Abstract
Invasive fish have a high disruptive potential in aquatic ecosystems, in which amphibians may be highly impacted due to intense competition and/or predation on their eggs and larvae. Most studies have focused on the effect of large invasive fishes such as salmonids, whereas the effect of smaller fish on amphibians has been seldom investigated. We experimentally studied effects of the invasive Eastern mosquitofish (Gambusia holbrooki) on pygmy newts (Triturus pygmaeus), a species endemic to the Iberian Peninsula. We set up outdoor mesocosms in Doñana National Park with native aquatic flora and invertebrate fauna, and containing larval newts at two experimental densities. Density of larval newts was also crossed with presence or absence of mosquitofish, either free-swimming or caged, in order to distinguish consumptive and non-consumptive effects. Increased density of coexisting larval newts did not reduce their survival, but reduced their growth and development. Newt survival and size at metamorphosis were dramatically reduced in the presence of free-swimming mosquitofish, whether at low or high fish densities. Caged mosquitofish, however, had no effect on larval newts. In laboratory trials, mosquitofish preyed more efficiently on insect larvae than did larval pygmy newts, highlighting the high competitive potential of mosquitofish. This was confirmed by the depletion of zooplankton that free fish caused in the experimental outdoor mesocosms. Our study suggests that invasive mosquitofish exert a high negative impact on coexisting newt populations. Such effects can be explained by a combination of direct predation, injuries caused by predation attempts, and intense competitive exploitation of common food resources.
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References
Alemadi SD, Jenkins DG (2008) Behavioral constraints for the spread of the eastern mosquitofish, Gambusia holbrooki (Poeciliidae). Biol Invasions 10:59–66
Altwegg R, Reyer H-U (2003) Patterns of natural selection on size at metamorphosis in water frogs. Evolution 57:872–882
Baber MJ, Babbitt KJ (2003) The relative impacts of native and introduced predatory fish on a temporary wetland tadpole assemblage. Oecologia 136:289–295
Baber MJ, Babbitt KJ (2004) Influence of habitat complexity on predator-prey interactions between the fish (Gambusia holbrooki) and tadpoles of Hyla squirella and Gastrophryne carolinensis. Copeia 2004:173–177
Becker A, Laurenson LJB, Jones PL, Newman DM (2005) Competitive interactions between the Australian native fish Galaxias maculatus and the exotic mosquitofish Gambusia holbrooki, in a series of laboratory experiments. Hydrobiologia 549:187–196
Blanco S, Romo S, Villena MJ (2004) Experimental study on the diet of mosquitofish (Gambusia holbrooki) under different ecological conditions in a shallow lake. Int Rev Hydrobiol 89:250–262
Brönmark C, Hansson L-A (2005) The biology of lakes and ponds. Oxford University Press, United Kingdom
Bucciarelli GM, Blaustein AR, Garcia TS, Kats LB (2014) Invasion complexities: the diverse impacts of nonnative species on amphibians. Copeia 4:611–632
Cabral JA, Mieiro CL, Marques JC (1998) Environmental and biological factors influence the relationship between a predator fish, Gambusia holbrooki, and its main prey in rice fields of the Lower Mondego River Valley (Portugal). Hydrobiologia 382:41–51
Cabrera-Guzmán E, Crossland MR, Brown GP, Shine R (2013) Larger body size at metamorphosis enhances survival, growth and performance of young cane toads (Rhinella marina). PLoS ONE 8:e70121. doi:10.1371/journal.pone.0070121
Caiola N, de Sostoa A (2005) Possible reasons for the decline of two native toothcarps in the Iberian Peninsula: evidence of competition with the introduced Eastern mosquitofish. J Appl Ichthyol 21:358–363
Carpenter SR, Kitchell JF (1993) The trophic cascade in lakes. Cambridge University Press, New York
Carpenter SR, Kitchell JF, Hodgson JR (1985) Cascading trophic interactions and lake productivity. Bioscience 35:634–639
Chelgren ND, Rosenberg DK, Heppell SS, Gitelman AI (2006) Carryover aquatic effects on survival of metamorphic frogs during pond emigration. Ecol Appl 16:250–261
