Hurricane Otto’s influence on a tropical forests soil carbon, nitrogen, decomposition, and decomposer microbial communities over 5 years

Highlights

	● Hurricane Otto caused sequential changes in tropical soil microbiota over 5 years.
	● Acidobacteria were critical early decomposers of deposited canopy debris for 3 years.
	● Complex C degrading fungi were critical later decomposers of debris starting at 4 years.
	● A suite of C, N and microbial indicators should prove valuable for forest managers.

Abstract

Hurricanes cause significant damage to tropical forests; however, little is known of their effects on decomposition and decomposer communities. This study demonstrated that canopy debris deposited during Hurricane Otto stimulated sequential changes in soil carbon (C) and nitrogen (N) components, and decomposer microbial communities over 5 years. The initial response phase occurred within 2 years post-hurricane and appeared associated with decomposition of the labile canopy debris, suggested by: increased DNA sequences (MPS) of the Acidobacterial community (as common decomposers of labile plant material), decreases in total organic C (TOC), increased biomass C, respiration, and ${\text{NH}}_{\text{4}}^{+}$, conversion of organic C in biomass, and decreased MPS of complex organic C decomposing (CCDec) Fungal community. After 3 years post-hurricane, the later response phase appeared associated with decomposition of the more stable components of the canopy debris, suggested by: increased MPS of the Fungal CCDec community, TOC, stabilized Respiration, decreased Biomass C, the return to pre-hurricane levels of the conversion of organic C to biomass, and decreased MPS of Acidobacterial community. These changes in the microbial community compositions resulted in progressive decomposition of the hurricane-deposited canopy material within 5 years, resulting several potential indicators of different stages of decomposition and soil recovery post-disturbance.

Graphical abstract

Keywords

hurricane effects on soil ecosystem / Acidobacterial response to disturbance / fungal decomposer response to disturbance / hurricane influences on qCO₂ and qMic / hurricane effects on microbial decomposers

References

[1] Alef, K., Nannipieri, P., 1995. Methods in Applied Soil Microbiology and Biochemistry. London, UK: Academic Press.

[2] Allison, S. D., Martiny, J. B. H., 2008. Colloquium paper: resistance, resilience, and redundancy in microbial communities. Proceedings of the National Academy of Sciences of the United States of America105, 1512–1519.

[3] Anderson, J. M., Ingram, J. S. I., 1993. Tropical Soil Biology and Fertility: A Handbook of Methods. 2nd ed. Wallingford, Oxfordshire, UK: CAB International.

[4] Anderson, M. J., Gorley, R. N., Clarke, R. K., 2008. PERMANOVA+ for Primer: Guide to Software and Statistical Methods. Plymouth, UK: PRIMER-e Learning Hub.

[5] Anderson, T. H., Domsch, K. H., 1989. Ratios of microbial biomass carbon to total organic-carbon in arable soils. Soil Biology and Biochemistry21, 471–479.

[6] Anderson, T. H., Domsch, K. H., 2010. Soil microbial biomass: the eco-physiological approach. Soil Biology and Biochemistry42, 2039–2043.

[7] Andrews, J. H., Harris, R. F., 1986. r- and K-selection and microbial ecology. In: Marshall, K. C., ed. Advances in Microbial Ecology. Boston, MA: Springer, 99–147.

[8] Banerjee, S., Kirkby, C. A., Schmutter, D., Bissett, A., Kirkegaard, J. A., Richardson, A. E., 2016. Network analysis reveals functional redundancy and keystone taxa amongst bacterial and fungal communities during organic matter decomposition in an arable soil. Soil Biology and Biochemistry97, 188–198.

[9] Bardgett, R. D., van der Putten, W. H., 2014. Belowground biodiversity and ecosystem functioning. Nature515, 505–511.

[10] Betcheva, R., Georgieva, N., Yotova, L., Valchev, I., Chadjiska, C., 2008. Biobleaching of flax fibers by degradation of lignin with Phanerochaete chrysosporium and Trichosporon cutaneum R57. Journal of Natural Fibers4, 31–40.

[11] Bohacz, J., Korniłłowicz-Kowalska, T., 2020. Modification of post-industrial lignin by fungal strains of the genus Trichoderma isolated from different composting stages. Journal of Environmental Management266, 110573.

