Different time patterns of the presence of red-eared slider influence the ontogeny dynamics of common frog tadpoles
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
35552438
PubMed Central
PMC9098440
DOI
10.1038/s41598-022-11561-6
PII: 10.1038/s41598-022-11561-6
Knihovny.cz E-zdroje
- MeSH
- biologická proměna MeSH
- larva MeSH
- predátorské chování * MeSH
- Rana temporaria MeSH
- žáby MeSH
- želvy * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
The coexistence of species in a given community depends on the set of species involved and the timing of their interactions. Many native communities are increasingly forced to face both direct and indirect pressures from new alien predators, which, in extreme cases, can lead to the extinction of prey populations. In this study, we examine the dynamics of the ontogeny of common frog (Rana temporaria) tadpoles under different time patterns of an alien predator-the red-eared slider (Trachemys scripta elegans) presence. We found that the tadpoles had a longer larval period and were smaller in size at metamorphosis and lower in body mass when the predator was present in early development than when the tadpoles developed without a predator. The early presence of a predator conspicuously reduced the growth increments of the tadpoles at early development. After the removal of the predator, growth accelerated above the level measured under the conditions of both the late predator and no predator. However, these growth rates did not exceed the growth rates of equally sized tadpoles in the other treatments and therefore were not sufficient to compensate for the growth slowdown in the first part of development. The presence of a predator in late tadpole development influenced neither the time to metamorphosis nor size/body mass at metamorphosis. In conclusion, the predator had the effect on metamorphosis traits only if it was present in the early development of tadpoles.
Zobrazit více v PubMed
Gerber BD, Karpanty SM, Randrianantenaina J. Activity patterns of carnivores in the rain forests of Madagascar: Implications for species coexistence. J. Mammal. 2012;93:667–676. doi: 10.1644/11-MAMM-A-265.1. DOI
Azevedo F, Lemos F, Freitas-Junior M, Rocha D, Azevedo F. Puma activity patterns and temporal overlap with prey in a human-modified landscape at Southeastern Brazil. J. Zool. 2018;305:246–255. doi: 10.1111/jzo.12558. DOI
Wellborn GA, Skelly DK, Werner EE. Mechanisms creating community structure across a freshwater habitat gradient. Annu. Rev. Ecol. Syst. 1996;27:337–363. doi: 10.1146/annurev.ecolsys.27.1.337. DOI
Sitvarin MI, Rypstra AL, Harwood JD. Linking the green and brown worlds through nonconsumptive predator effects. Oikos. 2016;125:1057–1068. doi: 10.1111/oik.03190. DOI
Damien M, Tougeron K. Prey–predator phenological mismatch under climate change. Curr. Opin. Insect Sci. 2019;35:60–68. doi: 10.1016/j.cois.2019.07.002. PubMed DOI
Relyea RA, Werner EE. Quantifying the relation between predator-induced behavior and growth performance in larval anurans. Ecology. 1999;80:2117–2124. doi: 10.1890/0012-9658(1999)080[2117:QTRBPI]2.0.CO;2. DOI
Relyea RA. Morphological and behavioral plasticity of larval anurans in response to different predators. Ecology. 2001;82:523–540. doi: 10.1890/0012-9658(2001)082[0523:MABPOL]2.0.CO;2. DOI
Osman RW, Whitlatch RB. The control of the development of a marine benthic community by predation on recruits. J. Exp. Mar. Biol. Ecol. 2004;311:117–145. doi: 10.1016/j.jembe.2004.05.001. DOI
Schmidt BR, Băncilă RI, Hartel T, Grossenbacher K, Schaub M. Shifts in amphibian population dynamics in response to a change in the predator community. Ecosphere. 2021;12:e03528. doi: 10.1002/ecs2.3528. DOI
Falaschi M, Melotto A, Manenti R, Ficetola GF. Invasive species and amphibian conservation. Herpetologica. 2020;76:216–227. doi: 10.1655/0018-0831-76.2.216. DOI
Gamradt SC, Kats LB. Effect of introduced crayfish and mosquito fish on California newts. Conserv. Biol. 1996;10:1155–1162. doi: 10.1046/j.1523-1739.1996.10041155.x. DOI
Matthews KR, Knapp RA, Pope KL. Garter snake distributions in high-elevation aquatic ecosystems: Is there a link with declining amphibian populations and nonnative trout introductions? J. Herpetol. 2002;36:16–22. doi: 10.1670/0022-1511(2002)036[0016:GSDIHE]2.0.CO;2. DOI
Dodds WK, Whiles MR. Freshwater Ecology: Concepts and Environmental Applications. 3. Elsevier; 2002.
