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Behavioral Ecology and Sociobiology

, Volume 66, Issue 9, pp 1363–1373 | Cite as

Untested assumptions about within-species sample size and missing data in interspecific studies

  • László Zsolt GaramszegiEmail author
  • Anders Pape Møller
Methods

Abstract

Phylogenetic comparative studies rely on species-specific data that often contain missing values and/or differ in sample size among species. These phenomena may violate statistical assumptions about the non-random variance component in sampling effort. A major reason why this assumption is often not fulfilled is because the probability of being sampled (i.e., being captured or observed) may depend on species-specific characteristics. Here, we test this assumption by using information on within-species sample sizes and missing data from five independent comparative datasets of European birds. First, we show that the two estimates of data availability (missing values and within-species sample size) are positively correlated and are associated with research effort in general (the number of papers published). Second, we demonstrate biologically meaningful relationships between data availability and phenotypic traits. For example, population size, risk-taking, and habitat specialization independently predicted within-species sample size. The key determinants of missing data were population size and distribution range. However, data availability was not structured by phylogenetic relationships. These results indicate that the accuracy of sampling is repeatable and distributed non-randomly among species, as several species-specific attributes determined the probability of observation. Therefore, data availability seems to be a species-specific trait that can be shaped by ecology, life history, and behavior. Such relationships raise issues about non-random sampling, which requires attention in comparative studies.

Keywords

Generalized least squares Independent contrasts Personality Research philosophy Statistics Trappability Weighted regression 

Notes

Acknowledgments

During this study LZG received a “Ramon y Cajal” research grant from the Spanish National Research Council (Consejo Superior de Investigaciones Científicas—CSIC, Spain). The study was supported by the ‘Plan Nacional’ program of the Spanish government (grant numbers: CGL2009-09439 and CGL2009-10652).

