https://doi.org/10.4081/jlimnol.2024.2200
Escape rooms: behavioural response of two invasive crayfish species under water decline scenarios
Submitted: 6 July 2024
Accepted: 20 July 2024
Published: 2 September 2024
Accepted: 20 July 2024
Abstract Views: 292
PDF: 92
HTML: 18
HTML: 18
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
Authors
Climate change and invasive alien species pose a significant threat to biodiversity and the survival of native species. This study considered the impact of drought conditions on the escape behaviour through terrestrial dispersal ability of two invasive freshwater crayfish species, the red swamp crayfish (Procambarus clarkii) and signal crayfish (Pacifastacus leniusculus). Using an experimental design simulating drought conditions and Mediterranean summer temperatures, we tested the hypothesis that P. clarkii exhibits a greater tendency to terrestrial migration and a higher land-walking speed than the P. leniusculus. The results indicated that both species demonstrated strong escape behaviour, with P. clarkii showing escape success higher than P. leniusculus, and increasing with decreasing mean night temperature and crayfish weight. Although drought conditions did not trigger escape, invasive species showed increased resistance and the ability to move to more favourable environments, suggesting that drought is not an effective geographic barrier against the spread of these species. These results underline the importance of considering invasive species' ability to escape and climb as part of management and control strategies.
Alcamo J, Flörke M, Märker M, 2007. Future long-term changes in global water resources driven by socio-economic and climatic changes. Hydrol Sci J 52:247-275.
DOI: https://doi.org/10.1623/hysj.52.2.247
Aquiloni L, Ilhéu M, Gherardi F, 2005. Habitat use and dispersal of the invasive crayfish Procambarus clarkii in ephemeral water bodies of Portugal. Mar Freshw Behav Physiol 38:225-236.
DOI: https://doi.org/10.1080/10236240500310195
Banha F, Anastácio PM, 2014. Desiccation survival capacities of two invasive crayfish species. Knowl Managt Aquatic Ecosyst 413:01.
DOI: https://doi.org/10.1051/kmae/2013084
Bates D, Maechler M, Bolker B, Walker S, Christensen RHB, Singmann H, et al., 2023. lme4: Linear Mixed-Effects Models using “Eigen” and S4. Available from: https://CRAN.R-project.org/package=lme4
Bond NR, Lake PS, Arthington AH, 2008. The impacts of drought on freshwater ecosystems: an Australian perspective. Hydrobiologia 600:3-16.
DOI: https://doi.org/10.1007/s10750-008-9326-z
Capinha C, Larson ER, Tricarico E, Olden JD, Gherardi F, 2013. Effects of climate change, invasive species, and disease on the distribution of native European crayfishes. Conserv Biol 27:731-740.
DOI: https://doi.org/10.1111/cobi.12043
Capon SJ, Stewart-Koster B, Bunn SE, 2021. Future of freshwater ecosystems in a 1.5°C warmer world. Front Environ Sc. 9:784642.
DOI: https://doi.org/10.3389/fenvs.2021.784642
Claussen DL, Hopper RA, Sanker AM, 2000. The effects of temperature, body size, and hydration state on the terrestrial locomotion of the crayfish Orconectes rusticus. J Crustacean Biol 20:218-223.
DOI: https://doi.org/10.1163/20021975-99990033
Colwell RK, Brehm G, Cardelús CL, Gilman AC, Longino JT, 2008. Global warming, elevational range shifts, and lowland biotic attrition in the wet tropics. Science 322:258-261.
DOI: https://doi.org/10.1126/science.1162547
Deinet S, Flint R, Puleston H, Baratech A, Royte J, Thieme ML, et al., 2024. The Living Planet Index (LPI) for migratory freshwater fish 2024 update - Technical Report. World Fish Migration Foundation.
Dickey BF, McCarthy TM, 2007. Predator-prey interactions between crayfish (Orconectes juvenilis) and snails (Physa gyrina) are affected by spatial scale and chemical cues. Invertebr Biol 126:57-66.
DOI: https://doi.org/10.1111/j.1744-7410.2007.00076.x
Dudgeon D, Arthington AH, Gessner MO, Kawabata Z-I, Knowler DJ, Lévêque C, et al., 2006. Freshwater biodiversity: importance, threats, status and conservation challenges. Biol Rev 81:163-182.
DOI: https://doi.org/10.1017/S1464793105006950
Edwards DH, Heitler WJ, Krasne FB, 1999. Fifty years of a command neuron: the neurobiology of escape behavior in the crayfish. Trends Neurosci 22:153-161.