[12] Brown, D. P., 2017. National Hurricane Center Tropical Cyclone Report Hurricane Otto (AL162016, EP22016). Miami: National Hurricane Center.

[13] Brown, M. E., Chang, M. C., 2014. Exploring bacterial lignin degradation. Current Opinion in Chemical Biology19, 1–7.

[14] Cantrell, S. A., Molina, M., Jean Lodge, D., Rivera-Figueroa, F. J., Ortiz-Hernández, M. L., Marchetti, A. A., Cyterski, M. J., Pérez-Jiménez, J. R., 2014. Effects of a simulated hurricane disturbance on forest floor microbial communities. Forest Ecology and Management332, 22–31.

[15] Caporaso, J. G., Lauber, C. L., Walters, W. A., Berg-Lyons, D., Lozupone, C. A., Turnbaugh, P. J., Fierer, N., Knight, R., 2011. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proceedings of the National Academy of Sciences of the United States of America108, 4516–4522.

[16] Chassot, O., Monge, G., Powell, G., Wright, P., Palminteri, S., 2005. San Juan-La Selva Biological Corridor, Costa Rica. 1–101.

[17] Clarke, K. R., Gorley, R. N., 2006. PRIMER v6: User Manual. Plymouth, UK: PRIMER-E Ltd.

[18] Cornwell, W. K., Cornelissen, J. H. C., Amatangelo, K., Dorrepaal, E., Eviner, V. T., Godoy, O., Hobbie, S. E., Hoorens, B., Kurokawa, H., Pérez‐harguindeguy, N., Quested, H. M., Santiago, L. S., Wardle, D. A., Wright, I. J., Aerts, R., Allison, S. D., Van Bodegom, P., Brovkin, V., Chatain, A., Callaghan, T. V., Díaz, S., Garnier, E., Gurvich, D. E., Kazakou, E., Klein, J. A., Read, J., Reich, P. B., Soudzilovskaia, N. A., Vaieretti, M. V., Westoby, M., 2008. Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecology Letters11, 1065–1071.

[19] Datta, R., Kelkar, A., Baraniya, D., Molaei, A., Moulick, A., Meena, R. S., Formanek, P., 2017. Enzymatic degradation of lignin in soil: a review. Sustainability9, 1163.

[20] De Chaves, M. G., Silva, G. G. Z., Rossetto, R., Edwards, R. A., Tsai, S. M., Navarrete, A. A., 2019. Acidobacteria subgroups and their metabolic potential for carbon degradation in sugarcane soil amended with vinasse and nitrogen fertilizers. Frontiers in Microbiology10, 1680.

[21] Eaton, W. D., Hamilton, D. A., 2023. Enhanced carbon, nitrogen and associated bacterial community compositional complexity, stability, evenness, and differences within the tree-soils of Inga punctata along an age gradient of planted trees in reforestation plots. Plant and Soil484, 327–346.

[22] Eaton, W. D., McGee, K. M., Alderfer, K., Jimenez, A. R., Hajibabaei, M., 2020a. Increase in abundance and decrease in richness of soil microbes following Hurricane Otto in three primary forest types in the Northern Zone of Costa Rica. PLoS One15, e0231187.

[23] Eaton, W. D., McGee, K. M., Donnelly, R., Lemenze, A., Karas, O., Hajibabaei, M., 2019. Differences in the soil microbial community and carbon-use efficiency following development of Vochysia guatemalensis tree plantations in unproductive pastures in Costa Rica. Restoration Ecology27, 1263–1273.

[24] Eaton, W. D., McGee, K. M., Donnelly, R., Lemenze, A., Larimer, M., Hajibabaei, M., 2021b. The impacts of a logging road on the soil microbial communities, and carbon and nitrogen components in a Northern Zone Costa Rican Forest. Applied Soil Ecology164, 103937.

[25] Eaton, W. D., McGee, K. M., Hoke, E., Lemenze, A., Hajibabaei, M., 2020b. Influence of two important leguminous trees on their soil microbiomes and nitrogen cycle activities in a primary and recovering secondary forest in the northern zone of Costa Rica. Soil Systems4, 65.

[26] Eaton, W. D., McGee, K. M., Larimer, M., Hoke, E., Karas, O., Hernandez, B., Wayland, N. A., 2021a. Changes in soil bacterial communities, and carbon and nitrogen metrics as potential indicators of land use effects in a humid tropical forest. Pedobiologia 85–86, 150730.

