Playing “Good Cop, Bad Cop” with Octopuses

Have you ever seen an octopus in an aquarium, or maybe even in the ocean, and thought, “I know you!”? No? Well, they might think that when they see you!

We’ve known for some time that many domestic animals, like dogs, can tell us people apart. It turns out that a lot of animal species can recognize individual people. But how do we humans know that? It’s not like you can walk right up to an animal and say “Hey! Remember me?” ...Well, I guess you could do that, but how would you interpret the answer?

Imagine everything that an animal would have to be capable of to be able to recognize different people: the animal would have to be able to discriminate, learn and remember. Those are pretty complex tasks. Despite our stereotypes of molluscs, octopuses (not “octopi”) are actually quite good at all of these things. They are visual animals that can differentiate between abstract shapes, remember visual patterns, and be conditioned (Conditioning is a process by which an animal learns to associate a behavior with some previously unrelated stimulus). Additionally, many people acknowledge octopuses as the most intelligent (and coolest) of all invertebrates. Furthermore, there have been several anecdotal reports of octopuses recognizing individual people. Some octopuses at aquariums consistently approach the keepers that feed them, even when the keeper is in a crowd of other people. One octopus being trained in a lever-pressing task regularly chose to squirt the researcher in the face rather than press the lever. Another octopus apparently only jetted water at a particular night guard. So octopuses seem like a pretty good species to test individual human recognition (and to test for a sense of humor, but that is for another day).

If you were an octopus, could you tell these two people apart?
Photo by Veronica von Allworden from a figure in the paper
in The Journal of Applied Animal Welfare Science

Roland Anderson and Stephanie Zimsen at the Seattle Aquarium, Jennifer Mather at the University of Lethbridge, and Mathieu Monette at the University of Brussels, set out to do just that. They caught eight giant Pacific octopuses from the wild and took them to the Seattle Aquarium. For 5 days a week over two weeks, they repeated the following process: Two identically-dressed testers played the roles of “good cop” and “bad cop”. Twice a day for each animal, each of the two testers would separately open the tank so they could be seen by the octopus and record its behavior: movements, inking, blowing water, funnel direction, skin color and texture, respiration rate, and the presence or absence of an eyebar (color-changing skin around the eye that may darken due to disturbance). Then, one of them would feed the octopus, and the other would gently poke it with a bristly stick (which was not harmful, but probably pretty irritating). The “good cop” always fed the octopus and the “bad cop” always poked it, although the people that played “good cop” and “bad cop” were different for each animal. The order of the “good cop” and “bad cop” treatments was determined randomly each day. On the last day of the second week, each tester opened the tanks, looked in, and recorded the animals’ behavior.

A giant Pacific octopus displaying his eyebar (shown with the white arrow)
in the wild. Photo by Veronica von Allworden from a figure in the paper in
The Journal of Applied Animal Welfare Science

In the first day or two of testing, octopuses generally moved away from both testers equally, did not have a difference in where their water jets faced or in displaying their eyebars. But in the second week, octopuses generally responded to testers that fed them by moving towards them, aiming their water jets away from them and not displaying eyebars; they generally responded to testers that poked them by displaying their eyebars, aiming their water jets at them, and moving away from them. And some of the octopuses (the larger ones) had faster breathing rates when they saw the testers that poked them than when they saw the testers that fed them.

So octopuses can recognize individual humans, and they treat people differently depending on how they have been treated by the humans. …Hmmm… If octopuses can do it, imagine what other species may be able to do it. Meditate on that the next time you interact with an animal.

Now add individual human recognition to other things we know octopuses can do, like learn and remember skills, play with toys, express personalities, and detect things by vision and smell. And they can do this:

and this:

and this:

I mean really, is there anything octopuses can’t do?

Do you want to get to know the octopuses from this study? Learn to recognize them at the Seattle Aquarium or the Seaside Aquarium, where they are now on exhibit.

