Elsevier

Aquaculture

Volume 503, 30 March 2019, Pages 583-588
Aquaculture

Evaluation of physiological stress and nutritional deficiency related to cannibalism in early paralarvae of Patagonian red octopus Enteroctopus megalocyathus

https://doi.org/10.1016/j.aquaculture.2018.12.087Get rights and content

Highlights

  • Nutritional deficiency would not be a factor that start cannibalism.

  • The onset of cannibalism would be related to stress at high density.

Abstract

Patagonian red octopus Enteroctopus megalocyathus is one of the two octopuses' species of great commercial importance in Chile. At the present time, the life cycle of this species in captivity has been closed at experimental level; however, high mortalities at the early paralarvae stage are a limiting factor for attaining sustainable production. Cannibalism has been identified as one of the main mortality causes at the early paralarvae rearing. Stress has been proposed as an important cause of cannibalism in cephalopods. Likewise, nutritional deficiency has been suggested as a potential cause to onset cannibalism. However, neither of both factors has been directly assessed in cephalopod paralarvae. In the present study, we aimed to elucidate if physiological stress due to a food shortage and/or to a high rearing density of paralarvae trigger cannibalism in E. megalocyathus. An experiment was carried out with newly hatched paralarvae, under conditions that trigger cannibalism with densities of 10 and 15 paralarvae L−1 combined with two measures of prey availability: 0 and 2 prey paralarva−1 day−1. Paralarvae alone in the aquarium fed ad libitum was used as a control to avoid cannibalism. Nutritional status was assessed as the total protein and energy content per paralarvae; and the 70 kD heat shock protein (HSP70) transcript level was used as a bioindicator of physiological stress, documented as a suitable stress biomarker for cephalopods. No differences were observed between the treatments and control in the absolute protein levels and energy content. There was a strong induction in HSP70 transcriptional level when high density and prey availability where combined, proving that there are only a few paralarvae rearing combinations that cause critical stress and trigger HSP70 transcription. In experimental conditions, nutritional status indicators showed that early paralarvae, with similar reserves of protein and energy, exhibited cannibalism. Results suggest that mortality as well as cannibalism is associated with competition for prey and with nutritional and energy imbalance due to food shortage that determines the expression of the related stress gene.

Introduction

The cephalopod rearing has not attained commercial production because several constraints, and the reliable production of viable numbers of juveniles is one of them (Vidal et al., 2014). In Chile, there are two species of octopuses with commercial importance, which are cought through artisanal fishing. One of them is the Patagonian red octopus Enteroctopus megalocyathus, and recently its life cycle under captivity has been completed studied at experimental level (Uriarte et al., 2017). However, the high mortality that occurs in the paralarvae phase, reaching 70–80% in the first 30 days (Farías et al., 2016), makes difficult to obtain the necessary juveniles for scaling its production in captivity (Uriarte and Farías, 2014). Among the causes of this high mortality, cannibalism accounts for up to 60% during the first 10–15 days post-hatching (Uriarte et al., 2013).

Cannibalism is likely to be an important mechanism of density-dependent regulation in aquatic animals, including cephalopods. Among cephalopods, E. megalocyathus is classified as a specie with high levels of cannibalism (Ibañez and Keyl, 2010). External factors that trigger cannibalism have been studied in several aquatic species; where population density, and the quality, variability and amount of available food have been proposed as the main causes (Fox, 1975; Polis, 1981; Hecht and Pienaar, 1993; Abdussamad and Thampy, 1994). Physiological stress has also been pointed as a potential trigger of cannibalism in animal kingdom (Fox, 1975), and in the case of cephalopods (Ibañez and Keyl, 2010); however, this factor has not been directly assessed. To the best of our knowledge, only one study has evaluated potential triggering factors of cannibalism in the paralarvae of small octopus Robsonella fontaniana, under captivity conditions (Miranda et al., 2011). These authors observed that the paralarvae density (independent of food availability) was the main cause of cannibalism, being only in the lowest density where cannibalism was absent. In a previous study on cannibalism of E. megalocyathus paralarvae until 30 post-hatching (Espinoza, 2018) it was determined that rearing conditions of paralarvae density and food availability that decrease the paralarvae survival were 15 paralarvae L−1 and 0 and 2 preys paralarva−1 day−1 as shown in Fig. S1.

