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Marine Biology

, Volume 160, Issue 12, pp 3125–3141 | Cite as

Measuring copepod naupliar abundance in a subtropical bay using quantitative PCR

  • Michelle J. Jungbluth
  • Erica Goetze
  • Petra H. Lenz
Original Paper

Abstract

Copepod nauplii are important in plankton food web dynamics, but limited information is available about their ecology due to methodological challenges. Reported here is a new molecular method that was developed, optimized, and tested in laboratory and field samples that uses quantitative PCR (qPCR) to identify and estimate the abundance of nauplii of the planktonic copepod, Parvocalanus crassirostris. The overall approach included collection of bulk zooplankton samples in the field, size fractionation to create artificial cohorts of relatively few developmental stages, obtaining DNA copy number for each size fraction by qPCR amplification of a target gene region, and estimation of the number of animals in each fraction through application of known DNA copy number across developmental stage. Method validation studies found that our qPCR-based approach has comparable accuracy to microscope-based counts of early developmental stages. Naupliar abundance estimates obtained using the two methods on cultured populations were similar; the regression of qPCR estimates on microscope-based counts resulted in a nearly 1:1 ratio (slope = 1.09). The qPCR-based method is superior to traditional identification and quantification methods for nauplii due to its higher taxonomic resolution, sensitive detection over a range of DNA quantities, and relatively high throughput sample processing.

Keywords

Size Fraction qPCR Method Microscope Count Naupliar Stage Direct Microscope Count 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank two anonymous reviewers for their thoughtful comments on the manuscript.  We thank K. Groom and numerous student volunteers who helped with field sampling, A. Orcine for assistance with molecular work, and S. Brown and A. Millan for equipment loans and help in the laboratory. This work was supported by a grant/cooperative agreement from the National Oceanic and Atmospheric Administration, Project R/HE-3, which is sponsored by the University of Hawaii Sea Grant College Program, SOEST, under Institutional Grant No. NA09OAR4170060 from NOAA Office of Sea Grant, Department of Commerce. The views expressed herein are those of the author(s) and do not necessarily reflect the views of NOAA or any of its subagencies. UNIHI-SEAGRANT-JC-11-20.

References

  1. Beaugrand G, Brander KM, Lindley JA, Souissi S, Reid PC (2003) Plankton effect on cod recruitment in the North Sea. Nature 426:661–664. doi: 10.1038/nature02164 CrossRefGoogle Scholar
  2. Beman JM, Popp BN, Alford SE (2012) Quantification of ammonia oxidation rates and ammonia-oxidizing archaea and bacteria at high resolution in the Gulf of California and eastern tropical North Pacific Ocean. Limnol Oceanogr 57:711–726. doi: 10.4319/lo.2012.57.3.0711 CrossRefGoogle Scholar
  3. Björnberg TKS (1966) The developmental stages of Undinula vulgaris (Dana) (Copepoda). Crustaceana 11:65–76CrossRefGoogle Scholar
  4. Björnberg TKS (1967) The larvae and young forms of Eucalanus dana (Copepoda) from tropical Atlantic waters. Crustaceana 12:59–73CrossRefGoogle Scholar
  5. Björnberg TKS (2001) The naupliar stages of Cyclopina yutimaete Lotufo (Cyclopinidae, Cyclopoida). Hydrobiologia 453:497–501. doi: 10.1023/a:1013118910352 CrossRefGoogle Scholar
  6. Borg CMA, Bruno E, Kiørboe T (2012) The kinematics of swimming and relocation jumps in copepod nauplii. PLoS ONE 7. doi: 10.1371/journal.pone.0047486