Chivers DP, Dixson DL, White JR, McCormick MI, Ferrari MCO (2013) Degradation of chemical alarm cues and assessment of risk throughout the day. Ecol Evol 3:3925–3934
Cruz MJ, Rebelo R (2005) Vulnerability of Southwest Iberian amphibians to an introduced crayfish, Procambarus clarkii. Amphibia-Reptilia 26:293–303
Denoël M, Dzukic G, Kalezic ML (2005) Effects of widespread fish introductions on paedomorphic newts in Europe. Conserv Biol 19:162–170
Denoël M, Scimè P, Zambelli N (2016) Newt life after fish introduction: extirpation of paedomorphosis in a mountain fish lake and newt use of satellite pools. Curr Zool 62:61–69
Díaz-Paniagua C (1980) Interacciones en la alimentación de las larvas de dos especies de tritones (Triturus marmoratus y Triturus boscai). Doñana Acta Vertebr 7:29–39
Díaz-Paniagua C (1989) Oviposition behavior of Triturus marmoratus pygmaeus. J Herpetol 23:159–163
Díaz-Paniagua C (1998) Reproductive dynamics of a population of small marbled newts (Triturus marmoratus pygmaeus) in South-Western Spain. Herpetol J 8:93–98
Díaz-Paniagua C, Mateo JA, Andreu AC (1996) Age and size structure of populations of small marbled newts (Triturus marmoratus pygmaeus) from Doñana National Park (SW Spain). A case of dwarfism among dwarfs. J Zool (Lond) 239:83–92
Díaz-Paniagua C, Gómez Rodríguez C, Portheault A, de Vries W (2005) Los anfibios de Doñana. Publicaciones del Organismo Autónomo de Parques Nacionales, Madrid
Díaz-Paniagua C, Fernández-Zamudio R, Florencio M, García-Murillo P, Gómez-Rodríguez C, Siljeström P, Serrano L (2010) Temporary ponds from the Doñana National Park: a system of natural habitats for the preservation of aquatic flora and fauna. Limnetica 29:41–58
Elvira B, Almodóvar A (2001) Freshwater fish introductions in Spain: facts and figures at the beginning of the 21st century. J Fish Biol 59:323–331
Ferrari MCO, Messier F, Chivers DP (2007) Degradation of chemical alarm cues under natural conditions: risk assessment by larval woodfrogs. Chemoecology 17:263–266
Fryxell DC, Arnett HA, Apgar TM, Kinnison MT, Palkovacs EP (2015) Sex ratio variation shapes the ecological effects of a globally introduced freshwater fish. Proc R Soc B 282:20151970
Gallardo B, Clavero M, Sánchez M, Vilà M (2016) Global ecological impacts of invasive species in aquatic ecosystems. Glob Change Biol 22:151–163
Gamradt SC, Kats LB (1996) Effect of introduced crayfish and mosquitofish on California Newts. Conserv Biol 10:1155–1162
García-París M (2002) Triturus pygmaeus. In: Pleguezuelos JM, Márquez R, Lizana M (eds) Atlas y libro rojo de los anfibios y Reptiles de España. Dirección General de Conservación de la Naturaleza- Asociación Herpetológica Española, Madrid, pp 70–72
Gomez-Mestre I, Díaz-Paniagua C (2011) Invasive predatory crayfish do not trigger inducible defences in tadpoles. Proc R Soc B 278:3364–3370
Gonzalo A, Cabido C, López P, Martín J (2012) Conspecific alarm cues, but not predator cues alone, determine antipredator behavior of larval southern marbled newts, Triturus pygmaeus. Acta Ethol 15:211–216
Hamer AJ, Lane SJ, Mahony MJ (2002) The role of introduced mosquitofish (Gambusia holbrooki) in excluding the native green and golden bell frog (Litoria aurea) from original habitats in south-eastern Australia. Oecologia 132:445–452
Hoffmann M, Hilton-Taylor C, Angulo A, Böhm M, Brooks TM et al (2010) The impact of conservation on the status of the world’s vertebrates. Science 330:1503–1509
Hunter DA, Smith MJ, Scroggie MP, Gilligan D (2011) Experimental examination of the potential for three introduced fish species to prey on tadpoles of the endangered Booroolong frog, Litoria booroolongensis. J Herpetol 45:181–185
Hurlbert SH, Mulla MS (1981) Impacts of mosquitofish (Gambusia affinis) predation on plankton communities. Hydrobiologia 83:125–151
Ivantsoff W, Aarn (1999) Detection of predation on Australian native fishes by Gambusia holbrooki. Mar Freshw Res 50:467–468
Kats LB, Ferrer RP (2003) Alien predators and amphibian declines: review of two decades of science and the transition to conservation. Divers Distrib 9:99–110
Keller K, Brown C (2008) Behavioural interactions between the introduced plague minnow Gambusia holbrooki and the vulnerable native Australian ornate rainbowfish Rhadinocentrus ornatus, under experimental conditions. J Fish Biol 73:1714–1729
