Abstract
Daphnia, keystone herbivores in lakes, routinely produce immediately hatching eggs; additionally, they also produce resting eggs enveloped by an ephippial case, a thickened carapace that allows population survival under harsh environmental conditions. To examine differences in ephippial morphology between Daphnia species in different subgenera, we conducted microscopic observations and genetic analyses based on the mitochondrial 12S rRNA gene in ephippia from surface sediment in Lake Biwa, Japan. The lengths and heights of ephippia identified as Daphnia galeata Sars (Hyalodaphnia) were less than 0.82 and 0.50 mm, respectively, whereas those of Daphnia pulicaria Forbes (Daphnia) were greater than 0.87 and 0.53 mm, respectively, with the ephippial lengths of the two species differing significantly. The results indicate that D. galeata and D. pulicaria inhabiting Lake Biwa can be distinguished based on ephippium size, with a boundary ephippium length of approximately 0.86 mm. In concordance with this inference, historical data indicated that the length of ephippia recovered from sediment cores did not exceed 0.86 mm prior to the 1980s when D. galeata was the predominant species; however, it exceeded the threshold after 2000, coinciding with the coexistence of D. galeata and D. pulicaria.
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References
Alric B, Möst M, Domaizon I et al (2016) Local human pressures influence gene flow in a hybridizing Daphnia species complex. J Evol Biol 29:720–735. https://doi.org/10.1111/jeb.12820
Appleby PG (2001) Chronostratigraphic techniques in recent sediments. In: Last WM, Smol JP (eds) Basin analysis, coring, and chronological techniques. Tracking environmental change using lake sediments, vol 1. Kluwer Academic Publishers, Dordrecht, pp 171–203. https://doi.org/10.1007/0-306-47669-x_9
Appleby PG, Oldfield F (1978) The calculation of lead-210 dates assuming a constant rate of supply of unsupported 210Pb to the sediment. CATENA 5:1–8. https://doi.org/10.1016/S0341-8162(78)80002-2
Benzie JAH (2005) Cladocera: the genus Daphnia (including Daphniopsis). Backhuys, Leiden
Billiones R, Brehm M, Klee J, Schwenk K (2004) Genetic identification of Hyalodaphnia species and interspecific hybrids. Hydrobiologia 526:43–53
Brede N, Sandrock C, Straile D, Spaak P, Jankowski T, Streit B, Schwenk K (2009) The impact of human-made ecological changes on the genetic architecture of Daphnia species. PNAS 106:4758–4763
Caceres CE (2012) Eggs interspecific variation in the abundance, production, and emergence of Daphnia diapausing eggs. Ecology 79:1699–1710
Carpenter SR, Kitchell JF (1993) The trophic cascade in lakes. Cambridge University Press, Cambridge
Černý M, Hebert PDN (1999) Intercontinental allozyme differentiation among four holarctic Daphnia species. Limnol Oceanogr 44:1381–1387
Colbourne JK, Hebert PD (1996) The systematics of North American Daphnia (Crustacea: Anomopoda): a molecular phylogenetic approach. Philos Trans R Soc B 351:349–360
Colbourne JK, Crease TJ, Weider L, Hebert PD, Duferesne F, Hobaek A (1998) Phylogenetics and evolution of a circumarctic species complex (Cladocera: Daphnia pulex). Biol J Linn Soc Lond 65:347–365
Crease TJ (1999) The complete sequence of the mitochondrial genome of Daphnia pulex (Cladocera: Crustacea). Gene 233:89–99
Crease TJ, Omilian AR, Costanzo KS, Taylor DJ (2012) Transcontinental phylogeography of the Daphnia pulex species complex. PLoS ONE 7:e46620
Cristescu ME, Constantin A, Bock DG, Caceres CE, Crease TJ (2012) Speciation with gene flow and the genetics of habitat transitions. Mol Ecol 21:1411–1422
Decaestecker E, Lefever C, DeMeester L, Ebert D (2004) Haunted by the past: evidence for dormant stage banks of microparasites and epibionts of Daphnia. Limnol Oceanogr 49:1355–1364
Faustová M, Petrusek A, Černý M (2004) Status of Daphnia resting egg banks in Bohemian forest lakes affected by acidification. Hydrobiologia 526:23–31
