Abstract
As the number of introductions of non-indigenous species (NIS) continues to rise, ecologists are faced with new and unique opportunities to observe interactions between species that do not naturally co-exist. These interactions can have important implications on the invasion process, potentially determining whether NIS become widespread and abundant, survive in small numbers, or fail to establish and disappear. Although many studies have naturally focused on the interactions between NIS and native species to examine their effects and the biological resistance of the recipient community to invasion, few have examined the effects that NIS have on each other. In some cases, interactions can facilitate the invasion process of one or both species (i.e., “invasional meltdowns”), but competition or predation can lead to negative interactions as well. The introduction of the vase tunicate, Ciona intestinalis, in Prince Edward Island (Canada) has harmed mussel aquaculture via heavy biofouling of equipment and mussels. Through both a broad-scale survey and small-scale field experiments, we show that Ciona recruitment is drastically reduced by caprellid amphipods, including the NIS Caprella mutica. This study provides an exciting example of how established invasive species can negatively impact the recruitment of a secondary invader, highlighting the potential for non-additive effects of multiple invasions.
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References
Ashton GV (2006) Distribution and dispersal of the non-native caprellid amphipod, Caprella mutica Schurin 1935. PhD Thesis, University of Aberdeen, Scotland
Ashton GV, Willis KJ, EJ Cook (2007) Global distribution of the Japanese skeleton shrimp, Caprella mutica (Crustacea, Amphipoda, Caprellidae) with a detailed account of the distribution in Scotland, U.K. Hydrobiologia
Ashton GV, Burrows MT, Willis KJ, Cook EJ (2010) Seasonal population dynamics of the non-native Caprella mutica (Crustacea, Amphipoda) on the west coast of Scotland. Mar Freshw Res 61:549–559
Boos K (2009) Mechanisms of a successful immigration from north-east Asia: population dynamics, life history traits and interspecific interactions in the caprellid amphipod Caprella mutica Schurin, 1935 (Crustacea: Amphipoda) in European coastal waters. PhD Thesis, Freie University, Berlin
Bullard SG, Whitlatch RB (2004) A guide to the larval and juvenile stages of Long Island Sound ascidians and bryozoans. Connecticut Seagrant Publication, CTSG-04-07
Buric M, Koci L, Petrusek A, Kouba A, Kozak P (2009) Invaders eating invaders: potential trophic interactions between the amphipod Dikerogammarus villosus and juvenile crayfish Orconectes limosus. Knowl Manag Aquat Syst 5:394–395
Buschbaum C, Gutow L (2005) Mass occurrence of an introduced crustacean (Caprella cf. mutica) in the south-eastern North Sea. Helgoland Mar Res 59:252–253
Caine EA (1977) Feeding mechanisms and possible resource partitioning of the Caprellidae (Crustacea: amphipoda) from Puget Sound, USA. Mar Biol 42:331–336
Carlton JT, Geller JB (1993) Ecological roulette: the global transportation of nonindigenous marine organisms. Sci 261:78–82
Colautti RI, MacIsaac HJ (2004) A neutral terminology to define ‘invasive’ species. Divers Distrib 10:135–141
Collin SB, Edwards PK, Leung B, Johnson LE (2013) Optimizing early detection of non-indigenous species: estimating the scale of dispersal of a nascent population of the invasive tunicate Ciona intestinalis (L.). Mar Poll Bull 73:64–69
Cook EJ, Willis KJ, Lozano-Fernandez M (2007) Survivorship, growth and reproduction of the non-native Caprella mutica Schurin, 1935 (Crustacea: Amphipoda). Hydrobiologia 590:55–64
