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Oecologia

, Volume 182, Issue 4, pp 1063–1074 | Cite as

Inter-class competition in stage-structured populations: effects of adult density on life-history traits of adult and juvenile common lizards

  • Luis M. San-JoseEmail author
  • Miguel Peñalver-Alcázar
  • Katleen Huyghe
  • Merel C. Breedveld
  • Patrick S. Fitze
Population ecology – original research

Abstract

Ecological and evolutionary processes in natural populations are largely influenced by the population’s stage-structure. Commonly, different classes have different competitive abilities, e.g., due to differences in body size, suggesting that inter-class competition may be important and largely asymmetric. However, experimental evidence states that inter-class competition, which is important, is rare and restricted to marine fish. Here, we manipulated the adult density in six semi-natural populations of the European common lizard, Zootoca vivipara, while holding juvenile density constant. Adult density affected juveniles, but not adults, in line with inter-class competition. High adult density led to lower juvenile survival and growth before hibernation. In contrast, juvenile survival after hibernation was higher in populations with high adult density, pointing to relaxed inter-class competition. As a result, annual survival was not affected by adult density, showing that differences in pre- and post-hibernation survival balanced each other out. The intensity of inter-class competition affected reproduction, performance, and body size in juveniles. Path analyses unravelled direct treatment effects on early growth (pre-hibernation) and no direct treatment effects on the parameters measured after hibernation. This points to allometry of treatment-induced differences in early growth, and it suggests that inter-class competition mainly affects the early growth of the competitively inferior class and thereby their future performance and reproduction. These results are in contrast with previous findings and, together with results in marine fish, suggest that the strength and direction of density dependence may depend on the degree of inter-class competition, and thus on the availability of resources used by the competing classes.

Keywords

Density-dependence Experimental populations Inter-class competition Intra-class competition Population dynamics 

Notes

Acknowledgments

We thank Cristina Romero-Diaz and Itziar López Zandueta for field assistance and two anonymous reviewers for their constructive comments. The capture and handling of lizards was conducted under the licenses provided by the Gobierno de Navarra. K.H. is a postdoctoral fellow of F.W.O-V1.

Author contribution statement

LMS-J and PSF conceived and designed the study. LMS-J, MP-A, KH, and MCB conducted the experiment. LMS-J, MP-A, and PSF analysed the data. LMS-J and PSF wrote the manuscript. All authors critically revised the manuscript.

Compliance with ethical standards

Funding

The work was supported by the Spanish Ministry of Education and Science (CGL2005-01187, CGL2008-01522) and the Swiss National Science Foundation (PPOOP3_128375) to P. S. F.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable institutional and national guidelines for the care and use of animals were followed.

Supplementary material

442_2016_3738_MOESM1_ESM.docx (343 kb)
Supplementary material 1 (DOCX 342 kb)

