Skip to main content
SpringerLink
Log in

Microbial biogeography through the lens of exotic species: the recent introduction and spread of the freshwater diatom Discostella asterocostata in the United States

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

The large population sizes and high dispersal potential of microbes suggests that a given microbial species should be found in all suitable habitats worldwide. Consequently, microbes should not exhibit the kinds of biogeographic patterns seen in macroorganisms. This paradigm is challenged by a growing list of exotic microbes with biogeographic disjunctions that instead promotes microbial dispersal as inherently limited. We sampled water bodies in the United States and compiled records from the literature and public databases to characterize the distribution of the freshwater planktonic diatom, Discostella asterocostata (Xie, Lin, and Cai) Houk and Klee. Discostella asterocostata was thought to be restricted to the Far East, but we report its presence in ecologically similar water bodies across the eastern United States. Populations from the U.S. and China are indistinguishable morphometrically, suggesting they may be recently separated—a hypothesis supported by paleolimnological data, which support an introduction of D. asterocostata into the U.S. as recently as the mid-1980s. The overlapping distributions of D. asterocostata and invasive carp species, in both their native and nonnative ranges, highlighted Asian carp as a possible vector for introduction of the diatom in the U.S. The existence of exotic diatoms underscores natural constraints on microbial dispersal, resulting in biogeographic distributions that can be upended through human activity.

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

Similar content being viewed by others

Availability of data and materials

Distribution records, diatom community counts, and morphometric measurements are available as Supplementary Information.

Code availability

Not applicable.

References

  • Acosta F, Zamor RM, Najar FZ et al (2015) Dynamics of an experimental microbial invasion. Proc Natl Acad Sci USA 112:11594–11599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Appleby PG, Oldfieldz F (1983) The assessment of 210Pb data from sites with varying sediment accumulation rates. Hydrobiologia 103:29–35

    Article  CAS  Google Scholar 

  • Ashby MN, Rine J, Mongodin EF et al (2007) Serial analysis of rRNA genes and the unexpected dominance of rare members of microbial communities. Appl Environ Microbiol 73:4532–4542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baas Becking LGM (1934) Geobiologie of inleiding tot de milieukunde. W.P. Van Stockum & Zoon, The Hague

    Google Scholar 

  • Bell T, Ager D, Song J-I et al (2005) Larger islands house more bacterial taxa. Science 308:1884

    Article  CAS  PubMed  Google Scholar 

  • Bennett JR, Cumming BF, Ginn BK, Smol JP (2010) Broad-scale environmental response and niche conservatism in lacustrine diatom communities. Glob Ecol Biogeogr 19:724–732

    Google Scholar 

  • Borsodi AK, Szabó A, Krett G et al (2017) Gut content microbiota of introduced bigheaded carps (Hypophthalmichthys spp.) inhabiting the largest shallow lake in Central Europe. Microbiol Res 195:40–50

    Article  PubMed  Google Scholar 

  • Branford SN, Duggan IC (2017) Grass carp (Ctenopharyngodon idella) translocations, including hitchhiker introductions, alter zooplankton communities in receiving ponds. Mar Freshw Res 68:2216–2227

    Article  Google Scholar 

  • Briski E, Bailey SA, Casas-Monroy O et al (2012) Relationship between propagule pressure and colonization pressure in invasion ecology: a test with ships’ ballast. Proc R Soc B 279:2990–2997

    Article  PubMed  PubMed Central  Google Scholar 

  • Carter FA, Beadles JK (1983) Range extension of the silver carp Hypophthalmichthys molitrix. J Ark Acad Sci 37:80

    Google Scholar 

  • Çelekli A, Öztürk B, Kapı M (2014) Relationship between phytoplankton composition and environmental variables in an artificial pond. Algal Res 5:37–41

    Article  Google Scholar 

  • Cristescu ME (2015) Genetic reconstructions of invasion history. Mol Ecol 24:2212–2225

    Article  PubMed  Google Scholar 

  • Curtis TP, Sloan WT, Scannell JW (2002) Estimating prokaryotic diversity and its limits. Proc Natl Acad Sci USA 99:10494–10499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Darling JA, Mahon AR (2011) From molecules to management: adopting DNA-based methods for monitoring biological invasions in aquatic environments. Environ Res 111:978–988

