Skip to main content
SpringerLink
Log in

Water Quality and Toxic Cyanobacteria in Oligohaline Estuary Beaches During the Longest Mississippi River Basin Flood Event in 2019

  • Published:
Estuaries and Coasts Aims and scope Submit manuscript

Abstract

Recent studies have shown that Lake Pontchartrain Estuary in Louisiana experiences frequent harmful cyanobacterial blooms (cyanoHABs). In 2019, the Bonnet Carré Spillway (BCS) that diverts Mississippi River water into the estuary opened twice in the same year for the first time in history to prevent flooding in New Orleans. Short-term water quality monitoring was conducted in shoreline areas with high public use for the presence of cyanoHABs and cyanotoxins to assess the public health risks. Field sampling methods and satellite imagery were used to determine water quality and quantify bloom intensity and toxicity across time and space. Long-term BCS opening created a fresh (salinity < 0.2) and nutrient-rich estuary that supported several cyanoHABs in warmer months during and after the second BCS closure. Cyanobacterial biomass ranged from 35 to 4972 µg PC L−1, while toxin microcystin ranged from undetected to 8.41 µg MC L−1. The highest biomass and toxin were detected on June 25 at the north shore, station LP8, Mandeville Beach, dominated by Microcystis and Dolichospermum species. CyanoHABs occurred mostly in the northern part of the estuary, where tributary discharge is also a strong influence. Some of these blooms exited the estuary and were transported to the Gulf of Mexico following passage through Lake Borgne and then Mississippi Sound. Modifications in the timing and duration of river diversion operations can create prolonged cyanobacterial blooms that can cause environmental and public health risks, especially in warmer months, and this may intensify due to a changing climate.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data Availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author upon reasonable request.

References

  • Anderson, D., P. Glibert, and J. Burkholder. 2002. Harmful algal blooms and eutrophication: Nutrient sources, composition, and consequences. Estuaries 25: 704–726.

    Article  Google Scholar 

  • Anselin, L. 2005. Spatial regression analysis in R: A workbook. Urbana 51: 61801.

    Google Scholar 

  • Backer, L.C. 2002. Cyanobacterial harmful algal blooms (CyanoHABs): Developing a public health response. Lake and Reservoir Management 18 (1): 20–31.

    Article  Google Scholar 

  • Bargu, S., J. White, C. Li, J. Czubakowski, and R. Fulweiler. 2011. Effects of freshwater input on nutrient loading, phytoplankton biomass, and cyanotoxin production in an oligohaline estuarine lake. Hydrobiologia 661: 377–389.

    Article  CAS  Google Scholar 

  • Bargu, S., D. Justic, J. White, R. Lane, J. Day, H. Paerl, and R. Raynie. 2019. Mississippi River diversions and phytoplankton dynamics in the deltaic Gulf of Mexico estuaries: A review. Estuarine, Coastal and Shelf Science 221: 39–52.

    Article  CAS  Google Scholar 

  • Bianchi, T.S., and M.A. Allison. 2009. Large-river delta-front estuaries as natural “recorders” of global environmental change. Proceedings of the National Academy of Sciences 106 (20): 8085–8092.

    Article  CAS  Google Scholar 

  • Botana, L.M. 2016. Toxicological perspective on climate change: aquatic toxins. Chemical Research in Toxicology 29 (4): 619–625.

  • Boyer, G.L. 2008. Cyanobacterial toxins in New York and lower Great Lakes ecosystems. Advances in Experimental Medicine and Biology 619: 153–165.

    Article  CAS  Google Scholar 

  • Cheung, M.Y., S. Liang, and J. Lee. 2013. Toxin-producing cyanobacteria in freshwater: A review of the problems, impact on drinking water safety, and efforts for protecting public health. Journal of Microbiology 51 (1): 1–10.

    Article  CAS  Google Scholar 

  • Conroy, J.D., D.D. Kane, R.D. Briland, and D.A. Culver. 2014. Systemic, early-season Microcystis blooms in western Lake Erie and two of its major agricultural tributaries (Maumee and Sandusky rivers). Journal of Great Lakes Research 40: 518–523.