  7. Bott NJ, Ophel-Keller KM, Sierp MT, Herdina, Rowling KP, McKay AC, Loo MGK, Tanner JE, Deveney MR (2010) Toward routine, DNA-based detection methods for marine pests. Biotechnol Adv 28: 706–714. doi  10.1016/j.biotechadv.2010.05.018
  8. Böttjer D, Morales CE, Bathmann U (2010) Trophic role of small cyclopoid copepod nauplii in the microbial food web: a case study in the coastal upwelling system off central Chile. Mar Biol 157:689–705. doi: 10.1007/s00227-009-1353-4 CrossRefGoogle Scholar
  9. Bradley CJ, Strickler JR, Buskey EJ, Lenz PH (2013) Swimming and escape behavior in two species of calanoid copepods from nauplius to adult. J Plankton Res 35:49–65. doi: 10.1093/plankt/fbs088 CrossRefGoogle Scholar
  10. Bruno E, Borg CMA, Kiørboe T (2012) Prey detection and prey capture in copepod nauplii. PLoS ONE 7. doi: 10.1371/journal.pone.0047906
  11. Bucklin A (2000) Methods for population genetic analysis of zooplankton. In: Harris R, Wiebe P, Lenz J, Skjoldal HR, Huntley M (eds) ICES zooplankton methodology manual. Academic Press, London, pp 533–570CrossRefGoogle Scholar
  12. Bucklin A, Bentley AM, Franzen SP (1998) Distribution and relative abundance of Pseudocalanus moultoni and P. newmani (Copepoda : Calanoida) on Georges Bank using molecular identification of sibling species. Mar Biol 132:97–106. doi: 10.1007/s002270050375 CrossRefGoogle Scholar
  13. Bucklin A, Guarnieri M, Hill RS, Bentley AM, Kaartvedt S (1999) Taxonomic and systematic assessment of planktonic copepods using mitochondrial COI sequence variation and competitive, species-specific PCR. Hydrobiologia 401:239–254. doi: 10.1023/a:1003790411424 CrossRefGoogle Scholar
  14. Bucklin A, Frost BW, Bradford-Grieve J, Allen LD, Copley NJ (2003) Molecular systematic and phylogenetic assessment of 34 calanoid copepod species of the Calanidae and Clausocalanidae. Mar Biol 142:333–343. doi: 10.1007/s00227-002-0943-1 Google Scholar
  15. Bucklin A, Hopcroft RR, Kosobokova KN, Nigro LM, Ortman BD, Jennings RM, Sweetman CJ (2010a) DNA barcoding of Arctic Ocean holozooplankton for species identification and recognition. Deep Sea Res II 57:40–48. doi: 10.1016/j.dsr2.2009.08.005 CrossRefGoogle Scholar
  16. Bucklin A, Ortman BD, Jennings RM, Nigro LM, Sweetman CJ, Copley NJ, Sutton T, Wiebe PH (2010b) A “Rosetta Stone” for metazoan zooplankton: DNA barcode analysis of species diversity of the Sargasso Sea (Northwest Atlantic Ocean). Deep Sea Res II 57:2234–2247. doi: 10.1016/j.dsr2.2010.09.025 CrossRefGoogle Scholar
  17. Burdick DS, Hartline DK, Lenz PH (2007) Escape strategies in co-occurring calanoid copepods. Limnol Oceanogr 52:2373–2385CrossRefGoogle Scholar
  18. 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 55:611–622. doi: 10.1373/clinchem.2008.112797 CrossRefGoogle Scholar
  19. Calbet A, Landry MR (2004) Phytoplankton growth, microzooplankton grazing, and carbon cycling in marine systems. Limnol Oceanogr 49:51–57. doi: 10.1093/plankt/23.3.319 CrossRefGoogle Scholar
  20. Calbet A, Landry MR, Scheinberg RD (2000) Copepod grazing in a subtropical bay: species-specific responses to a midsummer increase in nanoplankton standing stock. Mar Ecol Prog Ser 193:75–84. doi: 10.3354/meps193075 CrossRefGoogle Scholar
  21. Calbet A, Garrido S, Saiz E, Alcaraz M, Duarte CM (2001) Annual zooplankton succession in coastal NW Mediterranean waters: the importance of the smaller size fractions. J Plankton Res 23:319–331. doi: 10.1093/plankt/23.3.319 CrossRefGoogle Scholar
