Use of Fatty Acids From Aquatic Prey Varies With Foraging Strategy

Cornelia W Twining,Margaux Mathieu-Resuge,Tarn Preet Parmar,Jeremy Ryan Shipley,Dominik Martin-Creuzburg,Martin J Kainz

doi:10.3389/fevo.2021.735350

Abstract

Across ecosystems, resources vary in their nutritional composition and thus their dietary value to consumers. Animals can either access organic compounds, such as fatty acids, directly from diet or through internal biosynthesis, and the extent to which they use these two alternatives likely varies based on the availability of such compounds across the nutritional landscape. Cross-ecosystem subsidies of important dietary nutrients, like omega-3 long-chain polyunsaturated fatty acids (n-3 LC-PUFA), may provide consumers with the opportunity to relax the demands of synthesis and rely upon dietary flexibility rather than internal metabolic processes. Here, we examined how dietary flexibility and distance from a lake influenced the degree to which generalist insectivores relied upon dietary n-3 LC-PUFA from emergent aquatic insects versus n-3 LC-PUFA synthesized from precursor compounds found in terrestrial insects. We used bulk and compound-specific stable isotope analyses to understand spider and insectivorous bird (Blue Tit;Cyanistes caeruleus) reliance on aquatic and terrestrial resources, including dietary PUFA sources, along a riparian to upland gradient from a lake. We simultaneously investigated n-3 LC-PUFA synthesis ability in nestlings using13C fatty acid labeling. We found that riparian spiders took advantage of emergent aquatic insect subsidies, deriving their overall diet and their n-3 PUFA from aquatic resources whereas nestling birds at all distances and upland spiders relied upon terrestrial resources, including PUFA. Our13C labeling experiment demonstrated that nestling tits were able to synthesize the n-3 LC-PUFA docosahexaenoic acid from the dietary precursor α-linolenic acid, suggesting that they are not limited by aquatic resources to satisfy their LC-PUFA requirements. Overall, this study suggests that habitat generalist insectivores vary in the degree to which they can shift diet to take advantage of high-quality aquatic resources depending upon both their foraging flexibility and internal synthesis capacity.

Highlights

Cross-ecosystem subsidies can provide sources of physiologically important nutrients for a diversity of consumers
Animals require a diversity of organic compounds, such as vitamins, amino acids, and fatty acids, that vary in availability across the landscape (e.g., Hixson et al, 2015; Twining et al, 2019, 2021)
While a diversity of freshwater primary producers contain both EPA and DHA (Hixson et al, 2015; Twining et al, 2016a), few vascular terrestrial plants contain any detectable n-3 LC-PUFA (Hixson et al, 2015; Twining et al, 2016a). These ecosystem-based differences in fatty acid composition persist at higher trophic levels: studies suggest that terrestrial insects contain little to no n-3 LC-PUFA, while emergent freshwater insects are rich in these compounds, especially EPA (Hixson et al, 2015; Martin-Creuzburg et al, 2017; Twining et al, 2019)

Summary

INTRODUCTION

Cross-ecosystem subsidies can provide sources of physiologically important nutrients for a diversity of consumers. Aquatic ecosystems appear to be uniquely important sources of omega-3 long-chain polyunsaturated fatty acids (n-3 LC-PUFA) for consumers across ecosystems Both aquatic and terrestrial animals require n-3 LC-PUFA, in particular eicosapentaenoic acid (EPA, 20:5n-3) and docosahexaenoic acid (DHA, 22:6n-3), in order to survive and avoid growth limitation (e.g., Martin-Creuzburg et al, 2010; Brenna and Carlson, 2014). Web-building spiders and predatory beetles (e.g., Staphylinidae) that live across both upland and riparian zones opportunistically consume aquatic resources in areas where emergent insects are readily available (Kato et al, 2004; Paetzold et al, 2005; Stenroth et al, 2015; Kautza and Sullivan, 2016; Chari et al, 2020; Kowarik et al, 2021), suggesting that their foraging modes allow them to capture a wider array of different prey. We expected that upland tit nestlings would only have access to n-3 LC-PUFA-poor terrestrial arthropods, requiring greater internal n-3 LC-PUFA synthesis

MATERIALS AND METHODS

RESULTS

ETHICS STATEMENT