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Ecological distribution of Stephanodiscus niagarae Ehrenberg in central Mexico and niche modeling for its last glacial maximum habitat suitability in the Nearctic realm

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Abstract

Stephanodiscus niagarae Ehrenberg is currently restricted to specific regions of central Mexico, however, during the late Pleistocene, it had a wider distribution in the country. This change in distribution is similar to those observed for several organisms that migrated southwards during cold, glacial climates, supporting the hypothesis that central Mexico acted as glacial refugia for these species. This study aims to support this hypothesis for S. niagarae as well as to analyze its ecological distribution in modern environments in central Mexico. For this purpose we studied 18 samples from 16 lakes located around Mexico City, selected among 46 lakes along the Trans-Mexican Volcanic Belt. Diatom assemblages in superficial sediments, and climatic, hydrochemistry, and nutrient parameters of each lake were analyzed by means of canonical correspondence analyses. Additionally, we created an ecological niche model (ENM) with modern occurrence data (n = 47) and environmental variables (WorldClim) to produce potential distribution maps of S. niagarae during the present time and under the LGM conditions in the Nearctic realm. S. niagarae was recorded only in 4 sites in central Mexico (abundances < 10%) associated with temperate, subhumid conditions in freshwater lakes with [Mg2+] − [Ca2+] − [HCO3] ionic dominance and high turbidity, mesotrophic to hypertrophic systems (based on chlorophyll a values), but with a tendency to P-limitation. In our study sites S. niagarae showed low abundances in diatom assemblages dominated by Aulacoseira spp. Temperature (annual mean, coldest and warmest quarters means) was identified by ENM as the main environmental variable controlling its distribution, with its highest modern support in the USA, southern Canada, and a restricted distribution in the highlands of western and central Mexico. Whereas, the LGM scenario (− 5.5 °C) identified the western and central highlands in Mexico and southern USA as the highest probability distribution areas supporting the approach that the Sierra Madre Occidental could have acted as a migration corridor offering suitable habitats for a southward migration into central Mexico during colder (glacial) periods. In conclusion, S. niagarae distribution in the central and western mountains of Mexico is controlled by temperature changes and its presence may be associated with colder (glacial) periods.

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References

  • American Public Health Association (APHA) (1995) Standard methods for the examination of water and wastewater. American Public Health Association, Washington

    Google Scholar 

  • American Public Health Association (APHA) (1998) Standard methods for the examination of water and wastewater. American Public Health Association, Washington

    Google Scholar 

  • American Public Health Association (APHA), American Water Works Association (AWWA), Water Pollution Control Federation (WPCF) (2005) Standard methods for the examination of water and wastewater. American Public Health Association, Washington

    Google Scholar 

  • Armienta MA, Vilaclara G, De la Cruz-Reyna S et al (2008) Water chemistry of lakes related to active and inactive Mexican volcanoes. J Volcanol Geotherm Res 178:249–258. https://doi.org/10.1016/j.jvolgeores.2008.06.019

    Article  Google Scholar 

  • Avendaño D, Caballero M, Ortega-Guerrero B et al (2018) Environmental conditions at the end of the Isotopic Stage 6 (IS 6: > 130000 years) in the center of Mexico: Characterization of a section of laminated sediments from Lake Chalco. Rev Mex Ciencias Geol 35:168–178. https://doi.org/10.22201/cgeo.20072902e.2018.2.649

    Article  Google Scholar 

  • Bradbury JP (1971) Paleolimnology of Lake Texcoco, Mexico. Evidence from diatoms. Limnol Oceanogr 16:180–200. https://doi.org/10.4319/lo.1971.16.2.0180

    Article  Google Scholar 

  • Bradbury JP (2000) Limnologic history of Lago de Patzcuaro, Michoacan, Mexico for the past 48,000 years: impacts of climate and man. Palaeogeogr Palaeoclimatol Palaeoecol 163:69–95. https://doi.org/10.1016/S0031-0182(00)00146-2

