James E. Kanz.
The Orientation of Migrant and Non-Migrant Monarch Butterflies, Danaus plexippus (L.).
Psyche 84:120-141, 1977.

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THE ORIENTATION OF MIGRANT AND NON-MIGRANT MONARCH BUTTERFLIES, DANAUS PLEXIPPUS (L.) BY JAMES E. KANZ*
Department of Biology
Tufts University
Medford, Massachusetts 02155
Many species of butterflies migrate (Nielsen and Nielsen, 1952; Tilden, 1962; Williams, 1951, 1958). The fall southward migration of the North American Monarch butterfly, Danaus plexippus L., isa classic example of long-distance insect migration (Urquhart, 1960, 1976; Walker, 1914; Williams, Cockbill, Gibbs, and Downes, 1942). Evidence from tagging studies indicates that the same but- terflies traveling south in the fall return northward the following spring (Urquhart, personal communication). It is unlikely, how- ever, that fall migrants from the northern latitudes (48O N) return as far north in the spring.
Johnson (1969), Urquhart (1960), Williams et al. (1942), and Williams (1958) have provided descriptive information on several aspects of D. plexippus migration. However, little experimental work exists on the isolation of environmental orientation cues and their role in the seasonal movements of the Monarch. Baker (1968a) hypothesized an evolutionary scheme for the development of sun- orientation in a butterfly's search for new habitats. Using field data on general flight directions of migrating European butterflies, Baker (1968a,b) determined that sun orientation was apparently used by Pieris rapae, P. brassieae, P. napi, Maniola jurtina, Aglis urticae, and Inaehis io during their migrations. This paper reports which environmental orientation cues are used by caged migrant and non- migrant Monarchs, and suggests how such cues are used. 'Present address: Marine Biomedical Institute, University of Texas Medical Branch, 200 University Boulevard, Galveston, Texas 77550. Manuscript received by the editor August 20, 1977.



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Kanz - Monarch Butterfly Orientation
MATERIALS AND METHODS
Experiments used laboratory-reared and "wild-caught" Monarch butterflies (D. plexippus L.) of both sexes. The laboratory colony was reared from the egg under mid-summer conditions: 24OC under a 15:9 hour light/ dark schedule (Kanz, 1973; Urquhart and Stegner, 1966). Some laboratory-reared Monarchs were reared under a photoperiod advanced 6 hours. Predominantly laboratory-reared animals were used for summer experiments. Wild-caught migrants were used in fall tests. Fall migrants were maintained in the field in frame cages (3 X 3 X 2% m) covered with nylon netting and placed over patches of golden rod and asters.
Summer experiments with non-migrants were conducted in an open field in Lexington, Massachusetts. Studies with fall migrants were conducted at the Eastern Point Audubon Sanctuary in Glouces- ter, Massachusetts. Eastern Standard Time (EST) was used for summer and fall experiments.
Experimental orientation cages were circular (80 cm diameter) and mounted on a rotatable base. The floor of the cages was marked off into 45' sectors. The periphery (20 cm height) and top were wire screening. Entrance was through a door in the top. Two types of orientation cages were used: (1) transparent-periphery cages with both terrestrial and celestrial cues visible and (2) opaque- periphery cages with a beige strip of no-glare cloth around the periphery so only celestial cues were visible. Experiments were conducted under sky conditions ranging from clear to overcast. Orientation cages were placed in the center of a field so that terrestrial cues were symmetrical about the cages. Ter- restrial cues were distant enough so as not to be visible to animals in opaque-periphery cages. Cages were oriented to true north and the cages could be rotated to any desired azimuth. Male or female Monarch butterflies (N = 10-20) were released into an orientation cage, and data collection started 15 min later. Cage positions of the Monarchs were monitored at intervals rang- ing from 1 to 15 min and positions were scored on circular data sheets divided into 45' sectors. Each animal's position in relation to true north could be designated within k 5'. With few exceptions, the cage position recorded for each animal was a resting position (i.e., the butterfly was not in flight). Following each reading, the cage was usually rotated. The side of the cage from which the



