Research and Advances: Aquatic Sciences

Research Article

Body Patterning of Sepia officinalis in Captivity, from Feeding to Reproduction

Gioele Capillo1, Marilena Sanfilippo2*, Serena Savoca1, Marco Albano1, Francesco Fazio3, Giuseppe Panarello1, Giuseppe Scifo1 and Nunziacarla Spanò4

1Department of Chemical, Biological, Pharmaceutical and Environmental Science, University of Messina, Messina, Italy

2Stazione Zoologica Anton Dohrn, RIMAR Dept., Messina, Italy

3Department of Veterinary Sciences, University of Messina, Messina, Italy

4Department of Biomedical, Dental and Morphological and Functional Imaging University of Messina, Messina, Italy

Received: 02 July 2019

Accepted: 07 September 2019

Version of Record Online: 23 September 2019

Citation

Capillo G, Sanfilippo M, Savoca S, Albano M, Fazio F, et al. (2019) Body Patterning of Sepia officinalis in Captivity, from Feeding to Reproduction. Res Adv Aquat Sci 2019(1): 01-09.

Correspondence should be addressed to
Marilena Sanfilippo, Italy

E-mail: marilena.sanfilippo@szn.it
DOI: 
10.33513/RAAS/1901-01

Copyright

Copyright © 2019 Marilena Sanfilippo et al. This is an open access article distributed under the Creative Commons Attribution License which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and work is properly cited.

Abstract

The increasing demand of fish products and the depletion of natural fish stocks rise the need to develop aquaculture and enlarge the variety of farmed species (fishes and molluscs principally). Among the Cephalopods, the scientific research focused on the common Octopus (Octopus vulgaris) and on the European Cuttlefish (Sepia officinalis). The present study analysed the behaviour of S. officinalis in captivity focusing specially on body patterning during alimentation and reproduction, in order to collect data regarding the behaviour of the molluscs and the possibility to consider this cephalopod among the marine organisms successfully farmable in the aquaculture industry. The experiments have been carried out using adult wild-caught specimens of S. officinalis to determine the adaptability of brood-stock to artificial controlled conditions of the tanks, and the possibility/strategy to use dead feed for cuttlefish alimentation. The results of our experiments provided important information in this field, especially in the body patterning showed by the specimens during all the phases of rearing, providing the occurrence of “natural” behaviours in captivity of the cuttlefish and amplifying the knowledge on S. officinalis optimal rearing conditions.

Keywords

Aquaculture; Behaviour; Cuttlefish; Reproduction in Captivity; Sepioidea

Introduction

Global fish production has grown massively in the last five decades, with food fish supply increasing at an average annual rate of 3.2 percent, outpacing world population growth at 1.6 percent. World per capita apparent fish consumption increased from an average of 9.9 kg in the 1960s to 19.2 kg in 2012 [1]. Of course, the increasing demand of fish products and the depletion of natural fish stocks rise the need to develop aquaculture and enlarge the variety of farmed species. This is the reason why in the last years the Mediterranean aquaculture has been aiming at offering new species of fishes, molluscs, crustaceans and seaweeds [2-7]. Mainly, two fish species have been targeted for long time in the Mediterranean aquaculture: Dicentrarchus labrax and Sparus aurata [8-10]. Several species have been recently proposed to increase the number of species offered to the fish market: Dentex dentex, Pagellus bogaraveo, Pagellus erythrinus, Pagrus pagrus, Diplodus sargus, Diplodus puntazzo, Diplodus vulgaris, Seriola dumerili, Thunnus thynnus, Epinephelus marginatus, Umbrina cirrosa, Argyrosomus regius, Solea solea. Many studies have been carried out regarding the different features of these species, both in their natural environment and in captivity [11]. Also, Molluscs have been object of scientific studies in order to set up standard farming protocols [12,13]. Bivalves, especially mussels and clams, are currently the most commonly farmed species. Recently research and studies have focused on Abalone (Haliotis lamellosa) and Cephalopods, such as the common, Octopus Octopus vulgaris and the European Cuttlefish Sepia officinalis [14-20]. The class of Cephalopoda includes two sub-classes: Nautiloidea and Coleoidea; Coleoidea includes the four following orders: Octopoda, Teuthoidea, Vampyromorpha e Sepioidea. Sepia officinalis, commonly known as European Cuttlefish, belongs to the order Sepioidea and is part of Sepiidae family. Sepia officinalis is found in Mediterranean Sea and Eastern Atlantic.

