Abstract
Invasive species pose serious threats to global biodiversity, prompting studies to identify factors underlying invasion and establishment success. However, it's difficult to discern these factors due to the absence of survey data since the initial invasion, because introduced species often remain unnoticed until their population becomes large enough. Here, we investigated the establishment process of the alien zooplankton, Daphnia pulicaria, in the past 30 years using sedimentary archives at Lake Biwa. We performed genetic analysis on mitochondrial DNA sequences of the control region and ND5 gene of ephippia in sediments, as well as present females from water samples. Furthermore, we investigated the relationships between the abundance of D. pulicaria and its major predator fish, Ayu, based on the catch data, as well as its competitor, Daphnia galeata whose abundance was inferred from claw remains. Our analyses showed the studied mitochondrial sequences were identical between all samples. The abundance of D. pulicaria was not correlated with that of a competitor but was negatively with that of a predator. These findings suggest the successful establishment of D. pulicaria was primarily influenced by reduced predation pressure, with a limited impact from competitive interactions and potential hindrance for adaptation caused by loss of genetic variation.
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References
Allendorf, F. W. & L. L. Lundquist, 2003. Introduction: population biology, evolution, and control of invasive species. Conservation Biology 17: 24–30. https://doi.org/10.1046/j.1523-1739.2003.02365.x.
Appleby, P. G. & F. Oldfield, 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.
Appleby, P. G., 2001. Chronostratigraphic techniques in recent sediments. Tracking Environmental Change Using Lake Sediments. https://doi.org/10.1007/0-306-47669-X_9.
Benzie, J. A. H., 2005. The genus Daphnia (including Daphniopsis). Guides to the identification of the microinvertebrates of the continental waters of the world, volume 21. Kenobi Productions. Ghent & Backhuys Publishers, Leiden, Netherlands. pp. 376.
Brede, N., C. Sandrock, D. Straile, P. Spaak, T. Jankowski, B. Streit & K. Schwenk, 2009. The impact of human-made ecological changes on the genetic architecture of Daphnia species. Proceedings of the National Academy of Sciences 106: 4758–4763. https://doi.org/10.1073/pnas.0807187106.
Cáceres, C. E., A. J. Tessier, C. E. Cdceres & A. J. Tessier, 2004. To sink or swim: variable diapause strategies among Daphnia species. Limnology and Oceanography 49: 1333–1340. https://doi.org/10.4319/lo.2004.49.4_part_2.1333.
Colbourne, J. K., T. J. Crease, L. J. Weider, P. D. N. Hebert, F. Dufresne & A. Hobæek, 1998. Phylogenetics and evolution of a circumarctic species complex (Cladocera: Daphnia pulex). Biological Journal of the Linnean Society 65: 347–365. https://doi.org/10.1111/j.1095-8312.1998.tb01146.x.
Crease, T. J., A. R. Omilian, K. S. Costanzo & D. J. Taylor, 2012. Transcontinental phylogeography of the Daphnia pulex species complex. PLoS ONE. https://doi.org/10.1371/journal.pone.0046620.
Černý, M. & J. Bytel, 1991. Density and size distribution of Daphnia populations at different fish predation levels. Hydrobiologia 225: 199–208. https://doi.org/10.1007/BF00028398.
De Meester, L., A. Gómez, B. Okamura & K. Schwenk, 2002. The Monopolization Hypothesis and the dispersal-gene flow paradox in aquatic organisms. Acta Oecologica 23: 121–135. https://doi.org/10.1016/S1146-609X(02)01145-1.
Dlugosch, K. M. & I. M. Parker, 2008. Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Molecular Ecology 17: 431–449. https://doi.org/10.1111/j.1365-294X.2007.03538.x.
Drake, J. M., 2006. Heterosis, the catapult effect and establishment success of a colonizing bird. Biology Letters 2: 304–307. https://doi.org/10.1098/rsbl.2006.0459.
Dudycha, J. L., 2004. Mortality dynamics of Daphnia in contrasting habitats and their role in ecological divergence. Freshwater Biology 49: 505–514. https://doi.org/10.1111/j.1365-2427.2004.01201.x.
Early, R., B. A. Bradley, J. S. Dukes, J. J. Lawler, J. D. Olden, D. M. Blumenthal, P. Gonzalez, E. D. Grosholz, I. Ibañez, L. P. Miller, C. J. B. Sorte & A. J. Tatem, 2016. Global threats from invasive alien species in the twenty-first century and national response capacities. Nature Communications 7: 12485. https://doi.org/10.1038/ncomms12485.
Fatsi, P. S. K., S. Hashem, A. Kodama, E. K. Appiah, H. Saito & K. Kawai, 2020. Population genetics and taxonomic signatures of wild Tilapia in Japan based on mitochondrial DNA control region analysis. Hydrobiologia 847: 1491–1504. https://doi.org/10.1007/s10750-020-04203-3.