References

  1. Aljetlawi A, Leonardsson K (2002) Size-dependent competitive ability in a deposit-feeding amphipod, Monoporeia affinis. Oikos 97:31–44CrossRefGoogle Scholar
  2. Amarasekare P (2003) Competitive coexistence in spatially structured environments: a synthesis. Ecol Lett 6:1109–1122. doi: 10.1046/j.1461-0248.2003.00530.x CrossRefGoogle Scholar
  3. Asmussen MA (1983) Density-dependent selection incorporating intraspecific competition II: a diploid model. Genetics 103:335–350PubMedPubMedCentralGoogle Scholar
  4. Ayllón D, Nicola GG, Parra I et al (2013) Intercohort density dependence drives brown trout habitat selection. Acta Oecol 46:1–9. doi: 10.1016/j.actao.2012.10.007 CrossRefGoogle Scholar
  5. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. doi: 10.18637/jss.v067.i01 CrossRefGoogle Scholar
  6. Bauwens D, Verheyen RF (1985) The timing of reproduction in the lizard Lacerta vivipara: differences between individual females. J Herpetol 19:353–364CrossRefGoogle Scholar
  7. Bauwens D, Verheyen RF (1987) Variation of reproductive traits in a population of the lizard Lacerta vivipara. Holartic Ecol 10:120–127Google Scholar
  8. Beckerman A, Benton TG, Ranta E et al (2002) Population dynamic consequences of delayed life-history effects. Trends Ecol Evol 17:263–269. doi: 10.1016/S0169-5347(02)02469-2 CrossRefGoogle Scholar
  9. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289–300Google Scholar
  10. Blanckenhorn WU (1998) Adaptive phenotypic plasticity in growth, development, and body size in the yellow dung fly. Evolution 52:1394–1407. doi: 10.2307/2411309 CrossRefGoogle Scholar
  11. Bolnick D, Doebeli M (2003) Sexual dimorphism and adaptive speciation: two sides of the same ecological coin. Evolution 57:2433–2449CrossRefPubMedGoogle Scholar
  12. Both C (1998) Experimental evidence for density dependence of reproduction in great tits. J Anim Ecol 67:667–674. doi: 10.1046/j.1365-2656.1998.00228.x CrossRefGoogle Scholar
  13. Buchan JC, Alberts SC, Silk JB, Altmann J (2003) True paternal care in a multi-male primate society. Nature 425:179–181. doi: 10.1038/nature01866 CrossRefPubMedGoogle Scholar
  14. Bürger R, Schneider K, Willensdorfer M (2006) The conditions for speciation through intraspecific competition. Evolution 60:2185–2206CrossRefPubMedGoogle Scholar
  15. Calsbeek R, Smith TB (2007) Probing the adaptive landscape using experimental islands: density-dependent natural selection on lizard body size. Evolution 61:1052–1061. doi: 10.1111/j.1558-5646.2007.00093.x CrossRefPubMedGoogle Scholar
  16. Cavin L (1993) Structure d’une population subalpine de Lézards vivipares (Lacerta vivipara Jacquin 1787). Rev Suisse Zool 100:357–371CrossRefGoogle Scholar
  17. Claessen D, de Roos A, Persson L, de Roos AM (2000) Dwarfs and giants: cannibalism and competition in size-structured populations. Am Nat 155:219–237. doi: 10.1086/303315 CrossRefPubMedGoogle Scholar
  18. Cresswell W (1998) Variation in the strength of interference competition with resource density in blackbirds, Turdus merula. Oikos 81:152–160CrossRefGoogle Scholar
  19. de Roos AM, Persson L (2003) Competition in size-structured populations: mechanisms inducing cohort formation and population cycles. Theor Popul Biol 63:1–16CrossRefPubMedGoogle Scholar
  20. De Roos AM, Persson L, McCauley E (2003) The influence of size-dependent life-history traits on the structure and dynamics of populations and communities. Ecol Lett 6:473–487. doi: 10.1046/j.1461-0248.2003.00458.x CrossRefGoogle Scholar
  21. Ekman J, Griesser M (2002) Why offspring delay dispersal: experimental evidence for a role of parental tolerance. Proc R Soc B Biol Sci 269:1709–1713. doi: 10.1098/rspb.2002.2082 CrossRefGoogle Scholar
