Abstract
Marine copepods provide the major food-web link between primary producers and higher trophic levels, and their feeding ecology is of acute interest in light of global change impacts on food-web functioning. Recently, quantitative polymerase chain reaction (qPCR) protocols have been developed, which can complement classic diet quantification methods, such as stable isotope or fatty acid analyses tools. Here, we present first results of feeding experiments assessing sex- and stage-specific food intake by the ubiquitous calanoid copepod Acartia tonsa by 18S targeted qPCR and microscopic grazing assessment. In triplicated mixed-diet feeding treatments, three suitable A. tonsa diets, the cryptophyte Rhodomonas balthica, the haptophyte Isochrysis galbana, and the diatom Thalassiosira weissflogii, were offered in equal biomass proportions under constant conditions. Prey uptake substantially varied between different algal species, as did the extent of sex- and stage-specificity of prey uptake. Male adult copepods had higher R. balthica gut contents than females, and nauplii contained more of this prey source than copepodites or adult copepods in mixed treatments. A trend towards higher amounts of ingested T. weissflogii in adult females than in males and in nauplii than in other stages was detected. Genetic gut content quantifications indicated low feeding on I. galbana, and no consistent sex- or stage-specific differences of I. galbana content in A. tonsa. Our results highlight diet-specific feeding differences between Acartia life stages and sexes, which can have implications on food-web dynamics and specific nutrient transfer to higher trophic levels in copepod populations of varying age composition under changing environmental parameters, such as rising temperatures and increasing ocean acidification.
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References
Barofsky A, Simonelli P, Vidoudez C, Troedsson C, Nejstgaard JC, Jakobsen HH, Pohnert G (2010) Growth phase of the diatom Skeletonema marinoi influences the metabolic profile of the cells and the selective feeding of the copepod Calanus spp. J Plankton Res 32(3):262–273
Behrends G (1996) Long-term investigation of seasonal mesozooplankton dynamics in Kiel Bight, Germany. In: Proc. 13th Baltic Marine biology symposium, Jurmala, Latvia. Inst. Aquatic Ecology, University of Latvia, Riga, Latvia, pp 93–98
Blankenship LE, Yayanos AA (2005) Universal primers and PCR of gut contents to study marine invertebrate diets. Mol Ecol 14:891–899
Boersma M, Wesche A, Hirche HJ (2014) Predation of calanoid copepods on their own and other copepods’ offspring. Mar Biol 161:733–743
Broglio E, Jónasdóttir SH, Calbet A, Jakobsen HH, Saiz E (2003) Effect of heterotrophic food on feeding and reproduction of the calanoid copepod Acartia tonsa: relationship with prey fatty acid composition. Aquat Microb Ecol 31:267–278
Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE Guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55(4):611–622
Cervetto G, Pagano M, Gaudy R (1995) Feeding behavior and migrations in a natural population of the copepod Acartia tonsa. Hydrobiologia 300:237–248
Conroy BJ, Steinberg DK, Song B, Kalmbach A, Carpenter EJ, Foster RA (2017) Mesozooplankton graze on cyanobacteria in the Amazon River Plume and Western Tropical North Atlantic. Front Microbiol. https://doi.org/10.3389/fmicb.2017.01436
Cushing DH (1990) Plankton production and year-class strength in fish populations: an update of the match/mismatch hypothesis. Adv Mar Biol 26:249–293
Dassow P, Petersen TW, Chepumov VA, Armbrust EV (2008) Inter- and intraspecific relationships between nuclear DNA content and cell size in selected members of the centric diatom genus Thalassiosira (Bacillariophyceae). J Phycol 44:335–349
Durbin EG, Casas MC, Rynearson TA (2012) Copepod feeding and digestion rates using prey DNA and qPCR. J Plankton Res 34(1):72–82
Edwards M, Richardson AJ (2004) Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 430:881–884
Eiane K, Ohman MD (2004) Stage-specific mortality of Calanus finmarchicus, Pseudocalanus elongatus and Oithona similis on Fladen Ground, North Sea, during a spring bloom. Mar Ecol Progr Ser 268:183–193
Frost BW (1972) Effects of size and concentrations of food particles on the feeding behavior of the marine planktonic copepod Calanus pacificus. Limnol Oceanogr 14:805–815
Garzke J, Ismar SMH, Sommer U (2015) Climate change affects low trophic level marine consumers: warming decreases copepod size and abundance. Oecologia 177:849–860
Garzke J, Hansen T, Ismar SMH, Sommer U (2016) Combined effects of ocean warming and acidification on copepod abundance, body size and fatty acid content. PLoS ONE 11:e0155952
