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.

1 INTRODUCTION

Energy and nutrient exchanges between ecosystems, known as ecological subsidies, can increase consumer production beyond what would be possible with internal resources alone (Polis, Anderson, & Holt, 1997). Animals that move from aquatic to terrestrial ecosystems as part of their life cycles can subsidize terrestrial predators by providing them with additional sources of energy and nutrients (Baxter, Fausch, & Saunders, 2005; Muehlbauer, Collins, Doyle, & Tockner, 2013; Nakano & Murakami, 2001). Reciprocally, terrestrial leaves can serve as subsidies for a diversity of aquatic invertebrates while terrestrial insects can serve as subsidies for insectivorous fishes (Baxter et al., 2005; Nakano & Murakami, 2001). Previous work on the importance of ecological subsidies has largely focused on quantifying flux sizes of energy and nutrients moving between ecosystems (Polis et al., 1997; Gratton & Vander Zanden, 2009; but see Marcarelli, Baxter, Mineau, & Hall, 2011). However, because animals require a diverse array of elemental nutrients and organic compounds in addition to energy, examining subsidies based on flux sizes alone may not accurately represent the importance of subsidies to consumers. Even if reciprocal subsidies between ecosystems are similar in magnitude, but differ in nutritional content, they may not be equivalent from the perspective of consumers. Understanding the physiological importance of nutrients that vary between subsidized and local resources and documenting their movement across ecosystem boundaries remain key challenges in evaluating the significance of subsidies for consumers.

Emerging aquatic insects appear to play a unique role across the aquatic–terrestrial interface by providing terrestrial insectivores in riparian areas with a source of scarce, but nutritionally valuable highly unsaturated omega-3 fatty acids (HUFAs), especially the HUFA eicosapentaenoic acid (EPA, 20:5n-3; 7,8). HUFAs are physiologically important fats involved in animal nervous, hormonal, immune and cardiovascular systems (Twining, Brenna, Hairston, & Flecker, 2016). While their molecular precursor, the shorter-chain omega-3 fatty alpha-linolenic acid (ALA), is present throughout both aquatic and terrestrial food webs, HUFAs are extremely rare at the base of terrestrial food webs, but can be highly abundant at the base of aquatic food webs (Hixson, Sharma, Kainz, Wacker, & Arts, 2015; Twining, Brenna, Hairston, et al., 2016). For example, while very few terrestrial vascular plants contain any HUFAs, eukaryotic algae, the major primary producers in aquatic systems, are rich in both EPA and docosahexaenoic acid (DHA, 22:6n-3; Twining, Brenna, Hairston, et al., 2016). Thus, although aquatic and terrestrial insects have similar elemental composition (Elser et al., 2000), they are not nutritionally equivalent food sources for predators: aquatic insects have much higher concentrations of HUFAs, particularly EPA, than do terrestrial insects (Hixson et al., 2015). Consequently, emergent aquatic insects that enter riparian food webs are likely to be more nutritionally valuable as a source of scarce compounds for terrestrial consumers than reciprocal fluxes of terrestrial leaves or terrestrial insects are for freshwater consumers.

Some animals consuming HUFA-poor diets, such as terrestrial vertebrate herbivores, are relatively efficient at synthesizing HUFAs through elongation and desaturation from the molecular precursor, ALA (Twining, Brenna, Hairston, et al., 2016). In contrast, other animals that have HUFA-rich diets have effectively lost this capacity, either because they live in environments with an abundance of HUFA at the base of their food web in the case of marine fishes (Sargent, Bell, McEvoy, Tocher, & Estevez, 1999) or because their prey have done the work of conversion for them in the case of strict top carnivores like cats (Rivers, Sinclair, & Crawford, 1975). Like many fish and other animals with high dietary HUFA requirements, insectivorous birds in riparian zones have evolved in environments with access to HUFA-rich prey where the selective pressure to maintain highly efficient enzymes for ALA elongation and desaturation has likely been low. 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).

If birds and other riparian insectivores rely on aquatic insects for nutrients that are scarce in terrestrial ecosystems, they may be particularly susceptible to nutritional mismatches in the absence of access to aquatic prey. Especially in the light of recent rapid aerial insectivore declines (Nebel, Mills, McCracken, & Taylor, 2010; Smith, Hudson, Downes, & Francis, 2015), 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., 2018), which may ultimately contribute to population declines (Cox, Robertson, Fedy, Rendell, & Bonier, 2018). In contrast to terrestrial insectivores, aquatic consumers are unlikely to rely similarly upon reciprocal fluxes of terrestrial insects as sources of unique nutrients.