References

  1. Abouheif E (1999) A method for testing the assumption of phylogenetic independence in comparative data. Evol Ecol Res 1:895–909Google Scholar
  2. Ackerly DD (2000) Taxon sampling, correlated evolution, and independent contrasts. Evolution 54:1480–1492PubMedGoogle Scholar
  3. Arnold C, Nunn CL (2010) Phylogenetic targeting of research effort in evolutionary biology. Am Nat 176:601–612PubMedCrossRefGoogle Scholar
  4. Badyaev AV (1997) Altitudinal variation in sexual dimorphism: a new patern and alternative hypotheses. Behav Ecol 8:675–690CrossRefGoogle Scholar
  5. Belliure J, Sorci G, Møller AP, Clobert J (2000) Dispersal distances predict subspecies richness in birds. J Evol Biol 13:480–487CrossRefGoogle Scholar
  6. Bennett PM, Owens IPF (2002) Evolutionary ecology of birds. Oxford University Press, OxfordGoogle Scholar
  7. Bennett GF, Thommes F, Blancou J, Artois M (1982) Blood parasites of some birds from the Lorraine region, France. J Wildl Dis 18:81–88PubMedGoogle Scholar
  8. Blondel J, Catzeflis F, Perret P (1996) Molecular phylogeny and the historical biogeography of the warblers of the genus Sylvia (Aves). J Evol Biol 9:871–891CrossRefGoogle Scholar
  9. Blumstein DT (2003) Flight-initiation distance in birds is dependent on intruder starting distance. J Wildl Manag 67:852–857CrossRefGoogle Scholar
  10. Burfield I, van Bommel F (2004) Birds in Europe. BirdLife International, CambridgeGoogle Scholar
  11. Burger J, Gochfeld M (1991a) Human activity influence and diurnal and nocturnal foraging of sanderlings (Calidris alba). Condor 93:259–265CrossRefGoogle Scholar
  12. Burger J, Gochfeld M (1991b) Human distance and birds: tolerance and response distances of resident and migrant species in India. Environ Conserv 18:158–165CrossRefGoogle Scholar
  13. Cardillo M (2002) The life-history basis of latitudinal diversity gradients: how do species traits vary from the poles to the equator. J Anim Ecol 71:79–87CrossRefGoogle Scholar
  14. Cibois A, Pasquet E (1999) Molecular analysis of the phylogeny of 11 genera of the Corvidea. Ibis 141:297–306CrossRefGoogle Scholar
  15. Cohen J (1988) Statistical power analysis for the behavioural sciences, 2nd edn. Lawrence Erlbaum Associates, HillsdaleGoogle Scholar
  16. Cramp S, Perrins CM (eds) (1977–1994) The birds of the Western Palearctic, vol 4-9. Oxford University Press, OxfordGoogle Scholar
  17. Dickinson EC (ed) (2003) The Howard and Moore complete checklist of the birds of the world, 3rd edn. Princeton University Press, PrincetonGoogle Scholar
  18. Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15CrossRefGoogle Scholar
  19. Felsenstein J (2008) Comparative methods with sampling error and within-species variation: contrasts revisited and revised. Am Nat 171:713–725PubMedCrossRefGoogle Scholar
  20. Fernández-Juricic E, Jimenez MD, Lucas E (2001) Alert distance as an alternative measure of bird tolerance to human disturbance: implications for park design. Environ Conserv 28:263–269CrossRefGoogle Scholar
  21. Fernández-Juricic E, Jimenez MD, Lucas E (2002) Factors affecting intra- and inter-specific variations in the difference between alert and flight distances in forested habitats. Can J Zool 80:1212–1220CrossRefGoogle Scholar
  22. Fisher DO, Blomberg SP, Owens IPF (2003) Extrinsic versus intrinsic factors in the decline and extinction of Australian marsupials. Proc R Soc Lond B 270:1801–1808CrossRefGoogle Scholar
  23. Freckleton RP (2009) The seven deadly sins of comparative analysis. J Evol Biol 22:1367–1375PubMedCrossRefGoogle Scholar
  24. Freckleton RP (2011) Dealing with collinearity in behavioural and ecological data: model averaging and the problems of measurement error. Behav Ecol Sociobiol 65:91–101CrossRefGoogle Scholar
