Estimating trophic position in marine and estuarine food webs

Structural or binary approaches, based on presence-absence of feeding links, are the most common method of assembling food webs and form the basis of the most well explored food web models. Binary approaches to assembling feeding links are often criticized as being less powerful and accurate than flow-based methods. To test this assumption we compared binary estimates of trophic position with estimates based on stable isotope values of nitrogen (δ15N). For 366 species from eight marine and estuarine food webs we compared trophic position estimates based on binary (presence-absence) feeding links with estimates based on the stable isotope of nitrogen (δ15N). For a subset of 127 fish species in four of the webs we further compared trophic position estimates based on gut content analysis using a flow-based algorithm using data from FishBase.org with binary and δ15N estimates. Across all species and webs binary estimates of trophic position were strongly correlated (R = 0.644) with δ15N estimates. On average binary estimates differed from baseline corrected δ15N estimates by 2.33% for mean trophic position and 6.57% for maximum trophic position. On average the difference between binary δ15N estimates was 0.14 of a trophic level. For the subset of 127 fish species binary estimates performed similarly or more accurately in predicting δ15N values than the flow-based estimates. Binary approaches to assembling feeding links are often criticized as being less powerful and accurate than flow-based methods. Our results show a high concordance between binary and δ15N estimates of trophic position as well as showing that in some cases binary estimates are better predictors of δ15N than flow-based estimates, reaffirming the robustness of the structural approach to assembling food webs. Additional cross-validation studies in other ecosystems are necessary to determine whether our results can be generalized to terrestrial and freshwater ecosystems.

[1]  Chris W. Michiels,et al.  Lysozymes in the animal kingdom , 2010, Journal of Biosciences.

[2]  P. Yodzis,et al.  Local trophodynamics and the interaction of marine mammals and fisheries in the Benguela ecosystem , 1998 .

[3]  M. J. V. Zanden,et al.  PRIMARY CONSUMER δ13C AND δ15N AND THE TROPHIC POSITION OF AQUATIC CONSUMERS , 1999 .

[4]  Joel E. Cohen,et al.  Community Food Webs: Data and Theory , 1990 .

[5]  Robert R. Christian,et al.  Organizing and understanding a winter's seagrass foodweb network through effective trophic levels , 1999 .

[6]  A. Bode,et al.  Stable nitrogen isotopes reveal weak dependence of trophic position of planktivorous fish on individual size: A consequence of omnivorism and mobility , 2006 .

[7]  P. Marquet,et al.  On the relationship between trophic position, body mass and temperature: reformulating the energy limitation hypothesis , 2007 .

[8]  D. Pauly,et al.  Fishing down marine food webs , 1998, Science.

[9]  J. Hutchings,et al.  Trophic level scales positively with body size in fishes , 2011 .

[10]  Raymond L. Lindeman The trophic-dynamic aspect of ecology , 1942 .

[11]  K. Fritz,et al.  Comparing trophic position of stream fishes using stable isotope and gut contents analyses , 2008 .

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

[13]  C. Kendall,et al.  Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur , 2003 .

[14]  J. Kitchell,et al.  Long-term food web change in Lake Superior , 2009 .

[15]  G. Kling,et al.  Stable Isotopes and Planktonic Trophic Structure in Arctic Lakes , 1992 .

[16]  D. Pauly,et al.  Background and interpretation of the ‘Marine Trophic Index’ as a measure of biodiversity , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[17]  S. Scheu,et al.  Trophic niche differentiation in soil microarthropods (Oribatida, Acari): evidence from stable isotope ratios (15N/14N) , 2004 .

[18]  D. Hoeinghaus,et al.  Can stable isotope ratios provide for community-wide measures of trophic structure? , 2007 .

[19]  D. Schiel,et al.  Organismal traits are more important than environment for species interactions in the intertidal zone. , 2010, Ecology letters.

[20]  R. Latour,et al.  Turnover and fractionation of carbon and nitrogen stable isotopes in tissues of a migratory coastal predator, summer flounder (Paralichthys dentatus) , 2010 .

[21]  Robert G. Clark,et al.  Turnover of 13C in cellular and plasma fractions of blood: implications for nondestructive sampling in avian dietary studies , 1993 .

[22]  Jennifer A. Dunne,et al.  The Network Structure of Food Webs , 2005 .

[23]  Jennifer A Dunne,et al.  Major dimensions in food-web structure properties. , 2009, Ecology.