Komak S, Crossland MR (2000) An assessment of the introduced mosquitofish (Gambusia affinis holbrooki) as a predator of eggs, hatchlings and tadpoles of native and non-native anurans. Wildl Res 27:185–189
Kottelat M, Freyhof J (2007) Handbook of European freshwater fishes. Publications Kottelat, Cornol
Kuzmin SL (1991) Food resource allocation in larval newt guilds (genus Triturus). Amphibia-Reptilia 12:293–304
Lane SJ, Mahony MJ (2002) Larval anurans with synchronous and asynchronous development periods: contrasting responses to water reduction and predator presence. J Anim Ecol 71:780–792
Lawler SP, Dritz D, Strange T, Holyoak M (1999) Effects of introduced mosquitofish and bullfrogs on the threatened California Red-legged Frog. Conserv Biol 13:613–622
Lima SL (1998) Nonlethal effects in the ecology of predator-prey interactions. What are the ecological effects of anti-predator decision-making? Bioscience 48:25–34
Margaritora FG, Ferrara O, Vagaggini D (2001) Predatory impact of the mosquitofish (Gambusia holbrooki Girard) on zooplanktonic populations in a pond at Tenuta di Castelporziano (Rome, Central Italy). J Limnol 60:189–193
Matveev V, Matveeva L, Jones GJ (1994) Phytoplankton stimulation by mosquitofish in the presence of large Daphnia. Verh Int Vere Limnol 25:2193–2197
Meffe GK (1992) Plasticity of life-history characters in eastern mosquitofish (Gambusia holbrooki: Poeciliidae) in response to thermal stress. Copeia 1992:94–102
Miaud C, Joly P, Castanet J (1993) Variation in age structures in a subdivided population of Triturus cristatus. Can J Zool 71:1874–1879
Moreno-Valcárcel R, Oliva-Paterna FJ, Arribas C, Fernández-Delgado C (2012) Length–weight relationships for 13 fish species collected in the Doñana marshlands (Guadalquivir estuary, SW Spain). J Appl Ichthyol 28:663–664
Morgan LA, Buttemer WA (1996) Predation by the non-native fish Gambusia holbrooki on small Litoria aurea and L. dentata tadpoles. Aust Zool 30:143–149
Nesbit DH, Meffe GK (1993) Cannibalism frequencies in wild populations of the eastern mosquitofish (Gambusia holbrooki: Poeciliidae) in South Carolina. Copeia 3:867–870
Orizaola G, Braña F (2003a) Response of predator-naive newt larvae to food and predator presence. Can J Zool 81:1845–1850
Orizaola G, Braña F (2003b) Do predator chemical cues affect oviposition site selection in newts? Herpetol J 13:189–193
Page LM, Burr BM (1991) A field guide to freshwater fishes: North America North of Mexico. Houghton Mifflin Company, Boston
Pilliod DS, Peterson CR (2001) Local and landscape effects of introduced trout on amphibians in historically fishless watersheds. Ecosystems 4:322–333
Polo-Cavia N, Gonzalo A, López P, Martín J (2010) Predator-recognition of native but not invasive turtle predators by naïve anuran tadpoles. Anim Behav 80:461–466
Portheault A, Díaz-Paniagua C, Gómez-Rodríguez C (2007) Predation on amphibian eggs and larvae in temporary ponds. The case of Bufo calamita in Southwestern Spain. Rev Écol (Terre Vie) 62:315–322
Preston DL, Henderson JS, Johnson PTJ (2012) Community ecology of invasions: direct and indirect effects of multiple invasive species on aquatic communities. Ecology 93:1254–1261
Pyke GH (2005) A review of the biology of Gambusia affinis and G. holbrooki. Rev Fish Biol Fish 15:339–365
Pyke GH (2008) Plague minnow or mosquito fish? A review of the biology and impacts of introduced Gambusia species. Annu Rev Ecol Evol Syst 39:171–191
Pyke GH, White AW (2000) Factors influencing predation on eggs and tadpoles of the endangered green and golden bell frog Litoria aurea by the introduced plague minnow Gambusia holbrooki. Aust Zool 31:496–505
Rehage JS, Sih A (2004) Dispersal behavior, boldness, and the link to invasiveness: a comparison of four Gambusia species. Biol Invasions 6:379–391
Rehage JS, Barnett BK, Sih A (2005) Foraging behaviour and invasiveness: do invasive Gambusia exhibit higher feeding rates and broader diets than their noninvasive relatives? Ecol Freshw Fish 14:352–360
Relyea RA (2001) The relationship between predation risk and antipredator responses in larval anurans. Ecology 82:541–554
Reques R (2014) Tritón pigmeo—Triturus pygmaeus. In: Salvador A, Martínez-Solano I (eds) Enciclopedia Virtual de los Vertebrados Españoles. Museo Nacional de Ciencias Naturales, Madrid. http://www.vertebradosibericos.org. Accesed 12 Dec 2016