Want to know more? Check these out:

1. Anderson RC, Mather JA, Monette MQ, & Zimsen SR (2010). Octopuses (Enteroctopus dofleini) recognize individual humans. Journal of applied animal welfare science : JAAWS, 13 (3), 261-72 PMID: 20563906

2. Mather, J.A., Anderson, R.C and Wood, J.B. (2010). Octopus: The Ocean’s Intelligent Invertebrate. Timber Press, Portland, OR.

3. Octopus Chronicles, a Scientific American blog dedicated to everything fascinating and amazing about octopuses

4. AnimalWise, a blog about animal cognition

The "Love Hormone" of 2012

Hello and welcome to the Love Hormone Pageant Results Show!  You have cast your votes, the results are in, and the “Love Hormone” of 2012 is… (dramatic pause)… Dopamine!

Dopamine is arguably the most exciting of love hormones. A neurotransmitter produced in the brain, dopamine plays a key role in many motivated behaviors (and love, especially falling in love, involves a lot of motivated behavior). It does this mostly through the mesolimbic reward system, which largely consists of dopamine-producing neuron cells in a brain region called the ventral tegmental area and their projections to other brain regions, including the nucleus accumbens. The mesolimbic reward system exists and has been studied in mammals, birds, reptiles and fish, but the story of how dopamine may be involved in “love” has been explored most with one particular mammal species, the prairie vole.

Photo of a prairie vole pair from Young, Gobrogge, Liu
and Wang paper in Frontiers in Neuroendocrinology (2011)

The prairie vole is a small rodent from the grasslands of the central United States. Unlike approximately 97% of mammal species, prairie voles are socially monogamous and form long-term pair bonds. Male and female pairs travel together, nest together and share parenting duties. Pairs tend to stay together for life and when one partner dies, the surviving partner may never re-pair with a new mate. The role that dopamine plays in how these pair bonds are formed between prairie vole couples has been studied extensively over the last 13 years by Zuoxin Wang at Florida State University and over 30 of his colleagues. Kimberly Young, Kyle Gobrogge, Yan Liu and Zuoxin Wang summarize much of this work in a recent review.

Graph showing that prairie voles prefer to
spend time with their partner after 24 hours
of living together and mating:fromYoung,
Gobrogge, Liu and Wang paper in
Frontiers in Neuroendocrinology (2011)

If you put a virgin male and a virgin female prairie vole in an enclosure and let them live together and mate for 24 hours, they will reliably prefer to spend time with each other rather than with a stranger if given that choice – this is called partner preference. If you enhance dopamine action in the brain, this partner preference will happen even sooner and if you block dopamine receptors throughout the brain, it won’t happen at all. This pattern is even true if you change dopamine action only in the nucleus accumbens, showing that dopamine binding in the nucleus accumbens is critical for the formation of partner preference and pair bonds.

The effect of a hormone or neurotransmitter is completely dependent on its receptors: where they are, how many there are, and how well things bind to them. Dopamine receptors can be classified into two main families, called D1-like and D2-like receptors, and they often have opposite effects. For example, in the prairie vole nucleus accumbens, activating D2 receptors or blocking D1 receptors will cause partner preference to form faster, whereas blocking D2 receptors or activating D1 receptors will prevent it from forming at all. Furthermore, male prairie voles develop more D1 receptors in the nucleus accumbens during pair bonding, which likely work to prevent the animal from forming a pair bond with a second female and keeping him faithful to his mate. Interestingly, promiscuous meadow voles generally have more D1-like receptors in the nucleus accumbens than closely related but monogamous prairie voles. So in the prairie vole nucleus accumbens, activation of D2 receptors promotes the formation of pair bonds and activation of D1 receptors prevents the formation of pair bonds.

