Is heterogeneity of catchability in capture–recapture studies a mere sampling artifact or a biologically relevant feature of the population?

The heterogeneity of catchability (HC) among the individuals encountered during a capture–recapture study has long been regarded as a liability. However, heterogeneous capture probabilities may reflect interesting but hidden features of the population, such as social status. The difficulty is to distinguish between this intrinsic heterogeneity and the extrinsic heterogeneity induced by the study itself. So far, population ecologists have not been able to distinguish between these two sources of variation in capture heterogeneity because, in the presence of heterogeneity of capture in the data, they have frequently used a too simple approach. This traditional approach, which consists of incorporating two common sources of lack of fit (transience and trap-dependence), does not directly model the HC and thus cannot investigate its biological meaning. In this context, we propose, for open populations, to directly model the HC by employing multievent models. Multievent models make it possible to break HC into two classes of catchability viewed as uncertain states. With the introduction of a coefficient of heterogeneity to model proportional probabilities of capture over time in the two classes, our approach allows the investigation of HC in a parsimonious way. In this paper, we apply both this new approach and the traditional approach to a long-term data set of male deer mice Peromyscus maniculatus. We then compare 13 candidate models separately for each approach. Our results indicate that the new approach is superior to the traditional approach.

[1]  E. Paradis,et al.  Assessment of habitat quality in the Mediterranean pine vole (Microtus duodecimcostatus) by the study of survival rates , 1995 .

[2]  W. Link,et al.  Individual Covariation in Life‐History Traits: Seeing the Trees Despite the Forest , 2002, The American Naturalist.

[3]  M. Lima,et al.  Seasonal regulation in fluctuating small mammal populations: feedback structure and climate , 2001 .

[4]  J. Andrew Royle,et al.  Mixture Models for Estimating the Size of a Closed Population When Capture Rates Vary among Individuals , 2003, Biometrics.

[5]  D. S. Robson,et al.  Estimation of Time-Specific Survival Rates from Tag-Resighting Samples: A Generalization of the Jolly-Seber Model , 1983 .

[6]  J. L. Wolfe,et al.  Social Influences on Trap Response of the Cotton Rat, Sigmodon Hispidus , 1973 .

[7]  Roger Pradel,et al.  M-SURGE: new software specifically designed for multistate capture-recapture models , 2004, Animal Biodiversity and Conservation.

[8]  J. Norris,et al.  Capture-Recapture Models with Heterogeneity : I . Cormack-Jolly-Seber Model , 2003 .

[9]  J. Emlen,et al.  Heterogeneity of Trap Response in a Population of House Mice , 1952 .

[10]  M. Lima,et al.  Adult survival and population dynamics in the leaf-eared mouse Phyllotis darwini in central Chile , 2006 .

[11]  Roger Pradel,et al.  ESTIMATION OF SEX-AND AGE-RELATED SURVIVAL RATES IN A MICROTINE POPULATION , 1993 .

[12]  R. Dueser,et al.  Interspecific territoriality in two sympatric species of Peromyscus (Rodentia: Cricetidae) , 1983, Behavioral Ecology and Sociobiology.

[13]  James E. Hines,et al.  ESTIMATING TEMPORARY EMIGRATION USING CAPTURE-RECAPTURE DATA WITH POLLOCK'S ROBUST DESIGN , 1997 .

[14]  Søren Bondrup-Nielsen,et al.  Density estimation as a function of live-trapping grid and home range size , 1983 .

[15]  R. V. Van Horn,et al.  Disinfectant Effects on Capture Rates of Deer Mice (Peromyscus maniculatus) , 2000 .

[16]  S. Faux,et al.  Seasonally variable effects of conspecific odors upon capture of deer mice (Peromyscus maniculatus gambelii). , 1978, Behavioral biology.

[17]  David R. Anderson,et al.  Capture-Recapture and Removal Methods for Sampling Closed Populations , 1983 .

[18]  G. Seber A NOTE ON THE MULTIPLE-RECAPTURE CENSUS. , 1965, Biometrika.

[19]  L. Herman,et al.  ESTIMATING THE ADULT SURVIVAL RATE OF CENTRAL NORTH PACIFIC HUMPBACK WHALES (MEGAPTERA NOVAEANGLIAE) , 2004 .

[20]  S. Pledger Unified Maximum Likelihood Estimates for Closed Capture–Recapture Models Using Mixtures , 2000, Biometrics.

[21]  R. Ostfeld,et al.  DENSITY-DEPENDENT PROCESSES IN MEADOW VOLES: AN EXPERIMENTAL APPROACH' , 1995 .

[22]  David R. Anderson,et al.  Capture-recapture and removal methods for sampling closed populations , 1984 .

[23]  Roger Pradel,et al.  RE-EVALUATION OF ADULT SURVIVAL OF BLACK-HEADED GULLS (LARUS RIDIBUNDUS) IN PRESENCE OF RECAPTURE HETEROGENEITY , 1998 .

[24]  G. O. Batzli Population Dynamics of the White-footed Mouse in Floodplain and Upland Forests , 1977 .

[25]  Trap-response heterogeneity of house mice (Mus musculus) in outdoor enclosures , 1999 .

[26]  N. Stenseth,et al.  Survival in fluctuating bank vole populations: seasonal and yearly variations , 2002 .

[27]  J. Ogutu,et al.  Application of mark–recapture methods to lions: satisfying assumptions by using covariates to explain heterogeneity , 2006 .

[28]  J. O. Wolff The effects of density, food, and interspecific interference on home range size in Peromyscus leucopus and Peromyscus maniculatus , 1985 .

