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Flight altitude selection increases orientation performance in high-flying nocturnal insect migrants
Animal Behaviour 82 (2011) 1221e1225
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Articles
Flight altitude selection increases orientation performance in high-flying nocturnal insect migrants Prabhuraj Aralimarad a, b, Andy M. Reynolds a, Ka S. Lim a, Don R. Reynolds a, c, Jason W. Chapman a, * a
Rothamsted Research College of Agriculture, University of Agricultural Sciences, Raichur, India c Natural Resources Institute, University of Greenwich, U.K. b
a r t i c l e i n f o Article history: Received 12 July 2011 Initial acceptance 11 August 2011 Final acceptance 6 September 2011 Available online 5 October 2011 MS. number: 11-00548 Keywords: entomological radar flight altitude insect layer migration orientation cue turbulence
Many insects migrate at high altitudes where they utilize fast-flowing airstreams for long-distance transport. Nocturnal insect migrants typically exhibit a strongly unimodal distribution of flight headings (a phenomenon termed ‘common orientation’), and the mean heading is often aligned downwind. In addition, these nocturnal migrants are sometimes concentrated into shallow altitudinal zones (termed ‘layers’). The mechanism by which widely separated insects select and maintain common flight headings had until recently eluded explanation, but recent theoretical advances have shown that atmospheric turbulence might enable insects to perceive the downwind direction and orient accordingly. This theory predicts that common orientation downwind should be: (1) widespread in nocturnal insect migrants; (2) facilitated when insects are concentrated into layers; and (3) more pronounced in larger insects. We tested these ideas using radar observations of 647 independent nocturnal migration events, and found strong support for all three predictions: (1) common orientation occurred in 75e90% of events; (2) common orientation was more frequent, had significantly less scatter and was significantly closer to downwind when insects migrated in layers; and (3) large insects exhibited significantly tighter orientation than ‘medium-sized’ insects. Our results provide robust evidence that wind-related common orientation is mediated by detection of atmospheric turbulence. Ó 2011 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Although some insects such as butterflies migrate by flying near the ground within their ‘flight boundary layer’ (where the wind is light enough for the insect to make progress in any direction; Srygley & Dudley 2008), in the vast majority of species migration over any significant distance takes place at higher altitudes to utilize assistance from the wind (Gatehouse 1997; Chapman et al. 2011). In fact, as long as it is warm enough for flight, the lowest 2e3 km of the troposphere hosts an incessant ‘bioflow’ of insects involving myriad taxa (e.g. Chapman et al. 2004) and vast numbers of individuals (e.g. Riley et al. 1991). The flights are part of a ‘migration syndrome’: a group of adaptive traits that facilitate redistribution of populations, and this in turn enables migratory species to exploit spatiotemporal patterns of availability in various resources (Drake & Gatehouse 1995; Dingle 1996; Dingle & Drake 2007). Wind-assisted movements are particularly required where species migrate between climatic zones in order to take advantage of seasonal changes of temperature and rainfall (Drake & Gatehouse 1995; Drake et al. 2001; Chapman & Drake 2010).
* Correspondence: J. W. Chapman, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, U.K. E-mail address: [email protected] (J. W. Chapman).
The very low self-propelled speeds through the surrounding air (airspeeds) of small insects mean that these species make little contribution to their horizontal displacement speed during migratory flight (although they do control the initiation and, to a certain extent, the termination of migration). The same is not true of larger insects, and the recent evidence of sophisticated migration behaviour (e.g. control of timing and height of flight, and windrelated heading directions) has led to a paradigm shift in our understanding of wind-assisted migration strategies in these insect species (Chapman et al. 2008a, b, 2010). Among the responses of high-altitude migrants to their atmospheric environment, largely documented by radar (Chapman et al. 2011), are two frequently observed phenomena. These are the formation of ‘layer concentrations’ where insects concentrate at certain altitudes in stable night-time atmospheres (Wolf et al. 1986; Drake & Farrow 1988; Gatehouse 1997; Reynolds et al. 2005, 2009; Chapman et al. 2011; see Fig. 1a), and the adoption of common heading directions (‘common orientation’; Riley 1975; Drake 1983; Riley & Reynolds 1986; Reynolds et al. 2010a; Chapman et al. 2011). Both the layering and the persistent orientation pattern are broadscale phenomena which may extend over thousands of square kilometres on some occasions (e.g. Hobbs & Wolf 1996, who flew long transects over Texas with a nadir-pointing airborne radar,
0003-3472/$38.00 Ó 2011 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.anbehav.2011.09.013
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1400
(a)
1200 1000 800 600 400
Altitude (m)
200 0
0
1400
10
20
10
20
30
40
50
60
70
30 40 50 Number of insects
60
70
(b)
1200 1000 800 600 400 200 0
0
Figure 1. (a) A ‘layered profile’: the vertical distribution of insect numbers between 2200 and 2206 hours on 13 July 2006 detected by the Rothamsted vertical-looking radar. A pronounced layer of insects, centred about 600 m above ground, appeared to be associated with a temperature inversion and strong wind stream at that altitude. (b) A ‘nonlayered profile’: the vertical distribution of insect numbers between 2215 and 2236 hours on 15 July 2006 at Rothamsted. Although some structure is evident in the profile, it does not show the strong layering with most targets concentrated around one flight height, as in (a).
