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Energy depletion of embryos and yolk-sac feeding larvae of the liparid snailfish Careproctus pallidus (Vaillant 1888)

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Abstract

The snailfish, Careproctus pallidus, is a liparid fish that spawns within the branchial chambers of the king crab Lithodes santolla and develops its embryonic stages inside the chambers until it forms a well-developed free-living yolk-sac feeding larvae hatch. The aim of this work was to explore the decrease in energy content of C. pallidus during its early development. Five egg masses with embryos in cleavage stage were extracted from the branchial chambers of five different king crabs and kept in aquaria through hatching until complete absorption of the yolk-sac. To monitor energy content during development, subsamples of eggs (in cleavage, tail-bud, and late embryo stages) and larvae [1, 13, 20–22 and 24–26 days post-hatch (DPH)] were removed. Each stage of development (eggs and larvae) was weighed (wet weight), counted (N) and dried at 60°C. Both energy density (ED) and energy content (EC) per individual (egg or larva) were measured. Significant differences in ED and ECi were observed among the early stages of C. pallidus, although pairwise comparisons differed. From the earliest developmental stage (cleavage) to a larva of 24–26 DPH, the ED of C. pallidus decreased by approximately 40% and the ECi by 87%. Compared with other marine fish species, C. pallidus seems to begin life with lower energy if size of egg, incubation period, and degree of development until it reached the hatching stage are considered. Thus, the energy allocation during the early development of this liparid fish with a particular reproductive strategy is discussed.

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References

  • Armstrong JB, Schindler DE (2013) Excess digestive capacity in predators reflects a life of feast and famine. Nature 476:84–88

    Article  CAS  Google Scholar 

  • Balbontin C, Campodonico G, Guzman M (1979) Description of egg and larvae of species of Careproctus (Pisces: Liparidae) commensals of Paralomis granulosa and Lithodes antarctica (Crustacea: Lithodidae). Ans Inst Pat Punta Arenas (Chile) 10:235–243

    Google Scholar 

  • Brodersen J, Nilsson PA, Hansson LA, Skov C, Brönmark C (2008) Condition-dependent individual decision-making determines cyprinid partial migration. Ecology 89:1195–1200

    Article  PubMed  Google Scholar 

  • Bruno DO, Victorio MF, Acha EM, Fernández DA (2018) Fish early life stages associated with giant kelp forests in sub-Antarctic coastal waters (Beagle Channel, Argentina). Polar Biol 41:365–375

    Article  Google Scholar 

  • Dinno A (2017) dunn.test: Dunn's test of multiple comparisons using rank sums. R package version 1.3.5. https://CRAN.R-project.org/package=dunn.test

  • Eldridge MB, Echeverria T, Whipple JA (1977) Energetics of Pacific herring (Clupea harengus pallasi) embryos and larvae exposed to low concentrations of benzene, a monoaromatic component of crude oil. Trans Am Fish Soc 106:452–461

    Article  CAS  Google Scholar 

  • Ficke AD, Myrick CA, Hansen LJ (2007) Potential impacts of global climate change on freshwater fisheries. Rev Fish Biol Fish 17:51–613

    Article  Google Scholar 

  • Finn RN, Henderson JR, Fyhn HJ (1995) Physiological energetics of developing embryos and yolk-sac larvae of Atlantic cod (Gadus morhua). II. Lipid metabolism and enthalpy balance. Mar Biol 124:371–379

    Article  Google Scholar 

  • Froese R, Pauly D (eds) (2018) FishBase. World Wide Web electronic publication. https://www.fishbase.de/. Accessed 30 Jan 2019

  • Fuiman LA (2002) Chapter 1: special considerations of fish eggs and larvae. In: Fuiman LA, Werner RG (eds) Fishery science: the unique contributions of early life stages. Blackwell Science, Oxford, pp 1–32

    Google Scholar 

  • Gundry HA, Harrop D, Head AJ, Lewis GB (1969) Thermodynamic properties of organic oxygen compounds 21: enthalpies of combustion of benzoic acid, pentan-1-ol, octan-1-ol, and hexadecan-1-ol. J Chem Thermodyn 1:321–332

    Article  CAS  Google Scholar 

  • Houde ED (2002) Chapter 3: mortality. In: Fuiman LA, Werner RG (eds) Fishery science: the unique contributions of early life stages. Blackwell Science, Oxford, pp 64–87

    Google Scholar 

  • Johnson TB, Mason DM, Schram ST, Kitchell JF (1999) Ontogenetic and seasonal patterns in the energy content of piscivorous fishes in Lake Superior. J Great Lakes Res 25:275–281

    Article  CAS  Google Scholar 

  • Johnson BM, Pate WM, Hansen AC (2017) Energy density and dry matter content in fish: New observations and an evaluation of some empirical models. T Am Fish Soc 146:1262–1278

