TY - JOUR
AU - Carvalho, Lori A F, N
AB - Abstract We introduce a method to quantify flight ability and physical fitness of individual fruit flies which we term ‘Flight Burst Duration’ (FBD). This consisted of tethering individual insects by the dorsal thorax using a vacuum and measuring the length of time the insect beats its wings while suspended off a surface. Consecutive measurements with Bactrocera dorsalis Hendel (Dipera: Tephritidae) and Zeugodacus cucurbitae Coquillett (Diptera: Tephritidae) in the same day and across days indicated that a single measurement was sufficient, and that FBD was consistent and repeatable. Insects under stress from starvation displayed shorter FBD over time, and we suggest that the measure also relates to the physical condition or survival fitness of the individual. Though somewhat laborious and time-consuming, we propose that FBD can be useful for research studies requiring individual-level phenome data and for obtaining estimates quality and dispersive movement for insects. An essential component of many contemporary insect pest management programs is the ability to mass-rear large numbers of high-quality insects. The definition of quality in this context can be challenging, but usually is related to the general concept of ‘field performance.’ Quality mass production clearly applies to a range of programs, from those built around the sterile insect technique (SIT) (Knipling 1955), to classic or augmentative biological control through the release of insect predators or parasitoids (van Lenteren 2003), to recent efforts using genetically modified insects (e.g., Carvalho et al. 2014). For an SIT program, ‘field performance’ is still usually interpreted in terms of daily survival rates and mating competitiveness vis-à-vis wild fertile males (Fried 1971, Calkins and Parker 2005, Yuval et al. 2007). The negative effects of mass rearing on field performance have long been acknowledged (Boller 1972, Mackauer 1976), but these are not always directly addressed by existing ‘quality control’ (QC) metrics in production (Chambers 1977). Most QC in mass rearing facilities is built around quantities aiming to ensure efficient production rather than field performance (Sørensen et al. 2012). One important way to improve QC of mass reared insects for pest management is to select and measure phenotypic traits that are relevant to field performance. These fundamental measures could be useful to a range of goals, from applied pest management to studies of evolutionary biology (Sørensen et al. 2012). Mass-rearing of Tephritid fruit flies is a relatively mature field, having benefitted from decades of research and, today, some standardization. Current QC standards tests target sustaining production (fertility, fecundity, eclosion rates, sex ratios) as well as measures thought to relate to field performance (flight ability, survival). Direct field measurement via occasional MRR studies is also recommended (FAO/IAEA/USDA 2019). Despite this, there remains a need for laboratory tests that can be related to field performance. New methods to estimate quality and field performance in the laboratory or mass rearing facility might be expected from increasing automation. In fruit flies, one example is the use of automated locomotor activity measurements (LAM) (Dominiak et al. 2014), where the spontaneous activity of individual insects can be assessed by a machine with a simple optical sensor. More detailed methods employ video for assessing behavioral and performance differences (e.g., Lux et al. 2002), with the most sophisticated incorporating stereoscopic vision and 3D tracking to record lifetime behavior of individual Anastrepha ludens (Loew) in cages, termed the ‘Behavioral Monitoring System’ (Zou et al. 2011, Chiu et al. 2013). Such approaches are clearly valuable, but it is clear that there is a trade-off between complexity and equipment/expertise requirements versus simplicity and throughput; most new methods tend to require specialized equipment and/or significant expertise. Here we investigate the utility of a phenotypic character we term ‘flight burst duration’ (‘FBD’) as an indicator of the general physiological condition and, by extension, the field performance of two representative species of Tephritid fruit flies: Bactrocera dorsalis (Hendel) (‘Oriental fruit fly’) and Zeugodacus (Bactrocera) cucurbitae (Coquilett) (‘Melon fly’). Measuring this character is simple, but ‘low throughput.’ The method presented is related to well-established flight mill experiments that have a long pedigree in entomology (e.g., Sharp 1978), but simplified in that the time of flight rather than distance is recorded. We specifically do not address the question of reasonable throughput or efficiency in a program context, rather focus on the phenotypic character itself to evaluate if it might be useful for the goal of measuring any aspect of ‘field performance.’ We assess the viability of FBD by addressing three questions: 1) Is a single measurement of FBD likely to be sufficient, or is there high inter-measurement variation? 2) Is FBD consistent for a given individual relative to a population over short time periods? 3) Is there an observable relationship between FBD and physical condition? Materials and Methods Insects and FBD Measurement Oriental fruit fly, Bactrocera dorsalis (Hendel) and Melon fly, Zeugodacus cucurbitae (Coquillett) were obtained from the USDA-ARS- Daniel K. Inouye Pacific Basin Agricultural Research Center rearing facility. Both species were in colony for >30 yr at the time of the experiments, and were reared following standard protocol (Vargas 1989). The colony was housed in a building devoted exclusively to rearing, and was maintained at 22.5 ± 1ºC, 55% ± 3% RH, and a 14:10 (L:D) h photoperiod. Experiments were conducted between December 2015 and February 2017, and flies were around 10 d post-eclosion at the time of the assays (sexually mature, with mating opportunities). With the exception of the starvation experiment they were fed ad libitum and had access to water via a damp wick. Experimental flies were chilled at 5°C and placed in individual holding chambers. Flies were held in two nested 57 ml portion cups: one with a 1.3 cm diameter inch hole cut from the bottom, nested inside a cup of the same size. The inner cup was closed with a screened lid. [Cups and lids: Ingeo CF7057 2 oz compostable cups and lids (CF Biotech, Taiwan)]. Flies were allowed to return to room temperature for assays (22°C ± 1°C; 55% ± 5% RH) for 30 min prior to testing. A 60 cm length of 2 cm OD × 1.2 cm ID clear Tygon medical tubing (Saint-Gobain S.A., Akron, OH) was attached to the vacuum nozzle on a laboratory bench at one end and a 1-200 µl pipet tip (VWR, Radnor PA) inserted at the other end. The vacuum was set to a low pressure, enough to hold a fly by the dorsal side of the thorax but not damage it in handling (approx. 400 ml/min). The pipet tip was inserted into the 1.3 cm diameter hole in the bottom of the portion cup after removing the outer intact portion cup, and the insect was held by suction while FBD was measured manually using a stopwatch (Fig. 1). A ‘Burst’ was considered to be a continuous rapid motion of the wings with no visible interruption lasting between 5 s to 30 min. Fig. 1. Open in new tabDownload slide Zeugodacus cucurbitae females attached to a pipette tip via vacuum for FBD assay. Note the flush attachment of the tip to the thorax as the insect moves and beats its wings. If suspending the individual was not enough to start wing beating a small puff of air can be helpful. Photograph by S. Sim (USDA-ARS). Fig. 1. Open in new tabDownload slide Zeugodacus cucurbitae females attached to a pipette tip via vacuum for FBD assay. Note the flush attachment of the tip to the thorax as the insect moves and beats its wings. If suspending the individual was not enough to start wing beating a small puff of air can be helpful. Photograph