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Ensemble forecasting of the global potential distribution of the invasive Chinese mitten crab, Eriocheir sinensis

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Abstract

Invasive alien species have posed substantial threats to freshwater ecosystems and are generally difficult and cost-intensive to eradicate once established. Therefore, it is of great importance to identify their potential distribution and take preventive actions. Species distribution modelling has been regarded as a powerful tool to identify areas that provide suitable environmental conditions for the establishment of invaders. In this study, an ensemble species distribution model was developed for the Chinese mitten crab (Eriocheir sinensis), by using 188 worldwide occurrence records and 11 environmental variables to predict its global potential distribution in freshwater habitats. The ensemble model showed high predictive performance and indicated that annual mean temperature was the most important environmental variable that limits the distribution of this invasive crustacean. The model successfully predicted the known distribution of Chinese mitten crab in its native range and invasive ranges and suggested that this invader has not yet fully realized its potential distribution in Europe and North America. The model also predicted some additional suitable areas where this crab has not yet been observed (Japan, part of South America, Australia, and New Zealand). Management strategies are proposed to control this invasive crab in light of these results.

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References

  • Acosta, A. L., T. C. Giannini, V. L. Imperatriz-Fonseca & A. M. Saraiva, 2016. Worldwide alien invasion: a methodological approach to forecast the potential spread of a highly invasive pollinator. PLoS ONE 11: e0148295.

    Article  Google Scholar 

  • Aguirre-Gutiérrez, J., L. G. Carvalheiro, C. Polce, E. E. van Loon, N. Raes, M. Reemer & J. C. Biesmeijer, 2013. Fit-for-purpose: species distribution model performance depends on evaluation criteria–Dutch hoverflies as a case study. PLoS ONE 8: e63708.

    Article  Google Scholar 

  • Allouche, O., A. Tsoar & R. Kadmon, 2006. Assessing the accuracy of species distribution models: prevalence, kappa and the true skill statistic (TSS). Journal of Applied Ecology 43: 1223–1232.

    Article  Google Scholar 

  • Araújo, M. B. & M. New, 2007. Ensemble forecasting of species distributions. Trends in Ecology and Evolution 22: 42–47.

    Article  Google Scholar 

  • Barbet-Massin, M., F. Jiguet, C. H. Albert & W. Thuiller, 2012. Selecting pseudo-absences for species distribution models: how, where and how many? Methods in Ecology and Evolution 3: 327–338.

    Article  Google Scholar 

  • Blakeslee, A. M. H., C. L. Keogh, J. E. Byers, A. M. Kuris, K. D. Lafferty & M. E. Torchin, 2009. Differential escape from parasites by two competing introduced crabs. Marine Ecology Progress Series 393: 83–96.

    Article  Google Scholar 

  • Brodin, T. & M. K. Drotz, 2014. Individual variation in dispersal associated behavioral traits of the invasive Chinese mitten crab (Eriocheir sinensis, H. Milne Edwards, 1854) during initial invasion of Lake Vänern, Sweden. Current Zoology 60: 410–416.

    Article  Google Scholar 

  • Brockerhoff, A. & C. L. McLay, 2011. Human-mediated spread of alien crabs. In Galil, B. S., P. F. Clark & J. T. Carlton (eds), In the Wrong Place—Alien Marine Crustaceans: Distribution, Biology and Impacts. Invading Nature-Springer Series in Invasion Ecology, Vol. 6. Springer, Dordrecht: 27–106.

    Google Scholar 

  • Broennimann, O. & A. Guisan, 2008. Predicting current and future biological invasions: both native and invaded ranges matter. Biology Letters 4: 585–589.

    Article  Google Scholar 

  • Bureau of Fisheries of the Ministry of Agriculture of China, 2017. China Fishery Statistical Yearbook. China Agriculture Press, Beijing (in Chinese).

    Google Scholar 

  • Capinha, C. & P. Anastácio, 2011. Assessing the environmental requirements of invaders using ensembles of distribution models. Diversity and Distributions 17: 13–24.

    Article  Google Scholar 

  • Capinha, C., E. R. Larson, E. Tricarico, J. D. Olden & F. Gherardi, 2013. Effects of climate change, invasive species, and disease on the distribution of native European crayfishes. Conservation Biology 27: 731–740.