  22. Campbell RG, Wagner MM, Teegarden GJ, Boudreau CA, Durbin EG (2001) Growth and development rates of the copepod Calanus finmarchicus reared in the laboratory. Mar Ecol Prog Ser 221:161–183. doi: 10.3354/meps221161 CrossRefGoogle Scholar
  23. Castellani C, Irigoien X, Mayor DJ, Harris RP, Wilson D (2008) Feeding of Calanus finmarchicus and Oithona similis on the microplankton assemblage in the Irminger Sea, North Atlantic. J Plankton Res 30:1095–1116. doi: 10.1093/plankt/fbn074 CrossRefGoogle Scholar
  24. Church MJ, Jenkins BD, Karl DM, Zehr JP (2005) Vertical distributions of nitrogen-fixing phylotypes at Stn ALOHA in the oligotrophic North Pacific Ocean. Aquat Microb Ecol 38:3–14. doi: 10.3354/ame038003 CrossRefGoogle Scholar
  25. Cleary AC, Durbin EG, Rynearson TA (2012) Krill feeding on sediment in the Gulf of Maine (North Atlantic). Mar Ecol Prog Ser 455:157–172. doi: 10.3354/meps09632 CrossRefGoogle Scholar
  26. Costa FO, deWaard JR, Boutillier J, Ratnasingham S, Dooh RT, Hajibabaei M, Hebert PDN (2007) Biological identifications through DNA barcodes: the case of the Crustacea. Can J Fish Aquat Sci 64:272–295. doi: 10.1139/f07-008 CrossRefGoogle Scholar
  27. Cox EF, Ribes M, Kinzie III RA (2006) Temporal and spatial scaling of planktonic responses to nutrient inputs into a subtropical embayment. Mar Ecol Prog Ser 324:19–35. doi: 10.3354/meps324019 CrossRefGoogle Scholar
  28. Darling JA, Blum MJ (2007) DNA-based methods for monitoring invasive species: a review and prospectus. Biol Invasions 9:751–765. doi: 10.1007/s10530-006-9079-4 CrossRefGoogle Scholar
  29. Demeke T, Jenkins GR (2010) Influence of DNA extraction methods, PCR inhibitors and quantification methods on real-time PCR assay of biotechnology-derived traits. Anal Bioanal Chem 396:1977–1990. doi: 10.1007/s00216-009-3150-9 CrossRefGoogle Scholar
  30. Dias PJ, Sollelis L, Cook EJ, Piertney SB, Davies IM, Snow M (2008) Development of a real-time PCR assay for detection of Mytilus species specific alleles: application to a sampling survey in Scotland. J Exp Mar Biol Ecol 367:253–258. doi: 10.1016/j.jembe.2008.10.011 CrossRefGoogle Scholar
  31. Durbin EG, Durbin AG (1978) Length and weight relationships of Acartia clausi from Narragansett Bay, Rhode Island. Limnol Oceanogr 23:958–969CrossRefGoogle Scholar
  32. Durbin AG, Durbin EG (1981) Standing stock and estimated production rates of phytoplankton and zooplankton in Narragansett Bay, Rhode Island. Estuaries 4:24–41CrossRefGoogle Scholar
  33. Durbin EG, Casas MC, Rynearson TA, Smith DC (2008) Measurement of copepod predation on nauplii using qPCR of the cytochrome oxidase I gene. Mar Biol 153:699–707. doi: 10.1007/s00227-007-0843-5 CrossRefGoogle Scholar
  34. Durbin EG, Casas MC, Rynearson TA (2012) Copepod feeding and digestion rates using prey DNA and qPCR. J Plankton Res 34:72–82. doi: 10.1093/plankt/fbr082 CrossRefGoogle Scholar
  35. Eiane K, Aksnes DL, Ohman MD, Wood S, Martinussen MB (2002) Stage-specific mortality of Calanus spp. under different predation regimes. Limnol Oceanogr 47:636–645CrossRefGoogle Scholar
  36. Fukatsu T (1999) Acetone preservation: a practical technique for molecular analysis. Mol Ecol 8:1935–1945. doi: 10.1046/j.1365-294x.1999.00795.x CrossRefGoogle Scholar
  37. Gallienne CP, Robins DB (2001) Is Oithona the most important copepod in the world’s oceans? J Plankton Res 23:1421–1432. doi: 10.1093/plankt/23.12.1421 CrossRefGoogle Scholar
  38. Goetze E (2005) Global population genetic structure and biogeography of the oceanic copepods Eucalanus hyalinus and E. spinifer. Evolution 59:2378–2398. doi: 10.1554/05-077.1 Google Scholar