    Article  CAS  PubMed  Google Scholar 

  • Dixon P (2003) VEGAN, a package of R functions for community ecology. J Veg Sci 14:927–930

    Article  Google Scholar 

  • Domaizon I, Devaux J (1999) Experimental study of the impacts of silver carp on plankton communities of eutrophic Villerest reservoir (France). Aquat Ecol 33:193–204

    Article  CAS  Google Scholar 

  • Duarte LN, Coelho FJRC, Cleary DFR et al (2019) Bacterial and microeukaryotic plankton communities in a semi-intensive aquaculture system of sea bass (Dicentrarchus labrax): a seasonal survey. Aquaculture 503:59–69

    Article  Google Scholar 

  • Duggan IC, Pullan SG (2017) Do freshwater aquaculture facilities provide an invasion risk for zooplankton hitchhikers? Biol Invasions 19:307–314

    Article  Google Scholar 

  • Edlund MB, Taylor CM, Schelske CL, Stoermer EF (2000) Thalassiosira baltica (Grunow) Ostenfeld (Bacillariophyta), a new exotic species in the Great Lakes. Can J Fish Aquat Sci 57:610–615

    Article  Google Scholar 

  • Eichmiller JJ, Hamilton MJ, Staley C et al (2016) Environment shapes the fecal microbiome of invasive carp species. Microbiome 4:44

    Article  PubMed  PubMed Central  Google Scholar 

  • Fenchel T, Finlay BJ (2004) The ubiquity of small species: patterns of local and global diversity. Bioscience 54:777–784

    Article  Google Scholar 

  • Field CB, Behrenfeld MJ, Randerson JT, Falkowski P (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281:237–240

    Article  CAS  PubMed  Google Scholar 

  • Finlay BJ (2002) Global dispersal of free-living microbial eukaryote species. Science 296:1061–1063

    Article  CAS  PubMed  Google Scholar 

  • Finlay BJ, Monaghan EB, Maberly SC (2002) Hypothesis: the rate and scale of dispersal of freshwater diatom species is a function of their global abundance. Protist 153:261–273

    Article  PubMed  Google Scholar 

  • Foissner W (2006) Biogeography and dispersal of micro-organisms: a review emphasizing protists. Acta Protozool 45:111–136

    Google Scholar 

  • Freeze M, Henderson S (1982) Distribution and status of the Bighead Carp and Silver Carp in Arkansas. N Am J Fish Manag 2:197–200

    Article  Google Scholar 

  • Görgényi J, Boros G, Vitál Z et al (2016) The role of filter-feeding Asian carps in algal dispersion. Hydrobiologia 764:115–126

    Article  Google Scholar 

  • Greenfield DW (1973) An evaluation of the advisability of the release of the grass carp, Ctenopharyngodon idella, into the natural waters of the United States. Trans Ill State Acad Sci 66:47–53

    Google Scholar 

  • Hansson H, Renberg I (2008) The HTH sediment corer. J Paleolimnol 40:655–659

    Article  Google Scholar 

  • Harper MA (1994) Did Europeans introduce Asterionella formosa Hassall to New Zealand. In: Kociolek JP (ed) Proceedings of the 11th international diatom symposium. California Academy of Sciences, pp 479–484

  • Hawryshyn J, Rühland KM, Julius M, Smol JP (2012) Absence of evidence is not evidence of absence: is Stephanodiscus binderanus (Bacillariophyceae) an exotic species in the Great Lakes region? J Phycol 48:270–274

    Article  PubMed  Google Scholar 

  • Houk V (1992) Cyclotella asterocostata Lin, Xie et Cai (Bacillariophyceae): a little known stelligeroid Cyclotella species from China. Arch Hydrobiol Suppl Bd 95(95):33–43

    Google Scholar 

  • Houk V, Klee R, Tanaka H (2010) Atlas of freshwater centric diatoms with a brief key and descriptions. Part III. Stephanodiscaceae A: Cyclotella, Tertiarius Discostella. Fottea (Supplement) 10:1–498

