Parallel vector memories in the brain of a bee as foundation for flexible navigation.

Insects rely on path integration (vector-based navigation) and landmark guidance to perform sophisticated navigational feats, rivaling those seen in mammals. Bees in particular exhibit complex navigation behaviors including creating optimal routes and novel shortcuts between locations, an ability historically indicative of the presence of a cognitive map. A mammalian cognitive map has been widely accepted. However, in insects, the existence of a centralized cognitive map is highly contentious. Using a controlled laboratory assay that condenses foraging behaviors to short distances in walking bumblebees, we reveal that vectors learned during path integration can be transferred to long-term memory, that multiple such vectors can be stored in parallel, and that these vectors can be recalled at a familiar location and used for homeward navigation. These findings demonstrate that bees meet the two fundamental requirements of a vector-based analog of a decentralized cognitive map: Home vectors need to be stored in long-term memory and need to be recalled from remembered locations. Thus, our data demonstrate that bees possess the foundational elements for a vector-based map. By utilizing this relatively simple strategy for spatial organization, insects may achieve high-level navigation behaviors seen in vertebrates with the limited number of neurons in their brains, circumventing the computational requirements associated with the cognitive maps of mammals.

Vector navigation in walking bumblebees.

Path integration is a computational strategy that allows an animal to maintain an internal estimate of its position relative to a point of origin. Many species use path integration to navigate back to specific locations, typically their homes, after lengthy and convoluted excursions. Hymenopteran insects are impressive path integrators, directly returning to their hives after hundreds of meters of outward travel. Recent neurobiological insights have established hypotheses for how path integration vectors could be encoded in the brains of bees, but clear ways to test these hypotheses in the laboratory are currently unavailable. Here, we report that the bumblebee, Bombus terrestris, uses path integration while walking over short distances in an indoor arena. They estimate accurate vector distances after displacement and orient by artificial celestial cues. Walking bumblebees also exhibited systematic search patterns when home vectors failed to lead them accurately back to the nest, closely resembling searches performed by other species under natural conditions. We thus provide a robust experimental system to test navigation behavior in the laboratory that reflects most aspects of natural path integration. Importantly, we established this assay in an animal that is both readily available and resilient to invasive manipulations, as we demonstrate with the retention of the homing behavior post-anesthesia and surgery. In the future, our behavioral assay can therefore be combined with current electrophysiological techniques, opening a path toward directly probing the neural basis of the sophisticated vector navigation abilities of bees.

Mantis shrimp identify an object by its shape rather than its color during visual recognition.

Mantis shrimp commonly inhabit seafloor environments with an abundance of visual features including conspecifics, predators, prey and landmarks used for navigation. Although these animals are capable of discriminating color and polarization, it is unknown what specific attributes of a visual object are important during recognition. Here, we show that mantis shrimp of the species Neogonodactylus oerstedii are able to learn the shape of a trained target. Further, when the shape and color of a target that they had been trained to identify were placed in conflict, N. oerstedii tended to choose the target of the trained shape over the target of the trained color. Thus, we conclude that the shape of the target was more salient than its color during recognition by N. oerstedii, suggesting that the shapes of objects, such as landmarks or other animals, are important for their identification by the species.

Landmark navigation in a mantis shrimp.

Mantis shrimp commonly occupy burrows in shallow, tropical waters. These habitats are often structurally complex where many potential landmarks are available. Mantis shrimp of the species Neogonodactylus oerstedii return to their burrows between foraging excursions using path integration, a vector-based navigational strategy that is prone to accumulated error. Here, we show that N. oerstedii can navigate using landmarks in parallel with their path integration system, correcting for positional uncertainty generated when navigating using solely path integration. We also report that when the path integration and landmark navigation systems are placed in conflict, N. oerstedii will orientate using either system or even switch systems enroute. How they make the decision to trust one navigational system over another is unclear. These findings add to our understanding of the refined navigational toolkit N. oerstedii relies upon to efficiently navigate back to its burrow, complementing its robust, yet error prone, path integration system with landmark guidance.

Path integration error and adaptable search behaviors in a mantis shrimp.

Mantis shrimp of the species Neogonodactylus oerstedii occupy small burrows in shallow waters throughout the Caribbean. These animals use path integration, a vector-based navigation strategy, to return to their homes while foraging. Here, we report that path integration in N. oerstedii is prone to error accumulated during outward foraging paths and we describe the search behavior that N. oerstedii employs after it fails to locate its home following the route provided by its path integrator. This search behavior forms continuously expanding, non-oriented loops that are centered near the point of search initiation. The radius of this search is scaled to the animal's positional uncertainty during path integration, improving the effectiveness of the search. The search behaviors exhibited by N. oerstedii bear a striking resemblance to search behaviors in other animals, offering potential avenues for the comparative examination of search behaviors and how they are optimized in disparate taxa.

Mantis Shrimp Navigate Home Using Celestial and Idiothetic Path Integration.

Path integration is a robust mechanism that many animals employ to return to specific locations, typically their homes, during navigation. This efficient navigational strategy has never been demonstrated in a fully aquatic animal, where sensory cues used for orientation may differ dramatically from those available above the water's surface. Here, we report that the mantis shrimp, Neogonodactylus oerstedii, uses path integration informed by a hierarchical reliance on the sun, overhead polarization patterns, and idiothetic (internal) orientation cues to return home when foraging, making them the first fully aquatic path-integrating animals yet discovered. We show that mantis shrimp rely on navigational strategies closely resembling those used by insect navigators, opening a new avenue for the investigation of the neural basis of navigation behaviors and the evolution of these strategies in arthropods and potentially other animals as well. VIDEO ABSTRACT.