, Volume 151, Issue 4, pp 593–604 | Cite as

Environmental stress increases skeletal fluctuating asymmetry in the moor frog Rana arvalis

  • Fredrik Söderman
  • Stefan van Dongen
  • Susanna Pakkasmaa
  • Juha Merilä
Population Ecology


Whether fluctuating asymmetry (FA) provides a useful metric indicator of the degree of environmental stress experienced by populations is still a contentious issue. We investigated whether the degree of FA in skeletal elements is useful in elucidating the degree of environmental stress experienced by frog populations, and further, tested the proposition that a trait’s sensitivity to stress—as reflected in the degree of FA—is related to the degree of directional selection experienced by the given trait. We compared the degree of FA in four bilateral skeletal elements of male and female moor frogs (Rana arvalis) originating from low (acidified) and neutral pH populations. While the degree of uncorrected FA was unrelated to the degree of acidity, the growth rate and age of the individuals, the size-corrected FA was significantly higher in low than in neutral pH populations and decreased with individual ages and growth rates. In addition, both measures of FA were significantly higher in males and in particular in traits presumably under high sexual selection as indicated by the degree of sexual size dimorphism. All in all, the results indicate that individuals from acidified localities are smaller, younger and exhibit a significantly higher degree of FA than individuals from neutral pH populations. These results constitute the first assessment of FA in amphibians and suggest that the degree of FA in skeletal traits can be a useful indicator of the degree of environmental stress experienced by amphibian populations.


Amphibians Acidification Developmental stability FA Environmental stress 



We thank Anssi Laurila, Katja Räsänen and all other people who have helped us in the course of this work. In particular, thanks are due to Peter Mortensen and Jorma Uusitalo at the Swedish Natural History Museum for help in preparation of the skeletons and to Magnus Svensson and Mattias Sterner for doing all the measurements and preparations. The collection was performed with a licence from the Swedish Environmental Protection agency (409-1106-11). Our research was supported by the Swedish Natural Science Research Council, Swedish Forest and Agricultural Science Research Council, Oscar and Lili Lamm Foundation, Nils von Hoffsten Foundation, University of Helsinki Science Foundation and the Academy of Finland.


