Use of Fatty Acids From Aquatic Prey Varies With Foraging Strategy

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 using 13C 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. Our 13C 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.

Fatty acid composition differs between emergent aquatic and terrestrial insects—A detailed single system approach

“…Here, we explored this dichotomy in more detail, considering multiple aquatic and terrestrial insect orders as well as seasonal changes in the strength of FA separation between aquatic and terrestrial insects in a lake ecosystem. Emergent aquatic insects had higher mean PUFA content, specifically ALA, EPA, ARA, and DHA, than terrestrial insects, which is in line with previous studies on both river (Twining et al, 2019;Kowarik et al, 2021) and lake ecosystems (Mathieu-Resuge et al, 2021b;Twining et al, 2021b). Twining et al (2019) found higher ALA proportions in terrestrial Hymenoptera and Lepidoptera, but higher EPA proportions in aquatic insect taxa near streams in the Eastern United States during the 10.3389/fevo.2022.952292…”

“…In contrast, vascular terrestrial plants typically contain only C18-PUFA, such as linoleic acid (LIN; 18:2n-6) and α-linolenic acid (ALA; 18:3n-3), and lack the ability to synthesize LC-PUFA (Uttaro, 2006;Hixson et al, 2015). This ecosystem-based (i.e., aquatic compared to terrestrial) difference in primary producers' FA profiles is transferred to higher trophic levels and is also observed between the FA profiles of aquatic and terrestrial insects (Guo et al, 2018;Kowarik et al, 2021;Mathieu-Resuge et al, 2021b;Twining et al, 2021b).…”

“…Sampling in one ecosystem also revealed temporal differences in the dissimilarity between aquatic and terrestrial insect FA profiles, potentially impacting riparian predators that can feed on both aquatic and terrestrial prey. Consumers must either take up LC-PUFA from their prey or biosynthesize them from dietary C18-PUFA precursors in order to satisfy their physiological demands (Twining et al, 2021b). The high dissimilarity between aquatic and terrestrial insect FA profiles observed in spring and summer (e.g., May to August) emphasizes the importance of aquatic insects in providing LC-PUFA to riparian predators during the breeding season.…”

“…Although several insect families were represented in this global dataset, the insect sample size was rather limited (n < 70), which may explain the large variation observed in insect FA profiles. Insects from both ecosystems have also been compared in regard to their quality as prey for insectivorous riparian predators such as birds, spiders, and bats (Lam et al, 2013;Kowarik et al, 2021;Twining et al, 2021b). Aquatic insects have been found to be rich in EPA, while terrestrial insects were found to be higher in ALA (e.g., Hymenoptera and Lepidoptera; Twining et al, 2021c).…”

Climate change shifts the timing of nutritional flux from aquatic insects

“…The phenology of aquatic and terrestrial insect communities drives the seasonal availability of n-3 LCPUFA, which are important nutrients for a diversity of consumers reliant on insects, 33,54,55 including avian aerial insectivores. 11,14,56 We find that the peak biomass of aquatic insect emergence tends to occur earlier in the season and then declines in total output, whereas terrestrial insect biomass progressively increases throughout our observed season.…”