    Article  Google Scholar 

  • Jonsson B, Jonsson N (1993) Partial migration: niche shifts versus sexual maturation in fishes. Rev Fish Biol Fish 3:348–365

    Article  Google Scholar 

  • Jørgensen C, Ernande B, Fiksen Ø, Dieckmann U (2006) The logic of skipped spawning in fish. Can J Fish Aquat Sci 63:200–211

    Article  Google Scholar 

  • Kamler E (2005) Parent-egg-progeny relationships in teleost fishes: an energetics perspective. Rev Fish Biol Fish 15:399–421

    Article  Google Scholar 

  • Kamler E (2008) Resource allocation in yolk-feeding fish. Rev Fish Biol Fisher 18:143–200

    Article  Google Scholar 

  • Kunz YW (2004) Developmental biology of teleost fishes. Springer, Netherlands

    Book  Google Scholar 

  • Lasker R (1962) Efficiency and rate of yolk utilization by developing embryos and larvae of the Pacific sardine Sardinops caerulea (Girard). J Fish Res Board Can 19:867–875

    Article  Google Scholar 

  • Nelson JS, Grande TC, Wilson MVH (2016) Fishes of the world. Wiley, New Jersey

    Book  Google Scholar 

  • Ostrowski AC, Divakaran S (1991) Energy substrates for eggs and prefeeding larvae of the dolphin Coryphaena hippurus. Mar Biol 109:149–155

    Article  Google Scholar 

  • Post JR, Evans DO (1989) Size-dependent overwinter mortality of young-of-the-year Yellow Perch (Perca flavescens): laboratory, in situ enclosure, and field experiments. Can J Fish Aquat Sci 46:1958–1968

    Article  Google Scholar 

  • Post JR, Parkinson EA (2001) Energy allocation strategy in young fish: allometry and survival. Ecology 82:1040–1051

    Article  Google Scholar 

  • R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Somerton DA, Donaldson W (1998) Parasitism of the golden king crab, Lithodes aequispinus, by two species of snailfish, genus Careproctus. Fish Bull 96:871–888

    Google Scholar 

  • Stein DL (2005) Descriptions of four new species, redescription of Paraliparis membranaceus, and additional data on species of the fish family Liparidae (Pisces, Scorpaeniformes) from the west coast of South America and the Indian Ocean. Zootaxa 1019:1–25

    Article  Google Scholar 

  • Thorpe JE (1994) Reproductive strategies in Atlantic Salmon, Salmo salar L. Aquac Fish Manag 25:77–87

    Google Scholar 

  • Trabelsi A, Jaworski A, Kamler E, Gardeur JN, Teletchea F, Ayadi H, Fontaine P (2016) The effect of hatching time on the bioenergetics of northern pike (Esox lucius) larvae from a single egg batch during the endogenous feeding period. Fish Physiol Biochem 42:593–606

    Article  CAS  PubMed  Google Scholar 

  • Vanella FA, Fernández DA, Romero MC, Calvo J (2007) Changes in the fish fauna associated with a sub-Antarctic Macrocystis pyrifera kelp forest in response to canopy removal. Polar Biol 30:449–457

    Article  Google Scholar 

  • Wieser W (1995) Energetics of fish larvae, the smallest vertebrates. Acta Physiol Scand 154:279–290

    Article  CAS  PubMed  Google Scholar 

  • Wuenschel MJ, Jugovich AR, Hare JA (2006) Estimating the energy density of fish: the importance of ontogeny. Trans Am Fish Soc 135:379–385

    Article  Google Scholar 

  • Yúfera M, Parra G, Santiago R, Carrascosa M (1999) Growth, carbon, nitrogen and caloric content of Solea senegalensis (Pisces: Soleidae) from egg fertilization to metamorphosis. Mar Biol 134:43–49

    Article  Google Scholar 

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Acknowledgements

We are grateful to C.P. Alonso, M. Torres, O. Florentín, H. Sacristán, and P. Di Salvatore for providing the eggs’ masses extracted from the branchial chambers of Lithodes santolla specimens. We also thank Dieter Piepenburg and two anonymous reviewers for their useful comments on an earlier draft, which greatly improved this work. This study was supported by grants from the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET-Argentina), PIP 0440 2016–2018; and the Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT-FONCyT, Argentina), PICT 1804/2014 and PICT 0900/2015.

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Correspondence to Daniel O. Bruno.

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All sampling procedures and experimental manipulations follow the guidelines approved by the Universidad de Buenos Aires from Argentina (Facultad de Ciencias Exactas y Naturales, Bioterio Central, https://exactas.uba.ar/cicual/).

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Bruno, D.O., Rojo, J.H. & Boy, C.C. Energy depletion of embryos and yolk-sac feeding larvae of the liparid snailfish Careproctus pallidus (Vaillant 1888). Polar Biol 42, 1199–1204 (2019). https://doi.org/10.1007/s00300-019-02500-9

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