Dissecting Behavior

Dogs, Science, and the Biology of Behavior

Tag: behavior

What is behavior?

The Question of Behavior

What exactly is behavior?  What is it that we are examining when we inquire about the behavior of animals?  This question is not as straightforward as one might think.  There is a significant amount of disagreement on the subject that benefits from consideration.  In a paper by Levitis et al. (2009), the question of ‘what is behavior?’ was asked of professors and professionals from three different scientific societies.  Of the eight operational definitions the authors proposed from various texts, the highest agreement on any single definition only included 44% of the respondents.  Even more problematic is that 52% of the respondents showed contradictory answers—implying that the respondents’ conceptions of behavior was not guided by an operational definition of behavior but of their personal biases (most likely due to their individual areas of interest).  For instance, even though 99.1% of the respondents agreed that “geese flying in a V formation” constitutes behavior, 31% of the respondents answered that only individuals, not groups, are capable of behavior.  In argument form, this line of deduction would look like this:

Premise 1:       Only individuals, not groups, are capable of behaving
Premise 2:       Geese flying in a V formation constitute a group
———————————————————————————-
Therefore:       The group of geese is behaving

This is a flawed argument to say the least. The benefit of operational definitions is that they allow us to organize our observations through logical lines of reasoning, thus contradictions in logic are a significant red flag that bias has taken place of a scientific definition.  One potential explanation for this is that in Levitis et al.’s (2009) background research to gather published definitions for the term “behavior,” over one hundred publications that they felt should have had a definition for behavior had completely avoided defining the term, either by choice or due to the assumption that people intrinsically know what behavior is.  I hope it has been successfully illustrated that the latter conclusion is clearly not the case.

The Definition of Behavior

A quick thumb in the dictionary informs us about a common preconception: “behavior is the way in which an animal or person acts in response to a particular situation or stimulus.”  In fair agreement with this definition, Tinbergen defined behavior as “the total movements made by the intact animal” (Tinbergen, 1955).  However, what if we were to talk about the behavior of a plant?  Some species of orchids (e.g. Ophrys speculum) use chemical signals to mimic virgin females of their insect pollinators to deceive male insects into attempting reproduction with their flowers: thus causing the male insect to pollinate the orchid (Ayasse et al., 2003). Deception (the action of altering the perception of another to believe something that is not true in order to gain some personal advantage) is most certainly a phenomenon most anyone would associate with behavior.  However a plant is not an animal, so evidently the concept of behavior has to expand beyond just animals if it is going to include deception.

Looking-glass-orchid-flowers

Ophrys speculum evolved features which mimic female reproductive organs in order to deceive male insects, thus increasing their ability to be pollinated.

Conceivably then we could expand the parameter of the definition to multi-cellular organisms.  Having said that, such a classification would then exclude bacteria.  Bacteria are single-cell organisms that meet all eight of the requirements that define life: (1) they have an internal organization; (2) they store and retrieve information through the organization of nucleotides; (3) they have a metabolism that converts energy from an unusable to a usable form; (4) they respond to the environment; (5) they grow and develop; (6) they regulate and maintain homeostasis; (7) they reproduce; and finally, (8) they evolve.  One could argue that if you momentarily exclude reproduction and evolution, all of the requirements of life facilitate just one organismic phenomenon: homeostasis.  So the first argument from the skeptic must be to show that a living entity that is responding to its environment is not capable of behavior.

It might seem unorthodox for many readers to discuss the behavior of bacteria, however even Skinner was not without his philosophical views of the behavior of single-cell organisms and discussed the stretching of an amoeba’s limbs as a an example of early behavioral evolution (Skinner, 1984).  In fact, amoebas are part of the group Protozoa which comes from the Greek for “first animal.”  Protozoa were named this because of their animal-like behavior, from their movement to their reliance on consuming other organisms for survival.  While I share no disagreement with Skinner regarding the behavior of single cell organisms, where I do disagree is in the view that the work of Jacques Loeb (1915) is sufficient in providing a sound argument that the behavior of “lower” organisms only needs explication in what the organism does as a whole—a recurrent theme which Skinner also applied to the behavior of larger organisms as well (Skinner, 1987).

