Living on the edge: reproduction, dispersal potential, maternal effects and local adaptation in aquatic, extremophilic invertebrates

Abstract

Isolated extreme habitats are ideally suited to investigate pivotal ecological processes such as niche use, local adaptation and dispersal. Extremophilic animals living in isolated habitats face the problem that dispersal is limited through the absence of suitable dispersal corridors, which in turn facilitates local adaptation. We used five rotifer isolates from extremely acidic mining lakes with a pH of below 3 as model organisms to test whether these isolates are acidotolerant or acidophilic, whether they survive and reproduce at their niche edges (here pH 2 and circum-neutral pH) and whether local adaptation has evolved. To evaluate potential dispersal limitation, we tested whether animals and their parthenogenetic eggs survive and remain reproductive or viable at unfavourable pH-conditions. All five isolates were acidophilic with a pH-optimum in the range of 4–6, which is well above the pH (< 3) of their lakes of origin. At unfavourable high pH, in four out of the five isolates parthenogenetic females produced a high number of non-viable eggs. Females and eggs produced at favourable pH (4) remained vital at an otherwise unfavourable pH of 7, indicating that for dispersal no acidic dispersal corridors are necessary. Common garden experiments revealed no clear evidence for local adaptation in any of the five isolates. Despite their acidophilic nature, all five isolates can potentially disperse via circum-neutral water bodies as long as their residence time is short, suggesting a broader “dispersal niche” than their realized niche. Local adaptation might have been hampered by the low population sizes of the rotifers in their isolated habitat and the short time span the mining lakes have existed.

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References

  1. Aguilera A (2013) Eukaryotic organisms in extreme environments, the Río Tinto case. Life 3:363–374. https://doi.org/10.3390/life3030363

    Article  PubMed  PubMed Central  Google Scholar 

  2. Aguilera A, Souza-Egipsy V, Gómez F, Amils R (2007) Development and structure of eukaryotic biofilms in an extreme acidic environment, Río Tinto (SW Spain). Microb Ecol 53:294–305. https://doi.org/10.1007/s00248-006-9092-2

    Article  PubMed  Google Scholar 

  3. Amaral Zettler LA, Gómez F, Zettler E, Keenan BG, Amils R, Sogin ML (2002) Eukaryotic diversity in Spain’s River of fire. Nature 417:137. https://doi.org/10.1038/417137a

    CAS  Article  PubMed  Google Scholar 

  4. Amaral-Zettler LA (2013) Eukaryotic diversity at pH extremes. Front Microbiol 3:441. https://doi.org/10.3389/fmicb.2012.00441

    Article  PubMed  PubMed Central  Google Scholar 

  5. Bell EM, Weithoff G, Gaedke U (2006) Temporal dynamics and growth of Actinophrys sol (Sarcodina: Heliozoa), the top predator in an extremely acidic lake. Freshw Biol 51:1149–1161. https://doi.org/10.1111/j.1365-2427.2006.01561.x

    CAS  Article  Google Scholar 

  6. Belyaeva M, Deneke R (2013) Biology and ecosystem of acidic pit lakes: Zooplankton. In: Geller W, Schultze M, Kleinmann R, Wolkersdorfer C (eds) acidic pit lakes. Springer, Berlin, pp 117–126. https://doi.org/10.1007/978-3-642-29384-9

    Google Scholar 

  7. Bissinger V, Jander J, Tittel J (2000) A new medium free of organic carbon to cultivate organisms from extremely acidic mining lakes (pH 2.7). Acta Hydroch Hydrob 28:310–312. https://doi.org/10.1002/1521-401X(200012)28:6%3c310:AID-AHEH310%3e3.0.CO;2-H

    CAS  Article  Google Scholar 

  8. Bowers KJ, Wiegel J (2011) Temperature and pH optima of extremely halophilic archaea: a mini-review. Extremophiles 15:119–128. https://doi.org/10.1007/s00792-010-0347-y

