Abstract
Only a fraction of the species that are introduced succeed in the non-native environment, while others fail to survive, reproduce and/or disperse. Understanding the causes underlying each outcome is key to designing better early detection, prevention and management programs, and to deepen our knowledge of the invasion process. Here, we examine whether predator–prey interactions favor the invasion of a potentially neurotoxic mollusk in the South Western Atlantic (SWA). The grey side-gilled sea slug Pleurobranchaea maculata was recently detected in the SWA, where it has spread rapidly along the coast. In this work, we examine two hypotheses that may have driven the invasion success of P. maculata: (1) it has a high dietary plasticity, able to exploit resources in a variety of habitats within the invaded range and simultaneously (2) it lacks native predators that can control its abundance or spread. First, we identified the prey sources of P. maculata through experimental trials; then we compared its diet composition between different sites and seasons; and finally we experimentally assessed the effect of native potential predators. We found that diet composition is broad and varies in time and space, probably in relation to prey availability. Additionally, we observed that local predators do not recognize P. maculata as a prey. Probably, mechanisms underlying predator avoidance are related to the presence of chemical defenses that can be novel in the invaded environment. We propose that predator–prey interactions are key drivers favoring the establishment of non-native P. maculata via high levels of plasticity to exploit resources, the absence of biotic resistance and the increased availability of food associated with artificial substrates such as ports are probable mechanisms underlying the invasion success of this marine gastropod.
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References
Airoldi L, Bulleri F (2011) Anthropogenic disturbance can determine the magnitude of opportunistic species responses on marine urban infrastructures. PLoS ONE 6:e22985. https://doi.org/10.1371/journal.pone.0022985
Albins MA (2013) Effects of invasive Pacific red lionfish Pterois volitans versus a native predator on Bahamian coral-reef fish communities. Biol Invasions 15:29–43. https://doi.org/10.1007/s10530-012-0266-1
Albins MA, Hixon MA (2013) Worst case scenario: Potential long-term effects of invasive predatory lionfish (Pterois volitans) on Atlantic and Caribbean coral-reef communities. Environ Biol Fishes 96:1151–1157. https://doi.org/10.1007/s10641-011-9795-1
Anderson KJ (2006) Roboastra luteolineata eating Nembrotha kubaryana. Sea Slug Forum. Australian Museum, Sydney. http://www.seaslugforum.net/find/15757. Accessed 15 Nov 2017
Anderson KJ (2008) Gymnodoris rubropapulosa feeding. Sea Slug Forum. Australian Museum, Sydney. http://www.seaslugforum.net/find/20926. Accessed 15 Nov 2017
Anker A, Ivanov Y (2020) First record of the predation upon sea slugs (Cephalaspidea and Nudibranchia) by the peculiar elbow crab Lambrachaeus ramifer Alcock, 1895 (Decapoda: Parthenopidae). Mar Biodivers 50:24. https://doi.org/10.1007/s12526-020-01047-x
Arango C, Brodie GD (2003) Observations of predation on the tropical Nudibranch Okenia sp. by the sea spider Anoplodactylus longiceps Williams (Arthropoda: Pycnogonida). The Veliger 46:99–101
Avila C, Núñez-Pons L, Moles J (2018) From the tropics to the poles: chemical defensive strategies in sea slugs (Mollusca: Heterobranchia). In: Puglisi MP (ed) Chemical ecology: the ecological impacts of marine natural products. CRC Press, Boca Raton, pp 71–163
Barnes DKA, Bullough LW (1996) Some observations on the diet and distribution of Nudibranchs at Signy Island, Antarctica. J Molluscan Stud 62:281–287
Barney JN, Whitlow TH (2008) A unifying framework for biological invasions: the state factor model. Biol Invasions 10:259–272. https://doi.org/10.1007/s10530-007-9127-8
Battini N, Farías NE, Giachetti CB et al (2019) Staying aheadof invaders: can we cope with niche shifts? Mar Ecol Prog Ser 612:127–140. https://doi.org/10.3354/meps12878
Battini N (2020) Invasiones biológicas en áreas portuarias: evaluando estrategias de éxito en un molusco exótico, potencialmente neurotóxico y con alto riesgo de expansión regional. Dissertation. University of Buenos Aires.