found that the mean orientation direction was almost constant along the whole extent of the layer). Previous studies have speculated that common orientation and layering may be mechanistically linked (Drake 1983; Hobbs & Wolf 1989; Reynolds et al. 2009, 2010a, b; Chapman et al. 2011), but this idea has yet to be confirmed. Obtaining reliable visual cues for the purposes of taking up an adaptive flight orientation is particularly challenging at night, when light levels can be up to 11 orders of magnitude lower than they are during the day (Baird et al. 2011; Warrant & Dacke 2011). Thus it had been assumed that because of the difficulty of deriving visual information, those insects migrating hundreds of metres above the ground at night would exhibit random patterns of flight headings (reviewed in Reynolds et al. 2010a). However, it was clear from the earliest entomological radar observations (Riley 1975; Drake 1983) that, in the larger nocturnal migrants at least, the heading distributions can be remarkably clustered, and that the mean heading is often relatively close to the downwind direction (Reynolds et al. 2010a; Chapman et al. 2011). Downwind orientation is generally adaptive in these migrating insects because it adds their airspeed (ca. 1e5 m/s depending on their size) to the wind speed, resulting in significant increases to their migration distances (Chapman et al. 2008a, b, 2010; Alerstam et al. 2011). Furthermore, flying in layer concentrations at the altitude of the warmest and fastest-moving
airstreams (Wood et al. 2006; Reynolds et al. 2010a; Chapman et al. 2011) will also lead to significant increases in migration distances. But while the benefits are clear, the mechanisms that individual migrants use to select and maintain similar flight altitudes and wind-related headings, while migrating under very low illumination levels and up to 1.5 km above the ground, have remained mysterious (Reynolds et al. 2009, 2010a). Recent theoretical advances have, however, identified features of the wind (anisotropic turbulent velocity and acceleration fluctuations) that may provide plausible cues for detection of the downwind direction and preliminary observations indicate that insect orientation patterns are consistent with some of the predictions that arise from this theory (Reynolds et al. 2010a, b). Further investigation of these hypotheses by laboratory-scale experiments appear to be extremely difficult because they necessitate measuring turbulent airflows in the immediate vicinity of mobile free-flying migrants. State-of-the-art experiments can monitor and record the trajectories of inert particles as they are carried along by turbulent airflows but they cannot measure the turbulent flows directly experienced by the particles nor can they measure particle-turbulent interactions (Ayyalasomayajula et al. 2006). Turbulent flows, of course, can be measured at some distance from a particle, at fixed locations using anemometers, but at any instant these flows will be different from the turbulence experienced by the particle (Reynolds & Lo Iacono 2004). Another significant problem is that the spatiotemporal scales of turbulence produced in laboratory-scale experiments will not match those of atmospheric turbulence. In view of these difficulties, detailed analysis of insect density/height profiles under natural conditions appears to be the best way forward. Consequently, we examined some predictions of the turbulence theory that are testable using flight heading and altitude data from a large number of independent nocturnal migration events recorded by entomological radars situated in inland southern England. The predictions are that common orientation should be: (1) a common feature of populations of night-flying insect migrants (this appeared to be true in general terms, but needed quantifying); (2) more frequent and stronger when migrants are concentrated in narrow atmospheric layers rather than widely dispersed over a range of flight altitudes; and (3) more pronounced in larger insects than smaller ones. Additionally, we looked for confirmation that the mean heading of nocturnal migrants exhibiting common orientation should on average be offset to the right of the downwind direction, owing to the effect of the Ekman spiral, as previously reported (Reynolds et al. 2010a). METHODS We selected 647 nocturnal migration ‘events’ recorded by our two vertical-looking entomological radars (VLRs; Chapman et al. 2003, 2011) during the period May to September in recent intense migration years (namely 2000, 2003 and 2006; see Chapman et al. 2010). The VLR locations, equipment and operating procedures have been described in detail elsewhere (Chapman et al. 2003, 2011; Reynolds et al. 2005). Each of these migration events involved the detection of either >20 individual ‘mediumsized’ insects (body mass 10e69 mg, N ¼ 252 events involving 28 604 insects) or >20 individual ‘large’ insects (70e500 mg, N ¼ 395 events involving 56 631 insects), flying in the altitude range 300e800 m above one of the radar sites between 2130 and midnight GMT (and thus after the end of civil twilight). The vertical profile of insect aerial density was examined during each migration event, so that each could be categorized as either a ‘layered profile’ (N ¼ 149 events involving 34 970 insects) or a ‘nonlayered profile’ (N ¼ 498 events involving 50 265 insects). First, periods during an
P. Aralimarad et al. / Animal Behaviour 82 (2011) 1221e1225
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Table 1 Orientation and ground speed characteristics of the four categories of migratory events
Nonlayered Layered
Medium Large Medium Large
Overall
N (events)
Common orientation (%)
Heading r value
Heading offset ( )
Ground speed (m/s)
186 312 66 83 647
74.2 79.5 92.4 91.6 80.8
0.3880.013 0.4250.010 0.4370.022 0.4760.019 0.4220.007
39.31.8 38.41.4 31.92.9 28.32.1 36.40.9
13.70.3 13.90.2 13.10.5 14.00.4 13.80.2
Values are means 1 SE.
