Nutritional hotspots? Prey from one ecosystem provide key fatty acids required for consumers in multiple ecosystems

Ecosystem boundaries are porous, and flows of materials and organisms from one ecosystem to the next are ubiquitous. Although the idea that consumers can obtain energy from multiple energy production channels was first noted by Lindeman (1942), classic work by Polis and Hurd (1996) helped to begin a concerted effort to understand the energetic connections between ecosystems. These resources and energy, originating from other ecosystems, are incredibly important for the organisms that receive them (Allen & Wesner, 2016; Baxter, Fausch, & Carl Saunders, 2005; Polis, Anderson, & Holt, 1997). For example, seaweed produced in marine ecosystems that washes onto shorelines can increase the abundance of terrestrial primary consumers and their predators (Spiller et al., 2010). It is not uncommon that the quantity of carbon flowing into an ecosystem can exceed in situ carbon production (Gounand, Little, Harvey, & Altermatt, 2018). Though the quantities of materials flowing into an ecosystem are certainly important, the quality of inflowing materials is thought to be a key factor in determining their importance for recipient consumers (Marcarelli, Baxter, Mineau, & Hall, 2011; Subalusky & Post, 2019). Yet, the hundreds of studies that have been published on this topic have generally focused on the magnitude of consumer responses to removals of these connections (Allen & Wesner, 2016) or on the magnitude of these fluxes themselves (Gounand et al., 2018). Studies that explicitly focus on the quality of cross-ecosystem energetic fluxes are far less common, representing a key knowledge gap in the field. In riparian ecosystems (the terrestrial ecosystems that border aquatic ecosystems), terrestrial predators feed on terrestrial insects produced locally in addition to aquatic insects that have a flying terrestrial adult stage (Sabo & Power, 2002). In stream ecosystems, stream primary consumers feed on locally produced algae as well as terrestrially produced plant detritus (Wallace, Eggert, Meyer, & Webster, 1999). Stream predators feed on locally produced aquatic insects and terrestrial insects that inadvertently fall into streams (Nakano, Miyasaka, & Kuhara, 1999). These reciprocal flows of resources are important, structuring the food webs of each ecosystem (Baxter et al., 2005). New work by Twining et al. (2019) shows that prey originating in terrestrial and aquatic ecosystems differ in nutritional quality, with profound implications for both ecosystems. Omega-3 highly unsaturated fatty acids (HUFAs) are known to be highly important in consumer diets (Twining et al., 2016), and HUFAs have been shown to be more abundant in aquatic than terrestrial organisms (Hixson, Sharma, Kainz, Wacker, & Arts, 2015). Twining et al. (2019) analysed the relative abundance of the short-chain precursor to HUFAs (ALA, alpha linolenic acid) versus HUFAs themselves within aquatic and terrestrial prey items, collected at three different study sites, and found that aquatic prey contained a much higher overall percentage of HUFAs, but not more ALA, compared to terrestrial prey. Thus, aquatic insect prey contained more HUFAs relative to terrestrial prey on a per capita basis at their study sites. Twining et al. (2019) then used stable isotope analyses of bulk tissues of stream fish and riparian birds to document how much aquatic versus terrestrial prey contributed to their overall diets. They showed diets of multiple fish species were dominated by aquatic prey (averaging ~90%). Yet, the abundance of aquatic prey in riparian bird (Eastern Phoebe, Sayornis phoebe) chick diet was much lower (averaging ~50%). So, stream fish and riparian birds differed in the overall contribution of aquatic insect prey to their diets. It makes sense that fish would get more HUFAs from aquatic prey if the quantity of prey ingested were the only important factor. But compound-specific stable isotope analyses of four different fatty acids showed that both stream fish and riparian bird chicks relied on aquatic insects for HUFAs in their diets (Twining et al. 2019). This demonstrates that, irrespective of the aquatic prey contribution to their overall diet, HUFAs came predominantly from aquatic insect prey. Moreover, Eastern Phoebe chicks fed a high-HUFA diet had mass growth rates 2–3 times greater than those fed a low-HUFA diet. Body condition of chicks fed a high-HUFA diet also increased more over time compared to that of chicks fed a low-HUFA diet (Twining et al. 2019). Collectively, this study elegantly shows that (a) aquatic insect prey contained more HUFAs, (b) aquatic insect prey contributions to diet were ~90% for stream fish and ~50% for riparian birds, (c) both stream fish and riparian birds relied on aquatic insects for HUFAs, even though they contribute to a smaller portion of riparian bird diet, and (d) riparian bird chick growth and body condition are greater when they are fed a high-HUFA diet. More broadly, this means that different ecosystems within a landscape can generate resources that differ in nutritional quality, which can benefit consumers residing in all ecosystems within the landscape because of cross-ecosystem energetic connections that are ubiquitous in nature. This new article by Twining et al. (2019) has the potential to change the way we think about cross-ecosystem resource flows, because it means that energetic (caloric) content of resource flows may be less important than initially thought. Resource flows could be small in magnitude, but high in nutritional value, and still be ecologically important. This concept should guide future work in the field. For example, in the aquatic–terrestrial study system used by Twining et al. (2019), we know that aquatic insect fluxes into terrestrial ecosystems are greater at the margin of ecosystem boundaries and that a much smaller portion of the aquatic insect flux (~10%) is found at greater distances (>100 m) in terrestrial ecosystems (Muehlbauer, Collins, Doyle, & Tockner, 2014). But given that Twining et al. (2019) show how important aquatic insects are as a source of HUFAs, this smaller aquatic insect flux could be disproportionally important for terrestrial consumers. Future work could also investigate how the spatial arrangement of ecosystems within the landscape might lead to ‘nutritional hotspots’ for consumers if resources produced by these ecosystems vary in nutritional value. I thank CW Twining and CW Fox for helpful comments on previous versions of this commentary.