Changes in behavioural patterns from swimming to clinging, shelter utilization and prey preference of East Asian common octopus Octopus sinensis during the settlement process under laboratory conditions

https://doi.org/10.1016/j.jembe.2021.151537Get rights and content

Highlights

  • Behaviour during the day shifted rapidly from swimming to clinging.

  • Swimming continued at night even after swimming during the day had ceased.

  • Frequency of shelter-utilization behaviour increased gradually with growth.

  • Shift of feeding habit from planktivorous to benthivorous was also gradual.

  • Octopus sinensis may require a considerable period of time to complete settlement.

Abstract

Settlement is the process whereby benthic octopuses with a planktonic paralarval phase make a behavioural change from being active swimmers to assume adult life on the seabed. This process is poorly understood, mainly because octopus juveniles are highly cryptic in the natural habitat and they lack any distinct morphological changes (i.e. metamorphosis) in concert with settlement. To investigate behaviour during the settlement process, ontogenetic changes in swimming, clinging and shelter-utilizing behaviours were examined during both day- and night-time using laboratory-raised East Asian common octopus, Octopus sinensis, aged from 10 to 28 days after hatching (ranging from 1.7 to 16.4 mg mean dry weight, DW). The accompanying change in feeding habit from planktivorous to benthivorous was assessed by comparing rates of consumption of planktonic zoea (of the swimming crab Portunus trituberculatus) and benthic juveniles of the Manila clam, Ruditapes philippinarum. During the daytime, octopus behaviour changed rapidly from swimming to clinging onto the surface of the wall and bottom of the test tank during growth from 3 to 9 mg DW. At night, the frequency of clinging behaviour increased along with growth but the behavioural change progressed more slowly, indicating a tendency to continue swimming during darkness. Shelter utilization during the day commenced mainly after reaching 8 mg DW, after which shelter use gradually increased with growth. In contrast, shelter utilization at night was rarely observed throughout the experiment. Regarding octopus prey preference, consumption of clam juveniles increased with growth while zoeae consumption remained constant. The increase in clam consumption, however, was gradual, indicating that the shift of feeding habit from planktivorous to benthivorous is by no means an abrupt transition. These results indicate that O. sinensis requires a considerable period of time to complete the transition to benthic life. The alternating behaviours of diurnal clinging and nocturnal swimming in the water column may facilitate safe migration of the octopuses from the location to which they have been passively advected towards a more suitable benthic habitat while minimizing their exposure to visual predators. Since shelter utilization and feeding on bivalves are likely to require the use of a certain degree of force and complex coordination of the arms and suckers, the extended, gradual increase in shelter utilization frequency and clam consumption may be attributable to the degree of arm and sucker development.

Introduction

For marine benthic invertebrates with a planktonic larval phase, settlement is a pivotal event connecting two distinct life-history phases as plankton and benthos (Rodríguez et al., 1993). Since habitat conditions are quite different between these phases, the behavioural characteristics of such animals require dramatic change in order to assume the benthic phase of life in a short time at the end of the larval phase. These behavioural changes may include descent in the water column, migration to a suitable settlement habitat, clinging to bottom substrate, and a shift of feeding habit from planktivore to benthivore, detritivore or filter feeder (Rodríguez et al., 1993; Hunt and Scheibling, 1997).