RESULTS Common orientation of nocturnal flight headings was always frequent (Table 1), but occurred with greater frequency when migrants were in well-defined layers (>90% of events) than when nonlayered (ca. 75% of events). Well-defined nocturnal layering itself, however, only occurred on ca. 25% of occasions. Migrants concentrated within altitudinal layers showed significantly tighter distributions of individual flight headings than those insects migrating under nonlayered conditions (two-way ANOVA of heading r values: F1,643 ¼ 8.69, P ¼ 0.003; Fig. 2, Table 1). In addition, those in layers also had significantly smaller heading offsets from the downwind direction (two-way ANOVA: F1,519 ¼ 18.02, P < 0.001; Fig. 3, Table 1). Large insects showed significantly tighter orientation distributions than medium-sized insects (two-way ANOVA of heading r values: F1,643 ¼ 6.59, P ¼ 0.010; Fig. 2, Table 1), but there was no
effect of body size on the magnitude of the offset (two-way ANOVA: F1,519 ¼ 0.74, P ¼ 0.389; Fig. 3, Table 1). Mean displacement speeds did not differ between layered and nonlayered events or between medium and large insects (two-way ANOVA: profile: F1,642 ¼ 0.23, P ¼ 0.635; size: F1,642 ¼ 0.85, P ¼ 0.357; Table 1); the overall mean travel speed of 13.8 m/s corresponds to 50 km/h, and thus migrants were typically travelling at rather rapid ground speeds. There were no significant interactions between vertical profile and body size for any of the comparisons carried out (two-way ANOVA: heading r value: F1,643 ¼ 0.01, P ¼ 0.929; offset: F1,519 ¼ 0.42, P ¼ 0.516; speed: F1,642 ¼ 0.86, P ¼ 0.353). For the direction of the heading offsets relative to the downwind direction, offsets of both medium-sized and large insects were much more likely to occur to the right of the wind than the left, and differed significantly from zero under both nonlayered conditions (medium-sized insects: mean offset 21.0 7.2 (95% confidence interval, CI) to right of zero, N ¼ 138 events, 69% with a right bias, P < 0.0001; large insects: mean offset 23.4 4.9 (95% CI) to right of zero, N ¼ 248 events, 72% with a right bias, P < 0.0001) and layered conditions (medium-sized insects: mean offset 14.0 9.3 (95% CI) to right of zero, N ¼ 61 events, 69% with a right bias, P ¼ 0.003; large insects: mean offset 15.1 6.8 (95% CI) to right of zero, N ¼ 76 events, 75% with a right bias, P < 0.0001).
DISCUSSION Previous studies have found that insect layering is a relatively frequent phenomenon in nocturnal profiles, although it is by no means ubiquitous: for example, systematic studies have previously reported nocturnal layering frequencies of ca. 50% in Australia (Drake & Rochester 1994) and ca. 15e30% in the U.K. (Wood et al. 2009, 2010). Our observed layering frequency of ca. 25% in the
0.5 Heading distribution r value
evening on which layering was clear and pronounced (i.e. there was a single pronounced peak in the profile, and this contained a substantial proportion of the total insects flying at that time; e.g. Fig. 1a) were identified using our previously published ‘Layer Quality’ assessment (see Appendix 1 in Reynolds et al. 2005). Second, the profiles were checked by visual inspection to confirm strong vertical stratification before the period was allocated to the ‘layered’ category. Periods with profiles not so allocated comprised the ‘nonlayered’ category (which also contained weakly stratified and complex multipeaked profiles; e.g. Fig. 1b). The Rayleigh test of uniformity for circular data (Fisher 1993) was then used to calculate the following variables for each migration event: (1) the mean displacement direction, the mean resultant length ‘r’ (a measure of angular dispersion) of the distribution, and the probability that the distribution differed from uniform; (2) the mean flight heading and associated circular statistics; (3) the magnitude and direction (clockwise or anticlockwise) of the ‘heading offset’ (the angle between the displacement and the heading); and (4) the mean displacement speed. The proportion of events exhibiting a significant level of common orientation (those with a Rayleigh test P value < 0.05) was calculated for each body size and profile combination. Variation in the strength of common orientation between events was analysed with a two-way ANOVA of heading distribution r values, with profile (‘layered’ or ‘nonlayered’) and body size (‘medium’ or ‘large’) as the factors. Similarly, variation in the absolute size of the heading offset (ignoring the direction of the offset from the displacement), and the displacement speed of the migrants, was also assessed with two-way ANOVA using the same factors. In addition, distributions of heading offset directions were tested to see whether there was a significant bias to the left or right of the downwind direction (using mean displacement direction as a proxy for the downwind direction), by arbitrarily assigning negative values to left offsets and positive values to right offsets, and then comparing the mean 95% confidence intervals (CI) with an expected mean offset of zero (Reynolds et al. 2010a).
0.45
Medium Large
0.4
0.35
0.3
Nonlayered Layered Density–height profile
Figure 2. The tightness of common orientation during nocturnal migration events of medium-sized and large insects. Larger r values signify tighter distributions of individual headings around the mean direction. Error bars represent 1 SE.
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45 Medium Large
Heading offset (°)
40
35
30
25
20
Nonlayered Layered Density–height profile
Figure 3. The magnitude of mean heading offsets from the mean windborne displacement direction during nocturnal migration events of medium-sized and large insects. Smaller offsets signify orientation closer to the downwind direction. Error bars represent 1 SE.