In the present study we compared the physiological stress levels, measuring 70 kD heat shock protein (HSP70) transcriptional levels, in paralarvae where starting signs of cannibalism were observed versus control where cannibalism was absent. Heat shock proteins (HSPs) are molecular chaperones that perform numerous functions in cells (Mosser et al., 2000; Bukau and Horwich, 1998). Because they protect the three-dimensional structure and function of other proteins, HSP70 is usually induced under several environmental stress conditions. Looking for stress biomarkers, HSPs has been used this way in several mollusks (e.g., Jeno and Brokordt, 2014), including cephalopods (Trübenbach et al., 2013; Repolho et al., 2014; Capaz et al., 2017; Garrido et al., 2017). The evaluation of HSP70 at protein level usually do not discriminate between inducible and constitutive isoforms (Trübenbach et al., 2013), thus in the current study it was used the transcriptional level of an inducible HSP70 as indicator of physiological stress. In the present study, we aimed to elucidate if physiological stress due to a food deprivation and/or to a high rearing density of paralarvae is a factor that triggers cannibalism in E. megalocyathus.

Nutritional deficiency has also been suggested as potential cause to onset cannibalism in carnivorous early juveniles of fish (Hecht and Pienaar, 1993) and in Octopus bimaculoides paralarvae (Solorzano et al., 2009). However, in the latter study this parameter was not directly quantified. Therefore, we further assessed the paralarvae nutritional condition from treatments where cannibalism was starting and where this was absent, in order to associate this status with the beginning of cannibalism in E. megalocyathus early paralarvae.

Section snippets

Paralarvae rearing and cannibalism experiments

Enteroctopus megalocyathus females and males were captured in their natural environment at Hueihue, De Los Lagos region of Chile (42°S), and transferred to 200 L conditioning tanks in the Marine Invertebrate Hatchery at Universidad Austral de Chile (HIM-UACH). The methodology described by Uriarte et al. (2014) was followed for adult maintenance, reproduction, and egg brooding, until paralarvae hatching. Briefly, broodstock was conditioned during 4 months at 12 °C in 700 L tanks with sea water

Results and discussion

Regardless of the density and food availability under which Enteroctopus megalocyathus paralarvae were maintained, in general, cannibalism started early during the first 6 DAH (days after hatching) in 7 of the 12 total aquaria. There were no significant differences in mortality [Kruskall-Wallis H (3, N = 12) =1.91, P = .5903] and cannibalism onset [Kruskall-Wallis H (3, N = 12) =4.75, P = .1904] between treatments. The most delayed cannibalism onset was observed on the treatment of 10

Acknowledgements

We are very grateful for the technical support of Pablo Garcés, Matías Vega and Augusto Vargas. This work was supported by the doctoral scholarship CONICYT21140393 to V. Espinoza; and by the grants FONDECYT1131094 to I. Uriarte and FONDAP15110027 to A. Romero.

References (36)

  • E. Catalán

    Evaluation of gene expression of the immune system in organs of Patagonian red Octopus Enteroctopus megalocyathus by real-time PCR

  • P. Domingues et al.

    Alimentación y Nutrición de Moluscos Cefalópodos: Avances Recientes y Perspectivas Futuras

  • V. Espinoza

    Cannibalism in Patagonian red octopus, Enteroctopus megalocyathus, paralarvae reared in controlled environment

  • V. Espinoza et al.

    Effect of starvation on the performance of baby octopus (Robsonella fontaniana) paralarvae

    Aquac. Res.

    (2017)
  • A. Farías et al.

    Effect of zooplankton as diet for the early paralarvae of Patagonian red octopus, Enteroctopus megalocyathus, grown under controlled environment

    Aquac. Nutr.

    (2016)
  • L.R. Fox

    Cannibalism in natural populations

    Annu. Rev. Ecol. Syst.

    (1975)
  • J. Guillaume et al.

    Nutrición y alimentación de peces y crustáceos

    (2004)
  • T. Hecht et al.

    A review of cannibalism and its implications in fish larviculture

    J. W. Aquac. Soc.

    (1993)
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