    Article  Google Scholar 

  • D’Anglada, L.V. 2015. Harmful algal blooms (HABs) and public health: Progress and current challenges. Toxins 7 (11): 4437–4441.

    Article  Google Scholar 

  • Dash, P., N.D. Walker, D.R. Mishra, C. Hu, J.L. Pinckney, and E.J. D’Sa. 2011. Estimation of cyanobacterial pigments in a freshwater lake using OCM satellite data. Remote Sensing of Environment 115: 3409–3423.

    Article  Google Scholar 

  • Dokulil, M.T., and K. Teubner. 2000. Cyanobacterial dominance in lakes. Hydrobiologia 438 (1–3): 1–12.

    Article  CAS  Google Scholar 

  • Dortch, Q., M.L. Parsons, N.N. Rabalais, and R.E. Turner. 1999. What is the threat of harmful algal blooms in Louisiana coastal waters? In: Recent Research in Coastal Louisiana: Natural System Function and Response to Human Influence, eds. Rozas, L.P., J.A. Nyman, C.E. Proffitt, N.N. Rabalais, D.J. Reed, and R.E. Turner, 134–144. Louisiana: Louisiana Sea Grant College Program.

  • Fernandez, C., V. Estrada, and E. Parodi. 2015. Factors triggering cyanobacteria dominance and succession during blooms in a hypereutrophic drinking water supply reservoir. Water, Air, and Soil PollutIon 226 (3): 1–13.

    Article  CAS  Google Scholar 

  • Fleming, L.E., K. Broad, A. Clement, E. Dewailly, S. Elmir, A. Knap, S.A. Pomponi, S. Smith, H. Solo Gabriele, and P. Walsh. 2006. Oceans and human health: Emerging public health risks in the marine environment. Marine Pollution Bulletin 53 (10–12): 545–560.

    Article  CAS  Google Scholar 

  • Garcia, A.C., S. Bargu, P. Dash, N.N. Rabalais, M. Sutor, W. Morrison, and N.D. Walker. 2010. Evaluating the potential risk of microcystins to blue crab (Callinectes sapidus) fisheries and human health in a eutrophic Estuary. Harmful Algae 9: 134–143.

    Article  CAS  Google Scholar 

  • Glibert, P.M., D.M. Anderson, P. Gentien, E. Graneli, and K.G. Sellner. 2005. The global complex phenomena of harmful algal blooms. Oceanography 18: 136–147.

    Article  Google Scholar 

  • Hallegraeff, G.M. 2010. Ocean climate change, phytoplankton community responses, and harmful algal blooms: A formidable predictive challenge. Journal of Phycology 46 (2): 220–235.

    Article  CAS  Google Scholar 

  • Hammond, C.N. 2023. Controls of physical drivers on the formation and toxicity of harmful cyanobacteria blooms (cyanoHABs). Louisiana State University, MSc Thesis 79.

  • Hastings, R.W. 2009. The lakes of Pontchartrain: their history and environments. The University Press of Mississippi.

  • Hays, G.C., A.J. Richardson, and C. Robinson. 2005. Climate change and marine plankton. Trends in Ecology & Evolution 20: 337–344.

    Article  Google Scholar 

  • Heil, C.A., and A.L. Muni-Morgan. 2021. Florida’s harmful algal bloom (HAB) problem: Escalating risks to human, environmental and economic health with climate change. Frontiers in Ecology and Evolution 9: 646080.

    Article  Google Scholar 

  • Hudnell, H.K. 2010. The state of U.S. freshwater harmful algal blooms assessments, policy, and legislation. Toxicon 55(5): 1024–1034.

  • Huisman, J., and F.D. Hulot. 2005. Population dynamics of harmful cyanobacteria: Factors affecting species composition. In Harmful Cyanobacteria, ed. J. Huisman, H.C.P. Matthijs, and P.M. Visser, 143–176. Dordrecht, The Netherlands: Springer.