This view is incredibly limiting.  In the hundreds years following Loeb, we have discovered more about the behavior of all organisms (prokaryotes [archaea & bacteria] and eukaryotes) by investigating internal cellular functions.  Indeed, researchers recently discovered that bacteria are able to activate a host body’s immune response to attack an invading virus that threatens the survival of their host they are living symbiotically with (Ichinohe et al., 2011).  Researchers discovered this behavioral response by analyzing signals that lead to the synthesis of mRNA essential to the immune response—a discovery that has launched an entirely new field of inquiry to other ways medicine might fight deadly diseases.  However, this extraordinary level of symbiotic behavior is still poorly understood, so for our purposes let us take a look at a simple environmental response in a single cell of Escherichia coli as an example of adaptive behavior in bacteria.

When E. coli are in a high solute, hypertonic environment, their life is instantly endangered by diffusion’s closest relative: osmosis.  Osmosis is the movement of water from an area of higher free energy to an area of lower free energy (Saupe, 2013).  Solutes (dissolved molecules) affect this process by affecting the free energy of the water the same way that rush hour traffic decreases the kinetic energy of a freeway—the more traffic in the solution (presence of solutes), the less available free energy.  If the solutes from the E. coli’s environment diffuse across its membrane through its pores, osmosis might destroy and kill the cell because freely permeable water will pass across the membrane until the free energy inside the cell is equal to that outside.  If the presence of solutes is dense enough, the E. coli will explode and die.

E. coli would not have survived for the eons they have been around for if a handful of solutes made them explode, thus their behavioral response is an extremely effective defensive mechanism rooted in their DNA.  When E. coli senses the presence of solutes, they transmit a signal to begin transcribing and translating sections of DNA into proteins that will block the pores and prevent solutes from diffusing across the membrane—thus maintaining homeostasis.  There is no question that these actions of E. coli are essential for their survival and fit perfectly well along side the adaptive behaviors of plants and animals.

Permitting then that we include single-cell organisms in our definition of behavior, what then do we do about viruses?  Viruses have no cells.  They are purely microscopic packets of genetic code wrapped in a protein shell.  Consequently, viruses lack the essential organelles required for replication, thus in order for a virus to reproduce it literally breaks open the membrane of a host cell by using spikes on its protein shell that act like a medieval battering ram to break down the gates and invade.  This allows the virus to use the mechanisms within the fully functioning host cell to replicate its viral genetic code like nefarious molecular zombies (see Grove & Marsh, 2011).  Interestingly, scientists analyze viruses in terms of their (1) physical structure, (2) proximate causation, (3) temporal effect on the fitness of a host which impacts the virus’s capacity for survival, and (4) evolutionary development—Tinbergen’s four questions of behavior (Erkoreka, 2010; also see Tinbergen, 1963).  If viruses are incapable of behavior, are Tinbergen’s four questions irrelevant?  Such a claim would create an upheaval in the behavioral literature.

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Here is another way we might ask ourselves about the behavior of viruses.  Let us for the sake of argument claim that viruses are not capable of behavior.  If this is true and we are to exclude these molecular zombies from the definition of behavior, why then do we commonly say that viruses attack cells?  Are we just attributing the behavioral characteristics of animals to non-animal entities or is it really valid to say that these molecular zombies are truly attacking and threatening the homeostasis of an organism?  Even the dictionary cites a definition for “attack” as the aggressive action of a disease.  Viruses obviously meet this criterion so then are we to exclude the behavior of attacking from the definition of behavior just so we can deprive these mysterious molecules of behavior?  While colloquialisms are generally poor grounds for scientific exploration, in this case I would argue that they bear important consideration to the question at hand.  After all, it would be ignorant to deny that common expressions reflect our experiential perceptions of the world (known in science as empirical observation).