[27] Eichorst, S. A., Trojan, D., Roux, S., Herbold, C., Rattei, T., Woebken, D., 2018. Genomic insights into the Acidobacteria reveal strategies for their success in terrestrial environments. Environmental Microbiology20, 1041–1063.

[28] Ettema, C., 2002. Spatial soil ecology. Trends in Ecology & Evolution17, 177–183.

[29] Fierer, N., Bradford, M. A., Jackson, R. B., 2007. Toward an ecological classification of soil bacteria. Ecology88, 1354–1364.

[30] Gardes, M., Bruns, T. D., 1993. ITS primers with enhanced specificity for basidiomycetes -application to the identification of mycorrhizae and rusts. Molecular Ecology2, 113–118.

[31] Gavito, M. E., Sandoval-Pérez, A. L., del Castillo, K., Cohen-Salgado, D., Colarte-Avilés, M. E., Mora, F., Santibáñez-Rentería, A., Siddique, I., Urquijo-Ramos, C., 2018. Resilience of soil nutrient availability and organic matter decomposition to hurricane impact in a tropical dry forest ecosystem. Forest Ecology and Management426, 81–90.

[32] Giweta, M., 2020. Role of litter production and its decomposition, and factors affecting the processes in a tropical forest ecosystem: a review. Journal of Ecology and Environment44, 11.

[33] González, G., Lodge, D. J., Richardson, B. A., Richardson, M. J., 2014. A canopy trimming experiment in Puerto Rico: the response of litter decomposition and nutrient release to canopy opening and debris deposition in a subtropical wet forest. Forest Ecology and Management332, 32–46.

[34] Griffiths, B. S., Philippot, L., 2013. Insights into the resistance and resilience of the soil microbial community. FEMS Microbiology Reviews37, 112–129.

[35] Grimm, V., Wissel, C., 1997. Babel, or the ecological stability discussions: an inventory and analysis of terminology and a guide for avoiding confusion. Oecologia109, 323–334.

[36] Gutiérrez del Arroyo, O., Silver, W. L., 2018. Disentangling the long-term effects of disturbance on soil biogeochemistry in a wet tropical forest ecosystem. Global Change Biology24, 1673–1684.

[37] Hartshorn, G. S., Hammel, B. E., 1994. Vegetation types and floristic patterns. In: McDade, L. A., Bawa, K. S., Hespenheide, H. A., Hartshorn, G. S., eds. La Selva: Ecology and Natural History of a Neotropical Rain Forest. Chicago, IL: The University of Chicago Press.

[38] Hatakka, A., Hammel, K. E., 2010. Fungal biodegradation of lignocelluloses. In: Hofrichter, M., eds. Industrial Applications. 2nd ed. Berlin, Heidelberg: Springer, 319–340.

[39] Hsieh, H. M., Ju, Y. M., Rogers, J. D., 2005. Molecular phylogeny of Hypoxylon and closely related genera. Mycologia97, 844–865.

[40] Janusz, G., Pawlik, A., Sulej, J., Świderska-Burek, U., Jarosz-Wilkołazka, A., Paszczyński, A., 2017. Lignin degradation: microorganisms, enzymes involved, genomes analysis and evolution. FEMS Microbiology Reviews41, 941–962.

[41] Kamimura, N., Takahashi, K., Mori, K., Araki, T., Fujita, M., Higuchi, Y., Masai, E., 2017. Bacterial catabolism of lignin-derived aromatics: new findings in a recent decade: update on bacterial lignin catabolism. Environmental Microbiology Reports9, 679–705.

[42] Kielak, A. M., Barreto, C. C., Kowalchuk, G. A., van Veen, J. A., Kuramae, E. E., 2016. The Ecology of Acidobacteria: moving beyond genes and genomes. Frontiers in Microbiology7, 744.

[43] Knutson, T., 2023. Global Warming and Hurricanes: An Overview of Current Research Results. New York: Geophysical Fluid Dynamics Laboratory.

[44] Liu, K. L., Porras-Alfaro, A., Kuske, C. R., Eichorst, S. A., Xie, G., 2012. Accurate, rapid taxonomic classification of fungal large subunit rRNA genes. Applied and Environmental Microbiology78, 1523–1533.

