Alternatives to statistical hypothesis testing in ecology: a guide to self teaching.

Statistical methods emphasizing formal hypothesis testing have dominated the analyses used by ecologists to gain insight from data. Here, we review alternatives to hypothesis testing including techniques for parameter estimation and model selection using likelihood and Bayesian techniques. These methods emphasize evaluation of weight of evidence for multiple hypotheses, multimodel inference, and use of prior information in analysis. We provide a tutorial for maximum likelihood estimation of model parameters and model selection using information theoretics, including a brief treatment of procedures for model comparison, model averaging, and use of data from multiple sources. We discuss the advantages of likelihood estimation, Bayesian analysis, and meta-analysis as ways to accumulate understanding across multiple studies. These statistical methods hold promise for new insight in ecology by encouraging thoughtful model building as part of inquiry, providing a unified framework for the empirical analysis of theoretical models, and by facilitating the formal accumulation of evidence bearing on fundamental questions.

[1]  D. Diefenbach,et al.  VARIABILITY IN GRASSLAND BIRD COUNTS RELATED TO OBSERVER DIFFERENCES AND SPECIES DETECTION RATES , 2003 .

[2]  Michael J. Winterbourn,et al.  Top-down and bottom-up processes in grassland and forested streams , 2003, Oecologia.

[3]  Bruce C. Lubow,et al.  Fitting population models to multiple sources of observed data , 2002 .

[4]  Ray Hilborn,et al.  Food regulates the Serengeti wildebeest: a 40‐year record , 1999 .

[5]  H. Akaike,et al.  Information Theory and an Extension of the Maximum Likelihood Principle , 1973 .

[6]  R. Hilborn,et al.  The Ecological Detective: Confronting Models with Data , 1997 .

[7]  T. Clutton‐Brock,et al.  Noise and determinism in synchronized sheep dynamics , 1998, Nature.

[8]  Ulrich Sommer,et al.  Consumer versus resource control of species diversity and ecosystem functioning , 2002, Nature.

[9]  Douglas A. Frank,et al.  The ecology of the earth's grazing ecosystems: Profound functional similarities exist between the Serengeti and Yellowstone , 1998 .

[10]  R. Haven Wiley,et al.  5 – Adaptations for Acoustic Communication in Birds: Sound Transmission and Signal Detection , 1982 .

[11]  Randall M. Peterman,et al.  Statistical power analysis and the precautionary principle , 1992 .

[12]  Robert A. Garrott,et al.  Climate-induced variation in vital rates of an unharvested large-herbivore population , 2003 .

[13]  O. Sala,et al.  Patch structure, dynamics and implications for the functioning of arid ecosystems. , 1999, Trends in ecology & evolution.

[14]  W. R. Howard The Nature of Mathematical Modeling , 2006 .

[15]  Helmut Hillebrand,et al.  Consumer effects decline with prey diversity , 2004 .

[16]  K. Wachter,et al.  Disturbed by meta-analysis? , 1988, Science.

[17]  Robert M. May,et al.  Theoretical Ecology: Principles and Applications , 1981 .

[18]  H. J. Larson,et al.  Introduction to the Theory of Statistics , 1973 .

[19]  J. Wolfowitz,et al.  Introduction to the Theory of Statistics. , 1951 .

[20]  Daniel M. Weary,et al.  The evolution of bird song : comparative analyses , 1992 .

[21]  F. Ramsey,et al.  Distance estimation as a variable in estimating bird numbers from vocalizations , 1981 .

[22]  R. Royall Statistical Evidence: A Likelihood Paradigm , 1997 .

[23]  C. Walters,et al.  Quantitative fisheries stock assessment: Choice, dynamics and uncertainty , 2004, Reviews in Fish Biology and Fisheries.

[24]  Jon T. Schnute,et al.  Estimating salmon stockrecruitment relationships from catch and escapement data , 2002 .

[25]  R. Myers Stock and recruitment: generalizations about maximum reproductive rate, density dependence, and variability using meta-analytic approaches , 2001 .

[26]  Robert T. Clemen,et al.  Making Hard Decisions: An Introduction to Decision Analysis , 1997 .