    Article  Google Scholar 

  • Capinha, C., B. Leung & P. Anastácio, 2011. Predicting worldwide invasiveness for four major problematic decapods: an evaluation of using different calibration sets. Ecography 34: 448–459.

    Article  Google Scholar 

  • Costa, M. D. D. P., J. H. Muelbert, J. P. Vieira & J. P. Castello, 2015. Dealing with temporal variation and different life stages of whitemouth croaker Micropogonias furnieri (Actinopterygii, Sciaenidae) in species distribution modeling to improve essential estuarine fish habitat identification. Hydrobiologia 762: 195–208.

    Article  CAS  Google Scholar 

  • Dittel, A. I. & C. E. Epifanio, 2009. Invasion biology of the Chinese mitten crab Eriocheir sinensis: a brief review. Journal of Experimental Marine Biology and Ecology 374: 79–92.

    Article  Google Scholar 

  • Duan, R. Y., X. Q. Kong, M. Y. Huang, W. Y. Fan & Z. G. Wang, 2014. The predictive performance and stability of six species distribution models. PLoS ONE 9: e112764.

    Article  Google Scholar 

  • Elith, J. & C. H. Graham, 2009. Do they? How do they? Why do they differ? On finding reasons for differing performances of species distribution models. Ecography 32: 66–77.

    Article  Google Scholar 

  • Elith, J. & J. R. Leathwick, 2009. Species distribution models: ecological explanation and prediction across space and time. Annual Review of Ecology, Evolution, and Systematics 40: 677–697.

    Article  Google Scholar 

  • Elith, J., C. H. Graham, R. P. Anderson, M. Dudı, S. Ferrier, A. Guisan, R. J. Hijmans, F. Huettmann, J. R. Leathwick, A. Lehmann, J. Li, L. G. Lohmann, B. A. Loiselle, G. Manion, C. Moritz, M. Nakamura, Y. Nakazawa, J. M. Overton, A. T. Peterson, S. J. Phillips, K. Richardson, R. Scachetti-pereira, R. E. Schapire, J. Soberón, S. Williams, M. S. Wisz & N. E. Zimmermann, 2006. Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29: 129–151.

    Article  Google Scholar 

  • Fialho, C., F. Banha & P. M. Anastácio, 2016. Factors determining active dispersal capacity of adult Chinese mitten crab Eriocheir sinensis (Decapoda, Varunidae). Hydrobiologia 767: 321–331.

    Article  CAS  Google Scholar 

  • Fielding, A. H. & J. F. Bell, 1997. A review of methods for the assessment of prediction errors in conservation presence/absence models. Environmental Conservation 24: 38–49.

    Article  Google Scholar 

  • Fick, S. E. & R. J. Hijmans, 2017. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. International Journal of Climatology 37: 4302–4315.

    Article  Google Scholar 

  • Gama, M., D. Crespo, M. Dolbeth & P. M. Anastácio, 2017. Ensemble forecasting of Corbicula fluminea worldwide distribution: projections of the impact of climate change. Aquatic Conservation: Marine and Freshwater Ecosystems 27: 675–684.

    Article  Google Scholar 

  • Genovesi, P., 2005. Eradications of invasive alien species in Europe: a review. Biological Invasions 7: 127–133.

    Article  Google Scholar 

  • Gilbey, V., M. J. Attrill & R. A. Coleman, 2008. Juvenile Chinese mitten crabs (Eriocheir sinensis) in the Thames estuary: distribution, movement and possible interactions with the native crab Carcinus maenas. Biological Invasions 10: 67–77.

    Article  Google Scholar 

  • Gillard, M., G. Thiébaut, C. Deleu & B. Leroy, 2017. Present and future distribution of three aquatic plants taxa across the world: decrease in native and increase in invasive ranges. Biological Invasions 19: 2159–2170.

    Article  Google Scholar 

  • Global Invasive Species Database, 2018. Species profile: Eriocheir sinensis. [available on internet at http://www.iucngisd.org/gisd/species.php?sc=38]. Accessed 26 Feb 2018.

  • Gollasch, S., 2006. NOBANIS–invasive alien species fact sheet–Eriocheir sinensis. From: Online Database of the North European and Baltic Network on Invasive Alien Species–NOBANIS URL: www.nobanis.org.