by S. Sim (USDA-ARS). Consecutive Burst Assay Bactrocera dorsalis (n = 51 ♂ 45 ♀) and Z. cucurbitae (n = 48 ♂ 48 ♀) individuals from the same cohort were assayed for FBD five consecutive times in a single sitting to assess if a single measurement was sufficient to capture FBD or if significant variation was observed between measurements during the same observation. Consecutive assays were conducted with a < 5 s pause between them. Differences were assessed via linear regression of the first FBD against the average of the four following FBDs with log (x+1) transformation of both predictor and response variables so data conformed to test assumptions of normality. Longitudinal and Nutritional Deprivation Test B. dorsalis (n = 49 ♂, n = 46 ♀) and Z. cucurbitae (n = 44 ♂, n = 55 ♀) from the same cohort were held individually as above but with a vial cap (Wheaton), size 8–425, used to provide food/moisture or moisture alone. The vial caps had a 20 mm plastic circular disc glued to the bottom and was placed in the inner portion cup opening in the base to provide the treatment. Caps were filled with either a nutritional agar diet described below for control subjects (fed; 12 ♂ 23 ♀) or a 1% agar gel for hydration for experimental subjects (unfed; 32 ♂ 32♀). The nutritional agar was prepared by mixing 60 g protein hydrolysate, 20 g sugar, 15 g honey, 2g agar, and 200 ml water in a 500 ml beaker. The mixture was heated to a rapid boil and continued for an additional 5 min. After lowering the heat, the liquid was dispensed into diet caps using a plastic syringe. This was sufficient to fill 200 caps. Flies were chilled as before and introduced to individually numbered cups. FBD testing proceeded as discussed earlier. Flies were offered water daily via spray bottle post-test in addition to the cap diet. Individuals were tested for three consecutive days, and only complete observations (individuals that survived the entirety of the experiment) were used in the analysis. Diet was changed or rehydrated as needed during the 3-d trial. Comparisons between days within treatments were conducted via Wilcoxon paired signed-rank tests. Comparisons between treatments within days were conducted by the unpaired version of the same test. Results The results of five consecutive measurements of FBD for 192 individual Z. cucurbitae and B. dorsalis are shown in Fig. 2. Z. cucurbitae had longer FBD compared with B. dorsalis in every within-sex comparison (n = 10, probability if no true difference = 0.00098). For the latter species, males had a slightly higher average FBD for all five measurements. For both species, FBD decreased with as consecutive test number increased. For B. dorsalis and Z. cucurbitae, the first FBD measured was significantly correlated with the average of the following four FBD values (Table 1). Table 1. Linear regression between first FBD and the average of subsequent four FBD for Zeugodacus cucurbitae and Bactrocera dorsalis . Z. cucurbitae: R2 = 0.25; F = 30.93 on 1 and 94 df . . . . . Estimate . SE . t . P . Intercept 1.716 0.577 2.974 0.004* ln (1+average) 0.667 0.120 5.562 <0.001* B. dorsalis: R2 = 0.24; F = 29.45 on 1 and 94 df Intercept 2.001 0.323 6.202 <0.001* ln (1+average) 0.562 0.104 5.427 <0.001* . Z. cucurbitae: R2 = 0.25; F = 30.93 on 1 and 94 df . . . . . Estimate . SE . t . P . Intercept 1.716 0.577 2.974 0.004* ln (1+average) 0.667 0.120 5.562 <0.001* B. dorsalis: R2 = 0.24; F = 29.45 on 1 and 94 df Intercept 2.001 0.323 6.202 <0.001* ln (1+average) 0.562 0.104 5.427 <0.001* Both variables transformed using ln (x+1) to meet assumptions of normality. *indicates statistical significance at α = 0.05. Open in new tab Table 1. Linear regression between first FBD and the average of subsequent four FBD for Zeugodacus cucurbitae and Bactrocera dorsalis . Z. cucurbitae: R2 = 0.25; F = 30.93 on 1 and 94 df . . . . . Estimate . SE . t . P . Intercept 1.716 0.577 2.974 0.004* ln (1+average) 0.667 0.120 5.562 <0.001* B. dorsalis: R2 = 0.24; F = 29.45 on 1 and 94 df Intercept 2.001 0.323 6.202 <0.001* ln (1+average) 0.562 0.104 5.427 <0.001* . Z. cucurbitae: R2 = 0.25; F = 30.93 on 1 and 94 df . . . . . Estimate . SE . t . P . Intercept 1.716 0.577 2.974 0.004* ln (1+average) 0.667 0.120 5.562 <0.001* B. dorsalis: R2 = 0.24; F = 29.45 on 1 and 94 df Intercept 2.001 0.323 6.202 <0.001* ln (1+average) 0.562 0.104 5.427 <0.001* Both variables transformed using ln (x+1) to meet assumptions of normality. *indicates statistical significance at α = 0.05. Open in new tab Fig. 2. Open in new tabDownload slide Boxplots of consecutive FBD measurements in seconds (ln [x+1]) for each sex of Z. cucurbitae (black) and B. dorsalis (blue). For each box, the central mark is the median, the top and bottom edges are the 75th and 25th percentiles (respectively), and whiskers are 1.5 times the interquartile range (±2.7σ for normally distributed data); points outside this range are plotted using circles. Fig. 2. Open in new tabDownload slide Boxplots of consecutive FBD measurements in seconds (ln [x+1]) for each sex of Z. cucurbitae (black) and B. dorsalis (blue). For each box, the central mark is the median, the top and bottom edges are the 75th and 25th percentiles (respectively), and whiskers are 1.5 times the interquartile range (±2.7σ for normally distributed data); points outside this range are plotted using circles. For the longitudinal test, few B. dorsalis survived the starvation treatment; therefore, we focused on Z. cucurbitae. Even for the latter species, survivorship through 48 h of the experiment was much lower for unfed (24 out of 64, 37.5% survival) than for fed (24 out of 35, 68.6% survival). Table 2 shows the changes in the median and range of FBD for the two groups of Z. cucurbitae over the course of the experiment. Within treatments, Wilcoxon paired signed-rank tests showed no significant difference in the FBD of Z. cucurbitae in the fed (control) group among any of the days (day 0–day 1: V = 133, P = 0.562; day 1–day 2: V = 64, P = 0.076; day 0–day 2: V = 77, P = 0.191). However, for the unfed group, there was a statistically significant decrease in FBD between days 0 and 1 and between days 0 and 2 (day 0–day 1: V = 227, P = 0.027; day 1–day 2: V = 162, P = 0.747; day 0–day 2: V = 246, P < 0.005). Between treatments, the only comparison that showed statistical significance at α = 0.05 indicated that fed FBD was higher than unfed on day 2 (Wilcoxon unpaired signed-rank test [one tailed] V = 382, P = 0.027). Table 2. Median FBD (in seconds) over 3 d for Z. cucurbitae that were fed or subject to starvation (unfed) Treatment . N . Day 0 . Day 1 . Day 2 . Fed 21 222 (70–308) 126 (68–285) 312 (68–568) Unfed 24 283 (73–529) 110 (42–247) 77 (27–262) Treatment . N . Day 0 . Day 1 . Day 2 . Fed 21 222 (70–308) 126 (68–285) 312 (68–568) Unfed 24 283 (73–529) 110 (42–247) 77 (27–262) Values in brackets indicate the inter-quartile range. Open in new tab Table 2. Median FBD (in seconds) over 3 d for Z. cucurbitae that were fed or subject to starvation (unfed) Treatment . N . Day 0 . Day 1 . Day 2 . Fed 21 222 (70–308) 126 (68–285) 312 (68–568) Unfed 24 283 (73–529) 110 (42–247) 77 (27–262) Treatment . N . Day 0 . Day 1 . Day 2 . Fed 21 222 (70–308) 126 (68–285) 312 (68–568) Unfed 24 283 (73–529) 110 (42–247) 77 (27–262) Values in brackets indicate the inter-quartile range. Open in new tab Discussion Based on the results above, we suggest that FBD is a relatively consistent and repeatable measure of an important phenotypic trait that captures information on the overall physical condition of the specimen. We suggest that a single measurement is sufficient to capture relative flight performance and general survival fitness differences between fruit flies since consecutive measurements were strongly correlated within individuals, and generally consistent across days when considering individuals within populations. An important advantage of this method is