Many benthic invertebrates such as crustaceans, polychaetes, echinoderms, bivalves and gastropods have a planktonic phase and most of them exhibit massive morphogenetic change (metamorphosis) from larval to adult-like juvenile forms, to achieve the required rapid shifts of multiple traits in concert with settlement (Underwood and Fairweather, 1989; Jackson et al., 2002). Settlement success is also recognized as one of the major determinants of the population dynamics of such animals, because mortality rates during pre- and post-settlement periods (i.e. during the transition phase from plankton to benthos) are generally high (Underwood and Fairweather, 1989; Rodríguez et al., 1993; Hunt and Scheibling, 1997; Jackson et al., 2002; Freschetti et al., 2003). It can be expected that newly-settled juveniles suffer the risk of food limitation and predation due to their small size and immature performance as benthic organisms, while larger, pre-settled, descending larvae may also be noticeable by abundant suprabenthic predators. Furthermore, pre-settled larvae need to explore and migrate from the place where they were passively advected by ocean currents during their planktonic life to a habitat that is acceptable for following a successful juvenile benthic life (Rodríguez et al., 1993; Hunt and Scheibling, 1997; Metaxas, 2001). In this regard, ontogenetic changes in behaviour related to migration, avoidance of predation, and shifts in feeding habit during pre- and post-settlement periods are keys to understanding the effects of settlement success on population dynamics.

Many species of benthic octopus have an initial planktonic form, known as a ‘paralarva’ (Young and Harman, 1988), before taking up a benthic life (Villanueva and Norman, 2008; Villanueva et al., 2016). Unlike other marine benthic invertebrates, cephalopods show only gradual morphogenetic changes between hatching and juvenile-adult forms, with positive allometric arm growth, serial addition of new suckers on the arms, chromatophore genesis, and development of digestive system, but they lack any abrupt morphological change: that is, there is no true metamorphosis (Itami et al., 1963; Takeda, 1990; Okumura et al., 2005a; Villanueva and Norman, 2008; López-Peranza et al., 2014; Fernández-Gago et al., 2017). This absence of metamorphosis makes it difficult to clearly define the settlement timing of benthic octopuses. In addition, newly-settled juveniles are highly cryptic in the natural habitat (presumably because of their burrowing behaviour, excellent camouflage and small body size), so there are very few reports providing information about the settlement process of octopuses in the wild (Ambrose, 1988; Villanueva and Norman, 2008).

The East Asian common octopus, Octopus sinensis d'Orbigny, 1841, is one of the well-known benthic octopuses with a paralarval phase, distributed throughout the temperate northwestern Pacific Ocean (Gleadall, 2016). This octopus is an important fishery resource which has been heavily exploited by humans and has long attracted attention as a target for aquaculture, and much intensive effort has been expended on developing paralarval rearing technology in this and closely related species such as the Atlantic and Mediterranean common octopus, Octopus vulgaris (Itami et al., 1963; Villanueva, 1995; Villanueva et al., 1995; Iglesias et al., 2007; Sauer et al., 2020).

For these common octopuses, some information regarding settlement is available based on observations of laboratory-raised animals. Villanueva et al. (1995) reported that swimming performance of O. vulgaris increases with growth but reaches its maximum before the end of the planktonic phase and settlement commences when they reach a size of 7.5 mm mantle length, with the onset of crawling behaviour on the bottom of the rearing tank. They then completed the transition to benthic phase at 173 mg wet weight (Villanueva, 1995). Okumura et al. (2005b) reported that clinging behaviour on the tank wall was observed in O. sinensis paralarvae at 3.6–4.3 mg dry weight (DW) and they settled on the tank bottom at 6.2 mg DW.

Regarding migration during the pre-settlement phase, it was demonstrated that paralarvae of O. sinensis reaching the end of the planktonic phase (approximately 5 mg DW) exhibit characteristic behaviour alternating between diurnal descent swimming with temporal clinging and nocturnal upward swimming in the water column, indicating that they are preparing for settlement during the day and migrating to the settlement habitat at night (Dan et al., 2020). Recently-settled juveniles exhibit strong negative phototaxis and utilize shelters such as holes and gastropod shells (Itami et al., 1963; Villanueva, 1995).

