Maze Navigation and Route Memorization by Worker Bumblebees (Bombus impatiens (Cresson) (Hymenoptera: Apidae)

Abstract

Bumblebees move about their environments by flying and by walking. Most experimental studies have addressed navigation during foraging flights, but we presented our experimental bees with the challenge of learning to navigate while walking as they must do in nature within topographically complex spaces containing their nests. We trained bumblebee workers to navigate complex, nine-channel, mazes in the absence of specific visual, chemical or textural cues. They successfully navigated through complex multi-turn mazes (stereotypical "rat mazes") with several dead-ends by memorizing the entire sequence of appropriate turns, and their choice of correct first turn on entering the maze. Thus, their observed proficiencies indicated that the individual bumblebees had each memorized the maze by learning motor sequences which were not linked to visual, chemical or textural stimuli, and that their memories were triggered by contextual cues associated with the bees' positions in a sequence. Our findings have implications on natural ambulatory activities inside and outside the colony, and even in practical use as vectors of biological control agents.

The internal maps of insects

“…There is some evidence for sequence memory in insects. Bees have been shown able to execute a sequence of motor memories to navigate a maze [honeybees (Zhang et al, 2000); bumblebees (Mirwan and Kevan, 2015)], and may even persist in this sequence of manoeuvres when barriers are removed (Collett et al, 1993). Landmark countingwhere bees trained on a course with several similar landmarks on the way to the goal subsequently search after passing the usual number of landmarks, which have been moved either closer together or further apart (Chittka and Geiger, 1995;Dacke and Srinivasan, 2008a; but see also Menzel et al, 2010)might also be considered a form of sequence memory.…”

Maze learning and memory in a decapod crustacean

“…Learning the location of, and routes to, resources should, therefore, be an adaptive trait that we can investigate using mazes. Mazes provide a quantifiable measure of an animal's performance, and while investigations into spatial learning in insects have used some quite complex maze configurations [7,15,16], crustacean studies have used much simpler arrangements (cross-, Y-or Tshaped mazes [17][18][19][20]), and the ability of crustaceans to solve more complex mazes has not been explored since some very limited studies in the early twentieth century [21,22]. We, therefore, used a more complex, multiple-turn maze, resembling those used in classic mouse studies (reviewed in [3]), to investigate spatial learning in the European shore crab, Carcinus maenas; an important generalist predator and scavenger in intertidal and shallow sea ecosystems.…”

Visual and movement memories steer foraging bumblebees along habitual routes

“…While navigating along previously learnt habitual routes, ants and bees are guided by multiple systems relying on different types of memories, be they visual (Zeil, 2012;el Jundi et al, 2016;Wystrach et al, 2011;Menzel et al, 2019), olfactory (Buehlmann et al, 2014), path integration (Pfeffer and Wittlinger, 2016;Wittlinger et al, 2006) or sequence of movement memories (Zhang et al, 1996(Zhang et al, , 2012Macquart et al, 2008;Mirwan and Kevan, 2015). In the present study, the bees flew along a habitual route alternating left and right turns.…”

“…Thus, in the absence of other guidance systems, the insects may be guided by movement memories. Indeed, bees and ants are able to replicate a whole chain of manoeuvres in visually bare mazes (Collett et al, 1993;Zhang et al, 1996Zhang et al, , 2012Macquart et al, 2008;Mirwan and Kevan, 2015). The visual information is not present within the maze but only at its entrance.…”

“…Instead of frequently updating the direction in which to move, insects may encode the movement itself that needs to be carried out at specific locations, in the same way as a trained skier going downhill in a slalom will memorise every turn to travel as fast as possible. Although insects are capable of memorising and replicating a sequence of actions when olfactory and visual cues are not present (Collett et al, 1993;Zhang et al, 1996Zhang et al, , 2012Macquart et al, 2008;Mirwan and Kevan, 2015), movement memories have not usually been considered as an additional mechanism for following routes.…”