Battini N, Bravo G (2020) Unexpected meal: first record of predation upon a potentially neurotoxic sea slug by the European green crab Carcinus maenas. New Zeal J Zool. https://doi.org/10.1080/03014223.2020.1848889
Behrens DW, Petrinos C, Schrurs C (2005) Nudibranch behavior. New World Publications Incorporated, Jacksonville
Bell JJ, Barnes DKA, Shaw C et al (2003) Seasonal “fall out” of sessile macro-fauna from submarine cliffs: Quantification, causes and implications. J Mar Biol Assoc UK 83:1199–1208. https://doi.org/10.1017/S002531540300849X
Beltramino LE, Venerus LA, Trobbiani GA et al (2019) Activity budgets for the sedentary Argentine sea bass Acanthistius patachonicus inferred from accelerometer data loggers. Austral Ecol 44:397–408. https://doi.org/10.1111/aec.12696
Bielsa LM, Labisky RF (1987) Food habits of blueline tilefish, Caulolatilus microps, and snowy grouper, Epinephelus niveatus, from the lower Florida Keys. Northeast Gulf Sci 9:77–87. https://doi.org/10.18785/negs.0902.02
Bizzarro JJ, Robinson HJ, Rinewalt CS, Ebert DA (2007) Comparative feeding ecology of four sympatric skate species off central California, USA. Environ Biol Fishes 80:197–220. https://doi.org/10.1007/s10641-007-9241-6
Blake JA, Ruff E (2007) Polychaeta. In: Carlton JT (ed) The Light and Smith manual Intertidal invertebrates from central California to Oregon, 4th edn. University of California Press, Berkeley and Los Angeles, pp 309–410
Bökenhans V, Alfaya JEF, Bigatti G, Averbuj A (2019) Diet of the invasive sea slug Pleurobranchaea maculata in Patagonian coastal waters. N Zeal J Zool 46:87–94. https://doi.org/10.1080/03014223.2018.1464035
Bonnet A (2006) Gymnodoris ceylonica eating Stylocheilus. Sea Slug Forum. Australian Museum, Sydney. http://www.seaslugforum.net/find/15912. Accessed 15 Nov 2017
Boraso de Zaixso A (2013) Elementos para el estudio de las microalgas de Argentina, 1st edn. Editorial Universitaria de la Patagonia, Comodoro Rivadavia, Chubut
Bortolus A, Carlton JT, Schwindt E (2015) Reimagining South American coasts: unveiling the hidden invasion history of an iconic ecological engineer. Divers Distrib 21:1267–1283. https://doi.org/10.1111/ddi.12377
Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–443. https://doi.org/10.1890/1540-9295(2004)002[0436:NWISAT]2.0.CO;2
Caro T, Ruxton GD (2019) Aposematism: Unpacking the defences. Trends Ecol Evol 34:595–604. https://doi.org/10.1016/j.tree.2019.02.015
Catford JA, Jansson R, Nilsson C (2009) Reducing redundancy in invasion ecology by integrating hypotheses into a single theoretical framework. Divers Distrib 15:22–40. https://doi.org/10.1111/j.1472-4642.2008.00521.x
Chuk J (2007) Dining on a dorid. Sea Slug Forum. Australian Museum, Sydney. http://www.seaslugforum.net/find/20953. Accessed 15 Nov 2017
Connell SD (2001) Urban structures as marine habitats: an experimental comparison of the composition and abundance of subtidal epibiota among pilings, pontoons and rocky reefs. Mar Environ Res 52:115–125. https://doi.org/10.1016/S0141-1136(00)00266-X
Crocetta F, Gofas S, Salas C et al (2017) Local ecological knowledge versus published literature: a review of non-indigenous mollusca in Greek marine waters. Aquat Invasions 12:415–434. https://doi.org/10.3391/ai.2017.12.4.01
Dafforn KA (2017) Eco-engineering and management strategies for marine infrastructure to reduce establishment and dispersal of non-indigenous species. Manag Biol Invasions 8:153–161. https://doi.org/10.3391/mbi.2017.8.2.03
Dafforn KA, Glasby TM, Johnston EL (2012) Comparing the invasibility of experimental “reefs” with field observations of natural reefs and artificial structures. PLoS ONE 7:e38124. https://doi.org/10.1371/journal.pone.0038124
Dales RP (1955) Feeding and digestion in terebellid polychaetes. J Mar Biol Assoc UK 34:55–79. https://doi.org/10.1017/S0025315400008614
Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534. https://doi.org/10.1046/j.1365-2745.2000.00473.x
de Vlas J (1979) Secondary production by tail regeneration in a tidal flat population of lugworms (Arenicola marina), cropped by flatfish, Netherlands. J Sea Res 13:362–393. https://doi.org/10.1016/0077-7579(79)90012-7
Dhanya AM, Jeyabaskaran R, Prema D et al (2017) Non-indigenous sea slug Tenellia adspersa in the southeast coast of the Arabian Sea, India. Curr Sci 113:24–26
Dick JTA, Alexander ME, Ricciardi A et al (2017) Functional responses can unify invasion ecology. Biol Invasions 19:1667–1672. https://doi.org/10.1007/s10530-016-1355-3
Dray S, Dufour AB, Thioulouse J (2020) Package “ade4”: Analysis of ecological data: Exploratory and euclidean methods. Version: 1.7-15. Retrieved from https://cran.r-project.org/web/packages/ade4/index.html
Enders M, Havemann F, Ruland F et al (2020) A conceptual map of invasion biology: integrating hypotheses into a consensus network. Glob Ecol Biogeogr. https://doi.org/10.1111/geb.13082
Epherra L (2016) Evaluación del impacto de invertebrados herbívoros nativos sobre el alga invasora Undaria pinnatifida: Arbacia dufresnii (Echinodermata: Echinoidea) como modelo de estudio. Dissertation, Universidad Nacional de Mar del Plata
Farías NE, Obenat S, Goya AB (2015) Outbreak of a neurotoxic side-gilled sea slug (Pleurobranchaea sp.) in Argentinian coasts. New Zeal J Zool 42:51–56. https://doi.org/10.1080/03014223.2014.990045
Farías NE, Wood SA, Obenat SM, Schwindt E (2016) Genetic barcoding confirms the presence of the neurotoxic sea slug Pleurobranchaea maculata in southwestern Atlantic coast. New Zeal J Zool 43:292–298. https://doi.org/10.1080/03014223.2016.1159582
Farías NE, Goya AB, Schwindt E et al (2019) The invasive sea slug Pleurobranchaea maculata is a vector of two potent neurotoxins in coasts of Argentina. Mar Biol 166:1–11. https://doi.org/10.1007/s00227-019-3529-x
Fincham WNW, Dunn AM, Brown LE et al (2019) Invasion success of a widespread invasive predator may be explained by a high predatory efficacy but may be influenced by pathogen infection. Biol Invasions 21:3545–3560. https://doi.org/10.1007/s10530-019-02067-w
Fofonoff PW, Ruiz GM, Steves B, Simkanin C, Carlton JT (2018) National Exotic Marine and Estuarine Species Information System. http://invasions.si.edu/nemesis/. Access Date: 5-Aug-2020
Forcelli D, Narosky T (2015) Moluscos marinos de Argentina, Uruguay y Brasil—Uruguayan seashells, 1st edn. Vázquez Mazzini, Ciudad Autónoma de Buenos Aires
Fox LR (1975) Cannibalism in natural populations. Annu Rev Ecol Syst 6:87–106. https://doi.org/10.1146/annurev.es.06.110175.000511
Galea HR, Häussermann V, Försterra G (2007) Cnidaria, Hydrozoa: latitudinal distribution of hydroids along the fjords region of southern Chile, with notes on the world distribution of some species. Check List 3:308–320. https://doi.org/10.15560/3.4.308
Genzano G, Bremec CS, Diaz Briz L et al (2017) Faunal assemblages of intertidal hydroids (Hydrozoa, Cnidaria) from Argentinean Patagonia (Southwestern Atlantic Ocean). Lat Am J Aquat Res 45:177–187. https://doi.org/10.3856/vol45-issue1-fulltext-17
Giachetti CB, Battini N, Bortolus A et al (2019) Macropredators as shapers of invaded fouling communities in a cold temperate port. J Exp Mar Bio Ecol 518:151177. https://doi.org/10.1016/j.jembe.2019.151177
Gibson GD (2003) Larval development and metamorphosis in Pleurobranchaea maculata, with a review of development in the Notaspidea (Opisthobranchia). Biol Bull 205:121–132
Glasby TM, Connell SD, Holloway MG, Hewitt CL (2007) Nonindigenous biota on artificial structures: could habitat creation facilitate biological invasions? Mar Biol 151:887–895. https://doi.org/10.1007/s00227-006-0552-5
Gribben PE, Byers JE (2020) Comparative biogeography of marine invaders across their native and introduced ranges. Oceanogr Mar Biol An Annu Rev 58:395–438
