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

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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.

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References

  • Abouheif E (1999) A method for testing the assumption of phylogenetic independence in comparative data. Evol Ecol Res 1:895–909

    Google Scholar 

  • Ackerly DD (2000) Taxon sampling, correlated evolution, and independent contrasts. Evolution 54:1480–1492

    PubMed  CAS  Google Scholar 

  • Arnold C, Nunn CL (2010) Phylogenetic targeting of research effort in evolutionary biology. Am Nat 176:601–612

    Article  PubMed  Google Scholar 

  • Badyaev AV (1997) Altitudinal variation in sexual dimorphism: a new patern and alternative hypotheses. Behav Ecol 8:675–690

    Article  Google Scholar 

  • Belliure J, Sorci G, Møller AP, Clobert J (2000) Dispersal distances predict subspecies richness in birds. J Evol Biol 13:480–487

    Article  Google Scholar 

  • Bennett PM, Owens IPF (2002) Evolutionary ecology of birds. Oxford University Press, Oxford

    Google Scholar 

  • Bennett GF, Thommes F, Blancou J, Artois M (1982) Blood parasites of some birds from the Lorraine region, France. J Wildl Dis 18:81–88

    PubMed  CAS  Google Scholar 

  • Blondel J, Catzeflis F, Perret P (1996) Molecular phylogeny and the historical biogeography of the warblers of the genus Sylvia (Aves). J Evol Biol 9:871–891

    Article  Google Scholar 

  • Blumstein DT (2003) Flight-initiation distance in birds is dependent on intruder starting distance. J Wildl Manag 67:852–857

    Article  Google Scholar 

  • Burfield I, van Bommel F (2004) Birds in Europe. BirdLife International, Cambridge

    Google Scholar 

  • Burger J, Gochfeld M (1991a) Human activity influence and diurnal and nocturnal foraging of sanderlings (Calidris alba). Condor 93:259–265

    Article  Google Scholar 

  • Burger J, Gochfeld M (1991b) Human distance and birds: tolerance and response distances of resident and migrant species in India. Environ Conserv 18:158–165

    Article  Google Scholar 

  • 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 71:79–87

    Article  Google Scholar 

  • Cibois A, Pasquet E (1999) Molecular analysis of the phylogeny of 11 genera of the Corvidea. Ibis 141:297–306

    Article  Google Scholar 

  • Cohen J (1988) Statistical power analysis for the behavioural sciences, 2nd edn. Lawrence Erlbaum Associates, Hillsdale

    Google Scholar 

  • Cramp S, Perrins CM (eds) (1977–1994) The birds of the Western Palearctic, vol 4-9. Oxford University Press, Oxford

  • Dickinson EC (ed) (2003) The Howard and Moore complete checklist of the birds of the world, 3rd edn. Princeton University Press, Princeton

    Google Scholar 

  • Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15

    Article  Google Scholar 

  • Felsenstein J (2008) Comparative methods with sampling error and within-species variation: contrasts revisited and revised. Am Nat 171:713–725

    Article  PubMed  Google Scholar 

  • 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 28:263–269

    Article  Google Scholar 

  • 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 80:1212–1220

    Article  Google Scholar 

  • Fisher DO, Blomberg SP, Owens IPF (2003) Extrinsic versus intrinsic factors in the decline and extinction of Australian marsupials. Proc R Soc Lond B 270:1801–1808

    Article  Google Scholar 

  • Freckleton RP (2009) The seven deadly sins of comparative analysis. J Evol Biol 22:1367–1375

    Article  PubMed  CAS  Google Scholar 

  • Freckleton RP (2011) Dealing with collinearity in behavioural and ecological data: model averaging and the problems of measurement error. Behav Ecol Sociobiol 65:91–101

    Article  Google Scholar 

  • Freckleton RP, Harvey PH, Pagel M (2002) Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 160:712–726

    Article  PubMed  CAS  Google Scholar 

  • Garamszegi LZ (2006) Comparing effect sizes across variables: generalization without the need for Bonferroni correction. Behav Ecol 17:682–687

    Article  Google Scholar 

  • Garamszegi LZ, Møller AP (2010) Effects of sample size and intraspecific variation in phylogenetic comparative studies: a meta-analytic review. Biol Rev 85:797–805

