Bias in Diet Determination: Incorporating Traditional Methods in Bayesian Mixing Models

There are not “universal methods” to determine diet composition of predators. Most traditional methods are biased because of their reliance on differential digestibility and the recovery of hard items. By relying on assimilated food, stable isotope and Bayesian mixing models (SIMMs) resolve many biases of traditional methods. SIMMs can incorporate prior information (i.e. proportional diet composition) that may improve the precision in the estimated dietary composition. However few studies have assessed the performance of traditional methods and SIMMs with and without informative priors to study the predators’ diets. Here we compare the diet compositions of the South American fur seal and sea lions obtained by scats analysis and by SIMMs-UP (uninformative priors) and assess whether informative priors (SIMMs-IP) from the scat analysis improved the estimated diet composition compared to SIMMs-UP. According to the SIMM-UP, while pelagic species dominated the fur seal’s diet the sea lion’s did not have a clear dominance of any prey. In contrast, SIMM-IP’s diets compositions were dominated by the same preys as in scat analyses. When prior information influenced SIMMs’ estimates, incorporating informative priors improved the precision in the estimated diet composition at the risk of inducing biases in the estimates. If preys isotopic data allow discriminating preys’ contributions to diets, informative priors should lead to more precise but unbiased estimated diet composition. Just as estimates of diet composition obtained from traditional methods are critically interpreted because of their biases, care must be exercised when interpreting diet composition obtained by SIMMs-IP. The best approach to obtain a near-complete view of predators’ diet composition should involve the simultaneous consideration of different sources of partial evidence (traditional methods, SIMM-UP and SIMM-IP) in the light of natural history of the predator species so as to reliably ascertain and weight the information yielded by each method.

[1]  J. Logan,et al.  Erratum to: Diet of young Atlantic bluefin tuna (Thunnus thynnus) in eastern and western Atlantic foraging grounds , 2011 .

[2]  D. Phillips,et al.  Source partitioning using stable isotopes: coping with too many sources , 2003, Oecologia.

[3]  Karsten Berns,et al.  Probabilistic distance measures of the Dirichlet and Beta distributions , 2008, Pattern Recognit..

[4]  Brice X Semmens,et al.  Incorporating uncertainty and prior information into stable isotope mixing models. , 2008, Ecology letters.

[5]  M. J. Deniro,et al.  Influence of Diet On the Distribtion of Nitrogen Isotopes in Animals , 1978 .

[6]  M. Apollonio,et al.  Trophic niche overlap and wild ungulate consumption by red fox and wolf in a mountain area in Italy , 2012 .

[7]  R. Menni,et al.  Fish assemblages of the northern Argentine coastal system: spatial patterns and their temporal variations , 2006 .

[8]  E. Angulo,et al.  Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction , 2009 .

[9]  W. J. Dyer,et al.  A rapid method of total lipid extraction and purification. , 1959, Canadian journal of biochemistry and physiology.

[10]  P. A. Prince,et al.  Dietary segregation of krill-eating South Georgia seabirds , 2009 .

[11]  J. Testa,et al.  The diet of Weddell seals in McMurdo Sound, Antarctica as determined from scat collections and stable isotope analysis , 1998, Polar Biology.

[12]  C. Darimont,et al.  Intra-hair stable isotope analysis implies seasonal shift to salmon in gray wolf diet , 2002 .

[13]  A. Volpedo.  Ecomorphological patterns of the sagitta in fish on the continental shelf off Argentine , 2003 .

[14]  John Geweke,et al.  Evaluating the accuracy of sampling-based approaches to the calculation of posterior moments , 1991 .

[15]  E. Cortés.  A critical review of methods of studying fish feeding based on analysis of stomach contents: application to elasmobranch fishes , 1997 .

[16]  Over-representation of bird prey in pellets of South Polar Skuas , 2012, Journal of Ornithology.

[17]  Justin D. Yeakel,et al.  Tools for quantifying isotopic niche space and dietary variation at the individual and population level , 2012 .

[18]  K. Hobson,et al.  Using stable isotopes of nitrogen and carbon to study seabird ecology: applications in the Mediterranean seabird community* , 2003 .

[19]  Richard Inger,et al.  Source Partitioning Using Stable Isotopes: Coping with Too Much Variation , 2010, PloS one.

[20]  M. Perga,et al.  ‘Are fish what they eat’ all year round? , 2005, Oecologia.

[21]  M. Clarke.  A Handbook for the identification of cephalopod beaks , 1986 .

[22]  K. Hobson,et al.  Stable carbon and nitrogen isotopic fractionation between diet and tissues of captive seals: implications for dietary reconstructions involving marine mammals , 1996 .

[23]  V. Escalona,et al.  Intraspecific comparison of diet of California sea lions (Zalophus californianus) assessed using fecal and stable isotope analyses , 2011 .