    Google Scholar 

  • Jennings DP (1988) Bighead Carp (Hypophthalmichthys nobilis): A Biological Synopsis. Fish and Wildlife Service, U.S. Department of the Interior

  • Jia X, Dini-Andreote F, Falcão Salles J (2018) Community assembly processes of the microbial rare biosphere. Trends Microbiol 26:738–747

    Article  CAS  PubMed  Google Scholar 

  • Kelly AM, Engle CR, Armstrong ML et al (2011) History of introductions and governmental involvement in promoting the use of grass, silver, and bighead carps. In: Chapman DC, Hoff MH (eds) Invasive Asian Carps in North America. American Fisheries Society, Symposium. American Fisheries Society, Bethesda, pp 163–174

    Google Scholar 

  • Klein G, MacIntosh K, Kaczmarska I, Ehrman JM (2010) Diatom survivorship in ballast water during trans-Pacific crossings. Biol Invasions 12:1031–1044

    Article  Google Scholar 

  • Kolar CS (2007) Bigheaded carps: a biological synopsis and environmental risk assessment. American Fisheries Society, Bethesda

    Book  Google Scholar 

  • Krammer K, Lange-Bertalot H (1991) Bacillariophyceae: Teil 3: Centrales, Fragilariaceae. Gustav Fisher Verlag, Eunotiaceae

    Google Scholar 

  • Lê S, Josse J, Husson F et al (2008) FactoMineR: an R package for multivariate analysis. J Stat Softw 25:1–18

    Article  Google Scholar 

  • Lee JH, Chung J, Gotoh T (1995) Cyclotella orientalis sp. nov. (Bacillariophyceae) from South Korea. Phycol Res 43:145–149

    Article  Google Scholar 

  • Litchman E (2010) Invisible invaders: non-pathogenic invasive microbes in aquatic and terrestrial ecosystems. Ecol Lett 13:1560–1572

    Article  PubMed  Google Scholar 

  • Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20:223–228

    Article  PubMed  Google Scholar 

  • Lowe RL (1975) Comparative ultrastructure of the valves of some Cyclotella species (Bacillariophyceae). J Phycol 11:415–424

    Article  Google Scholar 

  • Malviya S, Scalco E, Audic S et al (2016) Insights into global diatom distribution and diversity in the world’s ocean. Proc Natl Acad Sci USA 113:E1516–E1525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martiny JBH, Bohannan BJM, Brown JH et al (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102–112

    Article  CAS  PubMed  Google Scholar 

  • Medvedeva L, Nikulina T, Genkal S (2009) Centric diatoms (Coscinodiscophyceae) of fresh and brackish water bodies of the southern part of the Russian Far East. Oceanol Hydrobiol Stud 38:139–164

    Article  Google Scholar 

  • Mitchell CP, Fish GR, Burnet AMR (1984) Limnological changes in a small lake stocked with grass carp. N Z J Mar Freshw Res 18:103–114

    Article  CAS  Google Scholar 

  • Nakov T, Beaulieu JM, Alverson AJ (2019) Diatoms diversify and turn over faster in freshwater than marine environments. Evolution 73:2497–2511

    Article  PubMed  Google Scholar 

  • Nemergut DR, Costello EK, Hamady M et al (2011) Global patterns in the biogeography of bacterial taxa. Environ Microbiol 13:135–144

    Article  PubMed  PubMed Central  Google Scholar 

  • Patrick R, Reimer CW (1966) The diatoms of the United States, exclusive of Alaska and Hawaii: Fragilariaceae, Eunotiaceae, Achnanthaceae, Naviculacae. Academy of Natural Sciences of Philadelphia, Philadelphia

    Book  Google Scholar 

  • Pearson AAC, Duggan IC (2018) A global review of zooplankton species in freshwater aquaculture ponds: what are the risks for invasion? Aquat Invasions 13:311–322

    Article  Google Scholar 

  • Peay KG, Bruns TD, Kennedy PG et al (2007) A strong species-area relationship for eukaryotic soil microbes: Island size matters for ectomycorrhizal fungi. Ecol Lett 10:470–480