  25. Freckleton RP, Harvey PH, Pagel M (2002) Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 160:712–726PubMedCrossRefGoogle Scholar
  26. Garamszegi LZ (2006) Comparing effect sizes across variables: generalization without the need for Bonferroni correction. Behav Ecol 17:682–687CrossRefGoogle Scholar
  27. Garamszegi LZ, Møller AP (2010) Effects of sample size and intraspecific variation in phylogenetic comparative studies: a meta-analytic review. Biol Rev 85:797–805PubMedGoogle Scholar
  28. Garamszegi LZ, Møller AP (2011) Nonrandom variation in within-species sample size and missing data in phylogenetic comparative studies. Syst Biol 60:876–880PubMedCrossRefGoogle Scholar
  29. Garamszegi LZ, Møller AP, Erritzøe J (2002) Coevolving avian eye size and brain size in relation to prey capture and nocturnality. Proc R Soc Lond B 269:961–967CrossRefGoogle Scholar
  30. Garamszegi LZ, Eens M, Erritzøe J, Møller AP (2005) Sperm competition and sexually size dimorphic brains in birds. Proc R Soc Lond B 272:159–166CrossRefGoogle Scholar
  31. Garamszegi LZ, Calhim S, Dochtermann N, Hegyi G, Hurd PL, Jørgensen C, Kutsukake N, Lajeunesse MJ, Pollard KA, Schielzeth H, Symonds MRE, Nakagawa S (2009a) Changing philosophies and tools for statistical inferences in behavioral ecology. Behav Ecol 20:1363–1375CrossRefGoogle Scholar
  32. Garamszegi LZ, Eens M, Török J (2009b) Behavioural syndromes and trappability in free-living collared flycatchers, Ficedula albicollis. Anim Behav 77:803–812CrossRefGoogle Scholar
  33. Glutz von Blotzheim UN, Bauer KM (eds) (1966–1997) Handbuch der Vögel Mitteleuropas, vol 1-15. Aula-Verlag, WiebelsheimGoogle Scholar
  34. Haberkorn A (1984) Observations on malaria in European perching birds (Passeriformes). Zbl Bakt Mik Hyg M 256:288–295Google Scholar
  35. Harmon LJ, Losos JB (2005) The effect of intraspecific sample size on type I and type II error rates in comparative studies. Evolution 59:2705–2710PubMedGoogle Scholar
  36. Ishak HD, Dumbacher JP, Anderson NL, Keane JJ, Valkiūnas G, Haig SM, Tell LA, Sehgal RNM (2008) Blood parasites in owls with conservation implications for the spotted owl (Strix occidentalis). PLoS One 3:e2304PubMedCrossRefGoogle Scholar
  37. Ives AR, Midford PE, Garland T (2007) Within-species variation and measurement error in phylogenetic comparative methods. Syst Biol 56:252–270PubMedCrossRefGoogle Scholar
  38. Iwaniuk AN, Nelson JE (2002) Can endocranial volume be used as an estimate of brain size in birds? Can J Zool 80:16–23CrossRefGoogle Scholar
  39. Iwaniuk AN, Nelson JE (2003) Developmental differences are correlated with relative brain size in birds: a comparative analysis. Can J Zool 81:1913–1928CrossRefGoogle Scholar
  40. Jeschke JM, Kokko H (2009) The roles of body size and phylogeny in fast and slow life histories. Evol Ecol 23:867–878CrossRefGoogle Scholar
  41. Kamilar JM, Bribiescas RG, Bradley BJ (2010) Is group size related to longevity in mammals? Biol Lett 6:736–739PubMedCrossRefGoogle Scholar
  42. Krone O, Priemer J, Streich J, Sommer P, Langgemach T, Lessow O (2001) Haemosporida of birds of prey and owls from Germany. Acta Protozool 40:281–289Google Scholar
  43. Krone O, Waldenström J, Valkiunas G, Lessow O, Müller K, Iezhova TA, Fickel J, Bensch S (2008) Haemosporidian blood parasites in European birds of prey and owls. J Parasitol 94:709–715PubMedGoogle Scholar
  44. Leisler B, Heidrich P, Schulze-Hagen K, Wink M (1997) Taxonomy and phylogeny of reed warblers (genus Acrocephalus) based on mtDNA sequences and morphology. J Ornithol 138:469–496CrossRefGoogle Scholar
  45. Maddison WP (2000) Testing character correlation using pairwise comparisons on a phylogeny. J Theor Biol 202:195–204PubMedCrossRefGoogle Scholar
