Abstract
Aquatic invaders often cause severe declines of native amphibian populations, either through competition, predation and/or alterations of the habitat. Such situation has raised additional concerns for the persistence of endemic species exhibiting rare and alternative phenotypes. Here, we experimentally assessed the impact of the invasive mosquitofish (Gambusia holbrooki) on adult newts (Lissotriton graecus) exhibiting paedomorphosis, the retention of larval traits such as gills, making them fully aquatic. Mosquitofish had a negative impact on paedomorphic newts by inducing both behavioral and phenotypic changes. Paedomorphic newts exhibited avoidance behavior and higher metamorphosis rates in the presence of fish. Both female and male newts responded by decreasing mobility and foraging activity. Females stopped investing in egg-laying in presence of fish and males metamorphosed earlier than females. Hence, our results show that mosquitofish introductions, particularly in areas with populations exhibiting paedomorphosis, might have detrimental consequences on the preservation of alternative developmental pathways. Both behavioral and phenotypic effects should be assessed to understand the impacts of introduced species.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. arXiv preprint arXiv:1406.5823
Beebee TJ, Griffiths RA (2005) The amphibian decline crisis: A watershed for conservation biology? Biol Conserv 125:271–285. https://doi.org/10.1016/j.biocon.2005.04.009
Blaustein AR, Kiesecker JM (2002) Complexity in conservation: lessons from the global decline of amphibian populations. Ecol Lett 5:597–608. https://doi.org/10.1046/j.1461-0248.2002.00352.x
Bowatte G, Perera P, Senevirathne G, Meegaskumbura S, Meegaskumbura M (2013) Tadpoles as dengue mosquito (Aedes aegypti) egg predators. Biol Control 67:469–474. https://doi.org/10.1016/j.biocontrol.2013.10.005
Bridges CM (2002) Tadpoles balance foraging and predator avoidance: effects of predation, pond drying, and hunger. J Herpetol 36:627–634
Brown TR, Coleman RA, Swearer SE, Hale R (2018) Behavioral responses to, and fitness consequences from, an invasive species are life-stage dependent in a threatened native fish. Biol Conserv 228:10–16. https://doi.org/10.1016/j.biocon.2018.10.003
Byers JE, Wright JT, Gribben PE (2010) Variable direct and indirect effects of a habitat-modifying invasive species on mortality of native fauna. Ecology 91:1787–1798. https://doi.org/10.1890/09-0712.1
Cabrera-Guzmán E, Díaz-Paniagua C, Gomez-Mestre I (2017) Competitive and predatory interactions between invasive mosquitofish and native larval newts. Biol Invasions 19:1449–1460. https://doi.org/10.1007/s10530-017-1369-5
Cabrera-Guzmán E, Díaz-Paniagua C, Gomez-Mestre I (2018) Invasive mosquitofish (Gambusia holbrooki) affect egg-laying and behaviour of Spanish pygmy newts (Triturus pygmaeus). Amphibia-Reptilia 40:103–112. https://doi.org/10.1163/15685381-20181019
Cadotte MW, Drake JA, Fukami T (2005) Constructing nature: Laboratory models as necessary tools for investigating complex ecological communities. Adv Ecol Res 37:333–353. https://doi.org/10.1016/S0065-2504(04)37011-X
Chelini M-C, Willemart RH, Hebets EA (2009) Costs and benefits of freezing behaviour in the harvestman Eumesosoma roeweri (Arachnida, Opiliones). Behav Process 82:153–159. https://doi.org/10.1016/j.beproc.2009.06.001
Cote J, Fogarty S, Weinersmith K, Brodin T, Sih A (2010) Personality traits and dispersal tendency in the invasive mosquitofish (Gambusia affinis). Proc R Soc B Biol Sci 277:1571–1579. https://doi.org/10.1098/rspb.2009.2128
Council of the European Union (2010) Protection of animals used for scientific purposes (2010/63/EU). Off J Eur Union 276:33–79