Histologically, one of the most important features of the Cuttlefish, with important consequences in the behavioural patterns and mimic skills of this mollusc, is the large presence of chromatophores and structural reflector cells (iridophores and leucophores), which, through dual action, mediate the body patterns [21-24]. Chromatophores are pigment-containing cells with a large, folded membrane forming an elastic sac. By contracting hundreds of muscles radiating from the centre of the chromatophore, the sac’s size and shape can be changed, thus changing the distribution of the pigment and its properties. Contracting and relaxing the radial muscles, the Cuttlefish can express different body patterning, using the body surface as a communication tool [25,26].

The behaviour of European Cuttlefish Sepia officinalis is fascinating and many features of this are brought about by their nervous system [27], which is the most complex of the invertebrates. In order to evaluate if this species might adjust to captivity for the purpose of industrial-scale aquaculture production cuttlefish, becomes important understand behavioural biology in captivity [28]. Cuttlefish behaviour in captivity might differ from behaviour in the natural environment, and that should be noted and analysed.

The sophisticated ethology of these invertebrates is mainly exhibited creating a wide variety of appearances, called body patterns, as a result of a combination of different components: chromatics, structural, postural and locomotors [29].

The present study focuses on the European Cuttlefish body patterning during alimentation and reproduction in captivity, in order to collect new data regarding the behaviour in captivity of S. officinalis and the possibility to consider this cephalopod among the marine organisms successfully farmable in the aquaculture industry.

Materials &Methods

Wild adult specimens of European Cuttlefishes have been caught in spring (March-April) using a traditional the trammel net [30] in a sandy bay of Messina (38°27'90"N 15°60'85"E, Messina, Sicily, Italy), in the Southern Tyrrhenian Sea [31,32]. The trammel net was used at a depth of 3 meters. The fishing net was used at night-time and the cuttlefishes were captured during two different trips.

14 specimens of cuttlefish were transferred, in the shortest possible time, to the research facility at University of Messina (Italy) in a special polyethylene transportation tanks (Narvalo model 120x100x90 cm, INNOVAQUA, Cadelbosco Sopra, Reggio Emilia, Italy) continuously oxygenated. For each transport tank 2 specimens were transported, to avoid stress phenomena.

As during transportation to the laboratory, a cuttlefish expelled the ink, the seawater was totally replaced. Once arrived to the laboratory, the cuttlefishes were transferred to two 500 l fiberglass tanks. Each tank was provided with a continuous seawater flow. Also, each tank was equipped with a cylinder-shaped plastic net in order to offer the female cuttlefishes a suitable surface where to attach the eggs they will have laid. Prior to reach the rearing tank, the seawater was treated by using drum filters, filters sock and UV filters.

Water parameters were measured on a weekly basis. Temperature and salinity were measured with multiparametric probe (YSI30, Yellow Spring Incorporated, Ohio, USA), pH was measured with a pH meter (pH110, XS Instruments, Singapore). Oxygen was detected by Winkler method [33-35]. About the photoperiod, as the laboratory has several windows, the tanks were exposed to natural daylight. During the experiment, all the specimens were fed with both live and non-live food including juveniles of shrimps. Few hours after the introduction in the tanks, the captive cuttlefishes observed in this experimental study showed to be ready to accept food. All the specimens were fed with both live and non-live food live food was including juveniles of Sparus aurata and Dicentrarchus labrax, and adult crabs (Eriphia verrucosa and Pachygrapsus marmoratus); non-live food was including fishes such as Sardina pilchardus, Sparus aurata, and the crabs Eriphia verrucosa, Pachygrapsus marmoratus. Also, a dry-pellets fish diet was tested.

S. officinalis clearly showed a preference for live food, thus confirming a hard-to-suppress predatory instinct. Despite this, it is understood that with the adoption of specific feeding strategy, it might be possible to feed the European Cuttlefish with non-live food.

Pictures using a camera Nikon D3200, equipped with underwater housing Nimar NI3D3200ZM were taken.

