Abstract
Species of the genus Euphausia dominate the euphausiid biomass of the Southern Ocean, the three largest being Euphausia superba, E. triacantha and E. crystallorophias. We measured a number of morphological features to identify differences between, and within, these species to obtain ecological insights. Interspecifically, the greatest difference was carapace size, with that of E. superba being by far the largest and most variable. This likely reflects its prolific spawning capacity compared with other euphausiid species. E. triacantha exhibited an extended sixth abdominal segment that could facilitate greater levels of thrust in the tail flip escape response. The pleopods, which provide propulsion in forward swimming, were more than 50% larger in E. superba, indicating a greater capacity for directional movement at high velocities. E. crystallorophias had eyes that were almost double the size of those in E. superba and E. triacantha, which may help retain visual resolution within its under-ice habitat. Intraspecifically, we found the above morphological features differed little between sexes and developmental stages in E. crystallorophias and E. triacantha, but differed significantly in E. superba. Compared to females and juveniles, male E. superba had significantly larger eyes and pleopods, whilst the carapace in males became shorter as a proportion of body length during growth. These features indicate a greater capacity for searching and swimming in males, which, we hypothesise, increases their ability to locate and fertilise females. This morphological specialisation in male E. superba is indicative of comparatively greater inter-male competition resulting from its tendency to form large, dense swarms.
Similar content being viewed by others
Data Availability
All raw data on which this study is based are published as an appendix (Appendix 1) to the present manuscript.
References
Amakasu K, Ono A, Moteki M, Ishimaru TJPS (2011) Sexual dimorphism in body shape of Antarctic krill (Euphausia superba) and its influence on target strength. Polar Sci 5:179–186. https://doi.org/10.1016/j.polar.2011.04.005
Baker AdC (1959) Distribution and life history of Euphausia triacantha. Discovery Rep XXIX: 309–340
Baker AdC, Boden BP, Brinton E (1990) A practical guide to the euphausiids of the world. British Museum (Natural History), London
Bargmann HE (1937) The reproductive system of Euphausia superba. Discovery Rep 14:327–349
Belcher A, Tarling G, Manno C, Atkinson A, Ward P, Skaret G, Fielding S, Henson S, Sanders R (2017) The potential role of Antarctic krill faecal pellets in efficient carbon export at the marginal ice zone of the South Orkney Islands in spring. Polar Biol 40:1–13. https://doi.org/10.1007/s00300-017-2118-z
Boden BP, Johnson MW, Brinton E (1955) Euphausiacea (Crustacea) of the North Pacific. Bull Scripps Inst Oceanogr 6:287–400
Croxall J, Reid K, Prince P (1999) Diet, provisioning and productivity responses of marine predators to differences in availability of Antarctic krill. Mar Ecol Prog Ser 177:115–131. https://doi.org/10.3354/meps177115
Cuzin-Roudy J, Amsler MO (1991) Ovarian development and sexual maturity staging in Antarctic Krill, Euphausia superba Dana (Euphausiacea). J Crust Biol 11:236–249. https://doi.org/10.1163/193724091X00059
Cuzin-Roudy J, Buchholz F (1999) Ovarian development and spawning in relation to the moult cycle in Northern krill Meganyctiphanes norvegica (Crustacea: Euphausiacea), along a climatic gradient. Mar Biol 133:267–281. https://doi.org/10.1007/s002270050466
Cuzin-Roudy J, Irisson J, Penot F, Kawaguchi S, Vallet C (2014) Southern Ocean Euphausiids. In: De Broyer C, Koubbi P (eds) Biogeographic Atlas of the Southern Ocean. Scientific Committee on Antarctic Research, Cambridge, UK, pp 309–320
