Effect of Microalgae Species and Concentration on Grazing Rate and Egg Production of Copepods Calanipeda aquaedulcis Kritschagin, 1873 and Arctodiaptomus salinus (Daday, 1885)

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Abstract

The effect of concentration of the microalgae, haptophyte Isochrysis galbana and dinophyte Prorocentrum cordatum, on the daily grazing rate (G) and daily egg production rate (EPR) of the brackish-water copepods Arctodiaptomus salinus and Calanipeda aquaedulcis was studied under experimental conditions. Daily grazing rates of copepods increased logarithmically with increasing microalgae concentration. The maximum grazing rates in both species were observed when feeding on I. galbana at a concentration of 170–196 µg C/mL. The maximum daily EPR in females of C. aquaedulcis (129% of body weight in carbon equivalent) were obtained when they fed on I. galbana at a concentration of 15.4 µg C/mL, or on P. cordatum at 4 µg C/mL. The maximum EPR values in A. salinus females were 34% of their weight in carbon equivalent when feeding on P. cordatum at a concentration of 26 µg C/mL, and 45% in their carbon equivalent at 8.9 µg C/mL of I. galbana. The further increase in the microalgae concentration led to the decrease in EPR values. The efficiency of ingested food utilization for egg production in carbon equivalent (gross growth efficiency, GGE, %) of C. aquaedulcis was significantly higher than that of A. salinus, regardless of the species and concentration of microalgae.

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L. O. Aganesova

Kovalevsky Institute of Biology of the Southern Seas, Russian Academy of Sciences

Author for correspondence.
Email: la7risa@gmail.com
ORCID iD: 0000-0003-4052-7985
Russian Federation, Sevastopol

A. N. Khanaychenko

Kovalevsky Institute of Biology of the Southern Seas, Russian Academy of Sciences

Email: la7risa@gmail.com
ORCID iD: 0000-0002-4334-9996
Russian Federation, Sevastopol

