Werewolves, ghosts, and vampires—with the days getting shorter and colder, and Halloween fast approaching, our imaginations turn to the ghouls that supposedly come out around this time of year. Vampires, one of history’s most popular
It’s been said that the eyes are the windows to the soul. They allow us to communicate feelings across a room, direct the attention of others, and express emotion better than words ever could. The importance of eye contact in non-human species is well known—we’ve all heard that you shouldn’t stare a bear or angry dog in the eyes—but we don’t know a whole lot about how gaze is used between individuals of the same species. Japanese researchers took on this topic in a recent PLOS ONE article, focusing specifically on how eye contact and communication is affected by eye visibility and facial patterning around the eyes of canids.
Their research observed 25 canid species, comparing variations in facial pattern and coloring to observations about their social behavior and evolutionary history. They found that canines may use facial markers to either highlight or de-emphasize their eyes. Species with more distinguishable eyes tended to live and hunt in groups, where gaze-communication facilitates the teamwork that is necessary to bring down large prey and stay safe. Those with camouflaged eyes were more likely to live alone or in pairs, where communication with other members of their species may not be needed in the same way.
Using photos of each species, the authors analyzed the contrast between five areas of the canine face: pupil, iris, eyelid margin, coat around the eyes, and facial area including the eyes, as shown in the figure above. They measured contrast assuming red-green colorblindness of the observer (fun fact: canids cannot see the full spectrum of color). Species were then grouped according to the visibility of their eyes, described in the figure below:
- Group A contained species with easily visible pupils and eye placement
- Group B contained species with camouflaged pupils but clearly defined eye placement
- Group C contained species with fully camouflaged eyes and pupils
The authors found the strongest correlation between eye visibility and living and hunting behavior. More species in Group A, like gray wolves, live and hunt in packs, whereas more species in Groups B and C, like the fennec fox and bush dog, live and hunt alone or in pairs. Species in Group A also spend significantly more time in “gazing postures,” with their sight and body directed at another animal, an action that accentuates their focused attention to other members of the group. The genetic similarity between species was not as useful in explaining these differences, with A-type faces found in 8 of 10 wolf-like species, and in 3 of 10 red fox-like species. The authors suggest that A-type markings developed independently once these groups had evolutionarily split.
Lighter iris coloring is thought to be an adaptation to ultraviolet light in many species, similar to variations in human skin pigmentation. To determine whether this adaptation could explain the variation seen in canid iris color, the researchers compared the eye coloring of three wolf subspecies from Group A originating from arctic, temperate, and subtropical regions, to see if any differences in their lighter coloring could be attributed to geographical origin. They found that iris color did not vary significantly between the subspecies, suggesting that it may have developed to facilitate communication and not as an adaptation to specific geographical locations.
When the authors reviewed social behaviors, they found a number of social species with B- and C-type faces, the groups normally found alone or in pairs. These species are known to use acoustic or other visual signals, like a howl or the flash of a white tail, to communicate with their comrades. This allows them to skirt one possible disadvantage of gaze-communication: when prey can also identify and follow a gaze, and realize they’ve been targeted.
Gaze communication may be an important tool for other canids, including our own companions, domestic dogs. Previous studies have shown that domestic dogs are more likely to make direct eye contact with humans than wolves raised in the same setting. This could mean that after thousands of years of cohabitation, dogs see us in socially useful ways that wolves never will. Luckily for us, that means we get to see this.
Citation: Ueda S, Kumagai G, Otaki Y, Yamaguchi S, Kohshima S (2014) A Comparison of Facial Color Pattern and Gazing Behavior in Canid Species Suggests Gaze Communication in Gray Wolves (Canis lupus). PLoS ONE 9(6): e98217. doi:10.1371/journal.pone.0098217
Images 2 and 3: Figures 1 and 2 from the article
In the spirit of Thanksgiving and sharing a warm meal with loved ones, we’d like to take a moment to give some social credit to our loving, faithful, and clever furry friends. Researchers have been investigating the question of whether animals can eavesdrop—or listen in on third-party interactions—for some time, and evidence of potential eavesdropping has been identified in dogs and other mammals, fish, and birds.
Dogs are especially good candidates for studying eavesdropping because they are social animals and have been domesticated, so they are accustomed to interacting with humans day-in and day-out. Most dog owners know how well their dogs can “read” them, and some might argue that their dogs can do this better than other people they know. Researchers have also confirmed that dogs can recognize human emotions, facial expressions, and friendliness versus hostility, the latter even in strangers.
