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Costs and compensation in zooplankton pigmentation under countervailing threats of ultraviolet radiation and predation

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Abstract

Evolutionary responses to opposing directions of natural selection include trade-offs, where the phenotype balances selective forces, and compensation, where other traits reduce the impact of one selective force. Zooplankton pigmentation protects from ultraviolet radiation (UVR) but attracts visual predators. This trade-off is understudied in the ocean where planktonic larvae in surface waters face ubiquitous UVR and visual predation threats. We tested whether crab larvae can behaviorally reduce UVR risk through downward swimming or expansion of photoprotective chromatophores. Then we examined whether more pigmented larvae are more heavily predated by silverside fish under natural sunlight in the tropics in three UVR treatments (visible light, visible + UVA, visible + UVA + UVB). Lastly, we tested the behavioral chromatophore response of larvae to predation threats in two light treatments. Armases ricordi avoided surface waters after exposure to sunlight with UVR. Armases ricordi, Armases americanum, and Eurypanopeus sp. consistently expanded chromatophores in UVR or visible light, while Mithraculus sculptus and Mithraculus coryphe showed no response. Fish preferred pigmented larvae on sunnier days in visible light lacking UVR. Lastly, both M. coryphe and M. sculptus unexpectedly expanded chromatophores in fish cues, but responses were inconsistent over trials and across light treatments. The more consistent larval responses to UVR than to predator cues and the lack of predator preferences in natural light conditions suggest that UVR may have a stronger influence on pigmentation than predation. This study improves our understanding of planktonic adaptation to countervailing selection caused by visual predation and exposure to UVR.

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Acknowledgements

Special thanks to Eric Sanford, Brian Gaylord, and three anonymous reviewers for comments on this manuscript; to Connor Dibble, Madeleine Rodríguez, Amit Aggarwal, and Cristina Provencio for field and laboratory assistance; to staff at STRI for logistical support. Collections were carried out under the República de Panamá Ministerio de Ambiente collecting permits SC/A-24-15 and SC/A-35-16. This project was funded by the National Geographic Young Explorer’s Grant, American Museum of Natural History Lerner-Gray Fund for Marine Research, UC Davis Hemispheric Institute of the Americas Tinker Summer Field Research Grant, UC Davis College of Agriculture and Environmental Science Jastro Shields Graduate Research Fellowship, and STRI Short-term Fellowship. SMB was funded by the National Defense Science and Engineering Graduate Fellowship during this project.

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  1. Samuel M. Bashevkin

    Present address: Delta Science Program, Delta Stewardship Council, 980 9th St. Suite 1500, Sacramento, CA, 95814, USA

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  1. Bodega Marine Laboratory and Department of Environmental Science and Policy, University of California, Davis, 2099 Westshore Rd, PO Box 247, Bodega Bay, CA, 94923, USA

    Samuel M. Bashevkin & Steven G. Morgan

  2. Smithsonian Tropical Research Institute, Panamá, República de Panamá

    John H. Christy

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SMB, JHC, and SGM conceived and designed the experiments. SMB performed the experiments, analyzed the data, and wrote the manuscript. JHC and SGM provided editorial advice.

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Correspondence to Samuel M. Bashevkin.

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Communicated by Pablo Munguia.

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Bashevkin, S.M., Christy, J.H. & Morgan, S.G. Costs and compensation in zooplankton pigmentation under countervailing threats of ultraviolet radiation and predation. Oecologia 193, 111–123 (2020). https://doi.org/10.1007/s00442-020-04648-2

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