The fact that these molecules are nothing but packets of genetic material and literally straddle the definitional requirements of life yet have actions attributable to behavior quickly leads us into questions about non-living entities—for example, do rocks behave?  If an individual was to pick up a rock and throw it, is the rock behaving?  A definition that relied purely on the reactions of matter to its environment would require us to include every rock on Earth as a behaving entity since rocks are quite literally orbiting the Sun as the Earth moves through our solar system.  Using Newtonian physics, we would stipulate that the rock is exerting a force on the Earth equal to that of the force of the Earth on the rock.  Instead of thinking about a small rock, what if we were to look at hydrogen dioxide (water).  The behavior of water makes it one of the most unique molecules in existence.  Three of waters most important behavioral characteristics (i.e. properties) are that it is a powerful solvent, it sticks to itself because it is polar and thus can generate incredible surface tensions, and it is denser as a liquid than as a solid.  If any one of these three properties were different, life would not exist as we know it today.  Molecules have observable, quantifiable properties which respond to other molecules in the environment, therefore why can’t molecules behave?

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One might argue for a definition that stipulated some kind of internal propulsion or energy source which might allow us to exclude a rock.  But would this criterion be valid?  Even though the energy used by animals is converted from an unusable to a useable form through internal metabolic processes, we have already established that the source of all energy for every organism comes from the Sun.  The survival of any animal would be immediately threatened without the energy mitochondria (prokaryotic organisms) produce or the symbiotic benefits offered by gut flora (prokaryotic organisms like E. coli), thus the behavior of animals cannot be observed without the impact of the organisms acting on them.  In a similar fashion, no organism lives in a void.  We shouldn’t forget, as silly as the concept of a rock behaving may seem, all animal behavior is subject to the physical laws of nature.  A bird cannot fly without overcoming the necessity to generate lift, neither could energy be converted to facilitate homeostasis or motion without adhering to the intrinsic properties of atomic theory.  If an owl is diving on a field mouse, prey capture could not occur without the effects of gravity—thus the very action pattern depends on the same phenomenon that determines the travel path of a rock that is thrown.  It should be mentioned that the skill of a bird negotiating with the physical properties of lift is equal to any human pilot, even though the mechanisms are obviously different, and while the Border Collie is unlikely to recite Newton’s laws of motion, they have a skill in predicting the motion of a Frisbee equal to any Ultimate Frisbee competitor.

Any general definition of behavior must allow for all of the nuances mentioned so far if it is to permit our inferences to take into account the immense diversity of behavior in the world.  Thus, returning to Tinbergen, I will modify and broaden his insight and offer that behavior is the total measurement of movements (both internal and external—regardless of physical or biological limitations) of an entity through its environment.  More simply: behavior is the response of a system to a stimulus.  Therefore, since every particle in the universe is in motion and endlessly responding to stimuli, by this definition we can conclude that everything—even a subatomic particle—is in a constant state of behavior.

Such an incredibly broad definition may at first seem either ridiculous or of little value, yet I would contend that there is nothing more valuable than to question our preconceptions with a logical and unbiased deductive thought process.  There is no reason to exclude rocks as behaving entities in the world, and a rejection of this has more to do with the novelty of it (“well I just don’t like it..”-type of response) than of the reasoning to the question.  Furthermore, I would argue that the benefit of such a definition provides a common concept to be discussed whether the system involves entire populations or just a single atom.

Previously I cited the opinion from Levitis et al’s (2009) study that 31% of participants believed that only individuals, not groups, are capable of behavior.  Problematically, the behavior of the human body is the result of the sum of movement of molecules from within—therefore how can we say that the movement of trillions of molecules inside a single organism is “behavior” yet preclude the sum of a group of geese performing an action (such as flying in a V formation) as a behaving entity?  I have no doubt that a five-minute discussion with a police officer that has had to respond to a riot can attest to the behavioral differences of an angry mob versus that of an angry individual.  The tendency for human nature to warp their perceptions to fit their preconceptions makes the ability to integrate new information very difficult; especially if that information negates beliefs we have held for a long time.  As Tinbergen states:

“… if we overdo this in itself justifiable tendency of making description subject to our analytical aims, we may fall into the trap some branches of Psychology have fallen into, and fail to describe any behaviour that seems ‘trivial’ to us; we might forget that naïve, unsophisticated, or intuitively guided observation may open our eyes to new problems.  Contempt for simple observation is a lethal trait in any science, and certainly in a science as young as ours.”  (Tinbergen, 1963)

A definition for behavior that includes all matter in the universe, while useful for expanding our perceptive lens, may not initially seem to provide a productive answer for our question of what is animal behavior.  If narrow perspectives risk losing the forest through the tree, this might be like losing the forest in the galaxy.  What should be emphasized is that the question of what is behavior is only productive if the nature of the entity exhibiting the behavior is definitively described.  The behavior of organisms is thus our aim, and this behavior is intrinsically tied to the fact that organisms—regardless of their complexity—are bound to their biological nature.