In a more nuanced form of social interaction, dogs have been shown to prefer certain people over others depending on the outcome of third-party interactions. To further investigate how dogs respond to interactions among people, the authors of this recently published PLOS ONE article asked whether dogs can develop a preference for or against givers, or “donors,” in a “begging” interaction between people.
The study recruited 72 dogs of various breeds and sizes and put them in a testing environment that either resembled a home or a dog care facility. While the dog watched from across the room, two human assistants acted as “donors” (females, pictured above) who offered food to a “beggar” (male, above), and the beggar either reacted positively or negatively to the offered food. The extent of the reaction was controlled to try to determine which social cues the dog was picking up on: gesture + verbal (GV), gesture only (G), or verbal (V) only.
In the GV group positive scenario, the beggar received a yummy corn flake, ate it, and said “So tasty!”; in the negative scenario, the beggar said “So ugly!” gave the corn flake back, and then turned his back. The G and V groups differed in that they isolated the gesture and verbal components, respectively. After the beggar left, the dog was released and had 10 seconds to decide between the donors, who did not signal the dog in any way. Dogs that did not make a choice were removed from the analysis.
As the results below show, dogs were more likely to choose the donor who received a positive reaction; the authors also noted that the dogs tended to watch or gaze at the donor who received a positive reaction longer than the donor who received a negative reaction. However, the authors state that both gesture and verbal cues (the GV group) were required to show a reliable difference among the groups.
Although these results alone are not conclusive, as it is difficult to control for all the variables affecting these scenarios (e.g., the authors note that dogs chose randomly if the donors switched places), the authors suggest that the dogs may have attributed a “reputation” to the donor based on the beggar’s reaction, where both gesture and verbal cues were required for the dog to make this association.
While not the same as a scientific experiment, it might be fun to “test” your dog in various eavesdropping scenarios, especially in relation to available food* on the Thanksgiving table.
Happy Thanksgiving from PLOS ONE!
Citation: Freidin E, Putrino N, D’Orazio M, Bentosela M (2013) Dogs’ Eavesdropping from People’s Reactions in Third Party Interactions. PLoS ONE 8(11): e79198. doi:10.1371/journal.pone.0079198
*food safe for pets to eat, of course!
In an age of 3D printing and bionic limbs, distinctions between the manmade and the natural can sometimes blur. Take, for example, the case of the robotic fish depicted above (part A). This little guy is modeled after Notemigonus crysoleucas (image, part B), also known as the golden shiner, and in a recent PLOS ONE study, researchers put it to the test: can a robotic fish influence the behavior of a real fish, and if so, what characteristics enable the robotic fish to do so? According to the researchers at Polytechnic Institute of New York University, answers may depend on the robot fish’s color and the frequency with which it waggles its tail.
To find out more, the authors commissioned the making of two robot fish for this study: one gray and one red. While both physically modeled the golden shiner in many respects, only the gray robot fish was painted to mimic its real-life counterpart. Other than color, the two robots were identical: both consisted of three rigid parts, connected on hinges, and sported silicone tail fins.
As illustrated above, one robot fish was placed in a water tunnel with a real fish during each trial. The real fish was free to swim in the tunnel while the robot fish “swam,” or waggled its tail fin, in the center of the apparatus. The robotic fish’s tail waggled at various frequencies, ranging from 0 Hz to 4 Hz, as webcams tracked the real fish’s movements. The middle of the tunnel was designated the “focal region” to indicate where fish and robot interaction was likely to occur. The researchers further divided the region behind the fish into four parts, explaining that the robot fish’s tail wagging was likely to affect the water flow, and thus the real fish’s behavior, in this area.
After reviewing the webcam footage, they found that neither factor (color, tail wagging frequency) working alone had a significant impact on the real fish’s swimming behavior. However, when the gray robot wagged its tail at 3 Hz, the real fish spent a significantly longer time swimming in the center of the tunnel, preferring to spend most of its time swimming right behind the robot. When this happened, the wake created by the robot’s tail wagging could allow the real fish to reduce its energy expenditure while swimming.
What’s so special about wagging your tail fin at 3 Hz, you ask? The researchers ascertained through preliminary research that when golden shiners swim, their tails waggle at 3.32 Hz. In addition, the gray robot’s coloring may have been more attractive to the golden shiner than the red robot’s, as it may have elicited a likeness-related social response in the real shiner. This suggestion is in line with other robot work in comparable fish species.
