Aquatic insects rich in omega‐3 fatty acids drive breeding success in a widespread bird

Twining, Cornelia W.; Shipley, J. Ryan; Winkler, David W.

doi:10.1111/ele.13156

Cited by 124 publications

(125 citation statements)

References 53 publications

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“…Recent studies highlight the importance of aquatic-derived EPA on the fitness of terrestrial predators. Using a 24-year dataset of tree swallows (Tachycineta bicolor), Twining et al (2018) were able to connect the breeding success in this bird species with availability of EPA-rich aquatic insects. Using a 24-year dataset of tree swallows (Tachycineta bicolor), Twining et al (2018) were able to connect the breeding success in this bird species with availability of EPA-rich aquatic insects.…”

Section: Discussionmentioning

confidence: 99%

“…While recent studies highlight the importance of PUFA-rich aquatic insects for the fitness of terrestrial predators (Fritz et al, 2017;Twining, Shipley, & Winkler, 2018), so far, our knowledge is limited about the variability in the export of fatty acids from aquatic ecosystems. First, predation can strongly regulate the abundance and biomass of emerging insects (Knight, McCoy, Chase, McCoy, & Holt, 2005;Wesner, 2016), including Chironomidae (Pitcher & Soluk, 2018).…”

Section: Introductionmentioning

confidence: 99%

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The emergence of fatty acids—Aquatic insects as vectors along a productivity gradient

et al. 2019

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1. Aquatic and terrestrial ecosystems differ fundamentally in the abundance of longchained polyunsaturated fatty acids (PUFAs), such as eicosapentaenoic acid (EPA; 20:5n-3), which are produced by aquatic algae, but only in low quantities by terrestrial plants. Aquatic insects, such as Chironomidae (non-biting midges) feed on algae during their larval stage, making them rich in EPA and therefore high-quality prey for insectivores after emergence. However, the magnitude of EPA subsidies from aquatic insects may be different among water bodies in response to abiotic (e.g. nutrient load) as well as biotic factors (e.g. food web structure).2. To test the predation effects of crucian carp (Carassius carassius), nutrient concentrations, and Chironomidae community composition on the fatty acid export from aquatic ecosystems, we conducted a 25-day experiment across 20 1,500-L mesocosms covering a total phosphorus (TP) gradient of 20-1,000 µg/L.3. Twice a week, we collected adult emerging Chironomidae and found differences in fatty acid composition in the two most abundant chironomid species emerging from the mesocosms. Two PUFAs, α-linolenic acid and EPA, contributed to most of the variation in Chironomidae fatty acid content across the nutrient gradient.Whereas the proportions of α-linolenic acid were positively correlated to the mesocosm TP concentration, we found a negative correlation for the proportions of Chironomidae EPA and mesocosm TP concentration. However, despite lower biomass-specific EPA content at higher TP, higher biomass of emerging Chironomidae at intermediate TP concentrations resulted in higher total export of PUFAs from water to land. 4. Predation pressure from carp decreased the biomass of emerging Chironomidae on average 8-fold. Chironomidae biomass showed a hump-shaped relationship along the TP-gradient and was strongly influenced by periphyton biomass. 5. Export rates of EPA and fatty acids in general responded in a quadratic manner along the nutrient gradient, reaching a maximum value at a TP of 400 µg/L and decreasing thereafter.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The emergence of fatty acids—Aquatic insects as vectors along a productivity gradient

et al. 2019

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“…Especially in the light of recent rapid aerial insectivore declines (Nebel, Mills, McCracken, & Taylor, ; Smith, Hudson, Downes, & Francis, ), nutritional mismatches between insectivores and aquatic insects have the potential for major species conservation consequences. For instance, mismatches between aquatic prey availability and nestling riparian bird demand, such as those that result as a consequence of human‐induced climate or land use changes, can result in reduced breeding success (Twining, Shipley, et al, ), which may ultimately contribute to population declines (Cox, Robertson, Fedy, Rendell, & Bonier, ). In contrast to terrestrial insectivores, aquatic consumers are unlikely to rely similarly upon reciprocal fluxes of terrestrial insects as sources of unique nutrients.…”

Section: Introductionmentioning

confidence: 99%

“…We therefore predict that riparian insectivores which, like many fish, consume aquatic prey are likely to have low capacity to synthesize HUFAs from ALA and as a consequence are likely to have high HUFA needs. Recent work shows that diets containing aquatic insects or with HUFA supplements can improve performance in riparian insectivores ranging from birds (Dodson, Moy, & Bulluck, 2016;Twining, Brenna, Lawrence, et al, 2016;Twining, Shipley, & Winkler, 2018) to spiders (Fritz et al, 2017), suggesting that riparian consumers may be uniquely reliant upon aquatic subsidies of HUFAs, especially EPA. Recent work also shows that Tree Swallow (Tachycineta bicolor) nestlings are limited in their ability to convert ALA into HUFA and thus likely require HUFAs from aquatic insects in nature (Twining, Lawrence, Winkler, Flecker, & Brenna, 2018).…”