Cook EJ, Shucksmith R, Orr H, Ashton GV, Berge J (2010) Fatty acid composition as a dietary indicator of the invasive caprellid, Caprella mutica (Crustacea: Amphipoda). Mar Biol 157:19–27
Cuddington K, Hastings A (2004) Invasive engineers. Ecol Model 178:335–347
Davis AR, Butler AJ, van Altena I (1991) Settlement behaviour of ascidian larvae: preliminary evidence for inhibition by sponge allelochemicals. Mar Ecol Prog Ser 72:117–123
deRivera CE, Ruiz GM, Hines AH, Jivoff P (2005) Biotic resistance to invasion: native predator limits abundance and distribution of an introduced crab. Ecol 86:3364–3376
Dick JTA, Platvoet D (2000) Invading predatory crustacean Dikerogammarus villosus eliminates both native and exotic species. Proc R Soc B 267:977–983
Elton CS (1958) The ecology of invasions by animals and plants. The University of Chicago Press, Chicago
Epelbaum A, Pearce CM, Barker DJ, Paulson A, Therriault TW (2009) Susceptibility of non-indigenous ascidian species in British Columbia (Canada) to invertebrate predation. Mar Biol 156:1311–1320
Fagan WF, Lewis MA, Neubert MG, van den Driessche P (2002) Invasion theory and biological control. Ecol Lett 5:148–157
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
Green PT, O’Dowd DJ, Abbott KL, Jeffery M, Retalick K, MacNally R (2011) Invasional meltdown: invader–invader mutualism facilitates a secondary invasion. Ecol 92:1758–1768
Griffen BD, Guyt T, Buck JC (2008) Inhibition between invasives: a newly introduced predator moderates the impacts of a previously-established invasive predator. J Anim Ecol 77:32–40
Grosberg RK (1981) Competitive ability influences habitat choice in marine invertebrates. Nature 290:700–702
Guerra-Garcia JM (2002) Re-descriptions of Caprella linearis (Linnaeus, 1767) and C. septentrionalis Kröyer, 1838 (Crustacea: Amphipoda: Caprellidae) from Scotland, with an ontogenetic comparison between the species and a study of the clinging behaviour. Sarsia 87:216–235
Guerra-Garcia JM, Tierno de Figueroa JM (2009) What do caprellids (Crustacea: Amphipoda) feed on? Mar Biol 156:1881–1890
Heimpel GE, Frelich LE, Landis DA, Hopper KR, Hoelmer KA, Sezen Z, Asplen MK, Wu K (2010) European buckthorn and Asian soybean aphid as components of an extensive invasional meltdown in North America. Biol Invasions 12:2913–2931
Helms KR, Hayden CP, Vinson SB (2011) Plant-based food resources, trophic interactions among alien species, and the abundance of an invasive ant. Biol Invasions 13:67–79
Holmström C, Rittschof D, Kjelleberg S (1992) Inhibition of settlement by larvae of Balanus amphitrite and Ciona intestinalis by a surface-colonizing marine bacterium. Appl Environ Microbiol 58:2111–2115
Johnson LE, Strathmann RR (1989) Settling barnacle larvae avoid substrata previously occupied by a mobile predator. J Exp Mar Biol Ecol 128:87–103
Kang PA, Bae PA, Pyen CK (1978) Studies on the suspended culture of oyster, Crassostrea gigas in Korean coastal waters. 5. On the fouling organisms associated with culturing oysters at the oyster culture farms in Chungmu. Bull Fish Res Dev Agency 20:121–127
Khalaman VV, Belyaeva DV, Flyachinskaya LP (2008) Effect of excretory-secretory products of some fouling organisms on settling and metamorphosis of the larvae of Styela rustica (Ascidiae). Russ J Mar Biol 34:170–173
Kolar CS, Lodge DM (2002) Ecological predictions and risk assessment for alien fishes in North America. Science 298:1233–1236
La Pierre KJ, Harpole WS, Suding KN (2010) Strong feeding preference of an exotic generalist herbivore for an exotic forb: a case of invasional antagonism. Biol Invasions 12:3025–3031
Lafferty KD, Kuris AM (1996) Biological control of marine pests. Ecology 77:1989–2000