By examining HUFA sources for both aquatic and riparian consumers, we examine the potential for aquatic resources to play a unique nutritional role across aquatic–terrestrial ecosystem boundaries. We focus on HUFA sources for stream fishes and Eastern Phoebe (Sayornis phoebe) chicks, which are common insectivorous riparian birds throughout Eastern North America (Weeks 2011). We first evaluated the nutritional quality of aquatic and terrestrial insects in terms of HUFAs as well as maternal fatty acid investment in Eastern Phoebe eggs. We then examined the degree to which stream and riparian consumers relied upon aquatic versus terrestrial resources by reconstructing the overall diets of wild Eastern Phoebe chicks as well as insectivorous stream fishes based on bulk δ¹³C, δ¹⁵N and δ²H analyses, expecting that birds would not be as reliant upon aquatic resources as fishes. To understand the nutritional significance of HUFAs for our chosen riparian consumer, we conducted a controlled laboratory manipulation of dietary fatty acid content for Eastern Phoebe chicks. We hypothesized that Eastern Phoebes would benefit from HUFA availability because they frequent riparian habitats with access to aquatic food resources, especially during the breeding season. Finally, we analysed the δ¹³C of fatty acids in Eastern Phoebe chicks, stream fishes and potential aquatic and terrestrial insect prey in nature to determine where stream and riparian consumers obtain their omega-3 fatty acids. We expected that riparian birds and stream fishes would both rely upon aquatic HUFA sources as a consequence of higher HUFA availability in aquatic systems.

2 MATERIALS AND METHODS

2.1 Resource use

To estimate the percentages of aquatic and terrestrial insects in overall Eastern Phoebe (Sayornis phoebe) diets, we used bulk carbon, nitrogen and hydrogen stable isotope analyses, which allowed us to discriminate between aquatic and terrestrial dietary resources. We collected aquatic insects, terrestrial insects and Eastern Phoebe chick blood from three temperate streams (see Table S1 for more details): West Candor Creek (42.2245°N, −76.4137°W), Miller Creek (42.2861°N, −76.4512°W) and Locke Creek (42.5755°N, −76.5293°W) in May and June of 2015 and 2016. Aquatic insects were captured with emergence traps, terrestrial insects were captured with pan traps, and both were captured with targeted sweep netting. Aquatic insect emergence rates from aquatic traps during the sampling period were generally low (West Candor Creek: mean of 0.11 mg m⁻² day⁻¹ ± 0.49 (1 SD); Miller Creek: 0.21 ± 1.21; and Locke Creek: 0.31 ± 1.64), but within the range of typical rates for temperate streams during the summer (Baxter et al., 2005; Kraus et al., 2014; Nakano & Murakami, 2001; Stenroth, Polvi, Fältström, & Jonsson, 2015). Aquatic insects included Baetidae (Ephemeroptera), Chironomidae (nematoceran Diptera), Heptageniidae (Ephemeroptera), Anisoptera (Odonata), Perlidae (Plecoptera), Tipulidae (nematoceran Diptera) and Trichoptera. Terrestrial insects included Coleoptera, Diptera, Hymenoptera and Lepidoptera. We confirmed that Eastern Phoebe parents were feeding chicks both aquatic and terrestrial insects with foraging observations. Eastern Phoebe chicks (clutch sizes of n = 5, n = 3 and n = 4 for West Candor Creek, Miller Creek and Locke Creek, respectively) were captured and bled for bulk and compound-specific stable isotope analyses with New York State Permit 1477, United States Fish and Wildlife Service Permit MB757670 and Cornell IACUC protocol 2001_0051.

To understand Eastern Phoebe resource use and omega-3 fatty acid sources compared with those of in-stream insectivorous predators, we also sampled stream fish, including Creek Chub (Semotilus atromaculatus), Blacknose Dace (Rhinichthys atratulus), Longnose Dace (Rhinichthys cataractae) and Slimy Sculpin (Cottus cognatus), with New York State Permit 1,233 and Cornell IACUC protocol 2013_0010. Individual chick blood samples, pooled insect samples (n ≥ 3 individuals per taxon) and individual fish samples (n = 3 fish per taxon) were dried at approximately 45°C for a minimum of 48 hr before being ground and packed for analyses. Approximately 0.5 mg of sample was used for δ¹³C and δ¹⁵N analyses carried out at the Cornell University Stable Isotope Laboratory on a Thermo DELTA V isotope ratio mass spectrometer interfaced to a NC2500 elemental analyser. Methionine and three additional in-house standards (www.cobsil.com) were used to standardize carbon stable isotopes values to Vienna Pee Dee Belemnite (VPDB) and nitrogen stable isotope values to N₂ of atmospheric air. Standard deviations for internal standards for δ¹³C and δ¹⁵N analyses ranged from 0.02‰ to 0.52‰ per run for five types of internal standards (n = 6–8 per standard per run). We also analysed bulk δ²H at the Cornell Stable Isotope Laboratory (standardized to Vienna standard mean ocean water). We accounted for exchangeable δ²H using an internal keratin standard corrected relative to two established standards (www.cobsil.com). Standard deviations for internal standards (n = 6–8 per run) for δ²H ranged from 0.13‰ to 5.51‰ per run for four types of internal standards (n = 6–8 per standard per run). We expected our consumers of interest to rely upon a mix of both aquatic and terrestrial prey, and we therefore chose not to correct δ²H for environmental water for either aquatic or terrestrial prey because environmental water corrections are not well-established for terrestrial taxa.

