Recently, the EU passed a directive that will require all of its member states to follow certain guidelines when using any animals for research. This piece of legislation, passed in 2010, replaced an older law from 1986 on the same topic. Besides updating the ethical and technical aspects of the law, it expanded the scope of the law to include more species than the 1986 law:
3. This Directive shall apply to the following animals:
(a) live non-human vertebrate animals, including:
(i) independently feeding larval forms; and
(ii) foetal forms of mammals as from the last third of their normal development; (b) live cephalopods.
The first question that comes to mind is: why cephalopods? The answer, it turns out, lies in a document published by the Animal Health and Animal Welfare Panel of the European Food Safety Authority – their scientific report revealed that they had initially considered “all invertebrate animals” for inclusion under the law, but ended up recommending that cyclostomes (a group including lampreys and hagfish,) decapod crustaceans (like lobsters and crabs), and cephalopods should be included in the law. They also noted that other invertebrates, like spiders, tunicates, social insects and amphioxus are on the “borderline” of inclusion – that is, they seem to be complex enough (in their behavior and their nervous systems) that it is reasonable to think that they could experience pain or suffering, but there’s not enough evidence to suggest that they do to justify including them in the law. In any case, the only group of animals from this recommendation that ended up making it into the law was cephalopods, with crustaceans being excluded despite the Panel’s recommendation.
The reasons that the Panel cited for recommending cephalopods seem pretty straightforward; cephalopods exhibit what might be called complex cognitive abilities, being able to learn and remember rather flexibly, have large complex brains, and have strong behavioral responses to a variety of stimuli that we’d call noxious. These points, and their relationship to the possibilities of pain and suffering in cephalopods, are far from settled issues, and there’s a lot of arguments that can be made about why they may or may not be adequate justification for including cephalopods in the directive. In a sense, though, it is too late for these arguments; the directive has already passed, and will be in force as early as 2013.
As one might expect, this whole shebang was big news to cephalopod researchers. As I mentioned a few posts ago, a conference (dubbed Euroceph) was called so that cephalopod researchers could get together and talk about what the new law means to them and their work, and what needs to be done next. And there is a lot to be done.
The directive requires that certain criteria be met when using any vertebrate or cephalopod in research: for example, steps must be taken to minimize the animal’s pain and suffering, the animals used should be (if possible) bred for the purpose of research by regulated suppliers and not taken from the wild, and kept in enclosures that “are appropriate to their health and well-being.” One might run into some problems in applying these standards, which have been used in one form or another for regulating the use of vertebrate lab animals for many years, to cephalopods; for example, there is very little known about to biology of how cephalopods might feel pain, and what the consequences of that pain might be to a cephalopod’s health and behavior. There are only a few anesthetics that are used for cephalopods, and since we know almost nothing about the (presumably existent) pain system of cephalopods, we have no drugs to give them as pain-killers – indeed, it’s hard to even know where to start looking to identify drugs that would work as analgesics in cephalopods.
Another problem that came up repeatedly at Euroceph was the requirement for captive-bred animals. So far, there have only been a few limited successes at breeding cephalopods in captivity – among these, the only real successes have been with cuttlefish. Even in this case, though, captive-bred animals appear to behave differently than their wild-caught brethren (which isn’t really a surprise, if you think about how different the two lifestyles are;) perhaps more troubling, captive-bred cuttlefish seem to lose their ability to produce healthy offspring over several generations, limiting the extent of captive breeding programs. For researchers who want to study the behavior of cephalopods as it might be relevant to their lives in the wild, there is “a fundamental scientific problem” with requiring the use of captive bred cephalopods, said Rogen Hanlon, a cephalopod researcher at the Marine Biological Laboratory at Wood’s Hole. ) “If you want the best model [of cephalopod behavior], you use nature’s fittest, and that’s what you get from wild-caught animals.” Having to use captive-bred cephalopods for behavioral research could require research conducted using wild-caught animals that has been relied upon for decades to be re-done with captive-bred animals; even after this, it would still be difficult to predict what this research would mean in terms of how wild cephalopods actually behave.
