They jet it out with some water in the siphon, a part of their bodies that helps them breathe, move, and feed themselves. Octopus ink is usually black, but squid ink is mostly a blue-black color. They use the ink to help them escape from predators. If they feel under attack, they will shoot out the ink so the predator will not be able to see clearly and then the squids will swim away and escape the predator. Cool right? Squid have an organ that contains ink inside of their bodies.
They have another organ that squirt water this is one of the ways that squid can move: they use jet propulsion.
A squid can squirt ink from its ink-containing organ instead of water. Great question! Inking is a defense coupled to jetting and changes in body coloration, such as in the blanch-ink-jet maneuver [ 2 , ]. Ejected ink can take several forms, including diffuse clouds of black ink containing relatively little mucus, darkened blobs with relatively more mucus and called pseudomorphs because they generally resemble the form of a cephalopod, and mucousy secretions called ropes because they are longer and thinner than pseudomorphs [ 6 , 8 , 34 ].
Actually, the diversity of types might be higher, or there may not even be types, but rather a continuum of different forms. These different forms of ink might defend cephalopods against predators in a variety of ways. Most obvious are the mechanisms operating in the visual channel of predators. In this way, ink clouds could serve as smoke-screens behind which inking cephalopods can hide or jet escape.
Pseudomorphs might mimic the form of the inking cephalopod and, by attracting the attention of the predator, buy the cephalopod time to escape [ ]. Ink ropes, by virtue of resembling elongate siphonophores, might serve as visual mimics of these stinging animals and allow deep-sea squid to escape [ 6 ].
Bush and Robison [ 6 ] also note that deep-sea Heteroteuthis squid have ink sacs and produce an ink containing mucus and luminescent bacteria from their light organs, thus creating luminescent clouds, which the squid might use as a visual defense to either conceal themselves or confuse predators. Observational studies in the field and laboratory amply support the idea that ink defends cephalopods from predators.
For example, Staudinger et al. The possibility that ink may act as a chemical defense against predators has been suggested from anecdotal observations, such as octopuses squirting ink at snails or crabs approaching their eggs [ ] and cuttlefish placing ink in their egg capsules [ 4 , ]. Rather, these chemicals can defend by being attractants or repellents, which might be used in mimicry, camouflage and other mechanisms, as shown for a variety of animals [ , , ].
Indeed, some of these mechanisms have been suggested for cephalopod ink. Ink has also been proposed as a candidate phagomimetic defense, due to its high levels of amino acids Section 4. Accordingly, the phagomimetic properties of ink would cause predators to attend to the ink, thus giving cephalopods more time to escape, as has been shown for sea hares Figure 2 D [ ].
Recent experimental tests have supported the idea that cephalopods use ink as an anti-predatory chemical defense. Ink from two species of squid, the Caribbean reef squid, Sepioteuthis sepioidea , and the longfin inshore squid, Doryteuthis pealeii , is unpalatable to predatory fish and, as such, might provide a defense during attacks [ 55 , ].
The molecular identities of these deterrents are unknown. The fraction of ink containing melanin granules has most of the deterrent activity, suggesting that compounds adhering to these granules or melanin itself might be unpalatable. This hypothesis is supported by the observations that ink of the giant octopus, Octopus dofleini martini , contains 8-hydroxyquinolone [ 79 ] and that quinones and related compounds are often used as chemical defenses by animals [ ]. Tests of cephalopod ink as a phagomimetic defense have yielded mixed results.
Ink from two species of squid was not found to be phagostimulants for predatory fish [ 55 , ]. However, ink from octopus ink was found to be attractive to moray eels, evoking searching and attack behaviors, much as did food-related chemicals [ ]. To date, there are no reports of experimental tests of cephalopod ink as an inactivator or disruptor of the chemical senses. Dolphins can cleverly elude the chemical defenses of cuttlefish by de-inking them after capture and before consumption, as shown in Figure 8 [ ].
This behavior is reminiscent of that of rodents when attacking insects that produce noxious chemicals, wherein the rodents stick the chemical-secreting end of the insect into the ground, to avoid that danger, and eat starting at the other end of the insect [ , ].
