First ecological analysis of lacustrine testate amoebae in Guatemala: A case study from the highland Lake Chichoj

Submitted: 20 July 2022
Accepted: 18 November 2022
Published: 30 November 2022
Abstract Views: 2218
PDF: 314
HTML: 48
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

Authors

Freshwater quality represents a central issue for human populations and the conservation of aquatic communities. In this sense, freshwater reservoirs, such as lakes, require proper management and monitoring plans to avoid their deterioration and pollution. Bioindicators, such as testate amoebae, are an excellent tool increasingly utilized for limnology and paleolimnology to assess the trophic status of lacustrine environments. However, despite their potential as bioindicators, the ecological research status of testate amoebae in Central American lakes remains poor. We conducted our research at highland Lake Chichoj, Alta Verapaz, Guatemala, which has become increasingly eutrophic since the 1980s. This study contributes to fill the knowledge gap about neotropical testate amoebae, parallel to testing their utility as bioindicators of lacustrine conditions. From a collection of 12 surface sediment samples (associated with different land uses), we found 19 testate amoebae taxa, and for the first time in Guatemala, we recorded Arcella megastoma, Arcella gibbosa, Cucurbitella tricuspis, Difflugia protaeiformis strain “acuminata”, Difflugia urceolata strain “elongata”, Lesquereusia spiralis, Lesquereusia modesta, and Mediolus corona. Our cluster analyses revealed three testate amoebae assemblages in connection to trophic conditions: 1) Stressed Conditions (SC), 2) Lowest Contamination Conditions (LC), and 3) Deep Transitional Conditions Assemblage (DT). After performing a transformation-based redundancy analysis (tb-RDA), we found total organic carbon as the only significant environmental parameter associated with testate amoebae assemblages (p<0.004). Our indicator species analysis (IndVal) confirms the eutrophic regime of Lake Chichoj in connection to the presence of Cucurbitella tricuspis and Centropyxis aculeata strain “aculeata” as indicators of nutrient enrichment and stressful conditions. The testate amoebae assemblages identified in Lake Chichoj represent a critical baseline for future studies of Guatemalan lakes, strengthening our understanding of the causal factors behind water quality in neotropical regions.

Dimensions

Altmetric

PlumX Metrics

Downloads

Downloads

Download data is not yet available.