present study thus fits well with previously published observations. There is a lack of data on the frequency of common orientation among nocturnal insect migrants, and thus our finding that, in the U.K., 75e90% of nocturnal migration events demonstrate this phenomenon is both novel and noteworthy. Recent theoretical advances (Reynolds et al. 2009, 2010a, b) have suggested that a single mechanism, involving fluctuations in turbulence properties with altitude, accounts for both wind-related layering and common orientation of nocturnally migrating insects. A previous study demonstrated that one of the predictions of this theory (that headings should be offset clockwise from the downwind direction in the northern hemisphere) was supported by radar observations of a limited set of data (Reynolds et al. 2010a), and the current study confirms this finding in a much larger and replicated data set. The results of the present systematic study of the vertical density profiles and patterns of wind-related orientation of nocturnally migrating insects over the U.K. provide the first confirmation that common orientation and layering are associated. When we compared the orientation performance of migrants either concentrated within narrow layers (typically 100e200 m deep) or more evenly dispersed throughout the air column, we found that common orientation was almost universal when insects migrated in layers, but was less frequent when insect profiles were not layered. Furthermore, the strength of common orientation was significantly greater, and the heading offsets were significantly smaller, in layered profiles in comparison to nonlayered ones. These results, in combination with the frequent coincidence of layer altitude with the height of attributes of the wind profile such as wind speed maxima (Wolf et al. 1986; Feng et al. 2004; Wood et al. 2006; Chapman et al. 2010), uphold the contention that layering, orientation and features of the wind field are intrinsically linked, and provide strong support for the turbulence-mediated mechanism for altitude selection and uptake of wind-related common headings (Reynolds et al. 2009, 2010a). We have also verified the previous finding that headings in the northern hemisphere are consistently offset to the right (clockwise) from the downwind direction owing to the action of the Ekman spiral (Reynolds et al. 2010a), as all four categories of nocturnal migrants exhibited a significant bias to the right in the present study. A final prediction of the theory is that larger insects should show stronger patterns of common orientation than smaller ones, owing to their larger inertia resulting in a greater lag between their velocity
fluctuations and the wind velocity fluctuations (Reynolds et al. 2010a). Our result matches the prediction precisely: ‘large’ insect migrants (e.g. noctuid moths weighing 70e500 mg) had significantly tighter distributions of their individual headings than the ‘medium-sized’ migrants (e.g. Neuroptera and micro-Lepidoptera weighing 10e69 mg), irrespective of whether they flew in layered or nonlayered profiles. Noctuid moths employ compass-mediated orientation strategies (Chapman et al. 2008a, b, 2010) in addition to the wind-related responses explored in this current study; the interplay between these two mechanistically different, but not mutually exclusive, strategies is likely to be complex and context dependent. Further work is underway that will explore the relationship between these two contrasting mechanisms which underlie the uptake of adaptive flight headings in nocturnal insects. The results of our study therefore provide robust evidence that a turbulence-mediated mechanism is the principal method by which nocturnal insects select wind-related flight altitudes and headings. However, considering the exquisite sensitivity of nocturnal insect eyes (Baird et al. 2011; Warrant & Dacke 2011), some role for a visually mediated mechanism (based on visual assessment of movement speed and direction over the ground) should not be ruled out. The mechanoreceptors responsible for detecting the weak turbulent fluctuations remain to be identified, but considering the function that antennae play in flight stabilization and migratory regulation in Lepidoptera (Sane et al. 2007, 2010; Merlin et al. 2009), they are probably the prime candidates. Whatever the underlying mechanism proves to be, there is no doubt that altitude selection and orientation in relation to features of the wind is highly beneficial for insect migrants, resulting in rapid displacement speeds and extended journeys. Acknowledgments This work was funded by a grant from the University of Agricultural Science in Raichur to P.A. We thank Alan Smith (Rothamsted Research) and Darcy Ladd (Chilbolton) for technical assistance. Rothamsted Research receives support from the Biotechnology and Biological Sciences Research Council (BBSRC). References Alerstam, T., Chapman, J. W., Bäckman, J., Smith, A. D., Karlsson, H., Nilsson, C., Reynolds, D. R., Klaassen, R. H. G. & Hill, J. K. 2011. Convergent patterns of long-distance nocturnal migration in noctuid moths and passerine birds. Proceedings of the Royal Society B, 278, 3074e3080. published online 9 March 2011, doi:10.1098/rspb.2011.0058. Ayyalasomayajula, S., Gyfason, A., Collins, L. R., Bodenschatz, E. & Warhaft, Z. 2006. Lagrangian measurements of inertial particle accelerations in grid generated wind tunnel turbulence. Physical Review Letters, 97, 144507. Baird, E., Kreiss, E., Wcislo, W., Warrant, E. & Dacke, M. 2011. Nocturnal insects use optic flow for flight control. Biology Letters, 9, 499e501. Chapman, J. W. & Drake, V. A. 2010. Insect migration. In: Encyclopedia of Animal Behavior. Vol. 2 (Ed. by M. D. Breed & J. Moore), pp. 161e166. Oxford: Academic Press. Chapman, J. W., Reynolds, D. R. & Smith, A. D. 2003. Vertical-looking radar: a new tool for monitoring high-altitude insect migration. Bioscience, 53, 503e511. Chapman, J. W., Reynolds, D. R., Smith, A. D., Smith, E. T. & Woiwod, I. P. 2004. An aerial netting study of insects migrating at high-altitude over England. Bulletin of Entomological Research, 94, 123e136. Chapman, J. W., Reynolds, D. R., Mouritsen, H., Hill, J. K., Riley, J. R., Sivell, D., Smith, A. D. & Woiwod, I. P. 2008a. Wind selection and drift compensation optimize migratory pathways in a high-flying moth. Current Biology, 18, 514e518. Chapman, J. W., Reynolds, D. R., Hill, J. K., Sivell, D., Smith, A. D. & Woiwod, I. P. 2008b. A seasonal switch in compass orientation in a high-flying migrant moth. Current Biology, 18, R908eR909. Chapman, J. W., Nesbit, R. L., Burgin, L. E., Reynolds, D. R., Smith, A. D., Middleton, D. R. & Hill, J. K. 2010. Flight orientation behaviours promote optimal migration trajectories in high- flying insects. Science, 327, 682e685. Chapman, J. W., Drake, V. A. & Reynolds, D. R. 2011. Recent insights from radar studies of insect flight. Annual Review of Entomology, 56, 337e356.