We used the R package MixSIAR (Stock et al. 2018) to reconstruct overall Eastern Phoebe and stream fish diets from bulk stable isotopes. We used these models to estimate the proportion of resources from either aquatic or terrestrial ecosystems that fish and Eastern Phoebes consumed and incorporated into tissues. Prior to running mixing models, we removed δ¹⁵N terrestrial insect taxa that had substantially higher δ¹⁵N values than those of Eastern Phoebes and which were unlikely to contribute substantially to insectivore diets (Drosophila spp., Staphylinidae and Scarabaeidae) based on past diet studies (Weeks, 2011) and our foraging observations. We ran mixing models for Eastern Phoebe chicks using trophic discrimination factors for bulk δ¹³C and δ¹⁵N (2.31 ± 0.119‰ for δ¹⁵N and 0.275 ± 0.093‰ for δ¹³C [means and standard deviations]) that we developed based on comparisons of Tree Swallow (Tachycineta bicolor) chick blood samples relative to known food under experimental conditions (Cornelia W. Twining, and Jeremy Ryan Shipley, personal communication). Our experimentally estimated TDF for Eastern Phoebe values are within range of those of other passerines (Healy et al., 2018). For stream fish, we used δ¹³C and δ¹⁵N TDF and their standard deviations from Post (2002). We assumed no TDF for δ²H (Solomon et al., 2009). We used uninformative priors in all models (i.e. we started with an assumption that Eastern Phoebes and insectivorous stream fishes have an equivalent probability of consuming either aquatic or terrestrial insects). All models included site as a random factor and were run with a long run time to reach model convergence. See Appendix S1 for MixSIAR diagnostic material.

2.2 Dietary manipulation

To test the effects of fatty acid composition on Eastern Phoebe performance, we raised Eastern Phoebe chicks in the laboratory on either (a) a high omega-3 (HUFA = EPA+DHA), but low short-chain omega-3 (ALA) diet, or (b) a high-ALA, low-HUFA diet. Total calories and per cent total omega-3 fatty acids were equivalent in both treatments (Twining, Brenna, Lawrence, et al., 2016; Table S2), allowing us to isolate the effects of omega-3 fatty acids generally versus HUFA specifically. We collected seventeen wild Eastern Phoebe chicks from 4 nests around Ithaca, NY, under New York State Permit 1477, United States Fish and Wildlife Service Permit MB757670 and Cornell Institutional Animal Care and Use Committee protocol 2001_0051. All chicks were approximately 4–5 days old and in their exponential growth stage (Murphy, 1981, 1994). To minimize effects of genes and shared pre- and post-hatch environment, chicks from individual nests were sorted into each of the two diet treatments. Additional details on chick care are described by Twining, Brenna, Lawrence, et al. (2016). We measured chick mass and headbill length and calculated specific growth rate ([ln(mass on day x) − ln(mass on day 0)]/[day x − day 0]) (Lampert & Trubetskova, 1996) and body condition (mass/headbill length) at the end of the experiment. We analysed growth rates and condition in R (3.3.3) using general linear models with combinations of food treatment, nest, experiment date and individual identity as factors (see Table S5). We assessed relative model support using Akaike's information criterion (Burnham & Anderson, 2003).

2.3 Fatty acid composition and compound-specific stable isotope analyses

To assess the fatty acid composition of potential prey items, we prepared fatty acid methyl esters (FAME) from whole aquatic insects, specifically, Baetidae, Chironomidae, Heptageniidae, Odonata, Perlidae, Tipulidae and Hydropsychidae, and whole terrestrial insects, specifically, Coleoptera, Diptera, Hymenoptera and Lepidoptera (adult Hesperiidae). To understand omega-3 fatty acid sources for aerial and in-stream insect predators, we prepared FAMEs from Eastern Phoebe chick blood and stream fish muscle plugs as well as potential insect prey. We quantified maternal fatty acid investment in eggs (i.e., the fatty acid composition that chicks start out with at hatch) by preparing FAMEs from whole Eastern Phoebe eggs that we collected opportunistically from a nest that was abandoned the night before (n = 4 eggs) at another local site (Cascadilla Creek: 42.44°N, −76.44°W).