Handling of giant cuttlefish Sepia apama by Indo-Pacific bottlenose dolphin Tursiops aduncus. Reproduced with permission from Finn et al. A second type of anti-predatory chemical defense in the ink of cephalopods functions indirectly—not by acting on the predators themselves, but rather are alarm cues for conspecifics.
Ink can cause jetting behavior in Loligo opalescens [ 59 , ] and cryptic camouflage , deimatic threatening or startling and protean unpredictable behaviors in Sepioteuthis sepioidea [ 54 ].
DOPA or dopamine at biologically-relevant concentrations is sufficient to evoke jetting in L. Melanin may play a role in the effects of these catecholamines. Melanin adsorbs dopamine, allowing melanin to be possibly a carrier of dopamine in ink [ 58 ]. In addition, ink may contain other antioxidants [ 59 ].
How might melanin have evolved as a component of the ink defensive secretion of cephalopods? Melanin is a scavenger of free radicals, and as such, it can play a photoprotective role, including in vision [ ]. Therefore, melanin may have initially functioned as a photoprotectant in the eyes, skin or other tissues of ancestral cephalopods.
Melanin in the skin of cephalopods may have then taken on a secondary function of camouflage, both passive and active, for which cephalopods are renowned [ 2 , 4 , ].
The ink sac may have had an early function in excretion in addition to the traditional excretory organs, the nephridia , playing a role in the excretion of melanin. Subsequently, the ink sac may have evolved its specific defensive function, with melanin taking on a new role as an anti-predatory defense. Interestingly, pigmented molecules, such as melanin, are rarely reported as being deterrents, though there are exceptions, as reviewed in [ ].
Cephalopod ink has been used by humans for many practical and commercial purposes over the millennia, especially in medicine, cuisine and art, but in even broader applications, as described in this section. Cephalopod ink has a long history of being used to promote human health.
Nair et al. Many health benefits have been ascribed to cephalopod ink as a traditional medicine, both in Western culture ancient Greece and Rome and Eastern culture China [ , ]. More recently, cephalopod ink has been used in an attempt to develop new drugs, through the search for new natural compounds with beneficial health effects. This is an especially active field in Asia, where cephalopods are a major fishery catch, for which ink sacs are a bi-product and where homeopathic medicine has deep roots.
It should be noted that the ink used in drug discovery is not always fresh, often being taken from dead animals, sometimes from preserved animals. Homogenized ink sacs are often used as the source material, and this is then digested or chemically processed. Therefore, caution must be used in assuming that compounds identified through this process of drug discovery might also be present in naturally released ink and used by cephalopods in their natural environment.
Furthermore, since such drug discovery involves intellectual property with commercial applications, identified bioactive compounds may not be reported. Consequently, published work in this field tends toward phenomenology in which effects are identified, but underlying molecules or mechanisms are not.
The following section reviews some of these effects. Cephalopod ink has antimicrobial properties against a diversity of organisms, including human pathogens [ , , , , , ]. Antimicrobial activity is found in various extracts of ink, including aqueous [ ] and organic solvents [ , ], and in the melanin fraction [ , ]. The molecular identities of these antimicrobials, if known, are not reported in the literature.
Cephalopod ink has potential as an anticancer agent, based on in vitro studies of various cell types and cell lines [ 60 , 78 , ]. The effect is often through the induction of apoptosis and is often associated with different chemicals in ink.
The specificity of the effects on cancerous cells is not often explored in studies in this field. Tyrosinase Section 4. This effect is mediated by purified tyrosinase with no added substrate, so the substrate is probably provided by the human cells themselves. Peptidoglycans from squid and cuttlefish ink Section 4. Mechanisms underlying the effects of cephalopod peptidoglycans may include fragmentation of DNA [ ] and apoptosis [ ], perhaps resulting in the inhibition of embryonic development [ ].
Sepiella maindroni ink polysaccharide SIP , derived by enzymatic digestion of the peptidoglycans Section 4. SIP-SII has anti-cancer activity, which may result from several of its properties: 1 suppression of the invasion and migration of carcinoma cells via inhibition of matrix metalloproteinase-2 [ 85 ]; 2 suppression of melanoma metastasis via inhibition of tumor adhesion mediated by intercellular adhesion molecule 1; and 3 inhibition of angiogenesis mediated by basic fibroblast growth factor [ 87 ].