References:

Ayasse, M., Schiestl, F. P., Paulus, H. F., Ibarra, F., & Francke, W. (2003). Pollinator attraction in a sexually deceptive orchid by means of unconventional chemicals. Proceedings of the Royal Society B: Biological Sciences, 270(1514), 517–522. doi:10.1098/rspb.2002.2271

Erkoreka, A. (2010). The Spanish influenza pandemic in occidental Europe (1918-1920) and victim age. Influenza and Other Respiratory Viruses, 4(2), 81–89. doi:10.1111/j.1750-2659.2009.00125.x

Freeman, S., Quiliin, K., & Allison, L. (2013). Pearson – Biological Science (5th edition.). San Fransisco, CA: Benjamin Cummings.

Grove, J., & Marsh, M. (2011). Host-pathogen interactions: The cell biology of receptor-mediated virus entry. The Journal of Cell Biology, 195(7), 1071–1082. doi:10.1083/jcb.201108131

Ichinohe, T., Pang, I. K., Kumamoto, Y., Peaper, D. R., Ho, J. H., Murray, T. S., & Iwasaki, A. (2011). Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proceedings of the National Academy of Sciences, 108(13), 5354–5359.

Levitis, D. A., Lidicker, W. Z., & Freund, G. (2009). Behavioural biologists do not agree on what constitutes behaviour. Animal Behaviour, 78(1), 103–110. doi:10.1016/j.anbehav.2009.03.018

Loeb, J. (1915). On the role of electrolytes in the diffusion of acid into the egg of Fundulus. Journal of Biological Chemistry, 23(1), 139–144.

Saupe, Stephen G. (2013). Letter to the Editor. American Biology Teacher, 75(1), 4-5.  DOI: 10.1525/abt.2013.75.1.2

Skinner, B. F. (1984). The evolution of behavior. Journal of the Experimental Analysis of Behavior, 41(2), 217–221.

Skinner, B. F. (1987). Whatever happened to psychology as the science of behavior? American Psychologist, 42(8), 780–786. doi:10.1037/0003-066X.42.8.780

Tinbergen, N. (1955). The Study of Instinct. Oxford: Clarendon.

Tinbergen, N. (1963). On aims and methods of Ethology. Zeitschrift für Tierpsychologie, 20(4), 410–433. doi:10.1111/j.1439-0310.1963.tb01161.x

Blogging Down Our Brains

“By giving us the opinions of the uneducated, journalism keeps us in touch with the ignorance of the community.” – Oscar Wilde

Anyone interested in furthering his or her knowledge of a subject is faced with a depressing enigma: the amount of bad information outnumbers the amount of good information.  As a person who lives life trying to acquire a deeper understanding of the world, bad information really pisses me off.

Recently, a blog was published titled “5 Incredible Ways Dogs Can Read Your Mind” (Emery, 2013).  In it, the author presents several claims to support the premise that dogs can read our minds.  Formally, this is referred to as Theory of Mind, which Emery defines as the “understanding that other beings have different perceptions, and that those perceptions can be valuable” (Coren, 2011a).  This is wrong.  To be fair, even scientists do not always define it accurately, however choosing a blogger to reference who actually took the time to read the conclusions and discussions of the studies they were reviewing might have been a beneficial start.

The correct definition:

Theory of mind is the ability to make accurate inferences to understand the behavior of other animals because of abstract (theory-like) representations of the causal relationship between unobservable mental states and observable behavior (Premack & Woodruff, 1978, as cited in Penn & Povinelli, 2007—emphasis my own).

More concisely, theory of mind requires the ability to know that the behavior of another animal is a product of their cognitive state—this is distinctly different from responding to environmental factors, including that of an animal’s behavior (Udell & Wynne, 2011).  While many authors have described theory of mind as dated and potentially no longer useful (e.g. Horowitz, 2011), the goal of this blog isn’t to provide alternative evidence as to whether or not theory of mind is a valid concept in non-human animals such as dogs—best to let that war rage on in the academic community.  Instead, this blog is two-fold: 1) to correct the dirge of fallacies that went viral with Emery’s blog and 2) to use it as a model for understanding how important the source of information is.  With that as our base, let’s start at the top.  If you haven’t read the blog I am referring to yet, here is the link.

