Phenotypic indicators of developmental instability in an endemic amphibian from an altered landscape (Monegros, NE Spain)

in Amphibia-Reptilia
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The great sensitivity of amphibians to land disturbance is one of the main causes that contributed to their worldwide decline. One fundamental approach in assessing amphibian ability to reflect habitat degradation is to measure their phenotypic changes in contrasting environments. We examined the extent to which several morphological traits of the endemic anuran Pelophylax perezi responded to agricultural conversion in Monegros, an arid region in NE Spain. Specifically, we determined how body size, body mass, body condition (BC) and fluctuating asymmetry (FA) of different frog classes varied among habitats with different degree of management, i.e. rice fields vs. control ponds (i.e. small reservoirs). Pelophylax perezi juveniles showed a decrease in size and mass in rice fields, revealing that early life stages are generally more susceptible to habitat alteration. Adult body condition, on the other hand, increased significantly in cultivated habitats, which apparently indicates a good fitness in this size class. Nonetheless, skeletal asymmetry of both, juveniles and adults was significantly higher in rice fields. Moreover, during postmetamorphic development FA increased significantly towards adult stage indicating that the development controlling mechanisms were not able to buffer the stress induced by land use change. Among traits, humerus, radio-ulna and metatarsal were highly sensitive in terms of expressing significant FA differences between habitats, contrary to tibio-fibula, whose precise symmetry is essential for animal locomotion. The former bones have therefore the potential to be used as sensitive indicators of stress in amphibians. FA showed no relationship with body condition. This, together with the previous results demonstrates that FA is able to capture habitat stress more reliably than the morphological estimates such as body size, mass and BC. Therefore, FA is a useful morphological tool, highly recommended to monitor stress levels in amphibian populations.

Phenotypic indicators of developmental instability in an endemic amphibian from an altered landscape (Monegros, NE Spain)

in Amphibia-Reptilia

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References

  • AlfordR.BradfieldK.S.RichardsS. (1999): Measuring and analyzing developmental instability as a tool for monitoring frog populations. In: Declines and Disappearances of Australian Frogs p.  34-44. CampbellA. Ed. Environment AustraliaCanberra.

  • AlfordR.A.BradfieldK.S.RichardsS.J. (2007): Global warming and amphibian losses. Nature 447: E3-E4.

  • AparicioJ.M. (2001): Patterns of growth and fluctuating asymmetry: the effects of asymmetrical investment in traits with determinate growth. Behav. Ecol. Sociobiol. 49: 273-282.

  • BeckerG.C.FonsecaC.R.HaddadC.F.B.BatistaR.F.PradoP.I. (2007): Habitat split and the global decline of amphibians. Science 318: 1775-1777.

  • BOE (Boletín Oficial del Principado de Asturias y de la Provincia) (1990): Decreto 32/90 de 30 de marzo: Catálogo regional de especies amenazadas de la fauna vertebrada del Principado de Asturias. BOE 75: 1389.

  • BonadaN.WilliamsD.D. (2002): Exploration of the utility of fluctuating asymmetry as an indicator of river condition using larvae of the caddisfly Hydropsyche morose (Trichoptera: Hydropsychidae). Hydrobiologia 481: 147-156.

  • BurgheleaC.I.ZaharescuD.G.Palanca-SolerA. (2010): Dietary overview of Pelophylax perezi from Monegros rice fields (NE Spain). Herpetol. J. 20: 219-224.

  • BurgheleaC.I.ZaharescuD.G.HoodaP.Palanca-SolerA. (2011): Predatory aquatic beetles, suitable trace elements bioindicators. J. Environ. Monitor. 13: 1308-1315.

  • ClarkeG.M. (1998): The genetic basis of developmental stability. IV. Individual and population asymmetry parameters. Heredity 80: 553-561.

  • CrochetP.A.ChalineO.CheylanM.GuillaumeC.P. (2004): No evidence of general decline in an amphibian community of Southern France. Biol. Conserv. 119: 297-304.

  • DavisA.K.MaerzJ.C. (2007): Spot symmetry predicts body condition in Spotted Salamanders, Ambystoma maculatum. Appl. Herpetol. 4: 195-205.

  • DebatV.DavidP. (2001): Mapping phenotypes: canalization, plasticity and developmental stability. Trends Ecol. Evol. 16: 555-561.

  • De BlockM.CamperoM.StoksR. (2008): Developmental costs of rapid growth in a damselfly. Ecol. Entomol. 33: 313-318.

  • Delgado-AcevedoJ.RestrepoC. (2008): The contribution of habitat loss to changes in body size, allometry, and bilateral asymmetry in two Eleutherodactylus frogs from Puerto Rico. Conserv. Biol. 22: 773-782.

