Erica A. G. Vidal

Cephalopod Culture: Current Status of Main Biological Models and Research Priorities

A recent revival in using cephalopods as experimental animals has rekindled interest in their biology and life cycles, information with direct applications also in the rapidly growing ornamental aquarium species trade and in commercial aquaculture production for human consumption. Cephalopods have high rates of growth and food conversion, which for aquaculture translates into short culture cycles, high ratios of production to biomass and high cost-effectiveness. However, at present, only small-scale culture is possible and only for a few species: the cuttlefish Sepia officinalis, the loliginid squid Sepioteuthis lessoniana and the octopuses Octopus maya and O. vulgaris. These four species are the focus of this chapter, the aims of which are as follows: (1) to provide an overview of the culture requirements of cephalopods, (2) to highlight the physical and nutritional requirements at each phase of the life cycle regarded as essential for successful full-scale culture and (3) to identify current limitations and the topics on which further research is required. Knowledge of cephalopod culture methods is advanced, but commercialization is still constrained by the highly selective feeding habits of cephalopods and their requirement for large quantities of high-quality (preferably live) feed, particularly in the early stages of development. Future research should focus on problems related to the consistent production of viable numbers of juveniles, the resolution of which requires a better understanding of nutrition at all phases of the life cycle and better broodstock management, particularly regarding developments in genetic selection, control of reproduction and quality of eggs and offspring.

Future challenges in cephalopod research

We thank Anto´nio M. de Frias Martins, past President of the Unitas Malacologica and Peter Marko, President of the American Malacological Society for organizing the 2013 World Congress of Malacology, and the Cephalopod International Advisory Committee for endorsing a symposium held in honour of Malcolm R. Clarke. In particular, we would like to thank the many professional staff from the University of the Azores for their hospitality, organization, troubleshooting and warm welcome to the Azores. We also thank Malcolm Clarke’s widow, Dorothy, his daughter Zoe¨, Jose´ N. Gomes-Pereira and numerous colleagues and friends of Malcolm’s from around the world for joining us at Ponta Delgada. We are grateful to Lyndsey Claro (Princeton University Press) for granting copyright permissions.

Current Status and Future Challenges in Cephalopod Culture

This chapter presents an overall perspective on the current status of cephalopod culture, its bottlenecks and future challenges. It focuses on the species that have received more research effort and consequently accumulated more sci- entific literature during the present century, namely Sepia officinalis, Sepioteuthis lessoniana, Octopus maya and Octopus vulgaris. Knowledge regarding physiology, metabolism and nutrition of different species is still lacking. Two main challenges are identified: the development of a sustainable artificial diet and the control of reproduction. Understanding cephalopod physiology and nutrition will probably be the biggest challenge in developing the large-scale culture of this group of molluscs

Early Mode of Life and Hatchling Size in Cephalopod Molluscs: Influence on the Species Distributional Ranges

Cephalopods (nautiluses, cuttlefishes, squids and octopuses) exhibit direct development and display two major developmental modes: planktonic and benthic. Planktonic hatchlings are small and go through some degree of morphological changes during the planktonic phase, which can last from days to months, with ocean currents enhancing their dispersal capacity. Benthic hatchlings are usually large, miniature-like adults and have comparatively reduced dispersal potential. We examined the relationship between early developmental mode, hatchling size and species latitudinal distribution range of 110 species hatched in the laboratory, which represent 13% of the total number of live cephalopod species described to date. Results showed that species with planktonic hatchlings reach broader distributional ranges in comparison with species with benthic hatchlings. In addition, squids and octopods follow an inverse relationship between hatchling size and species latitudinal distribution. In both groups, species with smaller hatchlings have broader latitudinal distribution ranges. Thus, squid and octopod species with larger hatchlings have latitudinal distributions of comparatively minor extension. This pattern also emerges when all species are grouped by genus (n = 41), but was not detected for cuttlefishes, a group composed mainly of species with large and benthic hatchlings. However, when hatchling size was compared to adult size, it was observed that the smaller the hatchlings, the broader the latitudinal distributional range of the species for cuttlefishes, squids and octopuses. This was also valid for all cephalopod species with benthic hatchlings pooled together. Hatchling size and associated developmental mode and dispersal potential seem to be main influential factors in determining the distributional range of cephalopods.