    Article  PubMed  Google Scholar 

  • Ping X, Jiankang L (1994) Phytoplankton, especially diatoms, in the gut contents and feces of two plantivorous cyprinids—silver carp and bighead carp. Chin J Oceanol Limnol 12:308–315

    Article  Google Scholar 

  • Pinseel E, Janssens SB, Verleyen E et al (2020) Global radiation in a rare biosphere soil diatom. Nat Commun 11:2382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Preston FW (1948) The commonness, and rarity, of species. Ecology 29:254–283

    Article  Google Scholar 

  • Robison HW, Buchanan TM (2020) Fishes of Arkansas. University of Arkansas Press, Fayetteville

    Google Scholar 

  • Round FE, Crawford RM, Mann DG (1990) Diatoms: biology and morphology of the genera. Cambridge University Press, Cambridge

    Google Scholar 

  • Schindelin J, Rueden CT, Hiner MC, Eliceiri KW (2015) The ImageJ ecosystem: an open platform for biomedical image analysis. Mol Reprod Dev 82:518–529

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shaw Chraïbi VL, Kireta AR, Reavie ED et al (2014) A paleolimnological assessment of human impacts on Lake Superior. J Great Lakes Res 40:886–897

    Article  Google Scholar 

  • Simonsen R (1987) Atlas and catalogue of the diatom types of Friedrich Hustedt Volumes I-III. J. Cramer, Wyndmoor

    Google Scholar 

  • Smol JP, Stoermer EF (2010) The diatoms: applications for the environmental and earth sciences. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Spaulding SA, Kilroy C, Edlund MB (2010) Diatoms as non-native species. In: Smol JP, Stoermer EF (eds) The diatoms: applications for the environmental and earth sciences. Cambridge University Press, Cambridge, pp 560–569

    Chapter  Google Scholar 

  • Stepien CA, Snyder MR, Elz AE (2019) Invasion genetics of the silver carp Hypophthalmichthys molitrix across North America: Differentiation of fronts, introgression, and eDNA metabarcode detection. PLoS ONE 14:e0203012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stevenson J (2014) Ecological assessments with algae: a review and synthesis. J Phycol 50:437–461

    Article  PubMed  Google Scholar 

  • Sturtevant RA, Mason DM, Rutherford ES et al (2019) Recent history of nonindigenous species in the Laurentian Great Lakes: An update to Mills et al., 1993 (25 years later). J Great Lakes Res 45:1011–1035

    Article  Google Scholar 

  • Tanaka H (2007) Taxonomic studies of the genera Cyclotella (Kützing) Brébisson, Discostella Houk et Klee, and Puncticulata Håkansson in the family Sephanodiscaceae Glezer et Makarova (Bacillariophyta) in Japan. J. Cramer, Wyndmoor

    Google Scholar 

  • Tedesco PA, Beauchard O, Bigorne R et al (2017) A global database on freshwater fish species occurrence in drainage basins. Sci Data 4:170141

    Article  PubMed  PubMed Central  Google Scholar 

  • Telford RJ, Vandvik V, Birks HJB (2006) Dispersal limitations matter for microbial morphospecies. Science 312:1015

    Article  CAS  PubMed  Google Scholar 

  • Theriot EC (1987) Principal component analysis and taxonomic interpretation of environmentally related variation in silicification in Stephanodiscus (Bacillariophyceae). Br Phycol J 22:359–373

    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

    Article  Google Scholar 

  • Tréguer P, Nelson DM, Van Bennekom AJ et al (1995) The silica balance in the world ocean: a reestimate. Science 268:375–379

    Article  PubMed  Google Scholar 

  • Tucker JK, Cronin FA, Hrabik RA et al (1996) The bighead carp (Hypophthalmichthys nobilis) in the Mississippi River. J Freshw Ecol 11:241–243

    Article  Google Scholar 

  • Tyler PA (1996) 13. Endemism in freshwater algae. Hydrobiologia 336:127–135

    Article  Google Scholar 

  • Vanormelingen P, Verleyen E, Vyverman W (2008) The diversity and distribution of diatoms: from cosmopolitanism to narrow endemism. Biodivers Conserv 17:393–405