However, dopamine is not all roses and chocolate hearts. The action of dopamine in the mesolimbic reward system, and especially in the nucleus accumbens, regulates much more than pair bonding; It regulates a whole suite of motivated social behaviors, like sexual, parental, play, and aggressive behaviors, as well as other motivated behaviors, like seeking food and drugs of addiction. Furthermore, mesolimbic dopamine seems to be at the heart of the interactions between drugs of abuse and social behavior. In another recent review by the same research group, Wang and his colleagues point out that brief exposure to any known drug of abuse activates dopamine activity in the nucleus accumbens and repeated drug exposure causes long-lasting or permanent changes to mesolimbic reward brain areas like the nucleus accumbens. For example, repeated exposure to psychostimulants increases the number and sensitivity of D1 receptors in the nucleus accumbens…Wait, what do active D1 receptors in the nucleus accumbens do? Oh yeah, they prevent pair bonding and partner preference formation. And not surprisingly, giving amphetamine (a psychostimulant) to prairie voles prevents them from forming partner preferences and pair bonds. So if you don’t want to hurt your chances of falling in love some day, just say “No” to drugs, mmmkay?

Dopamine is a busy neurohormone: It is not only involved in love and motivated behaviors, but is also involved in everything from voluntary movement, mood, punishment and reward, cognition, memory, learning, aggression, pain perception and sleep. It is also important to keep in mind that dopamine does not work alone. To regulate pair bonding and partner preference, dopamine interacts with oxytocin, vasopressin, glutamate, GABA, and corticotrophin-releasing factor. But then again, love is about as complex a brain function as you can get – we couldn’t expect a single hormone to go it alone!

So put your hands together one last time to celebrate the “Love Hormone” of 2012: Dopamine!

Want to know more? Check these out:

Young, K., Gobrogge, K., Liu, Y., & Wang, Z. (2011). The neurobiology of pair bonding: Insights from a socially monogamous rodent Frontiers in Neuroendocrinology, 32 (1), 53-69 DOI: 10.1016/j.yfrne.2010.07.006

Young, K., Gobrogge, K., & Wang, Z. (2011). The role of mesocorticolimbic dopamine in regulating interactions between drugs of abuse and social behavior Neuroscience & Biobehavioral Reviews, 35 (3), 498-515 DOI: 10.1016/j.neubiorev.2010.06.004

The "Love Hormone" Pageant

Since the beginning of…well, social animals, many hormones have been quietly working in their own ways to fill our world with love. Lately (over the last few decades), some of these hormones have been brought out of the background and into the limelight, credited with every crush, passionate longing, parental hug, embrace among friends, and cuddle between spouses. Our reining title-holder, Oxytocin, has received unbridled news attention about how it is responsible for creating and maintaining love and has even been marketed as a product to make people fall and stay in love! But is Oxytocin really the patron hormone of all that is love? Who truly deserves the title of The Love Hormone?

Let’s meet our contestants! Here's our reining title-holder, Oxytocin! Oxytocin is a peptide hormone, most of which is made in the brain. Some of this oxytocin is released into the blood and affects body organs, such as the uterus and cervix during child birth and the mammary glands during breast feeding. But some of it stays in the brain and spinal cord, acting on neurons with oxytocin receptors to affect a number of behaviors. Released during child birth and nursing, oxytocin is important for helping mammalian mothers behave like moms and in species in which both parents raise young, it helps fathers behave like dads. Also released during sex, oxytocin plays an important role in pair bonding in some monogamous species, like prairie voles (particularly in the female of the pair). In humans, people given oxytocin nasal sprays have been reported to have less fear, more financial trust in strangers, increased generosity, improved memory for faces, improved recognition of social cues, and increased empathy.

But before you fall head-over-heels for oxytocin, you should know a few more things. For one thing, oxytocin isn’t exclusively linked with feel-good emotions; It has also been associated with territoriality, aggressive defense of offspring, and forming racist associations. Also, oxytocin doesn’t work alone. It has been shown to interact with vasopressin, dopamine, adrenaline and corticosterone and all these interactions affect pair bonding.