  1. Alexander J (2002) Calcium requirement and growth in the hatchling loggerhead sea turtle Caretta caretta. NOAA Tech Memo 477:74–76Google Scholar
  2. Alford RA, Richards SJ (1999) Global amphibian declines: a problem in applied ecology. Annu Rev Ecol Syst 30:133–165CrossRefGoogle Scholar
  3. Berglind S-Å (1994) Sexual strategies and size dimorphism in the moor frog (Rana arvalis Nilsson)—M.Sc. Thesis University GöteborgGoogle Scholar
  4. Bertills U, Hanneberg P (1995) Försurningen i Sverige—vad vet vi egentligen? Naturvårdsverket, StockholmGoogle Scholar
  5. Berven KA (1981) Mate choice in the wood frog, Rana sylvatica. Evolution 35:707–722CrossRefGoogle Scholar
  6. Bisazza A, Cantalupo C, Robins A, Rogers LJ, Vallortigara G (1997) Pawedness and motor asymmetries in toads. Laterality 2:49–64CrossRefPubMedGoogle Scholar
  7. Björksten T, David P, Pomiankowski A, Fowler K (2000) Fluctuating asymmetry of sexual and nonsexual traits in stalk-eyed flies: a poor indicator of developmental stress and genetic quality. J Evol Biol 13:89–97CrossRefGoogle Scholar
  8. Blum M, Steinbeisser H, Campione M, Schweickert A (1999) Vertebrate left–right asymmetry: old studies and new insights. Cell Mol Biol 45:505–516PubMedGoogle Scholar
  9. Böhmer J, Rahmann H (1990) Influence of surface water acidification on amphibians. In: Hanke W (ed) Biology and physiology of amphibians. Gustav Fisher, Jena, pp 287–307Google Scholar
  10. Borkhvardt VG, Ivashintsova EB (1994) On the position of the epicoracoids in amphibian arciferal pectoral girdles. Russ J Herpetol 1:114–116Google Scholar
  11. Castanet J, Meunier FJ, De Ricqles A (1977) Recording of cyclic growth by bone tissue in poikilothermic vertebrates comparative data and conclusions. Bull Biol Fr Belg 111:183–202Google Scholar
  12. Clutton-Brock TH, Albon SD, Guiness FE (1985) Parental investment and sex differences in juvenile mortality in birds and mammals. Nature 313:131–133CrossRefGoogle Scholar
  13. Dill LM (1977) ‘Handedness’ in the pacific tree frog (Hyla regilla). Can J Zool 55:1926–1929CrossRefGoogle Scholar
  14. Elmberg J (1984) Åkergrodan Rana arvalis i norra Sverige. Fauna Flora 79:69–77Google Scholar
  15. Elmberg J (1991) Factors affecting male yearly mating success in the common frog, Rana temporaria. Behav Ecol Sociobiol 28:125–131CrossRefGoogle Scholar
  16. Emerson SB (1979) The ilio-sacral articulation in frogs: form and function. Biol J Linn Soc 77:153–168Google Scholar
  17. Folstad I, Karter A (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622CrossRefGoogle Scholar
  18. Gislén T, Kauri H (1959) Zoogeography of the Swedish amphibians and reptiles. Act Vertebr 1:270–395Google Scholar
  19. Graham JH, Freeman DC, Emlen JM (1993) Antisymmetry, directional asymmetry, and chaotic morphogenesis. Genetica 89:121–137CrossRefGoogle Scholar
  20. Hasselrot B, Hultberg H (1984) Liming of acidified Swedish lakes and streams and its consequences for aquatic ecosystems. Fisheries 9:4–9CrossRefGoogle Scholar
  21. Hedengren I (1987) Selection of body size, arm length and colour in male and female moor frogs (Rana arvalis). M. Sc. Thesis University StockholmGoogle Scholar
  22. Hemelaar A (1985) An improved method to estimate the number of year rings resorbed in Phalanges of Bufo bufo (L) and its application to populations from different latitudes and altitudes. Amphib-reptilia 6:323–341Google Scholar
  23. Hesthagen T, Sevaldrud IH, Berger HM (1999) Assessment of damage to fish populations in Norwegian lakes due to acidification. Ambio 28:112–117Google Scholar
  24. Höglund J, Säterberg L (1989) Sexual selection in common toads: correlates with age and body size. J Evol Biol 2:367–372CrossRefGoogle Scholar
  25. Howard RD (1981) Male age-size distribution and male mating success in bullfrogs. In: Alexander RD (ed) Natural selection and social behavior: recent research and new theory. Chiron Press, New York, pp 561–577Google Scholar
  26. Ischenko V (1997) Rana arvalis Nilsson 1842. In: Gasc J-P, et al (ed) Atlas of amphibians and reptiles in europe. Societas Europaea Herpetologica and Museum National d’Historie Naturelle, pp 128–129Google Scholar
  27. Jagoe CH, Haines TA (1985) Fluctuating asymmetry in fishes inhabiting acidified and unacidified lakes. Can J Zool 63:130–138Google Scholar
  28. Jenkins FA, Shubin NH (1998) Prosalirus bitis and the anuran caudopelvic mechanism. J Vertebr Pal 18:495–510CrossRefGoogle Scholar
  29. Jolicoeur P (1963) Bilateral symmetry and asymmetry in limb bones of Martes americana and man. Rev Can Biol 22:409–432PubMedGoogle Scholar
  30. Karvonen E, Merilä J, Rintamaki PT, van Dongen S (2003) Geography of fluctuating asymmetry in the greenfinch, Carduelis chloris. Oikos 100:507–516CrossRefGoogle Scholar
  31. Kleinenberg SE, Smirina EM (1969) Method of determining the age of amphibians. Zool Zh 48:1090–1094Google Scholar
  32. Kuzmin SL (1999) The Amphibians of the former Soviet Union. PensoftGoogle Scholar
  33. Lamb T, Novak JM, Mahoney DL (1990) Morphological asymmetry and interspecific hybridization: a case study using hylid frogs. J Evol Biol 3:295–309CrossRefGoogle Scholar
  34. Lauck B (2006) Fluctuating asymmetry of the frog Crinia signifera in response to logging. Wildl Res 33:313–320CrossRefGoogle Scholar