  39. Grabbert S, Renz J, Hirche HJ, Bucklin A (2010) Species-specific PCR discrimination of species of the calanoid copepod Pseudocalanus, P. acuspesand P. elongatus, in the Baltic and North Seas. Hydrobiologia 652:289–297. doi: 10.1007/s10750-010-0360-2 CrossRefGoogle Scholar
  40. Hirst AG, Bunker AJ (2003) Growth of marine planktonic copepods: global rates and patterns in relation to chlorophyll a, temperature, and body weight. Limnol Oceanogr 48:1988–2010. doi: 10.2307/3597565 CrossRefGoogle Scholar
  41. Holmborn T, Goetze E, Põllupüü M, Põllumäe A (2011) Genetic species identification and low genetic diversity in Pseudocalanus acuspes of the Baltic Sea. J Plankton Res 33:507–515. doi: 10.1093/plankt/fbq113 CrossRefGoogle Scholar
  42. Holzmann M, Pawlowski J (1996) Preservation of foraminifera for DNA extraction and PCR amplification. J Foraminiferal Res 26:264–267CrossRefGoogle Scholar
  43. Hoover RS, Hoover D, Miller M, Landry MR, De Carlo EH, Mackenzie FT (2006) Zooplankton response to storm runoff in a tropical estuary: bottom-up and top-down controls. Mar Ecol Prog Ser 318:187–201. doi: 10.3354/meps318187 CrossRefGoogle Scholar
  44. Hopcroft RR, Roff JC, Lombard D (1998) Production of tropical copepods in Kingston Harbour, Jamaica: the importance of small species. Mar Biol 130:593–604. doi: 10.1007/s002270050281 CrossRefGoogle Scholar
  45. Huntley ME, Lopez MDG (1992) Temperature-dependent production of marine copepods: a global synthesis. Am Nat 140:201–242. doi: 10.1086/285410 CrossRefGoogle Scholar
  46. Jungbluth MJ (2012) Development and demonstration of a quantitative PCR based method to enumerate copepod nauplii in field samples. MS thesis, University of Hawaii, ManoaGoogle Scholar
  47. Jungbluth MJ, Lenz PH (2013) Copepod diversity in a subtropical bay based on a fragment of the mitochondrial COI gene. J Plankton Res 35:630–643. doi: 10.1093/plankt/fbt015 CrossRefGoogle Scholar
  48. Karlen Y, McNair A, Perseguers S, Mazza C, Mermod N (2007) Statistical significance of quantitative PCR. BMC Bioinf 8:131. doi  10.1186/1471-2105-8-131
  49. Kiesling TL, Wilkinson E, Rabalais J, Ortner PB, McCabe MM, Fell JW (2002) Rapid identification of adult and naupliar stages of copepods using DNA hybridization methodology. Mar Biotechnol 4:30–39. doi: 10.1007/s10126-001-0077-3 Google Scholar
  50. Kreader CA (1996) Relief of amplification inhibition in PCR with bovine serum albumin or T4 gene 32 protein. Appl Environ Microbiol 62:1102–1106Google Scholar
  51. Landry MR (1978) Population dynamics and production of a planktonic marine copepod, Acartia clausi, in a small temperate lagoon on San Juan Island, Washington. Int Rev Gesamten Hydrobiol Hydrogr 63:77–119. doi: 10.1002/iroh.19780630106 CrossRefGoogle Scholar
  52. Landry MR, Hassett RP (1982) Estimating the grazing impact of marine micro-zooplankton. Mar Biol 67:283–288. doi: 10.1007/BF00397668 CrossRefGoogle Scholar
  53. Lawson TJ, Grice GD (1973) The developmental stages of Paracalanus crassirostris Dahl, 1894 (Copepoda, Calanoida). Crustaceana 24:43–56CrossRefGoogle Scholar
  54. Lee CE, Frost BW (2002) Morphological stasis in the Eurytemora affinis species complex (Copepoda: Temoridae). Hydrobiologia 480:111–128. doi: 10.1023/A:1021293203512 CrossRefGoogle Scholar
  55. Lindeque PK, Harris RP, Jones MB, Smerdon GR (2004) Distribution of Calanus spp. as determined using a genetic identification system. Sci Mar (Barcelona) 68:121–128Google Scholar
  56. Lučić D, Njire J, Morović M, Precali R, Fuks D, Bolotin J (2003) Microzooplankton in the open waters of the northern Adriatic Sea from 1990 to 1993: the importance of copepod nauplii densities. Helgol Mar Res 57:73–81Google Scholar