Gudgeon RI (2006) Roboastra gracilis eating Nembrotha kubaryana. Sea Slug Forum. Australian Museum, Sydney. http://www.seaslugforum.net/find/15816. Accessed 15 Nov 2017
Guiden PW, Bartel SL, Byer NW et al (2019) Predator–prey interactions in the Anthropocene: reconciling multiple aspects of novelty. Trends Ecol Evol 34:616–627. https://doi.org/10.1016/j.tree.2019.02.017
Guilford T, Cuthhill I (1991) The evolution of aposematism in marine Gastropods. Evolution 45:449–451. https://doi.org/10.1111/j.1558-5646.1991.tb04420.x
Gurevitch J, Fox GA, Wardle GM et al (2011) Emergent insights from the synthesis of conceptual frameworks for biological invasions. Ecol Lett 14:407–418. https://doi.org/10.1111/j.1461-0248.2011.01594.x
Harris LH (2006) Fish attacking Peltodoris nobilis. Sea Slug Forum. Australian Museum, Sydney. http://www.seaslugforum.net/find/17102
Häussermann V, Försterra G (eds) (2009) Fauna marina bentónica de la Patagonia chilena, 1st edn. Nature in focus, Santiago de Chile
Heger T, Pahl AT, Botta-Dukát Z et al (2013) Conceptual frameworks and methods for advancing invasion ecology. Ambio 42:527–540. https://doi.org/10.1007/s13280-012-0379-x
Hermosillo A (2002) Predation on sea slugs. Sea Slug Forum. Australian Museum, Sydney. http://www.seaslugforum.net/find/6682. Accessed 15 Nov 2017
Hewitt CL, Campbell ML, Thresher RE et al (2004) Introduced and cryptogenic species in Port Phillip Bay, Victoria, Australia. Mar Biol 144:183–202. https://doi.org/10.1007/s00227-003-1173-x
Hierro JL, Maron JL, Callaway RM (2005) A biogeographical approach to plant invasions: the importance of studying exotics in their introduced and native range. J Ecol 93:5–15. https://doi.org/10.1111/j.1365-2745.2004.00953.x
Hildering J, Miller G (2007) Cadlina luteomarginata? being eaten by a seastar. Sea Slug Forum. Australian Museum, Sydney. http://www.seaslugforum.net/find/20125. Accessed 15 Nov 2017
Holloway MG, Connell SD (2002) Why do floating structures create novel habitats for subtidal epibiota? Mar Ecol Prog Ser 235:43–52. https://doi.org/10.3354/meps235043
Horst D (2009) Re: Thuridilla hopei under predation attack. Sea Slug Forum. Australian Museum, Sydney. http://www.seaslugforum.net/find/22520. Accessed 15 Nov 2017
IPBES (2019) Summary for policymakers of the global assessment report on biodiversity and ecosystem services of the intergovernmental science-policy platform on biodiversity and ecosystem services. In: Díaz S, Settele J, Brondízio ES et al (eds) IPBES secretariat. Bonn, Germany, p 56
Irigoyen AJ, Galván DE, Venerus LA, Parma AM (2013) Variability in abundance of temperate reef fishes estimated by visual census. PLoS ONE 8:e61072. https://doi.org/10.1371/journal.pone.0061072
Itoi S, Yoshikawa S, Asahina K et al (2014) Larval pufferfish protected by maternal tetrodotoxin. Toxicon 78:35–40. https://doi.org/10.1016/j.toxicon.2013.11.003
Jeschke JM (2014) General hypotheses in invasion ecology. Divers Distrib 20:1229–1234. https://doi.org/10.1111/ddi.12258
Jeschke JM, Gómez Aparicio L, Haider S et al (2012) Support for major hypotheses in invasion biology is uneven and declining. NeoBiota 14:1–20. https://doi.org/10.3897/neobiota.14.3435
Johnson S (1999a) Feeding & breeding in Gymnodoris ceylonica. Sea Slug Forum. Australian Museum, Sydney. http://www.seaslugforum.net/find/1289. Accessed 15 Nov 2017
Johnson S (1999b) Feeding behaviour in Gymnodoris striata. Sea Slug Forum. Australian Museum, Sydney. http://www.seaslugforum.net/find/1369. Accessed 15 Nov 2017
Johnson S (2000) Cannibalism in Gymnodoris citrina. Sea Slug Forum. Australian Museum, Sydney. http://www.seaslugforum.net/find/1319. Accessed 15 Nov 2017
Keppel E, Sigovini M, Tagliapietra D (2012) A new geographical record of Polycera hedgpethi Er. Marcus, 1964 (Nudibranchia: Polyceridae) and evidence of its established presence in the Mediterranean Sea, with a review of its geographical distribution. Mar Biol Res 8:969–981. https://doi.org/10.1080/17451000.2012.706306