  • DenoëlM.LibonS.KestemontP.BrasseurC.FocantJ.F.De PauwE. (2013): Effects of a sublethal pesticide exposure on locomotor behavior: A video-tracking analysis in larval amphibians. Chemosphere 90: 945-951.

  • FicetolaG.F.ScaliS.DenoëlM.MontinaroG.VukovT.D.ZuffiM.A.L.Padoa-SchioppaE. (2010): Ecogeographical variation of body size in the newt Triturus carnifex: comparing the hypotheses using an information-theoretic approach. Global Ecol. Biogeogr. 19: 485-495.

  • FullerR.HouleD. (2002): Detecting genetic variation in developmental instability by artificial selection on fluctuating asymmetry. J. Evolution. Biol. 15: 954-960.

  • GrahamJ.H.RazS.Hel-OrH.NevoE. (2010): Fluctuating asymmetry: methods, theory, and applications. Symmetry 2: 466-540.

  • GrayM.J. (2002): Effect of anthropogenic disturbance and landscape structure on body size demographics and chaotic dynamics of Southern High Plains amphibians. Ph.D. Thesis Texas Tech University.

  • GrayM.J.SmithL.M. (2005): Influence of land use on postmetamorphic body size of playa lake amphibians. J. Wildl. Manage. 69: 515-524.

  • GrayM.J.SmithL.M.LeyvaR.I. (2004): Influence of agricultural landscape structure on a Southern High Plains, USA, amphibian assemblage. Landscape Ecol. 19: 719-729.

  • GreenA. (2001): Mass/length residuals: measures of body condition or generators of spurious results? Ecology 82: 1473-1483.

  • HayesT.CaseP.ChuiS.ChungD.HaefeleC.HastonK.LeeM.MaiV.P.MarjuoaY.ParkerJ. (2006): Pesticide mixtures, endocrine disruption, and amphibian declines: Are we underestimating the impact? Environ. Health Perspect. 114: 40-50.

  • HerreroJ.SnyderR.L. (1997): Aridity and irrigation in Aragón, Spain. J. Arid Environ. 35: 535-547.

  • IAEST (Instituto Aragonés de Estadística) (2009a): Usos municipales suelo 2006-2009. Available at: http://www.aragon.es/DepartamentosOrganismosPublicos/Departamentos/AgriculturaGanaderiaMedioAmbiente/AreasTematicas/EstadisticasAgrarias/estadisticasAgricolas/ci.11_Usos_agrarios_suelo.detalleDepartamento (accessed May 2012).

  • IAEST (Instituto Aragonés de Estadística) (2009b): Anuario estadístico agrario 2008-2009. Available at: http://www.aragon.es/DepartamentosOrganismosPublicos/Departamentos/AgriculturaGanaderiaMedioAmbiente/AreasTematicas/EstadisticasAgrarias/ci.10_Anuario_estadístico_agrario.detalleDepartamento#section2 (accessed May 2012).

  • IAEST (Instituto Aragonés de Estadística) (2011): Consumo de plaguicidas/pesticidas en kg/ha. Aragón. Años 1999-2010. Available at: http://www.aragon.es/DepartamentosOrganismosPublicos/Organismos/InstitutoAragonesEstadistica/AreasTematicas/MedioAmbiente/IndicadoresAmbientalesSectoriales/IndicadoresSectoriales/ci.Agricultura.detalleDepartamento (accessed May 2012).

  • JakobE.M.MarshallS.D.UetzG.W. (1996): Estimating fitness a comparison of body condition indices. Oikos 77: 61-67.

  • JayneB.C.BennettA.F. (1990): Selection on locomotor capacity in a natural population of garter snakes. Evolution 44: 1204-1229.

  • KellnerJ.R.AlfordR.A. (2003): The ontogeny of fluctuating asymmetry. Am. Nat. 161: 931-947.

  • LauckB. (2006): Fluctuating asymmetry of the frog Crinia signifera in response to logging. Wildlife Res. 33: 313-320.

  • LensL.Van DongenS.MatthysenE. (2002): Fluctuating asymmetry as an early warning system in the critically endangered Taita thrush. Conserv. Biol. 16: 479-487.

  • MacCrackenJ.G. (2002): Response of forest floor vertebrates to riparian hardwood conversion along the Bear River, Southwest Washington. Forest Sci. 48: 299-308.

  • MacklinM.G.PassmoreD.G.StevensonA.C.DavisB.A.BenaventeJ.A. (1994): Response of rivers and lakes to Holocene environmental change in the Alcaniz region, Teruel, North-East Spain. In: Environmental Change in Drylands: Biogeographical and Geomorphological Perspectives p.  113-130. MillingtonA.PyeK. Eds WileyUSA.

  • McCoyK.A.HarrisR.N. (2003): Integrating developmental stability analysis and current amphibian monitoring techniques: an experimental evaluation with the salamander Ambystoma maculatum. Herpetologica 59: 22-36.