  46. Malmkvist J, Hansen SW (2001) The welfare of farmed mink (Mustela vison) in relation to behavioural selection: a review. Anim Welf 10:41–52Google Scholar
  47. Martins EP, Hansen TF (1997) Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. Am Nat 149:646–667CrossRefGoogle Scholar
  48. Mendes L, Piersma T, Lecoq M, Spaans B, Ricklefs RE (2005) Disease-limited distributions? Contrasts in the prevalence of avian malaria in shorebird species using marine and freshwater habitats. Oikos 109:396–404CrossRefGoogle Scholar
  49. Merino S, Potti J, Fargallo JA (1997) Blood parasites of passerine birds from central Spain. J Wildl Dis 33:638–641PubMedGoogle Scholar
  50. Mills AD, Faure JM (2000) Ease of capture in lines of Japanese quail (Coturnix japonica) subjected to contrasting selection for fear or sociability. Appl Anim Behav Sci 69:125–134PubMedCrossRefGoogle Scholar
  51. Mitani JC, GrosLouis J, Manson JH (1996) Number of males in primate groups: comparative tests of competing hypotheses. Am J Primatol 38:315–332CrossRefGoogle Scholar
  52. Møller AP (2006a) Senescence in relation to latitude and migration in birds. J Evol Biol 20:750–757CrossRefGoogle Scholar
  53. Møller AP (2006b) Sociality, age at first reproduction and senescence: comparative analyses of birds. J Evol Biol 19:682–689PubMedCrossRefGoogle Scholar
  54. Møller AP (2008a) Flight distance and blood parasites in birds. Behav Ecol 19:1305–1313CrossRefGoogle Scholar
  55. Møller AP (2008b) Flight distance and population trends in breeding birds. Behav Ecol 19:1095–1102CrossRefGoogle Scholar
  56. Møller AP (2008c) Flight distance of urban birds, predation and selection for urban life. Behav Ecol Sociobiol 63:63–75CrossRefGoogle Scholar
  57. Møller AP (2008d) Relative longevity and field metabolic rate in birds. J Evol Biol 21:1379–1386PubMedCrossRefGoogle Scholar
  58. Møller AP (2009) Successful city dwellers: a comparative study of the ecological characteristics of urban birds in the Western Palearctic. Oecologia 159:849–858PubMedCrossRefGoogle Scholar
  59. Møller AP (2012) Behavioral and ecological predictors of urbanization. In: Gil D, Brumm H (eds) Avian urban ecology. Oxford University Press, Oxford (in press)Google Scholar
  60. Møller AP, Merino S, Brown CR, Robertson RJ (2001) Immune defense and host sociality: a comparative study of swallows and martins. Am Nat 158:136–145PubMedCrossRefGoogle Scholar
  61. Møller AP, Erritzøe J, Saino N (2003) Seasonal changes in immune response and parasite impact on hosts. Am Nat 161:657–671PubMedCrossRefGoogle Scholar
  62. Møller AP, Martín-Vivaldi M, Soler JJ (2004) Parasitism, host immune defence and dispersal. J Evol Biol 17:603–612PubMedCrossRefGoogle Scholar
  63. Møller AP, Erritzøe J, Garamszegi LZ (2005) Covariation between brain size and immunity in birds: implications for brain size evolution. J Evol Biol 18:223–237PubMedCrossRefGoogle Scholar
  64. Møller AP, Garamszegi LZ, Spottiswoode C (2008a) Genetic similarity, breeding distribution range and sexual selection. J Evol Biol 21:213–225PubMedCrossRefGoogle Scholar
  65. Møller AP, Nielsen JT, Garamszegi LZ (2008b) Risk taking by singing males. Behav Ecol 19:41–53CrossRefGoogle Scholar
  66. Møller AP, Garamszegi LZ, Peralta-Sanchez JM, Soler JJ (2011) Migratory divides and their consequences for dispersal, population size and parasite–host interactions. J Evol Biol 24:1744–1755. doi: 10.1111/j.1420-9101.2011.02302.x PubMedCrossRefGoogle Scholar
  67. Nakagawa S, Cuthill IC (2007) Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev 82:591–605PubMedCrossRefGoogle Scholar
  68. Nakagawa S, Freckleton R (2008) Missing inaction: the dangers of ignoring missing data. Trends Ecol Evol 23:592–596. doi: 10.1016/j.tree.2008.06.014 PubMedCrossRefGoogle Scholar