Dalpadado P, Hop H, Rønning J, Pavlov V, Sperfeld E, Buchholz F, Rey A, Wold A (2016) Distribution and abundance of euphausiids and pelagic amphipods in Kongsfjorden, Isfjorden and Rijpfjorden (Svalbard) and changes in their relative importance as key prey in a warming marine ecosystem. Polar Biol 39:1765–1784. https://doi.org/10.1007/s00300-015-1874-x
Einarsson H (1942) Notes on Euphausiacea I-III: On the systematic value of the spermatheca, on sexual dimorphism in Nematoscelis, on the male in Bentheuphausia. Vidensk Medd fra Dansk naturh Foren 106:263–286
Endo Y (1989) Allometric differences observed on the same sized immature and mature males of the Antarctic krill (Euphausia superba Dana). Bull Plankt Soc Japan
Everson I (1987) Some aspects of the small scale distribution of Euphausia crystallorophias. Polar Biol 8:9–15. https://doi.org/10.1007/Bf00297158
Färber-Lorda J (1990) Somatic length relationships and ontogenic morphometric differentiation of Euphausia superba and Thysanoessa macrura of the Southwest Indian-Ocean During Summer (February 1981). Deep Sea Res Part A 37:1135–1143. https://doi.org/10.1016/0198-0149(90)90055-Z
Färber-Lorda J (1991) Multivariate approach to the morphological and biochemical differentiation of Antarctic krill (Euphausia superba and Thysanoessa macrura). Deep Sea Research Part A Oceanographic Research Papers 38:771–779
Färber-Lorda J, Beier E, Mayzaud P (2009) Morphological and biochemical differentiation in Antarctic krill. J Marine Syst 78:525–535. https://doi.org/10.1016/j.jmarsys.2008.12.022
Färber-Lorda J, Ceccaldi HJ (2020) Relationship of morphometrics, total carotenoids, and total lipids with activity and sexual and spatial features in Euphausia superba. Scientific reports 10:1–15. https://doi.org/10.1038/s41598-020-69780-8
Hamner WM (1984) Aspects of schooling of Euphausia superba. J Crust Biol 4(5):67–74. https://doi.org/10.1163/1937240x84x00507
Hamner WM, Hamner PP (2000) Behavior of Antarctic krill (Euphausia superba): schooling, foraging, and antipredatory behavior. Can J Fish AquatSci 57:192–202. https://doi.org/10.1139/cjfas-57-S3-192
Hill HJ, Trathan PN, Croxall JP, Watkins JL (1996) A comparison of Antarctic krill Euphausia superba caught by nets and taken by macaroni penguins Eudyptes chrysolophus: Evidence for selection? Mar Ecol Prog Ser 140:1–11. https://doi.org/10.3354/meps140001
Hiller-Adams P, Case J (1988) Eye size of pelagic crustaceans as a function of habitat depth and possession of photophores. Vision Res 28:667–680. https://doi.org/10.1016/0042-6989(88)90047-8
Hopkins T (1987) Midwater food web in McMurdo Sound, Ross Sea, Antarctica. Mar Biol 96:93–106. https://doi.org/10.1007/Bf00394842
James P (1973) Distribution of dimorphic males of three species of Nematoscelis (Euphausiacea). Mar Biol 19:341–347. https://doi.org/10.1007/BF00348905
Johnson ML, Tarling GA (2008) Influence of individual state on swimming capacity and behaviour of Antarctic krill Euphausia superba. Mar Ecol Prog Ser 366:99–110. https://doi.org/10.3354/meps07533
Kattner G, Hagen W (1998) Lipid metabolism of the Antarctic euphausiid Euphausia crystallorophias and its ecological implications. Mar Ecol Prog Ser 170:203–213. https://doi.org/10.3354/meps170203
Kawaguchi S, Kilpatrick R, Roberts L, King RA, Nicol S (2011a) Ocean-bottom krill sex J Plankt Res 33:1134–1138. https://doi.org/10.1093/plankt/fbr006
Kawaguchi S, Kilpatrick R, Roberts L, King RA, Nicol S (2011b) Ocean-bottom krill sex. J Plankton Res 33:1134–1138. https://doi.org/10.1093/plankt/fbr006
Kils U (1979) Swimming speed and escape capacity of Antarctic krill, Euphausia superba. Meeresforsch 27:264–266