Citations

Albizurez-Palma JR, 1978. [Estudio Ecológico de La Laguna de Chichoj].[Thesis dissertation in Spanish]. USAC, Guatemala City.
Alves GM, Velho LFM, Simões NR, Lansac-Tôha FA, 2010. Biodiversity of testate amoebae (Arcellinida and Euglyphida) in different habitats of a lake in the Upper Paraná River floodplain. Eur. J. Protistol. 46:310-318.
American Public Health Association, American Water Works Association, & Water Environment Federation. 1998. Standard methods for the examination of water and wastewater, 20th ed. Washington, D.C.
Asioli A, Medioli FS, Patterson RT, 1996. Thecamoebians as a tool for reconstruction of paleoenvironments in some Italian lakes in the foothills of the southern Alps (Orta, Varese and Candia). J. Foramin. Res. 26:248-263.
Bastidas-Navarro M, Modenutti B, 2007. [Efecto de la estructuración por macrófitas y por recursos alimentarios en la distribución horizontal de tecamebas y rotíferos en un lago andino patagónico].[Article in Spanish]. Rev. Chil. Hist. Nat. 80:345-362.
Betancur J, Acevedo B, 2016. [Asociaciones de amebas testáceas ( Protozoa : Rhizopoda ), en una laguna volcánica tropical , volcán Barva , Costa Rica].[Article in Spanish]. Brenesia 85-86:21-29.
Brocard G, Adatte T, Magand O, Pfeifer H-R, Bettini A, Arnaud F, Anselmetti FS, Moran-Ical S, 2014. The recording of floods and earthquakes in Lake Chichój, Guatemala during the twentieth century. J. Paleolimnol. 52:155-169.
Brocard G, Bettini A, Pfeifer H, Adatte T, 2016a. [Eutrofización y contaminación por cromo en la laguna de Chichoj, Alta Verapaz, Guatemala].[Article in Spanish]. Rev. Guatem. Cienc. Tierra 3:20-43.
Brocard G, Moran-Ical S, Jared Vasquez O, Fernández-Irujo M, 2016b. [Riesgos naturales asociados a la génesis de la Laguna de Chichoj, Alta Verapaz].[Article in Spanish]. Rev. Guatem. Cienc. Tierra 3:5-19.
de Cáceres M, Legendre P, Moretti M, 2010. Improving indicator species analysis by combining groups of sites. Oikos 119:1674-1684.
Charqueño-Celis NF, Garibay M, Sigala I, Brenner M, Echeverria-Galindo P, Lozano-García S, Massaferro J, Pérez L, 2020. Testate amoebae (Amoebozoa: Arcellinidae) as indicators of dissolved oxygen concentration and water depth in lakes of the Lacandón Forest, Southern Mexico. J. Limnol. 79:82-91.
Cockburn CF, Gregory BRB, Nasser NA, Patterson RT, 2020. Intra-Lake Arcellinida (Testate Lobose Amoebae) Response to Winter De-icing Contamination in an Eastern Canada Road-Side “Salt Belt” Lake. Microb. Ecol. 80:366-383.
Dalby AP, Kumar A, Moore JM, Patterson RT, 2000. Preliminary survey of arcellaceans (thecamoebians) as limnological indicators in tropical Lake Sentani, Irian Jaya, Indonesia. J. Foramin. Res. 30:135-142.
Drexler JW, Rose WI, Sparks RSJ, Ledbetter MT, 1980. The Los Chocoyos Ash, guatemala: A major stratigraphic marker in middle America and in three ocean basins. Quat. Res. 13:327-345.
Ellison RL, Ogden CG, 1987. A Guide to the Study and Identification of Fossil Testate Amoebae in Quaternary Lake Sediments. Int. Rev. Hydrobiol. 72:639-652.
Escobar J, Brenner M, Whitmore TJ, Kenney WF, Curtis JH, 2008. Ecology of testate amoebae (thecamoebians) in subtropical Florida lakes. J. Paleolimnol. 40:715-731.
Farooqui A, Trivedi A, Swindles G, Chauhan MS, 2020. Distribution of Testate Amoebae (Thecamoebians) in a desiccating lake, India. J. Paleontol. Soc. Ind. 65:81–89.
Ferreira F, Leão CJ, Antonio M, Hansen F, 2007. [Tecamebas em sedimentos do rio Tramandaí e da lagoa do Passo, planície costeira norte do Estado do Rio Grande do Sul, Brasil].[Article in Portuguese]. GAEA 2:66-74.