    Chapter  Google Scholar 

  • Huisman, J.M., H.C.P. Matthijs, and P.M. Visser. 2005. Harmful cyanobacteria. Springer Aquatic Ecology Series Dordrecht, the Netherlands: Springer.

    Book  Google Scholar 

  • Katner, A., E. Ogunyinka, M. Sun, S. Soileau, D. Lavergne, D. Dugas, and M. Suffet. 2011. Fishing, fish consumption and advisory awareness among Louisiana’s recreational fishers. Environmental Research 111: 1037–1045.

    Article  CAS  Google Scholar 

  • Konopka, A., and T.D. Brock. 1978. Effect of temperature on blue-green algae (cyanobacteria) in Lake Mendota. Applied and Environmental Microbiology 36 (4): 572–576.

    Article  CAS  Google Scholar 

  • Lehman, P.W., K. Marr, G.L. Boyer, S. Acuna, and S.J. Teh. 2013. Long-term trends and causal factors associated with Microcystis abundance and toxicity in San Francisco Estuary and implications for climate change impacts. Hydrobiologia 718: 141–158.

    Article  CAS  Google Scholar 

  • Lincoln, R.A., J.P. Shine, E.J. Chesney, D.J. Vorhees, P. Grandjean, and D.B. Senn. 2010. Fish consumption and mercury exposure among Louisiana recreational anglers. Environmental Health Perspectives 119: 245–251.

    Article  Google Scholar 

  • Li, C., N. Walker, A. Hou, I. Georgiou, H. Roberts, E. Laws, A.J. McCorquodale, E. Weeks, X. Li, and J. Crochet. 2008. Circular plumes in Lake Pontchartrain Estuary under winds training. Estuarine, Coastal and Shelf Science 80 (1): 161–172.

    Article  Google Scholar 

  • Lunetta, R.S., B.A. Schaeffer, R.P. Stumpf, D. Keith, S.A. Jacobs, and M.S. Murphy. 2015. Evaluation of cyanobacteria calls count detection derived from MERIS imagery across the eastern USA. Remote Sensing of Environment 157: 24–34.

    Article  Google Scholar 

  • McCorquodale, J.A., R.J. Roblin, I.Y. Georgiou, and K.A. Haralampides. 2009. Salinity, nutrient, and sediment dynamics in the Pontchartrain Estuary. Journal of Coastal Research 54: 71–87.

    Article  Google Scholar 

  • Mize, S., and D.K. Demcheck. 2009. Water quality and phytoplankton communities in Lake Pontchartrain during and after the Bonnet Carré Spillway opening, April to October 2008, in Louisiana, USA. Geo-Marine Letters 29: 431–440.

    Article  CAS  Google Scholar 

  • Moe, S.J., K.D. Schamphelaere, W.H. Clements, M.T. Sorensen, P.J. Van den Brink, and M. Liess. 2013. Combined and interactive effects of global climate change and toxicants on populations and communities. Environmental Toxicology and Chemistry 32 (1): 49–61.

    Article  CAS  Google Scholar 

  • Msagati, T.A.M., B.A. Siame, and D.D. Shushu. 2006. Evaluation of methods for the isolation, detection, and quantification of cyanobacterial hepatotoxins. Aquatic Toxicology 78: 382–397.

    Article  CAS  Google Scholar 

  • Murrell, M.C., J.D. Hagy, E.M. Lores, and R.M. Greene. 2007. Phytoplankton production and nutrient distributions in a subtropical estuary: Importance of freshwater flow. Estuaries and Coasts 30: 390–402.

    Article  Google Scholar 

  • Ngwa, F.F., C.A. Madramootoo, and S. Jabaji. 2014. Comparison of the cyanobacterial microcystin synthetase (mcy) E gene transcript levels, mcy E gene copies, and biomass as indicators of microcystin risk under laboratory and field conditions. MicrobiologyOpen 3 (4): 411–425.

    Article  CAS  Google Scholar 

  • NOAA. 2021. Cyanobacteria algal bloom from a satellite in Lake Pontchartrain. https://coastalscience.noaa.gov/research/stressor-impacts-mitigation/hab-monitoring-system/cyanobacteria-algal-bloom-from-satellite-in-lake-pontchartrain-la/ [Accessed April 2021].