Fujioka, Y., 2020. Long-term changes in the Lake Biwa fisheries: changes in the catches of fishes over a century in Lake Biwa. In Kawanabe, H., M. Nishino & M. Maehata (eds), Lake Biwa: interactions between nature and people Springer, Berlin: 453–460.
Gouy, M., S. Guindon & O. Gascuel, 2010. Sea view version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution 27: 221–224. https://doi.org/10.1093/molbev/msp259.
Hairston, N. G., 1996. Zooplankton egg banks as biotic reservoirs in changing environments. Limnology and Oceanography 41: 1087–1092. https://doi.org/10.4319/lo.1996.41.5.1087.
Hairston, N. G., R. A. Van Brunt, C. M. Kearns & D. R. Engstrom, 1995. Age and survivorship of diapausing eggs in a sediment egg bank. Ecology 76: 1706–1711. https://doi.org/10.2307/1940704.
Hampton, S. E., S. McGowan, T. Ozersky, S. G. P. Virdis, T. T. Vu, T. L. Spanbauer, B. M. Kraemer, G. Swann, A. W. Mackay, S. M. Powers, M. F. Meyer, S. G. Labou, C. M. O’Reilly, M. DiCarlo, A. W. E. Galloway & S. C. Fritz, 2018. Recent ecological change in ancient lakes. Limnology and Oceanography 63: 2277–2304. https://doi.org/10.1002/lno.10938.
Hann, B. J., 1989. Methods in quaternary ecology #6. Cladocera. Geoscience Canada. 16: 17–26.
Heger, T., A. T. Pahl, Z. Botta-Dukát, et al., 2013. Conceptual frameworks and methods for advancing invasion ecology. AMBIO 42: 527–540. https://doi.org/10.1007/s13280-012-0379-x.
Hsieh, C. H., Y. Sakai, S. Ban, K. Ishikawa, T. Ishikawa, S. Ichise, N. Yamamura & M. Kumagai, 2011. Eutrophication and warming effects on long-term variation of zooplankton in Lake Biwa. Biogeosciences Discussions 8: 593–629. https://doi.org/10.5194/bg-8-1383-2011.
Hyodo, F., N. Tsugeki, J. Azuma, J. Urabe, M. Nakanishi & E. Wada, 2008. Changes in stable isotopes, lignin-derived phenols, and fossil pigments in sediments of Lake Biwa, Japan: implications for anthropogenic effects over the last 100 years. Science of the Total Environment 3: 139–147. https://doi.org/10.1016/j.scitotenv.2008.05.010.
Ishida, S., H. Ohtsuki, T. Awano, N. K. Tsugeki, W. Makino, Y. Suyama & J. Urabe, 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. https://doi.org/10.1007/s10201-012-0380-x.
ISSG, 2000. IUCN Guidelines for the prevention of biodiversity loss caused by alien invasive species.
Kadota, S., 1984. Animal microfossils. In Horie, S. (ed), Lake Biwa Junk, Netherlands: 545–555.
Kawabata, K., 2020. Fish predation on pelagic zooplankton. In Kawanabe, H., M. Nishino & M. Maehata (eds), Interactions between nature and people Springer, New York: 327–329.
Keane, R. M. & M. J. Crawley, 2002. Exotic plant invasions and the enemy release hypothesis. Trends in Ecology and Evolution 17: 164–170. https://doi.org/10.1016/S0169-5347(02)02499-0.
Korponai, J., E. K. Magyari, K. Buczkó, S. Iepure, T. Namiotko, D. Czakó, C. Kövér & M. Braun, 2011. Cladocera response to Late Glacial to Early Holocene climate change in a South Carpathian mountain lake. Hydrobiologia 676: 223–235. https://doi.org/10.1007/s10750-011-0881-3.
Lampert, W., 1993. Ultimate causes of diel vertical migration of zooplankton: new evidence for the predator-avoidance hypothesis. Arch Hydrobiol Beih Ergeb Limnolology 39: 79–88.
Lehman, N., M. E. Pfrender, P. A. Morin, T. J. Crease & M. Lynch, 1995. A hierarchical molecular phylogeny within the genus Daphnia. Molecular Phylogenetics and Evolution 4: 395–407. https://doi.org/10.1006/mpev.1995.1037.
Liu, X., G. Dur, S. Ban, Y. Sakai, S. Ohmae & T. Morita, 2020. Planktivorous fish predation masks anthropogenic disturbances on decadal trends in zooplankton biomass and body size structure in Lake Biwa, Japan. Limnology and Oceanography 65: 667–682. https://doi.org/10.1002/lno.11336.