[27]  Douglas H. Johnson The Insignificance of Statistical Significance Testing , 1999 .

[28]  Rolf O. Peterson,et al.  THE EFFECT OF PREY AND PREDATOR DENSITIES ON WOLF PREDATION , 2002 .

[29]  Douglas A. Frank,et al.  CONSUMER CONTROL OF GRASSLAND PLANT PRODUCTION , 2002 .

[30]  Jerald B. Johnson,et al.  Model selection in ecology and evolution. , 2004, Trends in ecology & evolution.

[31]  Nicholas J. Gotelli,et al.  A Primer of Ecology , 1995 .

[32]  L. Fahrig,et al.  HABITAT LOSS AND POPULATION DECLINE: A META‐ANALYSIS OF THE PATCH SIZE EFFECT , 1998 .

[33]  John Harris,et al.  Precautionary principle stifles discovery , 1999, Nature.

[34]  David A. Fournier,et al.  A General Theory for Analyzing Catch at Age Data , 1982 .

[35]  David Western,et al.  Ecological conditions that determine when grazing stimulates grass production , 1989, Oecologia.

[36]  A. Hastings Population Biology: Concepts and Models , 1996 .

[37]  Frank P. Howe,et al.  A SEVEN-YEAR COMPARISON OF RELATIVE-ABUNDANCE AND DISTANCE-SAMPLING METHODS , 2003 .

[38]  Brian Dennis,et al.  Joint effects of density dependence and rainfall on abundance of San Joaquin kit fox , 2000 .

[39]  Kai N. Lee Compass and Gyroscope: Integrating Science and Politics for the Environment, Kai N. Lee. 1993. Island Press, Washington, DC. 290 pages. ISBN: 1-59963-197-X. $25.00 , 1993 .

[40]  C. H. Taubes,et al.  Modeling differential equations in biology , 2000 .

[41]  Carl J. Walters,et al.  Valuation of experimental management options for ecological systems , 1997 .

[42]  C. Both,et al.  Climate change and population declines in a long-distance migratory bird , 2006, Nature.

[43]  David R. Anderson,et al.  LANDBIRD COUNTING TECHNIQUES: CURRENT PRACTICES AND AN ALTERNATIVE , 2002 .

[44]  J. Berger Statistical Decision Theory and Bayesian Analysis , 1988 .

[45]  W. Kendall,et al.  First-Time Observer Effects in the North American Breeding Bird Survey , 1996 .

[46]  Thomas Bell,et al.  The effect of temporal scale on the outcome of trophic cascade experiments , 2003, Oecologia.

[47]  S. Buckland Introduction to distance sampling : estimating abundance of biological populations , 2001 .

[48]  David R. Anderson,et al.  Model selection and multimodel inference : a practical information-theoretic approach , 2003 .

[49]  G. Cumming,et al.  Editors Can Lead Researchers to Confidence Intervals, but Can't Make Them Think , 2004, Psychological science.

[50]  J. Cameron,et al.  The Precautionary Principle: A Fundamental Principle of Law and Policy for the Protection of the Global Environment , 1991 .

[51]  Jon T. Schnute,et al.  A General Framework for Developing Sequential Fisheries Models , 1994 .

[52]  Pia Veldt Larsen,et al.  In All Likelihood: Statistical Modelling and Inference Using Likelihood , 2003 .

[53]  Sears,et al.  When is a trophic cascade a trophic cascade? , 2000, Trends in ecology & evolution.

[54]  N Thompson Hobbs,et al.  Deepening ecological insights using contemporary statistics. , 2006, Ecological applications : a publication of the Ecological Society of America.

[55]  L. Hedges,et al.  Statistical Methods for Meta-Analysis , 1987 .

[56]  Andrew P. Hendry,et al.  Brown bears selectively kill salmon with higher energy content but only in habitats that facilitate choice , 2004 .

[57]  Mathew A. Leibold,et al.  Ecosystem consequences of species richness and composition in pond food webs , 2002, Nature.

[58]  C. S. Robbins,et al.  Managing and Monitoring Birds Using Point Counts: Standards and Applications , 1995 .