Next up is Vasopressin! Vasopressin is closely related to oxytocin. Like oxytocin receptors, vasopressin receptors are expressed in different patterns in the brains of monogamous vole species compared to promiscuous vole species. Released during sex, vasopressin plays an important role in pair bonding in monogamous prairie voles (particularly in the male of the pair). If you block vasopressin in the brain of a paired male prairie vole, he will be more likely to prefer spending time around a new female rather than his mate. On the flip side, if you increase vasopressin activity in specific brain regions of an unpaired male prairie vole or even a promiscuous male meadow vole and introduce him to a female, he will prefer spending more time with her than with other females. Vasopressin may also make male prairie voles more paternal.

But vasopressin does a lot of things. In the body, its primary function is to regulate water retention. In the brain, it plays a role in memory formation and territorial aggression. And even its role in monogamy is not exclusive: Vasopressin interacts with oxytocin and testosterone when working to regulate pair bonding and parental behavior.

Please welcome Dopamine! Dopamine is a neurotransmitter produced in the brain. Sex increases dopamine levels in both males and females and blocking its effects during sex can prevent prairie voles from forming preferences for their own partner. Dopamine also plays a role in maternal and paternal behaviors. But dopamine is not just involved in love. It has a wide range of known functions in the brain, involved in everything from voluntary movement, mood, motivation, punishment and reward, cognition, addiction, memory, learning, aggression, pain perception and sleep. Abnormally high levels of dopamine have been linked to schizophrenia and psychosis.

Look out for Cortisol! Cortisol is produced by the adrenal glands (on top of the kidneys) and is involved in stress responses in humans and primates. Both men and women have increased cortisol levels when they report that they have recently fallen in love. Many studies have also found relationships between cortisol and maternal behavior in primates, but sometimes they show that cortisol increases maternal behavior and sometimes it prevents it. In rodents, where corticosterone plays a similar role to cortisol, the story is also not very clear. Corticosterone appears to be necessary for male prairie voles to form pair bonds and it plays a role in maintaining pair bonds and promoting parental behavior. But in female prairie voles, the opposite seems to be true! Corticosterone in females appears to prevent preference for spending time with their partner and pair bond formation.

Put your hands together for Testosterone! Testosterone is a steroid hormone and is primarily secreted from the gonads (testes in males and ovaries in females). Frequently referred to as “the male hormone”, both males and females have it and use it, although maybe a little differently. Testosterone is associated with sex drive in both men and women. But men who have recently fallen in love have lower testosterone levels than do single males, whereas women who have recently fallen in love have higher testosterone than single gals.

This is Estrogen! Estrogen is another steroid hormone, frequently referred to as “the female hormone”, although again, both males and females have it. Estrogen also seems to play a role in sex drive in both men and women. The combination of high estrogen levels and dropping progesterone levels (another steroid hormone) is critical for the development of maternal behavior in primates, sheep and rodents. But look closer and you will find that the activation of estrogen receptors in particular brain regions has also been associated with lower sexual responsiveness, less parental behavior, and less preference for spending time with the mate.

So let’s have a round of applause for this year’s contenders in The Love Hormone Pageant! Now it is your turn to voice your opinion in the comments section below. Vote for the hormone you believe deserves the title The Love Hormone. Or suggest an alternative pageant result!

And check back next week for the results of The Love Hormone Pageant!

Want to know more? Check these out:

1. Young, K.A., Gobrogge, K.L., Liu, Y. and Wang, Z. (2011). The neurobiology of pair bonding: Insights from a socially monogamous rodent. Frontiers in Neuroendocrinology, 32(2011), 53-69.
2. Van Anders, S.M. and Watson, N.V. (2006). Social neuroendocrinology: Effects of social contexts and behaviors on sex steroids in humans. Human Nature, 17(2), 212-237.
3. Marazziti, D. and Canale, D. (2004). Hormonal changes when falling in love. Psychoneuroendocrinology, 29, 931-936.
4. Fisher, H.E. (1998). Lust, attraction, and attachment in mammalian reproduction. Human Nature, 9(1) 23-52.