Garzke J, Sommer U, Ismar SMH (2017) Is the chemical composition of biomass the agent by which ocean acidification impacts on zooplankton ecology? Aquat Sci 79:233–249
Giesecke R, Vallejos T, Sanchez M, Teiguiel K (2017) Plankton dynamics and zooplankton carcasses in a mid-latitude estuary and their contributions to the local particulate organic carbon pool. Cont Shelf Res 132:58–68
Hansen FC, Möllmann C, Schütz U, Neumann T (2006) Spatio-temporal distribution and production of calanoid copepods in the central Baltic Sea. J Plankton Res 28(1):39–54
Harper GL, King RA, Dodd CS, Harwood JD, Glen DM, Bruford MW, Symondson WOC (2005) Rapid screening of invertebrate predators for multiple prey DNA targets. Mol Ecol 14:819–827
Helenius LK, Saiz E (2017) Feeding behavior of the marine calanoid copepod Paracartia grani Sars: functional response, prey size spectrum, and effects of the presence of alternative prey. PLoS ONE 12(3):e0172902
Hillebrand H, Dürselen C-D, Kirschtel D, Pollingher U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424
Hu S, Gao Z, Xu C, Huang H, Liu S, Lin S (2015) Molecular analysis on in situ diets of coral reef copepods: evidence of terrestrial plant detritus as a food source in Anya Bay, China. J Plankton Res 37(2):363–371
IPCC (2014) Climate Change 2014: mitigation of climate change. Contribution of Working Group III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, New York
Isari S, Antό M, Saiz E (2013) Copepod foraging on the basis of food nutritional quality: can copepods really choose? PLoS ONE 8:e84742
Ismar SMH, Hansen T, Sommer U (2008) Effect of food concentration and type of diet on Acartia survival and naupliar development. Mar Biol 154:335–343
Jager T, Slaberria I, Altin D, Nordtug T, Hansen BH (2017) Modelling the dynamics of growth, development and lipid storage in the marine copepod Calanus finmarchicus. Mar Biol 164(1):1
Jonsson PR, Tiselius P (1990) Feeding behaviour, prey detection and capture efficiency of the copepod Acartia tonsa feeding on planktonic ciliates. Mar Ecol Progr Ser 60:35–44
Jungbluth MJ, Goetze E, Lenz PH (2013) Measuring copepod naupliar abundance in a subtropical bay using quantitative PCR. Mar Biol 160:3125–3141
Jungbluth MJ, Selph KE, Lenz PH, Goetze E (2017) Species-specific and significant trophic impacts by two species of copepod nauplii, Parvocalanus crassirostris and Bestiolina similis. Mar Ecol Prog Ser 572:57–76
Kawabata K (1991) Ontogenetic changes in copepod behavior—an ambush cyclopoid predator and a calanoid prey. J Plankton Res 13(1):27–34
Kiørboe T (1998) Population regulation and role of mesozooplankton in shaping marine pelagic food webs. In: Tamminen T, Kuosa H (eds) Eutrophication in planktonic ecosystems: food web dynamics and elemental cycling. Springer, Netherlands, pp 13–27
Kiørboe T (2008) Optimal swimming strategies in mate searching pelagic copepods. Oecologia 155:179–192
Kiørboe T (2011) What makes pelagic copepods so successful? J Plankton Res 33:677–685
Kiørboe T, Bagøien E (2005) Motility patterns and mate encounter rates in planktonic copepods. Limnol Oceanogr 50:1999–2007
Kiørboe T, Ceballos S, Thygesen UH (2015) Interrelations between senescence, life-history traits, and behavior in planktonic copepods. Ecology 96(8):2225–2235
Knuckey RM, Semmens GL, Mayer RJ, Rimmer MA (2005) Development of an optimal microalgal diet for the culture of the calanoid copepod Acartia sinjiensis: effect of algal species and feed concentration on copepod development. Aquaculture 249:339–351
Lewandowska AM, Boyce DG, Hofmann M, Matthiessen B, Sommer U, Worm B (2014) Effects of sea surface warming on marine plankton. Ecol Lett 17(5):614–623
Lund JWG, Kipling C, LeCren ED (1958) The inverted microscope method of estimating algal numbers and the statistical basis of estimations by counting. Hydrobiologia 11:143–170
Mauchline J (1998) The biology of calanoid copepods. In: Blaxter JHS, Southward AJ, Tyler PA (eds) Advances in marine biology 33. Academic Press, New York, pp 1–710
Menden-Deuer S, Lessard EJ (2000) Carbon to volume relationships for dinoflagellates, diatoms, and of the protist plankton. Limnol Oceanogr 45:559–579
Meunier CL, Boersma M, Wiltshire K, Malzahn AM (2016) Zooplankton eat what they need: copepod selective feeding and potential consequences for marine systems. Oikos 125:50–58
Milione M, Zeng C (2007) The effects of algal diets on population growth and egg hatching success of the tropical calanoid copepod, Acartia sinjiensis. Aquaculture 273(4):656–664
Möllmann C, Kornilovs G, Fetter M, Köster FW (2005) Climate, zooplankton, and pelagic fish growth in the central Baltic Sea. ICES J Mar Sci 62:1270–1280