We extracted all FAMEs using a modified one-step method (Garces & Mancha, 1993). We then quantified fatty acid composition using a BPX-70 (SGE Inc.) column and a HP5890 series II gas chromatograph–flame ionization detector (GC-FID). Chromatogram data were processed using PeakSimple. Response factors were calculated using the reference standard 462a (Nu-Check-Prep). FAMEs were identified using a Varian Saturn 2000 ion trap with a Varian Star 3400 gas chromatography–mass spectrometer run in chemical ionization mass spectrometry mode using acetonitrile as reagent gas as discussed in detail elsewhere (Van Pelt & Brenna, 1999). Response factor coefficients of variation for individual fatty acids ranged from 0.03% to 0.20%. We tested for differences in ALA and EPA at each site by terrestrial or aquatic insect origin using general linear models in R (3.3.3). We did not test for differences in DHA by insect origin and do not display results for DHA for insects because we only found detectable levels of DHA in one group of predatory insects (Perlidae stoneflies). We also analysed differences in per cent ALA, per cent EPA and per cent DHA between eggs and chick blood samples using nonparametric Mann–Whitney U tests in R 3.3.3.

Next, we used gas chromatography–combustion–isotope ratio mass spectrometry (GCC-IRMS) to measure the δ¹³C values of ALA, EPA and DHA (Goodman & Brenna, 1992; Plourde et al., 2014). An Agilent 6890 GC was interfaced to a Thermo Scientific 253 isotope ratio mass spectrometer via a custom-built combustion interface. Peaks were confirmed to be baseline separated and were calibrated against working standards with isotope ratios traceable to international standards calibrated to VPDB (Caimi, Houghton, & Brenna, 1994; Zhang, Tobias, & Brenna, 2009). The standard deviations for repeated sample runs for compound-specific δ¹³C analyses ranged from <0.01‰ to 0.73‰. We present δ¹³C data on ALA, the HUFA precursor, the HUFAs EPA and DHA as well as DPA, the intermediate between EPA and DHA for insects, Eastern Phoebes and insectivorous stream fish across all sites.

3 RESULTS

3.1 Resource use

Eastern Phoebe chicks consumed both aquatic and terrestrial insects, but the proportions varied substantially across the landscape (Figure 1a–c). Mixing models based on δ¹³C and δ¹⁵N and mixing models based on δ²H and δ¹⁵N provided similar estimates of chick diet (Table S3). Eastern Phoebe chicks around West Candor Creek consumed more aquatic insects than terrestrial insects, chicks at Locke Creek consumed equivalent amounts of aquatic and terrestrial insects, and chicks at Miller Creek consumed more terrestrial insects than aquatic insects (Figure 1).

Details are in the caption following the image — **Figure 1**
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Estimated fraction of diet from aquatic (blue hatched) and terrestrial (green solid) insects based on carbon and nitrogen stable isotope mixing models for (a) West Candor Creek, (b) Locke Creek and (c) Miller Creek. Means and ±1 SD shown. Sample sizes used to create mixing model shown for each species

While Eastern Phoebe chicks relied on variable proportions of aquatic and terrestrial resources across the landscape, insectivorous fishes at all sites appeared to rely primarily on aquatic resources (Figure 1a–c). Blacknose Dace, Longnose Dace and Creek Chub all consumed over 80%–90% of their diets as aquatic insects (Figure 1a–c; Table S3). As was the case for Eastern Phoebes, mixing models based on δ¹³C and δ¹⁵N and mixing models based on δ²H and δ¹⁵N provided similar estimates of fish diet (Table S3). Slimy Sculpin had bulk δ¹³C and bulk δ²H that were much lower than those of either aquatic or terrestrial insects. Consequently, our mixing models for Slimy Sculpin diet fit poorly (Table S3).

