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Type I errors linked to faulty statistical analyses of endangered subspecies classifications. (English) Zbl 1306.62340

Summary: Legal issues related to subspecies identification frequently occur through the implementation of the 1973 Endangered Species Act (ESA). A listing under the ESA requires management actions to ensure the continued existence of the taxa. However, these actions often have important social, economic, and political implications. We examined the statistical methods of morphological analysis used in subspecies identification. Methods are illustrated using the California gnatcatcher (Polioptila californica), which was incorrectly listed under the ESA due to misinterpretation of morphological data. We found that inferences based on tests of sample means (i.e., \(t\)-test, Hotelling’s \(T^2\)-statistics), cluster analysis, and discriminant analysis were subject to high rates of false positives (identification of subspecies when none exist; Type I error). These simple tests ignore the common occurrence of spatial clines in animal tracts. Alternatively, spline-regression and step-regression procedures were found to be quite robust yet had high resolution in finding subspecies break locations.

MSC:

62P12 Applications of statistics to environmental and related topics

Software:

spatial
Full Text: DOI

References:

[1] Ahlberg, J. H., Nilson, E. N., and Walsh, J. L. (1967), The Theory of Splines and Their Applications, New York: Academic Press. · Zbl 0158.15901
[2] Allendorf, F. W., and Luikart, G. (2007), Conservation and the Genetics of Population, Malden, MA: Blackwell Publishing.
[3] Anderson, T. W. (1984), An Introduction to Multivariate Statistical Methods, New York: Wiley. · Zbl 0651.62041
[4] Atwood, J. L. (1988), ”Speciation and Geographic Variation in Black-Tailed Gnatcatchers,” Ornithological Monograph, 42.
[5] – (1991), ”Species Limits and Geographic Patterns of Morphological Variations in California Gnatcatchers (Polioptila Californica),” Bulletin of Southern California Academy of Sciences, 90, 118–133.
[6] Beckman, R. J., and Cook, R. D. (1979), ”Testing for Two Phase Regression,” Technometrics, 21, 65–69. · doi:10.1080/00401706.1979.10489723
[7] Beeny, L. (2001), ”The Name of the Game: Changes in Sage Grouse Taxonomy Raise New Issues in Management and Conservation of the Birds,” Wyoming Wildlife, 65, 16–23.
[8] Bernatchez, L. (1995), ”A Role for Molecular Systematics in Defining Evolutionary Significant Units in Fishes,” in Evolution and the Aquatic Ecosystem: Defining Unique Units in Population Conservation, Bethesda, MD: American Fisheries Society, pp. 114–132.
[9] Bhattacharya, P. K., and Frierson, F. J. (1981), ”A Nonparametric Control Chart for Detecting Small Disorders,” The American Statistician, 9, 544–554. · Zbl 0503.62077
[10] Bock, H.-H. (1996), ”Probability Models and Hypotheses Testing in Partitioning Cluster Analysis,” in Clustering and Classification, eds. P. Arabie, L. J. Hubert, and G. De Soete, River Edge, NJ: World Scientific, pp. 377–453. · Zbl 1031.62504
[11] Bozdogan, H. (1993), ”Choosing the Number of Component Clusters in the Mixture Model Using a New Informational Complexity Criterion of the Inverse Fisher Information Matrix,” in Information and Classification: Concepts, Methods and Applications: Proceedings of the 16th Annual Conference of The ”Gesellschaft Fur Klassifikati (Lecture Notes in Mathematics), eds. O. Opitz, B. Lausen, and K. Rudiger, Berlin: Springer, pp. 40–54.
[12] Brodsky, B. E., and Darkhovsky, B. S. (1989), ”A Nonparametric Method for Detection of Switching Times for Two Random Sequences,” Avtomatika i Telemekhanika, 10, 66–75.
[13] – (1993), Nonparametric Methods in Change-Point Problems, Dordrecht, The Netherlands: Klumer Academic Publishers. · Zbl 0779.62031