While the EU directive contains very specific guidelines for the care of common lab animals like rats and rabbits, it contains almost no specific guidelines about caring for or handling cephalopods. This is because, while there is a long history of requiring that lab mammals be dealt with in a certain way (ie. they must have so much space, be given such-and-such a drug before each procedure to reduce pain, be fed every so often, be kept at such-and-such a temperature,) this is the first time that the research community has been required to come up with a standardized set of guidelines for using cephalopods. This might actually be an advantage to cephalopod researchers – they’re in the position now to shape these guidelines themselves, since there are virtually no other sources of information about how it is best to keep cephalopods in captivity. Hopefully, with the help of forthcoming regulations that are tailored to suit cephalopod research in particular, and more research into the health and husbandry of cephalopods, cephalopod research will continue without too much trouble.
Back in September, the European Union passed a directive regarding the use of animals in research. This directive stated that all members of the EU should enforce certain guidelines for the care and use of animals in research; things like making sure that research animals have a certain minimum cage size, are looked after by trained veterinarians, and are handled, experimented on, and euthanized in humane ways. They don’t include all animals, though: species of animals are only covered under this law if the EU has determined that they can “sense and express pain, suffering, distress and lasting harm.” Let’s take a look at that list, shall we?
3. This Directive shall apply to the following animals:
(a) live non-human vertebrate animals, including:
(i) independently feeding larval forms; and
(ii) foetal forms of mammals as from the last third of their normal development; (b) live cephalopods.
That’s right, cephalopods made the cut as being ethically worth looking out for. Why is there an exception made for them, though, out of all of the invertebrates?
In addition to vertebrate animals including cyclostomes, cephalopods should also be included in the scope of this Directive, as there is scientific evidence of their ability to experience pain, suffering, distress and lasting harm.
By the time I reached this point in reading this document, it was clear to me that it was not written by scientists. Scientists probably would have talked about how the research suggests that cephalopods are rather likely to have the capacity for suffering and distress. You only ever really show that an animal *looks* like it’s suffering, in any case. Word choice aside, though, I think that it’s a worthwhile inclusion – it’s at least as easy for me to believe that an octopus can suffer as it is to believe that a lizard or fish can suffer.
That’s not why I brought it up, though.
In response to this directive, a group of cephalopod researchers decided to have a meeting. They’re calling it Euroceph, and besides being a forum for discussion about this particular EU directive, it’s also a scientific conference focused entirely on research in cephalopods, aimed to bring together in one place as many cephalopod researchers as possible to talk, share, network, and learn. And (here’s the most exciting part of all,) I’ll be there! Thanks to the generosity of the organizing committee (who are covering my registration fee), and my wonderful parents (who are helping me with airfare,) I’ll be at Euroceph to not only stroke my own academic interest in behavioral and neural research, but also to report on everything that is going on in the world of cephalopod research. Because I am the only blogger in the world without a laptop, I probably won’t post directly from the conference, but I’ll fill the weeks following it with posts that will hopefully convey not only my excitement but also all the cool stuff I learn about at Euroceph!
While I was reading Zooborns the other day, I came across this wonderful video of a mother Octopus vulgaris (common octopus) at the California Academy of Sciences hatching her eggs in captivity – she rubs them with an arm and a cloud of baby octopuses explode from the egg cluster!
Breeding is at once exciting and depressing in octopuses. With many species of octopus, they die after they breed. They’ll stop eating in order to tend the eggs, and die shortly thereafter. In addition, the young prove to be very difficult to rear. The young of so-called “small-egged” octopuses initially float freely in the water (they are planktonic at this point) and then settle down onto the floor of the ocean when they get a bit bigger – it’s not known how they should be fed while they are in the planktonic phase, or how to accomodate their “settling out” of the water. Who knows, though – the Steinhart Aquarium was the first facility to successfully breed dwarf cuttlefish in captivity (click through for lots of great cuttlefish photos.) These octopuses are more of a challenge, though; only time will tell, and it’s probably not realistic to be very optimistic.
To get things started, here’s a video of an octopus with a Mr. Potato Head Toy (and other things):
You’ll see why this is relevant in a minute. Now on to the post!
“Enrichment” is a psychological term that’s been thrown around a lot. It’s become a buzzword in publications about education, perhaps rightly so given its huge impact on the field of developmental psychology. It has been the subject of intense study in psychology, and continues to be the subject of study. But what exactly is it that we are referring to when we use the term “enrichment”?