Kiørboe T (2008) Optimal swimming strategies in mate-searching pelagic copepods. Oecologia 155:179–192. https://doi.org/10.1007/s00442-007-0893-x
Liszka C (2018) Zooplankton‐mediated carbon flux in the Southern Ocean: influence of community structure, metabolism and behaviour. PhD Thesis. Dept Environmental Sciences, Norwich, UK
Makarov RR, Denys CJ (1980) Stages of sexual maturity of Euphausia superba (BIOMASS Handbook). Scientific Committee for Antarctic Research, Cambridge
Mathew K (1980) Sexual dimorphism in Stylocheiron indicum Silas and Mathew (Crustacea: Euphausucea). J Mar Biol Assoc India 22:39–44
Mauchline J (1988) Egg and brood sizes of oceanic pelagic crustaceans. Mar Ecol Prog Ser 43:251–258. https://doi.org/10.3354/meps043251
Mauchline J, Fisher LR (1969) The biology of euphausiids. Adv Mar Biol 7:1–454
McLaughlin PA (1965) A redescription of the euphausiid crustacean. Nematoscelis difficilis Hansen Crustaceana 9(1):41–44
Miller D (1983) Variation in body length measurement of Euphausia superba Dana. Polar Biol 2:17–20. https://doi.org/10.1007/Bf00258280
Murphy DW, Webster DR, Kawaguchi S, King R, Yen J (2009) Locomotory biomechanics of Antarctic krill. Integr Comp Biol 49:E121–E121
Nemoto T (1966) Thysanoessa euphausiids, comparative morphology, allomorphosis and ecology. J Sci Rep Whales Res Inst 20:109–155
O’Brien DP (1987) Direct Observations of the Behavior of Euphausia superba and Euphausia crystallorophias (Crustacea, Euphausiacea) under Pack Ice During the Antarctic Spring of 1985. J Crust Biol 7:437–448. https://doi.org/10.2307/1548293
Ross R, Quetin L, Amsler M, Elias M (1987) Larval and adult Antarctic krill, Euphausia superba, winter-over at Palmer Station. Ant J, US 22:205–206
Ross RM, Quetin LB (2000) Reproduction in Euphausiacea. In: Everson I (ed) Krill: Biology, Ecology and Fisheries. Blackwell Science Ltd, Oxford, pp 150–181
Santora JA, Reiss CS, Loeb VJ, Veit RR (2010) Spatial association between hotspots of baleen whales and demographic patterns of Antarctic krill Euphausia superba suggests size-dependent predation. Mar Ecol Prog Ser 405:255–269. https://doi.org/10.3354/meps08513
Schmidt K, Atkinson A (2016) Feeding and food processing in Antarctic krill (Euphausia superba Dana). In: Siegel V (ed) Biology and Ecology of Antarctic Krill. Springer, pp 175–224
Siegel V (1982) Relationship of various length measurements of Euphausia superba Dana. Meeresforsch 29:114–117
Sogawa S, Sugisaki H, Tadokoro K, Ono T, Sato E, Shimode S, Kikuchi T (2017) Feeding habits of six species of euphausiids (Decapoda: Euphausiacea) in the northwestern Pacific Ocean determined by carbon and nitrogen stable isotope ratios. J Crust Biol 37:29–36. https://doi.org/10.1093/jcbiol/ruw014
Suh H-L, Choi S-D (1998) Comparative morphology of the feeding basket of five species of Euphausia (Crustacea, Euphausiacea) in the western North Pacific, with some ecological considerations. Hydrobiol 385:107–112. https://doi.org/10.1023/A:1003435622123
Sun S, Delamare W, Nicol S (1995) The compound eye as an indicator of age and shrinkage in Antarctic krill. Ant Sci 7:387–392. https://doi.org/10.1017/S0954102095000538
Tarling G, Hill S, Peat H, Fielding S, Reiss C, Atkinson A (2016) Growth and shrinkage in Antarctic krill Euphausia superba is sex-dependent. Mar Ecol Prog Ser 547:61–78. https://doi.org/10.3354/meps11634
Tarling GA (2003) Sex-dependent diel vertical migration in northern krill Meganyctiphanes norvegica and its consequences for population dynamics. Mar Ecol Prog Ser 260:173–188. https://doi.org/10.3354/meps260173
Tarling GA, Cuzin-Roudy J, Thorpe SE, Shreeve RS, Ward P, Murphy EJ (2007) Recruitment of Antarctic krill Euphausia superba in the South Georgia region: adult fecundity and the fate of larvae. Mar Ecol Prog Ser 331:161–179. https://doi.org/10.3354/meps331161