Preisser EL, Bolnick DI, Benard MF. Scared to death? The effects of intimidation and consumption in predator–prey interactions. Ecology. 2005;86:501–509. doi: 10.1890/04-0719. DOI
Le Roux E, Kerley GI, Cromsigt JP. Megaherbivores modify trophic cascades triggered by fear of predation in an African savanna ecosystem. Curr. Biol. 2018;28:2493–2499. doi: 10.1016/j.cub.2018.05.088. PubMed DOI
Daversa D, et al. Broadening the ecology of fear: Non-lethal effects arise from diverse responses to predation and parasitism. Proc. R. Soc. B. 2021;288:20202966. doi: 10.1098/rspb.2020.2966. PubMed DOI PMC
Benard MF. Predator-induced phenotypic plasticity in organisms with complex life histories. Annu. Rev. Ecol. Evol. Syst. 2004;35:651–673. doi: 10.1146/annurev.ecolsys.35.021004.112426. DOI
Van Buskirk J, Schmidt BR. Predator-induced phenotypic plasticity in larval newts: Trade-offs, selection, and variation in nature. Ecology. 2000;81:3009–3028. doi: 10.2307/177397. DOI
McCollum SA, Van Buskirk J. Costs and benefits of a predator-induced polyphenism in the gray treefrog Hyla chrysoscelis. Evolution. 1996;50:583–593. PubMed
Skelly DK. Tadpole communities: pond permanence and predation are powerful forces shaping the structure of tadpole communities. Am. Sci. 1997;85:36–45.
Sih A, Moore RD. Delayed hatching of salamander eggs in response to enhanced larval predation risk. Am. Nat. 1993;142:947–960. doi: 10.1086/285583. PubMed DOI
Warkentin KM. Adaptive plasticity in hatching age: A response to predation risk trade-offs. Proc. Natl. Acad. Sci. 1995;92:3507–3510. doi: 10.1073/pnas.92.8.3507. PubMed DOI PMC
Johnson JB, Saenz D, Adams CK, Conner RN. The influence of predator threat on the timing of a life-history switch point: Predator-induced hatching in the southern leopard frog (Rana sphenocephala) Can. J. Zool. 2003;81:1608–1613. doi: 10.1139/z03-148. DOI
Wilbur HM, Fauth JE. Experimental aquatic food webs: Interactions between two predators and two prey. Am. Nat. 1990;135:176–204. doi: 10.1086/285038. DOI
Laurila A. Behavioural responses to predator chemical cues and local variation in antipredator performance in Rana temporaria tadpoles. Oikos. 2000;88:159–168. doi: 10.1034/j.1600-0706.2000.880118.x. DOI
Gomez-Mestre I, et al. The shape of things to come: Linking developmental plasticity to post-metamorphic morphology in anurans. J. Evol. Biol. 2010;23:1364–1373. doi: 10.1111/j.1420-9101.2010.02016.x. PubMed DOI
Vieira EA, Duarte LFL, Dias GM. How the timing of predation affects composition and diversity of species in a marine sessile community? J. Exp. Mar. Biol. Ecol. 2012;412:126–133. doi: 10.1016/j.jembe.2011.11.011. DOI
Andrade MR, Albeny-Simões D, Breaux JA, Juliano SA, Lima E. Are behavioural responses to predation cues linked across life cycle stages? Ecol. Entomol. 2017;42:77–85. doi: 10.1111/een.12358. DOI
Knapp RA. Effects of nonnative fish and habitat characteristics on lentic herpetofauna in Yosemite National Park, USA. Biol. Conserv. 2005;121:265–279. doi: 10.1016/j.biocon.2004.05.003. DOI
Kiesecker JM, Blaustein AR. Population differences in responses of red-legged frogs (Rana aurora) to introduced bullfrogs. Ecology. 1997;78:1752–1760. doi: 10.1890/0012-9658(1997)078[1752:PDIROR]2.0.CO;2. DOI
Nunes AL, Orizaola G, Laurila A, Rebelo R. Rapid evolution of constitutive and inducible defenses against an invasive predator. Ecology. 2014;95:1520–1530. doi: 10.1890/13-1380.1. PubMed DOI
Polo-Cavia N, Gonzalo A, López P, Martín J. Predator recognition of native but not invasive turtle predators by naïve anuran tadpoles. Anim. Behav. 2010;80:461–466. doi: 10.1016/j.anbehav.2010.06.004. DOI
Zhang F, Zhao J, Zhang Y, Messenger K, Wang Y. Antipredator behavioral responses of native and exotic tadpoles to novel predator. Asian Herpetol. Res. 2015;6:51–58.
