Abstract
Effects caused by the invasive American bullfrog (Lithobates catesbeianus) are poorly understood at the community level. This study assessed the effects of a small feral bullfrog population (at lag invasion phase) on the different components of native aquatic communities (phytoplankton, zooplankton, invertebrates, fish and amphibians) of Aceguá, Uruguay. Our interest focused on exploring the early local effects of this invasion. We explored whether there existed any difference in taxa richness, abundances and size structure in association to bullfrog invasion, using four seasonal sampling of all the lentic system around the foci (two invaded and five non-invaded ponds). We analysed the occurrence of differences between the invaded and the non-invaded communities: for the taxa richness we used rarefaction, for the abundances and body sizes we used mean tests, and for the tadpole developmental stages we used G-test. We only found statistically significant bullfrog effects, in fish and anuran larvae. The fish assemblage was favoured, reaching greater abundance and body size in the bullfrog invaded ponds. In these ponds, the nektonic tadpoles diminished their abundances, and the benthic tadpoles also reached greater body sizes, but decreasing their recruitment. Our results suggest that bullfrog invasion could have complex effects, acting asymmetrically, affecting different trophic paths, and depending on native species’ habits and attributes. Understanding these effects, in early invasion foci, has a great relevance to awareness of local environmental authorities and the implementation of management plans.
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References
Adams MJ (2000) Pond permanence and the effects of exotic vertebrates on anurans. Ecol Appl 10:559–568. https://doi.org/10.1890/1051-0761(2000)010[0559:PPATEO]2.0.CO;2
Adams M, Pearl C (2007) Problems and opportunities managing invasive bullfrogs: is there any hope? In: Gherardi F (ed) Biological invaders in inland waters: profiles, distribution, and threats. Springer, Netherlands, pp 679–693
Adams MJ, Pearl CA, Bruce Bury R (2003) Indirect facilitation of an anuran invasion by non-native fishes. Ecol Lett 6:343–351. https://doi.org/10.1046/j.1461-0248.2003.00435.x
Altig R, Johnston GF (1989) Guilds of anuran larvae: relationships among developmental modes, morphologies, and habitats. Herpetol Monogr 3:81–109. https://doi.org/10.2307/1466987
Arim M, Abades SR, Laufer G et al (2010) Food web structure and body size: trophic position and resource acquisition. Oikos 119:147–153. https://doi.org/10.1111/j.1600-0706.2009.17768.x
Babbitt KJ, Tanner GW (1998) Effects of cover and predator size on survival and development of Rana utricularia tadpoles. Oecologia 114:258–262. https://doi.org/10.1007/s004420050444
Babbitt KJ, Baber MJ, Tarr TL (2003) Patterns of larval amphibian distribution along a wetland hydroperiod gradient. Can J Zool 81:1539–1552. https://doi.org/10.1139/z03-131
Batista M, Silva M, Barreto C (2015) Effects of introduction and decline of a bullfrog population (Lithobates catesbeianus) in a community of amphibians in the Cerrado from Central Brazil. Herpetol Notes 8:263–265
Baxter CV, Fausch KD, Murakami M, Chapman PL (2004) Fish invasion restructures stream and forest food webs by interrupting reciprocal prey subsidies. Ecology 85:2656–2663. https://doi.org/10.1890/04-138
Bellard C, Genovesi P, Jeschke JM (2016) Global patterns in threats to vertebrates by biological invasions. Proc R Soc B 283:20152454. https://doi.org/10.1098/rspb.2015.2454
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