Note: the titles of each section below correlate to the paragraph titles of Emery’s blog and are here to give sign posts regarding what statements I am pulling apart: they are not claims I am making.

#5: Dogs are Capable of Empathy

“Yawning is a phenomenon directly connected to empathy, and as such has only been found to occur in species capable of empathizing (i.e. humans, and other primates), and only then within a single species.” (Emery, 2013)

First, yawning behavior is widespread and believed to be common to ALL vertebrates: including mammals, birds, fish, amphibians and reptiles (Baenninger, 1997).  Second, there are EIGHT different hypotheses regarding the function of yawning, if it is indeed even functional, and so the communication (empathy) hypothesis is just one of several ‘stabs’ at why animals yawn (Guggisberg et al. 2010).  Problematically, the communication hypothesis is not unilaterally supported and the studies that do support it are plagued with a lack of controls to rule out competing hypotheses that would be direct confounds to the results.  Even if we accepted that contagious yawning as a function of empathy was viable and true, researchers employing more stringent methods have been unable to conclude that dogs show signs of contagious yawning behavior (Harr et al., 2009).

“So obviously dogs have an uncanny ability to read our emotions … but how? Well, it’s because all humans, whether right- or left-handed, display our emotions predominantly on the right side of our faces.” (Emery, 2013)

You’d think with a 50/50 chance she might have gotten this one right merely by dumb luck—but no, humans display their emotions predominantly on their LEFT side, not their right (Borod et al. 1997).  Regardless of problems between lefts and rights, associative learning is an alternate explanation for any gaze bias observed in dogs.  However, perhaps ironically, it could even be argued that if dogs could read our mind, then they wouldn’t need to check in with the more emotional side of our face to know if we are just slightly angry about the Christmas ham getting eaten, or really angry.  Empathy is an equally hot topic as theory of mind and definitions historically have tended to overlap—often stressing the importance of “cognitive perspective taking” (Davis 1983).  Despite the sticky separation of these concepts, empathy refers to the ability of one individual to infer and share the emotional spectrums of another (Gallese, 2003; Völlm et al., 2006).  Thus, regarding whether or not non-human animals have empathy, gaze research simply cannot possibly answer the question.

#4: Dogs Understand That Your Visual Perspective Is Different from Their Own

Yes, they do, but does this constitute evidence that they possess theory of mind?  Opponents to the “perspective taking” element supporting theory of mind make a compelling counterargument: simply that all animals learn.  If a moose walks into a tree, they do not turn around and walk the other way because at some point in their life they learned they could walk around it.  A group of gazelles foraging and scanning the environment have learned to scan for predators because being eaten by a cheetah sucks.  A prey animal thus wouldn’t survive very long without some knowledge of potential threats in the environment.  Knowing this, if a gazelle stops eating, freezes, and looks across the field, the fact that all the gazelles are likely to stop foraging and check for danger does not prove the presence of theory of mind, because alternatively they could be responding due to empirical knowledge that it is in their interest to keep a look out for hungry kittens.

If you’re walking along the street and you see someone looking up, we are likely to look up as well.  The novelty of seeing someone looking up is a pretty strong stimulus to evoke our social facilitation (looking up as well), just like the gazelle and their knowledge that the environment contains dangers to be aware of, we understand that pianos or stock brokers falling on our head is also likely to put a dent in our afternoon.

Many researchers have demonstrated how dogs and wolves have varying abilities to search around visual barriers (e.g. Bräuer et al., 2004; Range et al., 2011; Virányi et al., 2009); however, ultimately here is what you have to decide for yourself:

  1. The dog is reading your mind and knows that you are looking at an object around the corner
  2. The dog notices that your eyes are looking somewhere to their right or left (an observable behavior) and is curious to investigate – oh there is a barrier?  Hmmm, let me walk around that

I think this research is interesting, but even so, this does not constitute evidence for theory of mind because it does not rule out competing hypotheses; such that a dog could be simply taking information from a visual environment—not attenuating to the cognitive states to understand the causal relationship between unobserved mental states and observed behavior.  Just my opinion, argument 2 seems much more practical and is further supported by our understanding that dogs are extremely sensitive to gazing since it is one of the most common signals they use in agonistic (conflict) behavior.