[59]  Michael Hills,et al.  Statistical Models in Epidemiology , 1995 .

[60]  M. J. Hatcher,et al.  Modeling Biological Systems: Principles and Applications , 1997 .

[61]  Anthony F. Bartholomay,et al.  The Mathematical Approach to Biology and Medicine , 1967 .

[62]  James S. Clark,et al.  UNCERTAINTY AND VARIABILITY IN DEMOGRAPHY AND POPULATION GROWTH: A HIERARCHICAL APPROACH , 2003 .

[63]  A. Azzalini Statistical Inference Based on the likelihood , 1996 .

[64]  Colin Howson,et al.  Bayesian reasoning in science , 1991, Nature.

[65]  James O. Berger,et al.  Ockham's Razor and Bayesian Analysis , 1992 .

[66]  K R Foster,et al.  Risk management. Science and the precautionary principle. , 2000, Science.

[67]  R. McLain,et al.  Adaptive management: Promises and pitfalls , 1996, Environmental management.

[68]  Carl J. Walters,et al.  ECOLOGICAL OPTIMIZATION AND ADAPTIVE MANAGEMENT , 1978 .

[69]  H. Akaike INFORMATION THEORY AS AN EXTENSION OF THE MAXIMUM LIKELIHOOD , 1973 .

[70]  W. Link,et al.  The North American Breeding Bird Survey Results and Analysis , 1997 .

[71]  Leah Edelstein-Keshet,et al.  Mathematical models in biology , 2005, Classics in applied mathematics.

[72]  M. Dorn,et al.  Advice on West Coast Rockfish Harvest Rates from Bayesian Meta-Analysis of Stock−Recruit Relationships , 2002 .

[73]  Osvaldo E. Sala,et al.  Ecology: Price put on biodiversity , 2001, Nature.

[74]  D. C. Bowden,et al.  Dynamics of interacting Elk populations within and adjacent to Rocky Mountain National Park , 2002 .

[75]  Robert E. Ulanowicz,et al.  On the importance of higher-level models in ecology , 1988 .

[76]  James M. Bullock,et al.  Restoration of biodiversity enhances agricultural production , 2001 .

[77]  B. Schmid,et al.  ECOSYSTEM EFFECTS OF BIODIVERSITY: A CLASSIFICATION OF HYPOTHESES AND EXPLORATION OF EMPIRICAL RESULTS , 1999 .

[78]  Alan Hastings,et al.  FITTING POPULATION MODELS INCORPORATING PROCESS NOISE AND OBSERVATION ERROR , 2002 .

[79]  O. Bjørnstad,et al.  Dynamics of measles epidemics: Estimating scaling of transmission rates using a time series sir model , 2002 .

[80]  S. Goodman Toward Evidence-Based Medical Statistics. 1: The P Value Fallacy , 1999, Annals of Internal Medicine.

[81]  Ray Hilborn,et al.  Standing on the Shoulders of Giants: Learning from Experience in Fisheries , 1998, Reviews in Fish Biology and Fisheries.

[82]  Murdoch K. McAllister,et al.  Taking Uncertainty Seriously: From Permissive Regulation to Preventative Design in Environmental Decision Making , 1994, Osgoode Hall Law Journal.

[83]  Lenore Fahrig,et al.  EFFECT OF HABITAT FRAGMENTATION ON THE EXTINCTION THRESHOLD: A SYNTHESIS* , 2002 .

[84]  Jessica Gurevitch,et al.  Meta-analysis in ecology , 2001 .

[85]  Andrew B. Cooper,et al.  AN APPROACH FOR POPULATION ASSESSMENT IN THE ABSENCE OF ABUNDANCE INDICES , 2003 .

[86]  W. Thompson,et al.  TOWARDS RELIABLE BIRD SURVEYS: ACCOUNTING FOR INDIVIDUALS PRESENT BUT NOT DETECTED , 2002 .

[87]  Ray Hilborn,et al.  Inferring Bayesian Priors with Limited Direct Data: Applications to Risk Analysis , 2002 .