[45] Liu, X.B., Zeng, X. C., Zou, X. M., González, G., Wang, C., Yang, S., 2018a. Litterfall production prior to and during hurricanes Irma and Maria in four Puerto Rican forests. Forests9, 367.

[46] Liu, X. B., Zeng, X. C., Zou, X. M., Lodge, D. J., Stankavich, S., González, G., Cantrell, S. A., 2018b. Responses of soil labile organic carbon to a simulated hurricane disturbance in a tropical wet forest. Forests9, 420.

[47] Lodge, D. J., Cantrell, S. A., González, G., 2014. Effects of canopy opening and debris deposition on fungal connectivity, phosphorus movement between litter cohorts and mass loss. Forest Ecology and Management332, 11–21.

[48] Lodge, D. J., Winter, D., González, G., Clum, N., 2016. Effects of hurricane-felled tree trunks on soil carbon, nitrogen, microbial biomass, and root length in a wet tropical forest. Forests7, 264.

[49] Louca, S., Doebeli, M., 2016. Transient dynamics of competitive exclusion in microbial communities. Environmental Microbiology18, 1863–1874.

[50] Louca, S., Polz, M. F., Mazel, F., Albright, M. B. N., Huber, J. A., O’connor, M. I., Ackermann, M., Hahn, A. S., Srivastava, D. S., Crowe, S. A., Doebeli, M., Parfrey, L. W., 2018. Function and functional redundancy in microbial systems. Nature Ecology & Evolution2, 936–943.

[51] Lugo, A. E., 2008. Visible and invisible effects of hurricanes on forest ecosystems: an international review. Austral Ecology33, 368–398.

[52] McGee, K. M., Eaton, W. D., Shokralla, S., Hajibabaei, M., 2019. Determinants of soil bacterial and fungal community composition toward carbon-use efficiency across primary and secondary forests in a Costa Rican conservation area. Microbial Ecology77, 148–167.

[53] Moorhead, D. L., Sinsabaugh, R. L., 2006. A theoretical model of litter decay and microbial interaction. Ecological Monographs76, 151–174.

[54] Mori, A. S., Isbell, F., Fujii, S., Makoto, K., Matsuoka, S., Osono, T., 2016. Low multifunctional redundancy of soil fungal diversity at multiple scales. Ecology Letters19, 249–259.

[55] National Oceanic, Atmospheric Administration., 2023. State of the Science FACT SHEET: Atlantic Hurricanes and Climate Change.

[56] Navarrete, A. A., Venturini, A. M., Meyer, K. M., Klein, A. M., Tiedje, J. M., Bohannan, B. J. M., Nüsslein, K., Tsai, S. M., Rodrigues, J. L. M., 2015. Differential response of Acidobacteria subgroups to forest-to-pasture conversion and their biogeographic patterns in the western Brazilian Amazon. Frontiers in Microbiology6, 1443.

[57] Nemergut, D. R., Schmidt, S. K., Fukami, T., O’Neill, S. P., Bilinski, T. M., Stanish, L. F., Knelman, J. E., Darcy, J. L., Lynch, R. C., Wickey, P., Ferrenberg, S., 2013. Patterns and processes of microbial community assembly. Microbiology and Molecular Biology Reviews77, 342–356.

[58] Ortiz-Álvarez, R., Fierer, N., de los Ríos, A., Casamayor, E. O., Barberán, A., 2018. Consistent changes in the taxonomic structure and functional attributes of bacterial communities during primary succession. The ISME Journal12, 1658–1667.

[59] Ostertag, R., Scatena, F. N., Silver, W. L., 2003. Forest floor decomposition following hurricane litter inputs in several Puerto Rican forests. Ecosystems6, 261–273.

[60] Peng, J. W., Liu, H., Hu, Y., Sun, Y., Liu, Q., Li, J. G., Dong, Y. H., 2022. Shift in soil bacterial communities from K- to r-strategists facilitates adaptation to grassland degradation. Land Degradation & Development33, 2076–2091.

[61] Peng, R. H., Xiong, A. S., Xue, Y., Fu, X. Y., Gao, F., Zhao, W., Tian, Y. S., Yao, Q. H., 2008. Microbial biodegradation of polyaromatic hydrocarbons. FEMS Microbiology Reviews32, 927–955.

