Diet affects body color and energy metabolism in the Baikal endemic amphipod Eulimnogammarus cyaneus maintained in laboratory conditions

Abstract

Proper diet is critical for laboratory-reared animals, as it may affect not only their welfare, but also experimental results. Amphipods (Crustacea: Amphipoda) play important roles in ecosystems and are often used in environmental research. Endemic amphipods from the ancient Lake Baikal are promising for laboratory bioassays; however, there are currently no laboratory cultures. In this work, we determine how different diets affect the color and metabolism of a laboratory-reared Baikal amphipod, Eulimnogammarus cyaneus. We found that in freshly collected blue-colored animals, body color correlated with total carotenoid content. Total carotenoid levels did not differ after long-term (two months) feeding with a close to natural carotenoid-enriched, or even a carotenoid-depleted diet. Nevertheless, antennae color was closer to red in the natural-like diet group. It is likely that the carotenoids from the commercial diet are not properly metabolized in E. cyaneus. The animals fed commercial diets had a higher glycogen content, which may signify a higher metabolic rate. Overall, we show that a carotenoid-enriched diet optimized for decapods is not optimal for amphipods, likely due to different carotenoid compositions, and the diet for long-term rearing of E. cyaneus and other Baikal amphipods requires supplementation.

Keywords:

carotenoids, diet, laboratory rearing, Baikal, Amphipoda, Crustacea, Decapoda, culture, metabolites

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References

Alberts-Hubatsch, H., Slater, M. J., and Beermann, J. 2019. Effect of diet on growth, survival and fatty acid profile of marine amphipods: implications for utilisation as a feed ingredient for sustainable aquaculture. Aquaculture Environment Interactions 11:481–491. https://doi.org/10.3354/aei00329

Alonso, Á., De Lange, H. J., and Peeters, E. T. 2010. Contrasting sensitivities to toxicants of the freshwater amphipods Gammarus pulex and G. fossarum. Ecotoxicology 19(1):133. https://doi.org/10.1007/s10646-009-0398-y

Arfianti, T., Wilson, S., and Costello, M. J. 2018. Progress in the discovery of amphipod crustaceans. PeerJ 6:e5187. https://doi.org/10.7717/peerj.5187

Artal, M. C., Dos Santos, A., Henry, T. B., and de Aragão Umbuzeiro, G. 2018. Development of an acute toxicity test with the tropical marine amphipod Parhyale hawaiensis. Ecotoxicology 27(2):103–108. https://doi.org/10.1007/s10646-017-1875-3

Axenov-Gribanov, D. V., Bedulina, D. S., Shirokova, Y. A., Emshanova, V. A., Lubyaga, Y. A., Vereshchagina, K. P., Saranchina, A. E., Pobezhimova, T. P., and Timofeyev, M. A. 2019. Diet influence on mechanisms of non-specific stress-response in Baikal endemic amphipod species during long-term laboratory exposure. Crustaceana 92(11–12):1349–1368. https://doi.org/10.1163/15685403-00003951

Babin, A., Motreuil, S., Teixeira, M., Bauer, A., Rigaud, T., Moreau, J., and Moret, Y. 2020. Origin of the natural variation in the storage of dietary carotenoids in freshwater amphipod crustaceans. PloS ONE 15(4):e0231247. https://doi.org/10.1371/journal.pone.0231247

Baeza-Rojano, E., García, S., Garrido, D., Guerra-García, J. M., and Domingues, P. 2010. Use of amphipods as alternative prey to culture cuttlefish (Sepia officinalis) hatchlings. Aquaculture 300(1–4):243–246. https://doi.org/10.1016/j.aquaculture.2009.12.029

Beatty, R. A. 1949. The pigmentation of cavernicolous animals: III. The Carotenoid pigments of some amphipod Crustacea. Journal of Experimental Biology 26(2):125–130. https://doi.org/10.1242/jeb.26.2.125

Bedulina, D. S., Evgen'ev, M. B., Timofeyev, M. A., Protopopova, M. V., Garbuz, D. G., Pavlichenko, V. V., Luckenbach, T., Shatilina, Z. M., Axenov-Gribanov, D. V., Gurkov, A. N., Sokolova, I. M., and Zatsepina, O. G. 2013. Expression patterns and organization of the hsp70 genes correlate with thermotolerance in two congener endemic amphipod species (Eulimnogammarus cyaneus and E. verrucosus) from Lake Baikal. Molecular Ecology 22(5):1416–1430. https://doi.org/10.1111/mec.12136