3.2 Fatty acid composition

Fatty acid composition analyses allowed us to quantify nutritional differences between aquatic and terrestrial insects and to characterize parental nutritional investment in eggs and chicks. Across the landscape, the short-chain omega-3 HUFA precursor, ALA, was present in all terrestrial and aquatic insects (Figure 2a. Mean per cent ALA was not significantly different between terrestrial and aquatic insects at West Candor Creek (GLM: t = 0.87; df = 14; p = 0.40; Table S4), but mean per cent ALA was significantly higher across terrestrial insects compared to all aquatic insects at Locke Creek (GLM: t = 2.7; df = 20; p < 0.01; Table S4) and Miller Creek (GLM: t = 2.28; df = 20; p < 0.05; Table S4). The higher mean per cent ALA across terrestrial insects was driven mainly by high ALA in terrestrial Hymenoptera (i.e. bees) and Lepidoptera (i.e., butterflies; Figure 2a). Our data also demonstrate that aquatic insects were significantly richer in mean per cent EPA than were terrestrial insects across sites (Figure 2b). The HUFA EPA was significantly higher in aquatic insects than terrestrial insects at West Candor Creek (GLM: t = −8.17; df = 15; p < 0.0001; Table S4), Locke Creek (GLM: t = −19.11; df = 20; p < 0.0001; Table S4) and Miller Creek (GLM: t = −5.24; df = 20; p < 0.0001; Table S4). Within aquatic insects, mayflies and stoneflies had the highest per cent EPA (Figure 2b). Only predatory stoneflies contained trace amounts of DHA within our detection limits.

Eastern Phoebe chick blood and eggs contained the HUFA precursor ALA as well as both EPA (Figure 2a,b) and DHA (mean and one standard deviation in: chick blood = 3.20 ± 0.24%, 4.00 ± 0.20%, 4.53 ± 0.19% for West Candor Creek, Locke Creek and Miller Creek, respectively; egg DHA = 3.75 ± 2.24%). Per cent ALA was significantly higher in Eastern Phoebe chick blood than in eggs (Figure 2a; W = 0, p < 0.01). In contrast, per cent EPA was significantly higher in eggs than in chick blood (Figure 2b; W = 44, p < 0.001). Per cent DHA was similar in both eggs and chick blood (W = 14, p = 0.343).

3.3 Dietary manipulation

We manipulated the HUFA and ALA content, but not the overall energetic (i.e. carbon) content, of diets for chicks in the laboratory, feeding them either: (a) a high-HUFA (EPA and DHA), low-ALA diet, or (b) a high-ALA, low-HUFA diet. High-HUFA diets led to mass growth rates that were 2–3 times higher than those of chicks on HUFA diets (Figure 3a; Table S5). Chick body condition increased relative to initial body condition in both treatments: condition increased by 12% in low-HUFA chicks and 17% in high-HUFA chicks by day four of the experiment (Figure 3b; Table S5). Our best-supported model for mass-specific growth rates included treatment, experiment date and nest, all of which were highly significant (Table S5), while the best-supported model for condition included experiment date, treatment, the interaction of date and treatment and nest, which were highly significant (Table S5), as well as individual (Table S5). None of the factors that we included in our models had significant effects on headbill growth rate (Table S5), which was similar across treatments (Figure 3c).

3.4 Fatty acid sources

Our compound-specific δ¹³C data showed that even when terrestrial resources comprise a major portion of riparian predator diets, aquatic resources provide riparian predators with all of their EPA (Figure 4a–c). Even though Eastern Phoebe chicks were far more reliant upon terrestrial resources for overall diet than were stream fishes (Figure 1a–c), patterns in Eastern Phoebe chick compound-specific δ¹³C were strikingly similar to those in fishes, especially Creek Chub (Figure 4a–c). Compound-specific δ¹³C showed that Eastern Phoebe chicks as well as fish at all sites likely derived all EPA from aquatic sources (Figure 4a–c), reflecting the high EPA availability in aquatic insects: the standard deviations of chick and fish EPA δ¹³C values overlapped with mean aquatic insect EPA δ¹³C values, but chick and fish means were both slightly depleted relative those of aquatic insects. While mean terrestrial Lepidoptera EPA δ¹³C values were also similar to mean aquatic insect EPA δ¹³C values (Figure 4a–c), Lepidoptera contained only very minor amounts of EPA (Figure 2b), making it unlikely that either Eastern Phoebes or stream fishes were reliant upon Lepidoptera for their EPA and other HUFA. Across sites and predator species, DPA and DHA were generally enriched relative to their two possible precursors, ALA and EPA (Figure 4a–c).