References

  1. Аганесова Л.О. Длительность развития копепод Calanipeda aquaedulcis и Arctodiaptomus salinus при разном температурном режиме культивирования // Мор. экол. журн. 2013. Т. 12. № 1. С. 19–25.
  2. Аганесова Л.О. Размножение и развитие солоноватоводных копепод при кормлении микроводорослями разных видов // Биол. моря. 2021. Т. 47. № 2. С. 108–114. doi: 10.31857/S0134347521020029
  3. Вьюшкова В.П., Гурова Т.В. Находка солоноватоводного рачка Calanipeda aquaedulcis Kritsch (Copepoda, Calanoidae) в Волгоградском водохранилище // Зоол. журн. 1968. Т. 47. № 11. С. 1726–1727.
  4. Гарбер Б.И. Наблюдения за развитием и размножением Calanipeda aquae dulcis Kritsch (Copepoda: Calanoida) // Тр. Карадаг. биол. ст. 1951. Т. 2. С. 3–55.
  5. Гунько А.Ф., Алдакимова А.Я. Материалы о питании Calanipeda aquaedulcis (Crustacea, Calanoida) в Азовском море // Тр. АзНИИРХ. 1963. Вып. 6. С. 3–5.
  6. Ковалева Т.М. Влияние размеров и морфологических особенностей водорослей на потребление их копеподами // Биол. моря. 1977. Т. 42. С. 28–33.
  7. Кортунова Т.А., Буляева Л.Ф., Ярыгина О.К. Рачок калянипеда в Аральском море // Рыб. хоз-во. 1972. № 7. C. 32–34.
  8. Куделина Е.Н. Влияние температуры на размножение, развитие и плодовитость Calanipeda aquaedulcis Kritsch // Тр. Касп. бассейн. фил. ВНИРО. 1950. Т. 11. C. 265–286.
  9. Ханайченко А.Н. Влияние микроводорослевой диеты на характеристики воспроизводства копепод // Экол. моря. 1999. Т. 49. С. 56–61.
  10. Ханайченко А.Н., Поспелова Н.А., Аганесова Л.О., Рауэн Т.В. Каротиноидный состав каляноидных копепод Calanipeda aquaedulcis и Arctodiaptomus salinus при питании Dunaliella salina // Мор. экол. журн. 2014. Т. 13. № 1. С. 82–87.
  11. Шадрин Н.В., Батогова Е.А., Копейка А.В. Arctodiaptomus salinus (Daday, 1885) (Copepoda, Diaptomidae), редкий в северо-западной части Черного моря вид, обычен в прибрежных водах Крыма // Мор. экол. журн. 2008. Т. 7. № 2. С. 86.
  12. Andreev N.I., Plotnikov I.S., Aladin N.V. The fauna of the Aral Sea in 1989. 2. The zooplankton // Int. J. Salt Lake Res. 1992. V. 1. № 1. P. 111–116. doi: 10.1007/bf02904955
  13. Barkhatov Y.V., Tolomeev A.P., Drobotov A.V. The response of zooplankton abundance in saline meromictic Lake Shira to a change in circulation regime // J. Ocean. Limnol. 2023. V. 41. P. 1321–1330.
  14. doi: 10.1007/s00343-022-2132-z
  15. Berggreen U., Hansen B., Kiørboe T. Food size spectra, ingestion and growth of the copepod Acartia tonsa during development: implications for determination of copepod production // Mar. Biol. 1988. V. 99. № 3. P. 341–352. doi: 10.1007/bf02112126
  16. Besiktepe S., Dam H.G. Effect of diet on the coupling of ingestion and egg production in the ubiquitous copepod // Acartia tonsa, Prog. Oceanogr. 2020. V 186. Art. ID 102346. doi: 10.1016/j.pocean.2020.102346
  17. Brucet S., Compte J., Boix D. et al. Feeding of nauplii, copepodites and adults of Calanipeda aquaedulcis (Calanoida) in Mediterranean salt marshes // Mar. Ecol.: Prog. Ser. 2008. V. 355, P. 183–191.
  18. doi: 10.3354/meps07225
  19. Coutteau P. Micro-Algae / Manual on the Production and Use of Live Food for Aquaculture, FAO Fisheries Technical Paper, № 361, P. Lavens, P. Sorgeloos, Eds., Rome: FAO. 1996. P. 7–48.
  20. Dam H.G., Colin S.P. Prorocentrum minimum (clone Exuv) is nutritionally insufficient, but not toxic to the copepod Acartia tonsa // Harmful Algae. 2005. V. 4. P. 575–584. doi: 10.1016/j.hal.2004.08.007