    CAS  Article  PubMed  Google Scholar 

  9. Cáceres CE, Soluk DA (2002) Blowing in the wind: a field test of overland dispersal and colonization by aquatic invertebrates. Oecologia 131:402–408. https://doi.org/10.1007/s00442-002-0897-5

    Article  PubMed  Google Scholar 

  10. Canganella F, Wiegel J (2011) Extremophiles: from abyssal to terrestrial ecosystems and possibly beyond. Naturwissenschaften 98:253–279. https://doi.org/10.1007/s00114-011-0775-2

    CAS  Article  PubMed  Google Scholar 

  11. Cottenie K, Michels E, Nuytten N, de Meester L (2003) Zooplankton metacommunity structure: regional vs. local processes in highly interconnected ponds. Ecology 84:991–1000. https://doi.org/10.1890/0012-9658(2003)084%5b0991:ZMSRVL%5d2.0.CO;2

    Article  Google Scholar 

  12. Deneke R (2000) Review of rotifers and crustaceans in highly acidic environments of pH values ≤ 3. Hydrobiologia 433:167–172. https://doi.org/10.1023/A:1004047510602

    Article  Google Scholar 

  13. Dhakar K, Pandey A (2016) Wide pH range tolerance in extremophiles: towards understanding an important phenomenon for future biotechnology. Appl Microbiol Biotechnol 100:2499–2510. https://doi.org/10.1007/s00253-016-7285-2

    CAS  Article  PubMed  Google Scholar 

  14. Figuerola J, Green AJ (2002) Dispersal of aquatic organisms by waterbirds: a review of past research and priorities for future studies. Freshw Biol 47:483–494. https://doi.org/10.1046/j.1365-2427.2002.00829.x

    Article  Google Scholar 

  15. Figuerola J, Green AJ, Michot TC (2005) Invertebrate eggs can fly: evidence of waterfowl-mediated gene flow in aquatic invertebrates. Am Nat 165:274–280. https://doi.org/10.1086/427092

    Article  PubMed  Google Scholar 

  16. Frisch D, Green A, Figuerola J (2007) High dispersal capacity of a broad spectrum of aquatic invertebrates via waterbirds. Aquat Sci 69:568–574. https://doi.org/10.1007/s00027-007-0915-0

    Article  Google Scholar 

  17. Frisch D, Cottenie K, Badosa A, Green AJ (2012) Strong spatial influence on colonization rates in a pioneer zooplankton metacommunity. PLoS One 7:e40205. https://doi.org/10.1371/journal.pone.0040205

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  18. Hereford J (2009) A quantitative survey of local adaptation and fitness trade-offs. Am Nat 173:579–588. https://doi.org/10.1086/597611

    Article  PubMed  Google Scholar 

  19. Jenkins DG, Buikema AL (1998) Do similar communities develop in similar sites? A test with zooplankton structure and function. Ecol Monogr 68:421–443. https://doi.org/10.1890/0012-9615(1998)068%5b0421:DSCDIS%5d2.0.CO;2

    Article  Google Scholar 

  20. Jersabek CD, Weithoff G, Weisse T (2011) Cephalodella acidophila n. sp. (Monogononta: Notommatidae), a new rotifer species from highly acidic mining lakes. Zootaxa 2939:50–58

    Article  Google Scholar 

  21. Kamjunke N, Gaedke U, Tittel J, Weithoff G, Bell EM (2004) Strong vertical differences in the plankton composition of an extremely acidic lake. Arch Hydrobiol 161:289–306. https://doi.org/10.1127/0003-9136/2004/0161-0289

    Article  Google Scholar 

  22. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241. https://doi.org/10.1111/j.1461-0248.2004.00684.x

    Article  Google Scholar 

  23. Kwong YTJ, Lawrence JR (1998) Acid generation and metal immobilization in the vicinity of a naturally acidic lake in Central Yukon Territory, Canada. In: Geller W, Klapper H, Salomons W (eds) Acidic mine drainage. Springer, Berlin, pp 65–86

