Octopus aquaculture: Welfare practices and challenges

Perhaps the most perplexing and charismatic of invertebrate species is the octopus. An essential to any aquarium collection, a must-see on a SCUBA diving adventure, a research animal model for cognition and neurophysiology, an inspiration for mechanical engineering, and a growing worldwide demand in the restaurant industry, the octopus has made its way into several aspects of our society.

Octopuses belong to Cephalopoda, along with squid, cuttlefish, and nautiluses. There are approximately 300 species worldwide, all of which are exclusively marine, but occupy a wide range of habitats ranging from intertidal pools a few centimeters deep to the abyssopelagic zone, up to 5000 m deep. Octopuses are semelparous and have a short lifespan; most live for 1 to 2 y, with a few species estimated to live as long as 4 to 6 y. Depending on the species, an octopus may lay hundreds of thousands of eggs and provide dedicated parental care for months until they hatch. Like many other vertebrate and invertebrate species, many offspring do not survive to adulthood. After birth, the young exist as juvenile adults or as planktonic paralarvae, depending on the species. All life stages are carnivorous, feeding on a diverse range of invertebrates and fishes, predominantly crustaceans and shelled mollusks. Octopuses are solitary, congregating only in areas of high feed supply or for mating (1–3). Octopus stocks are periodically evaluated by national governments; however, establishing stock sustainability is widely hindered by limited biological information across species (4–7).

The commercial industry of cephalopods has expanded exponentially over the past few decades (1,2). Markets for cephalopods are common in southeast Asia, as well as Greece, Italy, Portugal, and Spain; however, demand has increased worldwide (1). The octopus fishery in Canada is minor, with most octopuses caught as by-catch or small-scale methods (4). Instead, most octopuses are imported from European or Asian industries. Operations range from small-scale fisheries that collect octopuses “by hand,” to the use of large-scale trawls. These techniques either yield a low harvest that is just enough to supply a small community or are destructive to a variety of benthic habitats, respectively. In addition, the cephalopod fishery is inherently difficult to manage due to the rapid maturation and relatively short lifespan of octopus species and that many major fishery stocks exist in international waters. In response to meeting market demand and habitat conservation, several countries, including Chile, China, Mexico, and Spain, have turned to aquaculture operations (1,2).

Aquaculture makes up 45.8% of total global fisheries and 19% of Canada’s total seafood production ($2.1 billion gross domestic product). Aquaculture serves as a sustainable means to supply local and international markets and is the primary economical contributor and source of protein in many developing countries (8,9). Aside from the food sector, aquaculture has saved hundreds of species of ornamental fish and invertebrate species from wild population decimation.

Successful aquaculture relies on careful selection of candidate species and thorough understanding of husbandry, including environment, diet, and disease. “Good” aquaculture candidates are:

1. legal;

2. of known biology and life history;

3. suitable for market value and demand;

4. readily available as broodstock and/or larvae;

5. able to be cultured at high population densities in a controlled environment;

6. able to efficiently grow with artificial feeds;

7. able to live out their natural life cycle in a controlled environment;

8. able to breed in a controlled environment;

9. able to grow to market size in a reasonable interval; and

10. relatively resistant to disease (10).

Culture systems should be well-researched, and the selected species and rearing system must also be economically viable and pose minimal environmental risk.

Successful global aquaculture of salmonids, Nile tilapia (Oreochromis niloticus), penaeid shrimp, and bivalve shellfish, amongst many others, as been attributed to careful selection and thorough research. As a potential new aquaculture candidate, octopuses provide a large set of challenges. For octopuses, the lack of knowledge regarding their complex life history, behavior, diseases, and medical treatment poses a challenge in becoming an aquaculture candidate. As such, publications concerning octopus aquaculture and husbandry guidelines, along with medical management, are scarce.

Benthic-dwelling inshore species of octopuses that produce juvenile adult offspring are often selected for aquaculture as their environment is best replicated in an artificial setting. However, selection of species is further complicated by an extensive variation in reproductive strategies, functional morphology, egg mass structure and development, fecundity, lifecycle length, and lifestyle variation between developmental stages (3). Provided such extensive research is completed and culture trials are successful, octopus aquaculture itself is not without difficulty. The biggest challenges that exist are cannibalism, trauma, sourcing feed, and raising paralarval stages (2). As aforementioned, octopus diets consist almost exclusively of crustaceans and bivalves. Therefore, sourcing and/or development of a sustainable feed becomes a challenge, particularly for paralarvae stages that require microfeeds (1,2,11).