[62] Rahman, M. M., Tsukamoto, J., Tokumoto, Y., Shuvo, M. A. R., 2013. The role of quantitative traits of leaf litter on decomposition and nutrient cycling of the forest ecosystems. Journal of Forest and Environmental Science29, 38–48.

[63] Rawat, S. R., Männistö, M. K., Bromberg, Y., Häggblom, M. M., 2012. Comparative genomic and physiological analysis provides insights into the role of Acidobacteria in organic carbon utilization in Arctic tundra soils. FEMS Microbiology Ecology82, 341–355.

[64] Shade, A., Peter, H., Allison, S. D., Baho, D. L., Berga, M., Bürgmann, H., Huber, D. H., Langenheder, S., Lennon, J. T., Martiny, J. B., Matulich, K. L., Schmidt, T.M., Handelsman, J., 2012. Fundamentals of microbial community resistance and resilience. Frontiers in Microbiology3, 417.

[65] Shiels, A. B., González, G., 2014. Understanding the key mechanisms of tropical forest responses to canopy loss and biomass deposition from experimental hurricane effects. Forest Ecology and Management332, 1–10.

[66] Shiels, A. B., Zimmerman, J. K., García-Montiel, D. C., Jonckheere, I., Holm, J., Horton, D., Brokaw, N., 2010. Plant responses to simulated hurricane impacts in a subtropical wet forest, Puerto Rico. Journal of Ecology98, 659–673.

[67] Silva, J. P., Ticona, A. R. P., Hamann, P. R. V., Quirino, B. F., Noronha, E. F., 2021. Deconstruction of lignin: from enzymes to microorganisms. Molecules26, 2299.

[68] Silver, W. L., Hall, S. J., González, G., 2014. Differential effects of canopy trimming and litter deposition on litterfall and nutrient dynamics in a wet subtropical forest. Forest Ecology and Management332, 47–55.

[69] Sun, L. Y., Zhang, J., Zhao, J., Lu, X. H., Xiao, C. L., Xiao, Z. F., Zhang, T., Gu, Y. Q., Sun, H., Liu, H., Li, Y. L., 2023. Effects of Cinnamomum camphora coppice planting on soil fertility, microbial community structure and enzyme activity in subtropical China. Frontiers in Microbiology14, 1104077.

[70] Suwannasai, N., Rodtong, S., Thienhirun, S., Whalley, A. J. S., 2005. New species and phylogenetic relationships of Hypoxylon species found in Thailand inferred from the internal transcribed spacer regions of ribosomal DNA sequences. Mycotaxon94, 303–324.

[71] Tanner, E. V. J., Kapos, V., Healey, J. R., 1991. Hurricane effects on forest ecosystems in the Caribbean. Biotropica23, 513–521.

[72] Thevenot, M., Dignac, M. F., Rumpel, C., 2010. Fate of lignins in soils: a review. Soil Biology and Biochemistry42, 1200–1211.

[73] Tilman, D., Reich, P. B., Knops, J. M. H., 2006. Biodiversity and ecosystem stability in a decade-long grassland experiment. Nature441, 629–32.

[74] Turbé, A., de Toni, A., Benito, P., Lavelle, P., Lavelle, P., Camacho, N. R., van Der Putten, W. H., Labouze, E., Mudgal, S., 2010. Soil biodiversity: functions, threats and tools for policy makers. Bio Intelligence Service, IRD, and NIOO, Technical Report.

[75] van Ruijven, J., Berendse, F., 2007. Contrasting effects of diversity on the temporal stability of plant populations. Oikos116, 1323–1330.

[76] Wallenstein, M. D., Burns, R. G., 2011. Ecology of extracellular enzyme activities and organic matter degradation in soil: a complex community-driven process. In: Dick, R. P., ed. Methods of Soil Enzymology. Hoboken: John Wiley and Sons, Ltd, 35–55.

[77] Wang, Q., Garrity, G. M., Tiedje, J. M., Cole, J. R., 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology73, 5261–5267.