Bedulina, D. S., Takhteev, V. V., Pogrebnyak, S. G., Govorukhina, E. B., Madyarova, E. V., and Lubyaga, Y. A. 2014. On Eulimnogammarus messerschmidtii, sp. n. (Amphipoda: Gammaridea). Zootaxa 3838(5):518–544. https://doi.org/10.11646/zootaxa.3838.5.2

Bedulina, D., Drozdova, P., Gurkov, A., von Bergen, M., Stadler, P. F., Luckenbach, T., Timofeyev, M. A., and Kalkhof, S. 2020. Proteomics reveals sex-specific heat shock response of Baikal amphipod Eulimnogammarus cyaneus. Science of the Total Environment 763:143008. https://doi.org/10.1016/j.scitotenv.2020.143008

Belykh, O. I., Ekaterina, G., Sorokovikova, T., Saphonova, A., and Tikhonova, I. V. 2006. Autotrophic picoplankton of Lake Baikal: composition, abundance and structure. Hydrobiologia 568(1):9–17. https://doi.org/10.1007/s10750-006-0340-8

Brix, S., Lorz, A. N., Jazdzewska, A. M., Hughes, L., Tandberg, A. H. S., Pabis, K., Stransky, B., Krapp-Schickel, T., and Sorbe, J. C. 2018. Amphipod family distributions around Iceland. ZooKeys 731:1–53. https://doi.org/10.3897/zookeys.731.19854

Chayen, N. E., Cianci, M., Grossmann, J. G., Habash, J., Helliwell, J. R., Nneji, G. A., Raftery, J., Pierre, J. R., and Zagalsky, P. F. 2003. Unravelling the structural chemistry of the colouration mechanism in lobster shell. Acta Crystallographica. Section D, Biological Crystallography 59(12):2072–2082. https://doi.org/10.1107/s0907444903025952

Coral-Hinostroza, G. N. and Bjerkeng, B. 2002. Astaxanthin from the red crab langostilla (Pleuroncodes planipes): optical R/S isomers and fatty acid moieties of astaxanthin esters. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 133(3):437–444. https://doi.org/10.1016/S1096-4959(02)00186-0

Czeczuga, B. 1975. Carotenoids in thirteen species of gammaridae from Lake Bajkał. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 50(2):259–268. https://doi.org/10.1016/0305-0491(75)90272-2

Czeczuga, B. 1980. Changes occurring during the annual cycle in the carotenoid content of Gammarus lacustris GO Sars (Crustacea: Amphipoda) specimens from the river Narew. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 66(4):569–572. https://doi.org/10.1016/0305-0491(80)90250-3

Dembitsky, V. M. and Rezanka, T. 1996. Comparative study of the endemic freshwater fauna of Lake Baikal-VII. Carotenoid composition of the deep-water amphipod crustacean Acanthogammarus (Brachyuropus) grewingkii. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 114(4):383–387. https://doi.org/10.1016/0305-0491(96)00066-1

Drozdova, P., Saranchina, A., Morgunova, M., Kizenko, A., Lubyaga, Y., Baduev, B., and Timofeyev, M. 2020. The level of putative carotenoid-binding proteins determines the body color in two species of endemic Lake Baikal amphipods. PeerJ 8:e9387. https://doi.org/10.7717/peerj.9387

Du, J., Xu, S., Zhou, Q., Li, H., Fu, L., Tang, J., Wang, Y., Peng, X., Xu, Y., and Du, X. 2020. A review of microplastics in the aquatic environmental: distribution, transport, ecotoxicology, and toxicological mechanisms. Environmental Science and Pollution Research 27:11494–11505. https://doi.org/10.1007/s11356-020-08104-9

Dybowsky, B. N. 1874. Beiträge zur näheren Kenntniss der in dem Baikal-See vorkommenden niederen Krebse aus der Gruppe der Gammariden (Vol. 10), St. Petersburg, Buchdrukerei. von W. Besobrasoff & Comp. https://doi.org/10.5962/bhl.title.9945

Fietz, S., Bleiß, W., Hepperle, D., Koppitz, H., Krienitz, L., and Nicklisch, A. 2005. First record of Nannochloropsis limnetica (Eustigmatophyceae) in the autotrophic picoplankton from Lake Baikal. Journal of Phycology 41(4):780–790. https://doi.org/10.1111/j.0022-3646.2005.04198.x