DOI: https://doi.org/10.1016/S0166-2236(98)01340-X
Ercoli F, Ghia D, Gruppuso L, Fea G, Bo T, Ruokonen TJ, 2021. Diet and trophic niche of the invasive signal crayfish in the first invaded Italian stream ecosystem. Sci Rep 11:8704.
DOI: https://doi.org/10.1038/s41598-021-88073-2
European Union, 2014. Regulation (EU) No 1143/2014 of the European Parliament and of the Council of 22 October 2014 on the prevention and management of the introduction and spread of invasive alien species. Official Journal, L 317, 4.11.2014, p. 35-55.
Friberg N, Dybkjær JB, Olafsson JS, Gislason GM, Larsen SE, Lauridsen TL, 2009. Relationships between structure and function in streams contrasting in temperature. Freshwater Biol 54:2051–2068.
DOI: https://doi.org/10.1111/j.1365-2427.2009.02234.x
Galib SM, Sun J, Twiss SD, Lucas MC, 2022. Personality, density and habitat drive the dispersal of invasive crayfish. Sci Rep 12:1114.
DOI: https://doi.org/10.1038/s41598-021-04228-1
Gherardi F, Tricarico E, Ilhéu M, 2002. Movement patterns of an invasive crayfish, Procambarus clarkii, in a temporary stream of southern Portugal. Ethol Ecol Evol 14:183-197.
DOI: https://doi.org/10.1080/08927014.2002.9522739
Glon MG, Reisinger LS, Pintor LM, 2018. Biogeographic differences between native and non-native populations of crayfish alter species coexistence and trophic interactions in mesocosms. Biol Invasions 20:3475-3490.
DOI: https://doi.org/10.1007/s10530-018-1788-y
Guan RZ, 2000. Abundance and production of the introduced signal crayfish in a British lowland river. Aquacult Int 8:59–76.
Hänfling B, Edwards F, Gherardi F, 2011. Invasive alien crustacea: dispersal, establishment, impact and control. BioControl 56:573-595.
DOI: https://doi.org/10.1007/s10526-011-9380-8
Hanshew BA, Garcia TS, 2012. Invasion of the shelter snatchers: behavioural plasticity in invasive red swamp crayfish, Procambarus clarkii. Freshwater Biol 57:2285-2296.
DOI: https://doi.org/10.1111/fwb.12002
Harris RML, Armitage PD, Milner AM, Ledger ME, 2007. Replicability of physicochemistry and macroinvertebrate assemblages in stream mesocosms: implications for experimental research. Freshwater Biol 52:2434–2443.
DOI: https://doi.org/10.1111/j.1365-2427.2007.01839.x
Haubrock PJ, Cuthbert RN, Haase P, 2023. Long-term trends and drivers of biological invasion in Central European streams. Sci Total Environ 876:162817.
DOI: https://doi.org/10.1016/j.scitotenv.2023.162817
Haubrock PJ, Kubec J, Veselý L, Buřič M, Tricarico E, Kouba A, 2019. Water temperature as a hindrance, but not limiting factor for the survival of warm water invasive crayfish introduced in cold periods. J Great Lakes Res 45:788-794.
DOI: https://doi.org/10.1016/j.jglr.2019.05.006
Heitler WJ, Fraser K, Ferrero EA, 2000. Escape behaviour in the stomatopod crustacean Squilla Mantis, and the evolution of the caridoid escape reaction. J Exp Biol 203:183-192.
DOI: https://doi.org/10.1242/jeb.203.2.183
Herberholz J, Sen MM, Edwards DH, 2004. Escape behavior and escape circuit activation in juvenile crayfish during prey-predator interactions. J Exp Bio. 207:1855-1863.
DOI: https://doi.org/10.1242/jeb.00992
Holdich DM, 2002. Biology of freshwater crayfish. Blackwell Science, London: 702 pp.
Holdich DM, James J, Jackson C, Peay S, 2014. The North American signal crayfish, with particular reference to its success as an invasive species in Great Britain. Ethol Ecol Evol 26:232-262.
DOI: https://doi.org/10.1080/03949370.2014.903380
Hunyadi J, Currier T, Modarres-Sadeghi Y, Flammang BE, Clotfelter ED, 2020. Morphology, performance and fluid dynamics of the crayfish escape response. J Exp Biol 223:219873.
DOI: https://doi.org/10.1242/jeb.219873
Johnson MF, Albertson LK, Algar AC, Dugdale SJ, Edwards P, et al., 2024. Rising water temperature in rivers: Ecological impacts and future resilience. WIREs Water 11:e1724.
