This blog post is provided by John Whiteman and tells the #StoryBehindThePaper for the article “Quantifying capital vs. income breeding: new promise with stable isotope measurements of individual amino acids“, which was recently published in the Journal of Animal Ecology.

It is an intensive process to grow and support offspring – just ask anyone who has raised children. For wild animals, supporting rapidly-developing, new organisms creates many challenges, whether reproduction is viviparous (giving birth to live young) or oviparous (laying and hatching eggs). One fundamental concern is simply providing enough physical material for the developing offspring to synthesize new tissues. Animals have evolved two strategies to meet this demand: first, they can allocate material from consumed food directly to their offspring. This “income breeding” requires that their habitat and behavior allows consumption of enough resources, which may not always be possible. For example, during reproduction, some animals may forego feeding and dedicate their time to courtship or migration. Such a scenario leads to the second strategy, “capital breeding”, in which animals grow and support new offspring by mobilizing previously stored, endogenous nutrients. The use of “capital” – that is, resources which the animal already possesses – requires obtaining and storing the resources beforehand.

Many animals fall somewhere between pure income and pure capital strategies, with profound consequences for their natural history. In income breeding, the requirement for quantity and quality of food intake can change foraging behavior. In capital breeding, physiological adaptations must preserve organ function even as tissues are broken down and the material is diverted towards a developing egg or fetus. Because of the consequences of the fundamental differences between these strategies, ecologists have long sought methods to quantify the income-capital spectrum. Unfortunately, most methods are indirect proxies and ultimately lack the resolution required to fully understand the reproductive biology of wild animals.

In a new paper in JAE, my co-authors Seth Newsome, Paco Bustamante, Yves Cherel, Keith Hobson, and I describe and validate a new method for placing animals on this spectrum. This method takes advantage of technological advancements that have enabled the measurement of the stable isotope values of carbon and nitrogen (δ¹³C and δ¹⁵N, respectively) in individual amino acids from animal tissue. Of the 20 standard amino acids used to build proteins, a subset known as “trophic amino acids” readily exchange nitrogen atoms with other molecules. And, because animals tend to preferentially retain ¹⁵N while excreting ¹⁴N in waste, the pool of endogenous, stored nitrogen available for this exchange tends to be rich in ¹⁵N. As a result, the nitrogen exchange of trophic amino acids increases their δ¹⁵N value. We predicted that this nitrogen exchange occurs when stored nutrients are mobilized and diverted towards egg production, causing δ¹⁵N values of trophic amino acids in offspring tissue to be higher in capital breeders than in income breeders.

To test our idea, we compared stable isotope values of parent and offspring tissue between herring gulls (Larus argentatus) and emperor penguins (Aptenodytes foresteri). Herring gulls are typically income breeders and they are known to have continued food availability while developing their eggs; in addition, amino acid isotope data from this species was recently published and was available for comparison (Hebert et al., 2016). In contrast, emperor penguins are a classic example of capital breeding. The females fast for several weeks before mating, as they march inland to their rookeries and engage in courtship, then continue to fast throughout egg development. The lack of food income requires that these female penguins mobilize previously stored nutrients to develop their eggs. As a result of long-term field work at rookeries in Antarctica, enough samples from emperor penguin carcasses and abandoned eggs were opportunistically collected to enable isotopic analysis.

To compare emperor penguins and herring gulls, we had to first account for variation in environmental δ¹⁵N values. We accomplished this by standardizing to the δ¹⁵N value of amino acids that do not readily exchange their nitrogen, known as “source amino acids”. The resulting value, Δ¹⁵N_{trophic-source}, represents an offset in isotopic value that is related to the extent of nitrogen exchange – such as the exchange that occurs during mobilization of stored nutrients in capital breeding.

As we predicted, the eggs of emperor penguins had higher Δ¹⁵N_{trophic-source} values, as compared to the adults, than did herring gulls. The difference was clear for the trophic-source amino acid pair of Proline-Phenylalanine: in penguins, Δ¹⁵N_Pro-Phe was ~4 ‰ higher in eggs than in adult muscle, whereas in gulls Δ¹⁵N_Pro-Phe was nearly identical in eggs and in adult muscle. This difference was biologically significant and easily detected (instrument error is ≤0.5 ‰). We also measured δ¹³C values, which suggested that the amino acids in emperor penguin egg yolk were synthesized from a variety of endogenous sources, including carbon from stored fat. In contrast, the amino acids in emperor penguin egg albumen tended to be routed directly from adult muscle into the egg.

Our results provide a new empirical index for placing animals on the spectrum from capital to income breeding, and we hope that future researchers build on this work by applying the methods to additional species, including non-avian taxa. In addition, we also reveal surprisingly heterogenous sourcing for the amino acids that emperor penguins use to build new egg tissue. While rearing offspring will always be challenging, understanding the process is now a little bit easier.

Read the paper

Read the full paper: Whiteman, J.P., Newsome, S.D., Bustamante, P., Cherel, Y. and Hobson, K.A. (2020), Quantifying capital vs. income breeding: new promise with stable isotope measurements of individual amino acids. J Anim Ecol. Accepted Author Manuscript. https://doi.org/10.1111/1365-2656.13402