The tethered flight technique as a tool for studying life-history strategies associated with migration in insects

Abstract

1. Every year billions of insects engage in long-distance, seasonal mass migrations which have major consequences for agriculture, ecosystem services and insect-vectored diseases. Tracking this movement in the field is difficult, with mass migrations often occurring at high altitudes and over large spatial scales. 2. As such, tethered flight provides a valuable tool for studying the flight behaviour of insects, giving insights into flight propensity (e.g. distance, duration and velocity) and orientation under controlled laboratory settings. By experimentally manipulating a variety of environmental and physiological traits, numerous studies have used this technology to study the flight behaviour of migratory insects ranging in size from aphids to butterflies. Advances in functional genomics promise to extend this to the identification of genetic factors associated with flight. Tethered flight techniques have been used to study migratory flight characteristics in insects for more than 50 years, but have never been reviewed. 3. This study summarises the key findings of this technology, which has been employed in studies of species from six Orders. By providing detailed descriptions of the tethered flight systems, the present study also aims to further the understanding of how tethered flight studies support field observations, the situations under which the technology is useful and how it might be used in future studies. 4. The aim is to contextualise the available tethered flight studies within the broader knowledge of insect migration and to describe the significant contribution these systems have made to the literature.

Keywords: Animal orientation; dispersal; insect movement; migration; tethered flight.

Figure 1

The rotational tethered flight mill system. (a) A diagram of a computerised tethered flight mill designed at Rothamsted Research (Lim et al., 2013). A lightweight flight mill arm is positioned between two magnets to reduce friction and encourage natural flight. The axis of the flight mill arm contains a striped disc which is scanned by the light detector on rotation of the mill arm. The light detector is wired to a computer connection in which the data are collected. The distance travelled is recorded to the nearest 10 cm and is updated every 5 s. The current system can fly 48 insects simultaneously. Insects are connected to one side of the mill arm via a pin attached to the thorax and fly in a circular trajectory with a one‐circuit circumference of 50 cm. (b) A time series plot of the flight activity of four adult moths Helicoverpa armigera flown over the course of the same night on the rotational flight mills between 19.00 and 08.30 hours (the following morning). [Colour figure can be viewed at http://wileyonlinelibrary.com].

Figure 2

Recorded maximum speeds obtained by various species in studies using rotational flight mills. The maximum flight speed was taken for the soybean aphid, Aphis glycines (Zhang et al., 2008), green lacewing, Chrysoperla sinica (Liu et al., 2011), brown planthopper, Nilaparvata lugens (Zhao et al., 2011), harlequin ladybird, Harmonia axyridis (Lombaert et al., 2014), beet webworm, Loxostege sticticalis (Cheng et al., 2012), cotton bollworm, Helicoverpa armigera (Jones et al. unpublished data), monarch butterfly, Danaus plexippus (Davis et al., 2012) and the painted lady, Vanessa cardui (Jones & Minter unpublished data). [Colour figure can be viewed at http://wileyonlinelibrary.com].

Figure 3

Variation in flight activity by Helicoverpa armigera recorded on the Rothamsted flight mill. (a) The total distance (m) covered by adult moths of H. armigera over the course of a single experiment. (b) Principal components analysis biplot of 16 tethered flight mill variables from flight activity of UK moths. The two first principal components (PC 1, PC 2) are plotted with the proportion of variance explained by each component printed next to the axis label, which together explain > 70% of variation in the data. Crosses indicate the 456 male individuals in the dataset; the top and right axes show principal component scores of the individuals. The arrows indicate the principal component loadings of the different tethered flight variables.

Figure 4

The flight simulator for determining flight orientation in day‐flying insects. (a) Diagram of the flight simulator designed by Mouritsen & Frost (2002). The insect is connected to an optical encoder via an attached pin on the back of the thorax that fits into a piece of plastic tubing at the end of a tungsten rod. The encoder possesses a low friction bearing allowing the insect to turn in any direction which is recorded to the nearest 3° every 200 ms. The fan at the bottom of the simulator creates a parallel air flow underneath the flying insect. (b) An example flight path produced by a painted lady butterfly, Vanessa cardui (Nesbit, 2009). (c) Individual mean flight headings of painted ladies flown under simulated overcast conditions; (d) individuals flown under clear‐sky conditions with visual access to the position of the sun during the autumn migration period and showing a mean orientation due south (Nesbit et al., 2009). Black arrows represent the mean direction with the length equivalent to the r‐value. Data were collected in 2006 (black circles), 2007 (grey circles) and 2008 (white circles). Solid lines are 95% confidence intervals. [Colour figure can be viewed at http://wileyonlinelibrary.com].

Figure 5

Insights into the migratory syndrome from tethered flight studies. (a) Coldness influences the direction of migratory flight in monarch butterflies, Danaus plexippus (Guerra & Reppert, 2013). (i) Mean monthly day lengths (yellow) and mean monthly low temperature (blue) at the monarch overwintering site; (ii) increasing photoperiod and low temperatures shift the orientation of fall migrants north; (iii) this orientation remains the same under constant photoperiod. (b) The association of oviposition and flight propensity in the female beet webworm, Loxostege sticticalis (Cheng et al., 2016). (i–iii) Changes in flight distance (m) (i), flight velocity (km h^–1) (ii) and flight duration (h) (iii) with increasing days after oviposition with mated (solid circle •) and virgin (empty circle ○) females. [Colour figure can be viewed at http://wileyonlinelibrary.com].