DOI: https://doi.org/10.1002/wat2.1724
Johović I, Verrucchi C, Inghilesi AF, Scapini F, Tricarico E, 2020. Managing the invasive crayfish Procambarus clarkii: Is manual sterilisation the solution? Freshwater Biol 65:621-631.
DOI: https://doi.org/10.1111/fwb.13450
Kerby JL, Riley SPD, Kats LB, Wilson P, 2005. Barriers and flow as limiting factors in the spread of an invasive crayfish (Procambarus clarkii) in southern California streams. Biol Conserv 126:402-409.
DOI: https://doi.org/10.1016/j.biocon.2005.06.020
Kingsford R, 2006. Ecology of desert rivers. Cambridge University Press, Cambridge: 368 pp.
Kouba A, Petrusek A, Kozák P, 2014. Continental-wide distribution of crayfish species in Europe: update and maps. Knowl Managt Aquatic Ecosyst 413:5.
DOI: https://doi.org/10.1051/kmae/2014007
Kouba A, Tíkal J, Císař P, Veselý L, Fořt M, Příborský J, et al., 2016. The significance of droughts for hyporheic dwellers: evidence from freshwater crayfish. Sci Rep 6:1-7.
DOI: https://doi.org/10.1038/srep26569
Krieg R, Zenker A, 2020. A review of the use of physical barriers to stop the spread of non-indigenous crayfish species. Rev Fish Biol Fisheries 30:423-435.
DOI: https://doi.org/10.1007/s11160-020-09606-y
Kuznetsova A, Brockhoff PB, Christensen RHB, Jensen SP, 2020. lmerTest: Tests in Linear Mixed Effects Models. Available from: https://CRAN.R-project.org/package=lmerTest
Lake PS, 2003. Ecological effects of perturbation by drought in flowing waters. Freshwater Biol 48:1161-1172.
DOI: https://doi.org/10.1046/j.1365-2427.2003.01086.x
Le Hen G, Balzani P, Haase P, Kouba A, Liu C, Nagelkerke LAJ, et al., 2023. Alien species and climate change drive shifts in a riverine fish community and trait compositions over 35 years. Sci Total Environ 867:161486.
DOI: https://doi.org/10.1016/j.scitotenv.2023.161486
Lehti-Koivunen SM, Kivivuori LA, 1994. Effect of temperature acclimation in the crayfish Astacus astacus L. on the locomotor activity during a cyclic temperature change. J Therm Biol 19:299-304.
DOI: https://doi.org/10.1016/0306-4565(94)90065-5
Lemmers P, van der Kroon R, van Kleef HH, Verhees JJF, van der Velde G, Leuven RSEW, 2022. Limiting burrowing activity and overland dispersal of the invasive alien red swamp crayfish Procambarus clarkii by sophisticated design of watercourses. Ecol Eng 185:106787.
DOI: https://doi.org/10.1016/j.ecoleng.2022.106787
Marques M, Banha F, Águas M, Anastácio P, 2015. Environmental cues during overland dispersal by three freshwater invaders: Eriocheir sinensis, Pacifastacus leniusculus, and Procambarus clarkii (Crustacea, Decapoda). Hydrobiologia 742:81-93.
DOI: https://doi.org/10.1007/s10750-014-1968-4
Peay S, Dunn AM, 2014. The behavioural response of the invasive signal crayfish Pacifastacus leniusculus to experimental dewatering of burrows and its implications for eradication treatment and management of ponds with crayfish. Ethol Ecol Evol 26:277-298.
DOI: https://doi.org/10.1080/03949370.2014.903379
Piersanti S, Pallottini M, Salerno G, Goretti E, Elia AC, Dörr AJM, Rebora M, 2018. Resistance to dehydration and positive hygrotaxis in the invasive red swamp crayfish Procambarus clarkii. Knowl Manag Aquat Ecosyst 419:36.
DOI: https://doi.org/10.1051/kmae/2018024
Pörtner H-O, Bock C, Mark FC, 2017. Oxygen- and capacity-limited thermal tolerance: bridging ecology and physiology. J Exp Biol 220:2685-2696.
DOI: https://doi.org/10.1242/jeb.134585
Ramalho RO, Anastácio PM, 2015. Factors inducing overland movement of invasive crayfish (Procambarus clarkii) in a ricefield habitat. Hydrobiologia 746:135-146.