    Article  Google Scholar 

  • Vörös L, Oldal I, Présing M, Balogh VK (1997) Size-selective filtration and taxon-specific digestion of plankton algae by silver carp (Hypophthalmichthys molitrix Val.). Hydrobiologia 342(343):223–228

    Article  Google Scholar 

  • Vyverman W, Sabbe K, Mann D et al (1998) Eunophora gen. nov. (Bacillariophyta) from Tasmania and New Zealand: Description and comparison with Eunotia and amphoroid diatoms. Eur J Phycol 33:95–111

    Article  Google Scholar 

  • Vyverman W, Verleyen E, Sabbe K et al (2007) Historical processes constrain patterns in global diatom diversity. Ecology 88:1924–1931

    Article  PubMed  Google Scholar 

  • Williams DM, Reid G (2006) Diatom biogeography and water babies: the search for meaning among the protists. Diatom Res 21:457–462

    Article  Google Scholar 

  • Xin S-Q, Lin B-Q, Cai S-X (1985) Studies by means of LM and EM on a new species, Cyclotella asterocostata Lin, Xie et Cai. Acta Phytotax Sin 23:473–475

    Google Scholar 

  • Yeager KM, Santschi PH, Rowe GT (2004) Sediment accumulation and radionuclide inventories (239,240 Pu, 210Pb and 234Th) in the northern Gulf of Mexico, as influenced by organic matter and macrofaunal density. Mar Chem 91:1–14

    Article  CAS  Google Scholar 

  • Zou Y, Yan Y, Zhang J et al (2015) 云龙天池湖泊水深与硅藻生物多样性的关系 (The relationship between the water depth of Yunlong Tianchi lake and diatom biodiversity). Quat Sci 35:988–996

    Google Scholar 

Download references

Acknowledgements

We thank Anna Yu for help obtaining the isotype material and Don Charles for facilitating access to public databases. Sediment cores were collected, subsampled, and processed for this project by Erika Smith, Helena Bierly, Ken Cleghorn, Jared Foster, and Corey Portwood.

Funding

Research was supported by the ISU Center for Student Research and Creativity, the ISU Department of Earth and Environmental Systems, the ISU Summer Undergraduate Research Experience program. This work was also supported by the National Science Foundation (Grant Number DEB-1651087 to AJA), a Student Undergraduate Research Fellowship from the Arkansas Department of Higher Education to KAJ, and multiple awards from the Arkansas Biosciences Institute to AJA.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, University of Arkansas, Fayetteville, AR, USA

    Andrew J. Alverson, Tyler K. Chafin, Kiley A. Jones, Teofil Nakov & Elizabeth C. Ruck

  2. Department of Biological and Environmental Sciences, Georgia College and State University, Milledgeville, GA, USA

    Kalina M. Manoylov

  3. Department of Earth and Environmental Systems, Indiana State University, Terre Haute, IN, USA

    Hillary Johnson & Jeffery R. Stone

  4. Department of Biological Sciences, St. Cloud State University, St. Cloud, MN, USA

    Matthew L. Julius

  5. Section of Integrative Biology, The University of Texas at Austin, Austin, TX, USA

    Edward C. Theriot

  6. Department of Earth and Environmental Sciences, University of Kentucky, Lexington, KY, USA

    Kevin M. Yeager

Authors
  1. Andrew J. Alverson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tyler K. Chafin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kiley A. Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kalina M. Manoylov
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hillary Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Matthew L. Julius
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Teofil Nakov
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Elizabeth C. Ruck
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Edward C. Theriot
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Kevin M. Yeager
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Jeffery R. Stone
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrew J. Alverson.

Ethics declarations

Conflict of interest

Not applicable.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alverson, A.J., Chafin, T.K., Jones, K.A. et al. Microbial biogeography through the lens of exotic species: the recent introduction and spread of the freshwater diatom Discostella asterocostata in the United States. Biol Invasions 23, 2191–2204 (2021). https://doi.org/10.1007/s10530-021-02497-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-021-02497-5

Keywords

Search

Navigation