  • Guisan, A. & W. Thuiller, 2005. Predicting species distribution: offering more than simple habitat models. Ecology Letters 8: 993–1009.

    Article  Google Scholar 

  • Guisan, A., W. Thuiller & N. E. Zimmermann, 2017. Habitat Suitability and Distribution Models: With Applications in R. Cambridge University Press, Cambridge.

    Book  Google Scholar 

  • Guo, C., S. Lek, S. Ye, W. Li, J. Liu & Z. Li, 2015. Uncertainty in ensemble modelling of large-scale species distribution: effects from species characteristics and model techniques. Ecological Modelling 306: 67–75.

    Article  Google Scholar 

  • Hänfling, B., F. Edwards & F. Gherardi, 2011. Invasive alien Crustacea: dispersal, establishment, impact and control. BioControl 56: 573–595.

    Article  Google Scholar 

  • Heikkinen, R. K., M. Marmion & M. Luoto, 2012. Does the interpolation accuracy of species distribution models come at the expense of transferability? Ecography 35: 276–288.

    Article  Google Scholar 

  • Herborg, L. M., S. P. Rushton, A. S. Clare & M. G. Bentley, 2003. Spread of the Chinese mitten crab (Eriocheir sinensis H. Milne Edwards) in Continental Europe: analysis of a historical data set. Hydrobiologia 503: 21–28.

    Article  Google Scholar 

  • Herborg, L. M., C. L. Jerde, D. M. Lodge, G. M. Ruiz & H. J. MacIsaac, 2007a. Predicting invasion risk using measures of introduction effort and environmental niche models. Ecological Applications 17: 663–674.

    Article  Google Scholar 

  • Herborg, L. M., D. A. Rudnick, Y. Siliang, D. M. Lodge & H. J. MacIsaac, 2007b. Predicting the range of Chinese mitten crabs in Europe. Conservation Biology 21: 1316–1323.

    Article  Google Scholar 

  • Howard, B. R., T. W. Therriault & I. M. Côté, 2017. Contrasting ecological impacts of native and non-native marine crabs: a global meta-analysis. Marine Ecology Progress Series 577: 93–103.

    Article  Google Scholar 

  • Jakubowska, M. & M. Normant, 2011. Effect of temperature on the physiology and bioenergetics of adults of the Chinese mitten crab Eriocheir sinensis: considerations for a species invading cooler waters. Marine and Freshwater Behaviour and Physiology 44: 171–183.

    Article  Google Scholar 

  • Kang, W., L. Wu, J. Liu, C. Zhang, M. Lin, J. Wang & C. Wang, 2016. Morphological differences and genetic admixture in mitten crabs in the Tumenjiang River. Journal of Fishery Sciences of China 23: 555–564.

    Google Scholar 

  • Lei, J., L. Chen & H. Li, 2017. Using ensemble forecasting to examine how climate change promotes worldwide invasion of the golden apple snail (Pomacea canaliculata). Environmental Monitoring and Assessment 189: 404.

    Article  Google Scholar 

  • Lowe, S., M. Browne, S. Boudjelas & M. De Poorter, 2000. 100 of the World’s Worst Invasive Alien Species: A Selection from the Global Invasive Species Database. The Invasive Species Specialist Group, World Conservation Union, Auckland.

    Google Scholar 

  • Mammola, S., S. L. Goodacre & M. Isaia, 2018. Climate change may drive cave spiders to extinction. Ecography 41: 233–243.

    Article  Google Scholar 

  • Morehouse, R. L. & M. Tobler, 2013. Invasion of rusty crayfish, Orconectes rusticus, in the United States: niche shifts and potential future distribution. Journal of Crustacean Biology 33: 293–300.

    Article  Google Scholar 

  • Nüchel, J., P. K. Bøcher, W. Xiao, A. X. Zhu & J. C. Svenning, 2018. Snub-nosed monkeys (Rhinopithecus): potential distribution and its implication for conservation. Biodiversity and Conservation 27: 1–22.

    Article  Google Scholar 

  • Pearson, R. G., W. Thuiller, M. B. Araujo, E. Martinez-Meyer, L. Brotons, C. McClean, L. Miles, P. Segurado, T. P. Dawson & D. C. Lees, 2006. Model-based uncertainty in species range prediction. Journal of Biogeography 33: 1704–1711.