Before I get to that, let’s take a step back and consider how brains work. Brains, in the sense that I am talking about, are simply big networks of neurons (there are other types of cells, but we can ignore them for now.) These neurons get sensory input from the body, talk amongst themselves, and send out signals that cause the organism to behave in a certain way. This is, in a nutshell, what brains do – they generate behavior. Importantly, though, they don’t just generate any behavior at a given time; they generate the appropriate behavioral response to the immediate situation. Even more impressively, in some animals, they generate the response that will lead to a positive outcome in some hypothetical future situation (for example, when birds hide food to recover later.) Thus, brains work because they can process incoming sensory information into relevant and adaptive behaviors. Neurons can do this because they are connected to each other in complex but well-controlled and highly-specific ways. Much in the way that an electrical device will only operate if all of its components are connected correctly, brains will only work if all of their neurons (or at least most of them) are “wired” together into functional circuits.
It may come as no surprise, then, that brains only wired the way they are because of the sensory input they receive. During brain development (and, to a lesser extent, throughout life,) neurons require sensory input and behavioral output to form proper connections as well as get rid of improper connections. At the cellular level, this phenomenon is called activity-dependent or experience-dependent plasticity. One can think of it this way: connections between neurons (called synapses) that are used a lot and produce functional behaviors get stronger; that is, they become more efficient and transmit larger signals from neuron to neuron. Synapses that are not used, or that don’t contribute or contribute negatively to the function of a certain circuit become weaker; that is, they become smaller and less efficient, and may even disappear altogether.
This can be demonstrated directly by looking at neurons that process incoming visual information from the eyes. Suppose we were to raise one group of animals (lets say, ferrets) completely in the dark, and another, otherwise identical group of animals normally. Then, we kill both groups of animals and look at the neurons in their visual system (for example, in visual cortex.) The group that was raised under normal light will have, by definition, normal connections between the neurons in the visual system – specifically, these neurons will form functional circuits that allow animals to sense and respond to their environment. In the animals that were reared in the dark (called, sensibly, “dark-reared” animals,) we’ll see a host of abnormalities – cells will have the wrong shapes, end up in the wrong places, and have the wrong connections. Besides this, we could demonstrate some deficiencies in visual perception in the dark-reared animals. Taken together, these results, which have been replicated in a variety of vertebrates, strongly support the idea that sensory systems need input during development in order to develop properly.
It’s a small logical step to tentatively extend the principal of experience-dependent plasticity to brain functions that are more complex than immediate sensory analysis. In the mammalian cortex (which is involved in such complex behaviors as navigation, auditory and visual perception, social behavior, speech, thought, and so forth,) normal development is dependent on the experience of the animal in question during development. The input that these brain areas deal with is almost unthinkably complex. Their function often involves the monitoring the interaction of large parts of the organism with the environment over an extended period of time. For example, cortical areas involved in directing complex hand movements (say, playing a musical instrument) receive their input in the context of a feedback loop that involves planning a movement, executing it, and then determining whether the movement was successful and, if it was not, how it needs to be changed in order to be successful the next time. More abstract cognitive processes become even more complicated, as the brain areas responsible for these have to take into account such complex “stimuli” as the animals current and previous emotional states, inferred emotional states in other animals, the value of various hypothetical outcomes to the organism, prior cognitive states the animal has had, and so forth.
Here’s where the idea of environmental enrichment comes into the picture. The logic goes like this: because neural development is facilitated by the nervous system’s interaction with the environment, and because the more integrative areas of the brain (like the cortex) interact with the environment in very complex ways, normal brain development requires interaction with a very complex environment. If this theory is true, animals raised in very restricted environments (we might call them “environmentally impoverished”) should show maladaptive or sub-normal behavior as adults. In fact, this prediction has been borne out in many studies, which find that (among other things) environmentally impoverished animals (and, although it has been less directly demonstrated, people) have altered learning abilities, exploratory behavior, cognition, stress reactivity, and social behavior.
A corollary of this theory is the idea that nervous systems which have evolved to deal with the environment in very complex ways function abnormally when they do not have complex environments to deal with, much like the way that muscles atrophy if they are not used. Part of successfully engaging a complex environment is continually interacting with and exploring it – indeed, many animals have evolved a propensity to explore and manipulate their environment. Thus, animals with complex behavioral repertoires require complex environments to interact with in order to maintain normal brain function. This theory predicts that a lack of complexity in some animals’ (or people’s) environments should lead to aberrant behavior, and that such behavior can be corrected by providing an appropriately complex environment to those animals (or people.) This prediction is borne out in a variety of studies that show that, in captive adult animals, providing more complex environments leads to lower stress levels, less aggression, and fewer pathological and stereotyped behaviors.
