Abstract
We know very little about the effects of two global stressors, elevated temperature and contaminants, on the grazing of marine copepods. To address this issue, we tested the hypotheses that the individual and combined effects of these two stressors may reduce grazing rates and may depend on food availability and gender. We exposed male and female Calanus finmarchicus copepods to pyrene at two temperatures (10 and 14 °C) and six food concentrations (25–800 μg C Rhodomonas baltica L−1) and measured fecal pellet size, and grazing rate (GR) from pellet production. Males had smaller fecal pellets and lower GR than did females. Temperature and pyrene exposure had no effect on pellet size. Temperature alone had no effect on GR of males, but females had lower GR at elevated temperature. Pyrene-exposed males and females had lower GR only at the food concentrations of 200–800 μg C R. baltica L−1 and those patterns were independent of temperature. Pyrene-induced reduction in GR was stronger in females than in males. The negative effects of both elevated temperature and pyrene may reduce the abundance and trophic success of C. finmarchicus in a warmer, more polluted future.


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Alexander MA, Scott JD, Friedland KD, Mills KE, Nye JA, Pershing AJ, Thomas AC (2018) Projected sea surface temperatures over the 21st century: changes in the mean, variability and extremes for large marine ecosystem regions of Northern Oceans. Elementa-Sci Anthropocene 6:9
Bakke T, Klungsøyr J, Sanni S (2013) Environmental impacts of produced water and drilling waste discharges from the Norwegian offshore petroleum industry. Mar Environ Res 92:154–169
Barata C, Calbet A, Saiz E, Ortiz L, Bayona JM (2005) Predicting single and mixture toxicity of petrogenic polycyclic aromatic hydrocarbons to the copepod Oithona davisae. Environ Toxicol Chem 24:2992–2999
Conover RJ (1966) Assimilation of organic matter by zooplankton. Limnol Oceanogr 11:338
Daase M, Kosobokova K, Last KS, Cohen JH, Choquet M, Hatlebakk M, Soreide JE (2018) New insights into the biology of Calanus spp. (Copepoda) males in the Arctic. Mar Ecol Prog Ser 607:53–69
Dell’Omo G (2002) Behavioural ecotoxicology. John Wiley & Sons, Chichester
Grenvald JC, Nielsen TG, Hjorth M (2013) Effects of pyrene exposure and temperature on early development of two co-existing Arctic copepods. Ecotoxicology 22:184–198
Gréve HV, Almeda R, Lindegren M, Kiorboe T (2017) Gender-specific feeding rates in planktonic copepods with different feeding behavior. J Plankton Res 39:631–644
Gusmao LFM, McKinnon AD (2009) Sex ratios, intersexuality and sex change in copepods. J Plankton Res 31:1101–1117
Helenius LK, Saiz E (2017) Feeding behaviour of the nauplii of the marine calanoid copepod Paracartia grani Sars: functional response, prey size spectrum, and effects of the presence of alternative prey. PLoS One 12:e0172902
Hinder SL, Gravenor MB, Edwards M, Ostle C, Bodger OG, Lee PLM, Walne AW, Hays GC (2014) Multi-decadal range changes vs. thermal adaptation for north east Atlantic oceanic copepods in the face of climate change. Glob Chang Biol 20:140–146
Hjorth M, Nielsen TG (2011) Oil exposure in a warmer Arctic: potential impacts on key zooplankton species. Mar Biol 158:1339–1347
IPCC (2013): Climate change 2013: The physical science basis: contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge
Irigoien X, Obermuller B, Head RN, Harris RP, Rey C, Hansen BW, Hygum BH, Heath MR, Durbin EG (2000) The effect of food on the determination of sex ratio in Calanus spp.: evidence from experimental studies and field data. ICES J Mar Sci 57:1752–1763
Jager T, Altin D, Miljeteig C, Hansen BH (2016) Stage-dependent and sex-dependent sensitivity to water-soluble fractions of fresh and weathered oil in the marine copepod Calanus finmarchicus. Environ Toxicol Chem 35:728–735
Jensen MH, Nielsen TG, Dahlloef I (2008) Effects of pyrene on grazing and reproduction of Calanus finmarchicus and Calanus glacialis from Disko Bay, West Greenland. Aquat Toxicol 87:99–107
Jiang ZB, Huang YJ, Chen QZ, Zeng JN, Xu XQ (2012) Acute toxicity of crude oil water accommodated fraction on marine copepods: the relative importance of acclimatization temperature and body size. Mar Environ Res 81:12–17
Karlson K, Bamstedt U (1994) Planktivorous predation on copepods. Evaluation of mandible remains in predator guts as a quantitative estimate of predation. Mar Ecol Prog Ser 108:79–89