  • Pade, N., and M. Hagemann. 2014. Salt acclimation of cyanobacteria and their application in biotechnology. Life (basel). 5 (1): 25–49.

    Google Scholar 

  • Paerl, H.W., R.S. Fulton, P.H. Moisander, and J. Dyble. 2001. Harmful freshwater algal blooms, with an emphasis on cyanobacteria. The Scientific World Journal 1: 76–113.

    Article  CAS  Google Scholar 

  • Paerl, H.W., and R.S. Fulton. 2006. Ecology of harmful cyanobacteria. In Ecology of Harmful Marine Algae, ed. E. Graneli and J. Turner, 95–107. Berlin, Germany: Springer-Verlag.

    Chapter  Google Scholar 

  • Paerl, H.W., and J. Huisman. 2008. Blooms like it hot. Science 320: 57–58.

    Article  CAS  Google Scholar 

  • Paerl, H.W., N.S. Hall, and E.S. Calandrino. 2011. Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change. Science of the Total Environment 409: 1739–1745.

    Article  CAS  Google Scholar 

  • Paerl, H.W., and V.J. Paul. 2012. Climate change: Links to global expansion of harmful cyanobacteria. Water Research 46 (5): 1349–1363.

    Article  CAS  Google Scholar 

  • Paerl, H.W., N.S. Hall, B.L. Peierls, and K.L. Rossignol. 2014. Evolving paradigms and challenges in estuarine and coastal eutrophication dynamics in a culturally and climatically stressed world. Estuaries and Coasts 37: 243–258.

    Article  Google Scholar 

  • Paerl, H.W., W.S. Gardner, K.E. Havens, A.R. Joyner, M.J. McCarthy, S.E. Newell, B. Qin, and J.T. Scott. 2016. Mitigating cyanobacterial harmful algal blooms in aquatic ecosystems impacted by climate change and anthropogenic nutrients. Harmful Algae 54: 213–222.

    Article  Google Scholar 

  • Paerl, H.W., and M.A. Barnard. 2020. Mitigating the global expansion of harmful cyanobacterial blooms: Moving targets in a human- and climatically-altered world. Harmful Algae 96: 101845.

    Article  CAS  Google Scholar 

  • Parsons, T.R., Y. Maita, and C.M.A. Lali. 1984. Manual of chemical and biological methods for seawater analysis. Oxford, UK: Pergamon Press.

    Google Scholar 

  • Preece, E.P., B.C. Moore, and F.J. Hardy. 2015. Transfer of microcystin from freshwater lakes to Puget Sound, WA and toxin accumulation in marine mussels (Mytilus trossulus). Ecotoxicology and Environmental Safety 122: 98–105.

    Article  CAS  Google Scholar 

  • Preece, E.P., F.J. Hardy, B.C. Moore, and M. Bryan. 2017. A review of microcystin detections in estuarine and marine waters: Environmental implications and human health risk. Harmful Algae 61: 31–45.

    Article  CAS  Google Scholar 

  • Reddy, K.R., S. Newman, T.Z. Osborne, J.R. White, and H.C. Fitz. 2011. Phosphorus cycling in the greater Everglades ecosystem: Legacy phosphorus implications for management and restoration. Critical Reviews in Environmental Science and Technology 41 (S1): 149–186.

    Article  CAS  Google Scholar 

  • Riekenberg, J., S. Bargu, and R. Twilley. 2015. Phytoplankton community shifts and harmful algae presence in a diversion influenced Estuary. Estuaries and Coasts 38: 2213–2226.

    Article  CAS  Google Scholar 

  • Robarts, R.D., and T. Zohary. 1987. Temperature effects on photosynthetic capacity, respiration, and growth rates of bloom-forming cyanobacteria. New Zealand Journal of Marine and Freshwater Research 21: 391–399.