Cruz MJ, Rebelo R, Crespo EG (2006) Effects of an introduced crayfish, Procambarus clarkii, on the distribution of south-western Iberian amphibians in their breeding habitats. Ecography 29:329–338. https://doi.org/10.1111/j.2006.0906-7590.04333.x
Denoël M (2012) Newt decline in Western Europe: highlights from relative distribution changes within guilds. Biodivers Conserv 21:2887–2898. https://doi.org/10.1007/s10531-012-0343-x
Denoël M (2017) On the identification of paedomorphic and overwintering larval newts based on cloacal shape: review and guidelines. Curr Zool 63:165–173. https://doi.org/10.1093/cz/zow054
Denoël M, Winandy L (2015) The importance of phenotypic diversity in conservation: Resilience of palmate newt morphotypes after fish removal in Larzac ponds (France). Biol Conserv 192:402–408. https://doi.org/10.1016/j.biocon.2015.10.018
Denoël M, Joly P, Whiteman HH (2005) Evolutionary ecology of facultative paedomorphosis in newts and salamanders. Biol Rev 80:663–671. https://doi.org/10.1017/S1464793105006858
Denoël M, Ficetola GF, Sillero N et al (2019a) Traditionally managed landscapes do not prevent amphibian decline and the extinction of paedomorphosis. Ecol Monogr 89:e01347. https://doi.org/10.1002/ecm.1347
Denoël M, Drapeau L, Oromi N, Winandy L (2019b) The role of predation risk in metamorphosis versus behavioural avoidance: a sex-specific study in a facultative paedomorphic amphibian. Oecologia 189:637–645. https://doi.org/10.1007/s00442-019-04362-8
Denoël M, Drapeau L, Winandy L (2019c) Reproductive fitness consequences of progenesis: sex-specific payoffs in safe and risky environments. J Evol Biol 32:629–637. https://doi.org/10.1111/JEB.13449
Durant SE, Hopkins WA (2008) Amphibian predation on larval mosquitoes. Can J Zool 86:1159–1164. https://doi.org/10.1139/Z08-097
El-Sabaawi RW, Frauendorf TC, Marques PS, Mackenzie RA, Manna LR, Mazzoni R, Philip DAT, Warbanski M, Zandona E (2016) Biodiversity and ecosystem risks arising from using guppies to control mosquitoes. Biol Lett 12:20160590. https://doi.org/10.1098/rsbl.2016.0590
Ficetola FG, Siesa ME, Manenti R, Bottoni L, De Bernardi F, Padoa-Schioppa E (2011) Early assessment of the impact of alien species: differential consequences of an invasive crayfish on adult and larval amphibians. Divers Distrib 17:1141–1151. https://doi.org/10.1111/j.1472-4642.2011.00797.x
Fraser LH, Keddy P (1997) The role of experimental microcosms in ecological research. Trends Ecol Evol 12:478–481
Friard O, Gamba M (2016) BORIS: a free, versatile open-source event-logging software for video/audio coding and live observations. Methods Ecol Evol 7:1325–1330. https://doi.org/10.1111/2041-210X.12584
Funk JL, Vitousek PM (2007) Resource-use efficiency and plant invasion in low-resource systems. Nature 446:1079–1081. https://doi.org/10.1038/nature05719
García-Berthou E (1999) Food of introduced mosquitofish: ontogenetic diet shift and prey selection. J Fish Biol 55:135–147. https://doi.org/10.1111/j.1095-8649.1999.tb00663.x
Garner TW, Walker S, Bosch J, Leech S, Marcus Rowcliffe J, Cunningham AA, Fisher MC (2009) Life history tradeoffs influence mortality associated with the amphibian pathogen Batrachochytrium dendrobatidis. Oikos 118:783–791. https://doi.org/10.1111/j.1600-0706.2008.17202.x
Halliday T (1974) Sexual behaviour of the smooth newt, Triturus vulgaris (Urodela, Salamandridae). J Herpetol 8:277–292
Halliday T (1990) The evolution of courtship behavior in newts and salamanders. Adv Stud Behav 19:137–169. https://doi.org/10.1016/S0065-3454(08)60202-8
Hartel T, Nemes S, Cogălniceanu D, Öllerer K, Schweiger O, Moga C-I, Demeter L (2007) The effect of fish and aquatic habitat complexity on amphibians. Hydrobiologia 583:173–182. https://doi.org/10.1007/s10750-006-0490-8