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122 Psyche [June
observations were made was randomized, but always excluded those sides directly toward and away from the sun. The presence of the experimenter during a reading (an elapsed time of 10-30 sec) did not appear to affect the butterflies' positions. Unless otherwise noted, animals were used for only one experiment and then released with vanishing azimuths recorded; males or females were used in a particular experiment.
The butterflies' orientation cage positions were converted to azimuths with a protractor. These orientation azimuths were then treated as a circular distribution and the following parameters ob- tained for each observation time (Batschelet, 1965; Greenwood and Durand, 1955): (1) mean orientation direction (6); (2) a grouping factor (r) indicating the extent to which the butterfly azimuths for an observation were concentrated about the 6 for that observation; (3) an angular deviation (AD) for 6; and (4) the probability (P) of r occurring by chance. Computer plots were made for 6 and the sun azimuth values as a function of time of day. The orientation response of the Monarchs was considered significant when the P for a distribution of animals (in the orientation cages or vanishing azimuths) was < 0.05.
Other data recorded at each reading included: (1) time of day; (2) temperature; (3) humidity; (4) surface wind velocity (with a Taylor 3105 anemometer) and direction; (5) sun azimuth and alti- tude computed from a Nautical Almanac and Tables of Computed Altitude and Azimuth for the appropriate latitude. Ambient tem- perature for the fall tests (10å¡-18 C) was lower than for summer (18'-32OC) experiments. When ambient temperatures fell below 16' C, the butterflies displayed sunning behavior: turning away from the sun and spreading the wings in order to increase surface area exposed to sun and thus body temperature (Kanz, 1973; Urqu- hart, 1960). Sunning is often accompanied by shivering (Kammer, 1968, 1970; Urquhart, 1960), and was only seen in fall migrants. Sunning Monarchs were indicated on the data sheets and in sub- sequent analyses, computation of 6, AD, r and P with and without sunning Monarchs were made.
Field Behavior of Migrant and Non-Migrant Monarch Butterflies Non-migrant summer Monarchs left their overnight roosting trees



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19771 Kanz - Monarch Butterfly Orientation 123 as soon as ambient temperatures permitted flight (approximately 13'C) and engaged in feeding and mating throughout the day until sunset.
Fall migrating Monarchs passing through Gloucester, Massa- chusetts, frequently remained in the area for several days, depend- ing upon weather conditions. Fall migrants left overnight roosting trees to feed (except when it rained) when ambient temperatures exceeded 10'-12' C (Kanz, 1973); mating occurred infrequently. At approximately 1600 hrs (EST) the butterflies returned to their roosting trees. This cycle was repeated each day until migration resumed.
Fall migratory flights occurred between 1000 and 1400 hrs, EST (Brower, personal communication; Urquhart, personal comminication).
Fall migratory flight occurred with north, north- east, or northwest winds.
Butterfly Orientation in Opaque Periphery Cages Laboratory-reared, non-migrants oriented toward the sun's azi- muth throughout the day when the sun was the only environmental cue available (Fig. 1). To examine the possibility that this orienta- tion was actually a shade-seeking response (i.e., orienting to the shaded area of the cage and thus the side toward the sun) a sun- shade was positioned so that a shadow was cast over the half of the orientation cage facing the sun. If butterflies were seeking shade, their cage positions should fall within the shaded area of the cage. If Monarchs were sun-orienting, the butterflies would move toward the sun's azimuth, stopping as they entered the shaded portion of the cage and their cage positions would fall along the shade line cast by the sun-shade. For such an experiment, 59% of the butterflies' cage positions were within k 5 cm of the shade line; and 72% of the cage positions were on the lid. Therefore, sunward orientation of caged, summer, non-migrants seemed to be an orien- tation to the sun and not an attempt to seek shade. Without celestial or terrestrial cues (overcast day), laboratory- reared, summer, non-migrants displayed a random orientation pat- tern (Fig. 2). With the sun visible, the mean absolute difference between a given 6 and the sun's azimuth for that 6 (i.e.,Ib-sun azimuth]) was 23' for opaque periphery cage, laboratory-reared, non-migrants, and 99O without the sun visible (Table I). Seventy- three percent of the sun-visible readings, versus 2% of the no-sun readings, showed significantly different Monarch cage distributions



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sun azimuth
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angular deviation
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TIME OF DAY IN HOURS (EST)
Fig. 1.
Orientation of laboratory-reared, summer, non-migrants in an opaque periphery cage on a clear day. 0's lie close to the sun azimuth line throughout the course of the test.
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TIME OF DAY IN HOURS (EST)
Fig. 2.
Random mean orientation of summer, laboratory-reared monarchs opaque periphery cages on an overcast day. (Raleigh Test, P < .05). Thus, caged non-migrant Monarchs re- sponded to the sun as an orientation cue. Two tests under sun- visible and no-sun-visible conditions using wild-caught summer, non-migrants, paralleled the results with laboratory-reared animals: wild-caught non-migrants, sun-oriented on clear days but oriented randomly on overcast days. However, if summer Monarch followed the azimuth of the sun, their daily movement would be to the south. Such a movement is inconsistent with the random wandering ob- served for summer non-migrants (Urquhart, 1960). Therefore, the sun orientation of summer non-migrant Monarchs in opaque cages