While aquatic insects appeared to be the main source of EPA for both stream and riparian predators, compound-specific δ¹³C analyses demonstrated that Eastern Phoebe chicks and stream fishes may get their ALA from either aquatic or terrestrial insects (Figure 4a–c), especially Lepidoptera, reflecting mixed predator diets and high ALA availability in Lepidoptera (Figure 2a). Following patterns in overall diet (Figure 1a–c), terrestrial Lepidoptera and aquatic insects appeared to be the main ALA source for chicks based the overlap or slight depletion of mean chick ALA δ¹³C values relative to Lepidoptera and aquatic insect ALA δ¹³C values (Figure 4). Stream fish also had variable ALA sources among species and sites again reflecting patterns in overall diet (Figure 1a–c). Like Eastern Phoebe chicks, Creek Chub and Blacknose Dace at Miller Creek may have derived ALA from either aquatic or terrestrial insects (Figure 4a). In contrast, Slimy Sculpin at Miller Creek, Blacknose and especially Longnose Dace at Locke Creek and Creek Chub and Blacknose Dace at West Candor had much more depleted δ¹³C-ALA values than did chicks and thus appeared to derive ALA from aquatic insects (Figure 4a–c).

4 DISCUSSION

We examined the nutritional composition of reciprocal aquatic–terrestrial subsidies between streams and surrounding riparian habitats, finding that aquatic and terrestrial subsidies are not equivalent from the perspective of consumers. Riparian and aquatic consumers alike relied upon aquatic ecosystems as a source of scarce, but physiologically important compounds. As in other recent studies, aquatic insects were substantially and significantly richer in HUFAs, most notably EPA, than were terrestrial insects. In spite of this major difference in resource quality, riparian birds and stream fishes relied upon terrestrial as well as aquatic resources for their overall diets. However, compound-specific stable isotope analyses revealed that regardless of their contribution to overall diet, aquatic insects provided EPA for Eastern Phoebe chicks as well as for stream fishes. In addition, we found that HUFAs increase growth and condition during Eastern Phoebe chick development. This echoes our previous findings in Tree Swallow chicks (Twining, Brenna, Lawrence, et al., 2016), which are also riparian insectivores, but are not closely related to Eastern Phoebes (Hirundinidae vs. Tyrannidae), suggesting that habitat and diet may have a strong selective influence on nutritional physiology independent of phylogeny.

Across sites, aquatic insects were significantly richer in per cent EPA compared to terrestrial insects, some of which are richer in per cent ALA, the HUFA precursor (Figure 2). These substantial differences in HUFA content, especially EPA, between aquatic and terrestrial insects are consistent with past meta-analysis findings (Hixson et al., 2015) and follow expectations based on the stark dichotomy in HUFA content at the base of aquatic and terrestrial food webs between major groups of freshwater algae, which are HUFA-rich, and most terrestrial vascular plants, which contain only the HUFA precursor ALA (Twining, Brenna, Hairston, et al., 2016). Aquatic insects most likely derived their EPA from diatoms, which are particularly rich in EPA and dominate many temperate stream periphyton communities (Honeyfield & Maloney, 2015). Interestingly, we found that DHA was only present above our detection limit in predatory stoneflies and constituted a much lower per cent composition than EPA. However, because individual predatory Perlidae stoneflies are relatively large, the total amount of DHA in a Perlidae stonefly may still be profitable for in-stream or riparian predators from a foraging efficiency perspective. In general, our findings for DHA are also consistent with previous findings in other predatory emergent insects, such as dragonflies (Popova et al., 2017) and phantom midges (Chaoborus flavicans; Martin-Creuzburg, Kowarik, & Straile, 2017).

Despite differing in their overall reliance upon aquatic versus terrestrial resources, stream and riparian consumers both relied on aquatic HUFA sources. Not surprisingly, given that aquatic insects made up the majority of their diets (Figure 1a–c), insectivorous stream fishes, especially Blacknose Dace and Creek Chub, relied on aquatic insects for their EPA (Figure 4a–c). Compound-specific δ¹³C data suggested that Slimy Sculpin, a benthic sit-and-wait stream insectivore, may have relied on other even more δ¹³C-depleted benthic sources of omega-3 fatty acids than the aquatic insects that we sampled, such as methanogen-processed carbon consumed by anoxia-tolerant insect taxa from the hyporheic zone (Kohzu et al., 2004). Although Eastern Phoebe chicks consumed both aquatic and terrestrial insects (Figure 1a–c), our compound-specific stable isotope data suggest that aquatic insects provided chicks with EPA (Figure 4a–c). Eastern Phoebes consume both aquatic and terrestrial insects (Weeks, 2011) and thus could have potentially derived their EPA and other HUFAs from their precursor ALA, which we found in terrestrial insects, especially Lepidoptera (Figure 2a). However, we argue that this possibility is unlikely because: (a) δ¹³C of ALA from aquatic insects and Lepidopterans overlapped, especially at Miller and Locke Creek (Figure 4a,b), suggesting that either could have provided ALA to insectivores, and (b) Eastern Phoebe compound-specific δ¹³C patterns were similar to those of stream fishes, which are unlikely to rely upon terrestrial Lepidoptera for either ALA or HUFAs (Figure 4). While fractionation can occur between dietary fatty acids and those in tissues (Bec et al., 2011; Twining and Shipley, personal observation), the strong δ¹³C separation between aquatic insects and terrestrial insects other than Lepidopterans suggests that fractionation processes alone were not responsible for the patterns we observed. Based on these results, we conclude that even when predators in the riparian zone consume a mix of both terrestrial and aquatic resources, aquatic resources can serve a unique nutritional role for riparian consumers as a source of compounds like HUFAs that are scarce in terrestrial ecosystems.