Beak development of early squid paralarvae (Cephalopoda: Teuthoidea) may reflect an adaptation to a specialized feeding mode

Morphological and morphometric development of the upper jaw (UJ) and lower jaw (LJ) and arm crown of Chiroteuthis cf. veranyi, Liocranchia reinhardti (oceanic species), and Doryteuthis opalescens (neritic species) paralarvae were analyzed in order to verify whether or not they are determined by developmental modes. Jaw measurements were taken, correlated with mantle length (ML) by multiple linear regression to determine relative influences on growth, and compared between species by ANOVA to identify differences. Development was expected to be similar between oceanic species, but was morphologically similar between L. reinhardti and D. opalescens, and morphometrically similar between the latter and C. cf. veranyi. UJ and LJ measurements with highest correlation with ML are larger in L. reinhardti, indicating greater beak development in this species. Rostrum robustness is higher in L. reinhardti, intermediate in D. opalescens, and lower in C. cf. veranyi, hinting at the respective prey type. Teeth (LJ) and slit, characteristics of ancestral cephalopods, are present, disappearing completely and partially on the largest specimens of L. reinhardti and D. opalescens, respectively, and remaining in all sizes of C. cf. veranyi. The results suggest that their presence in early paralarvae reflects an adaptation to sucking the pre-digested internal fluids of prey.

Morphological assessment of the Octopus vulgaris species complex evaluated in light of molecular‐based phylogenetic inferences

Cryptic species are common in the ocean, particularly among marine invertebrates such as octopuses. Delineating cryptic species is particularly problematic in octopus taxonomy where the plasticity recorded among taxonomic characters often results in low resolution at the species level. This study investigated the morphological relationships among seven phylogenetic clades (identified using cytochrome c oxidase subunit I) of the broadly distributed Octopus vulgaris species complex and close relatives. Morphological analyses in this study were successful in delimiting O. sinensis, Brazilian O. vulgaris and O. vulgaris sensu stricto, which was congruent with the molecular findings of this study. Analyses based on male morphology were successful in distinguishing 14 of 15 total pairwise comparisons and proved to be a more reliable indicator of species‐level relationships in comparison with female morphology. The majority of characters with the greatest discriminatory power were male sexual traits. Significant morphological differences were also recorded among sampling localities of conspecifics, with phenotype showing correlation with local environmental data. The findings of this study support the hypothesis that multiple O. vulgaris‐like species are currently being incorrectly treated under a single species name, O. vulgaris. Octopuses being exported globally under the name O. vulgaris are of extremely high fisheries market value and profile. Our findings have potentially significant implications for the naming and conservation of commercially harvested members of this species complex throughout their ranges.

First Description of the Eggs and Paralarvae of the Tropical Octopus, Octopus insularis, Under Culture Conditions

Abstract: Octopus insularis (Leite and Haimovici, 2008) occurs in a wide region of the tropical Atlantic, inhabiting shallow waters along the coast and oceanic islands of northeastern Brazil, where it is considered the primary target of octopus fisheries. This species was only recently described, and detailed information about its spawning, eggs, and paralarvae is unknown. The objective of this study was to estimate the fecundity, describe the eggs and paralarvae and the duration of embryonic development of O. insularis under culture conditions. Broodstock were captured and transported to the laboratory, where they were acclimated in a closed recirculation water system at 26 °C and 32 salinity. Eggs were obtained from two spawning females and were monitored throughout development; samples of 30 eggs were obtained 1 day after spawning and 1 day prior to the first hatching day, and their length, diameter and weights measured. The duration of embryonic development lasted from 30–38 days and fecundity was estimated as 85,000 eggs per female. The length and width of the eggs on the first day after spawning were 2.13 ± 0.06 mm and 0.82 ± 0.04 mm, respectively, and were 2.29 ± 0.06 mm and 0.92 ± 0.03 mm, respectively, one day before hatching. The newly hatched paralarvae exhibit 3 suckers per arm and a mean mantle length of 1.68 ± 0.13 mm. The chromatophore pattern of paralarvae is conspicuous, with ~ 90–111 chromatophores. A total of 32–40 and 56–69 chromatophores were found on the dorsal and ventral view, respectively. These results are of essential importance for identifying the eggs and paralarvae of O. insularis and in broadening our knowledge of this species.