All experimental procedures were carried out in accordance with European legislation regarding the protection of animals used for scientific purposes (European Directive 2010/63).

Results & Discussion

The results of our experiment were here reported and commented in table 1 and 2. In figure 1 the data plotted refer to the various moments and conditions of the cuttlefish.

of specimen

Sex

ML (mm)

W (g)

6

Male

127.2

152.7

8

Female

151.2

186.4

 Table 1: Specimen information.

Data are expressed as mean ML: Mantle Length. W: Weight.

Body-Patterning-of-Sepia-officinalis-in-Captivity-from-Feeding-to-Reproduction

Figure 1: Sepia officinalis body patterns plotted respect various phases of experiment: A) Female body patterns; B) Male body pattern.

 

Body pattern

Figure

General condition

Weak Zebra

2A

Alimentation

 

 

Fishes

Flamboyant

2B

Crabs

No specific

-

Dead preys

No specific

-

Reproduction

 

 

Male’s rivalry

Intense Zebra Display

2D

Coupling (male)

Intense Zebra

2C

Coupling (female)

No specific

-

Egg deposition

Weak Zebra

2A

Egg deposition (annoyed)

Deimatic

2E

Post deposition

Strong disruptive

2F

Table 2: Body patterning of specimens during the different phases of the experimental period.

In the right column is reported the figure related to body pattern.

Differences in body patterns expression have been recorded between male and female specimens; in figure 1 the data are plotted separately (female and male).

The chromatic components might be dark or light, depending upon the status of the chromatophores (expanded or retracted). Moreover, leucophores would appear to be responsible for the production of whiteness in cephalopods such as white fin spots, white zebra bands, white square, and white head bar [36].

The structural components concern the skin, which might be smooth or rough due to the presence of several papillae. The postural components describe the position and orientation of oral arms, tentacles, head and fins. At last, the locomotors components regard several acts such as resting, burying, jetting, hovering and many others.

The body patterning is used by the Cuttlefish to assume the pattern and shape of a background [37], to hide from the sight of predators and to approach a prey [38]. Of remarkable interest are some recent studies analysing the role of body patterns in communication [39].

Body patterns have been described in several Cephalopods, and the European Cuttlefish S. officinalis is one of the most explicative case studies.

Body patterns can be classified as chronic, which last for many hours and are used for camouflage, and acute, which last seconds and are used in hunting, defense and visual fights among males [40].

All Cephalopods are voracious carnivores able to use strategies to find and attack the prey [41].

As long as no preys were introduced into the rearing tanks, and no threatens were presented, the cuttlefishes used to lie on the bottom, showing the chronic body pattern named “Weak Zebra” [42]. “Weak Zebra” is a usual coloration of adult cuttlefishes, and it’s described as low-contrast striped pattern (Figure 2A).

As soon as live fishes were introduced into the tank, the predatory behaviour of the cuttlefishes was strongly stimulated. The first stage of the capture sequence was a visual attack, which is including three levels: attention, positioning and assault [43,44]. During attention, the cuttlefish identified the prey and showed the “Flamboyant” body pattern [26] (Figure 2B). In this body pattern the dorsal pair of oral arms is raised and is assume a brownish colour (postural component); at the same time the cuttlefish slowly swims toward the prey (locomotors component). The “Flamboyant” body pattern is considered a deceptive resemblance, with the purpose to distract the prey from what is actually going on. A chromatic component, which was often observed as part of Flamboyant display, was two longitudinal dark stripes across the mantle and two transverse dark stripes. The skin appeared covered by a number of papillae (structural component). The postural component is probably the distraction tool used to confuse fishes. The positioning is the second step of the visual attack. In the third and last part, a real seizure took place. The tentacles are ejected to grab the prey, with one of the quickest movements existent in the marine environment: about 15 meter per second [45]. The prey is then brought back to the arms and the beak at the centre of them. At this point, the animal starts eating his meal.