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19771 Kanz - Monarch Butterfly Orientation 125 with the sun visible may have been an escape reaction (see Discus- sion).
Fall migrants in opaque periphery cages also displayed a sun orientation when the sun was visible (Fig. 3): mean 1 &sun azimuth 1 = 39O, 31% of the readings showing significant Monarch concen- trations about the mean orientation direction (Table I). Low am- bient temperatures during fall tests (lo0 -IS0 C) compared to sum- mer tests (18O-32OC) might be one reason for the difference in sun-orienting response between the two populations. However, the data suggest that caged fall migrants sun-orient when the sun is their sole orientation cue. Sun orientation would result in fall migrants moving south, the direction Monarch butterflies take during their fall migration. A distinction can be seen between the sun orientation of fall migrants and summer non-migrants in opaque periphery cages: the mean 1 &sun azimuth 1 value for fall mi- grants was not as consistent throughout the day as it was for non- migrants. Caged fall migrants showed a mean orientation direction closer to the sun's azimuth (mean 1 &sun azimuth 1 = 3 lo) from 1000 to 1400 hrs (EST) than before or after this time period (mean 10-sun azimuth 1 = 44' and 52O, respectively). The 1000-1400 hrs time period corresponds to the migratory period of fall migrants (Brower, personal communication; Kanz, 1973; Urquhart, personal commu- nication; Kanz, 1973; Urquhart, personal communication). The sun-orienting response of non-migrants on the other hand, was consistent, or even improved, throughout the course of the day (30å¡ 27O, and 12O, respectively for prior to 1000 hrs, 1000-1400 hrs and after 1400 hrs). This suggests that there is more to the sun orientation of fall migrants than a sun-orienting escape response. The wider divergence of 0's from the sun's azimuth in the fall tests cannot wholly be ascribed to cooler autumn temperatures in the morning and late afternoon hours. Two fall experiments, in- cluding that illustrated in Fig. 3, were conducted when ambient temperatures ranged from 13O to l6O C. This temperature range was less than or equal to that recorded for the time period 1000- 1400 hrs for all but two of the remaining fifteen tests of this series (i.e., fall migrants in opaque periphery cages with the sun visible). Caged migrants from these two tests still showed a mean orienta- tion closer to that of the sun's azimuth during the observed 1000- 1400 hr migratory period. The orientation of caged fall migrants was random on overcast days (Table I).




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19771 Kanz - Monarch Butterfly Orientation 127 x 360
sun az imu t h
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TIME OF DAY IN HOURS fEST)
Fig. 3.
Orientation of fall migrants captured in the field and tested in opaque periphery orientation cages on a clear day. The orientation displayed by these migrants was a sun orientation.
The consistently random orientation of all Monarchs in no-sun tests, and the random orientation of summer non-migrants reared under a photoperiod advanced 6 hours and tested on no-sun days (Table I), argue against a time-compensating, sun-compass orienta- tion in experiments with opaque periphery cages. von Frisch (1967) showed that a patch of blue sky subtending an angle of only 10å to 15' was not only sufficient for the honeybee to localize the sun's position, but also that the honeybee was capable of a sun-compass orientation using polarized light. The sun's position can be uniquely described for most times of the day by the pattern of polarized light (Stockhammer, 1959; von Frisch, 1967). Experiments with summer laboratory-reared non-migrants and fall Monarchs suggested that the sun orientation of these animals was dependent on the sun being directly visible. On partly cloudy days, opaque periphery cage non-migrants and fall migrants oriented randomly when the sun was obscured by clouds but sun-oriented when the sun was not obscured by clouds. Summer non-migrants (laboratory-reared) and fall migrants, in opaque cages with a sun-shade blocking the sun but the remainder of the sky visible, showed a random orientation with the shade in place and a sun orientation when it was removed (Table I).
Orientation in Transparent Periphery Cages Tests performed with transparent periphery orientation cages exposed Monarchs to terrestrial as well as celestial orientation cues.