In other words, the robot fish exerted the most influence—or was the most convincing to the real fish—when its coloring and movements closely corresponded to the coloring and movements of a real fish. Go figure!
Citation: Polverino G, Phamduy P, Porfiri M (2013) Fish and Robots Swimming Together in a Water Tunnel: Robot Color and Tail-Beat Frequency Influence Fish Behavior. PLoS ONE 8(10): e77589. doi:10.1371/journal.pone.0077589
Image 1: Figure 1 from the paper
Image 2: Figure 2 from the paper
Image 3: Figure 4 from the paper
Few ideas excite the imagination more than virtual reality. We humans use virtual reality for training, entertaining, and even education, but we can also use it to study human and animal behavior. Adaptive behavior, or the ability to adjust to new situations, is influenced by what we see, hear, and experience in our environment; unfortunately, for this reason, it is difficult to isolate the possible stimuli that affect it. The authors of this recently published PLOS ONE paper developed a virtual reality environment to try to isolate and measure the impact of visual and sound cues on rats navigating through a virtual space.
The virtual reality navigation test is based on an experiment called the Morris Water Maze, a standard lab test where a rat swims through water using visual cues on the walls to navigate. The virtual version uses a 14 square-foot room with visual cues projected on each wall and sounds from 4 sides (pictured above). The rat is at the center of the room, wearing a harness (pictured on the right) on a spherical treadmill placed on a three-foot circular table.
Before beginning the navigation tasks, researchers trained nine male rats to move in virtual reality. The rat started from one of 4 random start locations, facing the wall (see video below). The northeast quadrant of the space was designated as the ‘reward zone,’ indicated by a white dot. Upon entry to this zone, the rat was rewarded with sugar water (if only all video games worked this way).
After training, the researchers tested each rat’s ability to navigate to the reward zone using one of three cues: audiovisual, visual, or auditory. Once the rat found the reward zone, a 2-second blackout period was initiated, and then the rat was ‘moved’ back to one of the 4 random start locations. The video below shows the visual cue test.
Scientists found that rats can learn to navigate to an unmarked location based on visual cues—with a moderate amount of training. However, the rats were unable to use the auditory cues to navigate to the reward zone, and instead moved in circles to try to locate it.
Although the rat’s harness may look a little funny, it is a relatively noninvasive test, and since the animal is not in water, like in the Morris Water Maze test, it is easier to combine this test with tools to measure neural and physical variables in the task. Additionally, the virtual maze may contribute to new methodology evaluating the underlying factors in adaptive behavior, specifically because no other cues besides the audiovisual, visual, and auditory defined the spatial location of reward, something that is difficult to achieve in the real world. Despite humans not yet understanding what virtual reality means to us, we can already use it to better understand animal learning and behavior.
Citation: Cushman JD, Aharoni DB, Willers B, Ravassard P, Kees A, et al. (2013) Multisensory Control of Multimodal Behavior: Do the Legs Know What the Tongue Is Doing? PLoS ONE 8(11): e80465. doi:10.1371/journal.pone.0080465
Image 1: doi:10.1371/journal.pone.0080465
Image 2: doi:10.1371/journal.pone.0080465
Video 1: doi:10.1371/journal.pone.0080465
Video 2: doi:10.1371/journal.pone.0080465
Who doesn’t love a good cuddle? A study published today in PLOS ONE demonstrates that lions are no different than us when it comes to snuggling, though they’re not only in it for the warm fuzzies. Researchers studying captive lions at the Tama Zoological Park, Tokyo, found that affectionate behavior between individual lions helps foster bonds and strengthens the pride as a whole.
Physical exchanges were common throughout the observed group of lions, though the males and females seemed to prefer different methods for showing their affection. While about 97% of observed licking occurred between lionesses, male lions in the zoo seemed to prefer the head rub, and directed a serious portion of their head-rubbing efforts towards other males. Females also used the head rub, but mainly in interactions with males in the group and less frequently with other females. Almost all behaviors were reciprocated, especially between males and females.
Researchers investigated why these behaviors differed from the affiliative behaviors seen in other animals, as well as the reasons for the apparent discrepancy between male and female behaviors. They postulate that shared group odors may explain why lions specifically choose to rub heads instead of any other behavior —the spotted hyena, for instance, exposes its genitals upon greeting members of the group. The lionesses licking each other could be an extension of their maternal behavior and instincts normally shown towards their cubs. More research, particularly on the behavior of lions in the wild, is needed before we can say for sure.