  22. Fitze P, Le Galliard J, Federici P et al (2005) Conflict over multiple-partner mating between males and females of the polygynandrous common lizards. Evolution 59:2451–2459. doi: 10.1554/05-208.1 CrossRefPubMedGoogle Scholar
  23. Forrester GE (1990) Factors influencing the juvenile demography of a coral reef fish. Ecology 71:1666–1681CrossRefGoogle Scholar
  24. Gaillard JM, Festa-Bianchet M, Yoccoz NG (1998) Population dynamics of large herbivores: variable recruitment with constant adult survival. Trends Ecol Evol 13:58–63CrossRefPubMedGoogle Scholar
  25. Heulin B (1986) Estival diet and use of trophic resources in 3 populations of Lacerta vivipara. Acta oecol Oecol Gen 7:135–150Google Scholar
  26. Heulin B, Osenegg-Leconte K, Michel D (1997) Demography of a bimodal reproductive species of lizard (Lacerta vivipara): survival and density characteristics of oviparous populations. Herpetologica 53:432–444Google Scholar
  27. Hill C (1992) Interactions between year classes in the benthic amphipod Monoporeia affinis: effects on juvenile survival and growth. Oecologia 91:157–162CrossRefGoogle Scholar
  28. Horváthová T, Cooney CR, Fitze PS et al (2013) Length of activity season drives geographic variation in body size of a widely distributed lizard. Ecol Evol 3:2424–2442. doi: 10.1002/ece3.613 CrossRefGoogle Scholar
  29. Huyghe K, San-Jose LM, Peñalver Alcazar M, Fitze PS (2013) An ecomorphological analysis of the determinants of mating success. Biol J Linn Soc 110:658–664. doi: 10.1111/bij.12140 CrossRefGoogle Scholar
  30. Imre I, Grant JWA, Cunjak RA (2005) Density-dependent growth of young-of-the-year Atlantic salmon Salmo salar in Catamaran Brook, New Brunswick. J Anim Ecol 74:508–516. doi: 10.1111/j.1365-2656.2005.00949.x CrossRefGoogle Scholar
  31. Jenssen TA, Marcellini DL, Buhlmann KA, Goforth PH (1989) Differential infanticide by adult curly-tailed lizards, Leiocephalus schreibersi. Anim Behav 38:1054–1061. doi: 10.1016/S0003-3472(89)80144-7 CrossRefGoogle Scholar
  32. Jones GP (1987) Competitive interactions among adults and juveniles in a coral reef fish. Ecology 68:1534–1547CrossRefGoogle Scholar
  33. Kaspersson R, Höjesjö J, Bohlin T (2012) Habitat exclusion and reduced growth: a field experiment on the effects of inter-cohort competition in young-of-the-year brown trout. Oecologia 169:733–742. doi: 10.1007/s00442-012-2248-5 CrossRefPubMedGoogle Scholar
  34. Kendall BE, Fox GA, Fujiwara M, Nogeire TM (2011) Demographic heterogeneity, cohort selection, and population growth. Ecology 92:1985–1993CrossRefPubMedGoogle Scholar
  35. Khodadoost M, Pilorge T, Ortega A (1987) The variations of density and body size of Lacerta vivipara, as a function of abundance and size of invertebrate prey on Mont-Lozere. Rev d’Écologie-La Terre La Vie 42:193–201Google Scholar
  36. Kinlan BP, Gaines SD (2003) Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology 84:2007–2020CrossRefGoogle Scholar
  37. Lande R, Engen S, Saether B-E (2009) An evolutionary maximum principle for density-dependent population dynamics in a fluctuating environment. Philos Trans R Soc B Biol Sci 364:1511–1518. doi: 10.1098/rstb.2009.0017 CrossRefGoogle Scholar
  38. Le Galliard J-F, Ferrière Clobert J, Ferriere R (2003) Mother-offspring interactions affect natal dispersal in a lizard. Proc R Soc Ser B Biol Sci 270:1163–1169. doi: 10.1098/rspb.2003.2360 CrossRefGoogle Scholar
  39. Le Galliard J-F, Ferrière R, Clobert J (2005) Juvenile growth and survival under dietary restriction: are males and females equal? Oikos 111:368–376. doi: 10.1111/j.0030-1299.2005.14163.x CrossRefGoogle Scholar
  40. Lichtenstein H (1823) Verzeichniss der Doubletten des Zoologischen Museums der Königl. Universität zu Berlin nebst Beschreibung vieler bisher unbekannter Arten von Säugethieren, Vögeln, Amphibien und Fröschen. Trautwein, Berlin, pp 1–118Google Scholar