Boelter RA, Cechin SZ (2007) Impact of the bullfrog diet (Lithobates catesbeianus-Anura, Ranidae) on native fauna: case study from the region of Agudo-RS-Brazil. Nat Conserv 5:115–123
Boone MD, Little EE, Semlitsch RD (2004) Overwintered bullfrog tadpoles negatively affect salamanders and anurans in native amphibian communities. Copeia. https://doi.org/10.1643/CE-03-229R1
Both C, Melo AS (2015) Diversity of anuran communities facing bullfrog invasion in Atlantic forest ponds. Biol Invasions 17:1137–1147. https://doi.org/10.1007/s10530-014-0783-1
Both C, Kaefer ÍL, Santos TG, Cechin ST (2008) An austral anuran assemblage in the Neotropics: seasonal occurrence correlated with photoperiod. J Nat Hist 42:205–222. https://doi.org/10.1080/00222930701847923
Both C, Solé M, dos Santos TG, Cechin SZ (2009) The role of spatial and temporal descriptors for neotropical tadpole communities in southern Brazil. Hydrobiologia 624:125–138. https://doi.org/10.1007/s10750-008-9685-5
Brazeiro A (2015) Eco-regiones de Uruguay: Biodiversidad, presiones y conservación. Aportes a la estrategia nacional de biodiversidad. Facultad de Ciencias, CIEDUR, VS-Uruguay, SZU, Montevideo
Bwanika GN, Chapman LJ, Kizito Y, Balirwa J (2006) Cascading effects of introduced Nile perch (Lates niloticus) on the foraging ecology of Nile tilapia (Oreochromis niloticus). Ecol Freshw Fish 15:470–481. https://doi.org/10.1111/j.1600-0633.2006.00185.x
Chao A, Jost L (2012) Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology 93:2533–2547. https://doi.org/10.1890/11-1952.1
Clavero M, Garcia-Berthou E (2005) Invasive species are a leading cause of animal extinctions. Trends Ecol Evol 20:110–110. https://doi.org/10.1016/j.tree.2005.01.003
Crooks JA (2005) Lag times and exotic species: the ecology and management of biological invasions in slow-motion. Ecoscience 12:316–329. https://doi.org/10.2980/i1195-6860-12-3-316.1
Duxbury C, Holland J, Pluchino M (2010) Experimental evaluation of the impacts of the invasive catfish Hoplostemum littorale (Hancock, 1828) on aquatic macroinvertebrates. Aquat Invasions 5:97–102. https://doi.org/10.3391/ai.2010.5.1.11
Echeverría DD, Volpedo AV, Mascitti VI (2007) Diet of tadpoles from a pond in Iguazu National Park, Argentina. Gayana 71:8–15
Entsminger GL (2012) EcoSim professional: null modeling software for ecologists, v 1. Acquired Intelligence Inc., Kesey-Bear. and Pinyon Publishing, Montrose
Garner TW, Perkins MW, Govindarajulu P et al (2006) The emerging amphibian pathogen Batrachochytrium dendrobatidis globally infects introduced populations of the North American bullfrog, Rana catesbeiana. Biol Lett 2:455–459. https://doi.org/10.1098/rsbl.2006.0494
Garner TWJ, Walker S, Bosch J et al (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
Gobel N, Cortizas S, Mautone JM et al (2013) Predation of Pseudis Minuta Günther 1858, by Lethocerus annulipes (Heteroptera: Belostomatidae). Cuad Herpetol 27:63–63
Gobel N, Laufer G, Serra WS (in press) Density, body size and diet overlap of four fish species in artificial reservoirs in the Pampas, Uruguay. North West J Zool e171401
Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190
Havel JE, Kovalenko KE, Thomaz SM, Amalfitano S, Kats LB (2015) Aquatic invasive species: challenges for the future. Hydrobiologia 750:147–170. https://doi.org/10.1007/s10750-014-2166-0
Hecnar SJ, M’Closkey RT (1997) The effects of predatory fish on amphibian species richness and distribution. Biol Conserv 79:123–131. https://doi.org/10.1016/S0006-3207(96)00113-9
Hirai T (2004) Diet composition of introduced bullfrog, Rana catesbeiana in the Mizorogaike pond of Kyoto, Japan. Ecol Res 19:375–380. https://doi.org/10.1111/j.1440-1703.2004.00647.x