While we don’t have any final answers on affectionate behavior between captive lions, this research reveals how these behaviors affect this pride’s group dynamics. In the wild, coalitions of male lions compete for the right to live among, and mate with, the lionesses of an established pride. Once a group of males has settled itself in a pride, they must be on the offensive at all times to ward off attacks from gangs of nomadic male lions. Understandably, greater numbers means greater power and a better chance of standing strong against outside invaders. So, how does a group of unruly male lions keep its numbers high? Head-rubbing seems to be at least part of the equation.
Citation: Matoba T, Kutsukake N, Hasegawa T (2013) Head Rubbing and Licking Reinforce Social Bonds in a Group of Captive African Lions, Panthera leo. PLoS ONE 8(9): e73044. doi:10.1371/journal.pone.0073044
Image: Image from Figure 1 of the manuscript
Whether it is unusual food habits, fighting over females, or snacking between meals, research published in PLOS ONE this week spans these and more diverse animal behaviors. These studies don’t aim to use animal research to interpret human behavior, but their results might nonetheless evoke navel-gazing for us humans.
For example, one study published today uses GPS trackers to reveal an internal ‘GPS’ in giant robber crabs, the world’s largest land-living arthropod. Researchers tracking the enormous coconut-eating crabs, whose bodies can grow bigger than a man’s head, with legs up to a meter in length, have identified previously unknown navigation and homing skills in this species.
Like GPS units, peculiar food choices are also not unique to humans. An ancient bear’s preference for munching on hard plant materials like bamboo has revealed that it might be the oldest known ancestor of the giant panda. The bear’s fossil tooth and jaw were discovered in Spain and are described in another study.
People and other animals go to great lengths to develop elaborate courtship rituals or even physical features, but few will fight to the death over a female. Researchers have found that one species of Australian grasshopper is an exception. Males of the species will resort to grappling, kicking and biting in aggressive fights, and the behaviors exhibited depend on whether the male is challenging another or defending himself (Watch a video here).
Research on bonobo apes tackles a behavior that is likely more familiar to most of us: contagious yawning. The authors find that just like humans, bonobos are more likely to yawn in response to one another’s yawns when they are more closely related than when they are unrelated to the first yawner, and when the first individual to yawn is a senior member of the group. Among other findings, their results support the idea that senior group members play a key role in affecting the emotional states of others.
Defining emotions in non-human species is always challenging, but researchers are beginning to understand what signs of boredom might look like in at least one species, mink. A study published today shows that mink without enough interesting things to do tend to snack on food treats more often between meals, and lie awake for longer periods of time without falling asleep. Providing animals with sufficient stimulation is considered critical to their well-being, but defining what might be considered adequate is still a challenge. As the authors of this study say, “Many people believe that farm and zoo animals in empty enclosures get bored, but since the animals can’t tell us how they feel, we can only judge this from seeing how motivated they are for stimulation.”
If all these behaviors have you thinking, “They’re just like us!” think again. Understanding the animal behaviors described in these studies is only a first step towards sharing human spaces with them, whether in zoos, on farms or on an island off the Indonesian coast.
Krieger J, Grandy R, Drew MM, Erland S, Stensmyr MC, et al. (2012) Giant Robber Crabs Monitored from Space: GPS-Based Telemetric Studies on
Christmas Island (Indian Ocean). PLoS ONE 7(11): e49809. doi:10.1371/journal.pone.0049809
Abella J, Alba DM, Robles JM, Valenciano A, Rotgers C, et al. (2012) Kretzoiarctos gen. nov., the Oldest Member of the Giant Panda Clade. PLoS ONE 7(11): e48985. doi:10.1371/journal.pone.0048985
Umbers KDL, Tatarnic NJ, Holwell GI, Herberstein ME (2012) Ferocious Fighting between Male Grasshoppers. PLoS ONE 7(11): e49600. doi:10.1371/
Demuru E, Palagi E (2012) In Bonobos Yawn Contagion Is Higher among Kin and Friends. PLoS ONE 7(11): e49613. doi:10.1371/journal.pone.0049613
Meagher RK, Mason GJ (2012) Environmental Enrichment Reduces Signs of Boredom in Caged Mink. PLoS ONE 7(11): e49180. doi:10.1371/journal.pone.0049180
top: Giant robber crabs on Christmas Island, Bill S. Hannson, Jakob Krieger, Steffen Harzsch
below: Empathetic yawning in bonobos, Elisa Demuru