Khor S, Wood SA, Salvitti L et al (2013) Development of a non-lethal biopsy technique for estimating total tetrodotoxin concentrations in the grey side-gilled sea slug Pleurobranchaea maculata. Toxicon 74:27–33. https://doi.org/10.1016/j.toxicon.2013.07.024
Kirkendale L (2006) Aplysia juliana eaten by Flatworm. Sea Slug Forum. Australian Museum, Sydney. http://www.seaslugforum.net/find/16272. Accessed 15 Nov 2017
Koh DB (2005a) Aplysia parvula - eaten by Nemertine worm. Sea Slug Forum. Australian Museum, Sydney. http://www.seaslugforum.net/find/13659. Accessed 15 Nov 2017
Koh (2005b) Aplysia juliana being eaten by crab. Sea Slug Forum. Australian Museum, Sydney. http://www.seaslugforum.net/find/13926. Accessed 15 Nov 2017
Koh DB (2006) Predator of nudibranchs - again. Sea Slug Forum. Australian Museum, Sydney. http://www.seaslugforum.net/find/17404. Accessed 15 Nov 2017
Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Ecol Evol 16:199–204. https://doi.org/10.1016/S0169-5347(01)02101-2
Kremer LP, da Rocha RM (2016) The biotic resistance role of fish predation in fouling communities. Biol Invasions 18:3223–3236. https://doi.org/10.1007/s10530-016-1210-6
Kuroe S, Mada A (2007) A case of Caphira yoodokai eating Tritoniopsis elegans. Sea Slug Forum. Australian Museum, Sydney. http://www.seaslugforum.net/find/20129. Accessed 15 Nov 2017
Lichtschein de Bastida V, Bastida R (1980) Los briozoos de las comunidades incrustantes de Puertos argentinos. In: 5th international congress on marine corrosion fouling, pp 371–390
Llewelyn J, Schwarzkopf L, Phillips BL, Shine R (2014) After the crash: how do predators adjust following the invasion of a novel toxic prey type? Austral Ecol 39:190–197. https://doi.org/10.1111/aec.12058
Locke A, Hanson JM, Ellis KM et al (2007) Invasion of the southern Gulf of St. Lawrence by the clubbed tunicate (Styela clava Herdman): potential mechanisms for invasions of Prince Edward Island estuaries. J Exp Mar Bio Ecol 342:69–77. https://doi.org/10.1016/j.jembe.2006.10.016
Loury EK (2011) Diet of the Gopher rockfish (Sebastes carnatus) inside and outside of marine protected areas in Central California. Dissertation, San José State University
Mack RN, Simberloff D, Lonsdale WM et al (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710
Martel C, Guarini JM, Blanchard G et al (2004) Invasion by the marine gastropod Ocinebrellus inornatus in France. III. Comparison of biological traits with the resident species Ocenebra erinacea. Mar Biol 146:93–102. https://doi.org/10.1007/s00227-004-1421-8
Martynov AV, Korshunova TA, Grintsov VA (2007) Opisthobranch molluscs of the Northern Black Sea. I. Short history of studies and the first record of a non-indigenous nudibranch species Trinchesia perca (Er. Marcus, 1958) (Nudibranchia: Tergipedidae). Ruthenica 17:43–54
McNabb PS, Selwood A, Munday R et al (2010) Detection of tetrodotoxin from the grey side-gilled sea slug—Pleurobranchaea maculata, and associated dog neurotoxicosis on beaches adjacent to the Hauraki Gulf, Auckland, New Zealand. Toxicon 56:466–473. https://doi.org/10.1016/j.toxicon.2010.04.017
Moksnes PO (2004) Self-regulating mechanisms in cannibalistic populations of juvenile shore crabs Carcinus maenas. Ecology 85:1343–1354. https://doi.org/10.1890/02-0750
Mollo E, Gavagnin M, Carbone M et al (2008) Factors promoting marine invasions: a chemoecological approach. Proc Natl Acad Sci USA 105:4582–4586. https://doi.org/10.1073/pnas.0709355105
Moltschaniwskyj NA, Hall K, Lipinski MR et al (2007) Ethical and welfare considerations when using cephalopods as experimental animals. Rev Fish Biol Fish 17:455–476. https://doi.org/10.1007/s11160-007-9056-8
Monniot, C., Monniot, F., Laboute, P., 1991. Coral reef Ascidians of New Caledonia. IRD Editions.