Lowe S, Browne M, Boudjelas S, De Poorter M. 100 of the World's Worst Invasive Alien Species: A Selection from the Global Invasive Species Database. Invasive Species Specialist Group; 2000.
TTWG. Conservation biology of freshwater turtles and tortoises: A compilation project of the IUCN/SSC tortoise and freshwater turtle specialist group. in Chelonian Research Monographs 7 Turtle of the World: Annotated Checklist and Atlas of Taxonomy, Synonymy, Distribution, and Conversation Status. 8th edn. (eds. Rhodin, A.G.J., Iverson, J.B., van Dijk, P.P., Saumure, R.A., Buhlmann, K.A., Pritchard, P.C.H., Mittermeier, R.A.). 1–292. (Chelonian Research Foundation and Turtle Conservancy, 2017).
GISD. Global Invasive Species Database. http://www.issg.org/database (2021).
Berec M, Klapka V, Zemek R. Effect of an alien turtle predator on movement activity of European brown frog tadpoles. Ital. J. Zool. 2016;83:68–76. doi: 10.1080/11250003.2016.1139195. DOI
Vodrážková M, Šetlíková I, Berec M. Chemical cues of an invasive turtle reduce development time and size at metamorphosis in the common frog. Sci. Rep. 2020;10:1–6. doi: 10.1038/s41598-020-64899-0. PubMed DOI PMC
Gibbons, J., Greene, J. & Congdon, J. Life history and ecology of the slider turtle. in Temporal and Spatial Movement Patterns of Sliders and Other Turtles (ed. Gibbons, J.). 201–215. (Smithsonian Institution Press, 1990).
Formanowicz DR. Anuran tadpole/aquatic insect predator-prey interactions: tadpole size and predator capture success. Herpetologica. 1986;42:367–373.
Semlitsch RD, Gibbons JW. Fish predation in size-structured populations of treefrog tadpoles. Oecologia. 1988;75:321–326. doi: 10.1007/BF00376932. PubMed DOI
Teplitsky C, Piha H, Laurila A, Merilä J. Common pesticide increases costs of antipredator defenses in Rana temporaria tadpoles. Environ. Sci. Technol. 2005;39:6079–6085. doi: 10.1021/es050127u. PubMed DOI
Travis J. Anuran size at metamorphosis: experimental test of a model based on intraspecific competition. Ecology. 1984;65:1155–1160. doi: 10.2307/1938323. DOI
Wilbur HM, Collins JP. Ecological aspects of amphibian metamorphosis: Nonnormal distributions of competitive ability reflect selection for facultative metamorphosis. Science. 1973;182:1305–1314. doi: 10.1126/science.182.4119.1305. PubMed DOI
Gosner KL. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica. 1960;16:183–190.
Woodward G, Hildrew AG. Body-size determinants of niche overlap and intraguild predation within a complex food web. J. Anim. Ecol. 2002;71:1063–1074. doi: 10.1046/j.1365-2656.2002.00669.x. DOI
Relyea RA. Getting out alive: How predators affect the decision to metamorphose. Oecologia. 2007;152:389–400. doi: 10.1007/s00442-007-0675-5. PubMed DOI
Pujol-Buxó E, San Sebastián O, Garriga N, Llorente GA. How does the invasive/native nature of species influence tadpoles’ plastic responses to predators? Oikos. 2013;122:19–29. doi: 10.1111/j.1600-0706.2012.20617.x. DOI
Phuge S, Shetye K, Pandit R. Effect of water level on insect-tadpole predator-prey interactions. Acta Oecol. 2020;108:103649. doi: 10.1016/j.actao.2020.103649. DOI
Loman J. Early metamorphosis in common frog Rana temporaria tadpoles at risk of drying: An experimental demonstration. Amphibia-Reptilia. 1999;20:421–430. doi: 10.1163/156853899X00466. DOI
Stav G, Kotler BP, Blaustein L. Direct and indirect effects of dragonfly (Anax imperator) nymphs on green toad (Bufo viridis) tadpoles. Hydrobiologia. 2007;579:85–93. doi: 10.1007/s10750-006-0388-5. DOI
Goldberg T, Nevo E, Degani G. Phenotypic plasticity in larval development of six amphibian species in stressful natural environments. Zool. Stud. 2012;51:345–361.