    Article  Google Scholar 

  • Phillips, S. J., R. P. Anderson & R. E. Schapire, 2006. Maximum entropy modeling of species geographic distributions. Ecological Modelling 190: 231–259.

    Article  Google Scholar 

  • Pimentel, D., L. Lach, R. Zuniga & D. Morrison, 2000. Environmental and economic costs of nonindigenous species in the United States. BioScience 50: 53–65.

    Article  Google Scholar 

  • Qiao, H. J., J. Soberón & A. T. Peterson, 2015. No silver bullets in correlative ecological niche modelling: insights from testing among many potential algorithms for niche estimation. Methods in Ecology and Evolution 6: 1126–1136.

    Article  Google Scholar 

  • R Development Core Team, 2014. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Version: 3.3.2.

  • Riul, P., C. H. Targino, L. A. Júnior, J. C. Creed, P. A. Horta & G. C. Costa, 2013. Invasive potential of the coral Tubastraea coccinea in the southwest Atlantic. Marine Ecology Progress Series 480: 73–81.

    Article  Google Scholar 

  • Rosewarne, P. J., R. J. Mortimer, R. J. Newton, C. Grocock, C. D. Wing & A. M. Dunn, 2016. Feeding behaviour, predatory functional responses and trophic interactions of the invasive Chinese mitten crab (Eriocheir sinensis) and signal crayfish (Pacifastacus leniusculus). Freshwater Biology 61: 426–443.

    Article  Google Scholar 

  • Rudnick, D. & V. Resh, 2005. Stable isotopes, mesocosms and gut content analysis demonstrate trophic differences in two invasive decapod crustacea. Freshwater Biology 50: 1323–1336.

    Article  Google Scholar 

  • Schrimpf, A., T. Schmidt & R. Schulz, 2014. Invasive Chinese mitten crab (Eriocheir sinensis) transmits crayfish plague pathogen (Aphanomyces astaci). Aquatic Invasions 9: 203–209.

    Article  Google Scholar 

  • Spiridonov, V. A. & A. K. Zalota, 2017. Understanding and forecasting dispersal of non-indigenous marine decapods (Crustacea: Decapoda) in East European and North Asian waters. Journal of the Marine Biological Association of the United Kingdom 97: 591–611.

    Article  CAS  Google Scholar 

  • Sui, L., F. Zhang, X. Wang, P. Bossier, P. Sorgeloos & B. Hänfling, 2009. Genetic diversity and population structure of the Chinese mitten crab Eriocheir sinensis in its native range. Marine Biology 156: 1573–1583.

    Article  Google Scholar 

  • Takeda, M. & M. Koizumi, 2005. Occurrence of the Chinese mitten crab, Eriocheir sinensis H. Milne Edwards, in Tokyo Bay, Japan. Bulletin of the National Science Museum, Series A, Zoology 31: 21–24.

    Google Scholar 

  • Tang, B., K. Zhou, D. Song, G. Yang & A. Dai, 2003. Molecular systematics of the Asian mitten crabs, genus Eriocheir (Crustacea: Brachyura). Molecular Phylogenetics and Evolution 29: 309–316.

    Article  CAS  Google Scholar 

  • Torchin, M. E. & K. D. Lafferty, 2009. Escape from Parasites. In: Rilov, G. & J. A. Crooks (eds), Biological Invasions in Marine Ecosystems. Springer, Berlin, Ecological Studies 204: 204–213.

  • Torchin, M. E., K. D. Lafferty & A. M. Kuris, 2002. Parasites and marine invasions. Parasitology 124: 137–151.

    Article  Google Scholar 

  • Thuiller, W., D. Georges & R. Engler, 2014. biomod2: ensemble platform for species distribution modeling. R package version 3.3.7.

  • Verbruggen, H., L. Tyberghein, G. S. Belton, F. Mineur, A. Jueterbock, G. Hoarau, C. F. D. Gurgel & O. De Clerck, 2013. Improving transferability of introduced species’ distribution models: new tools to forecast the spread of a highly invasive seaweed. PLoS ONE 8: e68337.

    Article  CAS  Google Scholar 

  • Walker, G. A., M. P. Robertson, M. Gaertner, L. Gallien & D. M. Richardson, 2017. The potential range of Ailanthus altissima (tree of heaven) in South Africa: the roles of climate, land use and disturbance. Biological Invasions 19: 3675–3690.

