOVA for soil carbon (C) variables. n = 3.
Table 1. Results from 5 soil treatment × 6 incubation time factorial ANOVA for soil carbon (C) variables. n = 3.
Response
Variable		Soil Treatment
f4,58		Soil Treatment
p		Time
f5,58		Time
p		S × T
f20,58		S × T
p
Total C3.50.0491.80.1221.20.332
Organic C13.7<0.00112.4<0.0011.10.395
Percent organic C7.80.0075.1<0.0011.60.092
Table
Table 2. Results from 5 soil treatment × 6 incubation time factorial ANOVA for soil nitrogen (N) variables. n = 3.
Table 2. Results from 5 soil treatment × 6 incubation time factorial ANOVA for soil nitrogen (N) variables. n = 3.
Response
Variable		Soil Treatment
f4,58		Soil Treatment
p		Time
f5,58		Time
p		S × T
f20,58		S × T
p
Total N 3.70.0541.60.1692.30.010
Ammonium N109.3<0.00156.6<0.00151.1<0.001
Nitrate N151.5<0.001203.4<0.00122.3<0.001
Available N269.6<0.001202.0<0.001105.7<0.001
Percent available N68.1<0.001111.0<0.00113.0<0.001
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Paulino, C.A.; Marler, T.E. Nitrogen and Carbon Mineralization from Green and Senesced Leaf Litter Differ between Cycad and Angiosperm Trees. Biology 2022, 11, 1758. https://doi.org/10.3390/biology11121758

AMA Style

Paulino CA, Marler TE. Nitrogen and Carbon Mineralization from Green and Senesced Leaf Litter Differ between Cycad and Angiosperm Trees. Biology. 2022; 11(12):1758. https://doi.org/10.3390/biology11121758

Chicago/Turabian Style

Paulino, Charles A., and Thomas E. Marler. 2022. "Nitrogen and Carbon Mineralization from Green and Senesced Leaf Litter Differ between Cycad and Angiosperm Trees" Biology 11, no. 12: 1758. https://doi.org/10.3390/biology11121758

APA Style

Paulino, C. A., & Marler, T. E. (2022). Nitrogen and Carbon Mineralization from Green and Senesced Leaf Litter Differ between Cycad and Angiosperm Trees. Biology, 11(12), 1758. https://doi.org/10.3390/biology11121758

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop