Abstract
Over recent decades, many Mediterranean and Ponto-Caspian aquatic invertebrate species have dispersed northwards and established as non-native species in colder regions. We hypothesized that these species have cold-tolerant traits, which facilitate dispersal into colder climates. Thanks to these traits, Southern European aquatic species are able to cross biogeographic boundaries. We downloaded the list of all alien invertebrate species that were fully aquatic (i.e. lacking terrestrial adults) from the GRIIS database and picked out those Mediterranean and Ponto-Caspian species that have undergone northwards range expansion. We identified traits that may facilitate dispersal to colder climates including the following: small size; capacity for behavioural thermoregulation; feeding habit (omnivorous, filter-feeders, food generalists); quiescence and dormancy (or diapause); freezing avoidance (presence of cryoprotectants); tolerance to low temperatures or eurythermicity; active dispersal; and enhanced reproduction. We statistically tested the null hypotheses that Mediterranean and Ponto-Caspian alien aquatic invertebrate species that dispersed into the north have all of these traits. We used contingency tables populated with raw frequency data with χ2—tests and assessed statistical significance at α of 0.05. We identified 95 Mediterranean and Ponto-Caspian alien aquatic invertebrate species that have shown northwards range extension, 10 (10%) of which were of Mediterranean origin and 85 (90%) of Ponto-Caspian origin. We found that this northwards dispersal from Southern Europe is mainly limited to a few following groups of aquatic invertebrates: small crustaceans, molluscs, cnidarians and annelids. Ability to go to diapause, hibernation or resting period, temperature tolerance and small size were the traits most commonly shared by these organisms. We conclude that Mediterranean and Ponto-Caspian aquatic invertebrate species showing northwards range expansion have cold-tolerant strategies. The traits analysed can favour the establishment of the species.
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Data availability
All data generated or analysed during this study are available via the Data repository of the University of Gdansk. Requests for material should be made to the corresponding author.
References
Abeli T, Vamosi JC, Orsenigo S (2018) The importance of marginal population hotspots of cold-adapted species for research on climate change and conservation. J Biogeogr 45(5):977–985. https://doi.org/10.1111/jbi.13196
Ahnoff M, Cazares LH, Skold K (2015) Thermal inactivation of enzymes and pathogens in biosamples for MS analysis. Bioanalysis 7(15):1885–1899. https://doi.org/10.4155/BIO.15.122
Aladin NV (1995) The conservation ecology of the Podonidae from the Caspian and Aral Seas. Hydrobiologia 307(1–3):85–97. https://doi.org/10.1007/BF00032000
Arribas P, Gutiérrez-Cánovas C, Botella-Cruz M, Cañedo-Arguelles M, Carbonell JA, Millán A, Pallarés S, Velasco J, Sánchez-Fernández D (2019) Insect communities in saline waters consist of realized but not fundamental niche specialists. Philos Trans R Soc B 374:20180008. https://doi.org/10.1098/rstb.2018.0008
Ateş AS (1999) Liocarcinus depurator (Linnaeus, 1758) and Brachynotus sexdentatus (Risso, 1827) (Decapoda, Brachyura), two new records for the Turkish Black Sea fauna. Turk J Zool 23(2):115–118
Banha F, Anastácio PM (2012) Waterbird-mediated passive dispersal of river shrimp Atyaephyra desmaresti. Hydrobiologia 694(1):197–204. https://doi.org/10.1007/s10750-012-1160-7
Basen T, Martin-Creuzburg D, Rothhaupt KO (2011) Role of essential lipids in determining food quality for the invasive freshwater clam Corbicula fluminea. J N Am Benthol Soc 30(3):653–664. https://doi.org/10.1899/10-087.1
Beermann J, Dick JTA, Thiel M (2015) Social recognition in amphipods: an overview. In: Aquiloni L, Tricarico E (eds) Social recognition in invertebrates: the knowns and the unknowns. Springer International Publishing, Cham, pp 85–100. https://doi.org/10.1007/978-3-319-17599-7_6
Bianchi CN, Morri C (2000) Marine biodiversity of the Mediterranean Sea: situation, problems and prospects for future research. Mar Pollut Bull 40(5):367–376
Bielecka L, Krajewska-Sołtys A, Mudrak-Cegiołka S (2014) Spatial distribution and population characteristics of the invasive cladoceran Cercopagis pengoi in the Polish coastal zone seven years after the first record. Oceanol Hydrobiol Stud 43:201–210. https://doi.org/10.2478/s13545-014-0134-y
Bij de Vaate A, Jażdżewski K, Ketelaars HAM, Gollasch S, Van der Velde G (2002) Geographical patterns in range extension of Ponto-Caspian macroinvertebrate species in Europe. Can J Fish Aquat Sci 59:1159–1174. https://doi.org/10.1139/f02-098
Blackburn TM, Pyšek P, Bacher S, Carlton JT, Duncan RP, Jarošík V, Wilson JRU, Richardson DM (2011) A proposed unified framework for biological invasions. Trends Ecol Evol 26(7):333–339. https://doi.org/10.1016/j.tree.2011.03.023
Bohonak AJ, Jenkins DG (2003) Ecological and evolutionary significance of dispersal by freshwater invertebrates. Ecol Lett 6:783–796. https://doi.org/10.1046/j.1461-0248.2003.00486.x
Bolotov IN, Makhrov AA, Gofarov MY, Aksenova OV, Aspholm PE, Bespalaya YV, Kabakov MB, Kolosova Y, Kondakov AV, Ofenböck T, Ostrovsky AN, Popov IYu, Von Proschwitz T, Rudzīte M, Rudzītis M, Sokolova SE, Valovirta I, Vikhrev IV, Vinarski MV, Zotin AA (2018) Climate warming as a possible trigger of keystone mussel population decline in oligotrophic rivers at the continental scale. Sci Rep 8(1):35. https://doi.org/10.1038/s41598-017-18873-y
Boscolo-Galazzo F, Crichton KA, Barker S, Pearson PN (2018) Temperature dependency of metabolic rates in the upper ocean: a positive feedback to global climate change? Global Planet Change 170:201–212. https://doi.org/10.1016/j.gloplacha.2018.08.017
Bradley NL, Leopold AC, Ross J, Huffaker W (1999) Phenological changes reflect climate change in Wisconsin. Proc Natl Acad Sci USA 96:9701–9704
Briski E, Chan FT, Darling JA, Lauringson V, MacIsaac HJ, Zhan A, Bailey SA (2018) Beyond propagule pressure: importance of selection during the transport stage of biological invasions. Front Ecol Environ 16(6):345–353. https://doi.org/10.1002/fee.1820
Britannica (2022) Reproduction biology. https://www.britannica.com/science/reproduction-biology. Accessed 4 May 2022
Bruno D, Belmar O, Maire A, Morel A, Dumont B, Datry T (2019) Structural and functional responses of invertebrate communities to climate change and flow regulation in alpine catchments. Glob Change Biol 25:1612–1628. https://doi.org/10.1111/gcb.14581
Carbonell JA, Wang YJ, Stoks R (2021) Evolution of cold tolerance and thermal plasticity in life history, behaviour and physiology during a poleward range expansion. J Anim Ecol 90(7):1666–1677. https://doi.org/10.1111/1365-2656.13482
Carlton JT, Geller JB (1993) Ecological roulette: The global transport of nonindigenous marine organisms. Science 261:78–82. https://doi.org/10.1126/science.261.5117.78
Chambers MR (1977) A comparison of the population ecology of Asellus aquaticus (L.) and Asellus meridianus Rac. in the reed beds of the Tjeukemeer. Hydrobiologia 53:147–154
Chovet M, Lecureuil JY (1994) Distribution of epigean Gammaridae (Crustacea, Amphipoda) in the Loire River and in the streams of the Region Centre (France). Ann Limnol 30(1):11–23. https://doi.org/10.1051/limn/1994001
Coll M, Piroddi C, Steenbeek J, Kaschner K, Ben Rais Lasram F et al (2010) The biodiversity of the Mediterranean Sea: estimates, patterns, and threats. PLoS ONE 5(8):e11842. https://doi.org/10.1371/journal.pone.0011842
Cristescu MEA, Hebert PDN, Onciu TM (2003) Phylogeography of Ponto-Caspian crustaceans: a benthic-planktonic comparison. Mol Ecol 12(4):985–996. https://doi.org/10.1046/j.1365-294X.2003.01.801.x
Crocetta F, Bitar G, Zibrowius H, Oliverio M (2020) Increase in knowledge of the marine gastropod fauna of Lebanon since the 19th century. Bull Mar Sci 96(1):1–22. https://doi.org/10.5343/bms.2019.0012
Descouturelle G (1980) Contribution à 1'étude du contrôle de l'évolution sexuelle, de la croissance, de la mue et de leurs interactions chez la crevette d'eau douce Atyaephyra desmaresti desmaresti (Millet, 1931). PhD thesis, University of Nancy, France
DISPERSE database (2022). http://irbas.inrae.fr/latest-news/disperse-database-sarremejane-et-al-2020. Accessed 9 Mar 2022
Dobrzycka-Krahel A, Graca B (2018) Effect of salinity on the distribution of Ponto-Caspian gammarids in a non-native area—environmental and experimental study. Mar Biol Res 14(1):1–8. https://doi.org/10.1080/17451000.2017.1406666
Dobrzycka-Krahel A, Medina-Villar S (2020) Alien species of Mediterranean origin in the Baltic Sea region: current state, potential introductions and risk assessment. Environ Rev 28(3):339–356. https://doi.org/10.1139/er-2019-0074
Dobrzycka-Krahel A, Tarała A, Chabowska A (2013) Expansion of alien gammarids in the Vistula Lagoon and the Vistula Delta (Poland). Environ Monit Assess 185:5165–5175. https://doi.org/10.1007/s10661-012-2933-1
Duarte S, Fidalgo ML, Pascoal C, Cássio F (2012) The role of the freshwater shrimp Atyaephyra desmarestii in leaf litter breakdown in streams. Hydrobiologia 680:149–157. https://doi.org/10.1007/s10750-011-0912-0
Dudaniec RY, Yong CJY, Lancaster LT, Svensson EI, Hansson B (2018) Signatures of local adaptation along environmental gradients in a range-expanding damselfly (Ischnura elegans). Mol Ecol 27(11):2576–2593. https://doi.org/10.1111/mec.14709
Fanelli E, Bianchelli S, Foglini F, Canals M, Castellan G, Güell-Bujons Q, Galil B, Goren M, Evans J, Fabri M-C, Vaz S, Ciuffardi T, Schembri PJ, Angeletti L, Taviani M, Danovaro R (2021) Identifying priorities for the protection of deep Mediterranean sea ecosystems through an integrated approach. Front Mar Sci 8:698890. https://doi.org/10.3389/fmars.2021.698890
Ferreira RCF, Graça MAS, Craveiro S, Santos LMA, Culp JM (2002) Integrated environmental assessment of BKME discharged to a Mediterranean river. Water Qual Res J Can 37(1):181–193. https://doi.org/10.2166/WQRJ.2002.011
Fidalgo ML (1985) Contribution to the knowledge of the biology of Atyaephyra desmaresti Millet. Some aspects of population dynamics and energy balance (Contribuição para o conhecimento da biologia de Atyaephyra desmaresti Millet. Alguns aspectos da dinâmica populacional e do balanço energético). PhD thesis, University of Porto, Portugal
Fidalgo ML, Gerhardt A (2003) Distribution of the freshwater shrimp, Atyaephyra desmarestii (Millet, 1831) in Portugal (Decapoda, Natantia). Crustaceana 75:1375–1385. https://doi.org/10.1163/156854002321629808
Galil B, Nehring S, Panov V (2007) Waterways as invasion highways—impact of climate change and globalization. In: Nentwig W (ed) Biological invasions. Springer, Berlin, Heidelberg, pp 59–74
Gallardo B, Aldridge DC (2015) Is Great Britain heading for a Ponto-Caspian invasional meltdown? J Appl Ecol 52:41–49. https://doi.org/10.1111/1365-2664.12348
García-Berthou E, Moreno-Amich R (2000a) Food of introduced pumpkinseed sunfish: ontogenetic diet shift and seasonal variation. J Fish Biol 57:29–40. https://doi.org/10.1111/j.1095-8649.2000.tb00773.x
García-Berthou E, Moreno-Amich R (2000b) Rudd (Scardinius erythrophtalmus) introduced to the Iberian Peninsula: feeding ecology in Lake Banyoles. Hydrobiologia 436:159–164
GBIF (2021) Global Biodiversity Information Facility. https://www.gbif.org. Accessed 21 Apr 2021
Gerber L, Overgaard J (2018) Cold tolerance is linked to osmoregulatory function of the hindgut in Locusta migratoria. J Exp Biol 221:jeb173930. https://doi.org/10.1242/jeb.173930
Gergs R, Rothhaupt KO (2008) Feeding rates, assimilation efficiencies and growth of two amphipod species on biodeposited material from zebra mussels. Freshw Biol 53:2494–2503. https://doi.org/10.1111/j.1365-2427.2008.02077.x
Gherardi F (ed) (2007) Biological invaders in inland waters: profiles, distribution and threats. Springer Science Business Media B.V., Dordrecht
GISD (2021) Global invasive species database. http://www.iucngisd.org/gisd/. Accessed 21 Apr 2021
Gismondi E, Beisel JN, Cossu-Leguille C (2012) Influence of gender and season on reduced glutathione concentration and energy reserves of Gammarus roeseli. Environ Res 118:47–52. https://doi.org/10.1016/j.envres.2012.06.004
GLANSIS (2021) Great Lakes Aquatic Nonindigenous Species Information System. https://www.glerl.noaa.gov/glansis/nisListGen.php. Accessed 21 Apr 2021
Gorokhova E, Aladin N, Dumont HJ (2000) Further expansion of the genus Cercopagis (Crustacea, Branchiopoda, Onychopoda) in the Baltic Sea, with notes on the taxa present and their ecology. Hydrobiologia 429(1/3):207–218. https://doi.org/10.1023/A:1004004504571
Grabowski M, Jażdżewski K, Konopacka A (2005) Alien Crustacea in Polish waters—introduction and Decapoda. Oceanol Hydrobiol Stud 34(Suppl. 1):43–61
Grabowski M, Jażdżewski K, Konopacka A (2007) Alien Crustacea in Polish waters—Amphipoda. Aquat Invasions 2(1):25–38. https://doi.org/10.3391/ai.2007.2.1.3
Grewe Y, Hof C, Dehling DM, Brandl R, Brändle M (2013) Recent range shifts of European dragonflies provide support for an inverse relationship between habitat predictability and dispersal. Glob Ecol Biogeogr 22(4):403–409. https://doi.org/10.1111/geb.12004
GRIIS (2021) Global Register of Introduced and Invasive Species. http://www.griis.org. Accessed 21 Apr 2021
Groom QJ (2013) Some poleward movement of British native vascular plants is occurring, but the fingerprint of climate change is not evident. PeerJ 1:e77. https://doi.org/10.7717/peerj.77
Hairston NG, Cáceres CE (1996) Distribution of crustacean diapause: micro- and macroevolutionary pattern and process. Hydrobiologia 320:27–44
Hayes KR, Barry SC (2008) Are there any consistent predictors of invasion success? Biol Invasions 10:483–506. https://doi.org/10.1007/s10530-007-9146-5
Heger T, Haider S, Saul WC, Jeschke JM (2015) Species from different taxonomic groups show similar invasion traits. Immed Sci Ecol 3:1–13. https://doi.org/10.7332/ise2015.3.1.dsc
Heino J, Virkkala R, Toivonen H (2009) Climate change and freshwater biodiversity: detected patterns, future trends and adaptations in northern regions. Biol Rev 84:39–54. https://doi.org/10.1111/j.1469-185X.2008.00060.x
Hickling R, Roy DB, Hill JK, Fox R, Thomas CD (2006) The distributions of a wide range of taxonomic groups are expanding polewards. Glob Change Biol 12(3):450–455. https://doi.org/10.1111/j.1365-2486.2006.01116.x
How Animals Survive in Cold Conditions. Science of the Cold (2021) https://www.coolantarctica.com/Antarctica%20fact%20file/science/cold_all_animals.php. Accessed 29 Nov 2021
Huguet D (2015) Micromorphologie comparée de la pars molaris mandibulaire. Éthologie alimentaire en corrélation avec le mode de vie chez deux crevettes dulcicoles de la famille des Atyidés. Bull Soc Zool Fr 140(3):199–215
Iwanyzki S, McCauley RW (1992) Upper lethal temperatures of adult zebra mussels (Dreissena polymorpha). In: Nalepa TF, Schloesser DW (eds) Zebra mussels: biology, impacts, and control. Lewis Publishers, CRC Press, Boca Raton, Florida, pp 667–673
Jażdżewski K, Konopacka A (1990) New, interesting locality of the Ponto-Caspian gammarid Echinogammarus ischnus (Stebbing, 1898) (Crustacea, Amphipoda) in Poland. Przegląd Zoologiczny 34(1):101–111
Jażdżewski K, Konopacka A (1995) Crustacea, excluding land isopods (Malacostraca excl. Oniscoidea). Catalogus Faunae Poloniae 1(13):1–165
Jażdżewski K, Roux AL (1988) Biogéographie de Gammarus roeselii Gervais en Europe, en particulier répartition en France et en Pologne. Crustaceana 13(Suppl):272–277
Jeschke JM, Pyšek P (2018) Tens rule. In: Jeschke JM, Heger HT (eds) Invasion biology: hypotheses and evidence. CAB International Publisher, Wallingford, UK, pp 124–132. https://doi.org/10.1079/9781780647647.0124
Jiménez-Valverde A, Lobo JM (2011) Tolerance limits, animal. In: Simberloff D, Rejmánek M (eds) Encyclopedia of Biological Invasions. University of California Press, Berkeley and Los Angeles, pp 661–663
Johnston EL, Piola RF, Clark GF (2009) The role of propagule pressure in invasion success. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems. Ecological studies 204. Springer-Verlag, Berlin, Heidelberg, pp 133–151
Keller RP, Drake JM, Drew MB, Lodge DM (2011) Linking environmental conditions and ship movements to estimate invasive species transport across the global shipping network. Divers Distrib 17:93–102. https://doi.org/10.1111/j.1472-4642.2010.00696.x
Kemp JL, Ballot A, Nilssen JP, Spikkeland I, Eriksen TE (2020) Distribution, identification and range expansion of the common Asellidae in Northern Europe, featuring the first record of Proasellus meridianus in the Nordic countries. Fauna Norvegica 40:93–108. https://doi.org/10.5324/fn.v40i0.3353
Kititsyna LA (1980) Ecological and physiological peculiarities of Dikerogammarus haemobaphes (Eichw.) in the region of the Tripolye State Supercentral Electric Station heated water discharge. Gidrobiologicheskij Zhurnal 16:77–85
Kley A, Maier G (2003) Life history characteristics of the invasive freshwater gammarids Dikerogammarus villosus and Echinogammarus ischnus in the Main and Main-Danau canal. Arch Hydrobiol 156:457–469. https://doi.org/10.1127/0003-9136/2003/0156-0457
Kley A, Maier G (2015) An example of niche partitioning between Dikerogammarus villosus and other invasive and native gammarids: a field study. J Limnol 64(1):85–88
Kun L, Heshan L, Xuebao H, Yaqin H, Zhong L, Junhui L, Jianfeng M, Shuyi Z, Longshan L, Jianjun W, Jun S (2019) Functional trait composition and diversity patterns of marine macrobenthos across the Arctic Bering Sea. Ecol Ind 102:673–685. https://doi.org/10.1016/j.ecolind.2019.03.029
Lal Hora S (1926) Hibernation and aestivation in Gastropod Molluscs. In: Proceedings of the Zoological Society of London, pp 357–373
Lancaster LT, Dudaniec RY, Hansson B, Svensson EI (2015) Latitudinal shift in thermal niche breadth results from thermal release during a climate-mediated range expansion. J Biogeogr 42(10):1953–1963. https://doi.org/10.1111/jbi.12553
Lancaster LT, Dudaniec RY, Hansson B, Svensson EI (2017) Do group dynamics affect colour morph clines during a range shift? J Evol Biol 30(4):728–737. https://doi.org/10.1111/jeb.13037
Lencioni V (2004) Survival strategies of freshwater insects in cold environments. J Limnol 63(Suppl. 1):45–55
Lenoir J, Svenning JC (2015) Climate-related range shifts—a global multidimensional synthesis and new research directions. Ecography 38(1):15–28. https://doi.org/10.1111/ecog.00967
Lester SE, Ruttenberg BI, Gaines SD, Kinlan BP (2007) The relationship between dispersal ability and geographic range size. Ecol Lett 10:745–758. https://doi.org/10.1111/j.1461-0248.2007.01070.x
Leuven RSEW, Van der Velde G, Baijens I, Snijders J, Van den Zwart C, Lenders HJR, Bij de Vaate A (2009) The river Rhine: a global highway for dispersal of aquatic invasive species. Biol Invasions 11:1989–2008. https://doi.org/10.1007/s10530-009-9491-7
Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20:223–228. https://doi.org/10.1016/j.tree.2005.02.004
Maazouzi C, Piscart C, Legier F, Hervant F (2011) Ecophysiological responses to temperature of the “killer shrimp” Dikerogammarus villosus: Is the invader really stronger than the native Gammarus pulex? Comp Biochem Physiol Part A 159:268–274. https://doi.org/10.1016/j.cbpa.2011.03.019
Margalef R (1953) Los crustáceos de las aguas continentales ibéricas. Série Biología de las aguas continentales 10. Ministerio de Agriculture, Dirección General de Montes, Caza y Pesca Fluvial, Instituto Forestal de Investigaciones y Experiencias, Madrid, pp 1–243
May ML (2013) A critical overview of progress in studies of migration of dragonflies (Odonata: Anisoptera), with emphasis on North America. J Insect Conserv 17:1–15. https://doi.org/10.1007/s10841-012-9540-x
Mayer G, Maier G, Maas A, Waloszek D (2008) Mouthparts of the Ponto-Caspian invader Dikerogammarus villosus (Amphipoda: Pontogammaridae). J Crustac Biol 28(1):1–15. https://doi.org/10.1651/07-2867R.1
Mayer G, Maier G, Maas A, Waloszek D (2009) Mouthpart morphology of Gammarus roeselii compared to a successful invader, Dikerogammarus villosus (Amphipoda). J Crustac Biol 29(2):161–174. https://doi.org/10.1651/08-3056R.1
Mayer G, Maas A, Waloszek D (2012) Mouthpart morphology of three sympatric native and nonnative Gammaridean species: Gammarus pulex, G. fossarum, and Echinogammarus berilloni (Crustacea: Amphipoda). Int J Zool Article ID 493420:23 pp. https://doi.org/10.1155/2012/493420
Meßner U, Zettler ML (2018) The conquest (and avoidance?) of the brackish environment by Ponto-Caspian amphipods: a case study of the German Baltic Sea. BioInvasions Records 7(3):269–278. https://doi.org/10.3391/bir.2018.7.3.07
Meurisse-Génin M, Reydams-Detollenaere A, Donatti O, Micha JC (1985) Caractéristiques biologiques de la crevette d’eau douce Atyaephyra desmaresti Millet dans la Meuse. Ann Limnol 21(2):127–140. https://doi.org/10.1051/limn/1985012
Milbrink G, Timm T (2001) Distribution and dispersal capacity of the Ponto-Caspian tubificid oligochaete Potamothrix moldaviensis Vejdovský et Mrázek, 1903 in the Baltic Sea region. Hydrobiologia 463:93–102. https://doi.org/10.1023/A:1013139221454
Osland MJ, Stevens PW, Lamont MM, Brusca RC, Hart KM, Waddle JH, Langtimm CA, Williams CM, Keim BD, Terando AJ, Reyier EA, Marshall KE, Loik ME, Boucek RE, Lewis AB, Seminoff JA (2021) Tropicalization of temperate ecosystems in North America: the northward range expansion of tropical organisms in response to warming temperatures. Glob Change Biol 27(13):3009–3034. https://doi.org/10.1111/gcb.15563
Packa Tchissambou B (1979) Étude "in situ" des effets de la température sur la biologie de la crevette d'eau douce, Atyaephyra desmaresti Millet: Cas particulier du bassin de rejet de la centrale thermique de la Maxe. Thèse de 3e cycle, Université de Metz, France
Pagad S, Genovesi P, Carnevali L, Schigel D, McGeoch MA (2018) Introducing the global register of introduced and invasive species. Scientific Data 5:170202. https://doi.org/10.1038/sdata.2017.202
Patarnello T, Volckaert FAMJ, Castilho R (2007) Pillars of Hercules: is the Atlantic-Mediterranean transition a phylogeographical break? Mol Ecol 16:4426–4444. https://doi.org/10.1111/j.1365-294X.2007.03477.x
Pauli N-C, Briski E (2018) Euryhalinity of Ponto-Caspian invaders in their native and introduced regions. Aquat Invasions 13(4):439–447. https://doi.org/10.3391/ai.2018.13.4.02
Perron FE (1978) Seasonal burrowing behavior and ecology of Aporrhais occidentalis (Gastropoda: Strombacea). Biol Bull 154(3):463–471. https://doi.org/10.2307/1541072
Perry AL, Low PJ, Ellis JR, Reynolds JD (2005) Climate change and distribution shifts in marine fishes. Science 308(5730):1912–1915. https://doi.org/10.1126/science.1111322
Pinkster S (1993) A revision of the genus Echinogammarus Stebbing, 1899 with some notes on related genera (Crustacea, Amphipoda). Memorie Del Museo Civico Di Storia Naturale Di Verona (II Series) 10:1–185
Piscart C, Manach A, Copp GH, Marmonier P (2007) Distribution and microhabitats of native and non-native gammarids (Amphipoda, Crustacea) in Brittany, with particular reference to the endangered endemic sub-species Gammarus duebeni celticus. J Biogeogr 34(3):524–533. https://doi.org/10.1111/j.1365-2699.2006.01609.x
Pöckl M (1993) Beiträge zur Ökologie des Bachflohkrebses (Gammarus fossarum) und Flussflohkrebses (Gammarus roeseli). Entwicklungszyklus Und Fortpflanzungskapazität Natur Und Museum 123:114–125
Pöckl M, Humpesch UH (1990) Intra- and interspecific variations in egg survival and brood development time for Austrian populations of Gammarus fossarum and G. roeseli (Crustacea: Amphipoda). Freshw Biol 23(3):441–455. https://doi.org/10.1111/j.1365-2427.1990.tb00286.x
Pöckl M, Webb BW, Sutcliffe DW (2003) Life history and reproductive capacity of Gammarus fossarum and G. roeseli (Crustacea: Amphipoda) under naturally fluctuating water temperatures: a simulation study. Freshw Biol 48:53–66. https://doi.org/10.1046/j.1365-2427.2003.00967.x
Poznańska M, Kobak J, Wolnomiejski N, Kakareko T (2009) Shallow-water benthic macroinvertebrate community of the limnic part of a lowland Polish dam reservoir. Limnologica 39(2):163–176. https://doi.org/10.1016/j.limno.2008.10.001
Redeke HC (1936) La crevette d’eau douce, Atyaephyra desmaresti (Mill.) dans les Pays-Bas. Mémoires Du Musée Royal D’histoire Naturelle De Belgique 2:227–231
Reid DF, Orlova MI (2002) Geological and evolutionary underpinnings for the success of Ponto-Caspian species invasions in the Baltic Sea and North American Great Lakes. Can J Fish Aquat Sci 59(7):1144–1158. https://doi.org/10.1139/F02-099
Ricciardi A, Rasmussen JB (1998) Predicting the identity and impact of future biological invaders: a priority for aquatic resource management. Can J Fish Aquat Sci 55:1759–1765. https://doi.org/10.1139/f98-066
Rio CM, Karasov WH (2010) Body size and temperature: Why they matter. Nature Education Knowledge 3(10):10. https://www.nature.com/scitable/knowledge/library/body-size-and-temperature-why-they-matter-15157011/. Accessed 29 Sept 2021
Romanenko DW, Krom JG, Lekoncewa TI, Podrugina AB (2014) Resistance of gammarids Pontogammarus robustoides and Chaetogammarus ischnus (Crustacea: Amphipoda) to elevation of temperature of the aquatic medium. Hydrobiol J 50(3):55–63. https://doi.org/10.1615/HYDROBJ.V50.I3.60
Rossi AM, Saidel WM, Gravante CJ, Sayers CW, Shain DH (2016) Mechanics of cocoon secretion in a segmented worm (Annelida: Hirudinidae). Micron 86:30–35. https://doi.org/10.1016/j.micron.2016.04.004
Sarremejane R, Cid N, Stubbington R, Datry T, Alp M, Cañedo-Argüelles M, Cordero-Rivera A, Csabai Z, Gutiérrez-Cánovas C, Heino J, Forcellini M, Millán A, Paillex A, Pařil P, Polášek P, Tierno de Figueroa JM, Usseglio-Polatera P, Zamora-Muñoz C, Bonada N (2020) DISPERSE, a trait database to assess the dispersal potential of European aquatic macroinvertebrates. Scientific Data 7:386. https://doi.org/10.1038/s41597-020-00732-7
Schmidt-Drewello A, Riss HW, Scharsack JP, Meyer EI (2016) Relative benefit of the invasive Echinogammarus berilloni (Catta, 1878) over native gammarids under fish predation (Gasterosteus aculeatus Linnaeus, 1758). Aquat Ecol 50:75–85. https://doi.org/10.1007/s10452-015-9555-y
Schneider C, Laizé CLR, Acreman MC, Flörke M (2013) How will climate change modify river flow regimes in Europe? Hydrol Earth Syst Sci 17:325–339. https://doi.org/10.5194/hess-17-325-2013
Science Direct (2021) The world’s platform of peer-reviewed literature. https://www.elsevier.com
Scopus (2021) Abstract and citation database of peer-reviewed literature. https://www.scopus.com
Spidle AP, May B, Mills EL (1995) Limits to tolerance of temperature and salinity in the quagga mussel (Dreissena bugensis) and the zebra mussel (Dreissena polymorpha). Can J Fish Aquat Sci 52(10):2108–2119. https://doi.org/10.1139/f95-804
Spikkeland I, Nilssen JP, Kinsten B, Kjellberg G (2013) A new freshwater isopod Proasellus coxalis in Norway—illegal introduction due to transboundary fishing? Fauna 66(1–2):54–62