DOI: https://doi.org/10.1007/s10750-014-2052-9
Román-Palacios C, Wiens JJ, 2020. Recent responses to climate change reveal the drivers of species extinction and survival. P Natl Acad Sci USA 117:4211-4217.
DOI: https://doi.org/10.1073/pnas.1913007117
Russo S, Sillmann J, Fischer EM, 2015. Top ten European heatwaves since 1950 and their occurrence in the coming decades. Environ Res Lett 10:124003.
DOI: https://doi.org/10.1088/1748-9326/10/12/124003
Sbragaglia V, Breithaupt T, 2022. Daily activity rhythms, chronotypes, and risk-taking behavior in the signal crayfish. Curr Zool.68:177-183.
DOI: https://doi.org/10.1093/cz/zoab023
Thomas JR, Fisher J, Cable J, Griffiths SW, 2018. Terrestrial dispersal of invasive signal crayfish during vulnerable life stages. Behav Processes 157:204-207.
DOI: https://doi.org/10.1016/j.beproc.2018.09.014
Thomas JR, Masefield S, Hunt R, Wood MJ, Hart AG, Hallam J, et al., 2019. Terrestrial emigration behaviour of two invasive crayfish species. Behav Processes 167:103917.
DOI: https://doi.org/10.1016/j.beproc.2019.103917
Tickner D, Opperman JJ, Abell R, Acreman M, Arthington AH, Bunn SE, et al., 2020. Bending the curve of global freshwater biodiversity loss: an emergency recovery plan. BioScience 70:330-342.
DOI: https://doi.org/10.1093/biosci/biaa002
Toutain M, Soto I, Rasmussen JJ, Csabai Z, Várbíró G, Murphy JF, et al., 2024. Tracking long-term shifts in non-native freshwater macroinvertebrates across three European countries. Sci Total Environ 906:167402.
DOI: https://doi.org/10.1016/j.scitotenv.2023.167402
Tramblay Y, Koutroulis A, Samaniego L, Vicente-Serrano SM, Volaire F, Boone A, et al., 2020. Challenges for drought assessment in the Mediterranean region under future climate scenarios. Earth-Sci Rev 210:103348.
DOI: https://doi.org/10.1016/j.earscirev.2020.103348
Tricarico E, Zanetti M, 2023. [Piano di gestione nazionale del gambero rosso della Louisiana (Procambarus clarkii)].[Report in Italian]. ISPR. Available from: https://www.mase.gov.it/sites/default/files/archivio/allegati/biodiversita/piano_gestione_gambero_louisiana.pdf
Turbelin AJ, Malamud BD, Francis RA, 2017. Mapping the global state of invasive alien species: patterns of invasion and policy responses. Glob Ecol Biogeogr 26:78-92.
DOI: https://doi.org/10.1111/geb.12517
van der Meeren GI, Uksnøy LE, 2000. A comparison of claw morphology and dominance between wild andcultivated male European lobster. Aquacult Int 8:77-94.
DOI: https://doi.org/10.1023/A:1009225001318
Vedia I, Galicia D, Baquero E, Oscoz J, Miranda R, 2016. Environmental factors influencing the distribution and abundance of the introduced signal crayfish in the north of Iberian Peninsula. Mar Freshwater Res 68:900-908.
DOI: https://doi.org/10.1071/MF16020
Verberk WCEP, Atkinson D, Hoefnagel KN, Hirst AG, Horne CR, Siepel H, 2021. Shrinking body sizes in response to warming: explanations for the temperature–size rule with special emphasis on the role of oxygen. Biol Rev 96:247-268.
DOI: https://doi.org/10.1111/brv.12653
Veselý L, Buřič M, Kouba A, 2015. Hardy exotics species in temperate zone: can “warm water” crayfish invaders establish regardless of low temperatures? Sci Rep 5:16340.
DOI: https://doi.org/10.1038/srep16340
Wanders N, van Vliet MTH, Wada Y, Bierkens MFP, van Beek LPH (Rens), 2019. High-resolution global water temperature modeling. Water Resour Res 55:2760-2778.
DOI: https://doi.org/10.1029/2018WR023250
Westhoff JT, Rosenberger AE, 2016. A global review of freshwater crayfish temperature tolerance, preference, and optimal growth. Rev Fish Biol Fisheries 26:329-349.
DOI: https://doi.org/10.1007/s11160-016-9430-5
Wutz S, Geist J, 2013. Sex- and size-specific migration patterns and habitat preferences of invasive signal crayfish (Pacifastacus leniusculus Dana). Limnologica 43:59-66.