    Article  CAS  Google Scholar 

  • Roberts, V.A., M. Vigar, L. Backer, G.E. Veytsel, E.D. Hilborn, E.I. Hamelin, K.L.V. Esschert, J.Y. Lively, J.R. Cope, M.C. Hlavsa, and J.S. Yoder. 2020. Surveillance for harmful algal bloom events and associated human and animal illnesses—one health harmful algal bloom system, United States, 2016–2018. MMWR Morbidity and Mortality Weekly Report 69 (50): 1889–1894.

    Article  Google Scholar 

  • Roy, E.D., N.T. Nguyen, S. Bargu, and J.R. White. 2012. Internal loading of phosphorus from sediments of Lake Pontchartrain (Louisiana, USA) with implications for eutrophication. Hydrobiologia 684: 69–82.

    Article  CAS  Google Scholar 

  • Roy, E.D., J.R. White, E.A. Smith, S. Bargu, and C. Li. 2013. Estuarine ecosystem response to three large-scale Mississippi River flood diversion events. Science of the Total Environment 458–460: 374–387.

    Article  Google Scholar 

  • Roy, E.D., E.A. Smith, S. Bargu, and J.R. White. 2016. Will Mississippi River diversions designed for coastal restoration cause harmful algal blooms? Ecological Engineering 91: 350–364.

    Article  Google Scholar 

  • Sapkota, Y., S. Bargu, and J.R. White. 2023 (In revision). Temporally-displaced Mississippi River spring flood pulse shows muted aquatic ecosystem response: a climate change warning for coastal food webs. Science of the Total Environment.

  • Sivonen, K., and G. Jones. 1999. Cyanobacterial toxins. In Toxic cyanobacteria in water: a guide to their public health consequences, monitoring, and management, eds. I. Chorus, J. Bartram, 41–111. E and FN Spon London, United Kingdom.

  • Tonk, L., K. Bosch, P.M. Visser and J. Huisman, J. 2007. Chapter 2: Salt tolerance of the harmful cyanobacterium Microcystis aeruginosa. Aquatic Microbial Ecology 46: 117–123.

  • Trainer, V.L., and F.J. Hardy. 2015. Integrative monitoring of marine and freshwater harmful algae in Washington State for public health protection. Toxins 7 (4): 1206–1234.

    Article  CAS  Google Scholar 

  • Turner, R.E., Q. Dortch, D. Justic, and E.M. Swenson. 2002. Nitrogen loading into an urban Estuary: Lake Pontchartrain (Louisiana, U.S.A.). Hydrobiologia 487: 137–152.

    Article  CAS  Google Scholar 

  • Turner, R.E., Q. Dortch, and N.N. Rabalais. 2004. Inorganic nitrogen transformations at high loading rates in an oligohaline Estuary. Biogeochemistry 68: 411–422.

    Article  CAS  Google Scholar 

  • USACE. 2020. https://www.mvn.usace.army.mil/Missions/Mississippi-River-Flood-Control/BonnetCarre-Spillway-Overview/Spillway-Operation-Information/

  • USEPA (United States Environmental Protection Agency). 1993. Methods of chemical analysis of water and wastes. Environmental Monitoring Support Laboratory, Cincinnati.

  • USEPA (United States Environmental Protection Agency). 2019. Recommended human health recreational swimming ambient water quality criteria or for microcystins and cylindrospermopsin.EPA Document Number EPA 822-R-19–001.

  • Vaitomaa, J., A. Rantala, K. Halinen, L. Rouhiainen, P. Tallberg, L. Mokelke, and K. Sivonen. 2003. Quantitative real-time PCR for determination of microcystin synthetase e copy numbers for microcystis and Anabaena in lakes. Applied and Environmental Microbiology 69 (12): 7289–7297.

    Article  CAS  Google Scholar 

  • Vézie, C., J. Rapala, J. Vaitomaa, J. Seitsonen, and K. Sivonen. 2002. Effect of nitrogen and phosphorus on growth of toxic and nontoxic Microcystis strains and on intracellular microcystin concentrations. Microbial Ecology 43: 443–454.

