Elsevier

Fisheries Research

Volume 238, June 2021, 105902
Fisheries Research

Ontogenetic variation of trophic habitat for sympatric benthic octopods in East China Sea derived from isotopic analysis on beaks

https://doi.org/10.1016/j.fishres.2021.105902Get rights and content

Highlights

  • Significant differences of beak δ13C and δ15N revealed the trophic variation of the four octopus species distributed in East China Sea.

  • The decreased isotopic overlap from immature to mature stage showed different feeding habits of the four octopus species during ontogeny.

  • Potential competition of four sympatric octopus species were observed with the evaluation of isotopic overlap by Bayesian framework.

Abstract

Sympatry is commonly observed in marine species, and always accompanied by high competition. Octopus consists of large amount of species and also widely distributed in the neritic area of the sea. As typical benthic species, octopus tend to live in the similar habitat with less movement during its lifetime. It is important to understand the trophic ecology of sympatric octopod species, which play an irreplaceable role in marine ecosystem. In this study, four neritic octopus species in the East China Sea (Amphioctopus fangsiao, Amphioctopus ovulum, Octopus minor and Octopus sinensis) were chose, we used stable isotope analysis (SIA) to analyze the variation of δ13C and δ15N derived from beak to assess the trophic variation among species and maturity stages. O. sinensis has the largest body and beak size than other species, and this species also had highest mean δ13C, δ15N value among species. The result of ANOVA showed that significant differences existed among four species for isotopic values. The overlaps among species were also calculated by standard ellipse area (SEAc). Isotopic overlap was decreased from immature stage to mature stage. The trophic niches were shrunk from immature to mature for all the four octopods species except for A. ovulum, which presented an expansion tendency. Trophic overlaps between specific two species in different groups were also calculated with distribution and mean values based on Bayesian model. The highest and lowest isotopic overlap occurred between O. minor and A. ovulum in immature group, A. fangsiao and O. sinensis in mature group, respectively. The four octopods species had very different trophic niches during ontogeny.

Introduction

Sympatry in marine animals have been discussed for different kinds of species (Brousseau and McSweeney, 2016; Curnick et al., 2019; Haak et al., 2019; Hamilton et al., 2019). As a worldwide important taxa of invertebrates, cephalopods with similar habitat behavior also tend to live in the same area (Rosas-Luis et al., 2016; Seco et al., 2016; Matias et al., 2019). Thus, species coexistence of cephalopods showed their utilization of food resources and ambient environment with different strategies (Rosas-Luis et al., 2016; Seco et al., 2016; Li et al., 2020). It is also indicated that different cephalopod species had the ability to handle their own niche space and not overlap with others from ecological aspect (Rosas-Luis et al., 2016; Bennice et al., 2019; Matias et al., 2019). Thus, studying the cephalopods sympatric characteristics will help us understand the importance for different species in the marine community.

As typical benthic species, Octopus is the largest and most important genus in the Octopodidae family (Sweeney and Roper, 1998), which also accounts for large proportion of total landings in neritic fishery (FishStatJ: http://www.fao.org/fishery/ “Accessed 1 st Sep 2020”). The octopods Amphioctopus fangsiao, Amphioctopus ovulum, Octopus minor and Octopus sinensis are the most abundant sympatric species in East China Sea (Song et al., 2009; Fang et al., 2018), where is the most abundant fishery resources area with high nutrition and varied currents (Wang et al., 2003; Xu et al., 2019a, 2019b). The octopus species are ecologically important and as main food for larger fish and marine mammals (Pethybridge et al., 2011; Bowen and Iverson, 2013). The above four species are always inhabiting in the similar area with similar depth (Norman and Hochberg, 1994; Gleadall, 2004; Guzik et al., 2005). As benthic species, the cooccurrence of same genera species induce species competition in some extent, which may lead to the trophic overlap (Seco et al., 2016).

One of the main characteristics for the feeding ecology in cephalopod is the dietary change during their life history. The diet of octopod changes from zooplankton in paralarvae (Nande et al., 2017) to fish and crustaceans in adult (Cortez et al., 1995; Rosas‐Luis et al., 2019), including O. minor (Bo et al., 2020) and O. vulguris (Ambrose and Nelson, 1983), which is the sibling species of O. sinensis (Amor et al., 2017). The dietary change is also a kind of adaptation with the body growth. The change of food preference has always occurred during the maturing period. Most of the pelagic cephalopod species had this characteristic (Fang et al., 2016; Liu et al., 2020). The switch of diet in octopus has always been discussed in some aquaculture studies. Wang et al. (2017) indicated that switch of diet for A. fangsiao larvae was needed at the benthic stage (0.1 g), and shrimp and fresh shellfish meat was the optimal combination for the benthic hatchlings. Rarely study has reported the dietary change of octopus in wild status.