The cuttlefishes readily accepted live food at any time during the day; they immediately attacked the preys introduced into the tank, even in presence of human observers above them or while the underwater camera was being used. It happened sometimes that late in the afternoon few live fishes were not consumed from the cuttlefishes; as the morning after no preys were found in the tank, it is understood that the fishes were eaten during the night. This confirms that the lack of light does not affect the hunting activity of the cuttlefish; these Cephalopods are, in fact, equipped with mechanoreceptors, which are sensitive to low-frequency vibrations, located on the oral arms and on head. This system similar to lateral line of finfishes, and it is thought to be used from the cuttlefish to locate the prey [29].

The European Cuttlefish exhibited prey specific hunting. When live crabs - which are among the preferred food from most of the cephalopods - the hunting tactic was different: the feeding appendages were not used, and no specific body pattern was exhibited. Once the crab was located the cuttlefish rapidly seized the prey using the oral arms only. Also, the cuttlefish always attacked the crab from behind in order to avoid any reaction of the prey that might result in a loss of harm or a wound. The crab is then paralyzed, approximately in ten seconds, thought the injection of a thermolabile toxin, known as Cephalotoxin, secreted by the posterior salivary glands of cephalopods [45,46].

As many other Cephalopods, the European Cuttlefish exhibited a remarkable preference for live preys; despite this, it was observed that the adoption of certain feeding strategies might help those cephalopods to accept dead preys.

In their natural environment, cuttlefishes might behave as a scavenger [47]. The present study highlighted how is important the way by that the food is introduced into the tank; in fact, if a dead pilchard or any other dead prey is thrown into the tank, the impact to the water surface would annoy the cuttlefish, which will react by immediately releasing the ink and swimming away. Another important aspect to consider is the buoyancy of the food. If the dead prey remained in upper levels of the water column, it was not eaten by the cephalopods in the tank; when using dead fishes as food, the highest percentage of attacks was noted when the prey was slowly sinking to the bottom of the tank, shining and swinging. Those stimuli definitely attracted the attention of the cuttlefish. When a dead fish reached the bottom of the tank without being seized, it was never eaten, except for few occasions.

When the dead prey was a crab, the result was totally different. Regardless of the fact that the crab reached or not the bottom of the tank, it was seized and eaten in the 80% of attempts. It can be supposed that the lack of motion did not affect significantly the feeding activity of the cuttlefish. It is evident that the shape of a dead crab is a stimulus strong enough to provoke an attack; and it was observed that captive cuttlefishes in this experiment get used to dead crabs as they were presented with this food day by day. In order to define this feature future further studies are needed; in fact, the role of learning in success rates and suitability of dead prey items is one of the most fascinating topics regarding the study of cephalopods behaviour for farming purposes.

The use of a dry diet in pellets did not bring encouraging results: the pellets were always left on the bottom of the tanks; regardless of the way they were presented to the cuttlefishes.

In general, cleanliness and proper maintenance of the tank had a positive impact in the acceptance of dead preys from cuttlefishes.

Reproductive behaviour of S. officinalis is complex and fascinating. In this study, we reported for the first time that the reproductive behaviour of the cuttlefish and related body patterns were not influenced by the farming condition. Our results are in contrast with previous studies [48,49]. To evaluate the intraspecific interactions generally involved in cuttlefish reproduction was observed the encounter between two adult specimens. If there was any male in the couple being observed, this immediately exhibited the body pattern “Intense Zebra” (Figure 2C). If the approached cuttlefish was a male too, the “Intense Zebra” body pattern was promptly returned to the opponent [37]. If the other specimen was a female, courtship and copulation took place. In the encounters between males, the body pattern “Intense Zebra” escalated most of the times to the body pattern “Intense Zebra Display” (Figure 2D), which differs from “Intense Zebra” due to the fourth arm extended towards the conspecific. White spots appear all over the arms’ skin, and this is considered one of the main signals in adult male of S. officinalis [29]. At this point, male circle one another either in parallel or anti-parallel position, intensifying the body pattern exhibition. This kind of visual fight might last several minutes. If neither male withdraws, the ritual escalated to a physical fighting, lasting few seconds only, where the cuttlefishes tried to bite each other. The loser immediately stopped the exhibition of the Intense Zebra Display and withdraws to a corner of the tank.