Tarling GA, Johnson ML (2006) Satiation gives krill that sinking feeling. Curr Biol 16:83–84. https://doi.org/10.1016/j.cub.2006.01.044
Tarling GA, Klevjer T, Fielding S, Watkins J, Atkinson A, Murphy E, Korb R, Whitehouse M, Leaper R (2009) Variability and predictability of Antarctic krill swarm structure. Deep Sea Res Part I 56:1994–2012. https://doi.org/10.1016/j.dsr.2009.07.004
Tarling GA, Shreeve RS, Hirst AG, Atkinson A, Pond DW, Murphy EJ, Watkins JL (2006) Natural growth rates in Antarctic krill (Euphausia superba): I. Improving methodology and predicting intermolt period. Limnol Oceanogr 51:959–972. https://doi.org/10.4319/lo.2006.51.2.0959
Tarling GA, Thorpe SE (2014) Instantaneous movement of krill swarms in the Antarctic Circumpolar Current. Limnol Oceanogr 59:872–886. https://doi.org/10.4319/lo.2014.59.3.0872
Tarling GA, Thorpe SE, Fielding S, Klevjer T, Ryabov A, Somerfield PJ (2018) Varying depth and swarm dimensions of open-ocean Antarctic krill Euphausia superba Dana, 1850 (Euphausiacea) over diel cycles. J Crust Biol 38:716–727. https://doi.org/10.1093/jcbiol/ruy040
Thomas P, Ikeda T (1987) Sexual regression, shrinkage, rematuration and growth in spent females Euphausia superba in the laboratory. Mar Biol 95:357–363. https://doi.org/10.1007/BF00409565
Watkins JL, Morris DJ, Ricketts C, Murray AWA (1990) Sampling biological characteristics of krill: effect of heterogenous nature of swarms. Mar Biol 107:409–415. https://doi.org/10.1007/BF01313422
Acknowledgements
We thank the officers and crew of the RRS John Biscoe and RRS James Clark Ross for their assistance in the collection of specimens. We are also grateful to laboratory supervisors Barry Penrose from the University of Hull and Paul Geissler and Guy Hillyard at BAS for facilitating collection of measurement data. GAT carried out this work as part of the Ecosystems programme at the British Antarctic Survey. We are grateful for the comments and suggestions of the three anonymous reviewers in helping to improve this manuscript.
Funding
The research was supported by the British Antarctic Survey, Natural Environment Research Council and by the University of Hull.
Author information
Authors and Affiliations
Contributions
CH, MLJ and GAT devised this study with supporting ideas from JFL. All measurements were performed by CH. GAT wrote the manuscript with support from all authors.
Corresponding authors
Ethics declarations
Conflicts of interest
We declare no conflicts of interest in the production of this work.
Ethical approval
All work was completed in compliance with British Antarctic Survey (BAS) procedures, following the Antarctic Treaty Environmental Protocol (1996), which requires the prior assessment of all activities in the Antarctic Treaty Area, and is applied by BAS with equal rigour to South Georgia. Work on Antarctic krill (Euphausia superba) and other euphausiid species is exempt from the UK Animals (Scientific Procedures) Act 1986, but all work was compliant with recommended procedures in the handling and treatment of specimens.
Consent to participate
We declare all relevant parties consented to participate in this study.
Consent for publication
We declare all relevant parties have consented to the publication of this work.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
G. A. Tarling and C. Hobbs are joint first authors
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Tarling, G., Hobbs, C., Johnson, M. et al. Comparative morphology of Southern Ocean Euphausia species: ecological significance of sexual dimorphic features. Polar Biol 43, 2043–2058 (2020). https://doi.org/10.1007/s00300-020-02764-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00300-020-02764-6