Joseph MB, Piovia-Scott J, Lawler SP, Pope KL (2011) Indirect effects of introduced trout on Cascades frogs (Rana cascadae) via shared aquatic prey. Freshw Biol 56:828–838. https://doi.org/10.1111/j.1365-2427.2010.02529.x
Lejeune B, Sturaro N, Lepoint G, Denoël M (2018) Facultative paedomorphosis as a mechanism promoting intraspecific niche differentiation. Oikos 127:427–439. https://doi.org/10.1111/oik.04714
Lenth RV (2016) Least-squares means: the R package lsmeans. J Stat Softw 69:1–33
Liden WH, Phillips ML, Herberholz J (2010) Neural control of behavioural choice in juvenile crayfish. Proc R Soc B Biol Sci 277:3493–3500. https://doi.org/10.1098/rspb.2010.1000
Magellan K, García-Berthou E (2016) Experimental evidence for the use of artificial refugia to mitigate the impacts of invasive Gambusia holbrooki on an endangered fish. Biol Invasions 18:873–882. https://doi.org/10.1007/s10530-016-1057-x
Malacarne G, Giacoma C (1986) Chemical signals in European newt courtship. Boll Zool 53:79–83. https://doi.org/10.1080/11250008609355487
Mathiron AG, Lena J-P, Baouch S, Denoël M (2017) The ‘male escape hypothesis’: sex-biased metamorphosis in response to climatic drivers in a facultatively paedomorphic amphibian. Proc R Soc B 284:20170176. https://doi.org/10.1098/rspb.2017.0176
Mills MD, Rader RB, Belk MC (2004) Complex interactions between native and invasive fish: the simultaneous effects of multiple negative interactions. Oecologia 141:713–721. https://doi.org/10.1007/s00442-004-1695-z
Orizaola G, Brana F (2006) Effect of salmonid introduction and other environmental characteristics on amphibian distribution and abundance in mountain lakes of northern Spain. Anim Conserv 9:171–178. https://doi.org/10.1111/j.1469-1795.2006.00023.x
Pyke GH (2005) A review of the biology of Gambusia affinis and G. holbrooki. Rev Fish Biol Fish 15:339–365. https://doi.org/10.1007/s11160-006-6394-x
Pyke GH (2008) Plague minnow or mosquitofish? A review of the biology and impacts of introduced Gambusia species. Annu Rev Ecol Evol Syst 39:171–191. https://doi.org/10.1146/annurev.ecolsys.39.11070.173451
R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 10 Dec 2018
Raffel TR, Michel PJ, Sites EW, Rohr JR (2010) What drives chytrid infections in newt populations? Associations with substrate, temperature, and shade. EcoHealth 7:526–536. https://doi.org/10.1007/s10393-010-0358-2
Remon J, Bower DS, Gaston TF, Clulow J, Mahony MJ (2016) Stable isotope analyses reveal predation on amphibians by a globally invasive fish (Gambusia holbrooki). Aquat Conserv 26:724–735. https://doi.org/10.1002/aqc.2631
Scrimgeour GJ, Culp JM (1994) Feeding while evading predators by a lotic mayfly: linking short-term foraging behaviours to long-term fitness consequences. Oecologia 100:128–134. https://doi.org/10.1007/BF00317139
Semlitsch R (1987) Interactions between fish and salamander larvae. Oecologia 72:481–486. https://doi.org/10.1007/BF00378972
Shulse CD, Semlitsch RD, Trauth KM (2013) Mosquitofish dominate amphibian and invertebrate community development in experimental wetlands. J Appl Ecol 50:1244–1256. https://doi.org/10.1111/1365-2664.12126
Skelly DK, Werner EE (1990) Behavioral and life-historical responses of larval American toads to an odonate predator. Ecology 71:2313–2322. https://doi.org/10.2307/1938642
Sotiropoulos K, Moustakas K, Konstantinidis K, Mantzana-Oikonomaki V, Siarabi S, Bounas A (2017) First record of facultative pedomorphosis in the Macedonian crested newt (Triturus macedonicus) and an additional record of Greek smooth newt (Lissotriton vulgaris) from Greece: implications of species conservation and preservation of alternative ontogenetic trajectories. Herpetol Notes 10:255–260
Stauffer H-P, Semlitsch RD (1993) Effects of visual, chemical and tactile cues of fish on the behavioural responses of tadpoles. Anim Behav 46:355–364. https://doi.org/10.1006/anbe.1993.1197