that the results can be related to real world performance and movement, which is impossible with traditional ‘flight-tube’ QC assays conduced in mass-rearing facilities (FAO/IAEA/USDA 2019) or can require sophisticated equipment or expertise with newer methods (Lux et al. 2002, Zou et al. 2011, Dominiak et al. 2014). Traditionally, flight mills have often been used for measurements of insect movement (Naranjo 2019). These produce detailed and valuable insights into individual dispersion in multiple taxa including Tephritids (Sharp et al. 1975, Chapman 1982, Makumbe et al. 2020), but generally rely on specialized equipment (Attisano et al. 2015). FBD measurements obtained via simple vacuum-based tethering and a stopwatch are a coarse version of these, somewhere in between full flight mills and flight tubes. We suggest that an application could be as follows: If the average flight speed of a fly is 0.45 m/s, an individual with an FBD of 7.5 min can be expected to have a maximum linear displacement of around 200 m per flight event, assuming ballistic movement (i.e., in a straight line) (Miller et al. 2015). This is a rough estimate of the maximum flight distance, as multiple factors (appetitive and not), will affect actual flight in nature. On its own, this estimate of linear displacement can be used to obtain the diffusion parameter D, a simple and commonly used measure of displacement in animals (Skellam 1951, Kareiva and Shigesada 1983). If combined with a point-estimate or range in the sinuosity of the flight for the species, the more sophisticated and realistic random correlated walk model can be used (Byers 2001). Applications include ascertaining areas for trapping, establishing pest-free zones, and other aspects of control programs (Barclay et al. 2005, Froerer et al. 2010, Dominiak et al. 2015). Our experiment and the method have important limitations. First, we only studied two representative Tephritid species, and it is possible that others will be less consistent across measurements, though we consider this unlikely. Second, we did not assess the relationship between FBD and actual survival fitness, rather we used starvation as a proxy for poor physical condition. Other measures of fitness, including reproductive fitness, would provide further insight into the usefulness of the FDB measurement. Third, the method was laborious and time consuming, and so to generate large datasets representative of a population would be challenging and likely more costly than current methods. Finally, the sensitivity of FBD remains to be determined with respect to more subtle fitness determinants than starvation. Despite these issues, we see additional applications of the method beyond estimation of dispersal ability mentioned earlier, particularly for research and laboratory studies that require individual-based data. These might include experiments to assess genes underlying flight ability (e.g., Montooth et al. 2003) or other fitness traits that might benefit from detailed phenotypic and performance data per individual. Future research should focus on relating FDB to ‘standard’ measures such as flight tube assays. Also, we are interested in accelerating and automating the process of FBD data collection, perhaps through the use of robotic systems, increasingly common in insect rearing (Crawford et al. 2020), though admittedly this would abrogate the simplicity of the current method. Acknowledgments Many technicians worked on this method and used it to collect data over the years, including Shannon Wilson, Kirsten Snook, Caley Saragosa, and Connor Rhyno; we thank them for their efforts. Thanks to Bernard C. Dominiak of the Department of Plant Industry, NSW Australia for reviewing an early draft of the manuscript. This research was funded by USDA-ARS. Opinions, findings, conclusions, and recommendations expressed in this publication are those of the authors and do not necessarily reflect the views of the USDA. The USDA is an equal opportunity provider and employer. References Cited Attisano , A , J T Murphy, A Vickers, and P J Moore. 