    Google Scholar 

  24. Leimuu R, Fischer M (2008) A meta-analysis of local adaptation in plants. PLoS One 3:e4010. https://doi.org/10.1371/journal.pone.0004010

    CAS  Article  Google Scholar 

  25. Linhart YB, Grant MC (1996) Evolutionary significance of local genetic differentiation in plants. Annu Rev Ecol Syst 27:237–277. https://doi.org/10.1146/annurev.ecolsys.27.1.237

    Article  Google Scholar 

  26. Low-Décarie E, Fussmann GF, Dumbrell AJ, Bell G (2016) Communities that thrive in extreme conditions captured from a freshwater lake. Biol Lett 12:20160562

    Article  Google Scholar 

  27. Méndez-Garcia C, Peláez AI, Mesa V, Sánchez J, Golyshina OV, Ferrer M (2015) Microbial diversity and metabolic networks in acid mine drainage habitats. Front Microbiol 6:475. https://doi.org/10.3389/fmicb.2015.00475

    Article  PubMed  PubMed Central  Google Scholar 

  28. Mesa V, Gallego JLR, González-Gil R, Lauga B, Sánchez J, Méndez-Garcia C, Peláez AI (2017) Bacterial, archaeal, and eukaryotic diversity across microhabitats in an acid mine drainage. Front Microbiol 8:1756. https://doi.org/10.3389/fmicb.2017.01756

    Article  PubMed  PubMed Central  Google Scholar 

  29. Moser M, Weisse T (2011) The most acidified Austrian lake in comparison to a neutralized mining lake. Limnologica 41:303–315. https://doi.org/10.1016/j.limno.2011.01.002

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. Nixdorf B, Lessmann D, Deneke R (2005) Mining lakes in a disturbed landscape: application of the EC Water Framework Directive and future management strategies. Ecol Eng 24:67–73. https://doi.org/10.1016/j.ecoleng.2004.12.008

    Article  Google Scholar 

  31. Packroff G, Woelfl S (2000) A review on the occurrence and taxonomy of heterotrophic protists in extreme acidic environments of pH values ≤ 3. Hydrobiologia 433:153–156. https://doi.org/10.1023/A:1004039309694

    Article  Google Scholar 

  32. Pedrozo F, Kelly L, Diaz M, Temporetti P, Baffico G, Kringel R, Friese K, Mages M, Geller W, Woelfl S (2001) First results on the water chemistry, algae and trophic status of an Andean acidic lake system of volcanic origin in Patagonia (Lake Caviahue). Hydrobiologia 452:129–137. https://doi.org/10.1023/A:1011984212798

    CAS  Article  Google Scholar 

  33. Savolainen O, Pyhäjärvi T, Knürr T (2007) Gene flow and local adaptation in trees. Annu Rev Ecol Evol Syst 38:595–619. https://doi.org/10.1146/annurev.ecolsys.38.091206.095646

    Article  Google Scholar 

  34. Schmidtke A, Bell EM, Weithoff G (2006) Potential grazing impact of the mixotrophic flagellate Ochromonas sp. (Chrysophyceae) on bacteria in an extremely acidic lake. J Plankton Res 28:991–1001. https://doi.org/10.1093/plankt/fbl034

    CAS  Article  Google Scholar 

  35. Slatkin M (1985) Gene flow in natural populations. Annu Rev Ecol Syst 16:393–430. https://doi.org/10.1146/annurev.es.16.110185.002141

    Article  Google Scholar 

  36. Spijkerman E (2005) Inorganic carbon acquisition by Chlamydomonas acidophila across a pH range. Can J Botany 83:872–878. https://doi.org/10.1139/b05-073

    CAS  Article  Google Scholar 

  37. Tittel J, Bissinger V, Gaedke U, Kamjunke N (2005) Inorganic carbon limitation and mixotrophic growth in Chlamydomonas from an acidic mining lake. Protist 156:63–75. https://doi.org/10.1016/j.protis.2004.09.001