Considering feeding habits, common octopus paralarvae are known to prey mostly on decapod crustacean larvae in the natural habitat (Roura et al., 2012; Olmos-Pérez et al., 2017), and the efficacy of decapod crustacean zoeae as feed for paralarvae has also been confirmed through rearing trials (Itami et al., 1963; Villanueva, 1994; Iglesias et al., 2014; Roo et al., 2017; Garrido et al., 2016; Nande et al., 2017; Dan et al., 2019). After settlement, juveniles search for prey on the tank bottom and the incidence of cannibalism intensifies, indicating that the feeding habit shifts to benthivorous, corresponding to that of the adult as a predator of various benthic animals (Itami et al., 1963; Hamada, 1974; Smale and Buchan, 1981; Mather and O'Dor, 1991; McQuaid, 1994; Fiorito and Gherardi, 1999; Villanueva and Norman, 2008). Thus, observations of laboratory-raised animals have provided reliable ecological information about octopus settlement, which is very difficult to obtain by field research, and has greatly improved our understanding of octopus life history traits. Nevertheless, more quantitative data are required to understand when and how octopuses change their behaviour in relation to adopting the benthic habitat as a step towards improving our knowledge of the settlement process.

In the present study, the aim was to investigate ontogenic changes in behavioural patterns and prey preferences of O. sinensis using laboratory-raised animals to more clearly define the ecological transition from plankton to benthos. Laboratory hatched O. sinensis paralarvae and juveniles aged between 10 and 28 days after hatching (DAH) were used in experiments to observe their swimming, clinging and shelter utilizing behaviours in test tanks during both day and night. Their prey preference was also assessed by examining the consumption of planktonic or benthic organisms by individual octopuses. The results illustrate that the behavioural changes of O. sinensis are not clearly demarcated and an extended period of time is required to complete the process of adopting the benthic mode of life, suggesting that the settlement process in the natural habitat involves a complex of gradual changes.

Section snippets

Paralarvae and juveniles

Paralarvae and juveniles that were used for the experiments originated from five different egg masses spawned by five female octopuses (broods A–E). The females were caught using octopus pots between 19 April and 19 May 2017 or between 19 April and 18 May 2018 in the central area of the Seto Inland Sea, off Hiroshima, Japan (34°20′N, 133°14′E); body weights were 1295 ± 475 g (mean ± SD). They were maintained in 3.3 kL cylindrical tanks with flow-through water systems (water exchange rate, ≥300%

Growth of octopus paralarvae and juveniles

Octopuses (aged 14 to 28 DAH) used in these experiments had a mean DW ranging from 4.5 to 16.1 mg, 4.6 to 16.4 mg and 4.6 to 15.5 mg for broods A, B and C, respectively (Figs. 2). For those from broods D, E1 and E2, the mean DW ranges were 1.7 to 2.0 mg at 10 DAH, and 2.5 to 3.2 mg at 13 DAH. Octopuses aged 16 and 17 DAH were from brood E2 and reached 3.3 and 4.2 mg DW, respectively. Octopus DW tended to become much more widely distributed after 20 DAH, probably related to the increasing

Discussion

The clinging behaviour of octopus paralarvae involves prolonged contact with, and adhesion to, hard substrates using the arms and suckers and has been widely recognized as a trait representing the onset of settlement for benthic octopuses with a paralarval phase. Early paralarvae are unable to maintain prolonged clinging due to morphological constraints such as relatively short arms with few suckers and a relatively large mantle (Villanueva, 1995; Villanueva and Norman, 2008). Most studies

Conclusions

The paralarvae of O. sinensis changed their daytime behaviour from swimming to clinging during the period of growth between 3 mg and 9 mg DW, and this behavioural change may be the first step of settlement. Shelter-utilizing behaviour of the octopuses commenced after completion of diurnal clinging. The octopuses began feeding on bivalve prey over the same period as shelter utilization, but shelter utilization and bivalve consumption proceeded gradually spanning a size up to >15 mg DW,

Ethical approval

This study followed all applicable international guidelines for the care and use of animals and was approved by the committee on the ethics of animal experiments at the National Research Institute of Fisheries and Environment of Inland Sea, Japan Fisheries Research and the Education Agency (permission number: 2016–11), where the experiments were carried out.