Gavel MJ, Patterson RT, Nasser NA, Galloway JM, Hanna BW, Cott PA, Roe HM, Falck H, 2018. What killed Frame Lake? A precautionary tale for urban planners. PeerJ 6:e4850.
Gough HL, Stahl DA, 2011. Microbial community structures in anoxic freshwater lake sediment along a metal contamination gradient. ISME J. 5:543-558.
Heiri O, Lotter AF, Lemcke G, 2001. Loss on ignition as a method for estimating organic and carbonate content in sediments: reproducibility and comparability of results. J. Paleolimnol. 25:101-110.
Heger TJ, Lara E, Mitchell EAD, 2011. Arcellinida testate amoebae (Amoebozoa: Arcellinida): Model of organisms for assessing microbial biogeography, p. 111-129 In: D. Fontaneto (ed.), Biogeography of Microscopic Organisms Is Everything Small Everywhere?. Imperial College London.
van Hengstum PJ, Reinhardt EG, Beddows PA., Huang RJ, Gabriel JJ, 2008. Thecamoebians (Testate Amoebae) and Foraminifera from trhee anchialine cenotes in Mexico: low salinity (1.5-4.5 psu) faunal transitions. J. Foramin. Res. 38:305-317.
International Commission on Zoological Nomenclature, 1999. International Code of Zoological Nomenclature. The Natural History Museum, London.
Jost, L. (2006). Entropy and diversity. Oikos. 113(2): 363-375.
Kihlman S, Kauppila T, 2012. Effects of mining on testate amoebae in a Finnish lake. J. Paleolimnol. 47:1-15.
Kornecki KM, Katz ME, 2020. Profundal testate amoebae (arcellacea) of Lake superior and Lake michigan. J. Foramin. Res. 50:3-10.
Kornecki KM, Schuler MS, Katz ME, Relyea RA, McCarthy FMG, Schaller MF, Gillikin DP, Stager JC, Boylen CW, Eichler LW, Nierzwicki-Bauer SA, 2020. The Canary in the Coal Mine: Testate Amoebae Record Anthropogenic Impacts in Sediments of Oligotrophy Lake George, NY, USA. J. Foramin. Res. 50:128-140.
Kosakyan A, Lahr DJG, Mulot M, Meisterfeld R, Mitchell EAD, Lara E, 2016. Phylogenetic reconstruction based on COI reshuffles the taxonomy of hyalosphenid shelled (testate) amoebae and reveals the convoluted evolution of shell plate shapes. Cladistics 32:606-623.
Kumar A, Dalby AP, 1998. Identification key for Holocene lacustrine arcellacean (thecamoebian) taxa. Paleontol. Electron. 1:1-39.
Laminger H, 1973. [Die Testaceen (Protozoa, Rhizopoda) einiger Hochgebirgsgewasser von Mexiko, Costa Rica und Guatemala].[Article in Germany]. Int. Rev. der gesamten Hydrobiol. und Hydrogr. 58:273-305.
Lamorgese L, Geneletti D, Partidario MR, 2015. Reviewing Strategic Environmental Assessment Practice in the Oil and Gas Sector. J. Env. Assmt. Pol. Mgmt. 17: 550017.
Lansac-Tôha FA, Bonecker CC, Velho LFM, Simões NR, Dias JD, Alves GM, Takahashi EM, 2009. Biodiversity of zooplankton communities in the Upper Paraná River floodplain: interannual variation from long-term studies. Braz. J. Biol. 69:539-549.
Legendre P, Gallagher ED, 2001. Ecologically meaningful transformations for ordination of species data. Oecologia 129:271-280.
Marcisz K, Jassey VEJ, Kosakyan A, Krashevska V, Lahr DJG, Lara E, Lamentowicz Ł, Lamentowicz M, Macumber A, Mazei Y, Mitchell EAD, Nasser NA, Patterson RT, Roe HM, Singer D, Tsyganov AN, Fournier B, 2020. Testate Amoeba Functional Traits and Their Use in Paleoecology. Front. Ecol. Evol. 8:57596.
Medioli FS, Scott DB, 1988. Lacustrine thecamoebians (mainly arcellaceans) as potential tools for palaeolimnological interpretations. Palaeogeogr. Palaeoclimatol. Palaeoecol. 62:361-386.
Mousinho LP, da Silva MLC, Arrieira RL, Schwind LTF, 2018. Species composition of testate amoebae in Lake Monte Alegre, Ribeirão Preto, SP, Brazil. Acta Sci. - Biol. Sci. 40:36768.