[24]  R. Langton.  DIET OVERLAP B,ETWEEN ATLANTIC COD, GADUS MORHUA, SILVER HAKE, MERLUCCIUS BILINEARIS, AND FIFTEEN OTHER NORTHWEST ATLANTIC FINFISH , 1982 .

[25]  Paul L. Koch,et al.  Using stable isotope biogeochemistry to study marine mammal ecology , 2010 .

[26]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[27]  S. Budge,et al.  Estimating diets of Atlantic salmon (Salmo salar) using fatty acid signature analyses; validation with controlled feeding studies , 2012 .

[28]  T. Rogers,et al.  Food transit times in captive leopard seals (Hydrurga leptonyx) , 2010, Polar Biology.

[29]  M. Kenward,et al.  An Introduction to the Bootstrap , 2007 .

[30]  Ll Allum,et al.  Unusual stability of diet of the New Zealand fur seal (Arctocephalus forsteri) at Banks Peninsula, New Zealand , 2012 .

[31]  J. Logan,et al.  Diet of young Atlantic bluefin tuna (Thunnus thynnus) in eastern and western Atlantic foraging grounds , 2010 .

[32]  A. Bond,et al.  Recent Bayesian stable-isotope mixing models are highly sensitive to variation in discrimination factors. , 2011, Ecological applications : a publication of the Ecological Society of America.

[33]  J. Q. Smith,et al.  1. Bayesian Statistics 4 , 1993 .

[34]  N. Polunin,et al.  Methodological uncertainty in resource mixing models for generalist fishes , 2012, Oecologia.

[35]  R. Briers,et al.  Ecology: From Individuals to Ecosystems , 2006 .

[36]  A. Velando,et al.  A three-isotope approach to disentangling the diet of a generalist consumer: the yellow-legged gull in northwest Spain , 2010 .

[37]  J. Sumich,et al.  Marine Mammals: Evolutionary Biology , 1999 .

[38]  R. Menni,et al.  Environmental factors structuring fish communities of the Río de la Plata estuary , 2004 .

[39]  R. Joy,et al.  DIETARY ANALYSIS FROM FECAL SAMPLES: HOW MANY SCATS ARE ENOUGH? , 2005 .

[40]  D. Post,et al.  Applying stable isotopes to examine food‐web structure: an overview of analytical tools , 2012, Biological reviews of the Cambridge Philosophical Society.

[41]  Lluís Jover,et al.  Feeding ecology of yellow-legged gulls Larus michahellis in the western Mediterranean: a comparative assessment using conventional and isotopic methods , 2009 .

[42]  Trophic interactions between brown and south polar skuas at Deception Island, Antarctica , 2012, Polar Biology.

[43]  R. Michener.  Stable isotope ratios as tracers in marine aquatic food webs , 1994 .

[44]  Vivien T. Kent,et al.  Reducing Potential Sources of Sampling Bias When Quantifying the Diet of the African Wild Dog Through Scat Analysis , 2010 .

[45]  V. Bontzorlos,et al.  Assessing bias in diet methods for the Long-legged Buzzard Buteo rufinus , 2012 .

[46]  R. Oliver,et al.  Carbon source accounting for fish using combined DNA and stable isotope analyses in a regulated lowland river weir pool , 2010, Molecular ecology.

[47]  Nicolaas Bouwes,et al.  A quantitative approach to combine sources in stable isotope mixing models , 2011 .

[48]  A. Powell,et al.  Evaluating gull diets: a comparison of conventional methods and stable isotope analysis , 2011 .

[49]  R. Vargas,et al.  DIET OF SOUTH AMERICAN FUR SEALS (ARCTOCEPHALUS AUSTRALIS) IN ISLA DE LOBOS, URUGUAY , 2002 .

[50]  Paulo R. Guimarães,et al.  Merging Resource Availability with Isotope Mixing Models: The Role of Neutral Interaction Assumptions , 2011, PloS one.

[51]  H. Hofer,et al.  An Advanced Method to Assess the Diet of Free-Ranging Large Carnivores Based on Scats , 2012, PloS one.

[52]  Daniel P. Costa,et al.  Foraging behavior of lactating South American sea lions (Otaria flavescens) and spatial-temporal resource overlap with the Uruguayan fisheries , 2013 .

[53]  R. J. Harrison.  Marine Mammals , 1972, Nature.

[54]  Daniel E. Schindler,et al.  Including source uncertainty and prior information in the analysis of stable isotope mixing models. , 2010, Environmental science & technology.

[55]  D. Macdonald,et al.  A comparison and critique of different scat‐analysis methods for determining carnivore diet , 2011 .

[56]  D. Berteaux,et al.  Sensitivity of stable isotope mixing models to variation in isotopic ratios: evaluating consequences of lipid extraction , 2010 .

[57]  A. Angerbjörn,et al.  Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes , 2005, Oecologia.

[58]  M. Lima,et al.  Prepartum and postpartum trophic segregation between sympatrically breeding female Arctocephalus australis and Otaria flavescens , 2012 .