Jancowski K, Orchard S (2013) Stomach contents from invasive American bullfrogs Rana catesbeiana (= Lithobates catesbeianus) on southern Vancouver island. B C Can NeoBiota 16:17–37. https://doi.org/10.3897/neobiota.16.3806
Jara F, Perotti M (2010) Risk of predation and behavioural response in three anuran species: influence of tadpole size and predator type. Hydrobiologia 644:313–324. https://doi.org/10.1007/s10750-010-0196-9
Kiesecker JM, Blaustein AR (1997a) Effects of introduced bullfrogs and smallmouth bass on microhabitat use, growth, and survival of sative red-legged frogs (Rana aurora). Conserv Biol 12:776–787. https://doi.org/10.1111/j.1523-1739.1998.97125.x
Kiesecker JM, Blaustein AR (1997b) Population differences in responses of red-legged frogs (Rana aurora) to introduced bullfrogs. Ecology 78:1752–1760. https://doi.org/10.1890/0012-9658(1997)078[1752:PDIROR]2.0.CO;2
Kiesecker JM, Blaustein AR, Miller CL (2001) Potential mechanisms underlying the displacement of native red-legged frogs by introduced bullfrogs. Ecology 82:1964–1970. https://doi.org/10.1890/0012-9658(2001)082[1964:PMUTDO]2.0.CO;2
Kottek M, Grieser J, Beck C, Rudolf B, Rubel F (2006) World map of the Köppen-Geiger climate classification updated. Meteorol Z 15:259–263. https://doi.org/10.1127/0941-2948/2006/0130
Kraus F (2009) Alien reptiles and amphibians A scientific compendium and analysis. Springer, Berlin
Kupferberg SJ (1997) Bullfrog (Rana catesbeiana) Invasion of a California river: the role of larval competition. Ecology 78:1736–1751. https://doi.org/10.1890/0012-9658(1997)078[1736:BRCIOA]2.0.CO;2
Lajmanovich RC (1997) Alimentación de larvas de anuros en ambientes temporales del sistema del río Paraná, Argentina. Doñana Acta Vertebr 24:191–202
Laufer G, Gobel N (2017) Habitat degradation and biological invasions as a cause of amphibian richness loss: a case report in Aceguá, Cerro Largo, Uruguay. Phyllomedusa 16:289–293. https://doi.org/10.11606/issn.2316-9079.v16i2p289-293
Laufer G, Canavero A, Núñez D, Maneyro R (2008) Bullfrog (Lithobates catesbeianus) invasion in Uruguay. Biol Invasions 10:1183–1189. https://doi.org/10.1007/s10530-007-9178-x
Laufer G, Piñeiro-Guerra JM, Pereira-Garbero R et al (2009) Distribution extension of Scinax aromothyella (Anura, Hylidae). Biota Neotrop 9:275–278. https://doi.org/10.1590/S1676-06032009000200028
Laufer G, Gobel N, Borteiro C, Soutullo A, Martinez-Debat C, de Sá RO (2018) Current status of American bullfrog, Lithobates catesbeianus, invasion in Uruguay and exploration of chytrid infection. Biol Invasions 20:285–291. https://doi.org/10.1007/s10530-017-1540-z
Legendre P, Legendre LF (1998) Numerical ecology, 2nd edn. Elsevier, Amsterdam
Leivas PT, Leivas FWT, Moura MO (2012) Diet and trophic niche of Lithobates catesbeianus (Amphibia: Anura). Zool Curitiba 29:405–412. https://doi.org/10.1590/S1984-46702012000500003
Leivas PT, Savaris M, Lampert S, Lucas EM (2013) Predation of Odontophrynus americanus (Anura: Odontophrynidae) by the invasive species Lithobates catesbeianus (Anura: Ranidae) in an Araucaria forest remnant in Southern Brazil. Herpetol Notes 6:603–606
Li Y, Ke Z, Wang Y, Blackburn T (2011) Frog community responses to recent American bullfrog invasions. Curr Zool 57:83–92. https://doi.org/10.1093/czoolo/57.1.83
Lowe S, Browne M, Boudjelas S, De Poorter M (2000) 100 of the world’s worst invasive alien species: a selection from the global invasive species database. Invasive Species Specialist Group, Auckland
Maezono Y, Miyashita T (2003) Community-level impacts induced by introduced largemouth bass and bluegill in farm ponds in Japan. Biol Conserv 109:111–121. https://doi.org/10.1016/S0006-3207(02)00144-1