Frisch D, Morton PK, Chowdhury PR, Culver BW, Colbourne JK, Weider LJ, Jeyasingh PD (2014) A millennial-scale chronicle of evolutionary responses to cultural eutrophication in Daphnia. Ecol Lett 17:360–368. https://doi.org/10.1111/ele.12237
Geerts AN, Vanoverbeke J, Vanschoenwinkel B, Doorslaer WV, Feuchtmayr H, Atkinson D, Moss B, Davidson TA, Sayer CD, De Meester L (2015) Rapid evolution of thermal tolerance in the water flea Daphnia. Nat Clim Change 5:665–668. https://doi.org/10.1038/nclimate2628
Gieβler S, Englbrecht CC (2009) Dynamic reticulate evolution in a Daphnia multispecies complex. J Exp Zool 311:530–548
Hairston NG, Van Brunt RA, Kearns CM, Engstrom DR (1995) Age and survivorship of diapausing eggs in a sediment egg bank. Ecology 76:1706–1711. https://doi.org/10.2307/1940704
Hairston NG Jr, Lampert W, Cáceres CE, Holtmeier CL, Weider LJ, Gaedke U, Fischer JM, Fox JA, Post DM (1999) Rapid evolution revealed by dormant eggs. Nature 401:446
Hampton SE, McGowan S, Ozersky T et al (2018) Recent ecological change in ancient lakes. Limnol Oceanogr 63:2277–2304. https://doi.org/10.1002/lno.10938
Hamrová E, Goliáš V, Petrusek A (2010) Identifying century-old long-spined Daphnia: species replacement in a mountain lake characterised by paleogenetic methods. Hydrobiologia 643:97–106. https://doi.org/10.1007/s10750-010-0127-9
Hsieh CH, Sakai Y, Ban S et al (2011) Eutrophication and warming effects on long-term variation of zooplankton in Lake Biwa. Biogeosci Discuss 8:593–629. https://doi.org/10.5194/bgd-8-593-2011
Hyodo F, Kuwae M, Sasaki N, Hayashi R, Makino W, Kusaka S, Tsugeki KN, Ishida S, Ohtsuki H, Omoto K, Urabe J (2017) Variations in lignin-derived phenols in sediments of Japanese lakes over the last century and their relation to watershed vegetation. Org Geochem 103:125–135. https://doi.org/10.1016/j.orggeochem.2016.11.001
Ishida S, Ohtsuki H, Awano T, Tsugeki NK, Makino W, Suyama Y, Urabe J (2012) DNA extraction and amplification methods for ephippial cases of Daphnia resting eggs in lake sediments: a novel approach for reconstructing zooplankton population structure from the past. Limnology 13:261–267
Jankowski T, Straile D (2003) A comparison of egg-bank and long-term plankton dynamics of two Daphnia Species, D. hyalina and D. galeata: potentials and limits of reconstruction. Limnol Oceanogr 48:1948–1955
Juračka PJ, Kořínek V, Petrusek A (2010) A new Central European species of the Daphnia curvirostris complex, Daphnia hrbaceki sp. nov. (Cladocera, Anomopoda, Daphniidae). Zootaxa 2718:1–22
Kaya M, Erdoğan S (2014) Morphological examination of the resting egg structure of 3 cladoceran species [Ceriodaphnia quadrangula (OF Müller, 1785), Daphnia longispina (OF Müller, 1776), and D. magna Straus, 1820]. Turk Zool Derg 38:131–135
Lehman N, Pfrender ME, Morin PA, Crease TJ, Lynch M (1995) A hierarchical molecular phylogeny within the genus Daphnia. Mol Phylo Evol 4:395–407
Liu X, Dur G, Ban S, Sakai Y, Ohmae S, Morita T (2020) Planktivorous fish predation masks anthropogenic disturbances on decadal trends in zooplankton biomass and body size structure in Lake Biwa, Japan. Limnol Oceanogr 65:667–682
Lorenzen CJ (1967) Determination of chlorophyll and pheopigments spectrophotometric equation. Limnol Oceanogr 12:343–346
Marková S, Černý M, Rees D, Stuchlík E (2006) Are they still viable? Physical conditions and abundance of Daphnia pulicaria resting eggs in sediment cores from lakes in the Tatra Mountains. Biologia (Bratisl) 61:S135–S146. https://doi.org/10.2478/s11756-006-0126-5
McCauley E, Nisbet RM, Murdoch WW, de Roos AM, Gurney WSC (1999) Large-amplitude cycles of Daphnia and its algal prey in enriched environments. Nature 402:653–656
Miura T, Cai QH (1990) Annual and seasonal occurrences of the zooplankters observed in the North Basin of Lake Biwa from 1965 to 1979. Lake Biwa Research Institute, Otsu
Möst M, Oexle S, Marková S, Aidukaite D, Baumgartner L, Stich HB, Wessels M, Martin-Creuzburg D, Spaak P (2015) Population genetic dynamics of an invasion reconstructed from the sediment egg bank. Mol Ecol 24:4074–4093