  35. Lens L, Van Dongen S (2000) Fluctuating and directional asymmetry in natural bird populations exposed to different levels of habitat disturbance, as revealed by mixture analysis. Ecol Lett 3:516–522CrossRefGoogle Scholar
  36. Lens L, Van Dongen S, Kark S, Talloen W, Hens L, Matthysen E (2001) The use of bilateral asymmetry in ecology and conservation: concept, developments and prospects. Recent Res Dev Ecol 1:21–41Google Scholar
  37. Leung B, Forbes MR (1996) Fluctuating asymmetry in relation to stress and fitness: effects of trait type as revealed by meta-analysis. Ecoscience 3:400–413Google Scholar
  38. Leuven RSEW, den Hartog C, Christiaans MMC, Heijligers WHC (1986) Effects of water acidification on the distribution pattern and the reproductive success of amphibians. Experientia 42:495–503CrossRefGoogle Scholar
  39. Lindmark GK (1984) Acidified lakes—ecosystem response following sediment treatment with sodium carbonate. Verh Int Ver Theor Angew Limnol 22:772–779Google Scholar
  40. Littell R, Stroup WW, Freund R (2002) SAS for Linear Models, 4th edn. Wiley, NYGoogle Scholar
  41. Malashichev YB, Nikitina NG (2002) Preferential limb use in relation to epicoracoid overlap in the shoulder girdle of toads. Laterality 7:1–18PubMedGoogle Scholar
  42. Merilä J, Söderman F, O’Hara R, Räsänen K, Laurila A (2004). Local adaptation and genetics of acid-stress tolerance in the moor frog, Rana arvalis. Conserv Genet 5:513–527CrossRefGoogle Scholar
  43. Møller AP, Pomiankowski A (1993) Punctuated equilibria or gradual evolution: fluctuating asymmetry and variation in the rate of evolution. J Theor Biol 161:359–367PubMedCrossRefGoogle Scholar
  44. Møller AP, Swaddle JP (1997) Developmental stability and evolution. Oxford University Press, New YorkGoogle Scholar
  45. Møller AP, Alatalo RV (1999) Good-genes effects in sexual selection. Proc R Soc Lond B Biol Sci 266:85–91CrossRefGoogle Scholar
  46. Moran P, Izquierdo JI, Pendas AM, GarciaVazquez E (1997) Fluctuating asymmetry and isozyme variation in Atlantic salmon: relation to age of wild and hatchery fish. Trans Am Fish Soc 126:194–199CrossRefGoogle Scholar
  47. Packard MJ, Jennings DH, Hanken J (1996) Growth and uptake of mineral by embryos of the direct-developing frog Eleutherodactylus coqui. Comp Biochem Physiol A 113A:343–349CrossRefGoogle Scholar
  48. Pierce BA (1985) Acid tolerance in amphibians. Bioscience 35:239–243CrossRefGoogle Scholar
  49. Räsänen K, Laurila A, Merilä J (2003a) Geographic variation in acid stress tolerance of the moor frog, Rana arvalis. I. Local adaptation. Evolution 57:352–362CrossRefGoogle Scholar
  50. Räsänen K, Laurila A, Merilä J (2003b) Geographic variation in acid stress tolerance of the moor frog, Rana arvalis. II. Adaptive maternal effects. Evolution 57:363–371CrossRefGoogle Scholar
  51. Ryan MJ, Warkentin KM, McClelland BE, Wilczynski W (1995) Fluctuating asymmetries and advertisement call variation in the cricket frog, Acris crepitans. Behav Ecol 6:124–131CrossRefGoogle Scholar
  52. Sheldon BC, Merilä J, Lindgren G, Ellegren H (1998) Gender and environmental sensitivity in nestling collared flycatchers. Ecology 79:1939–1948CrossRefGoogle Scholar
  53. Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fischman DL, Waller RW (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786PubMedCrossRefGoogle Scholar
  54. Tilgar V, Mand R, Ots I, Magi M, Kilgas P, Reynolds SJ (2004) Calcium availability affects bone growth in nestlings of free-living great tits (Parus major), as detected by plasma alkaline phosphatase. J Zool 263:269–274CrossRefGoogle Scholar
  55. Van Dongen S (2000) Unbiased estimation of individual asymmetry. J Evol Biol 13:107–112CrossRefGoogle Scholar
  56. Van Dongen S (2006) Fluctuating asymmetry and developmental instability in evolutionary biology: past, present and future. J Evol Biol 19:1727–1743Google Scholar
  57. Van Dongen S, Sprengers E, Löfstedt C, Matthysen E (1999) Heritability of tibia fluctuating asymmetry and developmental instability in the winter moth (Operophtera brumata L.) (Lepidoptera, Geometridae). Heredity 82:535–542PubMedCrossRefGoogle Scholar
  58. Verbeke G, Molenberghs G (2000) Linear mixed models for longitudinal data. Springer, Berlin Heidelberg New YorkGoogle Scholar
  59. Vøllestad LA, Hindar K (2001) Developmental stability in brown trout: are there any effects of heterozygosity or environmental stress? Biol J Linn Soc 74:351–364CrossRefGoogle Scholar
  60. Whitlock M (1996) The heritability of fluctuating asymmetry and the genetic control of developmental stability. Proc R Soc Lond B Biol Sci 263:849–853CrossRefGoogle Scholar
  61. Whitlock M (1998) The repeatability of fluctuating asymmetry: a revision and extension. Proc R Soc Lond 265:1429–1431CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Fredrik Söderman
    • 1
  • Stefan van Dongen
    • 2
  • Susanna Pakkasmaa
    • 1
    • 3
  • Juha Merilä
    • 4
  1. 1.Department of Population Biology and Conservation Biology, Evolutionary Biology CentreUppsala UniversityUppsalaSweden
  2. 2.Department of Biology, Group of Evolutionary BiologyUniversity of AntwerpAntwerpBelgium
  3. 3.Institute of Freshwater ResearchSwedish Board of FisheriesDrottningholmSweden
  4. 4.Ecological Genetics Research Unit, Department of Biological and Environmental SciencesUniversity of HelsinkiHelsinkiFinland

Personalised recommendations