Sepia ink oligopeptide SIO , extracted from enzymatically digested ink sacs Section 4. Cuttlefish ink may enhance immune responses by affecting hematopoiesis.
For example, it promotes the proliferation and differentiation of granulocyte-monocyte progenitor cells [ ]. An angiotensin-converting enzyme purified from squid ink causes dilation of blood vessels, resulting in lower blood pressure. This represents a potential treatment of hypertension [ ]. Ink from Loligo duvauceli and Sepiella inermis has been reported to have an anti-retroviral activity [ ].
Ink from squid and octopus inhibits gastric secretion of rats and, thus, has potential in the development of anti-ulcerogenic drugs [ , , , ].
The active fraction contains an unidentified low molecular weight melanoprotein that might be responsible for the activity, by enhancing the glycoprotein activity in the gastric mucosa. Mimura et al. Fahmy and Soliman [ ] reported anti-inflammatory effects of Sepia ink.
Cephalopod ink has anti-oxidant activity [ , , , ]. Activity resides in both the melanin and melanin-free fractions of ink [ , ]. This anti-oxidant activity may be related to some of the other effects reported in Section 6. Due to its color and permanence, sepia—the name used for the black ink from Sepia —was extensively used from Greco-Roman times through the 19th century as an ink and pigment used in writing, drawing and painting Figure 9 A.
It can be diluted to yield various shades. Sepia is available and used even today, though modern dyes and pigments with similar hues and other advantages have largely replaced sepia. A modern drawing using ink from a fossilized squid is shown in Figure 6. Cephalopods over the ages have been not only a source of artistic materials, but of artistic inspiration.
One example, a painting of marine life, including an octopus attacking a spiny lobster, is shown in Figure 9 B. Cephalopods in art. Cephalopod ink has been used in various ways in the food industry. Most common is its use as a food flavoring, used worldwide. Most commercially-sold squid ink is actually cuttlefish ink, because of its superior flavor [ ].
Arroz negro black rice , txipirones en su tinta baby squid in ink sauce , ikasumi jiru ink soup with pork and squid and Cavianne an imitation caviar are some of the dishes and foods that use cephalopod ink. Processed ink is used as a food coloring [ ]. Due to its antimicrobial properties see Section 6. Inking is a defining behavior of cephalopods that has attracted the interest of humans for millennia.
This review has summarized what little is known about inking behavior and ink. This section offers some directions that future studies of cephalopod ink and inking might take. In the realm of neuroecology [ ], what is known about the role of ink in defense against predation is almost entirely from observational studies.
Experimental studies are needed to identify molecules and mechanisms underlying ink behavior. Through which sensory channels—visual, chemical, mechanical—does ink affect predators and how? Other than the extensive work on melanin and its synthesis, very little is known about the chemistry of ink, so this is a priority, particularly from a functional perspective. The combined experimental approaches of bioassay-guided fractionation and biomarker targeting will likely be necessary to identify the bioactive molecules in ink, whose chemical composition is complex.
Laboratory studies need to be informed by, grounded in and extended to field observations and experiments. Is there a functional basis to the various forms of released ink—clouds, ropes, pseudomorphs, and so on?
Might these different forms defend individuals in different ways against diversity predators? Almost nothing is known about the funnel organ, which produces the mucus component of ink.
Likely it is to be much more than just mucus, similar to the opaline gland of sea hares, which, together with the ink gland, produces a rich array of bioactive molecules Figure 2 D [ ].
The innervation of the ink sac and funnel organ has received very little attention, and it is not even clear at present if the two organs are controlled by the same or different neural centers. Whether there are differences in signaling pathways neurotransmitters, second messengers, modulators for the two organs is also unknown.
Knowing the independence of the two pathways is essential in determining the mechanisms underlying the production of the different forms of released ink. Experimental approaches to gaining a molecular and biochemical understanding of inking are now available. So far, little has been done along these lines. Several individual genes from the ink sac involved in melanin synthesis have been cloned, for comparative studies of enzymes.