Muniain CM (2001) Taxonomical and ecological aspects of the Nudibranch Geitodoris patagonica Odhner, 1926 (Opisthobranchia, Doridina) from Argentina. Boll Malacol 37:171–176
Narahashi T (2001) Pharmacology of tetrodotoxin. J Toxicol Toxin Rev 20:67–84. https://doi.org/10.1081/TXR-100102537
Ogden CM (2008) Nembrotha aurea being eaten by Robostra luteolineata. Sea Slug Forum. Australian Museum, Sydney. http://www.seaslugforum.net/find/21526. Accessed 15 Nov 2017
Oksanen J, Blanchet FG, Friendly M et al (2019) Package “vegan”: Community ecology package. Version 2.5-4. Retrieved from https://cran.r-project.org/web/packages/vegan/index.html
Orensanz JM, Bortolus A, Darrigran GA et al (2002) No longer the pristine confines of the world ocean: a survey of exotic marine species in the southwestern Atlantic. Biol Invasions 4:115–143
Ottaway JR (1977) Pleurobranchaea novaezelandiae praying on Actinia tenebrosa. New Zeal J Mar Freshw Res 11:125–130. https://doi.org/10.1080/00288330.1977.9515665
Papalardo OL, Battini N (2019) Primer caso de posible intoxicación canina por neurotoxinas de la babosa de mar moteada (Pleurobranchaea maculata) en Puerto Madryn. Rev los Colegios Vet Patagónicos 42:19–22
Pejchar L, Mooney HA (2009) Invasive species, ecosystem services and human well-being. Trends Ecol Evol 24:497–504. https://doi.org/10.1016/j.tree.2009.03.016
Piel WH (1991) Pycnogonid predation on nudibranchs and ceratal autotomy. The Veliger 34:366–367
Pinheiro J, Bates D, DebRoy S et al (2018) Package “nlme”: Linear and nonlinear mixed effects models. Version 3.1-137. Retrieved from https://cran.r-project.org/web/packages/nlme/index.html
Polner A, Paul VJ, Scheuer PJ (1989) Kumepaloxane, a rearranged trisnor sesquiterpene from the bubble shell Haminoea cymbalum. Tetrahedron 45:617–622. https://doi.org/10.1016/0040-4020(89)80089-4
Pyšek P, Richardson DM (2010) Invasive species, environmental change and management, and health. Annu Rev Environ Resour 35:25–55. https://doi.org/10.1146/annurev-environ-033009-095548
R Core Team (2020) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. http://www.R-project.org/
Rechimont M, Galván DE, Sueiro MCM et al (2013) Benthic diversity and assemblage structure of a north Patagonian rocky shore: a monitoring legacy of the NaGISA project. J Mar Biol Assoc UK 93:1–10. https://doi.org/10.1017/S0025315413001069
Richards CL, Bossdorf O, Muth NZ, Gurevitch J, Pigliucci M (2006) Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecol Lett 9:981–993. https://doi.org/10.1111/j.1461-0248.2006.00950.x
Rivas AL, Ripa P (1989) Variación estacional de la estructura termo-halina de Golfo Nuevo, Argentina. Geofis Int 28:3–24
Roberts M (2005) 1000s of Sea Hares in Hawaii. Sea Slug Forum. Australian Museum, Sydney. http://www.seaslugforum.net/find/14074. Accessed 15 Nov 2017
da Rocha RM, Zanata TB, Moreno TR (2012) Keys for the identification of families and genera of Atlantic shallow water ascidians. Biota Neotrop 12:269–303. https://doi.org/10.1590/s1676-06032012000100022
Rogers C (2001) Pycnogonids - Sea Slug predators. Sea Slug Forum. Australian Museum, Sydney. http://www.seaslugforum.net/find/3407. Accessed 15 Nov 2017
Rogers CN, de Nys R, Steinberg PD (2000) Predation on juvenile Aplysia parvula and other small anaspidean, ascoglossan, and nudibranch Gastropods by Pycnogonids. The Veliger 43:330–337. https://doi.org/10.18941/venusjjma.21.1_118_2
Rogers TL, Byrnes JE, Stachowicz JJ (2016) Native predators limit invasion of benthic invertebrate communities in Bodega Harbor, California, USA. Mar Ecol Prog Ser 545:161–173. https://doi.org/10.3354/meps11611
Roig-Juñent S, Claps LE, Morrone JJ (eds) (2014) Biodiversidad de artrópodos argentinos, vol 3, 1st edn. Editorial INSUE-UNT, San Miguel de Tucumán, Tucumán, Argentina
Rojas-Vélez S, Tavera J, Acero A (2019) Unraveling lionfish invasion: Is Pterois volitans truly a morphologically novel predator in the Caribbean? Biol Invasions 21:1921–1931. https://doi.org/10.1007/s10530-019-01946-6
Roll U, Dayan T, Simberloff D, Mienis HK (2009) Non-indigenous land and freshwater gastropods in Israel. Biol Invasions 11:1963–1972. https://doi.org/10.1007/s10530-008-9373-4
