Geomagnetic and visual cues guide seasonal migratory orientation in the nocturnal fall armyworm, the world’s most invasive insect
- State Key Laboratory of Agricultural and Forestry Biosecurity, College of Plant Protection, Nanjing Agricultural University, China
- Lund Vision Group, Department of Biology, Lund University, Sölvegatan, Sweden
- Plant Protection Station of Yuanjiang County, China
- Key Laboratory of Surveillance and Management of Invasive Alien Species, Guizhou Education Department, Department of Biology and Engineering of Environment, Guiyang University, China
- Centre for Ecology and Conservation, University of Exeter, United Kingdom
Figures
Figure 1
Schematic of the experimental setup for studying magnetic orientation in fall armyworms.
Moths are tethered to a vertical shaft at the center of the virtual flight simulator, with an encoder recording their flight heading. A full-spectrum lamp illuminates the arena, while the computer controlling the experiment is positioned outside the light field to avoid interference. Moths are free to rotate in any direction during the assay. Full experimental details are given in Methods. The cylinder is illustrated as clear in the figure to reveal the internal setup, but it is opaque in the actual experiment.
Figure 2 with 3 supplements
The Earth’s magnetic field and visual cues guide migratory flight behavior in both a field population and lab-raised fall armyworms.
(A) Flight orientation behavior of a spring field population of moths (‘Spring Exp. Field’) in response to visual and geomagnetic cues. (B) Flight orientation behavior of a fall field population of moths (‘Fall Exp. Field’) in response to visual and geomagnetic cues. (C) Flight orientation behavior of lab-raised fall-conditioned moths (‘Fall Exp. Lab’) in response to visual and geomagnetic cues. (D) Flight orientation behavior of lab-raised control fall-conditioned moths (‘Fall Control’), tested with consistent visual and geomagnetic alignment. For simplicity and consistency, we tested only conditions in which the visual cue pointed in the putative migratory direction, coinciding with magnetic north in spring and with magnetic south in fall. The putative migratory direction was defined based on the seasonally different orientation directions revealed by our previous field experiments (Chen et al., 2023). Each group underwent five sequential 5 min phases (I–V), with each subplot representing individual moths’ flight directions in the simulator. The length of each vector represents individual directedness (r), ranging from 0 to 1, where the outer edge of the plot corresponds to r=1. The thick mean vector (MV) arrow represents the weighted average of individual orientations, calculated using Moore’s modified Rayleigh test (see Methods), and is red when there is significant group orientation but gray when it is not significant. The R* value quantifies the directedness of the MV. Dashed circles indicate thresholds for statistical significance, with radii corresponding to p<0.05 and p<0.01. Shaded sections of the outer diameters of the circles represent the 95% confidence limits of the group orientation. The outermost radius represents R*=2.5. The black triangle denotes the position of the visual cue, while the red triangle indicates the direction of the expected migratory orientation in each season (north in spring, south in fall). The experimental setup included both the natural magnetic field (NMF, panels with light green background) and a changed magnetic field (CMF, panels with light blue background) where the horizontal magnetic field direction was reversed; further details of the magnetic field parameters in the NMF and CMF are shown in Figure 2—figure supplement 1. The Fall Exp. Field is the only experiment for which results are based on pooled data from 2023 and 2024, with year-specific results provided in Figure 2—figure supplement 2.
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Figure 2—source data 1
Results of rayleigh tests for each individual.
- https://cdn.elifesciences.org/articles/109098/elife-109098-fig2-data1-v1.xlsx
Figure 2—figure supplement 1
The magnetic field conditions during experimental procedures in 2023 and 2024.
(A) Comparison of total magnetic field strength between the changed magnetic field (CMF) and natural magnetic field (NMF) (t-test, ECMF = 42.21 μT, ENMF = 42.02 μT, p=0.7869), showing no significant difference. (B) There is no significant difference in the intensity of the horizontal component between CMF and NMF (t-test, HCMF = 31.18, HNMF = 31.35, p>0.1). (C) There is no significant difference in magnetic inclination between CMF and NMF (Watson-U2, αCMF = 38.22°, αNMF = 38.28°, p=0.92). (D) Comparison of magnetic azimuth between CMF and NMF, demonstrating a highly significant difference (Watson-U2, βCMF = 175.62°, βNMF = 4.11°, p<0.001). (E) The magnetic component B, measured in nanoteslas (nT), of the time-dependent electromagnetic field across a 10 kHz resolution bandwidth (RBW), was analyzed as a function of frequency f, expressed in megahertz (MHz). The data shown in the figure represents the maximum locked values observed over a 40 min period at the experimental location (23.604°N, 101.977°E). Measurements were conducted using the Spectran NF5035 spectrum analyzer (1 Hz to 30 MHz, Aaronia AG), MDF9400 magnetic field antenna (9 kHz to 400 MHz, Aaronia AG), UBBV-MDF960X preamplifier (9 kHz to 60 MHz, with a gain of 25 dB), and a 10 m RF cable. The spectrum in the frequency range of 1 MHz to 10 MHz was first measured using the antenna paired with the preamplifier. Subsequently, low-frequency noise within the range of 2 kHz to 1 MHz was detected using the internal probe of the spectrum analyzer. Based on previous studies, electromagnetic noise can, under certain conditions, disrupt the magnetic compass of birds (Engels et al., 2014). Notably, a certain level of noise was present at the low-frequency end (left side of the spectrum) measured in the present study; however, our behavioral results indicate that this level of noise did not completely abolish the contribution of magnetic information to the observed behavioral responses.