These include peroxidase [ 77 ], tyrosinase [ ] and nitric oxide synthase [ ]. One transcriptome of the ink sac has been generated, which identified another gene involved in melanogenesis—arginine kinase—as well as other genes that are involved generally in metabolism and, therefore, that might play a role in the production, mobilization and release of ink [ ].
Ink has a diversity of benefits to offer us through industrial and medical applications. Two major potential benefits are identifying antimicrobials to treat products used in food, cosmetics and healthcare and developing drugs for use as antimicrobials, anti-cancer, anti-oxidants and more. Our current knowledge of such uses is largely phenomenological, and the chemicals in ink responsible for the effects and the underlying cellular or molecular mechanisms have not been identified.
It will be most useful to find anti-microbial drugs that act through novel mechanisms, given the prevalence of drug-resistant micro-organisms. Natural products have often offered new avenues for drug development [ , ], and given the diversity of medicinal effects of whole cephalopod ink, it offers promise for identifying new, prospective drugs.
This review has summarized what is known about cephalopod ink, particularly related to its production, chemical composition, use by cephalopods in predator-prey interactions, and human applications in drug discovery and development. It is evident from this review that cephalopod ink has been appreciated by humans for centuries, yet so little is known about it. It is hoped that this review encourages a deeper look at cephalopod ink, both as a mechanism of defense for these beautiful animals and as a source of drugs for human consumption.
I thank members of my lab, past and present, as well as other colleagues, who have contributed to the work on inking mollusks and have influenced the ideas expressed in this review. I thank Manfred Schmidt for comments on a draft of the manuscript and Shuichi Shigeno and Stavros Hadjisolomou for helpful discussions.
National Center for Biotechnology Information , U. Journal List Mar Drugs v. Mar Drugs. Published online May Charles D. Author information Article notes Copyright and License information Disclaimer. This article has been cited by other articles in PMC. Abstract One of the most distinctive and defining features of coleoid cephalopods—squid, cuttlefish and octopus—is their inking behavior. Keywords: Cephalopoda, cuttlefish, funnel organ, ink, ink sac, melanin, neuroecology, octopus, predator-prey, squid.
Open in a separate window. Figure 1. Which Cephalopods Produce Ink? Figure 2. What Is Cephalopod Ink? Figure 3. Ink Sac The ink sac has been the object of attention, both casually and scientifically, because of its dramatic black color. Funnel Organ The funnel organ is the second gland contributing to the ink secretion, though much less is known about it than the ink sac. Combining the Two Glandular Secretions Despite the early recognition that the funnel organ is a mucus-producing gland, its function in inking was not realized for some time.
Chemical Constituents of Ink 4. Methodology Matters To understand the roles played by chemicals in natural environments, it is critical to know the natural rates of release of these chemicals from their biological sources and the fluid dynamics in these natural environments and then to examine the effects of these chemicals in the laboratory or field at these ecologically relevant concentrations and temporal-spatial dynamics.
General Composition of Ink As described in Section 3. Melanin 4. What Is Melanin? Production of Melanin in Cephalopods A summary diagram of the pathways leading to the production of eumelanin in Sepia ink glands is shown in Figure 4.
Figure 4. Figure 5. Figure 6. Melanin-Related Compounds As described in the previous section, the melanin-producing pathway in the ink gland has a number of important chemicals, including tyrosine, dopamine and DOPA, and enzymes, such as tyrosinases, peroxidases and dopachrome-rearranging enzymes. Tyrosinases Prota et al. Peroxidases Peroxidases are associated with melanosomes in the ink gland [ 57 , 75 ], where they are thought to catalyze the formation of eumelanin from DHI and DHICA [ 76 ].
Catecholamines The catecholamines, DOPA and dopamine, which are monoamines derived from tyrosine, are substrates of tyrosinase and are reported in the ink of several cephalopods at concentrations ranging from low nanomolar to low micromolar. Peptidoglycans Fucose-rich peptidoglycans have been isolated from ink of several species of squid, including Illex argentines , Ommastrephes bartrami and Sepiella maindroni [ 80 , 81 , 82 , 83 , 84 , 85 , 86 , 87 , 88 , 89 ].