Fišer, C., Konec, M., Alther, R., Švara, V., and Altermatt, F. 2017. Taxonomic, phylogenetic and ecological diversity of Niphargus (Amphipoda: Crustacea) in the Hölloch cave system (Switzerland). Systematics and Biodiversity 15(3):218–237. https://doi.org/10.1080/14772000.2016.1249112

Gaillard, M., Juillet, C., Cézilly, F., and Perrot-Minnot, M. J. 2004. Carotenoids of two freshwater amphipod species (Gammarus pulex and G. roeseli) and their common acanthocephalan parasite Polymorphus minutus. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 139(1):129–136. https://doi.org/10.1016/j.cbpc.2004.07.001

Gurkov, A., Rivarola-Duarte, L., Bedulina, D., Casas, I. F., Michael, H., Drozdova, P., Nazarova, A., Govorukhina, E., Timofeyev, M., Stadler, P. F., and Luckenbach, T. 2019. Indication of ongoing amphipod speciation in Lake Baikal by genetic structures within endemic species. BMC Evolutionary Biology 19:138. https://doi.org/10.1186/s12862-019-1470-8

Hervant, F., Mathieu, J., and Barré, H. 1999. Comparative study on the metabolic responses of subterranean and surface-dwelling amphipods to long-term starvation and subsequent refeeding. Journal of Experimental Biology 202(24):3587–3595. https://doi.org/10.1242/jeb.202.24.3587

Hyne, R. V., Gale, S. A., and King, C. K. 2005. Laboratory culture and life‐cycle experiments with the benthic amphipod Melita plumulosa (Zeidler). Environmental Toxicology and Chemistry 24(8):2065–2073. https://doi.org/10.1897/04-409R1.1

Jakob, L., Bedulina, D. S., Axenov-Gribanov, D. V., Ginzburg, M., Shatilina, Z. M., Lubyaga, Y. A., Madyarova, E. V., Gurkov, A. N., Timofeyev, M. A., Pörtner, H.-O., Sartoris, F. J., Altenburger, R., and Luckenbach, T. 2017. Uptake kinetics and subcellular compartmentalization explain lethal but not sublethal effects of cadmium in two closely related amphipod species. Environmental Science & Technology 51(12):7208–7218. https://doi.org/10.1021/acs.est.6b06613

Jussila, J. 1997. Physiological responses of astacid and parastacid crayfishes (Crustacea: Decapoda) to conditions of intensive culture. Western Australia: University of Kuopio, 140 p.

Lubyaga, Y., Trifonova, M., Drozdova, P., Gurkov, A., Madyarova, E., Axenov-Gribanov, D., Kurashov, E, Vereshchagina, K., Shatilina, Z., and Timofeyev, M. 2020. Invader amphipods Gmelinoides fasciatus (Stebbing, 1899) inhabiting distant waterbodies demonstrate differences in tolerance and energy metabolism under elevated temperatures. Journal of Great Lakes Research 46(4):899–909. https://doi.org/10.1016/j.jglr.2020.05.011

Macdonald III, K. S., Yampolsky, L., and Duffy, J. E. 2005. Molecular and morphological evolution of the amphipod radiation of Lake Baikal. Molecular Phylogenetics and Evolution 35(2):323–343. https://doi.org/10.1016/j.ympev.2005.01.013

Maoka, T. 2011. Carotenoids in marine animals. Marine Drugs 9(2):278–293. https://doi.org/10.3390/md9020278

Maoka, T. 2020. Carotenoids as natural functional pigments. Journal of Natural Medicines 74:1–16. https://doi.org/10.1007/s11418-019-01364-x

McCahon, C. P. and Pascoe, D. 1988. Culture techniques for three freshwater macroinvertebrate species and their use in toxicity tests. Chemosphere 17(12):2471–2480. https://doi.org/10.1016/0045-6535(88)90157-9

Mekhanikova, I. V. 2015. Morphology of mouthpart and feeding of Eulimnogammarus cyaneus (Crustacea, Amphipoda), an inhabitant of the Lake Baikal nearshore zone. Zoologicheskii Zhurnal 94(12):1379–1386. https://doi.org/10.7868/S0044513415120107 (In Russian)