Moorthi SD, Countway PD, Stauffer BA, Caron DA (2006) Use of quantitative real-time PCR to investigate the dynamics of the red tide dinoflagellate Lingulodinium polyedrum. Micr Ecol 52:135–150
Nejstgaard JC, Frischer ME, Raule CL, Gruebel R, Kohlberg KE, Verity PG (2003) Molecular detection of algal prey in copepod guts and fecal pellets. Limnol Oceanogr Methods 1:29–38
Nejstgaard JC, Frischer ME, Simonelli P, Troedsson C, Brakel M, Adiyaman F, Sazhin AF, Artigas LF (2008) Quantitative PCR to estimate copepod feeding. Mar Biol 153:565–577
Pan YJ, Souissi A, Souissi S, Hwang JS (2016) Effects of salinity on the reproductive performance of Apocyclops royi (Copepoda, Cyclopoida). J Exp Mar Biol Ecol 475:108–113
Rayner TA, Jørgensen NO, Drillet G, Hansen BW (2017) Changes in free amino acid content during naupliar development of the Calanoid copepod Acartia tonsa. Comp Biochem Physiol A 210:1–6
Saiz E, Calbet A (2011) Copepod feeding in the ocean: scaling patterns, composition of their diet and the bias of estimates due to microzooplankton grazing during incubations. Hydrobiologia 666:181–196
Saiz E, Calbet A, Stamatina I (2014) Feeding rates and prey: predator size ratios of the nauplii and adult females of the marine cyclopoid Oithona davisae. Limnol Oceanogr 59(6):2077–2088
Shayegan M, Esmaeili FA, Agh N, Jani KK (2016) Effects of salinity on egg and fecal pellet production, development and survival, adult sex ratio and life span in the calanoid copepod Acartia tonsa: a laboratory study. Chin J Oceanol Limnol 34:709–718
Sheppard SK, Harwood JD (2005) Advances in molecular ecology: tracking trophic links through predator-prey food-webs. Funct Ecol 19:751–762
Simonelli P, Troedsson C, Nejstgaard JC, Zech K, Larsen JB, Frischer ME (2009) Evaluation of DNA extraction and handling procedures for PCR-based copepod feeding studies. J Plankton Res 31:1465–1474
Smith KF, Biessy L, Argyle PA, Trnski T, Halafihi T, Rhodes LL (2017) Molecular identification of Gambierdiscus and Fukuyoa (Dinophyceae) from environmental samples. Marine Drugs 15:243
Sommer U (2009) Copepod growth and diatoms: insensitivity of Acartia tonsa to the composition of semi-natural plankton mixtures manipulated by Si:N ratios in mesocosms. Oecologia 159:207–215
Sommer U, Lewandowska A (2011) Climate change and the phytoplankton spring bloom: warming and overwintering zooplankton have similar effects on phytoplankton. Glob Change Biol 17:154–162
Sommer U, Stibor H, Katechakis A, Sommer F, Hansen T (2002) Pelagic food web configuration at different levels of nutrient richness and their implications for the ratio fish production: primary production. Hydrobiologia 484:110–120
Sommer F, Saage A, Santer B, Hansen T, Sommer U (2005) Linking foraging strategies of marine calanoid copepods to patterns of nitrogen stable isotope signatures in a mesocosm study. Mar Ecol Prog Ser 286:99–106
Støttrup JG, Jensen J (1990) Influence of algal diet on feeding and egg-production of the calanoid copepod Arcatia tonsa Dana. J Exp Mar Biol Ecol 141:87–105
Støttrup JG, Richardson K, Kirkegaard E, Pihl NG (1986) The cultivation pf Acartia tonsa Dana for use as live food for marine fish larvae. Aquaculture 52(2):87–96
Troedsson C, Frischer ME, Nejstgaard JC, Thompson EM (2007) Molecular quantification of differential ingestion and particle trapping rates by the appendicularian Oikopleura dioica as a function of prey size and shape. Limnol Oceanogr 52:416–427
Troedsson C, Simonelli P, Nägele V, Nejstgaard JC, Frischer ME (2009) Quantification of copepod gut content by differential length amplification quantitative PCR (dla-qPCR). Mar Biol 156:253–259
Utermöhl (1958) Zur Vervollkommnung der quantitativen Phytoplankton Methodik. Mitt Int Ver Theor Angew Limnol 9:263–272
Van Duren LA, Videler JJ (1996) The trade-off between feeding, mate seeking and predator avoidance in copepods: Behavioural responses to chemical cues. J Plankton Res 18(5):805–818
Zervoudaki S, Krasakopoulou E, Moutsopoulos T, Protopapa M, Marro S, Gazeau F (2017) Copepod response to ocean acidification in a low nutrient-low chlorophyll environment in the NW Mediterranean Sea. Est Coast Shelf Sci 186:152–162
Acknowledgements
We thank K. Beining for helpful technical advice on real-time PCR, R. Nakad for advice on primer design, D. Riemann for Utermöhl counts of prey cell abundances, and two anonymous referees for helpful revision of our manuscript.
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Ismar, S.M.H., Kottmann, J.S. & Sommer, U. First genetic quantification of sex- and stage-specific feeding in the ubiquitous copepod Acartia tonsa. Mar Biol 165, 25 (2018). https://doi.org/10.1007/s00227-017-3281-z
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DOI: https://doi.org/10.1007/s00227-017-3281-z