    Article  Google Scholar 

  • Bradbury JP, Colman SM, Dean WE (2004) Limnological and climatic environments at Upper Klamath Lake, Oregon during the past 45 000 years. J Paleolimnol 31:167–188. https://doi.org/10.1023/B:JOPL.0000019232.74649.02

    Article  Google Scholar 

  • Brady EC, Otto-bliesner BL, Kay JE, Rosenbloom N (2013) Sensitivity to glacial forcing in the CCSM4. J Clim 26:1901–1925. https://doi.org/10.1175/JCLI-D-11-00416.1

    Article  Google Scholar 

  • Brugam RB (1983) The relationship between fossil diatom assemblages and limnological conditions. Hydrobiologia 98:223–235. https://doi.org/10.1007/BF00021023

    Article  Google Scholar 

  • Caballero M, Ortega Guerrero B (1998) Lake levels since about 40,000 years ago at Lake Chalco, near Mexico City. Quat Res 50:69–79. https://doi.org/10.1006/qres.1998.1969

    Article  Google Scholar 

  • Caballero M, Lozano S, Ortega B et al (1999) Environmental characteristics of Lake Tecocomulco, northern basin of Mexico, for the last 50,000 years. J Paleolimnol 22:399–411. https://doi.org/10.1023/A:1008012813412

    Article  Google Scholar 

  • Caballero M, Lozano-García S, Ortega-Guerrero B, Correa-Metrio A (2019) Quantitative estimates of orbital and millennial scale climatic variability in central Mexico during the last ∼40,000 years. Quat Sci Rev 205:62–75. https://doi.org/10.1016/j.quascirev.2018.12.002

    Article  Google Scholar 

  • Ceballos G, Arroyo-Cabrales J, Ponce E (2010) Effects of Pleistocene environmental changes on the distribution and community structure of the mammalian fauna of Mexico. Quat Res 73:464–473. https://doi.org/10.1016/j.yqres.2010.02.006

    Article  Google Scholar 

  • Cobos ME, Townsend Peterson A, Barve N, Osorio-Olvera L (2019) Kuenm: An R package for detailed development of ecological niche models using Maxent. PeerJ 7:e6281. https://doi.org/10.7717/peerj.6281

    Article  Google Scholar 

  • Colman SM, Bradbury JP, Rosenbaum JG (2004) Paleolimnology and paleoclimate studies in Upper Klamath Lake, Oregon. J Paleolimnol 31:129–138. https://doi.org/10.1023/B:JOPL.0000019235.72107.92

    Article  Google Scholar 

  • Correa-Metrio A, Bush M, Lozano-García S, Sosa-Nájera S (2013) Millennial-scale temperature change velocity in the continental northern neotropics. PLoS ONE 8:e81958. https://doi.org/10.1371/journal.pone.0081958

    Article  Google Scholar 

  • Davies SJ, Metcalfe SE, Caballero ME, Juggins S (2002) Developing diatom-based transfer functions for Central Mexican lakes. Hydrobiologia 467:199–213. https://doi.org/10.1023/A:1014971016298

    Article  Google Scholar 

  • Edlund M, Kingston J, Heiskary S (2004) Expanding a sediment diatom reconstruction model to eutrophic Southern Minnesota Lakes. Environmental Outcomes Division Minnesotta Pollution Control Agency. CFMS Contract No. A45276, Minnesota

  • Edmondson WT, Abella SEB, Lehman JT (2003) Phytoplankton in Lake Washington: long-term changes 1950–1999. Arch Hydrobiol Suppl 139:275–326

    Google Scholar 

  • Fritz S (2007) Salinity and climate reconstruction from diatoms in continental lake deposits. In: Elias SA (ed) Encyclopedia of quaternary science. Elsevier, Amsterdam, pp 514–522

    Chapter  Google Scholar 

  • Fritz SC, Juggins S, Battarbee RW (1993) Diatom assemblages and ionic characterization of lakes of the Northern Great Plains, North America: a tool for reconstructing past salinity and climate fluctuations. Can J Fish Aquat Sci 50:1844–1856. https://doi.org/10.1139/f93-207

