Harmonic radar tracking of individual melon flies, Zeugodacus cucurbitae, in Hawaii: Determining movement parameters in cage and field settings

Abstract

Tephritid fruit flies, such as the melon fly, Zeugodacus cucurbitae, are major horticultural pests worldwide and pose invasion risks due primarily to international trade. Determining movement parameters for fruit flies is critical to effective surveillance and control strategies, from setting quarantine boundaries after incursions to development of agent-based models for management. While mark-release-recapture, flight mills, and visual observations have been used to study tephritid movement, none of these techniques give a full picture of fruit fly movement in nature. Tracking tagged flies offers an alternative method which has the potential to observe individual fly movements in the field, mirroring studies conducted by ecologists on larger animals. In this study, harmonic radar (HR) tags were fabricated using superelastic nitinol wire which is light (tags weighed less than 1 mg), flexible, and does not tangle. Flight tests with wild melon flies showed no obvious adverse effects of HR tag attachment. Subsequent experiments successfully tracked HR tagged flies in large field cages, a papaya field, and open parkland. Unexpectedly, a majority of tagged flies showed strong flight directional biases with these biases varying between flies, similar to what has been observed in the migratory butterfly Pieris brassicae. In field cage experiments, 30 of the 36 flies observed (83%) showed directionally biased flights while similar biases were observed in roughly half the flies tracked in a papaya field. Turning angles from both cage and field experiments were non-random and indicate a strong bias toward continued "forward" movement. At least some of the observed direction bias can be explained by wind direction with a correlation observed between collective melon fly flight directions in field cage, papaya field, and open field experiments. However, individual mean flight directions coincided with the observed wind direction for only 9 out of the 25 flies in the cage experiment and half of the flies in the papaya field, suggesting wind is unlikely to be the only factor affecting flight direction. Individual flight distances (meters per flight) differed between the field cage, papaya field, and open field experiments with longer mean step-distances observed in the open field. Data on flight directionality and step-distances determined in this study might assist in the development of more effective control and better parametrize models of pest tephritid fruit fly movement.

Fig 1. A wild male melon fly, Zeugodacus cucurbitae, with a harmonic radar tag attached.

The tag shown weighed approximately 0.8 mg and was fabricated from a diode and superelastic nitinol wire.

Fig 2. Flight directions and lengths of HR tagged Zeugodacus cucurbitae for experiment 2 (field cage).

Each replicate consisted of a series of 10 flights with a single tagged fly. Blue arrows represent individual flights, while red arrows show the mean flight direction and length.

Fig 3

Combined pseudo-turning angles of HR tagged Zeugodacus cucurbitae for experiment 2 (A) and experiment 3 (B). A turning angle of zero indicated that a fly flew in the same direction as the directly previous flight. Combined turning angles were non-random by both Rayleigh and Hermans-Rasson tests, showed no right-left bias, but indicate a pronounced bias towards moving within 90° left or right of the directly previous flight.

Fig 4. Melon fly, Zeugodacus cucurbitae, flight step-distances for experiment 2–5.

Different letters, in parentheses, indicate significant differences by ANOVA followed by means separations with Student-Newman-Keuls (P = 0.05).

Fig 5. Flight directions and lengths of HR tagged Zeugodacus cucurbitae for experiment 3 (field cage).

Each replicate consisted of a series of 10 flights with a single tagged fly. Blue arrows represent individual flights, while red arrows show the mean flight direction and length.

Fig 6. HR tagged Zeugodacus cucurbitae flight directions and lengths for experiment 4 (papaya field).

Colored arrows represent a series of 5–10 flights for a single tagged fly. The large black arrow shows the mean wind direction for the duration of tracking. When all flights were taken together, flight directions were not homogeneous but showed directionality (P < 0.001, Rayleigh test; P < 0.001, Hermans-Rasson test) and a unimodal distribution correlated with the mean wind direction (P < 0.001, V-test).

Fig 7. Flight directions and lengths of HR tagged Zeugodacus cucurbitae for experiment 4 (papaya field).

Each replicate consisted of a series of 5–10 flights with a single tagged fly. Blue arrows represent individual flights, while red arrows show the mean flight direction and length.

Fig 8. Combined turning angles of HR tagged Zeugodacus cucurbitae for experiment 4 (papaya).

A turning angle of zero indicated that a fly flew in the same direction as the directly previous flight. Combined turning angles were non-random ($\overline{\mathrm{R}}$ = 0.419, P < 0.001, Rayleigh test, P = 0.001, Hermans-Rasson test), showed no right-left bias (P = 0.735, chi-squared test), but showed a pronounced “forward” movement bias (P < 0.001, chi-squared test).

Fig 9. Tagged melon fly, Zeugodacus cucurbitae, release points (black center with yellow or white border) and landing points (yellow or white dots) at Lokahi Park, Hilo, HI.

Yellow and white arrows indicate the mean wind direction during fly releases. Source: U.S. Geological Survey, 2011, USGS High Resolution State Orthoimagery for the East Side of Hawaii Island: 05QKB820780_200912_0x5000m_CL_1: U.S. Geological Survey.