Different abilities to regulate tissue hydration upon osmotic challenge in vitro, in the cephalopods Octopus vulgaris and O. insularis

The spatial distribution of cephalopods is influenced by salinity and temperature. In marine osmoconformers, one reason for different spatial distributions maybe the putative distinct capacity to regulate tissue hydration. Adult Octopus vulgaris (n = 6) and O. insularis (n = 6) were obtained by divers from sites along the southern and northeastern Brazilian coasts, respectively. In the laboratory, octopuses were acclimated to full-strength seawater (salinity 34), for 5–10 days. They were then anesthetized (10 min in 4 °C seawater), a portion of the second right arm was removed, and cut into three portions. Tissues were placed in control isosmotic saline (osmolality 1072 mOsm/kg H2O). Fragments were weighed and transferred to either isosmotic, hyposmotic (50%), or hyperosmotic (150%) salines, and their weight was observed for 120 min. Tissue from both species maintained their hydration/weight following the hyposmotic shock, but differed in their response to the hyperosmotic challenge, where hydration remained unchanged in O. insularis, but was significantly reduced in O. vulgaris. This result could partially explain why O. insularis is more abundant than O. vulgaris throughout the shallow reefs and tide pools in the warmer and salty tropical waters of the northeastern Brazilian coast.

Cranchiids of the South Atlantic Mid-Oceanic Ridge: results from the first southern MAR-ECO expedition

Cranchiids were the most diverse squid family collected during the first southern MAR-ECO expedition in late 2009, with nine taxa identified to species. A total of 45 young specimens were collected (mantle length 7.4–59.2 mm), allowing a survey of early ontogenetic tentacular morphology in cranchiids using scanning electron micrographs. Paralarval tentacular sucker morphology appeared similar among species within the same subfamily: in the Cranchiinae, the paralarval suckers possess relatively large, narrowly polygonal or ovoid-faced pegs in the innermost ring around the aperture, and the infundibular ring lacks the dentition observed in most taoniin genera. Hook development in Galiteuthis armata appears to vary widely among small individuals. Tissue samples were also collected from five genera (Cranchia, Galiteuthis, Helicocranchia, Leachia and Teuthowenia); phylogenetic trees (maximum-likelihood and Bayesian methods) built using these cytochrome oxidase subunit I sequences and others available from GenBank show some support for the subfamilies Cranchiinae and Taoniinae, and that within the latter, the hooked taxa group together. It is hoped that reporting this opportunistic systematic and genetic information may be of eventual assistance in helping to resolve this most problematic of squid families.

Dedication to Professor Malcolm R. Clarke (1930–2013)

We dedicate this special issue of cephalopods papers to the memory of Professor Malcolm R. Clarke. Malcolm had both the vision and initiative to become the ‘‘founding father’’ of the Cephalopod International Advisory Council (CIAC), and had a fundamental role in uniting the cephalopod research community throughout the 30 years since CIAC was founded. He was an inspiring mentor and colleague, and an enthusiastic and charismatic person. His outstanding and unique contributions truly made a difference in cephalopod research and will long be remembered. This special issue contains a selected assortment of papers from the CIAC 2012 Symposium held in Florianópolis, Brazil, from 29th October to 2nd November. We believe Malcolm would have read this issue with pleasure.