Morino, H., Kamaltynov, R. M., Nakai, K., and Mashiko, K. 2000. Phenetic analysis, trophic specialization and habitat partitioning in the Baikal amphipod genus Eulimnogammarus (Crustacea). Advances in Ecological Research 31:355–376. https://doi.org/10.1016/S0065-2504(00)31019-4

Naumenko, S. A., Logacheva, M. D., Popova, N. V., Klepikova, A. V., Penin, A. A., Bazykin, G. A., Etingova, A. E., Mugue, N. S., Kondrashov, A. S., and Yampolsky, L. Y. 2017. Transcriptome‐based phylogeny of endemic Lake Baikal amphipod species flock: fast speciation accompanied by frequent episodes of positive selection. Molecular Ecology 26(2):536–553. https://doi.org/10.1111/mec.13927

Pascoe, D. and Othman, M. S. 2001. Growth, development and reproduction of Hyalella azteca (Saussure, 1858) in laboratory culture. Crustaceana 74(2):171–181. https://doi.org/10.1163/156854001750096274

Podlesińska, W. and Dąbrowska, H. 2019. Amphipods in estuarine and marine quality assessment — a review. Oceanologia 61(2):179–196. https://doi.org/10.1016/j.oceano.2018.09.002

R Core Team. 2019. A language and environment for statistical computing. R foundation for statistical computing. Vienna, Austria. https://www.r-project.org

Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J.-Y., White, D. J., Hartenstein, V., Eliceiri, K., Tomancak, P., and Cardona, A. 2012. Fiji: an open-source platform for biological-image analysis. Nature Methods 9(7):676–682. https://doi.org/10.1038/nmeth.2019

Schneider, C. A., Rasband, W. S., and Eliceiri, K. W. 2012. NIH Image to ImageJ: 25 years of image. Nature Methods 9(7):671–675. https://doi.org/10.1038/nmeth.2089

Semsar-Kazerouni, M., Boerrigter, J. G., and Verberk, W. C. 2020. Changes in heat stress tolerance in a freshwater amphipod following starvation: The role of oxygen availability, metabolic rate, heat shock proteins and energy reserves. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 245:110697. https://doi.org/10.1016/j.cbpa.2020.110697

Spicer, J. I., Moore, P. G., and Taylor, A. C. 1987. The physiological ecology of land invasion by the Talitridae (Crustacea: Amphipoda). Proceedings of the Royal Society of London. Series B. Biological Sciences 232(1266):95–124. https://doi.org/10.1098/rspb.1987.0063

Su, F., Huang, B., and Liu, J. 2018. The carotenoids of shrimps (Decapoda: Caridea and Dendrobranchiata) cultured in China. Journal of Crustacean Biology 38(5):523–530. https://doi.org/10.1093/jcbiol/ruy049

Takhteev, V. V. 2019. On the current state of taxonomy of the Baikal Lake amphipods (Crustacea: Amphipoda) and the typological ways of constructing their system. Arthropoda Selecta 28(3):374–402. https://doi.org/10.15298/arthsel.28.3.03

Tanaka, Y., Matsuguchi, H., Katayama, T., Simpson, K. L., and Chichester, C. O. 1976. The biosynthesis of astaxanthin — XVI. The carotenoids in crustacea. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 54(3):391–393. https://doi.org/10.1016/0305-0491(76)90263-7

Thoen, H. H., Johnsen, G., and Berge, J. 2011. Pigmentation and spectral absorbance in the deep-sea arctic amphipods Eurythenes gryllus and Anonyx sp. Polar Biology 34(1):83–93. https://doi.org/10.1007/s00300-010-0861-5

Timofeyev, M. A., Protopopova, M., Pavlichenko, V., and Steinberg, C. E. 2009. Can acclimation of amphipods change their antioxidative response? Aquatic Ecology 43(4):1041. https://doi.org/10.1007/s10452-008-9217-4

Kamaltynov, R. M. 2001. Amphipods (Amphipoda, Gammaroidea); pp. 572–831 in: Timoshkin, O. A. (Ed.), Lake Baikal: diversity of fauna, problems of its immiscibility and origin, ecology and “exotic” communities. Index of animal species inhabiting Lake Baikal and its catchment area, Nauka, Novosibirsk.