Upon exhibition of “Intense Zebra” from a male, if the body pattern was not returned from the other cuttlefish, it was a female, and then the courtship behaviour was observed. This was lasting from few minutes to several hours and was followed by copulation. Initially, the male used to stay very closed to the female, touching her with the arms and following her constantly. It was observed that, during courtship, the female was eating whichever prey was passing in the within range; in contrast, the male never tried to grab any prey, most probably in order to avoid a distraction which might have resulted in losing the partner. Eventually, the male cuttlefish adjusted his position in order to be face-to-face with the female; the oral arms were opened to grab the anterior part of the female’s body. Few times the female was not willing to mate, therefore she swam away. Most of the times, the female accepted the male’s attempt, and then the copulation started. In aforementioned face-to-face position, the male cuttlefish was keeping the female with his oral arms. Copulation lasted up to 40 minutes. In this time frame, the male transfers the spermatophores, using the hectocotylus, to the female. Cephalopods’ sperm sacs are considered the most sophisticated spermatophores in the animal kingdom [50]. After copulation, male remained close to the female; on occasion, another male intimidated him. At this point the female was again subject to courtship.

Few hours after mating, the egg deposition took place. The female cuttlefish ready to lay eggs, approached with the forward extremity of the longitudinal body axis the plastic net cylinder, often maintaining the physical contact with the bottom of the tank. After that, the female left the bottom and started exploring and touching the cylinder with the arms for several seconds, then the first egg was attached to the net. After the egg was attached to the plastic net cylinder, the female cuttlefish used to blow two jets of water from the siphon, in order to clean the surface of the egg; then the specimen remained motionless for around two minutes, at the bottom of the tank before placing another egg. Cuttlefishes’ eggs are blackened with ink, in order to be preserved from high intensity light and predators.

The egg deposition requires a lot of energy to be carried out; also, during spawning, the female cuttlefish didn’t show any interest in preys.

In case the cuttlefish was annoyed (either by another specimen or by an observer), Deimatic (or Dymantic) body pattern was exhibited (Figure 2E). This body pattern is characterized by the sudden appearance of two black spots on the mantle. This body pattern is considered a warning given from the cuttlefish when approached by a predator or a human, and it’s often followed by escape. Once the egg deposition was completed, the cuttlefish used to stay at the bottom of the tank, motionless and exhibiting the body pattern “Strong Disruptive” (Figure 2F). This body pattern disrupts the normal outline of the animal as a result of spawning. Moreover, this kind of body patterns seemed to be exhibited as a response to the presence of contrast of light and dark in the environment.

Body-Patterning-of-Sepia-officinalis-in-Captivity-from-Feeding-to-Reproduction

Figure 2:Sepia officinalis body patterns: A) Weak Zebra; B) Flamboyant; C) Intense Zebra; D) Intense Zebra Display; E) Deimatic; F) Strong disruptive.

After spawning, several female specimens died, most probably due to the high level of energy required from this particular moment of their life cycle [51]. Around two months after spawning, the eggs hatched, and the newly born paralarvae started a new life cycle.

Conclusion

The study performed in our laboratory at University of Messina, reported for the first time that European Cuttlefish S. officinalis exhibits in captivity the same behaviour (including body patterns) observed in their natural environment. This is a remarkable fact to consider for evaluating the ability of a species to adapt to captivity.

Of remarkable interest, body patterning might also be considered a tool in order to evaluate the general health and behavioural status of the cephalopod being observed in farming conditions. Indeed, whenever a specimen displayed a change in behaviour, with regard to food consumption or intraspecific/interspecific relationships, the ability to perform certain body patterning was affected at the same time. Cuttlefishes affected by secondary bacterial infections as a result of aggressive behaviour causing external lesions, dead in 100% of the cases; and the lack of body patterning was the very first element among the behavioural aspects (appetite, camouflage, reactivity to outside stimuli) the animal lost around one week before death. The same feature in females at the end of spawning was observed.

In conclusion, our study provides the occurrence of “natural” behaviours in captivity of the cuttlefish and this might be relevant in order to gather knowledge concerning many subjects including but not limited to S. officinalis optimal rearing conditions. The results obtained in this study are very important because they indicate the possibility of inserting the cuttlefish among the species potentially rearable in aquaculture plants and representing an excellent product for future generations.

Conflict of Interests

“All authors declare no conflicts of interest in this article”.

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