An observational study of ballooning in large spiders: Nanoscale multifibers enable large spiders' soaring flight

Abstract

The physical mechanism of aerial dispersal of spiders, "ballooning behavior," is still unclear because of the lack of serious scientific observations and experiments. Therefore, as a first step in clarifying the phenomenon, we studied the ballooning behavior of relatively large spiders (heavier than 5 mg) in nature. Additional wind tunnel tests to identify ballooning silks were implemented in the laboratory. From our observation, it seems obvious that spiders actively evaluate the condition of the wind with their front leg (leg I) and wait for the preferable wind condition for their ballooning takeoff. In the wind tunnel tests, as-yet-unknown physical properties of ballooning fibers (length, thickness, and number of fibers) were identified. Large spiders, 16-20 mg Xysticus spp., spun 50-60 nanoscale fibers, with a diameter of 121-323 nm. The length of these threads was 3.22 ± 1.31 m (N = 22). These physical properties of ballooning fibers can explain the ballooning of large spiders with relatively light updrafts, 0.1-0.5 m s-1, which exist in a light breeze of 1.5-3.3 m s-1. Additionally, in line with previous research on turbulence in atmospheric boundary layers and from our wind measurements, it is hypothesized that spiders use the ascending air current for their aerial dispersal, the "ejection" regime, which is induced by hairpin vortices in the atmospheric boundary layer turbulence. This regime is highly correlated with lower wind speeds. This coincides well with the fact that spiders usually balloon when the wind speed is lower than 3 m s-1.

Fig 1. Experimental materials and methods for identification of ballooning lines.

(A) A schematic view of wind tunnel tests. (B) Sampling of ballooning fibers in front of an open jet wind tunnel. (C) Reel with a steel wire to measure the length of ballooning silks.

Fig 2. Experimental material and place for 3-dimensional wind velocity measurement.

(A) A 3-dimensional ultrasonic anemometer (Windmaster 1590-PK-020, Gill Instruments) is installed 0.95 m above the ground. (B) The simplest conditions (i.e., a flat surface) were selected. The flat place is covered with the 6 cm short cut grass. Within a radius of 300 m, there is no obstacle object.

Fig 3. Sequence of active sensing motion with front leg (leg I) (negative images).

(A) The spider first senses the condition of the wind current only through sensory hairs on its legs. (B) Then, if the condition seemed appropriate, the spider sensed more actively by raising leg I and keeping this pose for 8 sec. (C) If the spider decided to balloon, it altered its posture. (D) The spider rotated its body in the direction of the wind and assumed tiptoe posture.

Fig 4. A crab spider’s ballooning process (images were converted to negative images to visualize ballooning lines).

(A, B) Initial phase of spinning ballooning lines; (C, D, E, F) Fluttering of a bundle of ballooning lines. Because of turbulent flows in wind, the ballooning threads fluttered unsteadily. (G) Takeoff moment. (H) Airborne state of a ballooning spider. (Original video: see S3 Video).

Fig 5. Sequential relations between behaviors for ballooning.

(A) The percentage frequency of the behavior transition (the total number of transitions: N = 141). (B) The transition matrix between behaviors (the total numbers of categorized behaviors: N_I = 25, N_S = 65, N_T = 41, N_D = 8, N_H = 2). The corresponding underlying data can be found in S1 Data. B, takeoff; D, dropping and hanging behavior; E, escape; H, hiding motion; I, initial state; N, not flown; S, sensing motion; T, tiptoe behavior.

Fig 6. Frequency diagram of tiptoe behaviors according to tiptoe duration (N = 42).

Black columns are the tiptoe behaviors that were connected to the successful ballooning takeoffs (N = 4). The corresponding underlying data can be found in S1 Data.

Fig 7. Sketches of ballooning structures (body + ballooning threads).

These structures were observed above the water surface, at heights of 1–8 m. Wind was blowing from left to right. Therefore, these structures were transported in the same direction as the wind. Black, thick points represent the spider’s body. Black lines represent ballooning threads.

Fig 8. Distribution of the length of ballooning lines (N = 22).

The corresponding underlying data can be found in S2 Data.

Fig 9. Scanning electron microscopic images of ballooning lines and drag lines.

(A) Ballooning fibers of X. cristatus (1,300×). (B) Ballooning fibers of X. audax (10,000×). (C) Middle part of ballooning fibers of X. audax (20,000×). (D) Ballooning fibers of X. cristatus (30,000×). (E) One pair of drag fibers of X. cristatus (a weight of 18 mg) (20,000×). (F) Two pairs of drag fibers of Xysticus spp. (a weight of 15.6 mg), which attached together (20,000×).

Fig 10. Horizontal and vertical components of the wind speeds for 5 min on u–w domain. (20-Hz sensing rate).

(A) The case of 1.99 m s⁻¹ mean wind speed (30 October 2016 12:39–12:45 LT). (B) The case of 3.07 m s⁻¹ mean wind speed (29 October 2016 10:54–11:00 LT). Orange cross points: the quadrant data (Q1–Q4) of the measured wind speeds according to u′ and w′. Blue cross points: the ignored data regarding as a small-scale fluctuation (H < 1). Red lines are linear regression fit lines. The corresponding underlying data can be found in S3 Data.

Fig 11. Takeoff process for tiptoe ballooning.

The probabilities are calculated based on the total number of behaviors at each stage (see Fig 5B).

Fig 12. Required updraft wind speed and length of ballooning silks for the ballooning of 80–150 mg Stegodyphus spp.

It is assumed that Stegodyphus spp. use 2 minor ampullate silks (2.1–2.9 μm thickness) and 78 aciniform silks (650–900 nm thickness) for their ballooning. The corresponding underlying data can be found in S4 Data.

Fig 13. Schematic diagram of updraft generation by a vortex and vortices in near-surface atmospheric boundary layer.

(A) Schematic diagram of a single hairpin vortex in the wall boundary layer. Q2 is an “ejection” region whose velocity vectors are u′ < 0 and v′ > 0. Q4 is a “sweep” region whose velocity vectors are u′ > 0 and v′ < 0. (B) Cross-section of the x-y plane of the hairpin vortex. (C) Schematic diagram of the hairpin vortex packet. Yellow colors mean hairpins or cane-type vortices. Blue region means low momentum region, which contains upward air currents. (D) Coherent structure, “dual hairpin vortex,” on the plant field. Head-down hairpin vortex produces “sweep” event. Head-up hairpin vortex produces “ejection” event. (A, B) Redrawn from [68]. (C) Redrawn from [68, 69]. (D) Redrawn from [70].