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Reynolds, A. M., Reynolds, D. R., Smith, A. D. & Chapman, J. W. 2010a. A single wind-mediated mechanism explains high-altitude ‘non-goal oriented’ headings and layering of nocturnally migrating insects. Proceedings of the Royal Society B, 277, 765e772. Reynolds, A. M., Reynolds, D. R., Smith, A. D. & Chapman, J. W. 2010b. Orientation cues for high-flying nocturnal insect migrants: do turbulence-induced temperature and velocity fluctuations indicate the mean wind flow? PLoS One, 5, e15758. Riley, J. R. 1975. Collective orientation in night-flying insects. Nature, 253, 113e114. Riley, J. R. & Reynolds, D. R. 1986. Orientation at night by high-flying insects. In: Insect Flight: Dispersal and Migration (Ed. by W. Danthanarayana), pp. 71e87. Berlin: Springer-Verlag. Riley, J. R., Cheng, X. N., Zhang, X. X., Reynolds, D. R., Xu, G. M., Smith, A. D., Cheng, J. Y., Bao, A. D. & Zhai, B. P. 1991. The long distance migration of Nilaparvata lugens (Stål) (Delphacidae) in China: radar observations of mass return flight in the autumn. Ecological Entomology, 16, 471e489. Sane, S. P., Dieudonne, A., Willis, M. A. & Daniel, T. L. 2007. Antennal mechanosensors mediate flight control in moths. Science, 315, 863e866. Sane, S. P., Srygley, R. B. & Dudley, R. 2010. Antennal regulation of migratory flight in the neotropical moth Urania fulgens. Biology Letters, 6, 406e409. Srygley, R. B. & Dudley, R. 2008. Optimal strategies for insects migrating in the flight boundary layer: mechanisms and consequences. Integrative and Comparative Biology, 48, 119e133. Warrant, E. & Dacke, M. 2011. Vision and visual navigation in nocturnal insects. Annual Review of Entomology, 56, 239e254. Wolf, W. W., Westbrook, J. K. & Sparks, A. N. 1986. Relationships between radar entomological measurements and atmospheric structure in south Texas during March and April 1982. In: Long-range Migration of Moths of Agronomic Importance to the United States and Canada: Specific Examples of the Occurrence and Synoptic Weather Patterns Conducive to Migration (Ed. by A. N. Sparks), pp. 84e97. Washington: D.C.: US Department of Agriculture, Agricultural Research Service ARS-43. Wood, C. R., Chapman, J. W., Reynolds, D. R., Barlow, J. F., Smith, A. D. & Woiwod, I. P. 2006. The influence of the atmospheric boundary layer on nocturnal layers of moths migrating over southern Britain. International Journal of Biometeorology, 50, 193e204. Wood, C. R., Reynolds, D. R., Wells, P. M., Barlow, J. F., Woiwod, I. P. & Chapman, J. W. 2009. Flight periodicity and the vertical distribution of highaltitude moth migration over southern Britain. Bulletin of Entomological Research, 99, 525e535. Wood, C. R., Clark, S. J., Barlow, J. F. & Chapman, J. W. 2010. Layers of nocturnal insect migrants at high-altitude: the influence of atmospheric conditions on their formation. Agricultural and Forest Entomology, 12, 113e121.
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Articles
Flight altitude selection increases orientation performance in high-flying nocturnal insect migrants Prabhuraj Aralimarad a, b, Andy M. Reynolds a, Ka S. Lim a, Don R. Reynolds a, c, Jason W. Chapman a, * a
Rothamsted Research College of Agriculture, University of Agricultural Sciences, Raichur, India c Natural Resources Institute, University of Greenwich, U.K. b
a r t i c l e i n f o Article history: Received 12 July 2011 Initial acceptance 11 August 2011 Final acceptance 6 September 2011 Available online 5 October 2011 MS. number: 11-00548 Keywords: entomological radar flight altitude insect layer migration orientation cue turbulence
Many insects migrate at high altitudes where they utilize fast-flowing airstreams for long-distance transport. Nocturnal insect migrants typically exhibit a strongly unimodal distribution of flight headings (a phenomenon termed ‘common orientation’), and the mean heading is often aligned downwind. In addition, these nocturnal migrants are sometimes concentrated into shallow altitudinal zones (termed ‘layers’). The mechanism by which widely separated insects select and maintain common flight headings had until recently eluded explanation, but recent theoretical advances have shown that atmospheric turbulence might enable insects to perceive the downwind direction and orient accordingly. This theory predicts that common orientation downwind should be: (1) widespread in nocturnal insect migrants; (2) facilitated when insects are concentrated into layers; and (3) more pronounced in larger insects. We tested these ideas using radar observations of 647 independent nocturnal migration events, and found strong support for all three predictions: (1) common orientation occurred in 75e90% of events; (2) common orientation was more frequent, had significantly less scatter and was significantly closer to downwind when insects migrated in layers; and (3) large insects exhibited significantly tighter orientation than ‘medium-sized’ insects. Our results provide robust evidence that wind-related common orientation is mediated by detection of atmospheric turbulence. Ó 2011 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Although some insects such as butterflies migrate by flying near the ground within their ‘flight boundary layer’ (where the wind is light enough for the insect to make progress in any direction; Srygley & Dudley 2008), in the vast majority of species migration over any significant distance takes place at higher altitudes to utilize assistance from the wind (Gatehouse 1997; Chapman et al. 2011). In fact, as long as it is warm enough for flight, the lowest 2e3 km of the troposphere hosts an incessant ‘bioflow’ of insects involving myriad taxa (e.g. Chapman et al. 2004) and vast numbers of individuals (e.g. Riley et al. 1991). The flights are part of a ‘migration syndrome’: a group of adaptive traits that facilitate redistribution of populations, and this in turn enables migratory species to exploit spatiotemporal patterns of availability in various resources (Drake & Gatehouse 1995; Dingle 1996; Dingle & Drake 2007). Wind-assisted movements are particularly required where species migrate between climatic zones in order to take advantage of seasonal changes of temperature and rainfall (Drake & Gatehouse 1995; Drake et al. 2001; Chapman & Drake 2010).