Meerhoff M, Clemente JM, Teixeira de Mello F, Iglesias C, Pedersen AR, Jeppesen E (2007) Can warm climate-related structure of littoral predator assemblies weaken the clear water in shallow lake? Glob Change Biol 13:1888–1897. https://doi.org/10.1111/j.1365-2486.2007.01408.x
Moreira LFB, Machado IF, Lace ARGM, Maltchik L (2007) Calling period and reproductive modes in an anuran community of a temporary pond in southern Brazil. S Am J Herpet 2:129–135. https://doi.org/10.2994/1808-9798(2007)2[129:CPARMI]2.0.CO;2
Mugnai R, Nessimian JL, Baptista DF (2010) Manual de identificação de macroinvertebrados aquáticos do estado do Rio de Janeiro: para atividades técnicas, de ensino e treinamento em programas de avaliação da qualidade ecológica dos ecossistemas lóticos. Technical Books Editora, São Paulo
Parker IM, Simberloff D, Lonsdale WM, Goodell K, Wonham M, Kareiva PM, Williamson MH, Von Holle B, Moyle PB, Byers JE, Goldwasser L (1999) Impact: Toward a framework for understanding the ecological effects of invaders. Biol Invasions 1:3–19. https://doi.org/10.1023/A:1010034312781
Pearl CA, Adams MJ, Bury RB, McCreary B (2004) Asymmetrical effects of introduced bullfrogs (Rana catesbeiana) on native ranid frogs in Oregon. Copeia 2004:11–20. https://doi.org/10.1643/CE-03-010R2
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. https://doi.org/10.1016/j.anbehav.2010.06.004
Porej D, Hetherington TE (2005) Designing wetlands for amphibians: the importance of predatory fish and shallow littoral zones in structuring of amphibian communities. Wetl Ecol Manag 13:445–455. https://doi.org/10.1007/s11273-004-0522-y
Prigioni C, Borteiro C, Kolenc F (2011) Amphibia and reptilia, Quebrada de los Cuervos, departamento de Treinta y Tres, Uruguay. Check List 7:763–767. https://doi.org/10.15560/11021
Puth LM, Post DM (2005) Studying invasion: have we missed the boat? Ecol Lett 8:715–721. https://doi.org/10.1111/j.1461-0248.2005.00774.x
Pyšek P, Richardson DM, Pergl J, Jarošík V, Sixtová Z, Weber E (2008) Geographical and taxonomic biases in invasion ecology. Trends Ecol Evol 23:237–244. https://doi.org/10.1016/j.tree.2008.02.002
Quiroga LB, Moreno MD, Cataldo AA et al (2015) Diet composition of an invasive population of Lithobates catesbeianus (American bullfrog) from Argentina. J Nat Hist 49:1703–1716. https://doi.org/10.1080/00222933.2015.1005711
R Core Team (2015) R: a language and environment for statistical computing. R Foundation for statistical computing, Vienna. http://www.R-project.org. Accessed 20 Feb 2018
Relyea RA (2007) Getting out alive: how predators affect the decision to metamorphose. Oecologia 152:389–400. https://doi.org/10.1007/s00442-007-0675-5
Rodewald AD (2012) Spreading messages about invasives. Divers Distrib 18:97–99. https://doi.org/10.1111/j.1472-4642.2011.00817.x
Rodriguez LF (2006) Can invasive species facilitate native species? Evidence of how, when, and why these impacts occur. Biol Invasions 8:927–939. https://doi.org/10.1007/s10530-005-5103-3
Ruibal M, Laufer G (2012) Bullfrog Lithobates catesbeianus (Amphibia: Ranidae) tadpole diet: description and analysis for three invasive populations in Uruguay. Amphib Reptil 33:355–363. https://doi.org/10.1163/15685381-00002838
Sala OE, Chapin FS, Iii et al (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774. https://doi.org/10.1126/science.287.5459.1770
Santana DJ, de Medeiros Magalhães F, de Avelar V, Mângia S, Amado TF, Garda AA (2016) Calls and tadpoles of the species of Pseudis (Anura, Hylidae, Pseudae). Herpetol J 26:139–151