Nasser NA, Patterson RT, Roe HM, Galloway JM, Falck H, Palmer MJ, Spence C, Sanei H, Macumber AL, Neville LA, 2016. Lacustrine Arcellinina (Testate Amoebae) as Bioindicators of Arsenic Contamination. Microb. Ecol. 72:130-149.
Nasser NA, Patterson RT, Roe HM, Galloway JM, Falck H, Sanei H, 2020. Use of Arcellinida (testate lobose amoebae) arsenic tolerance limits as a novel tool for biomonitoring arsenic contamination in lakes. Ecol. Indic. 113:106177.
Neville LA, Mccarthy FMG, Mackinnon MD, 2010. Seasonal environmental and chemical impact on thecamoebian community composition in an oil sands reclamation wetland in northern Alberta. Palaeontol. Electron. 13:13A.
Neville LA, Patterson RT, Gammon P, Macumber AL, 2014. Relationship between ecological indicators (Arcellacea), total mercury concentrations and grain size in lakes within the Athabasca oil sands region, Alberta. Environ. Earth Sci. 72:577-588.
Ogden GG, Hedley RH, 1980. An Atlas of Freshwater Testate Amoebae. Oxford University Press, Londres: 222 pp.
Patterson RT, Barker T, Burbidge SM, 1996. Arcellaceans (thecamoebians) as proxies of arsenic and mercury contamination in northeastern Ontario lakes. J. Foramin. Res. 26:172-183.
Patterson RT, Dalby A, Kumar A, Henderson LA, Boudreau REA, 2002. Arcellaceans (thecamoebians) as indicators of land-use change: Settlement history of the Swan lake area, Ontario as a case study. J. Paleolimnol. 28:297-316.
Patterson RT, Fishbein E, 1989. Re-Examination of the statistical methods used to determine the number of point counts needed for micropaleontological quantitative research. J. Paleontol. 63:245-248.
Patterson RT, Huckerby G, Kelly TJ, Swindles GT, Nasser NA, 2015. Hydroecology of Amazonian lacustrine Arcellinida (testate amoebae): A case study from Lake Quistococha, Peru. Eur. J. Protistol. 51:460-469.
Patterson RT, Kumar A, 2000a. Use of Arcellacea (Thecamoebians) to Gauge Levels of Contamination and Remediation in Industrially Polluted Lakes, p. 257-278 In: R.E. Martin (ed.), Environmental Micropaleontology. Topics in Geobiology, Vol. 15, Springer.
Patterson RT, Kumar A, 2000b. Assessment of Arcellacean (Thecamoebian) Assemblages, Species, and Strains As Contaminant Indicators in James Lake, Northeastern Ontario, Canada. J. Foramin. Res. 30:310-320.
Patterson RT, Kumar A, 2002. A review of current testate rhizopod (thecamoebian) research in Canada. Palaeogeogr. Palaeoclimatol. Palaeoecol. 180:225-251.
Patterson RT, Lamoureux EDR, Neville LA, Macumber AL, 2013. Arcellacea (Testate Lobose Amoebae) as pH Indicators in a Pyrite Mine-Acidified Lake, Northeastern Ontario, Canada. Microb. Ecol. 65:541-554.
Patterson RT, Roe HM, Swindles GT, 2012. Development of an Arcellacea (testate lobose amoebae) based transfer function for sedimentary Phosphorus in lakes. Palaeogeogr. Palaeoclimatol. Palaeoecol. 348-349:32-44.
Payne RJ, Kishaba K, Blackford JJ, Mitchell EAD, 2006. Ecology of testate amoebae (Protista) in south-central Alaska peatlands: building transfer-function models for palaeoenvironmental studies. Holocene 16:403-414.
Payne RJ, Mitchell EAD, 2009. How many is enough? Determining optimal count totals for ecological and palaeoecological studies of testate amoebae. J. Paleolimnol. 42:483-495.
Prentice SV., Roe HM, Bennion H, Sayer CD, Salgado J, 2018. Refining the palaeoecology of lacustrine testate amoebae: insights from a plant macrofossil record from a eutrophic Scottish lake. J. Paleolimnol. 60:189-207.
Qin Y, Fournier B, Lara E, Gu Y, Wang H, Cui Y, Zhang X, Mitchell EAD, 2013. Relationships between testate amoebae communities and water quality in Lake Donghu, a large alkaline lake in Wuhan, China. Front. Earth Sci. 7:182-190.