  41. Lindström J (1999) Early development and fitness in birds and mammals. Trends Ecol Evol 14:343–348. doi: 10.1016/S0169-5347(99)01639-0 CrossRefPubMedGoogle Scholar
  42. Magnussoni WE, Lima AP, Faria AS et al (2001) Size and carbon acquisition in lizards from Amazonian savanna: evidence from isotope analysis. Ecology 82:1772–1780. doi:10.1890/0012-9658(2001)082[1772:SACAIL]2.0.CO;2CrossRefGoogle Scholar
  43. Maindonald J, Braun WJ (2003) Data analysis and graphics using R: an example approach. Cambridge University Press, CambridgeGoogle Scholar
  44. Marchetti K, Price T (1989) Differences in the foraging of juvenile and adult birds: the importance of developmental constraints. Biol Rev 64:51–70. doi: 10.1111/j.1469-185X.1989.tb00638.x CrossRefGoogle Scholar
  45. Maret T, Collins J (1994) Individual responses to population size structure: the role of size variation in controlling expression of a trophic polyphenism. Oecologia 100:279–285CrossRefGoogle Scholar
  46. Massot M, Aragón P (2013) Phenotypic resonance from a single meal in an insectivorous lizard. Curr Biol 23:1320–1323. doi: 10.1016/j.cub.2013.05.047 CrossRefPubMedGoogle Scholar
  47. Massot M, Clobert J, Pilorge T et al (1992) Density dependence in the common lizard: demographic consequences of a density manipulation. Ecology 73:1742–1756CrossRefGoogle Scholar
  48. Meylan S, Clobert J, Sinervo B (2007) Adaptive significance of maternal induction of density-dependent phenotypes. Oikos 116:650–661. doi: 10.1111/j.0030-1299.2007.15432.x Google Scholar
  49. Miller TEX, Rudolf VHW (2011) Thinking inside the box: community-level consequences of stage-structured populations. Trends Ecol Evol 26:457–466. doi: 10.1016/j.tree.2011.05.005 CrossRefPubMedGoogle Scholar
  50. Mugabo M, Marquis O, Perret S, Le Galliard JF (2010) Immediate and delayed life history effects caused by food deprivation early in life in a short-lived lizard. J Evol Biol 23:1886–1898CrossRefPubMedGoogle Scholar
  51. Mugabo M, Perret S, Legendre S, Le Galliard J-F (2013) Density-dependent life history and the dynamics of small populations. J Anim Ecol 82:1227–1239. doi: 10.1111/1365-2656.12109 CrossRefPubMedGoogle Scholar
  52. Nakayama S, Fuiman LA (2010) Body size and vigilance mediate asymmetric interference competition for food in fish larvae. Behav Ecol 21:708–713. doi: 10.1093/beheco/arq043 CrossRefGoogle Scholar
  53. Natusch DJD, Lyons JA (2012) Relationships between ontogenetic changes in prey selection, head shape, sexual maturity, and colour in an Australasian python (Morelia viridis). Biol J Linn Soc 107:269–276. doi: 10.1111/j.1095-8312.2012.01941.x CrossRefGoogle Scholar
  54. Olafsson EB (1986) Density dependence in suspension-feeding and deposit-feeding populations of the bivalve Macoma balthica: a field experiment. J Anim Ecol 55:517–526. doi: 10.2307/4735 CrossRefGoogle Scholar
  55. Pechenik J, Cerulli T (1991) Influence of delayed metamorphosis on survival, growth, and reproduction of the marine polychaete Capitella sp. I. J Exp Mar Bio Ecol 151:17–27CrossRefGoogle Scholar
  56. Pennings PS, Kopp M, Meszéna G et al (2008) An analytically tractable model for competitive speciation. Am Nat 171:E44–E71. doi: 10.1086/523952 CrossRefPubMedGoogle Scholar
  57. Pilorge T (1987) Density, size structure, and reproductive characteristics of three populations of Lacerta vivipara (Sauria: Lacertidae). Herpetologica 43:345–356Google Scholar
  58. Pinheiro J, Bates DM (2000) Mixed effects models in S and S-plus. Springer, New YorkCrossRefGoogle Scholar
  59. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2016) _nlme: linear and nonlinear mixed effects models_R package version 3.1-124, http://CRAN.R-project.org/package=nlme
  60. Polis G (1981) The evolution and dynamics of intraspecific predation. Annu Rev Ecol Syst 12:225–251CrossRefGoogle Scholar