    PubMed  Google Scholar 

  • Garamszegi LZ, Møller AP (2011) Nonrandom variation in within-species sample size and missing data in phylogenetic comparative studies. Syst Biol 60:876–880

    Article  PubMed  Google Scholar 

  • 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 269:961–967

    Article  Google Scholar 

  • Garamszegi LZ, Eens M, Erritzøe J, Møller AP (2005) Sperm competition and sexually size dimorphic brains in birds. Proc R Soc Lond B 272:159–166

    Article  Google Scholar 

  • 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 20:1363–1375

    Article  Google Scholar 

  • Garamszegi LZ, Eens M, Török J (2009b) Behavioural syndromes and trappability in free-living collared flycatchers, Ficedula albicollis. Anim Behav 77:803–812

    Article  Google Scholar 

  • Glutz von Blotzheim UN, Bauer KM (eds) (1966–1997) Handbuch der Vögel Mitteleuropas, vol 1-15. Aula-Verlag, Wiebelsheim

  • Haberkorn A (1984) Observations on malaria in European perching birds (Passeriformes). Zbl Bakt Mik Hyg M 256:288–295

    CAS  Google Scholar 

  • Harmon LJ, Losos JB (2005) The effect of intraspecific sample size on type I and type II error rates in comparative studies. Evolution 59:2705–2710

    PubMed  Google Scholar 

  • 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:e2304

    Article  PubMed  Google Scholar 

  • Ives AR, Midford PE, Garland T (2007) Within-species variation and measurement error in phylogenetic comparative methods. Syst Biol 56:252–270

    Article  PubMed  Google Scholar 

  • Iwaniuk AN, Nelson JE (2002) Can endocranial volume be used as an estimate of brain size in birds? Can J Zool 80:16–23

    Article  Google Scholar 

  • Iwaniuk AN, Nelson JE (2003) Developmental differences are correlated with relative brain size in birds: a comparative analysis. Can J Zool 81:1913–1928

    Article  Google Scholar 

  • Jeschke JM, Kokko H (2009) The roles of body size and phylogeny in fast and slow life histories. Evol Ecol 23:867–878

    Article  Google Scholar 

  • Kamilar JM, Bribiescas RG, Bradley BJ (2010) Is group size related to longevity in mammals? Biol Lett 6:736–739

    Article  PubMed  Google Scholar 

  • Krone O, Priemer J, Streich J, Sommer P, Langgemach T, Lessow O (2001) Haemosporida of birds of prey and owls from Germany. Acta Protozool 40:281–289

    Google Scholar 

  • 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 94:709–715

    PubMed  CAS  Google Scholar 

  • 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 138:469–496

    Article  Google Scholar 

  • Maddison WP (2000) Testing character correlation using pairwise comparisons on a phylogeny. J Theor Biol 202:195–204

    Article  PubMed  CAS  Google Scholar 

  • Malmkvist J, Hansen SW (2001) The welfare of farmed mink (Mustela vison) in relation to behavioural selection: a review. Anim Welf 10:41–52

    Google Scholar 

  • 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 149:646–667

    Article  Google Scholar 

  • 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 109:396–404

    Article  Google Scholar 

  • Merino S, Potti J, Fargallo JA (1997) Blood parasites of passerine birds from central Spain. J Wildl Dis 33:638–641

    PubMed  CAS  Google Scholar 

  • 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 69:125–134

    Article  PubMed  Google Scholar 

  • Mitani JC, GrosLouis J, Manson JH (1996) Number of males in primate groups: comparative tests of competing hypotheses. Am J Primatol 38:315–332

    Article  Google Scholar 

  • Møller AP (2006a) Senescence in relation to latitude and migration in birds. J Evol Biol 20:750–757

    Article  Google Scholar 

  • Møller AP (2006b) Sociality, age at first reproduction and senescence: comparative analyses of birds. J Evol Biol 19:682–689

    Article  PubMed  Google Scholar 

  • Møller AP (2008a) Flight distance and blood parasites in birds. Behav Ecol 19:1305–1313

    Article  Google Scholar 

  • Møller AP (2008b) Flight distance and population trends in breeding birds. Behav Ecol 19:1095–1102

    Article  Google Scholar 

  • Møller AP (2008c) Flight distance of urban birds, predation and selection for urban life. Behav Ecol Sociobiol 63:63–75

    Article  Google Scholar 

  • Møller AP (2008d) Relative longevity and field metabolic rate in birds. J Evol Biol 21:1379–1386