[14] Calinski, T., and Harabasz, J. (1974), ”A Dendrite Method for Cluster Analysis,” Communications in Statistics, 3, 1–27. · Zbl 0273.62010 · doi:10.1080/03610928308827180
[15] Cavalli-Sforza, L. L., and Edwards, A. W. F. (1967), ”Phylogenetic Analysis: Models and Estimation Procedures,” Evolution, 32, 550–570. · doi:10.2307/2406616
[16] Conner, M. M., Shenk, T. M., and Miller, E. H. (2003), ”Distinguishing Zapus Hudsonius Preblei from Zapus Princeps Princeps by Using Repeated Cranial Measurements,” Journal of Mammalogy, 84, 1456–1463. · doi:10.1644/BEM-020
[17] Cox, C. B., and Moore, P. D. (2005), Biogeography: An Ecological and Evolutionary Approach (7th ed.), Malden, MA: Blackwell Publishing.
[18] Cressie, N. A. C. (1993), Statistics for Spatial Data, New York: Wiley. · Zbl 0825.62477
[19] Cronin, M. A. (2003), ”Research on Deer Taxonomy and Its Relevance to Management,” Ecoscience, 10, 432–442.
[20] Darkhovsky, B. S. (1976), ”Nonparametric Method for Detection of the Change-Point of a Random Sequence,” Teoriia veroiatnostei i ee primeneniia, 21, 180–184.
[21] Dobey, S., et al. (2005), ”Ecology of Florida Black Bears in the Okefenokee-Osceola Ecosystem,” Wildlife Monographs, 158, 1–41.
[22] Duda, R. O., and Hart, P. E. (1973), Pattern Recognition and Science Analysis, New York: Wiley. · Zbl 0277.68056
[23] Engelman, L., and Hartigan, J. A. (1969), ”Percentage Points of a Test for Clusters,” Journal of the American Statistical Association, 64, 1647–1648. · doi:10.1080/01621459.1969.10501084
[24] Everitt, B. S. (1993), Cluster Analysis, New York: Halstead Press. · Zbl 0507.62060
[25] Everitt, B. S., Landau, S., and Leese, M. (2001), Cluster Analysis (4th ed.), London: Arnold. · Zbl 1205.62076
[26] Farley, J. V., and Hinich, M. J. (1970), ”A Test for a Shifting Slope Coefficient in a Linear Model,” Journal of the American Statistical Association, 64, 1320–1329. · Zbl 0214.46502 · doi:10.1080/01621459.1970.10481167
[27] Farris, J. S. (1973), ”A Probability Model for Inferring Evolutionary Trees,” Systematic Zoology, 22, 250–256. · doi:10.2307/2412305
[28] Feder, P. I. (1975), ”The Log Likelihood Ratio in Segmented Regression,” The Annals of Statistics, 3, 84–97. · Zbl 0324.62015 · doi:10.1214/aos/1176343000
[29] Felsenstein, J. (1973a), ”Maximum Likelihood and Minimum Step Methods for Estimating Evolutionary Trees from Data on Discrete Characters,” Systematic Zoology, 22, 240–249. · doi:10.2307/2412304
[30] – (1973b), ”Maximum Likelihood Estimation of Evolutionary Trees from Continuous Characteristics,” American Journal of Human Genetics, 25, 471–492.
[31] Forman, R. T. T., and Godron, M. (1986), Landscape Ecology, New York: Wiley.
[32] Fraley, C., and Raftery, A. E. (1998), ”How Many Clusters? Which Clustering Method? Answers Via Model-Based Cluster Analysis,” Computer Journal, 8. · Zbl 0920.68038
[33] Fraser, D. J., and Bernatchez, L. (2001), ”Adaptive Evolutionary Conservation: Towards a Unified Concept for Defining Conservation Units,” Molecular Ecology, 10, 2741–2752. · doi:10.1046/j.1365-294X.2001.t01-1-01411.x
[34] Gabriel, K. R., and Sokal, R. R. (1969), ”A New Statistical Approach to Geographic Variation Analysis,” Systematic Zoology, 18, 259–278. · doi:10.2307/2412323
[35] Gallant, A. R., and Fuller, W. A. (1973), ”Fitting Segmented Polynomial Regression Models Whose Join Points Have to Be Estimated,” Journal of the American Statistical Association, 68, 144–147. · Zbl 0277.62047 · doi:10.1080/01621459.1973.10481353
[36] Greville, T. N. E. (1969), Theory and Applications of Spline Functions, New York: Academic Press. · Zbl 0215.17601
[37] Harstell, T. D., and Ernst, C. H. (2004), ”A Review of Environmental Conditions Along the Coastal Range of the Diamondback Terrapin, Malaclemys Terrapin,” Herpetological Bulletin, 89, 12–20.
[38] Healy, M. J. R. (1969), ”Rao’s Paradox Concerning Multivariate Tests of Significance,” Biometrics, 25, 411–413. · doi:10.2307/2528798