[88]  Colin White,et al.  The Mathematical Approach to Biology and Medicine , 1967, The Yale Journal of Biology and Medicine.

[89]  Charles A. S. Hall,et al.  AN ASSESSMENT OF SEVERAL OF THE HISTORICALLY MOST INFLUENTIAL THEORETICAL MODELS USED IN ECOLOGY AND OF THE DATA PROVIDED IN THEIR SUPPORT , 1988 .

[90]  J. Platt Strong Inference: Certain systematic methods of scientific thinking may produce much more rapid progress than others. , 1964, Science.

[91]  Peter Müller,et al.  INCORPORATING MULTIPLE SOURCES OF STOCHASTICITY INTO DYNAMIC POPULATION MODELS , 2003 .

[92]  Jonathan Bart,et al.  Reliability of singing bird surveys: effects of song phenology during the breeding season , 1985 .

[93]  Brian Dennis,et al.  MODEL SELECTION FOR A SUBTERRANEAN TROPHIC CASCADE: ROOT‐FEEDING CATERPILLARS AND ENTOMOPATHOGENIC NEMATODES , 1999 .

[94]  Roger Sauter,et al.  In All Likelihood , 2002, Technometrics.

[95]  Huxel On the influence of food quality in consumer–resource interactions , 1999 .

[96]  A. J. Belsky Does Herbivory Benefit Plants? A Review of the Evidence , 1986, The American Naturalist.

[97]  John E. Gross,et al.  HERBIVORE FUNCTIONAL RESPONSE IN HETEROGENEOUS ENVIRONMENTS: A CONTEST AMONG MODELS , 2003 .

[98]  Brian Dennis,et al.  Discussion: Should Ecologists Become Bayesians? , 1996 .

[99]  James M. Yoder,et al.  INDIVIDUALS–AREA RELATIONSHIPS: THE RELATIONSHIP BETWEEN ANIMAL POPULATION DENSITY AND AREA , 2000 .

[100]  J. Nichols,et al.  A DOUBLE-OBSERVER APPROACH FOR ESTIMATING DETECTION PROBABILITY AND ABUNDANCE FROM POINT COUNTS , 2000 .

[101]  David W. Onstad,et al.  Population-dynamics theory: The roles of analytical, simulation, and supercomputer models , 1988 .

[102]  Anderson,et al.  Defoliation effects on reproductive biomass: Importance of scale and timing , 2003 .

[103]  Carl J. Walters,et al.  Calculation of Bayes Posterior Probability Distributions for Key Population Parameters , 1994 .

[104]  Carl J. Walters,et al.  Large‐Scale Management Experiments and Learning by Doing , 1990 .

[105]  Ransom A. Myers,et al.  What is the carrying capacity for fish in the ocean? A meta-analysis of population dynamics of North Atlantic cod , 2001 .

[106]  J. Detling,et al.  Grasslands and savannas: regulation of energy flow and nutrient cycling by herbivores , 1988 .

[107]  Nicholas J. Gotelli,et al.  A Primer of Ecology , 1996 .

[108]  Masanao Aoki,et al.  State Space Modeling of Time Series , 1987 .

[109]  Donald L. DeAngelis,et al.  Further Considerations on the Debate Over Herbivore Optimization Theory. , 1993, Ecological applications : a publication of the Ecological Society of America.

[110]  S. Fretwell Populations in a seasonal environment. , 1973, Monographs in population biology.

[111]  Ryuei Nishii,et al.  A model of deforestation by human population interactions , 1997, Environmental and Ecological Statistics.

[112]  David B. Dunson,et al.  Bayesian Data Analysis , 2010 .

[113]  M. Uriarte,et al.  Analysis of neighborhood dynamics of forest ecosystems using likelihood methods and modeling. , 2006, Ecological applications : a publication of the Ecological Society of America.

[114]  R. Callaway,et al.  Positive interactions among plants , 1995, The Botanical Review.

[115]  Imanuel Noy-Meir,et al.  Compensating Growth of Grazed Plants and Its Relevance to the Use of Rangelands. , 1993, Ecological applications : a publication of the Ecological Society of America.