    Article  Google Scholar 

  • Fritz SC, Cumming BF, Gasse F, Laird KR (2001) Diatoms as indicators of hydrologic and climatic change in saline lakes. In: Stoermer EF, Smol JP (eds) The diatoms: applications for the environmental and earth sciences. Cambridge University Press, Cambridge, pp 41–72

    Google Scholar 

  • Gasse F (1986) East African diatoms: Taxonomy, Ecological Distribution. Bibliotheca Diatomologica, Stuttgart

    Google Scholar 

  • Gent PR, Danabasoglu G, Donner LJ, Holland MM, Hunke EC, Jayne SR, Lawrence DM, Neale RB, Rasch PJ, Vertenstein M, Worley P, Yang ZL, Zhang M (2011) The community climate system model version 4. J Clim 24:4973–4991. https://doi.org/10.1175/2011JCLI4083.1

    Article  Google Scholar 

  • Graham RW, Lundelius EL Jr, Graham MA, Schroeder EK, Toomey RS III, Anderson E, Barnosky AD, Burns JA, Churcher CS, Grayson DK, Guthrie DR, Harington CR, Jefferson GT, Martin LD, McDonald GH, Morlan RE, Semken HA Jr, Webb DS, Werdelin L, Wilson MC (1996) Spatial response of mammals to late quaternary environmental fluctuations FAUNMAP working group. Science 272:1601–1606. https://doi.org/10.1126/science.272.5268.1601

    Article  Google Scholar 

  • Håkansson H (2002) A compilation and evaluation of species in the general Stephanodiscus, Cyclostephanos and Cyclotella with a new genus in the family Stephanodiscaceae. Diatom Res 17:1–139. https://doi.org/10.1080/0269249X.2002.9705534

    Article  Google Scholar 

  • Håkansson H, Locker S (1981) Stephanodiscus Ehrenberg 1846, a Revision of the species described by Ehrenberg. Nova Hedwigia 35:117–150

    Google Scholar 

  • Håkansson H, Kling H (1989) A light and electron microscope study of previously described and new Stephanodiscus species (Bacillariophyceae) from Central and Northern Canadian lakes, with ecological notes on the species. Diatom Res 4:269–288. https://doi.org/10.1080/0269249X.1989.9705076

    Article  Google Scholar 

  • Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913. https://doi.org/10.1038/35016000

    Article  Google Scholar 

  • Hijmans RJ, Cameron SE, Parra JL et al (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978. https://doi.org/10.1002/joc.1276

    Article  Google Scholar 

  • Israde-Alcántara I, Garduño-Monroy VH, Ortega Murillo R (2002) Paleoambiente lacustre del cuaternario tardío en el centro del lago de Cuitzeo. Hidrobiologica 12:61–78

    Google Scholar 

  • Israde-Alcántara I, Miller WE, Garduño-Monroy VH et al (2010a) Palaeoenvironmental significance of diatom and vertebrate fossils from Late Cenozoic tectonic basins in west-central México: a review. Quat Int 219:79–94. https://doi.org/10.1016/j.quaint.2010.01.012

    Article  Google Scholar 

  • Israde-Alcántara I, Velázquez-Durán R, Socorro Lozano García M et al (2010b) Evolución Paleolimnológica del Lago Cuitzeo, Michoacán durante el Pleistoceno-Holoceno. Bol Soc Geol Mex 62:345–357

    Article  Google Scholar 

  • Israde-Alcántara I, Domínguez-Vázquez G, Gonzalez S et al (2018) Five Younger Dryas black mats in Mexico and their stratigraphic and paleoenvironmental context. J Paleolimnol 59:59–79. https://doi.org/10.1007/s10933-017-9982-y

    Article  Google Scholar 

  • Jackson ST, Webb RS, Anderson KH et al (2000) Vegetation and environment in Eastern North America during the last glacial maximum. Quat Sci Rev 19:489–508