  21. Deason E.E. Grazing of Acartia hudsonica (A. clausi) on Skeletonema costatum in Narragansett Bay (USA): Influence of food concentration and temperature // Mar. Biol. 1980. V. 60. P. 101–113. doi: 10.1007/BF00389153
  22. Durbin E.G., Durbin A.G. Effects of temperature and food abundance on grazing and short term weight change in the marine copepod Acartia hudsonica // Limnol. Oceanogr. 1992. V. 37. № 2. P. 361–378. doi: 10.4319/lo.1992.37.2.0361
  23. Frisch D., Rodríguez-Pérez H., Green A.J. Invasion of artificial ponds in Donana Natural Park, southwest Spain, by an exotic estuarine copepod // Aquat. Conserv. 2006. V. 16. № 5. P. 483–492.
  24. doi: 10.1002/aqc.718
  25. Frost B.W. Effects of size and concentration of food particles on the feeding behavior of the marine planktonic copepod Calanus pacificus // Limnol. Oceanogr. 1972. V. 18. № 6. P. 805–815.
  26. doi: 10.4319/lo.1972.17.6.0805
  27. Gonçalves A.M.M., Azeiteiro U.M., Pardal M.A., De Troch M. Fatty acid profiling reveals seasonal and spatial shifts in zooplankton diet in a temperate estuary // Estuarine, Coastal Shelf Sci. 2012. V. 109. P. 70–80. doi: 10.1016/j.ecss.2012.05.020
  28. Gubanova A.D., Prusova I.Yu., Niermann U. et al. Dramatic change in the copepod community in Sevastopol Bay (Black Sea) during two decades (1976–1996) // Senckenbergiana Maritima. 2001. V. 31. № 1. P. 17–27. doi: 10.1007/bf03042833
  29. Guerrero F., Jiménez-Melero R., Parra G. et al. Lipid composition of Arctodiaptomus salinus (Copepoda: Calanoida) // J. Freshwater Ecol. 2007. V. 22. № 1. P. 147–150. doi: 10.1080/02705060.2007.9664155
  30. Gurkan S., Aragoneses P., Innal D. et al. Trophic niches of two congeneric pipefishes in the Aegean Sea (Bargilya Wetland, Turkey), based on stable isotope analyses // Preprint. 2023. № 2023072072. doi: 10.20944/preprints202307.2072.v1
  31. Helenius L., Budge S.M., Johnson C.L. Stable isotope labeling reveals patterns in essential fatty acid growth efficiency in a lipid-poor coastal calanoid copepod // Mar. Biol. 2020. V. 167. Art. ID 178. doi: 10.1007/s00227-020-03794-8
  32. Jiménez-Melero R., Parra G., Guerrero F. Effect of temperature, and individual variability on the embryonic development time and fecundity of Arctodiaptomus salinus (Copepoda: Calanoida) from a shallow saline pond // Hydrobiologia. 2012. V. 686. P. 241–256. doi: 10.1007/s10750-012-1014-3
  33. Jiménez-Melero R., Parra G., Souissi S., Guerrero F. Post-embryonic developmental plasticity of Arctodiaptomus salinus (Copepoda: Calanoida) at different temperatures // J. Plankton Res. 2007. V. 29. № 6. P. 553–567. doi: 10.1093/plankt/fbm038
  34. Khanaychenko A.N., Telesh I.V., Skarlato S.O. Bloom-forming potentially toxic dinoflagellates Prorocentrum cordatum in marine plankton food webs // Protistology. 2019. V. 13. № 3. P. 95–125. doi: 10.21685/1680-0826-2019-13-3-1
  35. Kiørboe T., Sabatini M. Reproductive and life cycle strategies in egg-carrying cyclopoid and free-spawning calanoid copepods // J. Plankton Res. 1994. V. 16. № 10. P. 1353–1366. doi: 10.1093/plankt/16.10.1353
  36. Lacoste A., Poulet S.A., Cueff A. et al. New evidence of the copepod maternal food effects on reproduction // J. Exp. Mar. Biol. Ecol. 2001. V. 259. № 1. P. 85–107. doi: 10.1016/S0022-0981(01)00224-6
  37. Lapesa S., Snell T.W., Fields D.M., Serra M. Selective feeding of Arctodiaptomus salinus (Copepoda, Calanoida) on co-occurring sibling rotifer species // Freshwater Biol. 2004. V. 49. № 8. P. 1053–1061. doi: 10.1111/j.1365-2427.2004.01249.x
  38. Lazareva V.I. The Mediterranean copepod Calanipeda aquaedulcis Kritschagin, 1873 (Crustacea, Calanoida) in the Volga River Reservoirs // Inland Water Biol. 2018. V. 11. P. 303–309. doi: 10.1134/S1995082918030112
