My research program focuses on addressing the ways in which animals cope with nutritional challenges from the scales of macromolecules to ecosystems.
While earth’s primary producers are limited by inorganic compounds and energy, animals face the additional challenge of acquiring a multitude of organic compounds, from vitamins to proteins, that they cannot make themselves and which are often species-specific. When an animal’s diet does not fulfill its physiological requirements, nutritional mismatches can result in problems ranging from reduced condition and survival at the individual level to decreased secondary production and food chain inefficiency at the ecosystem level.
A central goal of my research program is to understand how environmental pressures such as habitat degradation and phenological shifts under global climate change alter the nutritional environment for and affect fitness in physiologically constrained species. While primary producers at the base of some ecosystems provide animals with all of their required nutrients, other primary producers are either deficient in necessary nutrients or contain only their biochemical precursors. Because both energy and nutrients are essential for growth and reproduction, there is strong selection pressure on animals to adapt to nutritionally incomplete resources. Some animals, especially herbivores, have adapted by becoming efficient at converting available precursors into the crucial organic compounds they require. Other animals cope by: 1) consuming prey that have already done the work of conversion for them (predation), 2) relying on inputs of nutrients from other surrounding ecosystems (nutrient subsidies), or 3) specifically seeking out rare foods that contain scarce nutrients (nutrient-specific foraging). Although these forms of foraging-based adaptation require less in the way of biochemical machinery, they impose energetic costs through foraging and may expose animals to challenging environmental conditions, including predators and parasites. Moreover, animals may suffer from nutritional mismatches with local resources when nutritionally complete prey, subsidies, or rare resources are not available.
nutritional physiology: Molecules
Since beginning my PhD, I have focused on highly unsaturated omega-3 fatty acids (HUFAs), which are key organic compounds that animals can obtain through two very distinct eco-physiological pathways. Many algae at the base of aquatic food webs are rich in HUFAs and thus marine and freshwater food chains can provide animals in both aquatic and surrounding terrestrial ecosystems direct sources of HUFAs. In contrast, most vascular terrestrial primary producers completely lack HUFAs and contain only alpha linolenic acid (ALA), the precursor to HUFAs. As a consequence of this stark dichotomy in HUFA availability, animals from aquatic ecosystems are themselves richer in HUFAs than are animals from terrestrial ecosystems. To obtain HUFAs, animals that consume foods containing only ALA must convert ALA into HUFAs through the energy-demanding processes of elongation and desaturation. Because HUFAs are vital for all animals, there is likely to be selection for animals, such as mice, that consume terrestrial primary producers and other HUFA-poor foods to be highly efficient at converting ALA into HUFAs. In contrast, selection for conversion efficiency is likely to be relaxed for animals, such as marine fishes, that consume HUFA-rich foods.
I use studies at the scale of molecules to determine the ability of and efficiency with which animals can obtain nutrients from their molecular precursors. One of my goals is to understand whether or not individual nutrients are: 1) strictly essential (i.e., nutrients that animals cannot synthesize de novo from precursors), 2) dispensable (i.e., nutrients that animals can synthesize from precursors in sufficient quantities to fulfill their physiological needs in natural systems), or 3) ecologically essential (i.e., nutrients that animals are capable of synthesizing from precursors, but not in sufficient quantities to fulfill their needs). During my PhD research, I developed a new field-based d13C-enriched tracer method and found that while Tree Swallow (Tachycineta bicolor) chicks, which consume HUFA-rich aquatic insects, are able to synthesize HUFA from their precursor ALA, they are not able to do so efficiently and require additional direct dietary sources of HUFAs. In my postdoctoral research, I am building upon these findings to test how phenotypically plastic nestling Great Tits (Parus major) are in their ability to convert ALA to HUFAs based on their individual diets and proximity to aquatic habitats.
Twining, C. W., J. T. Brenna, N. G. Hairston, and A. S. Flecker. 2016. Highly unsaturated fatty acids in nature: what we know and what we need to learn. Oikos 125:749-760.
Twining, C. W., P. Lawrence, D. W. Winkler, A. S. Flecker, and J. T. Brenna. 2018. Conversion efficiency of alpha linolenic acid to omega-3 highly unsaturated fatty acids in aerial insectivore chicks. Journal of Experimental Biology 221(3).