More egregiously though, Emery continues and states that dogs will abandon all morality and go for a piece of food the second you close your eyes, or turn your back, or place a barrier between you and the food, and this is a complete misinterpretation to the research done on this phenomena and thus absolute gibberish.  Leaving a food item alone is trainable.  Browse around YouTube and you will find plenty of videos where a dog is told to wait before his or her dinner bowl is set down, and then the owner walks out of the room, or even the house, before returning to release the dog to eat the food.  Honestly, a solid ‘leave it’ is one of the easiest behaviors to train, so this kind of research has to be interpreted very carefully regarding what it actually means, if anything, for the lives of our dogs.

#3 Dogs Assume That You Know Something They Don’t

As if I wasn’t already pounding my head against the desk, the author then uses the observation that dogs want to eat what we are eating as support for doggie mind reading abilities.  Unfortunately, this is not a trait unique to dogs (or humans for that matter).  Many social mammals select food preference by their group’s behavior.  For example, rats learn from group members how to determine what to eat and will learn to avoid the smell of poisoned food, a neophobic response—this is one of the reasons why rat poison doesn’t eliminate rat populations (Galef & Clark, 1971).  It is a fascinating behavior, but it does not require mind reading—rather rudimentary social facilitation.

#2 Dogs Understand Pointing

“…but the fact of the matter is that dogs and humans are the only two species currently clinging to our big blue spaceball who understand the point of pointing.”  (Emery, 2013)

Other than wolves (Udell et al., 2008), cats (Miklosi et al., 2005), parrots (Giret et al., 2009), bats (Hall et al., 2011), Jackdaws (Von Bayern & Emery, N., 2009), goats (Kaminski et al., (2005), dolphins (Pack & Herman, 2004), fur seals (Scheumann & Call, 2004), Ravens (Schloegel et al., 2007; for a review, see Udell et al., 2012)… hmm, only two species you say?  Monty Python jokes about the Spanish Inquisition aside, the ability for an animal to learn that they can walk around a tree is no different from the ability to learn that a finger might be directing towards food.  Animals who learn this distinction are socialized to people—period.  Nobody has snatched a dog that has never seen a human, tossed it in a room, pointed at a cup with food inside, and seen the dog dive in and say “thank you master!”  No, it would be shaking in the corner terrified for its life.  Animals who have been socialized to humans respond to pointing and other human communicative gestures (e.g. gazing and pointing with foot): pick your species.  Variance in this skill can be as easily explained by the failure for many animals to follow directions (just ask any school teacher how many times they have to remind students to write their name at the top of a test).

inquisition

#1 Dogs Know When You Like Someone Else More

Finally, Ms. Emery claims that oxytocin is a “love- and jealousy-related hormone” (Coren, 2011b).  This claim comes from a single study involving humans playing a computer game (Shamay-Tsoory et al., 2009), however the conclusions the authors make can be reinterpreted to fit the standard functional understanding of oxytocin (Tops, 2010).  Oxytocin is a mammalian hormone that triggers milk letdown in nursing females and is involved in a wide variety of social behaviors: such as increasing pleasure during orgasm, increasing time of social contact, facilitating memory of sexual partners, protects fetal neurons from injury during delivery, improves navigational strategies, and works with vasopressin receptors to aid pair-bonding (Breedlove et al., 2010).

If you don’t see references: assume the author is an idiot

It should be clear by now that cracked.com might be just about the worst source for dog behavior science, and if you have been following some of the citation trails, Psychology Today might appear as a questionable source as well.  There are more authors writing books and blogging about dogs than there are dogs in family homes and they range from people with high school diplomas to PhDs. Citations and a reference list is an excellent way to begin to decipher the quality of information, however it is not everything either.