* Correspondence: J. W. Chapman, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, U.K. E-mail address: [email protected] (J. W. Chapman).
The very low self-propelled speeds through the surrounding air (airspeeds) of small insects mean that these species make little contribution to their horizontal displacement speed during migratory flight (although they do control the initiation and, to a certain extent, the termination of migration). The same is not true of larger insects, and the recent evidence of sophisticated migration behaviour (e.g. control of timing and height of flight, and windrelated heading directions) has led to a paradigm shift in our understanding of wind-assisted migration strategies in these insect species (Chapman et al. 2008a, b, 2010). Among the responses of high-altitude migrants to their atmospheric environment, largely documented by radar (Chapman et al. 2011), are two frequently observed phenomena. These are the formation of ‘layer concentrations’ where insects concentrate at certain altitudes in stable night-time atmospheres (Wolf et al. 1986; Drake & Farrow 1988; Gatehouse 1997; Reynolds et al. 2005, 2009; Chapman et al. 2011; see Fig. 1a), and the adoption of common heading directions (‘common orientation’; Riley 1975; Drake 1983; Riley & Reynolds 1986; Reynolds et al. 2010a; Chapman et al. 2011). Both the layering and the persistent orientation pattern are broadscale phenomena which may extend over thousands of square kilometres on some occasions (e.g. Hobbs & Wolf 1996, who flew long transects over Texas with a nadir-pointing airborne radar,
0003-3472/$38.00 Ó 2011 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.anbehav.2011.09.013
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1400
(a)
1200 1000 800 600 400
Altitude (m)
200 0
0
1400
10
20
10
20
30
40
50
60
70
30 40 50 Number of insects
60
70
(b)
1200 1000 800 600 400 200 0
0
Figure 1. (a) A ‘layered profile’: the vertical distribution of insect numbers between 2200 and 2206 hours on 13 July 2006 detected by the Rothamsted vertical-looking radar. A pronounced layer of insects, centred about 600 m above ground, appeared to be associated with a temperature inversion and strong wind stream at that altitude. (b) A ‘nonlayered profile’: the vertical distribution of insect numbers between 2215 and 2236 hours on 15 July 2006 at Rothamsted. Although some structure is evident in the profile, it does not show the strong layering with most targets concentrated around one flight height, as in (a).
found that the mean orientation direction was almost constant along the whole extent of the layer). Previous studies have speculated that common orientation and layering may be mechanistically linked (Drake 1983; Hobbs & Wolf 1989; Reynolds et al. 2009, 2010a, b; Chapman et al. 2011), but this idea has yet to be confirmed. Obtaining reliable visual cues for the purposes of taking up an adaptive flight orientation is particularly challenging at night, when light levels can be up to 11 orders of magnitude lower than they are during the day (Baird et al. 2011; Warrant & Dacke 2011). Thus it had been assumed that because of the difficulty of deriving visual information, those insects migrating hundreds of metres above the ground at night would exhibit random patterns of flight headings (reviewed in Reynolds et al. 2010a). However, it was clear from the earliest entomological radar observations (Riley 1975; Drake 1983) that, in the larger nocturnal migrants at least, the heading distributions can be remarkably clustered, and that the mean heading is often relatively close to the downwind direction (Reynolds et al. 2010a; Chapman et al. 2011). Downwind orientation is generally adaptive in these migrating insects because it adds their airspeed (ca. 1e5 m/s depending on their size) to the wind speed, resulting in significant increases to their migration distances (Chapman et al. 2008a, b, 2010; Alerstam et al. 2011). Furthermore, flying in layer concentrations at the altitude of the warmest and fastest-moving
airstreams (Wood et al. 2006; Reynolds et al. 2010a; Chapman et al. 2011) will also lead to significant increases in migration distances. But while the benefits are clear, the mechanisms that individual migrants use to select and maintain similar flight altitudes and wind-related headings, while migrating under very low illumination levels and up to 1.5 km above the ground, have remained mysterious (Reynolds et al. 2009, 2010a). Recent theoretical advances have, however, identified features of the wind (anisotropic turbulent velocity and acceleration fluctuations) that may provide plausible cues for detection of the downwind direction and preliminary observations indicate that insect orientation patterns are consistent with some of the predictions that arise from this theory (Reynolds et al. 2010a, b). Further investigation of these hypotheses by laboratory-scale experiments appear to be extremely difficult because they necessitate measuring turbulent airflows in the immediate vicinity of mobile free-flying migrants. State-of-the-art experiments can monitor and record the trajectories of inert particles as they are carried along by turbulent airflows but they cannot measure the turbulent flows directly experienced by the particles nor can they measure particle-turbulent interactions (Ayyalasomayajula et al. 2006). Turbulent flows, of course, can be measured at some distance from a particle, at fixed locations using anemometers, but at any instant these flows will be different from the turbulence experienced by the particle (Reynolds & Lo Iacono 2004). Another significant problem is that the spatiotemporal scales of turbulence produced in laboratory-scale experiments will not match those of atmospheric turbulence. In view of these difficulties, detailed analysis of insect density/height profiles under natural conditions appears to be the best way forward. Consequently, we examined some predictions of the turbulence theory that are testable using flight heading and altitude data from a large number of independent nocturnal migration events recorded by entomological radars situated in inland southern England. The predictions are that common orientation should be: (1) a common feature of populations of night-flying insect migrants (this appeared to be true in general terms, but needed quantifying); (2) more frequent and stronger when migrants are concentrated in narrow atmospheric layers rather than widely dispersed over a range of flight altitudes; and (3) more pronounced in larger insects than smaller ones. Additionally, we looked for confirmation that the mean heading of nocturnal migrants exhibiting common orientation should on average be offset to the right of the downwind direction, owing to the