Rosas-Luis R, Jiménez Badillo M de L, Montoliu-Elena L, Morillo-Velarde PS (2019) Food and feeding habits of Octopus insularis in the Veracruz Reef System National Park and confirmation of its presence in the southwest Gulf of Mexico. Mar Ecol. https://doi.org/10.1111/maec.12535
Salvitti L, Wood SA, Winsor L, Cary S (2015) Intracellular Immunohistochemical Detection of Tetrodotoxin in Pleurobranchaea maculata (Gastropoda) and Stylochoplana sp. (Turbellaria). Mar Drugs 13:756–769. https://doi.org/10.3390/md13020756
Saul W-C, Jeschke JM, Heger T (2013) The role of eco-evolutionary experience in invasion success. NeoBiota 17:57–74. https://doi.org/10.3897/neobiota.17.5208
Schwindt E, Battini N, Giachetti CB et al (2018) Especies exóticas marino-costeras de Argentina, Primera. Vázquez Mazzini Editores, Buenos Aires
Schwindt E, Carlton JT, Orensanz JM et al (2020) Past and future of the marine bioinvasions along the Southwestern Atlantic. Aquat Invasions 15:11–29
Schwindt E, López Gappa J, Raffo MP et al (2014) Marine fouling invasions in ports of Patagonia (Argentina) with implications for legislation and monitoring programs. Mar Environ Res 99:60–68. https://doi.org/10.1016/j.marenvres.2014.06.006
Sher AA, Hyatt LA (1999) The disturbed resource-flux invasion matrix: a new framework for patterns of plant invasion. Biol Invasions 1:107–114. https://doi.org/10.1023/A:1010050420466
Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: Invasional meltdown? Biol Invasions 1:21–32. https://doi.org/10.1023/a:1010086329619
Simberloff D, Martin JL, Genovesi P et al (2013) Impacts of biological invasions: What’s what and the way forward. Trends Ecol Evol 28:58–66. https://doi.org/10.1016/j.tree.2012.07.013
Silva JP (2008) Spurilla neapolitana predator. Sea Slug Forum. Australian Museum, Sydney. http://www.seaslugforum.net/find/21086. Accessed 15 Nov 2017
Taylor DI, Wood SA, McNabb PS (2011) Population surveys of Pleurobranchaea maculata and tetrodotoxin in Waitemata Harbour. Report prepared to the Auckland Council. Nelson, New Zealand.
Taylor DI, Wood SA, McNabb PS et al (2015) Facilitation effects of invasive and farmed bivalves on native populations of the sea slug Pleurobranchaea maculata. Mar Ecol Prog Ser 537:39–48. https://doi.org/10.3354/meps11466
Thompson TE (1969) Acid secretion in the Pacific Ocean gastropods. Aust J Zool 17:755–764. https://doi.org/10.1071/ZO9690755
Toh CH (2008) Re: Gymnodoris rubropapulosa feeding. Sea Slug Forum. Australian Museum, Sydney. http://www.seaslugforum.net/find/21510. Accessed 15 Nov 2017
Trowbridge CD (1991) Diet specialization limits herbivorous sea slug’s capacity to switch among food species. Ecology 72:1880–1888. https://doi.org/10.2307/1940985
Trowbridge CD (1994) Defensive responses and palatability of specialist herbivores: predation on NE Pacific ascoglossan gastropods. Mar Ecol Prog Ser 105:61–70. https://doi.org/10.3354/meps105061
Valdés Á, Blanchard L, Marti W (2013) Caught naked: first report a Nudibranch Sea Slug Attacked by a Cone Snail. Am Malacol Bull 31:337–338. https://doi.org/10.4003/006.031.0213
van Kleunen M, Dawson W, Schlaepfer DR et al (2010) Are invaders different? A conceptual framework of comparative approaches for assessing determinants of invasiveness. Ecol Lett 13:947–958. https://doi.org/10.1111/j.1461-0248.2010.01503.x
Vitousek PM, D'Antonio CM, Loope LL et al (1997) Introduced species: a significant component of Human-caused global environmental change: the scope and distribution of invasions. New Zeal J Ecol 21:1–16
Wacasey J, Atkinson E (1987) Energy values of marine benthic invertebrates from the Canadian Arctic. Mar Ecol Prog Ser 39:243–250. https://doi.org/10.3354/meps039243
Wägele H (1989) Diet of some Antarctic nudibranchs (Gastropoda, Opisthobranchia, Nudibranchia). Mar Biol 100:439–441. https://doi.org/10.1007/BF00394819
Wägele H, Ballesteros M, Avila C (2006) Defensive glandular structures in Opisthobranch molluscs—from histology to ecology. Oceanogr Mar Biol 44:197–276. https://doi.org/10.1201/9781420006391.ch5