  39. Marrone F., Castelli G., Barone R., Naselli-Flores L. Ecology and distribution of calanoid copepods in Sicilian inland waters (Italy) // Verh. – Int. Ver. Theor. Angew. Limnol. 2006. V. 29. P. 2150–2156. doi: 10.1080/03680770.2006.11903072
  40. Paffenhöffer G.-A. Feeding rates and behavior of zooplankton // Bull. Mar. Sci. 1988. V. 43. № 3. P. 430–445.
  41. Plotnikov I.S., Aladin N.V., Mossin J., Høeg J.T. Crustacean fauna of the Aral Sea and its relation to ichthyofauna during the modern regression crisis and efforts at restoration // Zool. Studs. 2021. V. 60. № 25. doi: 10.6620/ZS.2021.60-25
  42. Ramdani M., Elkhiati N., Flower R.J. et al. Open water zooplankton communities in North African wetland lakes: the CASSARINA Project // Aquatic Ecol. 2001. V. 35. № 3–4. P. 319–333. doi: 10.1023/A:1011926310469
  43. Rokneddine A., Chentoufi M. Study of salinity and temperature tolerance limits regarding four crustacean species in a temporary salt water swamp (Lake Zima, Morocco) // Anim. Biol. 2004. V. 54. № 3. P. 237–253. doi: 10.1163/1570756042484719
  44. Støttrup J.G., Jensen J. Influence of algal diet on feeding and egg-production of the calanoid copepod Acartia tonsa Dana // J. Exp. Mar. Biol. Ecol. 1990. V. 141. № 2–3. P. 87–105. doi: 10.1016/0022-0981(90)90216-Y
  45. Svetlichny L., Hubareva E., Khanaychenko A. Calanipeda aquaedulcis and Arctodiaptomus salinus are exceptionally euryhaline osmoconformers: Evidence from mortality, oxygen consumption, and mass density patterns // Mar. Ecol.: Prog. Ser. 2012a, V. 470. P. 15–29. doi: 10.3354/meps09907
  46. Svetlichny L., Khanaychenko A., Hubareva E., Aganesova L. Partitioning of respiratory energy and environmental tolerance in the copepods Calanipeda aquaedulcis and Arctodiaptomus salinus // Estuarine, Coastal Shelf Sci. 2012b. V. 114. P. 199–207. doi: 10.1016/j.ecss.2012.07.023
  47. Suh S.S., Kim S.J., Hwang J. et al. Fatty acid methyl ester profiles and nutritive values of 20 marine microalgae in Korea // Asian Pac. J. Trop. Med. 2015. V. 8. № 3. P. 191–196. doi: 10.1016/S1995-7645(14)60313-8
  48. Tolomeev A.P. Phytoplankton diet of Arctodiaptomus salinus (Copepoda, Calanoida) in Lake Shira (Khakasia) // Aquat. Ecol. 2002. V. 36. № 2. P. 229–234.
  49. Tolomeev A.P., Sushchik N.N., Gulati R.D. et al. Feeding spectra of Arctodiaptomus salinus (Calanoida, Copepoda) using fatty acid trophic markers in seston food in two salt lakes in South Siberia (Khakasia, Russia) // Aquat. Ecol. 2010. V. 44. № 3. P. 513–530.
  50. doi: 10.1007/s10452-010-9331-y
  51. Ustaoğlu M.R. A check-list for zooplankton of Turkish inland waters // Eur. Union J. Fish. Aquat. Sci. 2004. V. 21. № 3–4. P. 191–199.
  52. Vincent M., Ceccaldi H.J. Relations entre acides gras et pigments caroténoïdes chez un crustacé copépode, Calanipeda aquae-dulcis // Biochem. Syst. Ecol. 1988. V. 16. № 3. P. 317–324. doi: 10.1016/0305-1978(88)90017-8

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2. Fig. 1. The carbon equivalent of the diets of Calanipeda aquaedulcis and Arctodiaptomus salinus (G, mcg/day) depending on the concentration of microalgae (mcg/ml). a – Isochrysis galbana (ISO), b – Prorocentrum cordatum (PRO) (M, 95% CI, p < 0.05)

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3. Fig. 2. Female (a) and male (b) Calanipeda aquaedulcis with fat droplets after excessive microalgae feeding (Photo by L.S. Svetlichny)

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