DNA barcoding increases resolution and changes structure in Canadian boreal shield lake food webs

Abstract

Food webs are important in understanding the structure, function, and behaviour of ecosystems, but, due to methodological limitations, are often poorly resolved in ways that impact food-web properties. Although DNA barcoding has proven useful in determining the diet of consumers, few studies have used this technique to determine food-web structure. These studies report mixed impacts on various food-web properties, but are limited by their taxonomic focus and their failure to evaluate DNA barcoding for both diet analysis and food-web structure. In this study, we show that, when compared to a morphological approach, DNA barcoding increases foodweb resolution by increasing the number and frequency of prey species identified in the stomach contents of eight species of Canadian boreal shield predatory fishes. In addition, we observed differences in food-web structure, such as increased generalism, habitat coupling, and omnivory, that have strong implications for food-web stability and dynamics. We conclude that DNA barcoding is a powerful tool to evaluate how resolution impacts foodweb properties and can help further our understanding of how food webs are structured by identifying feeding Research Article Open Access © 2015 Timothy J. Bartley et al. licensee De Gruyter Open. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivs 3.0 License. Timothy J. Bartley*, Heather E. Braid, Kevin S. McCann, Nigel P. Lester, Brian J. Shuter, Robert H. Hanner DNA barcoding increases resolution and changes structure in Canadian boreal shield lake food webs *Corresponding author:Timothy J. Bartley, Department of Integrative Biology, University of Guelph, 50 Stone Road East, Guelph, Ontario, Canada N1G 2W1, E-mail: timothy.bartley@gmail. com Heather E. Braid, Institute for Applied Ecology New Zealand, Auckland University of Technology, Private Bag 92006, Auckland, New Zealand 1010 Kevin S. McCann, Department of Integrative Biology, University of Guelph, 50 Stone Road East, Guelph, Ontario, Canada N1G 2W1 Nigel P. Lester, Brian J. Shuter, Science and Research Branch, Ontario Ministry of Natural Resources, Peterborough, Ontario, Canada K9J 7B8 Brian J. Shuter, Department of Ecology and Evolution, University of Toronto, Toronto, Ontario, Canada M5S 3G5 Robert H. Hanner, Biodiversity Institute of Ontario, University of Guelph, 50 Stone Road East, Guelph, Ontario, Canada N1G 2W1 Unauthenticated Download Date | 12/4/15 10:11 PM Lake food web resolution and DNA barcoding 31 highly refined picture of feeding interactions required to address issues surrounding food-web resolution. DNA barcoding is increasingly recognized as an effective means for identifying trophic interactions [15, 16, 17], making it a potentially powerful tool to parse out food-web structure [18, 19]. Barcoding uses a short, standardized DNA sequence and a molecular reference library (i.e., the Barcode of Life Data Systems, BOLD [20]) to identify species [21]. The efficacy of barcoding to establish feeding interactions comes in large part from its proven utility in identifying animal tissues when little or no morphological information is available [22, 23]. Many studies have now confirmed the value of barcoding in identifying prey in the stomach contents or feces of certain predators, such as bats [24], beetles [25], marine invertebrates [26, 27], seabirds [28], sharks [29], and other marine fishes [28, 30]. Additionally, some researchers have used taxon-specific approaches that rely on the DNA barcode region to identify feeding interactions of interest in bats [31] and insects [32], but very few studies have used barcoding at the scale of whole food webs. A small number of studies have used barcoding to establish feeding links in a whole food web, rather than the identification of prey species for a single consumer or prey taxon of interest [33, 34, 35]. These studies have consistently demonstrated that barcoding increases species diversity [33, 34], reveals more feeding links (about three times as many in Wirta et al. [35]), changes identifications (31% of links to the number of possible links [8] (connectance, although see Martinez [6]), and the presence of distinct subwebs [9] (compartmentation). Many observed patterns in food webs may be caused by poor resolution, implying a need for improved data and the development of new methods for evaluating food webs [2, 10]. Food-web resolution has largely been limited by methodological constraints. Accurate identification of the many feeding interactions that comprise food webs is difficult, especially in systems where direct observation of feeding by predators is impractical or nearly impossible. Morphological identification of prey from the stomach contents or feces of consumers has traditionally been used to describe detailed food-web structure. The constituent species in these morphology-based food-web datasets are often aggregated into taxonomic or trophic groups because of the considerable time, expense, and difficulty associated with identifying the vast number of species and feeding interactions present in ecosystems (e.g., [11]). This has led to alternative methods for establishing foodweb structure. For example, stable isotopes of carbon and nitrogen have been widely used because they can infer the trophic position and determine the carbon sources of consumers [12]. As a result, stable-isotope analysis provides a useful broad metric of food-web structure because it can identify the presence of major energy pathways [13] and shifts in the feeding habits of key species [14]; however, stable-isotope analysis does not provide the Table 1. Definitions of key terms.