    Article  Google Scholar 

  • Webster, J. M., P. F. Clark & D. Morritt, 2015. Laboratory based feeding behaviour of the Chinese mitten crab, Eriocheir sinensis (Crustacea: Decapoda: Brachyura: Varunidae): fish egg consumption. Aquatic Invasions 10: 313–326.

    Article  Google Scholar 

  • Wenger, S. J. & J. D. Olden, 2012. Assessing transferability of ecological models: an underappreciated aspect of statistical validation. Methods in Ecology and Evolution 3: 260–267.

    Article  Google Scholar 

  • Xu, J., T. Y. Chan, L. M. Tsang & K. H. Chu, 2009. Phylogeography of the mitten crab Eriocheir sensu stricto in East Asia: Pleistocene isolation, population expansion and secondary contact. Molecular Phylogenetics and Evolution 52: 45–56.

    Article  Google Scholar 

  • Yuan, Q., Q. Wang, T. Zhang, Z. Li & J. Liu, 2017. Effects of water temperature on growth, feeding and molting of juvenile Chinese mitten crab Eriocheir sinensis. Aquaculture 468: 169–174.

    Article  Google Scholar 

  • Zhang, Z., M. Yokota & C. A. Strüssmann, 2016. Autotomy patterns in the Japanese mitten crab, Eriocheir japonica. Crustacean Research 45: 49–58.

    Article  Google Scholar 

  • Zhang, Z., M. Yokota & C. A. Strüssmann, 2017. Relative growth pattern and relative condition factor in the Japanese mitten crab Eriocheir japonica (De Haan, 1835) (Brachyura: Varunidae). Journal of Crustacean Biology 37: 571–578.

    Article  Google Scholar 

  • Zhang, Z., M. Yokota & C. A. Strüssmann, 2018. Cannibalism in the Japanese mitten crab, Eriocheir japonica. Hydrobiologia 807: 367–376.

    Article  CAS  Google Scholar 

  • Zhao, N., N. Du, X. Bao & L. Zhang, 1988. Artificial breeding, propagation and culture of Chinese mitten crab. Anhui Science and Technology Press, Hefei. (in Chinese).

    Google Scholar 

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Acknowledgements

We wish to thank Dr. Lian Chen (Jiangsu Second Normal University, China), Dr. Juncheng Lei (Gannan Normal University, China), and Dr. Stefano Mammola (University of Torino, Italy) for their constructive suggestions on the model. We express our thanks to Fakai Li (East Sea Information Center, SOA China, Shanghai, China) for his assistance with the data collection. We thank two anonymous reviewers for their constructive comments. This work was financially supported by the Central Public-interest Scientific Institution Basal Research Fund, CAFS (2018SJ-YZ01).

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Authors and Affiliations

  1. Graduate School of Marine Science and Technology, Tokyo University of Marine Science and Technology, Konan, Minato, Tokyo, 1088477, Japan

    Zhixin Zhang

  2. CIBIO/InBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto, 4485661, Vairão, Portugal

    César Capinha

  3. CEABN/InBIO-Centro de Estudos Ambientais ‘Prof. Baeta Neves’, Instituto Superior de Agronomia, Universidade de Lisboa, Tapada da Ajuda, 1349-017, Lisbon, Portugal

    César Capinha

  4. Cat Drop Foundation, 9204, Drachten, Netherlands

    Robbie Weterings

  5. School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch, New Zealand

    Colin L. McLay

  6. College of Biological and Agricultural Engineering, Weifang University, Key Laboratory of Biochemistry and Molecular Biology in Universities of Shandong, Weifang, 261061, China

    Dan Xi

  7. Key Laboratory of Freshwater Fish Reproduction and Development, Ministry of Education, College of Animal Science and Technology, Southwest University, Chongqing, 400715, China

    Hongjian Lü

  8. Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou, 510380, China

    Lingyun Yu

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  1. Zhixin Zhang
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  4. Colin L. McLay
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  7. Lingyun Yu
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Zhang, Z., Capinha, C., Weterings, R. et al. Ensemble forecasting of the global potential distribution of the invasive Chinese mitten crab, Eriocheir sinensis. Hydrobiologia 826, 367–377 (2019). https://doi.org/10.1007/s10750-018-3749-y

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