    Article  Google Scholar 

  • Walker, S.R., J.C. Lund, D.G. Schumacher, P.A. Brakhage, B.C. McManus, J.D. Miller, M.M. Augustine, J.J. Carney, R.S. Holland, K.D. Hoagland, J.C. Holz, T.M. Barrow, D.C. Rundquist, A.A., and Gitelson. 2008. Chapter 6: Nebraska experience. Agronomy & Horticulture -- Faculty Publications. 180.

  • Wetz, M.S., and D.W. Yoskowitz. 2013. An ‘extreme’ future for estuaries? Effects of extreme climatic events on estuarine water quality and ecology. Marine Pollution Bulletin 69: 7–18.

    Article  CAS  Google Scholar 

  • White, J.R., R.W. Fulweiler, C.Y. Li, S. Bargu, N. Walker, R.R. Twilley, and S. Green. 2009. The Mississippi River flood of 2008 – Effects of a large freshwater diversion on physical, chemical, and biological characteristics of a shallow, estuarine lake. Environmental Science & Technology 43: 5599–5604.

    Article  CAS  Google Scholar 

  • Wynne, T.T., M.C. Tomlinson, R.P. Stumpf, R.A. Warner, P.A. Tester, J. Dyble, and G.L. Fahnenstiel. 2008. Relating spectral shape to cyanobacterial blooms in the Laurentian Great Lakes. International Journal of Remote Sensing 29 (12): 3665–3672.

    Article  Google Scholar 

  • Wynne, T., A. Meredith, T. Briggs, W. Litaker, and R. Stumpf. 2018. Harmful algal bloom forecasting branch ocean color satellite imagery processing guidelines. NOAA Technical Memorandum NOS NCCOS 252. Silver Spring, MD. 48.https://doi.org/10.25923/twc0-f025

  • Yu, J., C. Fan, J. Zhong, Y. Zhang, C. Wang, and L. Zhang. 2016. Evaluation of in situ simulated dredging to reduce internal nitrogen flux across the sediment-water interface in Lake Taihu, China. Environmental Pollution 214: 866–877.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We sincerely thank the editor and reviewers for taking the time to review our manuscript and providing constructive feedback to improve our manuscript. We thank Quay Dortch for her scientific guidance and expertise about Lake Pontchartrain and the northern Gulf of Mexico and the NCCOS Event Response team of Quay Dortch, MaryKate Rogener, and Maggie Broadwater for their coordination of this organizationally complex response. Pontchartrain Conservancy field volunteers are acknowledged for collecting and transporting the samples to Dr. Bargu’s lab at Louisiana State University. Nicholas Lee and Laura Scott at Tulane University were also acknowledged for their assistance with laboratory analysis.

Funding

Funding was provided by the National Centers for Coastal Ocean Science (NCCOS) HAB Event Response Program. This is NCCOS HAB ER publication #31.

Author information

Authors and Affiliations

  1. Department of Oceanography and Coastal Sciences, College of the Coast and Environment, Louisiana State University, Baton Rouge, LA, 70803, USA

    Sibel Bargu, Monique Boudreaux, Courtney N. Hammond & Callie Snow

  2. Water Quality Department, Pontchartrain Conservancy, Metairie, LA, 70002, USA

    Brady Skaggs

  3. Department of Environmental Health Sciences, School of Public Health and Tropical Medicine, Tulane University, New Orleans, LA, 70112, USA

    Tiong Gim Aw

  4. National Oceanic and Atmospheric Administration, National Centers for Coastal Ocean Science, Silver Spring, MD, 20910, USA

    Richard Stumpf

Authors
  1. Sibel Bargu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Brady Skaggs
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Monique Boudreaux
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Courtney N. Hammond
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Callie Snow
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tiong Gim Aw
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Richard Stumpf
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sibel Bargu.

Additional information

Communicated by Hans W. Paerl

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bargu, S., Skaggs, B., Boudreaux, M. et al. Water Quality and Toxic Cyanobacteria in Oligohaline Estuary Beaches During the Longest Mississippi River Basin Flood Event in 2019. Estuaries and Coasts 46, 1865–1879 (2023). https://doi.org/10.1007/s12237-023-01247-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12237-023-01247-1

Keywords

Search

Navigation