Willan RC (1984) A review of diets in the Notaspidea (Mollusca: Opisthobranchia). J Malacol Soc Aust 6:125–142. https://doi.org/10.1080/00852988.1984.10673965
Williams BL (2010) Behavioral and chemical ecology of marine organisms with respect to tetrodotoxin. Mar Drugs 8:381–398. https://doi.org/10.3390/md8030381
Woodin SA (1982) Browsing: Important in marine sedimentary environments? Spionid polychaete examples. J Exp Mar Bio Ecol 60:35–45. https://doi.org/10.1016/0022-0981(81)90178-7
Wright WG (2006) Navanax - Aplysia interactions. Sea Slug Forum. Australian Museum, Sydney. http://www.seaslugforum.net/find/16251. Accessed 15 Nov 2017
Yamamori K, Nakamura M, Matsui T, Hara TJ (1988) Gustatory responses to tetrodotoxin and saxitoxin in fish: A possible mechanism for avoiding marine toxins. Can J Fish Aquat Sci 45:2182–2186. https://doi.org/10.1139/f88-253
Yang M-S, Nelson MW (1999) Food habits of the commercially important groundfishes in the Gulf of Alaska in 1990, 1993, and 1996
Yorisue T, Ellrich JA, Momota K (2019) Mechanisms underlying predator-driven biotic resistance against introduced barnacles on the Pacific coast of Hokkaido, Japan. Biol Invasions 21:2345–2356. https://doi.org/10.1007/s10530-019-01980-4
Zajac RN (1995) Sublethal predation on Polydora cornuta (Polychaeta: Spionidae): patterns of tissue loss in a field population, predator functional response and potential demographic impacts. Mar Biol 123:531–541. https://doi.org/10.1007/BF00349232
Zajac RN (1985) The effects of sublethal predation on reproduction in the spionid polychaete Polydora ligni Webster. J Exp Mar Bio Ecol 88:1–19. https://doi.org/10.1016/0022-0981(85)90197-2
Zar JH (2010) Biostatistical analysis, 5th edn. Prentice-Hall Inc, Englewood Cliffs
Zeileis A, Cribari-Neto F, Gruen B et al (2018) Package “betareg”: Beta regression. Version 3.1–1. Retrieved from https://cran.r-project.org/web/packages/betareg/index.html
Zenni RD, Nuñez MA (2013) The elephant in the room: the role of failed invasions in understanding invasion biology. Oikos 122:801–815. https://doi.org/10.1111/j.1600-0706.2012.00254.x
Acknowledgements
We are grateful to Ramiro Braga (IBIOMAR-CONICET, Argentina), Guillermo Gutiérrez (IDEAus-CONICET, Argentina), Gastón Trobbiani, Alejo Irigoyen, Lucas Beltramino (CESIMAR-CONICET, Argentina), Néstor Ortiz, Facundo Yrigoyen, Fabián Quiroga and Ricardo “Bebo” Vera (CONICET-CENPAT, Argentina) for their assistance in the field and to Mariano Moris, Angelina Gorosito (directors of the Servicio de Acuario Experimental (SAE) in CONICET-CENPAT, Argentina) and Nicolás Ortiz (IBIOMAR-CONICET, Argentina) for their assistance with the aquarium setup and experiments. We also thank María Emilia Diez (IBIOMAR-CONICET, Argentina) and Ximena González-Pisani (CESIMAR-CONICET, Argentina) for their advice with taxonomical identification and to Alejo Irigoyen for the illustrations of the fish. Finally, we are grateful to Francisco Sylvester, Paul Gribben and two anonymous reviewers for their valuable advice and constructive comments on earlier versions of the manuscript. This research was partially funded by PADI Foundation (#21773 to N.B.); CONICET (PIP 20130100508) and ANPCyT (PICT P. BID No. 2016-1083) to E.S. and A.B. N.B., C.B.G. and K.L.C. are supported by a Doctoral Fellowship from CONICET. This work is part of the doctoral thesis of N.B.
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All authors contributed to the study conception and design. Experimental setup and aquarium maintenance were performed by Nicolás Battini and Clara Belen Giachetti. Sample preparation and processing was performed by Nicolás Battini and Karen Lidia Castro. Statistical analyses and the first draft of the manuscript were written by Nicolás Battini, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Battini, N., Giachetti, C.B., Castro, K.L. et al. Predator–prey interactions as key drivers for the invasion success of a potentially neurotoxic sea slug. Biol Invasions 23, 1207–1229 (2021). https://doi.org/10.1007/s10530-020-02431-1
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DOI: https://doi.org/10.1007/s10530-020-02431-1