Figure 7. Amino Acids Cephalopod ink is high in dissolved free amino acids. Metals Relatively high levels of metals, such as cadmium, copper, and lead, have been found in cephalopod ink. Toxins Cephalopod ink is not generally known to contain toxins.
Ink as an Anti-Predator Defense 5. Interspecific Effects: Ink as a Direct Deterrent of Predators Inking is a defense coupled to jetting and changes in body coloration, such as in the blanch-ink-jet maneuver [ 2 , ]. Figure 8. Intraspecific Effects: Ink as an Alarm Cue for Conspecifics A second type of anti-predatory chemical defense in the ink of cephalopods functions indirectly—not by acting on the predators themselves, but rather are alarm cues for conspecifics.
Evolution of Melanin as a Defense How might melanin have evolved as a component of the ink defensive secretion of cephalopods? Human Applications of Cephalopod Ink Cephalopod ink has been used by humans for many practical and commercial purposes over the millennia, especially in medicine, cuisine and art, but in even broader applications, as described in this section.
Drugs Cephalopod ink has a long history of being used to promote human health. Antimicrobial Properties Cephalopod ink has antimicrobial properties against a diversity of organisms, including human pathogens [ , , , , , ]. Cephalopod ink can contain a number of different chemicals in a variety of different concentrations based on the certain species. The main component in Cephalopods ink is melanin.
Sound familiar? This is because us humans have this same dark pigment that is responsible for the color of our hair and skin. How cool is that! This special dye is contained in an ink sac, but not all octopuses have an ink sac or the ability to produce ink. Different species of cephalopods also produce different colors of ink as well.
Typically octopus and squid produce black ink, but ink can also be brown, reddish, or even a dark blue. Octopus and Squid use their ink as a defense mechanism to escape from prey. Ink from a few species has been studied but the contents have been shown to vary depending on the extraction technique. Generally, cephalopod ink includes melanin, enzymes related to melanin production, catecholamines, peptidoglycans, free amino acids and metals Derby Cephalopod ink and ink sacs have been processed for a variety of human applications including anti-microbial, immune response enhancing, anti-retroviral and potential anticancer drugs as well as ink for writing and painting.
The most studied component of ink is melanin. Melanin is a natural pigment found across life, it is the pigment in human skin, hair and eyes and it gives ink its characteristic black or dark brown colour. In addition to the clouds of ink created to limit vision and provide an escape route cephalopods can create different effects by changing the amount of ink released, the direction and speed with their flexible funnels and presumably varying mixes of ink and mucus. In combination with changing colour, some cephalopods have been observed creating pseudomorphs of ink, ejections which are interpreted to resemble a cephalopod-like form to would-be predators to confuse them.
Another form of longer thinner streams of ink are called ropes and are speculatively assumed to bear resemblance to stinging tentacles of jellyfish. Experimentally, some ink has been shown to be unpalatable to fish Wood et al. Mucus-rich ink is supposedly a dangerous or annoying substance that interferes with fish gills and some cephalopods react adversely to their own inkings in small containers or in the lab.
The blue-ringed octopus Hapalochlaena lunulata has tetrodotoxin, the deadly toxin it also releases in a bite, in their ink but the concentrations and effect in inking are not known. Living species of the externally shelled nautiluses do not possess an ink sac. Notably, it is absent in the deep-sea octopus group Cirrina and the confusingly named octopus relative the vampire squid. Surprisingly, considering how much we bang on here at Lost Worlds Revisited about preservation biases, ink sacs are found extensively in the fossil record, the earliest described by William Buckland in Although the extinct externally shelled cephalopods ammonoids have an extensive fossil record, their soft tissues are very poorly known and, like extinct and living nautiloids, they are largely presumed to not have possessed an ink sac.
There is some inconclusive evidence that some ammonites may have possessed an ink sac, most recently tiny globules of possible ink remnants were described in Austrachyceras Doguzhaeva et al. In fact the presence of an ink sac is a characteristic feature of this group. Ink is currently unknown from other extinct Coleoidea although this could be due to preservation bias or through secondary loss.
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