Leung B, Roura-Pascual N, Bacher S, Heikkila J, Brotons L, Burgman MA, Dehnen-Schmutz K, Essl F, Hulme PE, Richardson DM, Dol D, Vila M (2012) TEASIng apart alien species risk assessments: a framework for best practices. Ecol Lett 15:1475–1493
Locke A, Hanson JM, Ellis KM, Thompson J, Rochette R (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 Biol Ecol 342:69–77
Lodge DM (1993) Biological invasions: lessons for ecology. Trends Ecol Evol 8:133–137
Lodge DM, Williams S, MacIsaac HT, Hayes KR, Leung B, Richard S, Mack RN, Moyle PB, Smith M, Andow DA, Carlton JT, McMichael A (2006) Biological invasions: recommendations for U.S. policy and management. Ecol Appl 16:2035–2054
Lohrer AM, Whitlatch RB (2002) Interactions among aliens: apparent replacement of one exotic species by another. Ecol 83:719–732
Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710
McFadyen REC (1998) Biological control of weeds. Annu Rev Entomol 43:369–393
Millar RH (1958) Some ascidians from Brazil. J Nat Hist Ser 13(1):497–514
Montgomery WI, Lundy MG, Reid N (2012) ‘Invasional meltdown’: evidence for unexpected consequences and cumulative impacts of multispecies invasions. Biol Invasions 14:1111–1125
O’Dowd DJ, Green PT, Lake PS (2003) Invasional ‘meltdown’ on an oceanic island. Ecol Lett 6:812–817
Occhipinti-Ambrogi A, Savini D (2003) Biological invasions as a component of global change in stressed marine ecosystems. Mar Pollut Bull 46:542–551
Occipinti-Ambrogi A (2007) Global change and marine communities: alien species and climate change. Mar Pollut Bull 55:342–352
Osman RW, Whitlatch RB (2004) The control of the development of a marine benthic community by predation on recruits. J Exp Mar Biol Ecol 311:117–145
Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288
Platvoet D, Dick JTA, MacNeil C, van Riel MC, van der Velde G (2009) Invader-invader interactions in relation to environmental heterogeneity leads to zonation of two invasive amphipods, Dikerogammarus villosus (Sowinsky) and Gammarus tigrinus Sexton: amphipod pilot species project (AMPIS) report 6. Biol Invasions 11:2085–2093
Ramsay A, Davidson J, Bourque D, Stryhn H (2009) Recruitment patterns and population development of the invasive ascidian Ciona intestinalis in Prince Edward Island, Canada. Aquat Invasions 4:169–176
Relva MA, Nunez MA, Simberloff D (2010) Introduced deer reduce native plant cover and facilitate invasion of non-native tree species: evidence for invasional meltdown. Biol Invasions 12:303–311
Ricciardi A (2001) Facilitative interactions among aquatic invaders: is an “invasional meltdown” occurring in the Great Lakes? Can J Fish Aquat Sci 58:2513–2525
Ricciardi A, MacIsaac HJ (2000) Recent mass invasion of the North American Great Lakes by Ponto-Caspian species. Trends Ecol Evol 15:62–65
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
Ricciardi A, Whoriskey FG (2004) Exotic species replacement: shifting dominance of dreissenid mussels in the Soulanges canal, upper St. Lawrence River Canada. J N Am Benthol Soc 23:507–514
Rius M, Branch GM, Griffiths CL, Turon X (2010) Larval settlement behaviour in six gregarious ascidians in relation to adult distribution. Mar Ecol Prog Ser 418:151–163
Rius M, Potter EE, Aguirre JD, Stachowicz JJ (in press) Mechanisms of biotic resistance across complex life cycles. J Anim Ecol. doi:10.1111/1365-2656.12129
Roberts B, Davidson B, MacMaster G, Lockhart V, Ma E, Smith Wallace S, Swalla BJ (2007) A complement response may activate metamorphosis in the ascidian Boltenia villosa. Dev Genes Evol 217:449–458
Rodriguez SR, Ojeda FP, Inestrosa NC (1993) Settlement of benthic marine invertebrates. Mar Ecol Prog Ser 97:193–207