Author statement

SD and KH designed the study. SS, AT, SD, ST, HY, and AI performed the laboratory experiments. SD and KH analysed the data and prepared the manuscript. All authors approved the final manuscript.

Declaration of Competing Interest

The authors have no conflicts of interest directly relevant to the content of this article.

Acknowledgements

We thank the staff of the Research Center for Marine Invertebrates, National Research Institute of Fisheries and Environment of Inland Sea, Japan Fisheries Research and Education Agency (FRA), for supporting our laboratory work. We thank Ian G. Gleadall (AiCeph LLC, Sendai) for assistance in preparing the manuscript and valuable advice. We are also grateful to the editor and the reviewer for valuable comments and suggestions, which have improved the manuscript. This research was supported by

References (51)

  • S. Dan et al.

    Effects of co-supply ratios of swimming crab Portunus trituberculatus zoeae and Artemia on survival and growth of East Asian common octopus Octopus sinensis paralarvae under an upwelling culture system

    Aquac. Res.

    (2019)
  • S. Dan et al.

    Ontogenic change in the vertical swimming of East Asian common octopus Octopus sinensis paralarvae under different water flow conditions

    Aquat. Ecol.

    (2020)
  • R. Fernández-Gago et al.

    3D reconstruction of the digestive system in Octopus vulgaris Cuvier, 1797 embryos and paralarvae during the first month of life

    Front. Physiol.

    (2017)
  • S. Freschetti et al.

    Pre- and post-settlement events in benthic community dynamics

    Oceanol. Acta

    (2003)
  • D. Garrido et al.

    Meta-analysis approach to the effects of live prey on the growth of Octopus vulgaris paralarvae under culture conditions

    Rev. Aquacult.

    (2016)
  • I.G. Gleadall

    Octopus sinensis d’Orbigny, 1841 (Cephalopoda: Octopodidae): valid species name for the commercially valuable East Asian common octopus

    Spec. Div.

    (2016)
  • L.A. Gosselin et al.

    Juvenile mortality in benthic marine invertebrates

    Mar. Ecol. Prog. Ser.

    (1997)
  • B.M. Greenwell et al.

    Investr: an R package for inverse estimation. R. J. 6/1

    (2014)
  • S. Hamada

    Feeding behavior of Octopus vulgaris Cuvier on molluscs

    Venus

    (1974)
  • K. Hamasaki et al.

    Effect of marine microalgae Nannochloropsis sp. on survival and growth on rearing pelagic paralarvae of Octopus vulgaris, and results of mass culture in the tank of 20 m3

    Saibai Giken

    (1991)
  • N. Hasegawa et al.

    Allometric equations between the shell length and the weight of the Asari clam Ruditapes philippinarum in Ise Bay

    Aquacults Sci.

    (2010)
  • V. Hernández-García et al.

    Evidence of external digestion of crustaceans in Octopus vulgaris paralarvae

    J. Mar. Biol. Assoc. U.K.

    (2000)
  • H.L. Hunt et al.

    Role of post-settlement mortality in recruitment of benthic marine invertebrate

    Mar. Ecol. Prog. Ser.

    (1997)
  • J. Iglesias et al.

    The completed life cycle of octopus (Octopus vulgaris, Cuvier) under culture conditions: paralarval rearing using Artemia and zoeae, and first data on juvenile growth up to 8 months of age

    Aquacult. Int.

    (2004)
  • J. Iglesias et al.

    The effects of using crab zoeae (Maja brachydactyla) on growth and biochemical composition of Octopus vulgaris (Cuvier 1797) paralarvae

    Aquacult. Int.

    (2014)
  • Cited by (10)

    • Cephalopod ontogeny and life cycle patterns

      2023, Frontiers in Marine Science
    View all citing articles on Scopus
    View full text