When testing the discrimination abilities of an animal, the researcher usually depends upon the animal subjects to make a certain response to indicate their choice. Monkeys can push buttons or move joysticks, pigeons can peck at different keys, rats can press levers. Compared to these common laboratory animals, the behavioral repertoires of most fish might seem limited. But there is one fish that has a unique and reliable method for indicating its response in behavioral tests: the archerfish.

The archerfish is a champion spitter. In the wild, they spit well-aimed jets of water to knock insects off vegetation above the water.

Scientists at the University of Queensland in Australia took advantage of this propensity to spit to test how archerfish make decisions. Cait Newport, with colleagues Guy Wallis, Shelby Temple, and Ulrike Siebeck, trained archerfish to spit a jet of water at particular images presented on a computer monitor suspended above their tanks. "Archerfish are great research subjects as they are inquisitive and generally motivated to complete tasks in exchange for food," says Newport. "Plus, they are fast learners and so keen to spit at things, including the researcher."

Go Fish

The researchers decided to test their archerfish using what's known as a forced-choice task. These type of tasks are commonly used to probe the discrimination abilities of different animals. In this test, the animal is usually presented with two choices: a "target" which is rewarded and a "distractor" which is not. It's generally assumed that when an animal learns a two-choice forced-choice task, it is selecting the rewarded target. But it is equally possible that the animal is instead learning to avoid the unrewarded distractor.

With only two choices, the animal's performance is the same whether it is choosing the reward or avoiding the non-reward. In order to see how archerfish make decisions, Newport and her colleagues gave the fish a four-alternative forced-choice task.

They trained archerfish to spit at one target image that was presented simultaneously with three different distractor images. After the fish showed that they could easily master this task, Newport and her colleagues repeated the experiment with either the rewarded target or the distractors replaced with completely novel images that the fish had never encountered before. If the fish were making their decision by choosing the rewarded target image, then changing the distractor images to something new shouldn't affect their performance. Alternatively, if they were making their decision instead by avoiding the distractor images, then substituting a new image for the rewarded target shouldn't have an effect on their performance.

Video: Shelby E. Temple and Peter Kraft

Newport and her colleagues discovered that the archerfish's performance was disrupted when the distractors were changed, but not when the target was changed. When the target was substituted with a novel image, the fish continued to avoid the distractor images. However, when the distractor images were replaced with novel images, the fish chose the target image at about chance levels. It seems they were solving the task by avoiding the unrewarded stimuli, rather than choosing the rewarded image.

Next, Newport and her colleagues challenged the fish further by giving them the choice between the target image, one novel image, and two distractor images. This time, three of the fish selected the target more often than the novel image, but one fish chose the target and the novel image at about equal rates. The fish that selected the novel image and the target image equally seemed to be using the strategy "avoid unrewarded images." The other three fish might have used a different decision-making strategy, as they continued to select the target more frequently.

To explain their subjects' behavior, the researchers modeled different possible decision rules and found the behavior of the archerfish generally matched more complicated decision rules. The models also predicted that the order in which the fish viewed the four images plays a role in their decision-making. Not all fish used the same decision rules, and their strategies appeared to be flexible and dependent on the type and combination of images presented.

Ready, Aim, Shoot

Photo: Cait Newport

Newport and her colleagues believe the archerfish's tendency to avoid unrewarded images can be explained by their feeding ecology. Learning to avoid unrewarded stimuli — in the wild, these might be distasteful prey items or bugs that are difficult to dislodge and knock into the water — is likely very important for the survival of the fish, as going after these prey items wastes valuable time and energy. At the same time, the number of different potential rewarding prey items is huge — they may encounter hundreds or even thousands of different species of small, edible invertebrates in the foliage above the water, and the abundance of these different species changes over the seasons. The ability to recognize new potential prey items may be more important than learning to recognize a previously rewarded prey item that the fish may never encounter again. Archerfish might benefit from taking risks and sampling novel prey items when they see them.

So the archerfish's tendency to select novel images in the experiments might reflect a strategy that allows them to explore unknown potential food sources in the wild. "While the reward for selecting the [target stimulus] is known, from the fish's perspective the novel stimulus may provide an even greater reward," Newport and her colleagues write. The novel image may have seemed worth trying to the fish.

The differences in the individual archerfish's decision-making strategies may be driven by differences in the fish's personalities or previous experiences that impact their willingness to take risks. Newport says that like humans, different individual fish can respond to the same situation in different ways.

"I think fish are smarter than most people realize," Newport says. "Although we sometimes say they have 'simpler' brains, in reality their brains may just be organized differently and our findings show that they are still capable of performing remarkable tasks and showing complex learning."

Reference:

Newport, C., Wallis, G., Temple, S. E., and Siebeck, U. E. (2013). Complex, context-dependent decision strategies of archerfish, Toxotes chatareus. Animal Behaviour. doi: 10.1016/j.anbehav.2013.09.031.