Ruiz GM, Fofonoff PW, Carlton JT, Wonham MJ, Hines AH (2000) Invasion of coastal marine communities in North America: apparent patterns, processes, and biases. Annu Rev Ecol Syst 31:481–531
Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332
Sano M, Omori M, Taniguchi K (2003) Predator-prey systems of drifting seaweed communities off the Tohoku coast, northern Japan, as determined by feeding habitat analysis of phytal animals. Fish Sci 6:260–268
Shucksmith R, Cook EJ, Hughes DJ, Burrows MT (2009) Competition between the non-native amphipod Caprella mutica and two native species of caprellids Pseudoprotella phasma and Caprella linearis. J Mar Biol Assoc UK 89:1125–1132
Simberloff D (2006) Invasional meltdown 6 years later: important phenomenon, unfortunate metaphor, or both? Ecol Lett 9:912–919
Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biol Invasions 1:21–32
Stachowicz JJ, Whitlatch RB, Osman RW (1999) Species diversity and invasion resistance in a marine ecosystem. Science 286:1577–1579
Stachowicz JJ, Fried H, Osman RW, Whitlatch RB (2002) Biodiversity, invasion resistance, and marine ecosystem function: reconciling pattern and process. Ecology 83:2575–2590
Szewzyk U, Holmström C, Wrangstadh M, Samuelsson MO, Maki JS, Kjelleberg S (1991) Relevance of exopolysaccharide of marine Pseudomonas sp. strain S9 for the attachment of Ciona intestinalis larvae. Mar Ecol Prog Ser 75:259–265
Tan CKF, Nowak BF, Hodson SL (2002) Biofouling as a reservoir of Neoparamoeba pemaquidensis (page, 1970), the causative agent of amoebic gill disease in Atlantic salmon. Aquaculture 210:49–58
Uribe E, Etchepare I (1999) Effects of biofouling by Ciona intestinalis on suspended culture of Argopecten purpuratus in Bahia Inglesa, Chile. Bull Aquac Assoc Can 102:93–95
Uygun N, Ulusoy MR, Sekeroglu E, Ohnesorge B, Gozel U (1994) Interactions between two introduced species of whiteflies in the Mediterranean area of Turkey: Dialeurodes citri (Ashmead) and Parabemisia myricae (Kuwana) (Hom., Aleyrodidae). J Appl Entomol 118:365–369
Wieczorek SB, Todd CD (1997) Inhibition of Bugula flabellata and facilitation of Ciona intestinalis settlement by natural multi-species biofilms: effects of film age and the roles of active and passive larval attachment. Mar Biol 128:463–473
Williamson M, Fitter A (1996) The varying success of invaders. Ecology 77:1661–1666
Willis KJ, Cook EJ, Lozano-Fernandez M, Takeuchi I (2004) First record of the alien caprellid amphipod, Caprella mutica, for the U.K. J Mar Biol Assoc UK 84:1027–1028
Young CM, Chia FS (1981) Laboratory evidence for delay of larval settlement in response to a dominant competitor. Int J Invertebr Reprod 3:221–226
Acknowledgments
We thank Chris McKindsey, Brian Leung and Paul Edwards for their constructive comments and thank Valerie Nearing and Maura Forrest for their assistance in the field. We also thank the Natural Sciences and Engineering Research Council (NSERC) of Canada for supporting this study through the Canadian Aquatic Invasive Species Network (CAISN) and Fisheries and Oceans Canada generally for its support of CAISN and specifically for assistance in the field. Québec-Océan and the Département de biologie of Université Laval also provided much appreciated financial and logistic support to this research.
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Collin, S.B., Johnson, L.E. Invasive species contribute to biotic resistance: negative effect of caprellid amphipods on an invasive tunicate. Biol Invasions 16, 2209–2219 (2014). https://doi.org/10.1007/s10530-014-0659-4
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DOI: https://doi.org/10.1007/s10530-014-0659-4