[29]  P. Marchand Life in the cold : an introduction to winter ecology , 1988 .

[30]  N. Stenseth,et al.  Survival-variation within and between functional categories of the African multimammate rat , 1999 .

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

[32]  N. Yoccoz,et al.  Are Alpine Bank Voles Larger and More Sexually Dimorphic because Adults Survive Better , 1998 .

[33]  Roger Pradel,et al.  Principles and interest of GOF tests for multistate capture-recapture models , 2005, Animal Biodiversity and Conservation.

[34]  L. C. Drickamer,et al.  Conspecific Odors and Trappability of Deer Mice (Peromyscus leucopus noveboracensis) , 1976 .

[35]  A. Carothers Quantifying Unequal Catchability and its Effect on Survival Estimates in an Actual Population , 1979 .

[36]  G. Jolly EXPLICIT ESTIMATES FROM CAPTURE-RECAPTURE DATA WITH BOTH DEATH AND IMMIGRATION-STOCHASTIC MODEL. , 1965, Biometrika.

[37]  J. Grace,et al.  Life in the Cold--An Introduction to Winter Ecology. , 1989 .

[38]  Roger Pradel,et al.  CAPTURE-RECAPTURE SURVIVAL MODELS TAKING ACCOUNT OF TRANSIENTS , 1997 .

[39]  L. Metzgar Dispersion and numbers in Peromyscus populations. , 1980 .

[40]  T. S. Jensen Trappability of Various Functional Groups of the Forest Rodents Clethrionomys glareolus and Apodemus flavicollis, and Its Application in Density Estimations , 1975 .

[41]  Individual turnover among wintering teal in Camargue: A mark-recapture study , 1997 .

[42]  Roger Pradel,et al.  Multievent: An Extension of Multistate Capture–Recapture Models to Uncertain States , 2005, Biometrics.

[43]  L. Scott Mills,et al.  OF MICE AND MEN AND TRILLIUM: CASCADING EFFECTS OF FOREST FRAGMENTATION , 2003 .

[44]  J. Lebreton,et al.  Marked Individuals in the Study of Bird Population , 1993 .

[45]  K. Burnham,et al.  Program MARK: survival estimation from populations of marked animals , 1999 .

[46]  G. Singleton,et al.  Abundance estimators and truth: Accounting for individual heterogeneity in wild house mice , 2003 .

[47]  N. Stenseth,et al.  The demography ofClethrionomys rufocanus: From mathematical and statistical models to further field studies , 1998, Researches on Population Ecology.

[48]  R. Cormack Estimates of survival from the sighting of marked animals , 1964 .

[49]  Shirley Pledger,et al.  The Performance of Mixture Models in Heterogeneous Closed Population Capture–Recapture , 2005, Biometrics.

[50]  David R. Anderson,et al.  Modeling Survival and Testing Biological Hypotheses Using Marked Animals: A Unified Approach with Case Studies , 1992 .

[51]  Mauricio Lima,et al.  Supervivencia adulta y dinmica poblacional del lauchn orejudo Phyllotis darwini en Chile central , 2006 .

[52]  Michael Begon,et al.  The effects of cowpox virus on survival in natural rodent populations: increases and decreases , 2002 .

[53]  Olivier Gimenez,et al.  Parameter Redundancy in Multistate Capture‐Recapture Models , 2003 .

[54]  Roger Pradel,et al.  Program E-Surge: A Software Application for Fitting Multievent Models , 2009 .

[55]  Mark Trinder,et al.  Oil pollution and climate have wide-scale impacts on seabird demographics. , 2005, Ecology letters.

[56]  Roger Pradel,et al.  LOCAL RECRUITMENT IN THE GREATER FLAMINGO: A NEW APPROACH USING CAPTURE-MARK-RECAPTURE DATA , 1997 .

[57]  Alan R. Johnson,et al.  SEX‐ AND AGE‐RELATED VARIATION IN SURVIVAL AND COST OF FIRST REPRODUCTION IN GREATER FLAMINGOS , 2001 .

[58]  Kenneth H. Pollock,et al.  Estimation of Recruitment from Immigration Versus In Situ Reproduction Using Pollock's Robust Design , 1990 .

[59]  P. Thompson,et al.  North Atlantic climate variation influences survival in adult fulmars , 2005 .

[60]  N. Stenseth,et al.  Delayed maturation in female bank voles: optimal decision or social constraint? , 1999 .

[61]  G. Adler,et al.  Ecological correlates of trap response of a Neotropical forest rodent, Proechimys semispinosus , 1997, Journal of Tropical Ecology.

[62]  S. Wanless,et al.  Increased adult mortality and reduced breeding success with age in a population of common guillemot Uria aalge using marked birds of unknown age , 2006 .

[63]  S. Wanless,et al.  Factors influencing the survival of Puffins Fratercula arctica at a North Sea colony over a 20-year period , 1997 .

[64]  M. Frederiksen,et al.  Evidence for density-dependent survival in adult cormorants from a combined analysis of recoveries and resightings. , 2000, The Journal of animal ecology.

[65]  L. Metzgar Behavioral Population Regulation in the Woodmouse, Peromyscus leucopus , 1971 .

[66]  L. C. Drickamer Captures of Two Species of Peromyscus at Live Traps Baited with Male and Female Odors , 1984 .

[67]  B. Hörnfeldt,et al.  Vole cycles, snow depth and fox predation , 1994 .

[68]  H. Leirs,et al.  Survival and maturation rates of the African rodent, Mastomys natalensis: density-dependence and rainfall. , 2007, Integrative zoology.