Liu, X., G. Dur, S. Ban, Y. Sakai, S. Ohmae & T. Morita, 2021. Quasi-decadal periodicities in growth and production of the copepod Eodiaptomus japonicus in Lake Biwa, Japan, related to the Arctic Oscillation. Limnology and Oceanography. https://doi.org/10.1002/lno.11918.
Marini, M., I. R. Pedrosa-Gerasmio, M. D. Santos, T. Shibuno, A. Daryani, M. R. R. Romana-Eguia & A. Wibowo, 2021. Genetic diversity, population structure and demographic history of the tropical eel Anguilla bicolor pacifica in Southeast Asia using mitochondrial DNA control region sequences. Global Ecology and Conservation 26: e01493. https://doi.org/10.1016/j.gecco.2021.e01493.
Maron, J. L. & M. Vilà, 2001. When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95: 361–373. https://doi.org/10.1034/j.1600-0706.2001.950301.x.
Mergeay, J., D. Verschuren & L. De Meester, 2006. Invasion of an asexual American water flea clone throughout Africa and rapid displacement of a native sibling species. Proceedings of the Royal Society b: Biological Sciences 273: 2839–2844. https://doi.org/10.1098/rspb.2006.3661.
Monchamp, M. E., I. Enache, P. Turko, F. Pomati, G. Rîşnoveanu & P. Spaak, 2017. Sedimentary and egg-bank DNA from 3 European lakes reveal concurrent changes in the composition and diversity of cyanobacterial and Daphnia communities. Hydrobiologia 800: 155–172. https://doi.org/10.1007/s10750-017-3247-7.
Nakane, K., X. Liu, H. Doi, G. Dur, M. Kuwae, S. Ban & N. Tsugeki, 2023. Sedimentary DNA can reveal the past population dynamics of a pelagic copepod. Freshwater Biology 68: 1799–2026. https://doi.org/10.1111/fwb.14096.
Ohtsuki, H., T. Awano, N. K. Tsugeki, S. Ishida, H. Oda, W. Makino & J. Urabe, 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: 1–19. https://doi.org/10.1371/journal.pone.0119767.
Otake, Y., H. Innan, H. Ohtsuki, J. Urabe, K. Yamada & T. Yoshida, 2022. Population genetic dynamics during colonisation and establishment of an obligate parthenogenetic Daphnia pulex population in a small lake of a continental archipelago. Freshwater Biology. https://doi.org/10.1111/fwb.13951.
Paradis, E., 2010. Pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26: 419–420. https://doi.org/10.1093/bioinformatics/btp696.
Paradis, E. & K. Schliep, 2019. Ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35: 526–528. https://doi.org/10.1093/bioinformatics/bty633.
Richardson, D. M., P. Pyšek & J. T. Carlton, 2011. A compendium of essential concepts and terminology in invasion ecology. Fifty Years of Invasion Ecology: The Legacy of Charles Elton. https://doi.org/10.1002/9781444329988.ch30.
Sakai, A. K., F. W. Allendorf, J. S. Holt, M. Lodge, J. Molofsky, K. A. With, R. J. Cabin, J. E. Cohen, C. Norman, D. E. Mccauley, P. O. Neil, M. Parker, J. N. Thompson & S. G. Weller, 2001. The population biology of invasive species. Annual Review of Ecology and Systematics 32: 305–332. https://doi.org/10.1146/annurev.ecolsys.32.081501.114037.
Schrieber, K. & S. Lachmuth, 2017. The genetic paradox of invasions revisited: the potential role of inbreeding × environment interactions in invasion success. Biological Reviews 92: 939–952. https://doi.org/10.1111/brv.12263.
Sinclair, J. S. & S. E. Arnott, 2017. Relative importance of colonist quantity, quality, and arrival frequency to the extinction of two zooplankton species. Oecologia 184: 441–452. https://doi.org/10.1007/s00442-017-3874-8.
Ślusarczyk, M., 1995. Predator-induced diapause in Daphnia. Ecology 76: 1008–1013. https://doi.org/10.2307/1939364.
Slusarczyk, M., 2001. Food threshold for diapause in Daphnia. Ecology 82: 1089–1096. https://doi.org/10.1890/0012-9658(2001)082[1089:FTFDID]2.0.CO;2.
Smith, A. S., K. Acharya & J. Jack, 2009. Overcrowding, food and phosphorus limitation effects on ephipphia production and population dynamics in the invasive species Daphnia lumholtzi. Hydrobiologia 618: 47–56. https://doi.org/10.1007/s10750-008-9546-2.
So, M., H. Ohtsuki, W. Makino, S. Ishida, H. Kumagai, K. G. Yamaki & J. Urabe, 2015. Invasion and molecular evolution of Daphnia pulex in Japan. Limnology and Oceanography 60: 1129–1138. https://doi.org/10.1002/lno.10087.
