Parmar, Tarn Preet
Aquatic-terrestrial linkages : export of polyunsaturated fatty acids from aquatic ecosystems via emerging insects and potential consequences for terrestrial invertebrate consumers
2023, Parmar, Tarn Preet
Freshwater and surrounding terrestrial ecosystems are tightly connected via bidirectional fluxes of organisms and materials that can support and maintain adjacent food webs. Emergent aquatic insects represent an important pathway through which freshwater-derived energy and nutrients are transferred across the aquatic-terrestrial ecosystem boundary. During their larval stage, aquatic insects incorporate essential biochemical nutrients that become available to riparian predators as they emerge into the terrestrial ecosystem as adults. Algae, unlike terrestrial plants, contain high proportions of long-chain polyunsaturated fatty acids (LC-PUFA) that are transferred to higher trophic levels (i.e., emergent insect larvae). Emergent insects are an important dietary energy and LC-PUFA source for riparian terrestrial predators such as birds, bats, and spiders. LC-PUFA, such as eicosapentaenoic acid (EPA), play an important role in animal physiology as they influence growth and reproduction in both aquatic and terrestrial consumers. In addition, they have many important cellular functions, such as maintaining membrane fluidity and serving as eicosanoid precursors. Consumers that cannot biosynthesize LC-PUFA from C18 PUFA precursors rely on a dietary supply of LC-PUFA. The general aim of this thesis was to better understand emergent aquatic insects from lentic ecosystems and their potential importance for riparian terrestrial predators. To achieve this, I together with colleagues, collected aquatic emergent insects, terrestrial insects, birds, and web-building spiders from and around several lakes. We used a combination of fatty acid analysis, stable isotopes (δ13C, δ15N), and compound-specific stable isotope analysis (CSIA) to quantify LC-PUFA export and the incorporation of those LC-PUFA into riparian predators. With this research, I demonstrated the importance of aquatic insects, as opposed to terrestrial insects, to potential riparian predators due to higher LC-PUFA content (e.g., EPA). My colleagues and I were also able to show higher emergent aquatic insect biomass from shallower lakes, in general, and in shallower areas of lakes compared to their pelagic areas. We also demonstrated the importance of fishponds in providing LC-PUFA to riparian predators in surrounding terrestrial ecosystems via emergent aquatic insects. We were also able to demonstrate the importance of lakes and riparian zones as critical habitats where riparian predators, such as web-building spiders, can have greater access to LC-PUFA as opposed to further inland. Finally, we demonstrated that future global warming may disrupt the timing of bird-breading season and peak aquatic insect emergence, resulting in lower availability of physiologically important LC-PUFA in a changing world. My research showed that emergent aquatic insects are an important vector of how LC-PUFA can be transferred from aquatic ecosystems to riparian terrestrial food webs. Future work can build on these findings and further quantify the LC-PUFA biosynthesis ability of riparian birds and spiders as a way to predict the physiological effect of a changing world with lower LC-PUFA availability on riparian terrestrial predators.
Dietary availability determines metabolic conversion of long‐chain polyunsaturated fatty acids in spiders : a dual compound‐specific stable isotope approach
2022-07, Mathieu‐Resuge, Margaux, Pilecky, Matthias, Twining, Cornelia W., Martin-Creuzburg, Dominik, Parmar, Tarn Preet, Vitecek, Simon, Kainz, Martin J.