[24]  M. Huxham,et al.  Do Parasites Reduce the Chances of Triangulation in a Real Food Web , 1996 .

[25]  Neo D. Martinez,et al.  Limits to Trophic Levels and Omnivory in Complex Food Webs: Theory and Data , 2004, The American Naturalist.

[26]  Jean-Pierre Gabriel,et al.  Phylogenetic constraints and adaptation explain food-web structure , 2004, Nature.

[27]  Robert R. Christian,et al.  Evaluation of ecological network analysis : Validation of output , 2008 .

[28]  J. Rasmussen,et al.  Variation in δ15N and δ13C trophic fractionation: Implications for aquatic food web studies , 2001 .

[29]  T. Pedersen,et al.  Trophic studies in a high-latitude fjord ecosystem — a comparison of stable isotope analyses (δ13C and δ15N) and trophic-level estimates from a mass-balance model , 2008 .

[30]  Jennifer A. Dunne,et al.  Network structure and robustness of marine food webs , 2004 .

[31]  C. Harvey,et al.  A stable isotope evaluation of the structure and spatial heterogeneity of a Lake Superior food web , 2000 .

[32]  R. Ulanowicz,et al.  The Seasonal Dynamics of The Chesapeake Bay Ecosystem , 1989 .

[33]  Andrew D. Huberman,et al.  Finger-length ratios and sexual orientation , 2000, Nature.

[34]  Jason S. Link,et al.  Does food web theory work for marine ecosystems , 2002 .

[35]  P. McLoughlin,et al.  A hierarchical pattern of limiting factors helps explain variation in home range size , 2000 .

[36]  J. Olden,et al.  Quantitative approaches to the analysis of stable isotope food web data. , 2007, Ecology.

[37]  K. Stergiou,et al.  The effect of season and sex on trophic levels of marine fishes , 2008 .

[38]  J. E. Cohen,et al.  Food webs and niche space. , 1979, Monographs in population biology.

[39]  Werner Ulrich,et al.  Consumer-resource body-size relationships in natural food webs. , 2006, Ecology.

[40]  P. Marquet,et al.  Food web structure and body size: trophic position and resource acquisition , 2010 .

[41]  Neo D. Martinez,et al.  Simple rules yield complex food webs , 2000, Nature.

[42]  S. Allesina,et al.  Using trophic hierarchy to understand food web structure , 2009 .

[43]  J. Casselman,et al.  Stable isotope evidence for the food web consequences of species invasions in lakes , 1999, Nature.

[44]  S. Carpenter,et al.  Long-term variation in isotopic baselines and implications for estimating consumer trophic niches , 2008 .

[45]  D. Post USING STABLE ISOTOPES TO ESTIMATE TROPHIC POSITION: MODELS, METHODS, AND ASSUMPTIONS , 2002 .

[46]  W. Keegan,et al.  Stable Carbon- and Nitrogen-Isotope Ratios of Bone Collagen Used to Study Coral-Reef and Terrestrial Components of Prehistoric Bahamian Diet , 1988, American Antiquity.

[47]  S. Jennings,et al.  Weak cross‐species relationships between body size and trophic level belie powerful size‐based trophic structuring in fish communities , 2001 .

[48]  T. Romanuk,et al.  Stable isotope analysis of trophic position and terrestrial vs. marine carbon sources for juvenile Pacific salmonids in nearshore marine habitats , 2005 .

[49]  M. J. V. Zanden,et al.  Comparing trophic position of freshwater fish calculated using stable nitrogen isotope ratios (δ15N) and literature dietary data , 1997 .

[50]  K. Winemiller,et al.  Preservation Effects on Stable Isotope Analysis of Fish Muscle , 2002 .

[51]  M. Hemberg,et al.  Trophic levels and trophic tangles: the prevalence of omnivory in real food webs. , 2007, Ecology.

[52]  K. Gido,et al.  Use of Stable Isotopes to Test Literature-based Trophic Classifications of Small-bodied Stream Fishes , 2006 .

[53]  M. Minagawa,et al.  Stepwise enrichment of 15N along food chains: Further evidence and the relation between δ15N and animal age , 1984 .

[54]  Marta Coll,et al.  Structural Degradation in Mediterranean Sea Food Webs: Testing Ecological Hypotheses Using Stochastic and Mass-Balance Modelling , 2008, Ecosystems.

[55]  D. Pauly,et al.  Cross-Validation of Trophic Level Estimates from a Mass-Balance Model of Prince William Sound Using 15N/14N Data , 1998 .