    Article  PubMed  Google Scholar 

  • Møller AP (2009) Successful city dwellers: a comparative study of the ecological characteristics of urban birds in the Western Palearctic. Oecologia 159:849–858

    Article  PubMed  Google Scholar 

  • Møller AP (2012) Behavioral and ecological predictors of urbanization. In: Gil D, Brumm H (eds) Avian urban ecology. Oxford University Press, Oxford (in press)

  • Møller AP, Merino S, Brown CR, Robertson RJ (2001) Immune defense and host sociality: a comparative study of swallows and martins. Am Nat 158:136–145

    Article  PubMed  Google Scholar 

  • Møller AP, Erritzøe J, Saino N (2003) Seasonal changes in immune response and parasite impact on hosts. Am Nat 161:657–671

    Article  PubMed  Google Scholar 

  • Møller AP, Martín-Vivaldi M, Soler JJ (2004) Parasitism, host immune defence and dispersal. J Evol Biol 17:603–612

    Article  PubMed  Google Scholar 

  • Møller AP, Erritzøe J, Garamszegi LZ (2005) Covariation between brain size and immunity in birds: implications for brain size evolution. J Evol Biol 18:223–237

    Article  PubMed  Google Scholar 

  • Møller AP, Garamszegi LZ, Spottiswoode C (2008a) Genetic similarity, breeding distribution range and sexual selection. J Evol Biol 21:213–225

    Article  PubMed  Google Scholar 

  • Møller AP, Nielsen JT, Garamszegi LZ (2008b) Risk taking by singing males. Behav Ecol 19:41–53

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Nakagawa S, Cuthill IC (2007) Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev 82:591–605

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Nakagawa S, Freckleton RP (2011) Model averaging, missing data and multiple imputation: a case study for behavioural ecology. Behav Ecol Sociobiol 65:103–116

    Article  Google Scholar 

  • Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884

    Article  PubMed  CAS  Google Scholar 

  • 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 4:8–12

    Google Scholar 

  • Paradis E (2011) Analysis of phylogenetics and evolution with R, 2nd edn. Springer, Berlin

    Google Scholar 

  • 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 61:942–957

    Article  PubMed  Google Scholar 

  • 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 60:589–597

    Article  PubMed  Google Scholar 

  • Seibold I, Helbig AJ, Wink M (1993) Molecular systematics of falcons (family Falconidae). Naturwissenschaften 80:87–90

    Article  CAS  Google Scholar 

  • 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 109:173–185

    Google Scholar 

  • Shurulinkov P, Golemansky V (2003) Plasmodium and Leucocytozoon (Sporozoa: Haemosporida) of wild birds in Bulgaria. Acta Protozool 42:205–214

    Google Scholar 

  • Sibley CG, Ahlquist JE (1990) Phylogeny and classification of birds: a study in molecular evolution. Yale University Press, New Haven

    Google Scholar 

  • Suhonen J, Alatalo RV, Gustafsson L (1994) Evolution of foraging ecology in Fennoscandian tits (Parus spp.). Proc R Soc Lond B 258:127–131

    Article  Google Scholar 

  • 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 51:127–129

    Google Scholar 

  • 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 94:1395–1401

    Article  PubMed  CAS  Google Scholar 

  • 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 6:183–199

    Google Scholar 

  • Webster AJ, Gittleman JL, Purvis A (2004) The life history legacy of evolutionary body size change in carnivores. J Evol Biol 17:396–407

    Article  PubMed  CAS  Google Scholar 

  • 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 847–872

    Google Scholar 

  • Westoby M (2002) Choosing species to study. Trends Ecol Evol 17:587

    Article  Google Scholar 

  • Wiersch SC, Lubjuhn T, Maier WA, Kampen H (2007) Haemosporidian infection in passerine birds from Lower Saxony. J Ornithol 148:17–24

    Article  Google Scholar 

  • 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 107:250–260

    Article  Google Scholar 

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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).

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Correspondence to László Zsolt Garamszegi.

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Communicated by E. Fernandez-Juricic

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Garamszegi, L.Z., Møller, A.P. Untested assumptions about within-species sample size and missing data in interspecific studies. Behav Ecol Sociobiol 66, 1363–1373 (2012). https://doi.org/10.1007/s00265-012-1370-z

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