Consumers feeding at the aquatic–terrestrial ecosystem interface may obtain a mixture of aquatic and terrestrial diet resources that vary in nutritional composition. However, in lake riparian spiders, the relative significance of aquatic versus terrestrial diet sources remains to be explored. We investigated the trophic transfer of lipids and polyunsaturated fatty acids (PUFA) from emergent aquatic and terrestrial insects to spiders at varying distances from the shoreline of a subalpine lake in Austria, using differences in fatty acid profiles and compound-specific stable carbon (δ13C) and hydrogen (δ2H) isotopes. The omega-3 PUFA content of emergent aquatic insects was higher than that of terrestrial insects. Emergent aquatic insects contained on average 6.6 times more eicosapentaenoic acid (EPA) and 1.2 times more α-linolenic acid (ALA) than terrestrial insects, whereas terrestrial insects contained on average 2.6 times more linoleic acid (LIN) than emergent aquatic insects. Spiders sampled directly on the lake and in upland habitats had similar EPA contents, but this EPA was derived from different diet sources, depending on the habitat. The δ13CEPA and δ2HEPA values of ‘lake spiders' revealed an aquatic diet pathway (i.e. EPA of aquatic origin). In contrast, EPA of spiders collected in terrestrial habitats was depleted in both 13C and 2H compared to any potential food sources, and their ALA isotopic values, suggesting that EPA was partly bioconverted from its dietary precursor ALA (i.e. internal pathway). The δ2H values of fatty acids clearly indicated that diet sources differed depending on the spider's habitat, which was less evident from the δ13C values of the fatty acids. Our data highlight that spiders can use two distinct pathways (trophic versus metabolic) to satisfy their physiological EPA demand, depending on habitat use and dietary availability.
Use of Fatty Acids From Aquatic Prey Varies With Foraging Strategy
2021-08-27, Twining, Cornelia W., Parmar, Tarn Preet, Mathieu-Resuge, Margaux, Kainz, Martin J., Shipley, Jeremy Ryan, Martin-Creuzburg, Dominik
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.
Export of dietary lipids via emergent insects from eutrophic fishponds
2022-10, Fehlinger, Lena, Mathieu-Resuge, Margaux, Pilecky, Matthias, Parmar, Tarn Preet, Twining, Cornelia W., Martin-Creuzburg, Dominik, Kainz, Martin J.
Fishponds, despite being globally abundant, have mainly been considered as food production sites and have received little scientific attention in terms of their ecological contributions to the surrounding terrestrial environment. Emergent insects from fishponds may be important contributors of lipids and essential fatty acids to terrestrial ecosystems. In this field study, we investigated nine eutrophic fishponds in Austria from June to September 2020 to examine how Chlorophyll-a concentrations affect the biomass of emergent insect taxa (i.e., quantity of dietary subsidies; n = 108) and their total lipid and long-chain polyunsaturated fatty acid content (LC-PUFA, i.e., quality of dietary subsidies; n = 94). Chironomidae and Chaoboridae were the most abundant emergent insect taxa, followed by Trichoptera, Ephemeroptera, and Odonata. A total of 1068 kg of emergent insect dry mass were exported from these ponds (65.3 hectares). Chironomidae alone exported 103 kg of total lipids and 9.4 kg of omega-3 PUFA. Increasing Chl-a concentrations were associated with decreasing biomass export and a decrease in total lipid and LC-PUFA export via emergent Chironomidae. The PUFA composition of emergent insect taxa differed significantly from dietary algae, suggesting selective PUFA retention by insects. The export of insect biomass from these eutrophic carp ponds was higher than that previously reported from oligotrophic lakes. However, lower biomass and diversity are exported from the fishponds compared to managed ponds. Nonetheless, our data suggest that fishponds provide crucial ecosystem services to terrestrial consumers by contributing essential dietary nutrients to consumer diets via emergent insects.
Climate change shifts the timing of nutritional flux from aquatic insects
2022, Shipley, J. Ryan, Twining, Cornelia W., Mathieu-Resuge, Margaux, Parmar, Tarn Preet, Kainz, Martin, Martin-Creuzburg, Dominik, Weber, Christine, Winkler, David W., Graham, Catherine H., Matthews, Blake
Climate change can decouple resource supply from consumer demand, with the potential to create phenological mismatches driving negative consequences on fitness. However, the underlying ecological mechanisms of phenological mismatches between consumers and their resources have not been fully explored. Here, we use long-term records of aquatic and terrestrial insect biomass and egg-hatching times of several co-occurring insectivorous species to investigate temporal mismatches between the availability of and demand for nutrients that are essential for offspring development. We found that insects with aquatic larvae reach peak biomass earlier in the season than those with terrestrial larvae and that the relative availability of omega-3 long-chain polyunsaturated fatty acids (n-3 LCPUFAs) to consumers is almost entirely dependent on the phenology of aquatic insect emergence. This is due to the 4- to 34-fold greater n-3 LCPUFA concentration difference in insects emerging from aquatic as opposed to terrestrial habitats. From a long-sampled site (25 years) undergoing minimal land use conversion, we found that both aquatic and terrestrial insect phenologies have advanced substantially faster than those of insectivorous birds, shifting the timing of peak availability of n-3 LCPUFAs for birds during reproduction. For species that require n-3 LCPUFAs directly from diet, highly nutritious aquatic insects cannot simply be replaced by terrestrial insects, creating nutritional phenological mismatches. Our research findings reveal and highlight the increasing necessity of specifically investigating how nutritional phenology, rather than only overall resource availability, is changing for consumers in response to climate change.