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Figure 2—figure supplement 1—source data 1
Frequency spectrum of magnetic field (B) at 10 kHz RBW.
- https://cdn.elifesciences.org/articles/109098/elife-109098-fig2-figsupp1-data1-v1.xlsx
Figure 2—figure supplement 2
Year-specific analysis of orientation behavior in field-captured armyworms during the fall migration season (2023 and 2024).
(A) Orientation behavior of the field-captured population in fall 2023. (B) Orientation behavior of the field-captured population in fall 2024. Experiments were conducted using fall armyworms captured from the field, revealing consistent orientation behavior across both years. In both 2023 and 2024, moths oriented significantly toward the visual cue when visual and geomagnetic cues were aligned. However, after reversing the magnetic field, the strength of directional orientation gradually diminished. Due to limited sample sizes in each year, data from both years were pooled for a comprehensive analysis, as presented in Figure 2B.
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Figure 2—figure supplement 2—source data 1
Results of rayleigh tests for each individual in fall field experiments (2023–2024).
- https://cdn.elifesciences.org/articles/109098/elife-109098-fig2-figsupp2-data1-v1.xlsx
Figure 2—figure supplement 3
Spectral distribution of light provided by the full-spectrum lamp.
The spectral distribution of the full-spectrum lamp used in the experiment was measured using an ATP2000P spectrometer (Optosky Technology Co. Ltd., Xiamen, China). The sensor was positioned vertically upward at the location originally occupied by the moth’s head to measure the spectral irradiance of the light after it passed through the softbox, diffusion paper, and transparent acrylic cover. The results indicate that light radiation was detectable across most wavelengths between 200 and 850 nm, confirming that our experimental setup provided a full-spectrum light environment from ultraviolet to near-infrared wavelengths. This spectral range encompasses the known visual sensitivity of moths (Warrant and Somanathan, 2022). Consequently, the acrylic plate and diffusion paper did not significantly block light radiation at any specific wavelength within this range. The ambient light level in the experimental environment was measured to be below 1 lux using a Testo 540 lux meter, manufactured by Testo SE & Co. KGaA (Titisee-Neustadt, Germany).
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Figure 2—figure supplement 3—source data 1
Spectral distribution of light provided by the full-spectrum lamp.
- https://cdn.elifesciences.org/articles/109098/elife-109098-fig2-figsupp3-data1-v1.csv
Figure 3
Fall armyworms exhibit a delayed response to changes in magnetic-visual cue alignment.
The behavioral data for (A) fall field population experimental (‘Fall Exp. Field’, data from Figure 2B), (B) fall lab-raised experimental (‘Fall Exp. Lab’, data from Figure 2C), and (C) fall lab-raised control (‘Fall Control’, data from Figure 2D) groups were analyzed in 30 s time bins, resulting in 10 bins over each 5 min phase of the experiment. For each group, Moore’s modified Rayleigh test was applied, and the obtained R* values were plotted against time. R*>1 indicates a significant collective orientation within that 30 s interval, while R*<1 indicates the absence of significant group-level orientation.
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Figure 3—source data 1
Time-binned analysis of collective orientation using Moore’s modified rayleigh test (R*).
- https://cdn.elifesciences.org/articles/109098/elife-109098-fig3-data1-v1.xlsx
Figure 4 with 1 supplement
Visual information is essential for maintaining group flight orientation in fall armyworms.