While bad information frustrates the daylights out of me, ultimately, the burden falls on the consumer to be sure to examine the evidence. This is one of many reasons why a list of references is so important, and why it is best to assume the author is likely an idiot if they don’t bother to acknowledge the sources of their information in a clear, concise reference section at the end.  If there is no reference list, than be sure to ask yourself whether you believe you are reading an opinion piece or an opinion piece veiled as accurate science.

References:

Baenninger, R. (1997). On yawning and its functions. Psychonomic bulletin & review, 4(2), 198–207.

Bräuer, J., Call, J., & Tomasello, M. (2004). Visual perspective taking in dogs (Canis familiaris) in the presence of barriers. Applied Animal Behaviour Science, 88(3–4), 299–317. doi:10.1016/j.applanim.2004.03.004

Breedlove, S. M., Watson, N. V., & Rosenzweig, M. R. (2010). Biological Psychology: An Introduction to Behavioral, Cognitive, and Clinical Neuroscience, Sixth Edition (6th ed.). Sinauer Associates, Inc.

Borod, J. C., Haywood, C. S., & Koff, E. (1997). Neuropsychological aspects of facial asymmetry during emotional expression: A review of the normal adult literature. Neuropsychology Review, 7(1), 41–60.

Coren, S. (2011a). Can Your Dog Read Your Mind? Retrieved September 23, 2013, from http://www.psychologytoday.com/blog/canine-corner/201106/can-your-dog-read-your-mind

Coren, S. (2011b). Do Dogs Feel Jealousy and Envy? Retrieved September 23, 2013, from http://www.psychologytoday.com/blog/canine-corner/201111/do-dogs-feel-jealousy-and-envy

Davis, M. H. (1983). Measuring individual differences in empathy: Evidence for a multidimensional approach. Journal of Personality and Social Psychology, 44(1), 113–126. doi:10.1037/0022-3514.44.1.113

Emery, L. (2013). 5 Incredible Ways Dogs Can Read Your Mind.  Retrieved September 23, 2013, from http://www.cracked.com/article_20572_5-incredible-ways-dogs-can-read-your-mind.html

Galef, B. G., & Clark, M. M. (1971). Social factors in the poison avoidance and feeding behavior of wild and domesticated rat pups. Journal of Comparative and Physiological Psychology, 75(3), 341–357. doi:10.1037/h0030937

Gallese, V. (2003). The roots of empathy: the shared manifold hypothesis and the neural basis of intersubjectivity. Psychopathology, 36(4), 171–180. doi:72786

Giret, N., Miklósi, Á., Kreutzer, M., & Bovet, D. (2008). Use of experimenter-given cues by African gray parrots (Psittacus erithacus). Animal Cognition, 12(1), 1–10. doi:10.1007/s10071-008-0163-2

Guggisberg, A. G., Mathis, J., Schnider, A., & Hess, C. W. (2010). Why do we yawn? Neuroscience & Biobehavioral Reviews, 34(8), 1267–1276. doi:10.1016/j.neubiorev.2010.03.008

Hall, N. J., Udell, M. A. R., Dorey, N. R., Walsh, A. L., & Wynne, C. D. L. (2011). Megachiropteran bats (Pteropus) utilize human referential stimuli to locate hidden food. Journal of comparative psychology (Washington, D.C.: 1983), 125(3), 341–346. doi:10.1037/a0023680

Harr, A. L., Gilbert, V. R., & Phillips, K. A. (2009). Do dogs (Canis familiaris) show contagious yawning? Animal Cognition, 12(6), 833–837. doi:10.1007/s10071-009-0233-0

Horowitz, A. (2011). Theory of mind in dogs? Examining method and concept. Learning & Behavior, 39(4), 314–317. doi:10.3758/s13420-011-0041-7

Kaminski, J., Riedel, J., Call, J., & Tomasello, M. (2005). Domestic goats, Capra hircus, follow gaze direction and use social cues in an object choice task. Animal Behaviour, 69(1), 11–18. doi:10.1016/j.anbehav.2004.05.008

Miklósi, Á., Pongrácz, P., Lakatos, G., Topál, J., & Csányi, V. (2005). A Comparative Study of the Use of Visual Communicative Signals in Interactions Between Dogs (Canis familiaris) and Humans and Cats (Felis catus) and Humans. Journal of Comparative Psychology, 119(2), 179–186. doi:10.1037/0735-7036.119.2.179

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