2015 . A simple flight mill for the study of tethered flight in insects . J Vis Exp . 106: e53377 . OpenURL Placeholder Text WorldCat Barclay , H J , J W Hargrove, A Clift, and A Meats. 2005 . Procedures for declaring pest free status, pp. 363 – 386 . In V A Dyck, J Hendrichs, A S Robinson (eds.), Sterile insect technique: principles and practice in area-wide integrated pest management . Springer , Dordrecht, The Netherlands . Google Scholar Crossref Search ADS Google Scholar Google Preview WorldCat COPAC Boller , E . 1972 . Behavioral aspects of mass-rearing of insects . Entomophaga . 17 : 9 – 25 . Google Scholar Crossref Search ADS WorldCat Byers , J A . 2001 . Correlated random walk equations of animal dispersal resolved by simulation . Ecology 82 : 1680 – 1690 . Google Scholar Crossref Search ADS WorldCat Calkins , C O , and A G Parker. 2005 . Sterile insect quality, pp. 269 – 296 . In A S Robinson, J Hendrichs, V A Dyck (eds.), Sterile insect technique: principles and practice in area-wide integrated pest management . Springer , Dordrecht, The Netherlands . Google Scholar Crossref Search ADS Google Scholar Google Preview WorldCat COPAC Carvalho , D O , D Nimmo, N Naish, A R McKemey, P Gray, A B B Wilke, M T Marrelli, J F Virginio, L Alphey, and M L Capurro. 2014 . Mass production of genetically modified Aedes aegypti for field releases in Brazil . J Vis Exp . 83: e3579 . OpenURL Placeholder Text WorldCat Chambers , D L . 1977 . Quality control in mass rearing . Annu. Rev. Entomol . 22 : 289 – 308 . Google Scholar Crossref Search ADS WorldCat Chapman , M G . 1982 . Experimental analysis of the pattern of tethered flight in the Queensland fruit fly, Dacus tryoni . Physiol. Entomol . 7 : 143 – 150 . Google Scholar Crossref Search ADS WorldCat Chiu , J C , K Kaub, S Zou, P Liedo, L Altamirano-Robles, D Ingram, and J R Carey. 2013 . Deleterious effect of suboptimal diet on rest-activity cycle in Anastrepha ludens manifests itself with age . Sci. Rep . 3 : 1773 . Google Scholar Crossref Search ADS PubMed WorldCat Crawford , J E , D W Clarke, V Criswell, M Desnoyer, D Cornel, B Deegan, K Gong, K C Hopkins, P Howell, J S Hyde, et al. 2020 . Efficient production of male Wolbachia-infected Aedes aegypti mosquitoes enables large-scale suppression of wild populations . Nat. Biotechnol . 38 : 482 – 492 . Google Scholar Crossref Search ADS PubMed WorldCat Dominiak , B C , B G Fanson, S R Collins, and P W Taylor. 2014 . Automated locomotor activity monitoring as a quality control assay for mass-reared tephritid flies . Pest Manag. Sci . 70 : 304 – 309 . Google Scholar Crossref Search ADS PubMed WorldCat Dominiak , B C , B Wiseman, C Anderson, B Walsh, M McMahon, and R Duthie. 2015 . Definition of and management strategies for areas of low pest prevalence for Queensland fruit fly Bactrocera tryoni Froggatt . Crop Prot . 72 : 41 – 46 . Google Scholar Crossref Search ADS WorldCat FAO/IAEA/USDA . 2019 . Product quality control for sterile mass-reared and released Tephritid fruit flies, version 7.0 . International Atomic Energy Agency , Vienna, Austria . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Fried , M . 1971 . Determination of sterile-insect competitiveness . J. Econ. Entomol . 64 : 869 – 872 . Google Scholar Crossref Search ADS WorldCat Froerer , K M , S L Peck, G T McQuate, R I Vargas, E B Jang, and D O McInnis. 2010 . Long-distance movement of Bactrocera dorsalis (Diptera: Tephritidae) in Puna, Hawaii: how far can they go? Am. Entomol . 56 : 88 – 95 . Google Scholar Crossref Search ADS WorldCat Kareiva , P M , and N Shigesada. 1983 . Analyzing insect movement as a correlated random walk . Oecologia . 56 : 234 – 238 . Google Scholar Crossref Search ADS PubMed WorldCat Knipling , E F . 1955 . Possibilities of insect control or eradication through the use of sexually sterile males . J. Econ. Entomol . 