(A) The lab-raised, fall-conditioned population lost significant group orientation under complete darkness (‘Fall Exp. Dark’). (B) The lab-raised, fall-conditioned population exhibited a significant loss of group orientation under illuminated conditions where visual cues were reduced to the bare minimum (‘Fall Exp. BMVC’), i.e., obvious visual cues such as the black triangle shown in Figure 1 were not provided; however, because the experiments were conducted under illuminated conditions, complete elimination of all visual information is impossible. (C) The distribution of Rayleigh test r-values for individual moth orientations across different treatment groups (left) and the distribution of average directional change per second (right), the latter reflecting flight stability. The box plots represent the interquartile range (IQR), with the horizontal line inside indicating the median. Whiskers extend to the most extreme data points within 1.5 times the IQR. Pairwise comparisons of the r-values were performed using the Wilcoxon rank-sum test and Wilcoxon signed-rank test. (The Wilcoxon signed-rank test is only used to compare non-independent [i.e. paired or related] samples. For more information, please refer to the Statistical analysis section.) Multiple comparisons were corrected by the Benjamini-Hochberg method. Detailed statistical results are provided in Supplementary file 4. Comparisons of the average directional change per second were performed using the same method as that used for r-values, with statistical results provided in Supplementary file 5. Groups labeled with different letters differ significantly (p<0.05). We also analyzed the r-values and average directional change per second in the Fall Exp. Field, Fall Exp. Lab, Exp. Fall Control, and the experiment shown in this figure, with results consistent with those shown here (see Supplementary files 4 and 5, Figure 4—figure supplement 1).
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Figure 4—source data 1
Individual rayleigh test data from Fall Exp. Dark and Fall Exp. BMVC.
- https://cdn.elifesciences.org/articles/109098/elife-109098-fig4-data1-v1.xlsx
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Figure 4—source data 2
Individual r values and mean directional change in Fall Exp. Dark and Fall Exp. BMVC.
- https://cdn.elifesciences.org/articles/109098/elife-109098-fig4-data2-v1.xlsx
Figure 4—figure supplement 1
The Lack of Visual Cues and Other Necessary Visual Information Significantly Affects Moth Orientation Ability and Flight Stability.
(A) Box plots show the distribution of Rayleigh test r-values for individual orientations of moths in different treatment groups. (B) Box plots show the distribution of average directional degree change per second, reflecting flight stability, across treatment groups. Boxes represent the interquartile range (IQR), with the horizontal line inside indicating the median. The ‘whiskers’ extend to the most extreme data points within 1.5 times the IQR. Error bars indicate data variability, facilitating comparison between groups. Pairwise comparisons in (A) were conducted using the Wilcoxon rank-sum test with multiple comparisons corrected by the Benjamini-Hochberg method. Detailed statistical results are provided in Supplementary file 4. In (B), comparisons were performed using the Wilcoxon rank-sum test. Groups labeled with different letters differ significantly (p<0.05). Detailed statistical results are provided in Supplementary file 5.
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Figure 4—figure supplement 1—source data 1
Rayleigh test r values and mean directional change for individual moth orientations across treatment groups.
- https://cdn.elifesciences.org/articles/109098/elife-109098-fig4-figsupp1-data1-v1.csv
Additional files
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Supplementary file 1
Detailed data of flight orientation behavior assay.
- https://cdn.elifesciences.org/articles/109098/elife-109098-supp1-v1.xlsx
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Supplementary file 2
Friedman test results of Rayleigh’s r values across experimental groups.
- https://cdn.elifesciences.org/articles/109098/elife-109098-supp2-v1.xlsx
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Supplementary file 3
Pairwise comparison results of the mean Rayleigh’s r values of Exp. Spring across different experimental phases, using the Wilcoxon signed-rank test with multiple-comparison correction performed by the Benjamini-Hochberg method.
- https://cdn.elifesciences.org/articles/109098/elife-109098-supp3-v1.xlsx
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Supplementary file 4
Multiple comparisons of mean Rayleigh test r values across experimental conditions using the Wilcoxon rank-sum test (adjusted by the Benjamini–Hochberg method).
Note: A: Fall Exp. Field; B: Fall Exp. Lab; C: Fall Control; D: Fall Exp. Dark I; E: Fall Exp. Dark II; F: Fall Exp. BMVC.
- https://cdn.elifesciences.org/articles/109098/elife-109098-supp4-v1.xlsx
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Supplementary file 5
Wilcoxon rank-sum test for mean angular velocity (directional change per second) across experimental conditions (Benjamini–Hochberg correction).
Note: A: Fall Exp. Field; B: Fall Exp. Lab; C: Fall Control; D: Fall Exp. Dark-I; E: Fall Exp. Dark-II; F: Fall Exp. BMVC.
- https://cdn.elifesciences.org/articles/109098/elife-109098-supp5-v1.xlsx
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Geomagnetic and visual cues guide seasonal migratory orientation in the nocturnal fall armyworm, the world’s most invasive insect
eLife 14:RP109098.
https://doi.org/10.7554/eLife.109098.4