DOI: https://doi.org/10.1016/j.limno.2012.02.002
Zhang B, Hastings A, Grosholz ED, Zhai L, 2023. The comparison of dispersal rate between invasive and native species varied by plant life form and functional traits. Mov Ecol 11:73.
DOI: https://doi.org/10.1186/s40462-023-00424-y
Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM, 2009. Mixed effects models and extensions in ecology with R. Springer, New York: 574 pp.
DOI: https://doi.org/10.1007/978-0-387-87458-6
Edited by
Diego Fontaneto, National Research Council, Water Research Institute (CNR-IRSA), Verbania Pallanza, ItalyHow to Cite
Ghia, Daniela, Gianluca Fea, Fabio Ercoli, and Roberto Sacchi. 2024. “Escape Rooms: Behavioural Response of Two Invasive Crayfish Species under Water Decline Scenarios”. Journal of Limnology 83 (1). https://doi.org/10.4081/jlimnol.2024.2200.
Copyright (c) 2024 The Author(s)
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
Similar Articles
- Francisco Diogo R. Sousa, Alexandre V. Palaoro, Lourdes M.A. Elmoor-Loureiro, Alexey A. Kotov, Predicting the invasive potential of the cladoceran Daphnia lumholtzi Sars, 1885 (Crustacea: Cladocera: Daphniidae) in the Neotropics: are generalists threatened and relicts protected by their life-history traits? , Journal of Limnology: Vol. 76 No. 2 (2017)
- Jianming Deng, Yunlin Zhang, Boqiang Qin, Xiaolong Yao, Yubing Deng, Trends of publications related to climate change and lake research from 1991 to 2015 , Journal of Limnology: Vol. 76 No. 3 (2017)
- Claude Lang, Phosphorus decreases in Lake Geneva but climate warming hampers the recovery of pristine oligochaete communities whereas chironomids are less affected , Journal of Limnology: Vol. 75 No. 2 (2016)
- Robin J. Smith, Dayou Zhai, Suktonthip Savatenalinton, Takahiro Kamiya, Na Yu, A review of rice field ostracods (Crustacea) with a checklist of species , Journal of Limnology: Vol. 77 No. 1 (2018)
- Muhammed Shikhani, Chenxi Mi, Artur Gevorgyan, Gor Gevorgyan, Amalya Misakyan, Levon Azizyan, Klemens Barfus, Martin Schulze, Tom Shatwell, Karsten Rinke, Simulating thermal dynamics of the largest lake in the Caucasus region: The mountain Lake Sevan , Journal of Limnology: Vol. 81 No. s1 (2022): Lake Sevan. Past, present, and future state of a unique alpine lake
- Margherita Abbà, Carlo Ruffino, Tiziano Bo, Davide Bonetto, Stefano Bovero, Alessandro Candiotto, Claudio Comoglio, Paolo Lo Conte, Daniel Nyqvist, Michele Spairani, Stefano Fenoglio, Distribution of fish species in the upper Po River Basin (NW Italy): a synthesis of 30 years of data , Journal of Limnology: Vol. 83 (2024)
- Oscar Wembo Ndeo, Torsten Hauffe, Diana Delicado, Alidor Kankonda Busanga, Christian Albrecht, Mollusk communities of the central Congo River shaped by combined effects of barriers, environmental gradients, and species dispersal , Journal of Limnology: Vol. 76 No. 3 (2017)
- Armine Hayrapetyan, Gor Gevorgyan , Martin Schultze, Muhammed Shikhani, Termine Khachikyan, Aleksandr Krylov, Karsten Rinke, Contemporary community composition, spatial distribution patterns, and biodiversity characteristics of zooplankton in large alpine Lake Sevan, Armenia , Journal of Limnology: Vol. 81 No. s1 (2022): Lake Sevan. Past, present, and future state of a unique alpine lake
- Vanessa Pendino, Luca Vecchioni, Fabio Stoch, Federico Marrone, Checklist and distribution of the groundwater crustacean fauna from Sicily, Italy , Journal of Limnology: Vol. 83 (2024)
- Thaisa S. Michelan, Márcio J. Silveira, Danielle K. Petsch, Gisele D. Pinha, Sidinei M. Thomaz, The invasive aquatic macrophyte Hydrilla verticillata facilitates the establishment of the invasive mussel Limnoperna fortunei in Neotropical reservoirs , Journal of Limnology: Vol. 73 No. 3 (2014)
You may also start an advanced similarity search for this article.