[39] Hennig, C., and Hausdorf, B. (2004), ”Distance-Based Parametric Bootstrap Tests for Clustering of Species Ranges,” Computational Statistics & Data Analysis, 45, 875–896. · Zbl 1429.62068 · doi:10.1016/S0167-9473(03)00091-4
[40] Hinkley, D. V. (1971), ”Inference in Two-Phase Regression,” Journal of the American Statistical Association, 66, 736–743. · Zbl 0226.62068 · doi:10.1080/01621459.1971.10482337
[41] Holm, S. (1979), ”A Simple Sequentially Rejective Multiple Test Procedure,” Scandinavian Journal of Statistics, 6, 65–70. · Zbl 0402.62058
[42] Huberty, G. J. (1994), Applied Discriminant Analysis, New York: Wiley. · Zbl 0853.62045
[43] Huijbrechts, C. (1975), ”Regionalized Variables and Quantitative Analysis of Spatial Data,” in Display and Analysis of Spatial Data, eds. J. D. Davis and M. J. McCullagh, New York: Wiley, pp. 38–53.
[44] Husková, M. (1995), ”Nonparametric Procedures for Detecting a Change in Simple Linear Regression Models,” in Applied Change Point Problems in Statistics, eds. B. Sinha, A. Rukhin, and M. Ashanuhullah, Commack, New York: Nova Science Publishers, pp. 16–36.
[45] Ingles, L. G. (1965), Mammals of the Pacific States: California, Oregon, and Washington, Stanford, CA: Stanford University Press.
[46] Jackson, J. E. (1991), A User’s Guide to Principal Components, New York: Wiley. · Zbl 0743.62047
[47] Jain, A. K., and Dubes, R. C. (1988), Algorithms for Clustering Data, Englewood Cliffs, NJ: Prentice Hall, Inc. · Zbl 0665.62061
[48] Kaufman, L., and Rousseuw, P. J. (1990), Finding Groups in Data: An Introduction to Cluster Analyses, New York: Wiley.
[49] Kern, J. W., Anderson-Sprecher, R., and Borgman, L. E. (1996), ”Estimation and Hypothesis Testing for the Difference in Spatial Means,” Technical Report 96-01, University of Wyoming, Department of Statistics.
[50] King, T. L., Switzer, J. F., Morrison, C. L., Eackles, M. S., Young, C. Y., Lubinski, B., and Cryan, P. (2006), ”Comprehensive Analysis of Molecular Phylogenetic Structure among Meadow Jumping Mice (Zapus Hudsonius) Reveals Evolutionarily Distinct Subspecies,” technical report submitted to U.S. Fish and Wildlife Service.
[51] Knudsen, K. L., and Allendorf, F. W. (1985), ”Preliminary Survey of Genetic Variation in Grizzly Bears,” Technical Report, University of Montana.
[52] Larson, A. (1989), ”The Relationship between Speciation and Morphological Evolution,” in Speciation and Its Consequences, eds. D. Otte and J. A. Endler, Sunderland, MA: Sinauer Associates, Inc., pp. 579–598.
[53] Larson, H. J. (1992), ”Least Squares Estimation of Linear Splines with Unknown Knot Locations,” Computational Statistics & Data Analysis, 13, 1–8. · Zbl 0742.62077 · doi:10.1016/0167-9473(92)90149-A
[54] LeFranc, M. N., Jr., Moss, M. B., Patnode, K. A., and Snugg, W. C., III. (eds.) (1987), Grizzly Bear Compendium, Washington, DC: National Wildlife Federation, Interagency Grizzly Bear Committee.
[55] Legendre, P., and Fortin, M. (1989), ”Spatial Pattern and Ecological Analysis,” Vegetatio, 80, 107–138. · doi:10.1007/BF00048036
[56] Legge, J. T., Roush, R., DeSalle, R., Vogler, A. P., and May, B. (1996), ”Genetic Criteria for Establishing Evolutionarily Significant Unit in Cryan’s Buckmoth,” Conservation Biology, 10, 85–98. · doi:10.1046/j.1523-1739.1996.10010085.x
[57] Lipeika, A. (1977), ”Detection of Change-Point Moments for an Autoregressive Sequence,” Statisticeskije Problemy Upravlenija, 24, 27–71.
[58] Mayr, E. (1942), Systematics and the Origin of Species, New York: Columbia University Press.
[59] – (1963), Animal Species and Evolution, Cambridge, MA: Harvard University Press.
[60] Mayr, E. (1969), Principles of Systematic Zoology, New York: McGraw-Hill.
[61] – (1971), Populations, Species and Evolution, Cambridge, MA: Belknap Press of Harvard University.
[62] McDonald, L. L., Erickson, W. P., and Kern, J. W. (1994), ”Statistical Results Concerning Subspecies Limits and Geographic Patterns of Morphological Variation of California Gnatcatcher (Polioptila Californica),” Technical Report, West, Inc.