Kiørboe T (2006) Sex, sex-ratios, and the dynamics of pelagic copepod populations. Oecologia 148:40–50
Kiørboe T (2007) Mate finding, mating, and population dynamics in a planktonic copepod Oithona davisae: There are too few males. Limnol Oceanogr 52:1511–1522
Krause KE, Dinh KV, Nielsen TG (2017) Increased tolerance to oil exposure by the cosmopolitan marine copepod Acartia tonsa. Sci Total Environ 607–608:87–94
Medina M, Barata C, Telfer R, Baird DJ (2002) Age- and sex-related variation in sensitivity to the pyrethroid cypermethrin in the marine copepod Acartia tonsa Dana. Arch Environ Contam Toxicol 42:17–22
Michels J, Schnack-Schiel SB (2005) Feeding in dominant Antarctic copepods - does the morphology of the mandibular gnathobases relate to diet? Mar Biol 146:483–495
Miesner AK, Lundholm N, Krock B, Nielsen TG (2016) The effect of Pseudo-nitzschia seriata on grazing and fecundity of Calanus finmarchicus and Calanus glacialis. J Plankton Res 38:564–574
Norwegian Oil and Gas (2013): Environmental Report 2013. In: The Norwegian Oil and Gas Association (Hrsg.), Oslo
Norwegian Oil and Gas (2016): Environmental Report 2016. In: The Norwegian Oil and Gass Association (Hrsg.), Oslo
Noyes PD, McElwee MK, Miller HD, Clark BW, Van Tiem LA, Walcott KC, Erwin KN, Levin ED (2009) The toxicology of climate change: environmental contaminants in a warming world. Environ Int 35:971–986
Ottersen G (2010) A digital temperature atlas for the Norwegian Sea. ICES J Mar Sci 67:1525–1537
Pelletier MC, Burgess RM, Ho KT, Kuhn A, McKinney RA, Ryba SA (1997) Phototoxicity of individual polycyclic aromatic hydrocarbons and petroleum to marine invertebrate larvae and juveniles. Environ Toxicol Chem 16:2190–2199
Raymont JEG, Gross F (1942) On the feeding and breeding of Calanus finmarchicus under laboratory conditions. Proc R Soc Edinb B Biol 61:267–287
Reddy CM, Quinn JG (2001) The North Cape oil spill: hydrocarbons in Rhode Island coastal waters and Point Judith Pond. Mar Environ Res 52:445–461
Reddy CM, Arey JS, Seewald JS, Sylva SP, Lemkau KL, Nelson RK, Carmichael CA, McIntyre CP, Fenwick J, Ventura GT, Van Mooy BAS, Camilli R (2012) Composition and fate of gas and oil released to the water column during the Deepwater Horizon oil spill. Proc Natl Acad Sci U S A 109:20229–20234
Roemmich D, McGowan J (1995) Climatic warminng and the decline of zooplankton in the California current. Science 267:1324–1326
Saiz E, Griffell K, Calbet A, Isari S (2014) Feeding rates and prey: predator size ratios of the nauplii and adult females of the marine cyclopoid copepod Oithona davisae. Limnol Oceanogr 59:2077–2088
Skogen MD, Hjøllo SS, Sandø AB, Tjiputra J, Morgane T-T (2018) Future ecosystem changes in the Northeast Atlantic: a comparison between a global and a regional model system. ICES J Mar Sci 75(7):2355–2369 fsy088-fsy088
Swalethorp R, Kjellerup S, Duenweber M, Nielsen TG, Moller EF, Rysgaard S, Hansen BW (2011) Grazing, egg production, and biochemical evidence of differences in the life strategies of Calanus finmarchicus, C. glacialis and C. hyperboreus in Disko Bay, western Greenland. Mar Ecol Prog Ser 429:125–144
Toxværd K, Dinh KV, Henriksen O, Hjorth M, Nielsen T (2018) Impact of pyrene exposure during overwintering of the Arctic copepod Calanus glacialis. Environ Sci Technol 52:10328–10336
Wernberg T, Smale DA, Tuya F, Thomsen MS, Langlois TJ, de Bettignies T, Bennett S, Rousseaux CS (2013) An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nat Clim Chang 3:78–82
Acknowledgments
We thank two anonymous reviewers for their constructive comments that improved the manuscript. We thank the assistance from Anders J. Olsen and Iurgi Imanol Salaverria-Zabalegui at NTNU Sealab, Norwegian University of Science and Technology. We also thank Minh T.T. Vu for the comments on the manuscript.
Funding
This study was financially funded by a H.C. Ørsted fellowship to Khuong Van Dinh and by the Norwegian Research Council project no. 243923/E40 to Torkel Gissel Nielsen.
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Van Dinh, K., Olsen, M.W., Altin, D. et al. Impact of temperature and pyrene exposure on the functional response of males and females of the copepod Calanus finmarchicus. Environ Sci Pollut Res 26, 29327–29333 (2019). https://doi.org/10.1007/s11356-019-06078-x
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DOI: https://doi.org/10.1007/s11356-019-06078-x