Octopuses have a highly complex, developed nervous system and may suffer from lack of stimulation in a bland environment (12–15). They may exhibit darting behavior with stress or “boredom,” resulting in trauma and ulceration (12,16,17). Their skin is soft and thin, covered in a layer of mucus that allows them to fit in small crevices and spaces, as such, they are easily traumatized and prone to secondary infection. Common secondary invaders are Vibrio sp., Pseudomonas sp., and Aeromonas sp. In addition, octopuses have been shown to demonstrate self-trauma when stressed (12,16,18), which has been extensively documented in captive octopuses (14,15,19–21). Since most species are solitary, they become territorial or aggressive when in close quarters, which may lead to substantial injuries. Very few species have been documented to have complex social interaction within a given space (22).

Poor growth rates are attributed to poor quality or quantity of feed, competition or territorialism between individuals, stress from overcrowding, unsuitable artificial light, and temperature; these factors present major welfare concerns (3,11). As with other aquaculture species, high stocking densities, particularly when paired with poor nutritional status and trauma, favor disease outbreaks (23). However, unlike those species, there are no approved treatments nor withdrawal times.

No officially established husbandry and welfare guidelines exist for aquacultured octopuses (24). Regulations do, however, exist for accredited aquaria and research in several countries (11,14–16). Individual aquaculture operations may have their own guidelines; however, there is no standardization nor oversight by a governing organization or committee. In general, invertebrates are not protected by the Animal Protection Act nor by an Institutional Animal Care and Use Committee (IACUC). Therefore, ethical care and treatment in octopus aquaculture is highly variable.

There is also the evolving concern regarding the sentience in all cephalopods. Although sentience is a highly debated topic in veterinary medicine, it is becoming a conversation and increasingly being incorporated into the position statements of several countries. Increasing numbers of studies provide evidence of sentience of cephalopods due to their cognitive ability (i.e., solving puzzles) and response to injurious stimuli and analgesics. When encountered with an injurious stimulus, octopuses rub the affected area, avoid environmental areas where injury occurred, and both seek and respond positively to analgesic therapy (18,25–29). We know they possess a variety of unique “personalities” and can exhibit behavior that can be likened to boredom and even curiosity. In a captive setting, such boredom is often remedied by environmental enrichment through the introduction of novel puzzles and interactable objects (12,14,15,30,31). Providing enrichment in aquaculture is a current pressing topic in finfish aquaculture that is not yet adopted by many organizations. Enrichment improves feeding behavior and reduces fin and eye injuries; however, challenges concerning cost and sterilizing enrichment equipment to prevent transmission of disease or excess fouling still exist (32).

Octopuses are intelligent animals with complicated life histories and behaviors that need to be considered to mitigate maladaptation to translate to life in captivity. They are thought to be able to experience feelings such as boredom, they display complex social behaviors, react to painful stimuli, and employ complex reasoning to avoid poor environmental conditions and seek analgesic therapy. Their life history, diet, and behavior make them challenging animals to maintain in a research or aquarium setting; however, they are able to live out their anticipated life expectancies with specific husbandry practices.

The growing demand for octopus in the food industry presents a relatively recent problem of supply. As with many fish and invertebrate species in high demand, aquaculture provides constant, sustainable supply where the ocean is unable to meet consumer demands. However, the octopus is a unique animal, and such a solution is not easy. Many, if not all, known species of octopus do not meet the basic criteria for species selection for aquaculture. Major welfare concerns exist about establishing the appropriate environment and sourcing sustainable feed for a given species, ensuring adequate nutrition, intolerance of high stocking densities (cannibalism), self-mutilation (autophagy), darting behavior (possible stereotypy) and resultant trauma, secondary infection, and need for environmental enrichment.

Therefore, official, enforceable guidelines for octopus husbandry and welfare in aquaculture are urgently needed before pursuit of such an endeavor. Veterinarians, along with aquaculture operation owners and staff, are morally obligated to provide good welfare for all farmed animals. At this time, the behavioral, environmental, and medical needs of cephalopods are not fully understood. Until we can successfully and consistently provide what is needed to these complex animals, it is the hope of this author that the raising of octopuses in aquaculture remains largely hypothetical or experimental. At this time, consumer education is greatly needed to reduce market demand and promote acquisition from sustainable wild octopus stocks using humane and environmentally responsible collection techniques.