[63] McLachlan, G. J. (1992), Discriminant Analysis and Statistical Pattern Recognition, New York: John Wiley. · Zbl 1108.62317
[64] Mojen, R. (1977), ”Hierarchical Grouping Methods and Stopping Rules: An Evaluation,” Computer Journal, 20, 359–363. · Zbl 0364.62065 · doi:10.1093/comjnl/20.4.359
[65] Morrison, D. F. (1976), Multivariate Statistical Methods, New York: McGraw-Hill. · Zbl 0355.62049
[66] Neter, J., Wasserman, W., and Kutner, M. H. (1985), Applied Linear Statistical Models, Homewood, IL: Irwin.
[67] O’Neill, J. P. (1982), ”The Subspecies Concept in the 1980s,” Auk, 99, 609–612.
[68] Pianka, E. G. (1974O, Evolutionary Ecology, New York: Harper & Row.
[69] Pielou, E. C. (1984), The Interpretation of Ecological Data: A Primer on Classification and Ordination, New York, Wiley.
[70] Quandt, R. E. (1960), ”Test of the Hypothesis That a Linear Regression System Obeys Two Separate Regimes,” Journal of the American Statistical Association, 55, 324–330. · Zbl 0095.13602 · doi:10.1080/01621459.1960.10482067
[71] Ramey, R. R., II, Liu, H. P., Epps, C. W., Carpenter, L. M., and Wehausen, J. D. (2005), ”Genetic Relatedness of the Preble’s Meadow Jumping Mouse (Zapus Hudsonius Preblei) to Nearly Subspecies of Z. Hudsonius as Inferred from Variation in Cranial Morphology, Mitochondrial DNA and Microsatellite DNA: Implications for Taxonomy and Conservation,” Animal Conservation, 8, 329–346. · doi:10.1017/S1367943005002313
[72] Rao, C. R. (1966), ”Covariance Adjustment and Related Problems in Multivariate Analyses,” in Multivariate Analysis, ed. P. Krishnaich, New York: Academic Press, pp. 87–103.
[73] Ripley, B. D. (1981), Spatial Statistics, New York: Wiley. · Zbl 0583.62087
[74] Royle, J. A., and Nychka, D. (1996), ”The Effect of Spatial Covariance Heterogeneity on Prediction Variance,” in Spatial Accuracy Assessment in Natural Resources and Environmental Sciences: Second International Symposium, Fort Collins, CO: Rocky Mountain Forest and Range Experiment Station, pp. 137–146.
[75] Ryder, O. A. (1986), ”Species Conservation and Systematics: The Dilemma of Subspecies,” Trends in Ecology and Evolution, 1, 9–10. · doi:10.1016/0169-5347(86)90059-5
[76] Sinha, B., Ruklin, A., and Ahsanullah, M. (1995), Applied Change Point Problems in Statistics, Commack, NY: Nova Science Publishers.
[77] Snedecor, G. W., and Cochran, W. G. (1989), Statistical Methods (8th ed.), Ames, IA: Iowa State Press. · Zbl 0727.62003
[78] Sokal, R. R. (1979), ”Ecological Parameters Inferred from Spatial Correlograms,” in Contemporary Quantitative Ecology and Related Econometrics (Vol. 12), eds. G. P. Patil and M. L. Rosenweig, Fairland, MD: International Co-operative Publishing House, pp. 167–196.
[79] Stephen, C. L. et al. (2005), ”Population Genetic Analysis of Sonoran Pronghorn (Antilocapra americana son oriensis),” Journal of Mammalogy, 86, 782–792. · doi:10.1644/1545-1542(2005)086[0782:PGAOSP]2.0.CO;2
[80] Thomas, J. W., and Pletscher, D. H. (2000), ”The Convergence of Ecology, Conservation Biology, and Wildlife: Necessary or Redundant?”, Wildlife Society Bulletin, 28, 546.
[81] Zar, J. H. (1996), Biostatistical Analysis, Upper Saddle River, NJ: Prentice Hall.
[82] Zink, R. M. (2004), ”The Role of Subspecies in Obscuring Avian Biological Diversity and Misleading Conservation Policy,” Proceedings of the Royal Society of London, Biological Sciences, 271, 561–564. · doi:10.1098/rspb.2003.2617
[83] Zink, R. M., Barrowclough, G. F., Atwood, J. L., and Blackwell-Rago, R. C. (2000), ”Genetics, Taxonomy, and Conservation of the Threatened California Gnaicathcer,” Conservation Biology, 1349–1405.
[84] Zink, R. M., Drovetski, S. V., and Rohwer, S. (2002), ”Phylogeographic Patterns in the Great Spotted Woodpecker Dendrocopos Major across Eurasia,” Journal of Avian Biology, 33, 175–178. · doi:10.1034/j.1600-048X.2002.330208.x
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