Section: Introductionmentioning

confidence: 99%

Aquatic and terrestrial resources are not nutritionally reciprocal for consumers

et al. 2019

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Aquatic and terrestrial ecosystems are connected through reciprocal fluxes of energy and nutrients that can subsidize consumers. Past research on reciprocal aquatic–terrestrial subsidies to consumers has generally focused on subsidy quantity while ignoring major differences in the nutritional composition of aquatic and terrestrial resources. Because aquatic resources contain substantially more highly unsaturated omega‐3 fatty acids (HUFAs) than terrestrial resources, aquatic subsidies may play a unique role by supplying these critical compounds to both aquatic and terrestrial consumers. Here, we first characterized nutritional quality in terms of HUFA content in aquatic and terrestrial insect prey. We then used bulk stable isotope analyses to estimate subsidy use by stream and riparian consumers coupled with compound‐specific stable isotope analyses, which allowed us to document consumer HUFA sources. Finally, in order to understand the nutritional importance of aquatic‐derived HUFAs for riparian consumers, we conducted manipulative diet experiments on Eastern Phoebe (Sayornis phoebe) chicks in the laboratory. Aquatic insects were significantly enriched in HUFAs, mainly in terms of eicosapentaenoic acid (EPA), compared with terrestrial insects. Stream fishes relied mainly upon aquatic resources, while insectivorous birds varied in their use of aquatic subsidies across sites. However, like stream fishes, Eastern Phoebe chicks received HUFAs from aquatic insects, even when they were heavily reliant upon terrestrial insects for their overall diet. In the laboratory, dietary HUFAs, such as those supplied by aquatic insects, increased the growth rate and condition of Eastern Phoebe chicks. This study demonstrates that aquatic and terrestrial subsidies are not nutritionally reciprocal from the perspective of consumers because aquatic resources are the main source of critical fatty acids for both stream and riparian consumers. It also confirms previous findings on the nutritional importance of HUFAs for riparian birds, demonstrating that an insectivorous riparian lifestyle influences avian nutritional needs. Finally, our findings raise the possibility that birds and other riparian insectivores may experience nutritional mismatches with terrestrial prey if they do not have access to high‐quality aquatic subsidies as a consequence of aquatic habitat degradation or shifts in consumer and resource phenology. A free Plain Language Summary can be found within the Supporting Information of this article.

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“…Females with brighter plumage, higher stress resilience and—to a lesser extent—weaker negative feedback in the glucocorticoid stress response had lower overall methylation at a set of DMRs throughout the genome. Because tree swallows routinely experience challenging environmental conditions in the breeding season (Twining et al, ; Winkler et al, ), resilience to challenges is a major predictor of breeding success (Zimmer et al, ), impacting both individual fitness and population vulnerability. Plumage brightness also predicts both stress resilience and social connectivity (Taff et al, ).…”

Section: Discussionmentioning

confidence: 99%

Genome‐wide variation in DNA methylation is associated with stress resilience and plumage brightness in a wild bird

2019

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Individuals often differ in their ability to cope with challenging environmental and social conditions. Evidence from model systems suggests that patterns of DNA methylation are associated with variation in coping ability. These associations could arise directly if methylation plays a role in controlling the physiological response to stressors by, among other things, regulating the release of glucocorticoids in response to challenges. Alternatively, the association could arise indirectly if methylation and resilience have a common cause, such as early‐life conditions. In either case, methylation might act as a biomarker for coping ability. At present, however, relatively little is known about whether variation in methylation is associated with organismal performance and resilience under natural conditions. We studied genome‐wide patterns of DNA methylation in free‐living female tree swallows (Tachycineta bicolor) using methylated DNA immunoprecipitation (MeDIP) and a tree swallow genome that was assembled for this study. We identified areas of the genome that were differentially methylated with respect to social signal expression (breast brightness) and physiological traits (ability to terminate the glucocorticoid stress response through negative feedback). We also asked whether methylation predicted resilience to a subsequent experimentally imposed challenge. Individuals with brighter breast plumage and higher stress resilience had lower methylation at differentially methylated regions across the genome. Thus, widespread differences in methylation predicted both social signal expression and the response to future challenges under natural conditions. These results have implications for predicting individual differences in resilience, and for understanding the mechanistic basis of resilience and its environmental and social mediators.

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Aquatic insects rich in omega‐3 fatty acids drive breeding success in a widespread bird

Cited by 124 publications

References 53 publications

The emergence of fatty acids—Aquatic insects as vectors along a productivity gradient

The emergence of fatty acids—Aquatic insects as vectors along a productivity gradient

Aquatic and terrestrial resources are not nutritionally reciprocal for consumers

Genome‐wide variation in DNA methylation is associated with stress resilience and plumage brightness in a wild bird

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