Elsevier

Aquaculture

Volumes 424–425, 20 March 2014, Pages 158-166
Aquaculture

Key aspects of egg incubation in Patagonian red octopus (Enteroctopus megalocyathus) for cultivation purposes

https://doi.org/10.1016/j.aquaculture.2013.12.039Get rights and content

Highlights

  • Out of 16 conditioned females, 69% laid eggs and 36.4% hatched paralarvae

  • At stage VII it is conspicuous that the eggs were fertilized and the embryos are alive

  • Embryos showed an exponential growth rate fueled by protein and lipids of yolk-sac

  • Saturated fatty acids were the most consumed during embryonic development (69.77%)

  • n-3 PUFA were 5 times more consumed than the n-6 PUFA in E. megalocyathus embryos

Abstract

Patagonian red octopus, Enteroctopus megalocyathus, is a valuable resource of the artisanal fishery in southern Chile, however, due to overfishing the E. megalocyathus fishery was banned for 3 years in Chile, therefore its cultivation became a target for the Chilean aquaculture. The rearing of octopus paralarvae is currently the biggest bottleneck for the aquaculture of merobenthic octopus species. Besides, the embryos of Patagonian red octopus require 5 months for embryonic development, a very long period of incubation that involves high risks of contamination and detachment, therefore, little advance has been achieved in the larviculture of this species. This study represents the first investigation to evaluate the embryo viability, embryo morphometrics, embryo growth and the biochemical composition and fatty acid dynamics during early development of Patagonian red octopus under captive reproduction. The eggs obtained from broodstock conditioning were incubated under maternal care and the embryos were studied until hatching in their main morphometric and biochemical features during development. Most females showed a tending behavior of the eggs along the incubation period, losing between 40 and 100% of the eggs in the first 3 months of incubation. The results of incubation at 11 °C were successful observing the complete gastrulation, onset of organogenesis and first inversion about 48 days after spawning, the complete organogenesis and second reversion were observed about 152 days after spawning, hatching was observed 168 days after spawning without any external yolk-sac on the hatched paralarvae. During their development, embryos showed an exponential growth rate in length and weight, fueled by the protein and lipids of external yolk-sac. Metabolism of lipids showed over a 70% depletion of the saturated fatty acids (SFA), and the fatty acids 16:1, 18:2n-6, 18:3n-3 and 22:5n-3 during development. The DHA/EPA ratio remained constant throughout the incubation period. The early embryos showed a fatty acid profile dominated by both SFA and highly unsaturated fatty acids (HUFA), while the newly hatched paralarvae showed a profile dominated by HUFA.

Introduction

Over the last few years, aquaculture research in Chile has been strongly focused towards the diversification of species that have problems in fisheries and are demanded in the global markets. Two Chilean octopus species have been investigated as serious candidates for aquaculture in terms of their biological and market potential, one of them is the Changos octopus (Octopus mimus), found from Tumbes, Northern Perú (3° 34′ 00″S) to San Vicente Bay in Chile (33° 37′ 60″N), and the other is found in Southern Chile (from 34° 20´S to 72° 00´W to the Beagle Channel in Chile, up to Southern Argentina), known as Patagonian red octopus, Enteroctopus megalocyathus (Cardoso et al., 2004, Ibáñez and Chong, 2008, Ortíz et al., 2006, Rocha and Vega, 2003). In November 2008, the E. megalocyathus fishery was banned for 3 years in Chile, a reason that has made their aquaculture an important issue (Uriarte et al. 2011).

According to Uriarte et al. (2011), the embryo incubation is a bottleneck for the aquaculture of this particular species, and this difficulty adds up to the problem of cultivating paralarvae of developing octopuses with merobenthic development (Berger, 2010, Iglesias et al., 2007).

It is highly likely that E. megalocyathus might be a species that stems from a predecessor of direct development belonging to clade 5 as proposed by Ibáñez et al. (2013) that re-evolved into a species with pelagic paralarva, therefore, according to these authors it should be a species with a low to moderate fertility, large eggs and a paralarva that should be very large, with ambiguous swimming behavior in between pelagic and benthic. The information available from the literature shows that E. megalocyathus fits well with the predictions of Ibáñez et al. (2013) because under culture conditions this species has shown moderate spawning that does not exceed 5000 eggs sized approximately 10 mm (Uriarte et al., 2013), the hatched paralarvae exceed 10 mm and they present a swimming behaviour that ranges in between pelagic and benthic which has been described as suprabenthic hatchlings by Ortíz et al. (2006) and planktonic hatchlings Enteroctopus-type by Villanueva and Norman (2008).