Tlusty, M. and Hyland, C. 2005. Astaxanthin deposition in the cuticle of juvenile American lobster (Homarus americanus): implications for phenotypic and genotypic coloration. Marine Biology 147(1):113–119. https://doi.org/10.1007/s00227-005-1558-0

Vargas-Abúndez, J. A., López-Vázquez, H. I., Mascaró, M., Martínez-Moreno, G. L., and Simões, N. 2021. Marine amphipods as a new live prey for ornamental aquaculture: exploring the potential of Parhyale hawaiensis and Elasmopus pectenicrus. PeerJ 9:10840. https://doi.org/10.7717/peerj.10840

Vereshchagina, K. P., Lubyaga, Y. A., Shatilina, Z., Bedulina, D., Gurkov, A., Axenov-Gribanov, D. V., Baduev, B., Kondrateva, E. S., Gubanov, M., Zadereev, E., Sokolova, I., and Timofeyev, M. 2016. Salinity modulates thermotolerance, energy metabolism and stress response in amphipods Gammarus lacustris. PeerJ 4:e2657. https://doi.org/10.7717/peerj.2657

Villacorta, C., Jaume, D., Oromí, P., and Juan, C. 2008. Under the volcano: phylogeography and evolution of the cave-dwelling Palmorchestia hypogaea (Amphipoda, Crustacea) at La Palma (Canary Islands). BMC Biology 6(1):1–14. https://doi.org/10.1186/1741-7007-6-7

Väinölä, R., Witt, J. D. S., Grabowski, M., Bradbury, J. H., Jazdzewski, K., and Sket, B. 2008. Global diversity of amphipods (Amphipoda; Crustacea) in freshwater. Hydrobiologia 595:241–255. https://doi.org/10.1007/s10750-007-9020-6

Wade, N. M., Gabaudan, J., and Glencross, B. D. 2017. A review of carotenoid utilisation and function in crustacean aquaculture. Reviews in Aquaculture 9(2):141–156. https://doi.org/10.1111/raq.12109

Wang, W., Ishikawa, M., Koshio, S., Yokoyama, S., Hossain, M. S., and Moss, A. S. 2018. Effects of dietary astaxanthin supplementation on juvenile kuruma shrimp, Marsupenaeus japonicus. Aquaculture 491:197–204. https://doi.org/10.1016/j.aquaculture.2018.03.025

Wattier, R., Mamos, T., Copilaş-Ciocianu, D., Jelić, M., Ollivier, A., Chaumot, A., Danger, M., Felten, V., Piscart, C., Žganec, K., and Rewicz, T. 2020. Continental-scale patterns of hyper-cryptic diversity within the freshwater model taxon Gammarus fossarum (Crustacea, Amphipoda). Scientific Reports 10(1):1–16. https://doi.org/10.1038/s41598-020-73739-0

Weaver, R. J., Gonzalez, B. K., Santos, S. R., and Havird, J. C. 2020. Red coloration in an anchialine shrimp: carotenoids, genetic variation, and candidate genes. The Biological Bulletin 238(2):119–130. https://doi.org/10.1086/708625

Wickham, H. 2016. ggplot2: elegant graphics for data analysis. Springer. https://doi.org/10.1007/978-3-319-24277-4

Wildish, D. J., Pavesi, L., and Ketmaier, V. 2012. Talitrid amphipods (Crustacea: Amphipoda: Talitridae) and the driftwood ecological niche: a morphological and molecular study. Journal of Natural History 46(43–44):2677–2700. https://doi.org/10.1080/00222933.2012.717971

Woods, C. M. 2009. Caprellid amphipods: an overlooked marine finfish aquaculture resource? Aquaculture 289(3–4):199–211. https://doi.org/10.1016/j.aquaculture.2009.01.018

Xavier, J. C., Cherel, Y., Boxshall, G., Brandt, A., Coffer, T., Forman, J., Havermans, C., Jażdżewska, A., Kouwenberg, J., Schnabel, K., and Schiaparelli, S. 2020. Crustacean guide for predator studies in the Southern Ocean. Scientific Committee on Antarctic Research, 253 p.

Published
2021-11-12
How to Cite
Saranchina, A., Drozdova, P., Mutin, A., & Timofeyev, M. (2021). Diet affects body color and energy metabolism in the Baikal endemic amphipod <em>Eulimnogammarus cyaneus</em&gt; maintained in laboratory conditions. Biological Communications, 66(3), 245–255. https://doi.org/10.21638/spbu03.2021.306
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