Friends with Benefits

"It is not so much our friends' help that helps us
as the confident knowledge that they will help us."
-Epicurus, Greek philosopher (341 - 270 BC)

“Silences make the real conversations between friends.
Not the saying but the never needing to say is what counts.”
-Margaret Lee Runbeck, American author (1905 - 1956)

photo by Jérôme Micheletta, Macaca Nigra Project

Where would we be without our friends? Friends lend a hand in bad times and cheer us on in good times. They make us laugh, share their food, and tell us where to find interesting things… like fruit or coconuts!

Okay, so maybe finding fruit and coconuts isn’t that high on your priority list, but it seems to be pretty high on the list for crested macaques. And lucky for them, they have friends to rely on too.

Jérôme Micheletta and Bridget Waller at the University of Portsmouth in the United Kingdom set out to determine whether social factors influence the ability of crested macaques to follow the eye gaze of a group-mate and potentially gain important information. To do this, they hung out at the Marwell Wildlife Zoological Park in Winchester, U.K. every day to watch and video record the crested macaques. An experimenter would wait for two crested macaques to be within 1 meter of each other with one individual facing the experimenter (they called this animal “the informant”… not to be confused with Matt Damon) and the other individual facing the informant and facing away from the experimenter (they called this animal “the subject”). You can imagine, this process involved a lot of waiting around. Once the animals were in place, the experimenter held up a yummy treat (an orange, a banana, or a coconut). The informant would see the treat and then the subject would either look at the treat or not. In these cases, the subjects looked at the treats 64% of the time.

This figure from Micheletta and Waller's Animal Behaviour
paper shows their experimental procedures.

But how do we know that the subjects followed the informants’ gaze and didn’t respond to something the experimenter or some distant cage-mate did? Micheletta and Waller also recorded the responses of the same animals in a control situation: the experimenter would wait for a subject to be away from its cage-mates, but with its back turned to the experimenter. Then the experimenter would hold up the yummy treat. In these control trials, the subjects looked at the treats only 7% of the time.

So it looks like crested macaques use their peers’ eye gaze as information on where to look. They also were faster to look if their cage-mate moved his/her head in combination with an eye movement, rather than just the eyes. But, does the social context matter? For each pair of macaques, Micheletta and Waller calculated the relative dominance status and friendship strength. They used months of observations of aggressive encounters in which they knew the winners and losers of each encounter to rank the overall dominance hierarchy of each animal in the group. A typical aggressive encounter either involved one monkey chasing another (which would either run away or crouch) or a monkey approaching another and taking away his/her food or grooming-buddy or mate (How rude!). They also determined friendship strength by calculating the average number of times they sat in contact with or groomed a specific individual versus other animals in the group.

If the informant was a friend, the subject was quicker to look at the food than if the informant was not a friend, although friendship did not influence the overall success rate. And the relative dominance status didn’t seem to have any effect.

Why might macaques follow their friends’ gazes faster than nonfriends’ gazes? Maybe they are generally more visually attentive to their friends than their nonfriends, as is true in chimpanzees, siamangs, chacma baboons and ring-tailed lemurs.  Or maybe a friend’s information is more relevant than a nonfriend’s information. Friends often share motivations and needs and often compete less and share more with each other than with nonfriends (although there are many exceptions to this, as you may have experienced). All of these possibilities leave open new avenues for future research. But one thing is clear: It sure is good to have friends.

Want to know more? Check this out:

Micheletta, J., & Waller, B. (2012). Friendship affects gaze following in a tolerant species of macaque, Macaca nigra Animal Behaviour, 83 (2), 459-467 DOI: 10.1016/j.anbehav.2011.11.018

Do you have a thought on friends that you would like to share? Comment below.