    Article  Google Scholar 

  • Julius M, Stoermer EF, Taylor CM, Schelske CL (1998) Local extirpation of Stephanodiscus niagarae (Bacillariophyceae) in the recent limnological record of Lake Ontario. J Phycol 34:766–771. https://doi.org/10.1046/j.1529-8817.1998.340766.x

    Article  Google Scholar 

  • Kilham SS, Theriot EC, Fritz SC (1996) Linking planktonic diatoms and climate change in the large lakes of the Yellowstone ecosystem using resource theory. Limnol Oceanogr 41:1052–1062. https://doi.org/10.4319/lo.1996.41.5.1052

    Article  Google Scholar 

  • Kolbe RW (1927) Zur ökologie, morphologie und systematik der brackwasser-diatomeen: Die kieselalgen des Sperenberger salzgebiets. G. Fischer Jena, Berlin-Dahlem

    Google Scholar 

  • Krammer K, Lange-Bertalot H (1986) 2/1. Bacillariophyceae. 1. Teil: Naviculaceae. In: Ettl H, Gerloff J, Heynig H, Mollenhauer D (eds) Sübwasserflora von Mitteleuropa. G. Fischer Verlag, Stuttgart

  • Krammer K, Lange-Bertalot H (1988) 2/2. Bacillariophyceae. 2. Teil: Bacillariaceae, Epithemiaceae, Surirellaceae. In: Ettl H, Gerloff J, Heynig H, Mollenhauer D (eds) Sübwasserflora von Mitteleuropa. G. Fischer Verlag, Stuttgart

  • Krammer K, Lange-Bertalot H (1991) 2/4. Bacillariophyceae. 4. Teil: Achnanthaceae. Kritische Ergänzungen zu Navicula (Lineolatae) und Gomphonema. In: Ettl H, Gerloff J, Heynig H, Mollenhauer D (eds) Sübwasserflora von Mitteleuropa. G. Fischer Verlag, Stuttgart

  • Krammer K, Lange-Bertalot H, Håkansson H, Nörpel M (1991) 2/3 Bacillariophyceae. 3. Teil: Centrales, Fragilariaceae, Eunotiaceae. In: Ettl H, Gerloff J, Heynig H, Mollenhauer D (eds) Sübwasserflora von Mitteleuropa. G. Fischer Verlag, Stuttgart

  • Lashaway AR, Carrick HJ (2010) Effects of light, temperature and habitat quality on meroplanktonic diatom rejuvenation in Lake Erie: Implications for seasonal hypoxia. J Plankton Res 32:479–490. https://doi.org/10.1093/plankt/fbp147

    Article  Google Scholar 

  • Meeks CJ (1974) Chlorophylls. In: Stewart PDW (ed) Algal physiology and biochemistry. Blackwell Scientific Publications, Oxford, pp 161–175

    Google Scholar 

  • Metcalfe S (1995) Holocene environmental change in the Zacapu Basin, Mexico: a diatom-based record. The Holocene 5:196–208. https://doi.org/10.1177/095968369500500207

    Article  Google Scholar 

  • Metcalfe S, Say A, Black S et al (2002) Wet conditions during the last glaciation in the Chihuahuan Desert, Alta Babicora Basin, Mexico. Quat Res 57:91–101. https://doi.org/10.1006/qres.2001.2292

    Article  Google Scholar 

  • Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2019) Vegan: community ecology package. The R Project for Statistical Computing. http://CRAN.R

  • Oliva-Martínez MG, Ramírez-Martínez JG, Garduño-Solórzano G, Cañetas Ortega J, Ortega MM (2005) Diatoms of three bodies of water from wetlands Jilotepec-Ixtlahuaca, Estado de Mexico. Hidrobiologica 15:1–26

    Google Scholar 

  • Organization for Economic Cooperation and Development (OECD) (1982) Eutrophication of waters. Organization for Economic Cooperation and Development, Paris

    Google Scholar 

  • Osorio-Olvera L, Lira-Noriega A, Soberón J, Townsend PA, Falconi M, Contreras-Díaz RG, Martínez-Meyer E, Barve V, Barve N (2020) ntbox: an R package with graphical user interface for modeling and evaluating multidimensional ecological niches. Methods Ecol Evol 11:1199–1206. https://doi.org/10.1111/2041-210X.13452