Sunday JM, Bates AE, Dulvy NK (2012) Thermal tolerance and the global redistribution of animals. Nat Clim Chang 2:686–690. https://doi.org/10.1038/nclimate1539
Sutcliffe DW (1993) Reproduction in Gammarus (Crustacea: Amphipoda): basic processes. Freshwater Forum 3:26–64
Travis JMJ, Delgado M, Bocedi G, Baguette M, Barton K, Bonte D, Boulangeat I, Hodgson JA, Kubisch A, Penteriani V, Saastamoinen M, Stevens VM, Bullock JM (2013) Dispersal and species’ responses to climate change. Oikos 122(11):1532–1540. https://doi.org/10.1111/j.1600-0706.2013.00399.x
Urban MC (2020) Climate-tracking species are not invasive. Nat Clim Chang 10(5):382–384. https://doi.org/10.1038/s41558-020-0770-8
Von Vaupel Klein JC, Schram FR (eds) (2000) The biodiversity crisis and Crustacea. In: Proceedings of the Fourth International Crustacean Congress, Amsterdam, the Netherlands, 20–24 July 1998. vol. 2. A.A. Balkema Publishers, Rotterdam (Netherlands), Brookfield (Vermont)
Vera-Vera VC, Guerrero F, Blasco J, Araújo CVM (2019) Habitat selection response of the freshwater shrimp Atyaephyra desmarestii experimentally exposed to heterogenous copper contamination scenarios. Sci Total Environ 662:816–823. https://doi.org/10.1016/j.scitotenv.2019.01.304
Vittoz P, Cherix D, Gonseth Y, Lubini V, Maggini R, Zbinden N, Zumbach S (2013) Climate change impacts on biodiversity in Switzerland: a review. J Nat Conserv 21(3):154–162. https://doi.org/10.1016/j.jnc.2012.12.002
Walther G-R, Roques A, Hulme PE, Sykes MT, Pyšek P, Kuhn I, Zobel M, Bacher S, Botta-Dukát Z, Bugmann H, Czúcz B, Dauber J, Hickler T, Jarošík V, Kenis M, Klotz S, Minchin D, Moora M, Nentwig W, Ott J, Panov VE, Reineking B, Robinet C, Semenchenko V, Solarz W, Thuiller W, Vilà M, Vohland K, Settele J (2009) Alien species in a warmer world: risks and opportunities. Trends Ecol Evol 24(12):686–693. https://doi.org/10.1016/j.tree.2009.06.008
Web of Science (2021) A platform with access to multiple databases that provide reference and citation data from academic journals, conference proceedings, and other documents in various academic disciplines. https://www.webofknowledge.com
Wertheim B, Van Baalen EJA, Dicke M, Vet LEM (2005) Pheromone-mediated aggregation in nonsocial arthropods: an evolutionary ecological perspective. Annu Rev Entomol 50:321–346. https://doi.org/10.1146/annurev.ento.49.061802.123329
Wijnhoven S, Van Riel MV, Van der Velde G (2003) Exotic and indigenous freshwater gammarid species: physiological tolerance to water temperature in relation to ionic content of the water. Aquat Ecol 37(2):151–158. https://doi.org/10.1023/A:1023982200529
Williamson MH (1996) Biological invasions. Chapman and Hall, London
Wilson RJ, Gutiérrez D, Gutiérrez J, Martínez D, Agudo R, Monserrat VJ (2005) Changes to the elevational limits and extent of species ranges associated with climate change. Ecol Lett 8:1138–1146. https://doi.org/10.1111/j.1461-0248.2005.00824.x
Wittfoth AKJ, Zettler ML (2013) The application of a biopollution index in German Baltic estuarine and lagoon waters. Manage Biol Invasions 4(1):43–50. https://doi.org/10.3391/mbi.2013.4.1.06
WORMS (2022) World Register of Marine Species. https://www.marinespecies.org/about.php
WWF/IUCN (2004) The Mediterranean deep-sea ecosystems: an overview of their diversity, structure, functioning and anthropogenic impacts, with a proposal for conservation. IUCN, Málaga and WWF, Rome
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Dobrzycka-Krahel, A., Kemp, J.L. & Fidalgo, M.L. Cold-tolerant traits that favour northwards movement and establishment of Mediterranean and Ponto-Caspian alien aquatic invertebrates. Aquat Sci 84, 47 (2022). https://doi.org/10.1007/s00027-022-00879-y
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DOI: https://doi.org/10.1007/s00027-022-00879-y