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19771 Kanz - Monarch Butterfly Orientation 129 The orientation of summer laboratory-reared, non-migrant Mon- archs in transparent periphery cages was random with or without the sun visible (Table 11), and was comparable to the random orientation shown by opaque periphery cage non-migrants and migrants in the absence of sun cues. Therefore, the presence of terrestrial cues over-rides the sun-orienting escape response of non-migrant Monarchs. It is possible that using terrestrial instead of sun cues each non-migrant butterfly persisted in its orientation cue for escape. These experiments demonstrate that the majority of non-migrant Monarchs chose terrestrial rather than sun cues for orientation when both were available.
Fall migrants, exposed to both terrestrial and sun cues, continued to orient to the sun's azimuth (Fig. 4, Table 11) with an orientation closer to the sun's azimuth from 1000-1400 hrs, EST, than either before or after this period (10-sun azimuth 1 value being 35O, 52O and 77O, respectively). An exception was seen in one sun-visible test, in which 0's from most significantly grouped animals main- tained an approximately 240' heading (southwest). However, this occurred only once and one cannot determine whether terrestrial or celestial cues were used. Random orientation resulted with terrestrial cues present but sun clues absent (Table 11). The per- sistent sun orientation of fall migrants, when the sun and terrestrial cues were visible, is additional support for the hypothesis that the sun orientation of fall migrants is a migratory response and not merely an escape response.
Flight Directions Following Release
Monarchs were released after each experiment and an azimuth reading taken on the vanishing direction of each butterfly using a Silva compass compensated for declination angle. Only those but- terflies that flew to the horizon were used in the analysis of Monarch vanishing directions. All Monarchs exhibited speed flight (Urqu- hart, 1960) immediately upon release. Occasionally Monarchs showed a feeding flight pattern with short randomly directional flights between flowers. When feeding flight took a butterfly to the horizon of the test field within 2 minutes, its azimuth at the periphery was included in the analysis; if feeding flight persisted, the vanishing azimuths of such animals were excluded from com- putations. Flight altitudes of released Monarchs were evenly di- vided between those above and below approximately 8 meters.



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s u n azimuth line
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TIME OF DAY IN HOURS (EST)
Fig. 4. Orientation displayed by fall migrants in a transparent periphery cage on a clear day. In contrast to summer non-migrants, fall migrants continue to sun-orient in the presence of both sun and terrestrial cues. Readings beginning at 1345 hrs (EST) were an artifact of a sudden ambient temperature drop. The results of summer Monarch releases with the sun visible showed that most vanishing azimuths appeared to be down-wind rather than toward the sun (Fig. 5). Only the releases of (c), (f) and (h) were significantly grouped about their respective mean orientation direction. Vanishing azimuths for summer non-mi- grants on overcast days were down-wind (Fig. 6). The distribution of releases in all but (c) were significant about their respective 0's. The releases of (f), with only a light surface wind, appear to be in the direction of the sun's azimuth even though the sun's position was obscured by clouds. However, most of these butterflies flew at an altitude 2 20 m and, therefore, likely encountered stronger winds. The vanishing directions of summer Monarchs, therefore, appeared more influenced by wind than by sun. Vanishing azimuths were more scattered with light winds (< 5 mph or 8 km/ hr). Low flight enabled Monarchs to fly against head winds that exceeded 10 mph (16 km/hr). Thus, Monarch flight direction was greatly influenced by the wind but was not competely determined by wind direction.
Figure 7 shows the patterns of vanishing azimuths for fall mi- grants when the sun was visible. All 20 distributions were signifi- cant about their respective 0's. The vanishing azimuths generally corresponded to the direction in which the wind was blowing with the exception of (a), (m) and (t). The releases of (a) occurred from a site that was surrounded by water except to the west; Urquhart



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19771
Kanz - Monarch Butterfly Orientation
Fig. 5. Release orientation for summer monarchs on clear days. For each circle: Dot indicates the vanishing direction of a butterfly; star indicates sun position at the time of release; radial arrow indicates direction in which wind was blowing and its velocity in miles per hour; N indicates true north. Most vanishing azimuths are seen to be down-wind.




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Fig. 6.
Release orientation for summer monarchs on overcast days. Symbols are as in Fig. 5. Most vanishing directions were down-wind. (1960) has observed that Monarchs tend to avoid flying over water when possible, Most flights in (m) were low to the ground, as was true for the majority of flights showing vanishing azimuth into the wind. The releases of (t) occurred at 1600 hrs (EST) when migrants return to roosting trees for the night. The roosting trees for mi- grants at Gloucester were west and northwest of the release and feeding sites. Thus, the migrants of (t) were possibly returning to their roosting trees; however, it is unclear why the butterflies in (c) chose a similar direction at 1300 hrs (EST) with the same wind velocity as in (t).
Vanishing directions appeared to be down-wind, particularly when winds exceeded 10 mph (16 km/ hr) unless the butterfly flew low to the ground. Two-way analysis of variance between the mean angular deviation of 22' for (h), (i), (k), (l), (n) and (0) and the mean angular deviation of 42' for the remaining fourteen release distributions indicate significant differences (F = 9.5, df = 16, P < .01). In the former case, the wind was blowing in the same direction (southwest) as the sun's azimuth. In the latter case, the wind and sun azimuth directions did not coincide. Analysis of variance of



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Kanz - Monarch Butterfly Orientation
133
Fig. 7.