Kishida O, Costa Z, Tezuka A, Michimae H. Inducible offences affect predator–prey interactions and life-history plasticity in both predators and prey. J. Anim. Ecol. 2014;83:899–906. doi: 10.1111/1365-2656.12186. PubMed DOI
Leips J, Travis J. Metamorphic responses to changing food levels in two species of hylid frogs. Ecology. 1994;75:1345–1356. doi: 10.2307/1937459. DOI
Alford RA, Harris RN. Effects of larval growth history on anuran metamorphosis. Am. Nat. 1988;131:91–106. doi: 10.1086/284775. DOI
Loman J. Temperature, genetic and hydroperiod effects on metamorphosis of brown frogs Rana arvalis and R. temporaria in the field. J. Zool. 2002;258:115–129. doi: 10.1017/S0952836902001255. DOI
Laugen AT, et al. Quantitative genetics of larval life-history traits in Rana temporaria in different environmental conditions. Genet. Res. 2005;86:161–170. doi: 10.1017/S0016672305007810. PubMed DOI
Brodie ED, Formanowicz DR. Prey size preference of predators: Differential vulnerability of larval anurans. Herpetologica. 1983;39:67–75.
Eklöv P, Werner EE. Multiple predator effects on size-dependent behavior and mortality of two species of anuran larvae. Oikos. 2000;88:250–258. doi: 10.1034/j.1600-0706.2000.880203.x. DOI
Urban MC. Predator size and phenology shape prey survival in temporary ponds. Oecologia. 2007;154:571–580. doi: 10.1007/s00442-007-0856-2. PubMed DOI
Jara FG, Perotti MG. Risk of predation and behavioural response in three anuran species: influence of tadpole size and predator type. Hydrobiologia. 2010;644:313–324. doi: 10.1007/s10750-010-0196-9. DOI
Wassersug RJ, Sperry DG. The relationships of locomotion to differential predation on Pseudacris triseriata (Anura: Hylidae) Ecology. 1977;58:830–839. doi: 10.2307/1936218. DOI
Huey RB. Sprint velocity of tadpoles (Bufo boreas) through metamorphosis. Copeia. 1980;1980:537–540. doi: 10.2307/1444534. DOI
Laurila A, Kujasalo J. Habitat duration, predation risk and phenotypic plasticity in common frog (Rana temporaria) tadpoles. J. Anim. Ecol. 1999;68:1123–1132. doi: 10.1046/j.1365-2656.1999.00354.x. DOI
Metcalfe NB, Monaghan P. Compensation for a bad start: grow now, pay later? Trends Ecol. Evol. 2001;16:254–260. doi: 10.1016/S0169-5347(01)02124-3. PubMed DOI
Downie J, Weir A. Developmental arrest in Leptodactylus fuscus tadpoles (Anura: Leptodactylidae) III effect of length of arrest period on growth potential. Herpetol. J. 1997;7:85–92.
Smith DC. Adult recruitment in chorus frogs: Effects of size and date at metamorphosis. Ecology. 1987;68:344–350. doi: 10.2307/1939265. DOI
Altwegg R, Reyer HU. Patterns of natural selection on size at metamorphosis in water frogs. Evolution. 2003;57:872–882. doi: 10.1111/j.0014-3820.2003.tb00298.x. PubMed DOI
Brunelli E, et al. Environmentally relevant concentrations of endosulfan impair development, metamorphosis and behaviour in Bufo bufo tadpoles. Aquat. Toxicol. 2009;91:135–142. doi: 10.1016/j.aquatox.2008.09.006. PubMed DOI
Boone MD. Juvenile frogs compensate for small metamorph size with terrestrial growth: Overcoming the effects of larval density and insecticide exposure. J. Herpetol. 2005;39:416–423. doi: 10.1670/187-04A.1. DOI
Schmidt BR, Hödl W, Schaub M. From metamorphosis to maturity in complex life cycles: Equal performance of different juvenile life history pathways. Ecology. 2012;93:657–667. doi: 10.1890/11-0892.1. PubMed DOI