Getting around is complicated business. Every year, animals traverse miles of sky and sea (and land), chasing warmth or food or mates as the planet rotates and the seasons change. And with such precision! Some animals rely on visual landmarks, others on subtle changes in magnetic fields, and yet others match their internal clocks with the movement of the sun and stars across the sky.
One researcher, Jennifer A. Mather, wondered: how do octopuses navigate? Do they rely on chemotactile sensory information, or do they orient towards visual landmarks? Octopuses occupy "homes" for several days or in some instances for several weeks, and when they go out looking for food, they are sometimes gone for several hours at a time. Therefore, they must use some sort of memory to find their way back home.
Many molluscs use trail-following, and follow their own mucus trails, or the trails of others. You might expect that octopuses use trail-following as well, since they forage by using chemotactile exploration - at least four different types of receptors on their suckers gather chemical and tactile information as they move along the rocky seafloor.
However, many other species use visual scene recognition to aid in navigation: ants, bees, gerbils, hamsters, pigeons, and even humans, use visual landmarks to navigate around their environments. Since octopuses use visual information to distinguish among different objects, they could use visual landmarks to get home as well.
First, Mather and various Earthwatch volunteers observed the foraging movements of four wild octopuses, for a total of 113 complete round-trips. Since only trips which would have required the use of memory were of interest, trips of less than ten minutes, or less than two meters from the starting point were excluded, leaving sixty trips (53%) to be analyzed. The average distance was 9.3 meters, and the average duration was 55 minutes - so memory would surely be required to get home.
In general, the homebound trips were not retracings of the outbound trips, suggesting that the octopuses are not simply following their own trails. Also, the trips were generally in different directions, so they couldn't have simply used chemotactile information gathered on previous trips. Further, it was noted that for longer trips, the octopuses used jet propulsion to move through the water, instead of crawling along with their arms. Since they did not have continuous contact with the ground, it is unlikely that they relied on chemotactile information alone, if at all.
Interestingly, there was a significant correlation between the distance from home at time of capture and the choice of whether or not the captured prey would be eaten immediately, or brought home for consumption. This suggests that the octopuses may represent their distance from home, or the time elapsed since they left home.
Then, the researchers and volunteers placed artificial landmarks in front of (but not blocking) the entrance to the octopuses' homes. These landmarks were 6 cm square and 20 cm tall, and painted in alternating patterns of black and white stripes. The landmarks were left untouched for three days, and on the third day, when an octopus was seen leaving home, a volunteer moved the landmark one meter away from its previous location.
Would the movement of this visual landmark affect the ability of the octopuses to find their way home? Not really. This doesn't mean, however, that they don't use visual landmarks - it is indeed possible that they were relying on bigger more obvious natural landmarks (big rocks, cliffs, etc) instead of the smaller foreign landmark. In order to address these outstanding questions, Mather conducted a set of controlled laboratory studies (aided by an undergraduate Zen Faulkes!)
Four juvenile east pacific red octopuses (octopus rubescens) were housed in one aquarium, but were separated into their own sections.
Each octopus had, in its section of the tank, a black plexiglass cube with one end open that was used as its "home." For testing, the animal was moved (while inside the "home" cube) into a different tank. The testing tank was circular, and was positioned in the room so that no visual landmarks were available to the octopus from outside the tank. Two pieces of plastic tubing were used as visual landmarks, and were placed directly opposite the opening of the black cube. It took two months for two of the octopuses to become habituated to the testing tank. Two of the octopuses never habituated, and were not tested.
The two pieces of plastic tubing were hollow, 3.3 cm in diameter, and 10 cm tall. The question was whether or not the octopuses could use the tubes as visual landmarks to find food.
First, crabs were simply released into the tank so that the octopuses would become used to hunting and eating the crabs. Once they readily captured the crabs, the crabs were confined to a glass bowl near the plastic tubes. Finally, the crabs would be dropped into the hollow tubes to be retrieved by the octopus, but only after the octopus had grasped the tube - this ensured that the octopus wasn't relying on chemical cues. After this training paradigm which lasted more than two weeks, testing began.
During testing, the two landmarks were systematically moved around the tank with respect to the opening of the home cube. Would the octopuses orient to the visual location of the landmark instead of towards any particular direction, or towards the previous location of the landmark? What about if additional landmarks were added, and the entire visual scene was moved? What if landmarks were switched within the visual scene?
What happens when there is only one visual landmark, and it is moved 90 degrees each day relative to the home cube?
The first octopus was accurate on 6/8 responses, and the second one was accurate on 7/9 responses. Overall, both animals learned to go to the visual landmark for the food reward, regardless of its location.
Next, Mather wondered what would happen if the visual scene included more than one visual landmark? Could the octopuses navigate effectively in an environment with three landmarks?
This task was only given to one of the two octopuses. The octopus began by orienting towards the larger more obvious black box and then moved from the box to the tube, but by day 3, it had learned to go straight for the plastic tube.
Once the octopus had learned to navigate around the three landmarks, they were rearranged.
The first time the tube was moved, the octopus moved to the box, and then reoriented to the tube. The second time, when the tube was back in the starting location, the octopus initially started moving towards its previous location, but then corrected itself and found the tube. The third day, the octopus explored the box and dish, returned home, and then went directly to the tube. Finally on day four, the first response was to search in the tube's previous location.
Then, the tube was removed entirely. First, the octopus went to the box, then the dish, then to the tube's previous location, then back to the box, then it circled the entire tank. On the second day of this condition, the octopus first went to the tube's most recent location, then to the box, back home, and back to the box. The third day was similar.
Taken together, this evidence suggests that octopuses do use visual spatial information. Field studies indicated that the octopuses are not in constant contact with the sea floor, did not retrace their outbound paths to get home, and set out on different paths each day. Given this evidence, it is unlikely that they relied on chemical or tactile information to guide their navigation.
The laboratory tests indicated that they can learn to orient towards visual landmarks, and that they continue to do so even with the landmarks are moved. They could also encode a larger scene consisting of multiple landmarks, and seemed to preferentially orient to larger more obvious objects. The artificial landmark displacement experiment in the field also suggests that octopuses rely on larger, stationary objects (e.g. big rocks) even if smaller objects are more conspicuous.
The systematic errors made by the octopuses in the lab, as well as the distribution of foraging paths in the field, suggest that octopuses maintain working memory for where they have been, and where food has been previously found. Further, in the field, the octopuses' decision to eat their prey immediately or to take it home to eat was partly based on the distance between its current location and home. Importantly, there was no significant contribution of the size of the captured prey to this decision. This suggests that octopuses maintain an internal mental map of their home range (~15 meters diameter), as well as their location within that map relative to home. Not bad for a critter whose brains are located inside its arms.
Mather, J. (1991). Navigation by spatial memory and use of visual landmarks in octopuses Journal of Comparative Physiology A, 168 (4), 491-497. DOI: 10.1007/BF00199609
For more on spatial navigation:
Image: East Pacific Red Octopus via Flickr/Ken-ichi.