[116]  David R. Anderson,et al.  Null Hypothesis Testing: Problems, Prevalence, and an Alternative , 2000 .

[117]  K. Pollock,et al.  EXPERIMENTAL ANALYSIS OF THE AUDITORY DETECTION PROCESS ON AVIAN POINT COUNTS , 2007 .

[118]  C. Mann Meta-analysis in the breech. , 1990, Science.

[119]  Kenneth R. Foster,et al.  Science and the Precautionary Principle , 2000, Science.

[120]  Kenneth H. Pollock,et al.  A REMOVAL MODEL FOR ESTIMATING DETECTION PROBABILITIES FROM POINT-COUNT SURVEYS , 2002 .

[121]  Jonathan M. Chase,et al.  Species Turnover and the Regulation of Trophic Structure , 1997 .

[122]  B. Efron Why Isn't Everyone a Bayesian? , 1986 .

[123]  Neil Gershenfeld,et al.  The nature of mathematical modeling , 1998 .

[124]  Alan Hastings,et al.  Trophic cascades and trophic trickles in pelagic food webs , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[125]  J. Nichols,et al.  OF BUGS AND BIRDS: MARKOV CHAIN MONTE CARLO FOR HIERARCHICAL MODELING IN WILDLIFE RESEARCH , 2002 .

[126]  S. McNaughton,et al.  Grazing as an Optimization Process: Grass-Ungulate Relationships in the Serengeti , 1979, The American Naturalist.

[127]  B. Worm,et al.  Biodiversity, productivity and stability in real food webs , 2003 .

[128]  J. Berger,et al.  Testing a Point Null Hypothesis: The Irreconcilability of P Values and Evidence , 1987 .

[129]  R. Hilborn,et al.  Fisheries stock assessment and decision analysis: the Bayesian approach , 1997, Reviews in Fish Biology and Fisheries.

[130]  S. T. Buckland,et al.  Hidden process models for animal population dynamics. , 2006, Ecological applications : a publication of the Ecological Society of America.

[131]  P. Holgate,et al.  Matrix Population Models. , 1990 .

[132]  Kenneth H. Pollock,et al.  TIME-OF-DETECTION METHOD FOR ESTIMATING ABUNDANCE FROM POINT-COUNT SURVEYS , 2007 .

[133]  D. Bystrak,et al.  The role of observer bias in the North American Breeding Bird Survey , 1981 .

[134]  Andrew A. Rosenberg,et al.  The Precautionary Approach and risk management: can they increase the probability of successes in fishery management? , 2001 .

[135]  S. McNaughton,et al.  Serengeti Grassland Ecology: The Role of Composite Environmental Factors and Contingency in Community Organization , 1983 .

[136]  E. Morton Ecological Sources of Selection on Avian Sounds , 1975, The American Naturalist.

[137]  Carl J. Walters,et al.  Adaptive Management of Renewable Resources , 1986 .

[138]  David S. Hik,et al.  What determines disturbance‐productivity‐diversity relationships? The effect of scale, species and environment on richness patterns in an Australian woodland , 2003 .

[139]  O. Schmitz,et al.  Trophic Cascades in Terrestrial Systems: A Review of the Effects of Carnivore Removals on Plants , 2000, The American Naturalist.

[140]  N. Stenseth,et al.  Population dynamics of Norwegian red deer: density–dependence and climatic variation , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[141]  F. Thompson,et al.  Nest Predators and Fragmentation: a Review and Meta‐Analysis , 2002 .

[142]  Kenneth P. Burnham,et al.  Summarizing remarks: environmental influences , 1981 .

[143]  W. Link,et al.  Observer differences in the North American Breeding Bird Survey , 1994 .

[144]  W. Link,et al.  HIERARCHICAL MODELING OF POPULATION STABILITY AND SPECIES GROUP ATTRIBUTES FROM SURVEY DATA , 2002 .

[145]  Scott L. Collins,et al.  FEEDBACK LOOPS IN ECOLOGICAL HIERARCHIES FOLLOWING URINE DEPOSITION IN TALLGRASS PRAIRIE , 2001 .