effect of the Ekman spiral, as previously reported (Reynolds et al. 2010a). METHODS We selected 647 nocturnal migration ‘events’ recorded by our two vertical-looking entomological radars (VLRs; Chapman et al. 2003, 2011) during the period May to September in recent intense migration years (namely 2000, 2003 and 2006; see Chapman et al. 2010). The VLR locations, equipment and operating procedures have been described in detail elsewhere (Chapman et al. 2003, 2011; Reynolds et al. 2005). Each of these migration events involved the detection of either >20 individual ‘mediumsized’ insects (body mass 10e69 mg, N ¼ 252 events involving 28 604 insects) or >20 individual ‘large’ insects (70e500 mg, N ¼ 395 events involving 56 631 insects), flying in the altitude range 300e800 m above one of the radar sites between 2130 and midnight GMT (and thus after the end of civil twilight). The vertical profile of insect aerial density was examined during each migration event, so that each could be categorized as either a ‘layered profile’ (N ¼ 149 events involving 34 970 insects) or a ‘nonlayered profile’ (N ¼ 498 events involving 50 265 insects). First, periods during an
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Table 1 Orientation and ground speed characteristics of the four categories of migratory events
Nonlayered Layered
Medium Large Medium Large
Overall
N (events)
Common orientation (%)
Heading r value
Heading offset ( )
Ground speed (m/s)
186 312 66 83 647
74.2 79.5 92.4 91.6 80.8
0.3880.013 0.4250.010 0.4370.022 0.4760.019 0.4220.007
39.31.8 38.41.4 31.92.9 28.32.1 36.40.9
13.70.3 13.90.2 13.10.5 14.00.4 13.80.2
Values are means 1 SE.
RESULTS Common orientation of nocturnal flight headings was always frequent (Table 1), but occurred with greater frequency when migrants were in well-defined layers (>90% of events) than when nonlayered (ca. 75% of events). Well-defined nocturnal layering itself, however, only occurred on ca. 25% of occasions. Migrants concentrated within altitudinal layers showed significantly tighter distributions of individual flight headings than those insects migrating under nonlayered conditions (two-way ANOVA of heading r values: F1,643 ¼ 8.69, P ¼ 0.003; Fig. 2, Table 1). In addition, those in layers also had significantly smaller heading offsets from the downwind direction (two-way ANOVA: F1,519 ¼ 18.02, P < 0.001; Fig. 3, Table 1). Large insects showed significantly tighter orientation distributions than medium-sized insects (two-way ANOVA of heading r values: F1,643 ¼ 6.59, P ¼ 0.010; Fig. 2, Table 1), but there was no
effect of body size on the magnitude of the offset (two-way ANOVA: F1,519 ¼ 0.74, P ¼ 0.389; Fig. 3, Table 1). Mean displacement speeds did not differ between layered and nonlayered events or between medium and large insects (two-way ANOVA: profile: F1,642 ¼ 0.23, P ¼ 0.635; size: F1,642 ¼ 0.85, P ¼ 0.357; Table 1); the overall mean travel speed of 13.8 m/s corresponds to 50 km/h, and thus migrants were typically travelling at rather rapid ground speeds. There were no significant interactions between vertical profile and body size for any of the comparisons carried out (two-way ANOVA: heading r value: F1,643 ¼ 0.01, P ¼ 0.929; offset: F1,519 ¼ 0.42, P ¼ 0.516; speed: F1,642 ¼ 0.86, P ¼ 0.353). For the direction of the heading offsets relative to the downwind direction, offsets of both medium-sized and large insects were much more likely to occur to the right of the wind than the left, and differed significantly from zero under both nonlayered conditions (medium-sized insects: mean offset 21.0 7.2 (95% confidence interval, CI) to right of zero, N ¼ 138 events, 69% with a right bias, P < 0.0001; large insects: mean offset 23.4 4.9 (95% CI) to right of zero, N ¼ 248 events, 72% with a right bias, P < 0.0001) and layered conditions (medium-sized insects: mean offset 14.0 9.3 (95% CI) to right of zero, N ¼ 61 events, 69% with a right bias, P ¼ 0.003; large insects: mean offset 15.1 6.8 (95% CI) to right of zero, N ¼ 76 events, 75% with a right bias, P < 0.0001).
DISCUSSION Previous studies have found that insect layering is a relatively frequent phenomenon in nocturnal profiles, although it is by no means ubiquitous: for example, systematic studies have previously reported nocturnal layering frequencies of ca. 50% in Australia (Drake & Rochester 1994) and ca. 15e30% in the U.K. (Wood et al. 2009, 2010). Our observed layering frequency of ca. 25% in the
0.5 Heading distribution r value
evening on which layering was clear and pronounced (i.e. there was a single pronounced peak in the profile, and this contained a substantial proportion of the total insects flying at that time; e.g. Fig. 1a) were identified using our previously published ‘Layer Quality’ assessment (see Appendix 1 in Reynolds et al. 2005). Second, the profiles were checked by visual inspection to confirm strong vertical stratification before the period was allocated to the ‘layered’ category. Periods with profiles not so allocated comprised the ‘nonlayered’ category (which also contained weakly stratified and complex multipeaked profiles; e.g. Fig. 1b). The Rayleigh test of uniformity for circular data (Fisher 1993) was then used to calculate the following variables for each migration event: (1) the mean displacement direction, the mean resultant length ‘r’ (a measure of angular dispersion) of the distribution, and the probability that the distribution differed from uniform; (2) the mean flight heading and associated circular statistics; (3) the magnitude and direction (clockwise or anticlockwise) of the ‘heading offset’ (the angle between the displacement and the heading); and (4) the mean displacement speed. The proportion of events exhibiting a significant level of common orientation (those with a Rayleigh test P value < 0.05) was calculated for each body size and profile combination. Variation in the strength of common orientation between events was analysed with a two-way ANOVA of heading distribution r values, with profile (‘layered’ or ‘nonlayered’) and body size (‘medium’ or ‘large’) as the factors. Similarly, variation in the absolute size of the heading offset (ignoring the direction of the offset from the displacement), and the displacement speed of the migrants, was also assessed with two-way ANOVA using the same factors. In addition, distributions of heading offset directions were tested to see whether there was a significant bias to the left or right of the downwind direction (using mean displacement direction as a proxy for the downwind direction), by arbitrarily assigning negative values to left offsets and positive values to right offsets, and then comparing the mean 95% confidence intervals (CI) with an expected mean offset of zero (Reynolds et al. 2010a).