Schiesari L, Werner EE, Kling GW (2009) Carnivory and resource-based niche differentiation in anuran larvae: implications for food web and experimental ecology. Freshw Biol 54:572–586. https://doi.org/10.1111/j.1365-2427.2008.02134.x
Semlitsch RD, Peterman WE, Anderson TL, Drake DL, Ousterhout BH (2015) Intermediate pond sizes contain the highest density, richness, and diversity of pond-breeding amphibians. Plos One 10:e0123055. https://doi.org/10.1371/journal.pone.0123055
Silva ETD, Reis EPD, Feio RN, Filho OPR (2009) Diet of the invasive frog Lithobates catesbeianus (Shaw, 1802) (Anura: Ranidae) in Viçosa, Minas Gerais state, Brazil. South Am J Herpetol 4:286–294. https://doi.org/10.2994/057.004.0312
Simberloff D (2004) Community ecology: is it time to move on? (An American Society of Naturalists Presidential Address). Am Nat 163:787–799. https://doi.org/10.1086/420777
Simberloff D (2014) Biological invasions: what’s worth fighting and what can be won? Ecol Eng 65:112–121. https://doi.org/10.1016/j.ecoleng.2013.08.004
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
Smith GR, Burgett AA, Temple KG, Sparks KA (2016) Differential effects of bluegill sunfish (Lepomis macrochirus) on two fish-tolerant species of tadpoles (Anaxyrus americanus and Lithobates catesbeianus). Hydrobiologia 773:77–86. https://doi.org/10.1007/s10750-016-2680-3
Sokal RR, Rohlf FJ (2009) Introduction to biostatistics, 2nd edn. Dover Publications, New York
Speziale KL, Lambertucci SA, Carrete M, Tella JL (2012) Dealing with non-native species: what makes the difference in South America? Biol Invasions 14:1609–1621. https://doi.org/10.1007/s10530-011-0162-0
Teixeira de Mello F, González-Bergonzoni I, Loureiro M (2011) Peces de agua dulce de Uruguay. PPR-MGAP, Montevideo
Townsend CR (2003) Individual, population, community, and ecosystem consequences of a fish invader in New Zealand streams. Conserv Biol 17:38–47. https://doi.org/10.1046/j.1523-1739.2003.02017.x
White EM, Wilson JC, Clarke AR (2006) Biotic indirect effects: a neglected concept in invasion biology. Divers Distrib 12:443–455. https://doi.org/10.1111/j.1366-9516.2006.00265.x
Wiser SK, Allen RB, Clinton PW, Platt KH (1998) Community structure and forest invasion by an exotic herb over 23 years. Ecology 79:2071–2081. https://doi.org/10.1890/0012-9658(1998)079[2071:CSAFIB]2.0.CO;2
Wu Z, Li Y, Wang Y, Adams MJ (2005) Diet of introduced bullfrogs (Rana catesbeiana): predation on and diet overlap with native frogs on Daishan island, China. J Herpetol 39:668–674. https://doi.org/10.1670/78-05N.1
Ziegler L, Maneyro R (2008) Clave para la identificación de los anfibios de Uruguay (Chordata: Amphibia). Universidad de la República, Montevideo
Acknowledgements
GL and NG thank the Agencia Nacional de Investigación e Innovación (ANII) (POS_NAC_2015_1_109517) and the Programa de Desarrollo de las Ciencias Básicas (PEDECIBA), Uruguay, for their postgraduate grants. GL is a member of the Sistema Nacional de Investigadores (SNI), Uruguay. NG and SC thank the ANII for the Beca de Iniciación. We all thank the support of the Rufford Foundation and the local habitants of the studied sites for their contributions during fieldwork. All the used animal welfare protocols were authorized by the National Commission for Animal Experimentation, Museo Nacional de Historia Natural (Code 013/11).
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Gobel, N., Laufer, G. & Cortizas, S. Changes in aquatic communities recently invaded by a top predator: evidence of American bullfrogs in Aceguá, Uruguay. Aquat Sci 81, 8 (2019). https://doi.org/10.1007/s00027-018-0604-1
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DOI: https://doi.org/10.1007/s00027-018-0604-1