Y'all tawk funny, doncha know

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Within the last year, I have moved from Wisconsin to Texas and back to Wisconsin and no matter where I am people poke fun at my occasional word choices and pronunciations. For a girl who didn’t grow up in either state, it can be a lot to keep straight. In Texas, if I couldn’t fit my bucket under the water fountain to fill it, I would fill it at the spigot. But in Wisconsin, if my pail doesn’t fit under the bubbler, I fill it at the faucet. Usually, it’s not a problem, because I don’t often fill buckets or pails. But it has also affected my fashion-sense, because I can never remember if I have a “whaht bag” or a “white bague”… so now I just carry a black purse.

All of our struggles for dialectal conformity (admit it, even you have tried to talk like the cool kids at times) have come from the fact that we learn language through both vertical and horizontal transmission (and no, I’m not talking about the way STDs are spread). We learn language both from our parents (vertical transmission) and our peers (horizontal transmission). We now suspect that orcas (also called killer whales) do too.

Photo by Olga Filatova

Orcas live in matrilineal units consisting of a mother and her offspring. Related matrilineal units will travel together in larger groups, called pods. Although pods may come together for hunting, mating or other social interactions, each pod has a unique collection of call types (called a vocal repertoire or dialect). Some call types may be similar among some pods, and pods that share some call types are considered to be part of the same clan. Pods that do not share any call types are considered to be from different clans.

Orca individuals learn their pod’s dialect from their mothers. This in itself is pretty impressive: vocal learning is rare in mammals (exceptions being humans and some whales, dolphins, seals, and bats). The classical theory of orca dialects (yes, there is a classical theory of nearly everything) argues that dialects are transmitted only vertically (from mother to calf), and that changes in dialects between pods occur due to the accumulation of copying errors. Think of the game of “Telephone”, where one person whispers a message, such as “I like vanilla ice cream with caramel on top”, which is then whispered to the next person and then the next person, until the message received by the person at the end of the line is something like, “Ike the gorilla had a nice dream about Carrot Top". A collaborative research team from Russia and the UK are now challenging that idea with evidence suggesting that adult orcas also learn from other adult orcas.

This research team, including Olga Filatova at Moscow State University, Alexander Burdin at the Pacific Institute of Geography, and Erich Hoyt at the Whale and Dolphin Conservation Society, determined which call types were included in the repertoires of 11 orca pods that were all members of the same clan. Then for each call type, they compared how similar the calls were across all pods that produced it. This data doesn’t come easy: they recorded orca calls off the Kamchatka Peninsula from an inflatable motor boat with an outboard motor for the better part of a decade. After analyzing all of the recordings, they discovered that different call types can vary in their degree of similarity across pods, suggesting different patterns and rates of change from pod to pod. If differences in pod dialects come about only due to copying errors when calves are learning from Mom, we would expect more consistent rates and patterns of change of calls across pods. One possible explanation is that when pods come into contact with one another and socially interact, adult orcas learn new call types (like we learn new words) and/or adjust features of call types (like we change our pronunciation of a word) from individuals in other pods. So the next time you find yourself far from home and talkin’ a little differ’nt, at least you’ll know you ain’t the only one.

Here are two orca recordings from two different clans (Kaplya pod and Avacha clan). Personally, I think they both sound like clowns making animal balloons. But if you can tell the difference, maybe you have a future in animal behavior research… or maybe you’re the next Dr. Doolittle.

Wanna know if you talk funny? Take this test.

Want to know more? Check these out:
1. Filatova, O.A., Burdin, A.M., Hoyt, E. (2010). Horizontal transmission of vocal traditions in killer whale (Orcinus orca) dialects. Biology Bulletin, 37(9), 965-971.
2. Ivkovich, T., Filatova, O.A., Burdin, A.M., Sato, H., Hoyt, E. (2010). The social organization of resident-type killer whales (Orcinus orca) in Avacha Gulf, Northwest Pacific, as revealed through association patterns and acoustic similarity. Mammalian Biology, 75(3), 198-210.
3. Deecke, V.B., Ford, J.K.B., Spong, P. (2000). Dialect change in resident killer whales: implications for vocal learning and cultural transmission. Animal Behaviour. 60. 629-638.
4. The Russian Orcas Homepage

Join the conversation by leaving a comment below.