Dr. James Wood’s article, “Environmental Enrichment in the Giant Pacific Octopus; Happy as a clam?” makes the case that aquariums should provide environmental enrichment for captive octopuses. I won’t follow his arguments exactly, but I will examine some of the same questions that he covers, and make reference to and critiques of his work as I find it relevant.
The big question is this: Should we provide environmental enrichment to captive cephalopods? Let me rephrase this: do the benefits of providing environmental enrichment to cephalopods justify the costs incurred by doing so?
First, let’s consider the possible benefits. Anderson and Wood point out several:
1. Captive animals should be kept healthy and allowed to behave normally. Behavioral health is as important to the longevity and quality of animal’s lives as is physiologic health. The real question here is whether cephalopods have complex enough behavior that they might show pathological behavior in response to captive conditions. Put in a more cognitive frame: are cephalopods smart enough to be hurt by captivity and, consequently, to benefit from enrichment?
Indeed, it is hard to tell whether cephalopods could benefit from enrichment. To the question of how we can tell if giant pacific octopuses could benefit from enrichment, Anderson and Wood succinctly conclude: “Simply put, we cannot.” Because cephalopods have evolved under predation from fishes, they reason, they spend most of the time during which they are not hunting hiding in their dens. It’s hard to tell if this is “good” for the octopus (after all, it seems like it would be nice not to have the daily stress of fleeing from predators and risking death during hunting) or bad (because, if cephalopods can become bored, this behavior certainly seems like it would be really boring.) In addition, little is know about how behavioral pathology might look in cephalopods, because we know so little about their behavior in general.
In sum, cephalopods may or may not benefit from enrichment. Given how complex their behavior appears to be, and the likelihood that at least some cephalopods possess cognitive capacities to rival at least some vertebrates, it seems like there’s a reasonably good chance that they could. This isn’t a convincing case in itself – it really depends on the costs of providing enrichment to cephalopods. If the costs are low, this might be enough of a reason to do it; with increasing costs, it becomes an increasingly bad bet.
2. Animal enclosures should meet the expectations of the public. Showing the public what they want to see – which is, it seems, natural-looking enclosures that animals can interact with) will lead to financial success and public support for zoos and aquariums. Researchers, institutions, and the enterprise of biological science in general stand to benefit from the increased public support that comes with presenting a public-pleasing image of animal husbandry in research. Also, if the public sees naturally-behaving animals instead of pathologically-behaving animals, they learn more about the animal’s behavior. A primary function of zoos and aquariums is to educate the public about animals, and so the potential to improve on this education is an important possible result of providing enrichment to cephalopods.
This is an interesting idea to me. Octopuses are popular aquarium animals, but not very popular research animals. The public face of animal research is usually mammalian, including rats, mice, rabbits, and primates. It’s doubtful to me that researchers would benefit from an improved public image if all octopuses used in research were given lots of enrichment. In zoos and aquariums, though, this seems like a valid concern. Indeed, it could offset the monetary costs of providing enrichment for these institutions, which allows less tangible benefits (like the possibility of relieving the suffering of bored octopodes) to be given more weight in deciding whether or not to provide enrichment for captive cephalopods.
3. Finally, zoos and aquariums often care for animals with the goal of eventually releasing them into the wild. Animals whose behavior is dependent on learning need to practice skills that will allow them to succeed, such as hunting, defending from predators and rivals, and maintaining good relationships with other individuals of their species. The Seattle aquarium, for example, does this with their giant pacific octopuses. They catch individuals, hold and display them for a few years, and then release them into the wild so that they have a chance to breed.
It’s doubtful to me that enrichment benefits cephalopods in this way. I can’t say that it’s impossible, but it seems unlikely. While cephalopods are able learners, the basics of cephalopod behavior – feeding, escape, and mating – appear to be largely innate. For example, octopuses learn things in order to adapt to the specific micro-environments they end up in. The characteristics of these environments are impossible for aquariums to predict, and so they cannot be simulated. Feeding a cephalopod common local prey species so that it learns how to eat those species efficiently might help it succeed if it is released, but besides this one example there seems to be relatively little to do in the way of “preparing” a cephalopod for release.
