Individuals of many species use cues derived from their environment to facilitate ecologically important goal-directed movement within the landscape. The long-distance fall migration of the iconic monarch butterfly, Danaus plexippus (Lepidoptera; Nymphalidae), is a spectacular example of goal-directed animal movement phenomena during which individuals use environmental sensory cues to guide them during their long journey, in order to reach their goal destination [1, 2]. During the fall, millions of Eastern North American monarchs leave their summer breeding grounds in Southern Canada and the Northern United States, and migrate to a handful of select overwintering sites high atop a few mountain ranges in Central Mexico [3, 4].
Fall migrant monarchs have previously been shown to use sensory-based compass mechanisms to maintain the proper southwards flight orientation during the fall migration . The dominant compass used by monarchs is the time-compensated sun compass [5, 6, 7]. Monarchs use the sun as a skylight visual cue to maintain the proper southwards flight heading. Given the sun’s apparent change in position in the sky throughout the day due to the Earth’s daily rotation about its axis, monarchs use their internal circadian clock as a timing mechanism to compensate for the sun’s movement, in order to properly use the sun as a directional cue throughout the fall migration. On cloudy days when directional daytime skylight cues are unavailable, e.g., overcast conditions, migrants can use a magnetic compass as a backup mechanism for southwards directionality . Monarchs use the inclination angle of the Earth’s magnetic field that co-varies predictably with latitude, as another directional cue for flying southwards. Although these compasses can be used for maintaining proper flight directionality, monarchs cannot use these mechanisms for locating and stopping at the overwintering sites, as they only allow monarchs to orient in the direction of their goal destination. It remains a great mystery as to how naïve fall migrant monarchs on their maiden flight, find the same overwintering grounds year after year.
It is possible that monarchs use a map sense for locating the overwintering sites. A map sense allows monarchs to know both the direction that they should fly in and their respective geographic location relative to their goal [2, 9]. This map sense most likely consists of a genetically imprinted “overwintering site” location, as fall monarchs reaching the overwintering sites have never been there before. One type of map sense possessed by long-distance migrants is that of a geomagnetic map sense , as demonstrated by long-distance migratory animals such as sea turtles , birds , salmonid fish , eels , newts , and spiny lobsters . The innate map sense of naïve individuals on their first migratory journey (and only southwards migratory journey for fall monarchs) is hypothesized to rely on the recognition of specific regional and site-specific geomagnetic conditions (e.g., bicoordinate map coordinates based on inclination angle and total intensity; ) that serve as geomagnetic cues or signposts on a magnetic map that can lead individuals to the approximate location of their goal destination. These geomagnetic conditions can also elicit specific behavioral responses that then allow individuals to find their actual goal destination, a finely-tuned process which might rely on sensing other environmental cues that are correlated with these geomagnetic map signatures, or that are present at the geographical locations indicated by these geomagnetic conditions [9, 10]. Therefore, in addition to using magnetic cues for southwards flight directionality, fall migrant monarchs may therefore use their magnetic sense to recognize the geomagnetic signatures of the overwintering sites as part of an inherited magnetic map sense for locating the small number of overwintering sites in Mexico . The possibility that monarchs possess a map sense remains controversial [16, 17, 18].
To test for a geomagnetic map sense, researchers have used displacement trials. Here, individuals are physically displaced to unfamiliar, geographical locations to determine if they will adjust their behavior to correct for the displacement, e.g., [15, 19, 20]. Alternatively, animals have been tested in simulated magnetic displacement experiments. These studies subject individuals to artificially generated magnetic fields of locations that are different from the testing site and the behavior of individuals is monitored for the expression of predicted responses or for any changes in behavior, e.g., a change in orientation behavior relative to what is observed or expected at a control site . A similar, but less frequently used method for testing for the existence of a geomagnetic map sense is to examine the behavior of animals in response to the Earth’s shifting magnetic field over time, i.e., secular variation of the geomagnetic field . This approach examines the behavior of individuals in response to the natural displacement of the Earth’s magnetic field under natural conditions over time.
In this study, we used a natural experiment, the change in the Earth’s magnetic field from 2004 to 2018, to test the provocative hypothesis that D. plexippus uses innate responses tuned to specific geomagnetic cues to facilitate map sense navigation to a specific location, i.e., the overwintering sites in Central Mexico. We hypothesize that if D. plexippus navigates to specific locations based on an innate magnetic map sense, that there should be a progressive shift in the overwintering range from southern to northern sites, as monarchs track the decreases in the intensity and inclination angle of the magnetic field over time. As the geomagnetic parameters associated with the geographical locations of the overwintering sites have naturally shifted northwards, monarchs should adjust where they stop in Mexico and where they form overwintering aggregations, if they rely exclusively or predominantly on an innate magnetic map sense calibrated to specific geomagnetic signatures. Alternatively, if monarchs do not respond to changes in the Earth’s magnetic field, e.g., they continue to overwinter in geographical locations that now possess significantly different geomagnetic signatures due to the shifting geomagnetic field, this would indicate that they do not have a map sense navigation system that relies on responding to specific geomagnetic signatures in Mexico for finding the overwintering sites. This would suggest that monarchs might then rely on other cues for stopping at the overwintering sites once they are nearing or are in Mexico [9, 21].