    Article  Google Scholar 

  • Pardi MI, Graham RW (2019) Changes in small mammal communities throughout the late Quaternary across eastern environmental gradients of the United States. Quat Int 530–531:80–87. https://doi.org/10.1016/j.quaint.2018.05.041

    Article  Google Scholar 

  • Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Modell 190:231–259. https://doi.org/10.1016/j.ecolmodel.2005.03.026

    Article  Google Scholar 

  • Pla S, Paterson AM, Smol JP et al (2005) Spatial Variability in Water Quality and Surface Sediment Diatom Assemblages in a Complex Lake Basin: Lake of the Woods, Ontario, Canada. Int J Gt Lake Res 31:253–266. https://doi.org/10.1016/S0380-1330(05)70257-4

    Article  Google Scholar 

  • R Development Core Team (2009) R: a language and environment for statistical computing, 3.1. http://www.R-project.org

  • Rawson DS (1956) Algal indicators of trophic lake types. Limnol Oceanogr 1:18–25

    Article  Google Scholar 

  • Reavie ED, Barbiero RP, Allinger LE, Warren GJ (2014a) Phytoplankton trends in the Great Lakes 2001–2011. J Gt Lake Res 40:618–639. https://doi.org/10.1016/j.jglr.2014.04.013

    Article  Google Scholar 

  • Reavie ED, Heathcote AJ, Chraïbi S (2014b) Laurentian Great Lakes phytoplankton and their water quality characteristics, including a diatom-based model for paleoreconstruction of phosphorus. PLoS ONE 9:e104705. https://doi.org/10.1371/journal.pone.0104705

    Article  Google Scholar 

  • Redfield AC (1958) The biological control of chemical factors in the environment. Am Sci 64:205–221

    Google Scholar 

  • Reynolds CS (1999) Non-determinism to probability, or N: P in the community ecology of phytoplankton nutrient ratios: Arch. Fur Hydrobiol 146:23–35

    Google Scholar 

  • Servicio Meteorológico Nacional (SMN) (2019) Información Estadística Climatológica. https://smn.conagua.gob.mx/es/climatologia/informacion-climatologica/informacion-estadistica-climatologica. Accessed 1 May 2019

  • Sigala I, Caballero M, Correa-Metrio A et al (2017) Basic limnology of 30 continental waterbodies of the Transmexican Volcanic Belt across climatic and environmental gradients. Bol Soc Geol Mex 69:313–370. https://doi.org/10.18268/bsgm2017v69n2a3

    Article  Google Scholar 

  • Spaulding SA, Kociolek JP, Wong D, Kociolek IP (1999) A taxonomic and systematic revision of the genus Muelleria (Bacillariophyta). Phycologia 38:314–341. https://doi.org/10.2216/i0031-8884-38-4-314.1

    Article  Google Scholar 

  • Spaulding SA, Van de Vijver B, Hodgson DA, McKnigth DM, Verleyen E, Stanish L (2010) Diatoms as indicators of environmental change in antarctic and subantarctic freshwaters. In: Smol J, Stoermer EF (eds) The diatoms: applications for the environmental and earth sciences. Cambridge University Press, New York, pp 267–284

    Chapter  Google Scholar 

  • Stewart JR, Lister AM, Barnes I, Dalén L (2009) Refugia revisited: Individualistic responses of species in space and time. Proc R Soc B Biol Sci 277:661–671. https://doi.org/10.1098/rspb.2009.1272

    Article  Google Scholar 

  • Stoermer EF, Jang JJ (1970) Distribution and relative abundance of dominant plankton diatoms in Lake Michigan. Gt Lakes Res Div, Michigan

  • Stoermer EF, Ladewski TB (1976) Apparent optimal temperatures for the occurrence of some common phytoplankton species in southern Lake Michigan. Gt Lakes Res Div, Michigan