Before I hash out some of the costs of providing enrichment to captive cephalopods, let’s consider what providing such enrichment entail. Anderson and Wood suggest several ideas for giant pacific octopuses, most of which could work with other species of cephalopods. The one that sticks out to me is feeding the animals a variety of live prey. This would provide them with a good deal of activity, a variety of problems to solve (how to catch and eat different species of prey,) and is very entertaining for the public to watch. Some cephalopods (cuttlefish come to mind – I’ve read cuttlefish keepers complaints about this) will only reliably eat live food, anyways.
The authors also suggest that the octopuses be given objects to explore, which can be smeared with fish drippings or have food hidden in them to attract the octopus and encourage exploration. In my favorite quote of the paper, they recount a particular use of this technique:
Wood and Wood… hid food in a play ship – the octopus had to “sink” the ship to get the proffered food. Such a demonstration with a large octopus… would interest the paying customers of a public aquarium by invoking a “sea monster” image.”
The future of cephalopod husbandry.
They also suggest the use of “training” to provide enrichment to octopuses (I put “training” in scare quotes, because some of their specific suggestions, such as smearing fish-smelling fluid on parts of the tank, don’t necessarily involve learning.) This seems like a moot point to me. There are two ways in which you can train a cephalopod – by rewarding it with food, or by punishing it with electric shocks (or some other unpleasant stimulus.) In the first case, you might as well simply give the animal the food, the capture of which seems like it would provide most of the activity inherent in training. In the latter case, well, who’s going to argue that training an animal by electric shock improves its quality of life or reduces its suffering (assuming that the training isn’t absolutely necessary, such as teaching it not to attack people or run into traffic, etc.)?
What would be the costs of providing this sort of enrichment to cephalopods? In my estimation, they would be small. Here’s my reasoning:
It should be relatively easy for aquariums, especially those near coasts, to obtain live prey to feed to cephalopods. By advertising the feeding times (as is done with the animals like sharks, dolphins, and sea lions) aquariums could turn this into a way to entertain visitors and draw more business. The increased popularity of octopus exhibits would likely make up for the extra cost of providing more live food. One of the complaints I hear about the giant pacific octopus exhibit at the Niagara Falls Aquarium is that it just sits there all the time. In the interest of furthering public interest in cephalopods, I make sure to write “Please publicize octopus feeding times!” in their guestbook each time I visit. I’m sure that if they did this, their visitors would be more interested in the octopus and happier with the aquarium overall.
Similar reasoning applies to constructing interesting enclosures that encourage cephalopods to explore. The public likes to see animals doing things, and the increased public interest will more than make up for the expenses of outfitting an octopus tank (which can be as cheap as a few plastic toys) These forms of enrichment are probably very cost effective, at least for public aquariums, even if they have only a small chance of benefit the captive animals.
When we consider animals used for research, the costs become larger. Giving animals a less monotonous environment may exaggerate inter-individual variation. It is usually argued that enrichment produces consistently healthy experimental animals, and so reduces variation in experimental results. The research that is used to make this argument in the case of mammals, however, has not been replicated in cephalopods. Without such evidence, it’s hard to say what effect different kinds of enrichment would have on behavioral experiments with octopuses. Such evidence would be rather expensive and time-consuming to obtain, and providing enriched environments to experimental cephalopods on the assumption that it would improve results could be, if that assumption were wrong, very costly as well. If behavioral research on cephalopods becomes more popular, this will become a more urgent question, and somebody will have to take on the task and expense of answering it.
Generally, providing enrichment for captive cephalopods seems worth it. Given the (even relatively slight) chance that they could benefit from basic environmental enrichment and the small cost of such enrichment, there’s no reason not to do it. The deal only becomes sweeter when you take into account the benefits to aquarium popularity and public education. Even if the cephalopods don’t benefit from it, it can hardly hurt.
Thanks for reading!