  57. Machida RJ, Miya MU, Nishida M, Nishida S (2004) Large-scale gene rearrangements in the mitochondrial genomes of two calanoid copepods Eucalanus bungii and Neocalanus cristatus (Crustacea), with notes on new versatile primers for the srRNA and COI genes. Gene 332:71–78. doi: 10.1016/j.gene.2004.01.019 CrossRefGoogle Scholar
  58. Mackie JA, Geller J (2010) Experimental parameters affecting quantitative PCR of Artemia franciscana: a model for a marine zooplanktonic target in natural plankton samples. Limnol Oceanogr Methods 8:337–347. doi: 10.4319/lom.2010.8.337 CrossRefGoogle Scholar
  59. Mandrioli M, Borsatti F, Mola L (2006) Factors affecting DNA preservation from museum-collected lepidopteran specimens. Entomol Exp Appl 120:239–244. doi: 10.1111/j.1570-7458.2006.00451.x CrossRefGoogle Scholar
  60. McKinnon AD, Duggan S (2001) Summer egg production rates of paracalanid copepods in subtropical waters adjacent to Australia’s North West Cape. Hydrobiologia 453:121–132. doi: 10.1023/A:1013115900841 CrossRefGoogle Scholar
  61. McKinnon AD, Duggan S (2003) Summer copepod production in subtropical waters adjacent to Australia’s North West Cape. Mar Biol 143:897–907. doi: 10.1007/s00227-003-1153-1 CrossRefGoogle Scholar
  62. McKinnon AD, Duggan S, Nichols PD, Rimmer MA, Semmens G, Robino B (2003) The potential of tropical paracalanid copepods as live feeds in aquaculture. Aquaculture 223:89–106. doi: 10.1016/S0044-8486(03)00161-3 CrossRefGoogle Scholar
  63. McLaren IA, Marcogliese DJ (1983) Similar nucleus numbers among copepods. Can J Zool 61:721–724CrossRefGoogle Scholar
  64. Möllmann C, Müller-Karulis B, Kornilovs G, St John MA (2008) Effects of climate and overfishing on zooplankton dynamics and ecosystem structure: regime shifts, trophic cascade, and feedback coops in a simple ecosystem. ICES J Mar Sci 65:302–310. doi: 10.1093/icesjms/fsm197 CrossRefGoogle Scholar
  65. Nagy ZT (2010) A hands-on overview of tissue preservation methods for molecular genetic analyses. Org Divers Evol 10:91–105. doi: 10.1007/s13127-010-0012-4 CrossRefGoogle Scholar
  66. Nejstgaard JC, Frischer ME, Simonelli P, Troedsson C, Brakel M, Adiyaman F, Sazhin AF, Artigas FL (2008) Quantitative PCR to estimate copepod feeding. Mar Biol 153:565–577. doi: 10.1007/s00227-007-0830-x CrossRefGoogle Scholar
  67. Ortman BD, Bucklin A, Pagès F, Youngbluth M (2010) DNA barcoding the medusozoa using mtCOI. Deep Sea Res II 57:2148–2156. doi: 10.1016/j.dsr2.2010.09.017 CrossRefGoogle Scholar
  68. Paffenhöfer GA, Lewis KD (1989) Feeding behavior of nauplii of the genus Eucalanus (Copepoda, Calanoida). Mar Ecol Prog Ser 57:129–136. doi: 10.3354/meps057129 CrossRefGoogle Scholar
  69. Paffenhöfer GA, Lewis KD (1990) Perceptive performance and feeding behavior of calanoid copepods. J Plankton Res 12:933–946. doi: 10.1093/plankt/12.5.933 CrossRefGoogle Scholar
  70. Paffenhöfer GA, Strickler JR, Lewis KD, Richman S (1996) Motion behavior of nauplii and early copepodid stages of marine planktonic copepods. J Plankton Res 18:1699–1715. doi: 10.1093/plankt/18.9.1699 CrossRefGoogle Scholar
  71. Pan M, McBeath AJA, Hay SJ, Pierce GJ, Cunningham CO (2008) Real-time PCR assay for detection and relative quantification of Liocarcinus depurator larvae from plankton samples. Mar Biol 153:859–870. doi: 10.1007/s00227-007-0858-y CrossRefGoogle Scholar
  72. Paradis V, Sirois P, Castonguay M, Plourde S (2012) Spatial variability in zooplankton and feeding of larval Atlantic mackerel (Scomber scombrus) in the southern Gulf of St. Lawrence. J Plankton Res 34:1064–1077. doi: 10.1093/plankt/fbs063 CrossRefGoogle Scholar