R Core Team, 2020. R: A Language and Environment for Statistical Computing. Foundation for Statistical Computing., Vienna.
Rahbek C, Borregaard MK, Colwell RK, Dalsgaard B, Holt BG, Morueta-Holme N, Nogues-Bravo D, Whittaker RJ, Fjeldså J, 2019. Humboldt’s enigma: What causes global patterns of mountain biodiversity? Science 365, 1108.
Rao, CR, 1995. A review of canonical coordinates and an alternative to correspondence analysis using Hellinger distance. Qüestiió 19: 23-63
Reimann C, Filzmoser P, Garrett R, Dutter R, 2008. Statistical Data Analysis Explained : Applied Environmental Statistics with R. John Wiley & Sons, England: 84 pp.
Reinhardt EG, Little M, Donato S, Findlay D, Krueger A, Clark C, Boyce J, 2005. Arcellacean (thecamoebian) evidence of land-use change and eutrophication in Frenchman’s Bay, Pickering, Ontario. Environ. Geol. 47:729-739.
Riou L, Nasser NA, Patterson RT, Gregory BRB, Galloway JM, Falck H, 2021. Lacustrine Arcellinida (testate lobose amoebae) as bioindicators of arsenic concentration within the Yellowknife City Gold Project, Northwest Territories, Canada. Limnologica 87:125862.
Roe HM, Patterson RT, 2006. Distribution of thecamoebians (testate amoebae) in small lakes and ponds, Barbados, West Indies. J. Foramin. Res. 36:116-134.
Roe HM, Patterson RT, 2014. Arcellacea (Testate Amoebae) as Bio-indicators of Road Salt Contamination in Lakes. Microb. Ecol. 68:299-313.
Roe HM, Patterson RT, Swindles GT, 2010. Controls on the contemporary distribution of lake thecamoebians (testate amoebae) within the Greater Toronto Area and their potential as water quality indicators. J. Paleolimnol. 43:955-975.
Sigala I, García SL, Alvarado LP, Caballero M, Vázquez AL, 2018. Ecological drivers of testate amoebae diversity in tropical water bodies of central Mexico. J. Limnol. 77:385-399.
Sigala I, Lozano-García S, Escobar J, Pérez L, Gallegos-Neyra E, 2016. Testate Amoebae (Amebozoa: Arcellinida) in Tropical Lakes of Central Mexico. Rev. Biol. Trop. 64:377-397.
Steele RE, Nasser NA, Patterson RT, Gregory BRB, Roe HM, Reinhardt EG, 2018. An Assessment of Sub-Meter Scale Spatial Variability of Arcellinida (Testate Lobose Amoebae) Assemblages in a Temperate Lake: Implications for Limnological Studies. Microb. Ecol. 76:680-694.
Tejada C, 2011. [Línea Base de La Laguna de Chichoj, Ubicada En El Municipio de San Cristóbal, Departamento de Alta Verapaz].[Book in Spanish]. Unidad de Recursos Hídricos y Cuencas de la Dirección General de Gestión Ambiental y Recursos Naturales, Guatemala City: 121 pp.
Velho LFM, Bini LM, Lansac-Tôha FA, 2004. Testate Amoebae (Rhizopoda) Diversity in Plankton of the Upper Paraná River floodplain, Brazil. Hydrobiologia 523:103-111.
Ward JH, 1963. Hierarchical Grouping to Optimize an Objective Function. J. Am. Stat. Assoc. 58:236-244.
Watts SH, Jump AS, 2022. The benefits of mountain woodland restoration. Restor. Ecol. 30:e13701.

Edited by

Alberto Doretto, Department of Environmental and Life Sciences, University of Piemonte Orientale “Amedeo Avogadro”, Alessandria, Italy

Supporting Agencies

Secretaria Nacional de Ciencia y Tecnologia

How to Cite

Rodas-Moran, Andrea Eunice, Carlos Avendaño, Itzel Sigala, and Bessie Evelyn Oliva-Hernandez. 2022. “First Ecological Analysis of Lacustrine Testate Amoebae in Guatemala: A Case Study from the Highland Lake Chichoj”. Journal of Limnology 81 (1). https://doi.org/10.4081/jlimnol.2022.2082.

Similar Articles

1 2 3 4 5 6 7 8 9 10 > >> 

You may also start an advanced similarity search for this article.