Reynolds SJ (2009) Impact of the introduced poeciliid Gambusia holbrooki on amphibians in Southwestern Australia. Copeia 2009:296–302
Rincón PA, Correas AM, Morcillo F, Risueño P, Lobón-Cerviá J (2002) Interaction between the introduced eastern mosquitofish and two autochthonous Spanish toothcarps. J Fish Biol 61:1560–1585
Rowe D, Moore A, Giorgetti A, Maclean C, Grace P, Wadhwa S, Cooke J (2008) Review of the impacts of Gambusia, redfin perch, tench, roach, yellowfin goby and streaked goby in Australia. Commonwealth of Australia Publisher, Australian Government
R Core Development Team (2014) R: version 3.1.1. A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Segev O, Mangel M, Blaustein L (2009) Deleterious effects by mosquitofish (Gambusia affinis) on the endangered fire salamander (Salamandra infraimmaculata). Anim Conserv 12:29–37
Semlitsch RD, Gibbons JW (1988) Fish predation in size-structured populations of treefrog tadpoles. Oecologia 75:321–326
Shi DL, Boucaut JC (1995) The chronological development of the urodele amphibian Pleurodeles waltl (Michah). Int J Dev Biol 39:427–441
Skelly DK (1994) Activity level and the susceptibility of anuran larvae to predation. Anim Behav 47:465–468
Specziár A (2004) Life history pattern and feeding ecology of introduced eastern mosquitofish, Gambusia holbrooki, in a thermal spa under temperate climate, of Lake Hévíz, Hungary. Hydrobiologia 522:249–260
Stanback M (2010) Gambusia holbrooki predation on Pseudacris feriarum tadpoles. Herpetol Conserv Biol 5:486–489
Strayer DL (2010) Alien species in fresh waters: ecological effects, interactions with other stressors, and prospects for the future. Freshw Biol 55:152–174
US Geological Survey (2014) Nonindigenous aquatic species database. Gainesville, Florida. http://nas.er.usgs.gov/queries/FactSheet. Accessed 12 Sept 2014
Vilà M, García-Berthou E (2010) Monitoring biological invasions in freshwater habitats. In: Hurford C, Schneider M, Cowx IG (eds) Conservation monitoring in freshwater habitats: a practical guide and case studies, 1st edn. Springer, Dordrecht, pp 91–100
Wake DB (2012) Facing Extinction in real time. Science 335:1052–1053
Webb C, Joss J (1997) Does predation by the fish Gambusia holbrooki (Atheriniformes: Poeciliidae) contribute to declining frog populations? Aust Zool 30:316–324
Weihrauch F (2006) Eastern mosquitofish Gambusia holbrooki as a predator of dragonfly eggs (Teleostei: Poeciliidae; Odonata: Libellulidae). Libellula 25:209–214
Wellborn GA, Skelly DK, Werner EE (1996) Mechanisms creating community structure across a freshwater habitat gradient. Annu Rev Ecol Syst 27:337–363
Winandy L, Denoël M (2013a) Introduced Goldfish affect amphibians through inhibition of sexual behaviour in risky habitats: an experimental approach. PLoS ONE 8(11):e82736
Winandy L, Denoël M (2013b) Cues from introduced fish alter shelter use and feeding behaviour in adult Alpine Newts. Ethology 119:121–129
Winandy L, Denoël M (2015) The aggressive personality of an introduced fish affects foraging behavior in a polymorphic newt. Behav Ecol 26:1528–1536
Winandy L, Darnet E, Denoël M (2015) Amphibians forgo aquatic life in response to alien fish introduction. Anim Behav 109:209–216
Acknowledgments
We thank Lola Asencio, Rosa Arribas, Pablo Burraco, Rafael Carmona, Sara Castro, Carmen Fernández, Pilar Fernández, Ana Herrero, María León, Raquel López and Daniel Moen for help in the field or in the laboratory. The staff of the Doñana Biological Reserve provided logistical support. Financial support was provided by the Spanish Ministry of Economy and Competitiveness through the Severo Ochoa Program for Centers of Excellence in R&D&I (SEV-2012-0262, Grant SO-07), and by CONACYT (Consejo Nacional de Ciencia y Tecnología de México; postdoctoral fellowship to ECG: 204202).
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Cabrera-Guzmán, E., Díaz-Paniagua, C. & Gomez-Mestre, I. Competitive and predatory interactions between invasive mosquitofish and native larval newts. Biol Invasions 19, 1449–1460 (2017). https://doi.org/10.1007/s10530-017-1369-5
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DOI: https://doi.org/10.1007/s10530-017-1369-5