    CAS  Article  PubMed  Google Scholar 

  38. Vanschoenwinkel B, Gielen S, Seaman M, Brendonck L (2009) Wind mediated dispersal of freshwater invertebrates in a rock pool metacommunity: differences in dispersal capacities and modes. Hydrobiologia 635:363–372. https://doi.org/10.1007/s10750-009-9929-z

    Article  Google Scholar 

  39. Wacker A, Weithoff G (2009) Carbon assimilation mode in mixotrophs and the fatty acid composition of their consumers. Freshw Biol 54:2189–2199. https://doi.org/10.1111/j.1365-2427.2009.02251.x

    CAS  Article  Google Scholar 

  40. Weisse T, Berendonk T, Kamjunke N, Moser M, Scheffel U, Stadler P, Weithoff G (2011) Significant habitat effects influence protist fitness: evidence for local adaptation from acidic mining lakes. Ecosphere 2:134. https://doi.org/10.1890/es11-00157.1

    Article  Google Scholar 

  41. Weisse T, Laufenstein N, Weithoff G (2013a) Multiple environmental stressors confine the ecological niche of the rotifer Cephalodella acidophila. Freshw Biol 58:1008–1015. https://doi.org/10.1111/fwb.12104

    Article  PubMed  PubMed Central  Google Scholar 

  42. Weisse T, Moser M, Scheffel U, Stadler P, Berendonk T, Weithoff G, Berger H (2013b) Systematics and species-specific response to pH of Oxytricha acidotolerans sp. nov. and Urosomoida sp. (Ciliophora, Hypotricha) from acid mining lakes. Eur J Protistol 49:255–271. https://doi.org/10.1016/j.ejop.2012.08.001

    Article  PubMed  PubMed Central  Google Scholar 

  43. Weithoff G (2004) Vertical niche separation of two consumers (Rotatoria) in an extreme habitat. Oecologia 139:594–603. https://doi.org/10.1007/s00442-004-1545-z

    Article  PubMed  Google Scholar 

  44. Weithoff G (2005) On the ecology of the rotifer Cephalodella hoodi from an extremely acidic lake. Freshw Biol 50:1464–1473. https://doi.org/10.1111/j.1365-2427.2005.01423.x

    Article  Google Scholar 

  45. Weithoff G (2007) Dietary restriction in two rotifer species: the effect of the length of food deprivation on life span and reproduction. Oecologia 153:303–308. https://doi.org/10.1007/s00442-007-0739-6

    Article  PubMed  Google Scholar 

  46. Weithoff G, Wacker A (2007) The mode of nutrition of mixotrophic flagellates determines the food quality for their consumers. Funct Ecol 21:1092–1098. https://doi.org/10.1111/j.1365-2435.2007.01333.x

    Article  Google Scholar 

  47. Weithoff G, Moser M, Kamjunke N, Gaedke U, Weisse T (2010) Lake morphometry and wind exposure may shape the plankton community structure in acidic mining lakes. Limnologica 40:161–166

    CAS  Article  Google Scholar 

  48. Yin X, Niu C (2008) Effect of pH on survival, reproduction, egg viability and growth rate of five closely related rotifer species. Aquat Ecol 42:607–616. https://doi.org/10.1007/s10452-007-9136-9

    CAS  Article  Google Scholar 

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Acknowledgements

We greatly acknowledge the excellent support of Christina Schirmer and Michael Moser in the laboratory. Financial support was provided by the Austrian Science Fund (FWF), project P20118 (TW).

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GW and TW conceived the study. GW, TW and CN designed the experiments. GW, CN and JS performed the experiments. GW analyzed the data. GW wrote and TW and CN commented on the manuscript.

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Correspondence to Guntram Weithoff.

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Weithoff, G., Neumann, C., Seiferth, J. et al. Living on the edge: reproduction, dispersal potential, maternal effects and local adaptation in aquatic, extremophilic invertebrates. Aquat Sci 81, 40 (2019). https://doi.org/10.1007/s00027-019-0638-z

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Keywords

  • Common garden experiments
  • Extreme habitats
  • Extremophiles
  • Rotifers
  • Zooplankton