Spielman, D., B. W. Brook, D. A. Briscoe & R. Frankham, 2004. Does inbreeding and loss of genetic diversity decrease disease resistance? Conservation Genetics 5: 439–448. https://doi.org/10.1023/B:COGE.0000041030.76598.cd.
Stecher, G., K. Tamura & S. Kumar, 2020. Molecular Evolutionary Genetics Analysis (MEGA) for macOS. Molecular Biology and Evolution 37: 1237–1239. https://doi.org/10.1093/molbev/msz312.
Straughan, D. J. & N. Lehman, 2000. Genetic differentiation among Oregon lake populations of the Daphnia pulex species complex. Journal of Heredity 91: 8–17. https://doi.org/10.1093/jhered/91.1.8.
Tanaka, S., 1992. Morphology and variation of Daphnia galeata Sars in Japan from Lake Biwa and Lake Kizaki in Japan. Japanese Journal of Limnology 53: 47–54. https://doi.org/10.3739/rikusui.53.47.
Tsugeki, N. K., S. Ishida & J. Urabe, 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. https://doi.org/10.1007/s10933-008-9268-5.
Tsugeki, N., H. Oda & J. Urabe, 2003. Fluctuation of the zooplankton community in Lake Biwa during the 20th century : a paleolimnological analysis. Limnology 4: 101–107. https://doi.org/10.1007/s10201-003-0097-y.
Tsugeki, N. K., J. Urabe, Y. Hayami, M. Kuwae & M. Nakanishi, 2010. Phytoplankton dynamics in Lake Biwa during the 20th century: complex responses to climate variation and changes in nutrient status. Journal of Paleolimnology 44: 69–83. https://doi.org/10.1007/s10933-009-9386-8.
Tsugeki, N., M. N. Honjo & M. Kuwae, 2021. Interspecific variation in ephippial size between Daphnia galeata and D. pulicaria in Lake Biwa. Japan. Limnology 22: 197–207. https://doi.org/10.1007/s10201-020-00646-8.
Tsugeki, N., K. Nakane, H. Doi, N. Ochi & M. Kuwae, 2022. Reconstruction of 100-year dynamics in Daphnia spawning activity revealed by sedimentary DNA. Scientific Reports 12: 1741. https://doi.org/10.1038/s41598-021-03899-0.
Urabe, J., S. Ishida, M. Nishimoto & L. J. Weider, 2003. Daphnia pulicaria, a zooplankton species that suddenly appeared in 1999 in the offshore zone of Lake Biwa. Limnology 4: 35–41. https://doi.org/10.1007/s10201-002-0087-5.
Vanni, M. J., C. Luecke, J. F. Kitchell, Y. Allen, J. Temte & J. J. Magnuson, 1990. Effects on lower trophic levels of massive fish mortality. Nature 344: 333–335. https://doi.org/10.1038/344333a0.
Verschuren, D. & L. F. Marnell, 1997. Fossil zooplankton and the historical status of westslope cutthroat trout in a headwater lake of Glacier National Park, Montana. Transactions of the American Fisheries Society 126: 21–34. https://doi.org/10.1577/1548-8659(1997)126%3c0021:FZATHS%3e2.3.CO;2.
Walsh, J. R., S. E. Munoz & M. J. Van Der Zanden, 2016. Outbreak of an undetected invasive species triggered by a climate anomaly. Ecosphere 7: e01628. https://doi.org/10.1002/ecs2.1628.
Acknowledgements
We are grateful to Y. Goda, T. Akatsuka, S. Yamamoto, M. Kuwae, M. Ochiai, and H. Iwata for their assistance with laboratory analysis and field sampling. This study was supported by Grants-in-Aid for Scientific Research (17K00528, 21K12273 to NT, and 21H03654 to KU) from the Japan Society for the Promotion of Science (JSPS) and also partly supported by a special research grant from Matsuyama University, the Academic Research Organization Joint Usage/Research Grants from Leading Academia in Marine and Environment Pollution Research (LaMer), Ehime University, and the Center for Ecological Research (2017–2021 jurc-cer), Kyoto University.
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N.T. and K.U conceived the idea and designed the study; N.T., I.H., K.N., M.N.H., and K.U. conducted sampling and the experiments; I.H., K.N., and K.U. contributed to the data analysis; K.U. contributed to primer design; N.T., I.H., and K.U. wrote the first draft of the manuscript; all authors revised and commented on the manuscript.
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Tsugeki, N., Hashimoto, I., Nakane, K. et al. Establishment success of alien Daphnia in the ancient Lake Biwa: insights from sedimentary archives. Hydrobiologia 851, 3591–3602 (2024). https://doi.org/10.1007/s10750-024-05519-0
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DOI: https://doi.org/10.1007/s10750-024-05519-0