Ohtsuki H, Awano T, Tsugeki NK, Ishida S, Oda H, Makino W, Urabe J (2015) Historical changes in the ecosystem condition of a small mountain lake over the past 60 years as revealed by plankton remains and Daphnia ephippial carapaces stored in lake sediments. PLoS ONE 10:e0119767
Petrusek A, Černý M, Mergeay J, Schwenk K (2007) Daphnia in the Tatra Mountain lakes: multiple colonisation and hidden species diversity revealed by molecular markers. Fundam Appl Limnol 169:279–291. https://doi.org/10.1127/1863-9135/2007/0169-0279
Pinceel T, Brendonck L, Vanschoenwinkel B (2016) Propagule size and shape may promote local wind dispersal in freshwater zooplankton—a wind tunnel experiment. Limnol Oceanogr 61:122–131
Rother A, Pitsch M, Hülsmann S (2010) The importance of hatching from resting eggs for population dynamics and genetic composition of Daphnia in a deep reservoir. Freshw Biol 55:2319–2331. https://doi.org/10.1111/j.1365-2427.2010.02441.x
Skov T, Buchaca T, Amsinck SL, Landkildehus F, Odgaard BV, Azevedo J, Gonçalves V, Raposeiro PM, Andersen TJ, Jeppesen E (2010) Using invertebrate remains and pigments in the sediment to infer changes in trophic structure after fish introduction in Lake Fogo: a crater lake in the Azores. Hydrobiologia 654:13–25
Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci USA 101:11030–11035
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
Thompson J, Higgins D, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Tokishita S, Shibuya H, Kobayashi T, Sakamoto M, Ha J-Y, Yokobori S, Yamagata H, Hanazato T (2017) Diversification of mitochondrial genome of Daphnia galeata (Cladocera, Crustacea): comparison with phylogenetic consideration of the complete sequences of clones isolated from five lakes in Japan. Gene 611:38–46
Tsugeki NK, Oda H, Urabe J (2003) Fluctuation of zooplankton community in Lake Biwa during the 20th century: a paleolimnological analysis. Limnology 4:101–107
Tsugeki NK, Ishida S, Urabe J (2009) Sedimentary records of reduction in resting egg production of Daphnia galeata in Lake Biwa during the 20th century: a possible effect of winter warming. J Paleolimnol 42:155–165
Urabe J, Ishida S, Nishimoto M, Weider LJ (2003) Daphnia pulicaria, a zooplankton species that suddenly appeared in 1999 in the offshore zone of Lake Biwa. Limnology 4:0035–0041
Vandekerkhove J, Declerck S, Vanhove M, Brendonck L, Jeppesen E, Porcune JMC, DeMeester L (2004) Use of ephippial morphology to assess richness of anomopods: potentials and pitfalls. J Limnol 63:75–84
Weider LJ, Hobaek A, Colbourne JK, Crease TJ, Dufresne F, Hebert PD (1999) Holarctic phylogeography of an asexual species complex I. Mitochondrial DNA variation in arctic Daphnia. Evolution 53:777–792
Yoshida T, Kagami M, Bahadur Gurung T, Urabe J (2001) Seasonal succession of zooplankton in the north basin of Lake Biwa. Aquat Ecol 35:19–29
Acknowledgements
We are grateful to H. Kudoh, S. Nakano, H. Iwata, M. Ochiai, S. Goda, T. Akatsuka, M. Shoji, M. Sakamoto, S. Kawabuchi, I. Hashimoto, and G. Mitamura for their assistance with laboratory analysis and field sampling. This work was supported by a Grant-in-Aid for Scientific Research C (No. 17K00528 to NT) from the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan, and also supported by the Kurita Water and Environment Foundation (Grant No.17B050 to MH). The Joint Usage/Research Grant of Center for Ecological Research (2017–2019 jurc-cer), Kyoto University and a project on Joint Usage/Research Center–Leading Academia in Marine and Environment Pollution Research (LaMer) of the Center for Marine Environmental Studies, Ehime University, also supported this study.
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Tsugeki, N.K., Honjo, M.N. & Kuwae, M. Interspecific variation in ephippial size between Daphnia galeata and D. pulicaria in Lake Biwa, Japan. Limnology 22, 197–207 (2021). https://doi.org/10.1007/s10201-020-00646-8
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DOI: https://doi.org/10.1007/s10201-020-00646-8