  • Stoermer EF, Emmert G, Schelske CL (1989) Morphological variation of Stephanodiscus niagarae Ehrenb. (Bacillariophyta) in a Lake Ontario sediment core. J Paleolimnol 2:227–236. https://doi.org/10.1007/BF00202048

    Article  Google Scholar 

  • Theriot EC, Stoermer EF (1981) Some aspects of morphological variation in S. niagarae (Bacillariophyceae). J Phycol 17:64–72. https://doi.org/10.1111/j.1529-8817.1981.tb00820.x

    Article  Google Scholar 

  • Theriot EC, Stoermer EF (1984a) Principal component analysis of character variation in Stephanodiscus niagarae Ehrenb.: Morphological variation related to Lake Trophic status. In: Mann DG (ed) 7th international diatom symposium. Otto Koeltz Science Publishers, Koenigstein, pp 97–111

    Google Scholar 

  • Theriot EC, Stoermer EF (1984b) Principal component analysis of variation in Stephanodiscus rotula and S. niagarae (Bacillariophyceae). Syst Bot 9:53–59. https://doi.org/10.2307/2418407

    Article  Google Scholar 

  • Theriot EC, Fritz SC, Whitlock C, Conley DJ (2006) Late Quaternary rapid morphological evolution of an endemic diatom in Yellowstone Lake, Wyoming. Paleobiology 32:38–54. https://doi.org/10.1666/02075.1

    Article  Google Scholar 

  • Valadez F, Oliva G, Vilaclara G et al (2005) On the presence of Stephanodiscus niagarae Ehrenberg in central Mexico. J Paleolimnol 34:147–157. https://doi.org/10.1007/s10933-005-0810-4

    Article  Google Scholar 

  • Waltari E, Hijmans RJ, Peterson AT et al (2007) Locating pleistocene refugia: comparing phylogeographic and ecological niche model predictions. PLoS ONE 2:e563. https://doi.org/10.1371/journal.pone.0000563

    Article  Google Scholar 

  • Xu J, Ho AYT, Yin K et al (2008) Temporal and spatial variations in nutrient stoichiometry and regulation of phytoplankton biomass in Hong Kong waters: Influence of the Pearl River outflow and sewage inputs. Mar Pollut Bull 57:335–348. https://doi.org/10.1016/j.marpolbul.2008.01.020

    Article  Google Scholar 

  • Yu A (2011) Stephanodiscus niagarae. In: Diatoms North Am. https://diatoms.org/species/stephanodiscus_niagarae. Accessed 6 Sep 2019

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Acknowledgements

This research was funded by DGAPA-IV-100215 “Cambio Climático y Medio Ambiente en la historia del lago de Chalco” and DGAPA-PAPIIT-IN103819 “Variabilidad climática y paleoambientes durante la terminación II (130 ka): el paso del penúltimo glacial (MIS 6) al penúltimo interglaciar (MIS 5)”. Diana Avendaño thanks the Posgrado de Ciencias de la Tierra, UNAM and CONACyT (CVU 854736) for finnancial support. We also thank: Dr. Ma. Aurora Armienta and the staff in the Laboratorio de Quimica Análitica, Instituto de Geofisica, UNAM for major anions and SiO2 analysis; Ariadna Martinez and Daniela Cela from the “Red de Ecología Funcional” laboratory at the Instituto de Ecología, A.C. (INECOL), Xalapa, Mexico, for the nutrients analysis; Laura Gómez Lizárraga for excellent technical assistance with the different stages of sample preparation with the scanning electron microscope and Alejandra Ubaldo Guerra provided assistance during the field work. We also thank Dr. Whitmore, Dr. Reavie and two anonymous reviewers for their valuable comments that greatly improved our manuscript.

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Avendaño, D., Caballero, M. & Vázquez, G. Ecological distribution of Stephanodiscus niagarae Ehrenberg in central Mexico and niche modeling for its last glacial maximum habitat suitability in the Nearctic realm. J Paleolimnol 66, 1–14 (2021). https://doi.org/10.1007/s10933-021-00178-w

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