Fatty acid composition differs between emergent aquatic and terrestrial insects : a detailed single system approach
2022-08-16, Parmar, Tarn Preet, Kindinger, Alina L., Mathieu-Resuge, Margaux, Twining, Cornelia W., Shipley, Jeremy Ryan, Kainz, Martin J., Martin-Creuzburg, Dominik
Emergent insects represent a key vector through which aquatic nutrients are transferred to adjacent terrestrial food webs. Aquatic fluxes of polyunsaturated fatty acids (PUFA) from emergent insects are particularly important subsidies for terrestrial ecosystems due to high PUFA contents in several aquatic insect taxa and their physiological importance for riparian predators. While recent meta-analyses have shown the general dichotomy in fatty acid profiles between aquatic and terrestrial ecosystems, differences in fatty acid profiles between aquatic and terrestrial insects have been insufficiently explored. We examined the differences in fatty acid profiles between aquatic and terrestrial insects at a single aquatic-terrestrial interface over an entire growing season to assess the strength and temporal consistency of the dichotomy in fatty acid profiles. Non-metric multidimensional scaling clearly separated aquatic and terrestrial insects based on their fatty acid profiles regardless of season. Aquatic insects were characterized by high proportions of long-chain PUFA, such as eicosapentaenoic acid (20:5n-3), arachidonic acid (20:4n-6), and α-linolenic acid (18:3n-3); whereas terrestrial insects were characterized by high proportions of linoleic acid (18:2n-6). Our results provide detailed information on fatty acid profiles of a diversity of aquatic and terrestrial insect taxa and demonstrate that the fundamental differences in fatty acid content between aquatic and terrestrial insects persist throughout the growing season. However, the higher fatty acid dissimilarity between aquatic and terrestrial insects in spring and early summer emphasizes the importance of aquatic emergence as essential subsidies for riparian predators especially during the breading season.
Taxonomic composition and lake bathymetry influence fatty acid export via emergent insects
2021-12, Mathieu‐Resuge, Margaux, Martin-Creuzburg, Dominik, Twining, Cornelia W., Parmar, Tarn Preet, Hager, Hannes H., Kainz, Martin J.
1. The ecological role of emergent aquatic insects from lakes in exporting dietary polyunsaturated fatty acids (PUFA) across the freshwater-land interface is still poorly understood.
2. In this field study, we explored the seasonal biomass export of emergent insects from three subalpine lakes and investigated how lipids of emergent insects were related to lake bathymetry, lipids of organic matter in lake sediments (i.e., basal resources), and the taxonomic composition of insects.
3. The total lipid and PUFA fluxes of emergent insects were strongly related to taxonomy and lake bathymetry, but weakly associated with the PUFA content of the uppermost lake sediment layers. PUFA flux estimates of the dominant taxon, Chironomidae, from the shallowest lake (3 m depth; 125 g PUFA m−2 season−1) were considerably higher than those from the deepest lake (33 m depth; 56 g PUFA m−2 season−1), due to the higher per area biomass of emergent insects from this shallow lake. Insect taxonomy also affected the composition of PUFA transfer to land: Chironomidae were richer in ω-6 PUFA, such as linoleic acid (18:2n-6) and arachidonic acid (20:4n-6), whereas Ephemeroptera and Trichoptera contained more ω-3 PUFA, especially α-linolenic acid (18:3n-3) and eicosapentaenoic acid (20:5n-3).
4. Our findings suggest that taxon-specific differences in PUFA content and lake bathymetry jointly shape PUFA fluxes and thus the provisioning of emergent insects as dietary sources of physiologically important PUFA for riparian consumers.