  69. Nakagawa S, Freckleton RP (2011) Model averaging, missing data and multiple imputation: a case study for behavioural ecology. Behav Ecol Sociobiol 65:103–116CrossRefGoogle Scholar
  70. Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884PubMedCrossRefGoogle Scholar
  71. Palinauskas V, Markovets MY, Kosarev VV, Efremov VD, Sokolov LV, Valkiûnas G (2005) Occurrence of avian haematozoa in Ekaterinburg and Irkutsk districts of Russia. Ekologija 4:8–12Google Scholar
  72. Paradis E (2011) Analysis of phylogenetics and evolution with R, 2nd edn. Springer, BerlinGoogle Scholar
  73. Phillimore AB, Orme CDL, Davies RG, Hadfield JD, Reed WJ, Gaston KJ, Freckleton RP, Owens IPF (2007) Biogeographical basis of recent phenotypic divergence among birds: a global study of subspecies richness. Evolution 61:942–957PubMedCrossRefGoogle Scholar
  74. Réale D, Gallant BY, Leblanc M, Festa-Bianchet M (2000) Consistency of temperament in bighorn ewes and correlates with behaviour and life history. Anim Behav 60:589–597PubMedCrossRefGoogle Scholar
  75. Seibold I, Helbig AJ, Wink M (1993) Molecular systematics of falcons (family Falconidae). Naturwissenschaften 80:87–90CrossRefGoogle Scholar
  76. Sheldon FH, Slikas B, Kinnarney M, Gill FB, Zhao E, Silverin B (1992) DNA–DNA hybridization evidence of phylogenetic relationships among major lineages of Parus. Auk 109:173–185Google Scholar
  77. Shurulinkov P, Golemansky V (2003) Plasmodium and Leucocytozoon (Sporozoa: Haemosporida) of wild birds in Bulgaria. Acta Protozool 42:205–214Google Scholar
  78. Sibley CG, Ahlquist JE (1990) Phylogeny and classification of birds: a study in molecular evolution. Yale University Press, New HavenGoogle Scholar
  79. Suhonen J, Alatalo RV, Gustafsson L (1994) Evolution of foraging ecology in Fennoscandian tits (Parus spp.). Proc R Soc Lond B 258:127–131CrossRefGoogle Scholar
  80. Valkiūnas G, Iezhova T, Golemansky V, Pilarska D, Zehtindjiev P (1999) Blood protozoan parasites (Protozoa: Kinetoplastida and Haemosporida) in wild birds from Bulgaria. Acta Zool Bulg 51:127–129Google Scholar
  81. Valkiunas G, Iezhova TA, Krizanauskiene A, Palinauskas V, Sehgal RNM, Bensch S (2008) A comparative analysis of microscopy and PCR-based detection methods for blood parasites. J Parasitol 94:1395–1401PubMedCrossRefGoogle Scholar
  82. Vitone ND, Altizer S, Nunn CL (2004) Body size, diet and sociality influence the species richness of parasitic worms in anthropoid primates. Evol Ecol Res 6:183–199Google Scholar
  83. Webster AJ, Gittleman JL, Purvis A (2004) The life history legacy of evolutionary body size change in carnivores. J Evol Biol 17:396–407PubMedCrossRefGoogle Scholar
  84. Westoby M (1999) Generalization in functional plant ecology: the species sampling problem, plant ecology strategy schemes, and phylogeny. In: Pugnaire FI, Valladares F (eds) Handbook of functional plant ecology. M. Dekker, New York, pp 847–872Google Scholar
  85. Westoby M (2002) Choosing species to study. Trends Ecol Evol 17:587CrossRefGoogle Scholar
  86. Wiersch SC, Lubjuhn T, Maier WA, Kampen H (2007) Haemosporidian infection in passerine birds from Lower Saxony. J Ornithol 148:17–24CrossRefGoogle Scholar
  87. Wilson DS, Coleman K, Clark AB, Biederman L (1993) Shy bold continuum in pumpkinseed sunfish (Lepomis gibbosus)—an ecological study of a psychological trait. J Comp Psychol 107:250–260CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • László Zsolt Garamszegi
    • 1
    Email author
  • Anders Pape Møller
    • 2
  1. 1.Department of Evolutionary EcologyEstacion Biologica de Donana-CSICSevilleSpain
  2. 2.Laboratoire d’Ecologie, Systématique et Evolution, CNRS UMR 8079Université Paris-SudOrsay CedexFrance

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