48 : 459 – 462 . Google Scholar Crossref Search ADS WorldCat van Lenteren , J C . 2003 . Quality control and production of biological control agents: theory and testing procedures . CABI , Oxford, United Kingdom . Google Scholar Crossref Search ADS Google Scholar Google Preview WorldCat COPAC Lux , S A , J C Vilardi, P Liedo, K Gaggl, G E Calcagno, F N Munyiri, M T Vera, and F Manso. 2002 . Effects of irradiation on the courtship behavior of Medfly (Diptera, Tephritidae) mass reared for the sterile insect technique . Fla. Entomol . 85 : 102 – 112 . Google Scholar Crossref Search ADS WorldCat Mackauer , M . 1976 . Genetic problems in the production of biological control agents . Annu. Rev. Entomol . 21 : 369 – 385 . Google Scholar Crossref Search ADS WorldCat Makumbe , L D , T P Moropa, A Manrakhan, and C W Weldon. 2020 . Effect of sex, age and morphological traits on tethered flight of Bactrocera dorsalis (Hendel) (Diptera: Tephritidae) at different temperatures . Physiol. Entomol . 45 : 110 – 119 . Google Scholar Crossref Search ADS WorldCat Miller , J R , C G Adams, P A Weston, and J H Schenker. 2015 . Trapping of small organisms moving randomly: principles and applications to pest monitoring and management . Springer , Heidelburg, Germany . Google Scholar Crossref Search ADS Google Scholar Google Preview WorldCat COPAC Montooth , K L , J H Marden, and A G Clark. 2003 . Mapping determinants of variation in energy metabolism, respiration and flight in Drosophila . Genetics . 165 : 623 – 635 . Google Scholar PubMed OpenURL Placeholder Text WorldCat Naranjo , S E . 2019 . Assessing insect flight behavior in the laboratory: a primer on flight mill methodology and what can be learned . Ann. Entomol. Soc. Am . 112 : 182 – 199 . Google Scholar Crossref Search ADS WorldCat Sharp , J L . 1978 . Tethered flight of apple maggot flies . Fla. Entomol . 61: 199 – 200 . OpenURL Placeholder Text WorldCat Sharp , J L , D L Chambers, and F H Haramoto. 1975 . Flight mill and stroboscopic studies of Oriental fruit flies and melon flies, including observations of Mediterranean fruit flies . Proc. Hawaii. Entomol. Soc . 22 : 137 – 144 . OpenURL Placeholder Text WorldCat Skellam , J G . 1951 . Random dispersal in theoretical populations . Biometrika . 38 : 196 – 218 . Google Scholar Crossref Search ADS PubMed WorldCat Sørensen , J G , M F Addison, and J S Terblanche. 2012 . Mass-rearing of insects for pest management: challenges, synergies and advances from evolutionary physiology . Crop Prot . 38 : 87 – 94 . Google Scholar Crossref Search ADS WorldCat Vargas , R I . 1989 . Mass production of Tephritid fruit flies, pp. 141 – 151 . In World crop pests. Fruit flies: their biology, natural enemies and control . Elsevier , New York . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Yuval , B , M Maor, K Levy, R Kaspi, P Taylor, and T Shelly. 2007 . Breakfast of champions or kiss of death? Survival and sexual performance of protein-fed, sterile Mediterranean fruit flies (Diptera: Tephritidae) . Fla. Entomol . 90 : 115 – 122 . Google Scholar Crossref Search ADS WorldCat Zou , S , P Liedo, L Altamirano-Robles, J Cruz-Enriquez, A Morice, D K Ingram, K Kaub, N Papadopoulos, and J R Carey. 2011 . Recording lifetime behavior and movement in an invertebrate model . PLoS One 6 : e18151 . Google Scholar Crossref Search ADS PubMed WorldCat Published by Oxford University Press on behalf of Entomological Society of America 2020. This Open Access article contains public sector information licensed under the Open Government Licence v2.0 
(http://www.nationalarchives.gov.uk/doc/open-government-licence/version/2/).
TI - Flight Burst Duration as an Indicator of Flight Ability and Physical Fitness in Two Species of Tephritid Fruit Flies
JO - Journal of Insect Science
DO - 10.1093/jisesa/ieaa095
DA - 2020-09-01
UR - https://www.deepdyve.com/lp/oxford-university-press/flight-burst-duration-as-an-indicator-of-flight-ability-and-physical-jgGy8qO9FQ
VL - 20
IS - 5
DP - DeepDyve
ER -