Cephalopod beak is the main feeding organ with the stable structure and enriched valuable ecological information (Clarke, 1962). Beak morphology, including measurements and landmarks, could be used as a taxonomic character to distinguish different species (Ogden et al., 1998; Fang et al., 2018). The disparity of beak morphology suggested the difference of feeding behavior is also existed (Fang et al., 2018). With the development of techniques, stable isotope analysis (SIA) has been widely used in cephalopod trophic ecological studies (Golikov et al., 2018; Liu et al., 2018; Xu et al., 2019a, 2019b). This method can detect a long-term feeding information (few weeks to a month, Dantas et al., 2020), which traditional methods hard to do so. Beak is also a very useful material in the SIA study (Queirós et al., 2018, 2019, 2020). Thus, it is possible for us to reveal the trophic variation during the cephalopod lifetime derived from beak (Golikov et al., 2018; Queirós et al., 2020; Liu et al., 2020).

In this study, we used stable isotopes analysis (SIA) to measure the δ13C and δ15N of immature and mature groups for four octopus species, which collected in East China Sea. Corrected standard ellipse area (SEAc) were depicted and calculated under the Bayesian framework. This study aims to 1) understand trophic habitat of the four dominant octopus species in the neritic of East China Sea; 2) compared the feeding habits change between immature and mature stages; 3). evaluate the possible competition among the coexistence octopus species. This study may give us a comprehensive understanding of the octopus trophic ecology in nearshore of China and may provide a useful approach to analyze potential competition among coexistence species.

Section snippets

Sampling and measurements

Octopus samples were selected from the commercial trawl vessel F/V Zhelingyu 23860 in the East China Sea (125°–127 °E and 29°–32 °N) during September to December in 2018 (Table 1, Fig. 1). Samples were immediately frozen at −18 °C before ship to the laboratory. All of the octopus species, which belong to Amphioctopus fangsiao, Amphioctopus ovulum, Octopus minor, and Octopus sinensis, were identified based on morphological features (Song et al., 2009; Gleadall, 2016). The details of methods were

Body and beak size variation among four octopus species

The body size showed a difference among the four octopus species. O. sinensis had the largest body size (ML and BW) among the four species (Table 1). A. ovulum had the smallest ML and BW among the octopus species (Table 1). Mature group had larger body size than that of immature group in each species (Table 1). In terms of beak size, LRL of O. sinensis were larger than that of any other species (Table 1). O. minor had the smallest LRL among four species (Table 1). Similar with the body size,

Body and beak size related to feeding behavior

Octopus species distributed in the coast of China present varied morphological traits in the body size (Jereb et al., 2016). Just like the sibling species Octopus vulgaris, O. sinensis had relative larger body size than other octopus species (Amor et al., 2016). O. minor has longer arms and the weight of the arms account for more than 50 % of its total weight. Beak measurements also have the similar morphological traits with their body size (e.g. O. sinensis has the largest beak size among four

CRediT authorship contribution statement

Zhou Fang: Conceptualization, Data curation, Formal analysis, Methodology, Supervision, Writing - original draft, Writing - review & editing, Funding acquisition. Peiwu Han: Methodology, Resources, Writing - original draft. Siwenjia Shi: Conceptualization, Data curation, Formal analysis, Methodology, Writing - original draft. Xinjun Chen: Funding acquisition, Writing - review & editing.

Declaration of Competing Interest

The authors declare there is no conflicts of interest regarding the publication of the manuscript entitled “Different trophic ecology of sympatric benthic octopods in East China Sea derived from isotopic analysis on beaks”.

Acknowledgements

We are grateful to the captions and crews from trawl vessel for their supports in this survey. This work was funded by the National Key R&D Program of China (2019YFD0901404), National Science Foundation of China (41876141) and Fund of Key Laboratory of Open-Sea Fishery Development, Ministry of Agriculture, P. R. China (LOF 2018-02).

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