Anderson, R., & Wood, J. (2001). Enrichment for Giant Pacific Octopuses: Happy as a Clam? Journal of Applied Animal Welfare Science, 4 (2), 157-168 DOI: 10.1207/S15327604JAWS0402_10
I have three exams next week, so I won’t have another substantive post up until Thursday-ish, at least. In the mean time, enjoy this (under-viewed – only 600 views in 2 years!) video of some captive-bred baby cuttlefish munching on some copepods:
This will be a quick one – I’ll get back to the meat of my series on octopus sensory systems soon, but I wanted to write a post on this article because it struck me as cool (although it has a sort of sensational title.)
The authors used an apparently elegant experimental design to test whether octopuses can tell people from one another across a long period of time – specifically, this is operationally defined as meaning that they could learn an association between a person’s features and a good or bad stimulus. The experiment was conducted thus: eight octopuses were captured and habituated to their aquaria. Then, for 2 weeks, the octopuses had daily interaction with two people, one of whom fed them and one of whom (I’m not joking) poked them with a “bristly stick” (more specifically, “a length of PVC pipe with one end wrapped in Astroturf.”) Then, the octopuses were tested to see if they reacted differently to the two individuals – presumably, if they remember who is who, they should show anticipatory behaviors related to eating or defensive behaviors in response to the appropriate person.
To get a better feel for the task, here are the experimenters, shown in an image taken from the octopus’s point of view:
My problem with this experiment is that the term “individual” is usually used in cognitive research to mean some entity who is known to persist despite changes in their appearence in one specific sensory modality. When we get a haircut, our friends (and, usually, our pet dogs and cats) still recognize us – thus, we are individuals to them. However, if the visual stimulus of the two keepers didn’t change from day to day (and they took pains to make sure that it didn’t,) then this seems like little more than a complex visual discrimination task. It seems, judging from this image, that it would be pretty easy for an octopus to learn an association between, say, a shiny bald head and being jabbed with a stick, regardless of any ability she might have to recognize “individuals” in the cognitive sense. In any case, we are still a ways away from knowing whether octopuses can recognize individuals, and not just their constant visual features. With this in mind, let’s consider their results.
It turns out that the octopuses learned to move away from the irritator and towards the feeder within two weeks. In addition, the octopuses showed fewer defensive coloration responses to the feeders than to the irritators, as well as changes in their respiration rate and the orientation of their bodies relative to the people. In sum, it looks like (in this test, at least) the octopuses succeeded in learning basic traits about the people interacting with them. I don’t think that the title of the paper is fully supported, however – it’s hard to make the case that this single study proves that octopuses can identify individuals in any sort of robust way.
This paper is pretty solid (besides its unfounded title,) although it begs a few questions:
1. How fine of a discrimination can octopuses make? Would they treat two bald men of similar stature the same? What if the subjects wear different clothes? How is this piece of research fundamentally different from Wells’ experiments using simple visual cues? These are all important questions if we’re actually going to claim that octopuses can identify “individuals” as opposed to simple visual stimuli.
2. What does this mean functionally to the octopus in the wild? Is this sort of ability actually used to identify predators and prey items? Do octopuses remember individuals of any species in the wild? Unfortunately, there is not much literature on the development of behavior in the octopus, so we can’t know how much of octopus behavior is “instinct” and how much of it is based on learning (like that shown in this study.)
3. How does this generalize to other species of octopus? This study used Enteroctopus dofleini, the giant pacific octopus, because it is often kept in public aquaria. However, practically the whole body of research on octopus learning and vision has been done using O. vulgaris and, to a lesser extent, O. cyanea. We know that cephalopods have a pretty wide diversity of life-styles, so it seems important to me to know how these behaviors occur in different species if findings like this are going to be relevent to the rest of cephalopod research.
If nothing else, this study keeps alive my childish hope that Twister, the resident E. dofleini at the Niagara Falls Aquarium (which I visit almost weekly these days) will someday get to know me, if only in the most basic way.
Anyways, I hope this has been as fun for you as it was for me. Thanks for reading!
Anderson, R., Mather, J., Monette, M., & Zimsen, S. (2010). Octopuses (Enteroctopus dofleini) Recognize Individual Humans Journal of Applied Animal Welfare Science, 13 (3), 261-272 DOI: 10.1080/10888705.2010.483892
April 18, 2011
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Posted by Mike Lisieski
Categories: Uncategorized
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Tags: Cuttlefish, ethics, husbandry, nautilus, news, Octopus, politics, Squid
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8 Comments