The embryonic development and maturation of the embryo of E. megalocyathus to generate a large hatching paralarva have not been achieved easily; there are descriptions of 1) hatchlings from embryonated eggs captured on ground and reared for 88 days in laboratory at 11.7 °C (Ortíz et al., 2006), 2) critical bacterial infection during the embryonic period under controlled conditions (Uriarte et al., 2011) and 3) absence of embryonic development in 12 clutches obtained from broodstock conditioning under controlled conditions (Farías et al., 2011). Embryo development depends on the nutritional reserves of the egg, making relevant the studies on feeding females during the reproductive conditioning period that showed a strategy to maintain the quality of eggs under unfavorable environmental conditions (Farías et al., 2011). Sargent et al. (1999) have shown that in cold and hard environments fish larvae hatch with a high lipid content to ensure the survival, which could be the case for E. megalocyathus paralarvae hatching in the southern waters of South America. In cold marine waters, fish larvae show essential requirements of highly unsaturated fatty acids (HUFA i.e.,fatty acids with 20 or more carbon atoms and 3 or more double bonds) such as arachidonic acid (AA), eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), to maintain high DHA for neural development and to encourage a best species specific ratio EPA:AA affecting eicosanoid actions (Sargent et al., 1999), this would also be expected from newly hatched paralarvae of E. megalocyathus in Patagonic waters of South America.

This study aimed to characterize the morphometric variations and nutritional reserves of E. megalocyathus embryos from spawning to paralarvae hatching, obtained under controlled conditions of reproduction, to improve both egg incubation protocols obtaining development indicators over the five month period of embryonic life, and the future formulation of broodstock diets for more efficient captive reproduction of Patagonian red octopus E. megalocyathus.

Section snippets

Conditioning of females

16 females weighing 0.79 kg (± 0.079) and 12 males weighing 0.60 kg (± 0.031) of E. megalocyathus were captured in their natural environment at Hueihue, Xth region of Chile (42° lat.S), and transferred to conditioning tanks in the Marine Invertebrate Hatchery at Universidad Austral de Chile (HIM-UACH). The octopuses were kept in individual 100 L tanks using a circulation system with 5 μm-filtered and UV-sterilized sea water, and a 5 to 10% daily water exchange. Salinity was kept at 30‰ and the

Results

Out of 16 females that conditioned, 11 had laid eggs on the walls of their dens (69%) and four clutches showed complete embryonic development (36.4%). The average absolute fecundity was 2095 eggs (± 425) and average relative fecundity was 924 eggs kg 1 198). The clutches consisted of bunch sets of 34 eggs (± 3, n = 110 bunch sets). Two clutches of eggs were totally swept by the females (18.2% of egg clutches). Five clutches did not show any organogenesis signs (45.4%). From 4 egg clutches with

Discussion

This study represents the first investigation to evaluate the viability, morphometrics, growth and the biochemical composition and fatty acids dynamics during embryo development of Patagonian red octopus under captive reproduction.

The tending and loosening of eggs in most observed spawnings in this study could be a normal maternal behavior to remove contaminated eggs. The fact that some females lost all the laid eggs could be a response to stress caused on them by the sampling of eggs.

The

Acknowledgments

This study was supported by FONDEF D09 I1153 and FONDECYT 1131094. We would like to thank the technical support from Jessica Dörner.

References (31)

  • E.G. Bligh et al.

    A rapid method of total lipid extraction and purification

    Can. J. Biochem. Phys.

    (1959)
  • S.V. Boletzky

    Biology of early life in cephalopod molluscs

    Adv. Mar. Biol.

    (2003)
  • F. Cardoso et al.

    Observaciones sobre la biología de Octopus mimus (Cephalopoda: Octopoda) en la costa Peruana

    Rev. Peru. Biol.

    (2004)
  • H. Castro et al.

    Descripción del desarrollo embrionario y paralarvario de Octopus mimus (Gould, 1852) (Mollusca: Cephalopoda) en cautiverio

    Estud Oceanol.

    (2002)
  • J. Chong et al.

    Estudio biológico pesquero del recurso pulpo en la X y XI regiones, Fondo de Investigación pesquera

    Tech. Rep. FIP

    (1999)
  • Cited by (0)

    View full text