Moreover, our dietary experiment suggested that terrestrial resources alone may not allow riparian consumers to meet their nutrition requirements: we found that diets with equal amounts of either ALA or HUFA were not nutritionally equivalent for Eastern Phoebe chicks (Figure 3). Dietary HUFAs, but not ALA, increased mass growth rates and body condition (Figure 3a,b) for chicks undergoing rapid development, suggesting that riparian predators have high HUFA needs during development. These results have important implications for wild chicks because nestling body mass and body condition are key predictors of survival to fledging and overall breeding success in insectivorous songbirds (Winkler, 1993; Winkler & Adler, 1996). However, as in our previous study on Tree Swallow chicks (Twining, Brenna, Lawrence, et al., 2016), we found that dietary HUFAs did not impact skeletal growth rates (Figure 3c), which are thought to be relatively invariant in spite of dietary variation in many small passerine species during development (Leech & Leonard, 1997). Overall, these results fit with our previous findings in Tree Swallow chicks, which are also riparian insectivores, suggesting that riparian consumers may have high HUFA needs as a consequence of their diet and habitat.

The decreased growth and condition that we observed in chicks on low-HUFA, but high-ALA diets could have resulted from the energetic costs of converting precursors into HUFAs as well as direct HUFA limitation. ALA conversion to EPA and other HUFAs through elongation and desaturation is an energetically demanding process (Brenna & Carlson, 2014). Because they evolved in habitats with access to HUFA-rich aquatic insects, riparian insectivores have likely experienced little selection for highly efficient ALA to HUFA conversion. Although insects in general contained far more EPA than DHA, per cent DHA was much higher than per cent EPA in blood samples of Eastern Phoebe chicks (Figure 2b,c). This suggests that Eastern Phoebe chicks were most likely able to convert dietary EPA from aquatic insects into the other HUFAs DPA and DHA. While direct dietary sources of DPA and DHA may be preferable to EPA alone when available (e.g., in predatory stoneflies, dragonflies or phantom midges), EPA alone from aquatic insects likely provides riparian consumers with a more cost-effective route for HUFA acquisition than full process of ALA to HUFA conversion. For example, in Tree Swallow nestlings ALA to HUFA conversion efficiency appears to be too low to satisfy HUFA demand in natural systems (Twining, Lawrence, et al., 2018). Overall, our findings suggest that, like many fishes and other animals with access to HUFA-rich food resources (Twining, Brenna, Hairston, et al., 2016), terrestrial consumers with access to aquatic HUFA subsidies, such as those from aquatic insects, likely have limited ALA to HUFA conversion ability and thus high HUFA demands.

Our egg fatty acid composition data from the field, while based on a small sample size as a result of opportunistic sampling, further suggested that Eastern Phoebe chicks most likely access HUFAs from diet. The Eastern Phoebe eggs that we analysed contained only minor amounts of omega-3 fatty acids, including HUFAs, into eggs, which is consistent with expectations based on previously published data for other altricial (Speake and Wood 2005), income breeding birds (i.e., those that rely on local resources to fuel reproductive efforts, including both eggs and chicks). This means that Eastern Phoebe chicks, which more than double in mass during their first few days of life (Murphy, 1981, 1994), are unlikely to rely solely upon stored HUFAs from maternal investment into eggs. Instead, Eastern Phoebe parents appear to access local HUFAs from aquatic ecosystems to feed their chicks throughout the breeding season, thus creating the potential for a mismatch between nutritional requirement and resource availability if aquatic resources are not available. Future studies should examine the effects of aquatic resource availability on egg fatty acid composition to determine whether dietary HUFA availability influences maternal investment in Eastern Phoebes and other insectivores.

