Exploring the Role of Cognition in the Annual Fall Migration of the Monarch Butterfly (Danaus plexippus)

SIMPLE SUMMARY: Each year, millions of monarch butterflies in eastern North America undergo a spectacular fall migration to overwintering sites in central Mexico, where they remain until returning northward in the spring. In addition to the navigational challenges faced during the southward flight, migratory individuals are also challenged with the foraging task of locating high-quality nectar sources for overwinter survival in the face of unfamiliar floral landscapes that change in complex and unpredictable ways. In the research reported here, a proboscis extension paradigm is used to investigate learning and long-term memory abilities that might help fall migrants meet these unique foraging demands. Male and female migratory and captive-reared individuals were consecutively trained to perform color and odor cue discriminations and then tested for their ability to simultaneously retain reward information associated with each cue in memory without reinforcement over a period of 7 days. Results showed that male and female fall migrants can learn the reward properties of color and odor cues with over 75% accuracy after less than 40 s of exposure and can simultaneously retain visual and olfactory information predicting the availability of floral rewards in memory without reinforcement for at least 7 days. Captive-reared male butterflies also showed the ability to retain visual and olfactory information in long-term memory for 7 days; however, 80% of captive-reared females could not retain color cues in long-term memory for more than 24 h. These novel findings are consistent with the view that monarch butterflies have enhancements to long-term memory that enable them to minimize the amount of time and energy wasted searching for suitable nectar sources during their annual fall migration, thereby optimizing migratory performance and increasing the chance of overwinter survival. The possibility that female monarchs undergo a seasonal change in visual long-term memory warrants further empirical investigation. ABSTRACT: Each fall, monarch butterflies in eastern North America undergo an extraordinary long-distance migration to wintering areas in central Mexico, where they remain until returning northward in the spring. Migrants survive the overwintering period by metabolizing lipid reserves accumulated exclusively though floral nectar; however, there is little known about how individuals maximize foraging efficiency in the face of floral environments that constantly change in complex and unpredictable ways along their migratory route. Here, a proboscis extension paradigm is used to investigate the role of cognition during the foraging phase of monarch migration. Male and female migratory butterflies were consecutively trained to discriminate between two color and odor cues and then tested for their ability to simultaneously retain the information on the reward value of each cue in memory without reinforcement over a period of 7 days. To gain further insight into cognitive abilities of monarchs as a migratory species, a second set of captive-reared males and females were tested under harnessed conditions at the same time as wild-caught fall migrants. Results showed that male and female migrants can learn the reward properties of color and odor cues with over 75% accuracy after less than 40 s of exposure and can simultaneously retain visual and olfactory information predicting the availability of floral rewards in memory without reinforcement for at least 7 days. Captive-reared male butterflies also showed the ability to retain visual and olfactory information in long-term memory for 7 days; however, 80% of captive-reared females could not retain color cues in long-term memory for more than 24 h. These novel findings are consistent with the view that monarch butterflies, as a migratory species, have enhancements to long-term memory that enable them to minimize the amount of time and energy wasted searching for suitable nectar sources during their annual fall migration, thereby optimizing migratory performance and increasing the chance of overwinter survival. The possibility that female monarchs undergo a seasonal change in visual long-term memory warrants further empirical investigation.