  73. Paul AJ, Coyle KO, Haldorson L (1991) Interannual variations in copepod nauplii prey of larval fish in an Alaskan Bay. ICES J Mar Sci 48:157–165CrossRefGoogle Scholar
  74. Quicke DLJ, Lopez-Vaamonde C, Belshaw R (1999) Preservation of hymenopteran specimens for subsequent molecular and morphological study. Zool Scr 28:261–267. doi: 10.1046/j.1463-6409.1999.00004.x CrossRefGoogle Scholar
  75. Razouls C, De Bovée F, Kouwenberg J, Desreumaux N (2005–2012) Diversity and geographic distribution of marine planktonic copepods. http://copepodes.obs-banyuls.fr/en. Accessed 1 Dec 2012
  76. Reiss RA, Schwert DP, Ashworth AC (1995) Field preservation of coleoptera for molecular-genetic analyses. Environ Entomol 24:716–719Google Scholar
  77. Roff JC, Turner JT, Webber MK, Hopcroft RR (1995) Bacterivory by tropical copepod nauplii: extent and possible significance. Aquat Microb Ecol 9:165–175CrossRefGoogle Scholar
  78. Safi KA, Brian Griffiths F, Hall JA (2007) Microzooplankton composition, biomass and grazing rates along the WOCE SR3 line between Tasmania and Antarctica. Deep Sea Res I 54:1025–1041. doi: 10.1016/j.dsr.2007.05.003 CrossRefGoogle Scholar
  79. Saikaly PE, Barlaz MA, de los Reyes III FL (2007) Development of quantitative real-time PCR assays for detection and quantification of surrogate biological warfare agents in building debris and leachate. Appl Environ Microbiol 73:6557–6565. doi: 10.1128/aem.00779-07 CrossRefGoogle Scholar
  80. Sampey A, McKinnon AD, Meekan MG, McCormick MI (2007) Glimpse into guts: overview of the feeding of larvae of tropical shorefishes. Mar Ecol Prog Ser 339:243–257. doi: 10.3354/meps339243 CrossRefGoogle Scholar
  81. Savin MC, Martin JL, LeGresley M, Giewat M, Rooney-Varga J (2004) Plankton diversity in the Bay of Fundy as measured by morphological and molecular methods. Microb Ecol 48:51–65. doi: 10.1007/s00248-003-1033-8 CrossRefGoogle Scholar
  82. Scheinberg RD (2004) Food web structure and trophic dynamics of a subtropical plankton community, with an emphasis on appendicularians. PhD Dissertation. University of Hawaii, ManoaGoogle Scholar
  83. 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. doi: 10.1093/plankt/fbp087 CrossRefGoogle Scholar
  84. Sullivan BK, Meise CJ (1996) Invertebrate predators of zooplankton on Georges Bank, 1977–1987. Deep Sea Res II 43:1503–1519. doi: 10.1016/s0967-0645(96)00043-4 CrossRefGoogle Scholar
  85. Sullivan BK, Costello JH, Van Keuren D (2007) Seasonality of the copepods Acartia hudsonica and Acartia tonsa in Narragansett Bay, RI, USA during a period of climate change. Estuar Coast Shelf S 73:259–267. doi: 10.1016/j.ecss.2007.01.018 CrossRefGoogle Scholar
  86. Takahashi T, Uchiyama I (2007) Morphology of the naupliar stages of some Oithona species (Copepoda: Cyclopoida) occurring in Toyama Bay, southern Japan Sea. Plankton Benthos Res 2:12–27CrossRefGoogle Scholar
  87. Tiselius P, Jonsson PR (1990) Foraging behavior of six calanoid copepods: observations and hydrodynamic analysis. Mar Ecol Prog Ser 66:23–33. doi: 10.3354/meps066023 CrossRefGoogle Scholar
  88. Titelman J (2001) Swimming and escape behavior of copepod nauplii: implications for predator-prey interactions among copepods. Mar Ecol Prog Ser 213:203–213. doi: 10.3354/meps213203 CrossRefGoogle Scholar
  89. Titelman J, Kiørboe T (2003) Predator avoidance by nauplii. Mar Ecol Prog Ser 247:137–149. doi: 10.3354/meps247137 CrossRefGoogle Scholar
  90. Tobe K, Meyer B, Fuentes V (2010) Detection of zooplankton items in the stomach and gut content of larval krill, Euphausia superba, using a molecular approach. Polar Biol 33:407–414. doi: 10.1007/s00300-009-0714-2 CrossRefGoogle Scholar