Although it is well-established that emergent aquatic insects can subsidize riparian predators like birds, previous studies on reciprocal aquatic–terrestrial subsidies have generally focused on subsidy quantity (Nakano & Murakami, 2001; Baxter et al., 2005; but see Marcarelli et al., 2011) while ignoring differences in the nutritional composition of aquatic and terrestrial insects. Our data show that focusing on biomass fluxes alone may tell only part of the story in studies evaluating the impacts of subsidies on food webs because differences in the nutritional composition of aquatic and terrestrial prey are not trivial for consumers. Aquatic ecosystems provide nutritionally crucial compounds for aquatic consumers like as well as consumers in surrounding riparian food webs, whereas terrestrial subsidies do not provide an equivalent nutritional benefit for aquatic consumers (Bartels et al., 2012). Based on this, we argue that the nutritional composition of subsidies is an important but currently overlooked factor that must be considered when evaluating the importance of subsidies for consumers.

Based on our findings, we argue that birds and other riparian consumers that rely on aquatic ecosystems for nutrients that are scarce in terrestrial ecosystems, as HUFAs are, may be uniquely sensitive to aquatic habitat destruction or degradation even when terrestrial habitat quality remains high. Because aquatic insect emergence events are often highly pulsed, especially in temperate systems (Baxter et al., 2005; Nakano & Murakami, 2001), birds and other terrestrial consumers that rely upon emergent insects may also be highly susceptible to phenological mismatches, such as when shifts in peak insect availability and breeding timing do not track each other (Both & Visser, 2001). Without access to emergent aquatic insects during the chick-rearing period, riparian insectivores like Eastern Phoebes may experience decreased developmental performance of their chicks, with the potential to lead to nesting failure and subsequent population declines. For example, aquatic insect biomass during rapid development is associated with increased fledging success (i.e., surviving to leave the nest) in Tree Swallow chicks (Twining, Shipley, et al., 2018). While nutritional mismatches in and of themselves represent a potential threat to riparian aerial insectivores like Tree Swallows and Eastern Phoebes, they are an even more important conservation consideration in the light of ongoing rapid aerial insectivore declines whose causes remain unresolved (Nebel et al., 2010).

More broadly, our findings on the importance of subsidy quality highlight the importance of considering multiple aspects of ecosystem subsidies in conservation. For example, while healthy migrations of spawning anadromous Pacific salmon (Oncorhynchus spp.) are well-established as subsidies of limiting inorganic nutrients, especially nitrogen and phosphorus, in streams, lakes and their surrounding riparian areas (Naiman et al., 2002; Schindler et al. 2003), they may play an equally important role as subsidies of aquatic HUFA for riparian predators, such as bears and otters. While cross-ecosystem subsidies from more to less productive systems are already well-established as sources of energy and inorganic nutrients, adding a consideration of nutrition suggests that restoring and maintaining subsidies across ecosystems that also differ in nutritional quality, such as those from aquatic to terrestrial ecosystems, may have even greater than previously anticipated conservation benefits for consumers.

ACKNOWLEDGEMENTS

We thank Rachel Corona, Vivien Ikwuozom and Sara Gonzalez for assistance in the field and laboratory. We thank Donghao Wang and Zhen Wang for assistance with fatty acid composition analyses. We thank Troy Tollefson for assistance in developing and manufacturing feeds. We thank J. Ryan Shipley for assistance in raising Eastern Phoebe nestlings, running stable isotope mixing models and providing various helpful suggestions throughout this project. We also thank Cliff Kraft for help locating Eastern Phoebe nestlings and for helpful suggestions on this project. Fieldwork and laboratory analyses were supported by an NSF DDIG DEB-1500997 to C.W.T. and USDA Hatch NYC-399-7461 to J.T.B. The NSF Graduate Research Fellowship Program and teaching assistantships from Cornell University supported C.W.T. during this research.

AUTHORS' CONTRIBUTIONS

C.W.T. designed the study, carried out the fieldwork and laboratory work, performed statistical analyses and drafted the manuscript; J.T.B. participated in the design of this study; P.L. carried out GC-FID and GCC-IRMS analyses and processed raw data; D.W.W. participated in the design of this study, assisted with permitting for fieldwork and helped draft the manuscript; A.S.F. participated in the design of this study and helped draft the manuscript; N.G.H. participated in the design of this study and helped draft the manuscript. All authors gave final approval for publication.

Open Research

DATA AVAILABILITY STATEMENT

The datasets supporting this article are available on Dryad Digital Repository at: https://doi.org/10.5061/dryad.7mc125c (Twining et al., 2019).

Supporting Information

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Citing Literature

Volume33, Issue10

October 2019

Pages 2042-2052

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Haldane Prize 2019

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Aquatic and terrestrial resources are not nutritionally reciprocal for consumers

Abstract

1 INTRODUCTION