Nutritional Needs: Organisms and populations
I also work at the whole organism level to test the degree to which a species’ dietary composition over evolutionary time can relax or increase selection on nutritional physiology, ultimately feeding back to make species dependent upon food resources that contain specific nutrients. To understand the importance of HUFAs for animals that consume HUFA-rich resources, I manipulated dietary fatty acid composition for my species of interest under controlled laboratory conditions. I found that when Eastern Phoebe (Sayornis phoebe) chicks, which like Tree Swallows regularly consume HUFA-rich aquatic insects, consumed lab diets richer in HUFAs, they grew faster and were in better condition compared to those fed diets richer in ALA, the HUFA precursor. In a fully factorial experiment manipulating food availability as well as fatty acid composition in Tree Swallow chicks, I found that even chicks fed a low quantity of high HUFA food grew faster and were in better condition compared to those fed a high quantity of low HUFA food. Together, these findings suggest that trophic ecology can have strong selective pressure on nutritional requirements.
At the population-level, I use long-term studies to understand the importance of resource composition for consumers. During my PhD, I combined data sets on Tree Swallow breeding success and aerial insect composition and biomass that spanned over 30 years. This allowed me to test if the biomass of aquatic insects, which provide Tree Swallows with a direct dietary source of HUFAs, influenced Tree Swallow breeding success. I found that aquatic insects had a strong positive influence on whether or not chicks survived to leave their nest while terrestrial insects had little to no effect on any metrics of breeding success. These findings also suggest that without access to healthy freshwater ecosystems, Tree Swallows and other riparian aerial insectivores may suffer dietary mismatches with terrestrial insects.
Twining, C. W., J. T. Brenna, P. Lawrence, J. R. Shipley, T. N. Tollefson, and D. W. Winkler. 2016. Omega-3 long-chain polyunsaturated fatty acids support aerial insectivore performance more than food quantity. Proceedings of the National Academy of Sciences 113:10920-10925.
Twining, C.W., J.R. Shipley, and D.W. Winkler. 2018. Aquatic insects drive breeding success in a riparian aerial insectivore. Ecology Letters. doi:10.1111/ele.13156.
Food quality in food Webs
Because variation in resource composition within communities and across landscapes sets the stage for selection upon nutritional physiology, I am also engaged in documenting food quality across natural systems. I use fatty acid composition analyses to characterize and compare the quality of food resources. For example, my colleagues and I have investigated the fatty acid composition of both stream invertebrate and fish communities , finding strong patterns in both cases based on diet and habitat. At the landscape scale, I have found similarly strong habitat and diet-based differences between ecosystems: I found that aquatic insects contained substantially more HUFAs than did terrestrial insects echoing patterns between aquatic and terrestrial primary producers.
To understand how animals cope with tremendous variation in food quality that they encounter in nature, I also trace how energy as well as nutrients move through food webs and ecosystems. For example, to understand the degree to which animals rely on external energy and nutrient subsidies versus local resources, I use Bayesian mixing models based on bulk carbon, nitrogen, and hydrogen bulk stable isotopes to estimate the degree to which animals rely upon food resources from different habitats. I have also used compound-specific stable isotopes to document the movement of HUFAs across the landscape. I found that even when Eastern Phoebe chicks consumed diets largely composed of terrestrial insects, they relied upon aquatic insects for their HUFAs. In combination with my previous findings on the nutritional importance of HUFAs for these birds, this work suggests that even small subsidies of nutritionally important compounds can play a crucially important role in food webs. Overall, this work suggests high food availability in the absence of ecologically essential nutrients cannot guarantee a species’ survival and thus that food web dynamics can be driven by both food quality and availability.
Wang, D. H., J. R. Jackson, C. Twining, L. G. Rudstam, E. Zollweg-Horan, C. Kraft, P. Lawrence, K. Kothapalli, Z. Wang, and J. T. Brenna. 2016. Saturated Branched Chain, Normal Odd-Carbon-Numbered, and n-3 (Omega-3) Polyunsaturated fatty acids in freshwater fish in the Northeastern United States. Journal of Agricultural and Food Chemistry 64:7512-7519.
Twining, C. W., D. C. Josephson, C. E. Kraft, J. T. Brenna, P. Lawrence, and A. S. Flecker. 2017. Limited seasonal variation in food quality and foodweb structure in an Adirondack stream: insights from fatty acids. Freshwater Science 36:877-892.