Stynoski JL, Noble VR (2012) To beg or to freeze: multimodal sensory integration directs behavior in a tadpole. Behav Ecol Sociobiol 66:191–199. https://doi.org/10.1007/s00265-011-1266-3
Therneau TM, Lumley T (2015) Package ‘survival’. R Top Doc 128:112
Vannini A, Bruni G, Ricciardi G, Platania L, Mori E, Tricarico E (2018) Gambusia holbrooki, the ‘tadpolefish’: the impact of its predatory behaviour on four protected species of European amphibians. Aquat Conserv 28:476–484. https://doi.org/10.1002/aqc.2880
Vidal O, García-Berthou E, Tedesco PA, García-Marín JL (2010) Origin and genetic diversity of mosquitofish (Gambusia holbrooki) introduced to Europe. Biol Invasions 12:841–851. https://doi.org/10.1007/s10530-009-9505-5
Walther G-R, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin JM, Hoegh-Gildberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395. https://doi.org/10.1038/416389a
Whiteman HH (1994) Evolution of facultative paedomorphosis in salamanders. Q Rev Biol 69:205–221. https://doi.org/10.1086/418540
Wielstra B, Canestrelli D, Cvijanović M, Denoël M, Fijarczyk A, Jablonski D, Liana M, Naumov B, Olgun K, Pabijan M, Pezzarossa A, Popgeorgiev G, Salvi D, Si Y, Sillero N, Sotiropoulos K, Zieliński P, Babik W (2018) The distributions of the six species constituting the smooth newt species complex (Lissotriton vulgaris sensu lato and L. montandoni)—an addition to the New Atlas of Amphibians and Reptiles of Europe. Amphibia-Reptilia 39:252–259. https://doi.org/10.1163/15685381-17000128
Wilbur HM (1980) Complex life cycles. Ann Rev Ecol Syst 11:67–93
Winandy L, Denoël M (2013a) Cues from introduced fish alter shelter use and feeding behaviour in adult alpine newts. Ethology 119:121–129. https://doi.org/10.1111/eth.12043
Winandy L, Denoël M (2013b) Introduced goldfish affect amphibians through inhibition of sexual behaviour in risky habitats: an experimental approach. PloS ONE 8:e82736. https://doi.org/10.1371/journal.pone.0082736
Winandy L, Denoël M (2015) The aggressive personality of an introduced fish affects foraging behavior in a polymorphic newt. Behav Ecol 26:1528–1536. https://doi.org/10.1093/beheco/arv101
Winandy L, Darnet E, Denoël M (2015) Amphibians forgo aquatic life in response to alien fish introduction. Anim Behav 109:209–216. https://doi.org/10.1016/j.anbehav.2015.08.018
Winandy L, Legrand P, Denoël M (2017) Habitat selection and reproduction of newts in networks of fish and fishless aquatic patches. Anim Behav 123:107–115. https://doi.org/10.1016/j.anbehav.2016.10.027
Acknowledgements
We are thankful to Dr. Juha Merilä and Dr. Konstantinos Adamidis for their valuable comments on a previous version of the manuscript. We thank the Editor and two Reviewers for constructive comments and suggestions. This research was co-financed by Greece and the European Union (European Social Fund-ESF) through the Operational Programme “Human Resources Development, Education and Lifelong Learning” in the context of the project “Strengthening Human Resources Research Potential via Doctorate Research” (MIS-5000432), implemented by the State Scholarships Foundation (ΙΚΥ) to E.T. M.D. is a Research Director at Fonds de la Recherche Scientifique—FNRS.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
The experiments were approved by the Hellenic Ministry of the Environment & Energy under a special permit (code: 6ΦΠΘ4653Π8-ΑΟΤ), and all used methods were carried out in accordance with approved guidelines.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Toli, E.A., Chavas, C., Denoël, M. et al. A subtle threat: behavioral and phenotypic consequences of invasive mosquitofish on a native paedomorphic newt. Biol Invasions 22, 1299–1308 (2020). https://doi.org/10.1007/s10530-019-02181-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-019-02181-9