[78] Ward, N. L., Challacombe, J. F., Janssen, P. H., Henrissat, B., Coutinho, P. M., Wu, M., Xie, G., Haft, D. H., Sait, M., Badger, J., Barabote, R. D., Bradley, B., Brettin, T. S., Brinkac, L. M., Bruce, D., Creasy, T., Daugherty, S. C., Davidsen, T. M., Deboy, R. T., Detter, J. C., Dodson, R. J., Durkin, A. S., Ganapathy, A., Gwinn-Giglio, M., Han, C. S., Khouri, H., Kiss, H., Kothari, S. P., Madupu, R., Nelson, K. E., Nelson, W. C., Paulsen, I., Penn, K., Ren, Q. H., Rosovitz, M. J., Selengut, J. D., Shrivastava, S., Sullivan, S. A., Tapia, R., Thompson, L. S., Watkins, K. L., Yang, Q., Yu, C. H., Zafar, N., Zhou, L. W., Kuske, C. R., 2009. Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils. Applied and Environmental Microbiology75, 2046–2056.

[79] Weiss, S., Xu, Z. Z., Peddada, S., Amir, A., Bittinger, K., Gonzalez, A., Lozupone, C., Zaneveld, J. R., Vázquez-Baeza, Y., Birmingham, A., Hyde, E. R., Knight, R., 2017. Normalization and microbial differential abundance strategies depend upon data characteristics. Microbiome5, 27.

[80] Whigham, D. F., Olmsted, I., Cano, E. C., Harmon, M. E., 1991. The Impact of Hurricane Gilbert on Trees, Litterfall, and Woody Debris in a Dry Tropical Forest in the Northeastern Yucatan Peninsula. Biotropica23, 434–441.

[81] Wilhelm, R. C., Singh, R., Eltis, L. D., Mohn, W. W., 2019. Bacterial contributions to delignification and lignocellulose degradation in forest soils with metagenomic and quantitative stable isotope probing. The ISME Journal13, 413–429.

[82] Wingfield, B. D., Bills, G. F., Dong, Y., Huang, W. L., Nel, W. J., Swalarsk-Parry, B. S., Vaghefi, N., Wilken, P. M., An, Z. Q., de Beer, Z. W., De Vos, L., Chen, L., Duong, T. A., Gao, Y., Hammerbacher, A., Kikkert, J. R., Li, Y., Li, H. Y., Li, K., Li, Q., Liu, X. Z., Ma, X., Naidoo, K., Pethybridge, S. J., Sun, J. Z., Steenkamp, E. T., van der Nest, M. A., van Wyk, S., Wingfield, M. J., Xiong, C., Yue, Q., Zhang, X. L., 2018. Draft genome sequence of Annulohypoxylon stygium, Aspergillus mulundensis, Berkeleyomyces basicola (syn. Thielaviopsis basicola), Ceratocystis smalleyi, two Cercospora beticola strains, Coleophoma cylindrospora, Fusarium fracticaudum, Phialophora cf. hyalina, and Morchella septimelata. IMA Fungus9, 199–223.

[83] Xi, W. M., 2015. Synergistic effects of tropical cyclones on forest ecosystems: a global synthesis. Journal of Forestry Research26, 1–21.

[84] Xu, C. Y., Du, C., Jian, J. S., Hou, L., Wang, Z. K., Wang, Q., Geng, Z. C., 2021. The interplay of labile organic carbon, enzyme activities and microbial communities of two forest soils across seasons. Science Reports11, 5002.

Declaration of competing interest

The authors declare to have no conflicts of interest.

Data availability

The sequencing data used in this study was deposited in the National Center for Biotechnology Information (NCBI) of the National Library of Medicine under the accession numbers SAMN15405774-79, PRJNA1019742, PRJNA559202, PRJNA1007411, PRJNA944787.

Acknowledgements

We would like to thank Vinzenz and Kurt Schmack, and all the staff members at the Laguna del Lagarto Lodge for their assistance and on-going support for our work by providing lodging, access to the forests, guides, and lab space, the many Pace University students who helped collect soil samples, and the Pace University Dyson College Dean, the Dyson Faculty Research Grant Committee, and the Provost for research support. This work was conducted under the Costa Rican permits SINAC 55-2014, R-047-2019-OT-CONAGEBIO, and R-037-2023-OT-CONAGEBIO.

Funding

This work was funded by the Pace University Dyson College Office of the Dean, the Dyson Faculty Research Grant Committee, and the Pace University Provost’s Office for Research.

RIGHTS & PERMISSIONS

2025 Higher Education Press