  91. 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 52:416–427CrossRefGoogle Scholar
  92. Troedsson C, Simonelli P, Nägele V, Nejstgaard JC, Frischer ME (2008) Quantification of copepod gut content by differential length amplification quantitative PCR (dla-qPCR). Mar Biol 156:253–259. doi: 10.1007/s00227-008-1079-8 CrossRefGoogle Scholar
  93. Turner JT (2004) The importance of small planktonic copepods and their roles in pelagic marine food webs. Zool Stud 43:255–266Google Scholar
  94. Turner JT, Tester PA (1992) Zooplankton feeding ecology: bacterivory by metazoan microzooplankton. J Exp Mar Biol Ecol 160:149–167. doi: 10.1016/0022-0981(92)90235-3 CrossRefGoogle Scholar
  95. Uye S, Nagano N, Tamaki H (1996) Geographical and seasonal variations in abundance, biomass and estimated production rates of microzooplankton in the inland Sea of Japan. J Oceanogr 52:689–703CrossRefGoogle Scholar
  96. Vadopalas B, Bouma JV, Jackels CR, Friedman CS (2006) Application of real-time PCR for simultaneous identification and quantification of larval abalone. J Exp Mar Biol Ecol 334:219–228. doi: 10.1016/j.jembe.2006.02.005 CrossRefGoogle Scholar
  97. VanderLugt K, Lenz PH (2008) Management of nauplius production in the paracalanid, Bestiolina similis (Crustacea: Copepoda): Effects of stocking densities and culture dilution. Aquaculture 276:69–77. doi: 10.1016/j.aquaculture.2008.01.041 CrossRefGoogle Scholar
  98. Vestheim H, Kaartvedt S, Edvardsen B (2005) State-dependent vertical distribution of the carnivore copepod Pareuchaeta norvegica. J Plankton Res 27:19–26. doi: 10.1093/plankt/fbh144 CrossRefGoogle Scholar
  99. Waggett RJ, Buskey EJ (2007) Calanoid copepod escape behavior in response to a visual predator. Mar Biol 150:599–607. doi: 10.1007/s00227-006-0384-3 CrossRefGoogle Scholar
  100. Wesche A, Wiltshire KH, Hirche HJ (2007) Overwintering strategies of dominant calanoid copepods in the German Bight, southern North Sea. Mar Biol 151:1309–1320. doi: 10.1007/s00227-006-0560-5 CrossRefGoogle Scholar
  101. White JR, Roman MR (1992) Seasonal study of grazing by metazoan zooplankton in mesohaline Chesapeake Bay. Mar Ecol Prog Ser 86:251–261. doi: 10.3354/meps086251 CrossRefGoogle Scholar
  102. Wight NA, Suzuki J, Vadopalas B, Friedman CS (2009) Development and optimization of quantitative PCR assays to aid Ostrea lurida carpenter 1864 restoration efforts. J Shellfish Res 28:33–41. doi: 10.2983/035.028.0108 CrossRefGoogle Scholar
  103. Wilson IG (1997) Inhibition and facilitation of nucleic acid amplification. Appl Environ Microbiol 63:3741–3751Google Scholar
  104. Zervoudaki S, Christou ED, Nielsen TG, Siokou-Frangou I, Assimakopoulou G, Giannakourou A, Maar M, Pagou K, Krasakopoulou E, Christaki U, Moraitou-Apostolopoulou M (2007) The importance of small-sized copepods in a frontal area of the Aegean Sea. J Plankton Res 29:317–338. doi: 10.1093/plankt/fbm018 CrossRefGoogle Scholar
  105. Zhu F, Massana R, Not F, Marie D, Vaulot D (2005) Mapping of picoeucaryotes in marine ecosystems with quantitative PCR of the 18S rRNA gene. FEMS Microbiol Ecol 52:79–92. doi: 10.1016/j.femsec.2004.10.006 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Michelle J. Jungbluth
    • 1
    • 2
  • Erica Goetze
    • 1
  • Petra H. Lenz
    • 2
  1. 1.Department of Oceanography, School of Ocean and Earth Sciences and TechnologyUniversity of Hawaii at ManoaHonoluluUSA
  2. 2.Pacific Biosciences Research CenterUniversity of Hawaii at ManoaHonoluluUSA

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