Helpers at the nest buffer the oxidative costs of reproduction

A rare experiment with cooperatively breeding birds in the wild reveals high costs of reproduction but only in groups with few helpers.

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The white-browed sparrow weaver (Photo: Dom Cram)

Every breath we take damages our cells a little. This inevitable cost of metabolism, oxidative damage, accumulates with time and can contribute to pathology and senescence1. The potential role of oxidative stress in explaining inter-individual differences in life history trajectories and fitness has not gone unnoticed by evolutionary ecologists. Researchers have proposed that the accumulation of oxidative damage is expected to occur at greater rates during periods of heavy reproductive investment and thus may be a key physiological mechanism mediating life history trade-offs between current and future reproduction, and between reproduction and survival2,3. Empirical studies, however, have produced conflicting results4. The failure of some to show the expected relationship between reproduction and oxidative damage has been attributed to the lack of experimental manipulation of reproductive effort or to the fact that many studies were conducted in laboratory conditions where subjects are removed from ecological constraints5.

Writing in Proceedings of the Royal Society B: Biological Sciences, Cram and colleagues6 overcome some previous methodological issues by conducting a clutch-removal experiment with a cooperatively breeding bird in the Kalahari. The white-browed sparrow weaver, Plocepasser mahali, nests in territorial groups of 2-12 individuals, in which one dominant pair monopolises within-group reproduction and the remaining subadults help raise the offspring. To assess how reproductive effort affects oxidative status, Cram and colleagues monitored 20 groups of weavers until a full clutch of eggs was laid in each nest. They then captured all birds (except the incubating dominant females), weighed them and collected blood samples. In 9 of the groups, they removed all eggs. About a month after clutch-removal, Cram and colleagues re-captured the birds in all groups and collected follow-up measurements on condition and oxidative stress to compare if the birds with chicks differed from those without.

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An 8-day old chick (Photo by Dom Cram)

Contrary to expectations, there was no difference in weight loss between birds in groups that had their eggs removed and birds in groups that kept their eggs but had many helpers (group size 5-8 birds). Reproductive effort seemed to be cost-free. Individuals in small groups (2-4 birds) that raised chicks and had few helpers, however, lost more weight compared to the birds that underwent clutch removal. The data on oxidative stress paralleled the findings on weight loss.

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Dom Cram collecting a blood sample from one of the weavers.

Birds in small groups, rearing chicks, experienced increased levels of oxidative damage, compared to the birds whose eggs were removed. Breeding birds in large groups with chicks did not differ in oxidative damage from the birds not raising any chicks. Importantly, these effects were not due to differences in clutch size. Rather, it was the number of helpers available in large groups that acted as a buffer against the costs of increased reproductive
effort. This interpretation was further supported by the observation that among chick-raising birds, rates of provisioning were negatively associated with body mass – individual investment in reproductive effort carried significant energetic costs for the helpers. Although the level of oxidative damage was not associated with rates of provisioning, the level of total antioxidant protection was. Birds with higher provisioning rates exhibited lower antioxidant protection, making them more vulnerable to oxidative damage.

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As the weaver chicks grow, the demand on all the helpers to bring them food increases (Photo: Dom Cram)

This study measured only one marker of oxidative damage, lipid peroxidation, in plasma samples. Its conclusions are thus tentative, as oxidative damage to other biomolecules and in other tissues may reveal different patterns. Nevertheless, the contribuion of this work is important – not only because it is one of the few demonstrations of the oxidative costs of reproduction in the wild but because, uniquely, it reveals the role of cooperative breeding as a mechanism for mitigating these costs.

References

  1. Costantini, D. Oxidative Stress and Hormesis in Evolutionary Ecology and Physiology. (Springer Berlin Heidelberg, 2014). doi:10.1007/978-3-642-54663-1
  2. Metcalfe, N. B. & Alonso-Alvarez, C. Oxidative stress as a life-history constraint: the role of reactive oxygen species in shaping phenotypes from conception to death. Functional Ecology 24, 984–996 (2010).
  3. Monaghan, P., Metcalfe, N. B. & Torres, R. Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecology Letters 12, 75–92 (2009).
  4. Blount, J. D., Vitikainen, E., Stott, I. & Cant, M. A. Oxidative shielding and the cost of reproduction. Biological Reviews DOI: 10.1111 / brv, (2015).
  5. Metcalfe, N. B. & Monaghan, P. Does reproduction cause oxidative stress? An open question. Trends in Ecology & Evolution 28, 347–350 (2013).
  6. Cram, D. L., Blount, J. D. & Young, A. J. The oxidative costs of reproduction are group-size dependent in a wild cooperative breeder. Proceedings of the Royal Society B: Biological Sciences 282, 20152031–20152031 (2015).

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