  • Martín-QuellerE.Moreno-MateosD.PedrocchiC.CervantesJ.MartínezG. (2010): Impacts of intensive agricultural irrigation and livestock farming on a semi-arid Mediterranean catchment. Environ. Monit. Assess. 167: 423-435.

  • PalmerA.R. (1994): Fluctuating asymmetry analysis: a primer. In: Developmental Instability: Its Origins and Evolutionary Implications p.  335-364. MarkowT. Ed. Kluwer Academic PublishersDordrecht.

  • PalmerA.R.StrobeckC. (1986): Fluctuating asymmetry: measurement, analysis, patterns. Annu. Rev. Ecol. Syst. 17: 391-421.

  • PalmerA.R.StrobeckC. (2003): Fluctuating asymmetry analyses revisited. In: Developmental Instability: Causes and Consequences p.  279-319. PolakM. Ed. Oxford University PressUSA.

  • ParrisM.J.CorneliusT.O. (2004): Fungal pathogen causes competitive and developmental stress in larval amphibian communities. Ecology 85: 3385-3395.

  • PastorD.SanperaC.González-SolísJ.RuizX.AlbaigésJ. (2004): Factors affecting the organochlorine pollutant load in biota of a rice field ecosystem (Ebro Delta, NE Spain). Chemosphere 55: 567-576.

  • PetersR.H. (1983): The Ecological Implications of Body Size. Cambridge University PressUSA.

  • PihaH.LuotoM.MeriläJ. (2007): Amphibian occurrence influenced by current and historic landscape characteristics. Ecol. Appl. 17: 2298-2309.

  • PiscartC.MoreteauJ.C.BeiselJ.N. (2005): Decrease of fluctuating asymmetry among larval instars in an aquatic, holometabolous insect. C. R. Biol. 328: 912-917.

  • SemlitschR.D. (2002): Critical elements for biologically based recovery plans of aquatic-breeding amphibians. Conserv. Biol. 16: 619-629.

  • ServiaM.J.CoboF.GonzalezM.A. (2002): Ontogeny of individual asymmetries in several traits of larval Chironomus riparius Meigen, 1804 Diptera, Chironomidae. Can. J. Zoolog. 80: 1470-1479.

  • SödermanF.Van DongenS.PakkasmaaS.MeriläJ. (2007): Environmental stress increases skeletal fluctuating asymmetry in the moor frog Rana arvalis. Oecologia 151: 593-604.

  • SodhiN.S.BickfordD.DiesmosA.C.LeeT.M.KohL.P.BrookB.W.SekerciogluC.H.BradshawC.J.A. (2008): Measuring the meltdown: drivers of global amphibian extinction and decline. PLoS ONE 3: e1636.

  • St-AmourV.GarnerT.W.J.Schulte-HosteddeA.I.LesbarrèresD. (2010): Effects of two amphibian pathogens on the developmental stability of green frogs. Conserv. Biol. 24: 788-794.

  • SwaddleJ.P.WitterM.S. (1997): On the ontogeny of developmental stability in a stabilized trait. P. Roy. Soc. Lond. B. Bio. 264: 329-334.

  • Van ValenL. (1962): A study of fluctuating asymmetry. Evolution 16: 125-142.

  • WoodhamsD.C.AlfordR.A. (2005): Ecology of Chytridiomycosis in rainforest stream frog assemblages of tropical Queensland. Conserv. Biol. 19: 1449-1459.

Figures

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    Monegros arid region (NE Spain) on digital elevation map, with the location of sampling sites. Symbols legend: ○, locality; ■, reservoirs and □, rice fields. This figure is published in colour in the online version.

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    Example of radiograph of Pelophylax perezi illustrating bones and their length used for FA measurements (showed here by arrows). This figure is published in colour in the online version.

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    Box plots showing differences in: (A), (D) body size (SVL); (B), (E) body mass and (E), (F) body condition (BC) of Pelophylax perezi between rice fields and reservoirs. Significance level at P<0.01 (two way ANOVA). Rm: recently metamorphosed, Jv: juveniles, Fm: females and Ml: males.

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    Variations in fluctuating asymmetry of (A) tibio-fibula, (B) metatarsal, (C) humerus, (D) radio-ulna and (E) composite asymmetry index (mean ± SE) of Pelophylax perezi classes among habitats. Significance is showed at: P<0.05 and ∗∗P<0.01 (GLM, generalized linear model). Rm: recently metamorphosed, Jv: juveniles, Fm: females and Ml: males.

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    Trait fluctuating asymmetry variation between habitats. Significance at P<0.05 and ∗∗P<0.0001. TF: tibio-fibula, MT: metatarsal, HU: humerus and RU: radio-ulna.

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