  61. Post J, Parkinson E, Johnston N (1999) Density-dependent processes in structured fish populations: interaction strengths in whole-lake experiments. Ecol Monogr 69:155–175CrossRefGoogle Scholar
  62. R Core Team (2015) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. https://www.R-project.org/
  63. Rudolf VHW, Rasmussen NL (2013) Population structure determines functional differences among species and ecosystem processes. Nat Commun 4:2318. doi: 10.1038/ncomms3318 CrossRefPubMedGoogle Scholar
  64. Sæther B, Visser ME, Grøtan V, Engen S (2016) Evidence for r- and K -selection in a wild bird population: a reciprocal link between eology and evolution. Proc R Soc Lond B 283:20152411CrossRefGoogle Scholar
  65. Samhouri JF, Steele MA, Forrester GE (2009) Inter-cohort competition drives density dependence and selective mortality in a marine fish. Ecology 90:1009–1020. doi: 10.1890/07-1161.1 CrossRefPubMedGoogle Scholar
  66. San-Jose LM, Peñalver-Alcázar M, Milá B et al (2014) Cumulative frequency-dependent selective episodes allow for rapid morph cycles and rock-paper-scissors dynamics in species with overlapping generations. Proc R Soc Lond B 281:20140976. doi: 10.1098/rspb.2014.0976 CrossRefGoogle Scholar
  67. Schoener TW (1983) Field experiments on interspecific competition. Am Nat 122:240–285. doi: 10.1086/284133 CrossRefGoogle Scholar
  68. Shipley B (2000) A new inferential test for path models based on directed acyclic graphs. Struct Equ Model. doi: 10.1207/S15328007SEM0702 Google Scholar
  69. Shipley B (2009) Confirmatory path analysis in a generalized multilevel context. Ecology 90:363–368. doi: 10.1890/08-1034.1 CrossRefPubMedGoogle Scholar
  70. Sinervo B, Heulin B, Surget-Groba Y et al (2007) Models of density-dependent genic selection and a new rock-paper-scissors social system. Am Nat 170:663–680. doi: 10.1086/522092 CrossRefPubMedGoogle Scholar
  71. Stoinski TS, Czekala N, Lukas KE, Maple TL (2002) Urinary androgen and corticoid levels in captive, male Western lowland gorillas (Gorilla g. gorilla): age- and social group-related differences. Am J Primatol 56:73–87. doi: 10.1002/ajp.1065 CrossRefPubMedGoogle Scholar
  72. Szabo A (2002) Experimental tests of intercohort competition for food and cover in the tidepool sculpin (Oligocottus maculosus Girard). Can J Zool 80:137–144CrossRefGoogle Scholar
  73. van de Wolfshaar KE, de Roos AM, Persson L (2008) Population feedback after successful invasion leads to ecological suicide in seasonal environments. Ecology 89:259–268CrossRefPubMedGoogle Scholar
  74. van der Meer J (2006) Metabolic theories in ecology. Trends Ecol Evol 21:136–140. doi: 10.1016/j.tree.2005.11.004 CrossRefPubMedGoogle Scholar
  75. Webster M (2004) Density dependence via intercohort competition in a coral-reef fish. Ecology 85:986–994CrossRefGoogle Scholar
  76. Werner E (1992) Individual behavior and higher-order species interactions. Am Nat 140:S5–S32CrossRefGoogle Scholar
  77. Werner E, Gilliam J (1984) The ontogenetic niche and species interactions in size-structured populations. Annu Rev Ecol Syst 15:393–425CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Luis M. San-Jose
    • 1
    Email author
  • Miguel Peñalver-Alcázar
    • 2
  • Katleen Huyghe
    • 3
  • Merel C. Breedveld
    • 4
    • 5
  • Patrick S. Fitze
    • 1
    • 4
    • 5
    • 6
  1. 1.Department of Ecology and EvolutionUniversity of LausanneLausanneSwitzerland
  2. 2.Department of Biogeography and Global ChangeMuseo Nacional de Ciencias Naturales (MNCN, CSIC)MadridSpain
  3. 3.Department of BiologyUniversity of AntwerpAntwerpBelgium
  4. 4.Department of Biodiversity and Evolutionary BiologyMuseo Nacional de Ciencias Naturales (MNCN, CSIC)MadridSpain
  5. 5.Instituto Pirenaico de Ecología (MNCN, CSIC), Ntra. Señora de la VictoriaJacaSpain
  6. 6.Fundación Araid, Edificio CEEI AragónZaragozaSpain

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