0.45
Medium Large
0.4
0.35
0.3
Nonlayered Layered Density–height profile
Figure 2. The tightness of common orientation during nocturnal migration events of medium-sized and large insects. Larger r values signify tighter distributions of individual headings around the mean direction. Error bars represent 1 SE.
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45 Medium Large
Heading offset (°)
40
35
30
25
20
Nonlayered Layered Density–height profile
Figure 3. The magnitude of mean heading offsets from the mean windborne displacement direction during nocturnal migration events of medium-sized and large insects. Smaller offsets signify orientation closer to the downwind direction. Error bars represent 1 SE.
present study thus fits well with previously published observations. There is a lack of data on the frequency of common orientation among nocturnal insect migrants, and thus our finding that, in the U.K., 75e90% of nocturnal migration events demonstrate this phenomenon is both novel and noteworthy. Recent theoretical advances (Reynolds et al. 2009, 2010a, b) have suggested that a single mechanism, involving fluctuations in turbulence properties with altitude, accounts for both wind-related layering and common orientation of nocturnally migrating insects. A previous study demonstrated that one of the predictions of this theory (that headings should be offset clockwise from the downwind direction in the northern hemisphere) was supported by radar observations of a limited set of data (Reynolds et al. 2010a), and the current study confirms this finding in a much larger and replicated data set. The results of the present systematic study of the vertical density profiles and patterns of wind-related orientation of nocturnally migrating insects over the U.K. provide the first confirmation that common orientation and layering are associated. When we compared the orientation performance of migrants either concentrated within narrow layers (typically 100e200 m deep) or more evenly dispersed throughout the air column, we found that common orientation was almost universal when insects migrated in layers, but was less frequent when insect profiles were not layered. Furthermore, the strength of common orientation was significantly greater, and the heading offsets were significantly smaller, in layered profiles in comparison to nonlayered ones. These results, in combination with the frequent coincidence of layer altitude with the height of attributes of the wind profile such as wind speed maxima (Wolf et al. 1986; Feng et al. 2004; Wood et al. 2006; Chapman et al. 2010), uphold the contention that layering, orientation and features of the wind field are intrinsically linked, and provide strong support for the turbulence-mediated mechanism for altitude selection and uptake of wind-related common headings (Reynolds et al. 2009, 2010a). We have also verified the previous finding that headings in the northern hemisphere are consistently offset to the right (clockwise) from the downwind direction owing to the action of the Ekman spiral (Reynolds et al. 2010a), as all four categories of nocturnal migrants exhibited a significant bias to the right in the present study. A final prediction of the theory is that larger insects should show stronger patterns of common orientation than smaller ones, owing to their larger inertia resulting in a greater lag between their velocity
fluctuations and the wind velocity fluctuations (Reynolds et al. 2010a). Our result matches the prediction precisely: ‘large’ insect migrants (e.g. noctuid moths weighing 70e500 mg) had significantly tighter distributions of their individual headings than the ‘medium-sized’ migrants (e.g. Neuroptera and micro-Lepidoptera weighing 10e69 mg), irrespective of whether they flew in layered or nonlayered profiles. Noctuid moths employ compass-mediated orientation strategies (Chapman et al. 2008a, b, 2010) in addition to the wind-related responses explored in this current study; the interplay between these two mechanistically different, but not mutually exclusive, strategies is likely to be complex and context dependent. Further work is underway that will explore the relationship between these two contrasting mechanisms which underlie the uptake of adaptive flight headings in nocturnal insects. The results of our study therefore provide robust evidence that a turbulence-mediated mechanism is the principal method by which nocturnal insects select wind-related flight altitudes and headings. However, considering the exquisite sensitivity of nocturnal insect eyes (Baird et al. 2011; Warrant & Dacke 2011), some role for a visually mediated mechanism (based on visual assessment of movement speed and direction over the ground) should not be ruled out. The mechanoreceptors responsible for detecting the weak turbulent fluctuations remain to be identified, but considering the function that antennae play in flight stabilization and migratory regulation in Lepidoptera (Sane et al. 2007, 2010; Merlin et al. 2009), they are probably the prime candidates. Whatever the underlying mechanism proves to be, there is no doubt that altitude selection and orientation in relation to features of the wind is highly beneficial for insect migrants, resulting in rapid displacement speeds and extended journeys. Acknowledgments This work was funded by a grant from the University of Agricultural Science in Raichur to P.A. We thank Alan Smith (Rothamsted Research) and Darcy Ladd (Chilbolton) for technical assistance. Rothamsted Research receives support from the Biotechnology and Biological Sciences Research Council (BBSRC). References Alerstam, T., Chapman, J. W., Bäckman, J., Smith, A. D., Karlsson, H., Nilsson, C., Reynolds, D. R., Klaassen, R. H. G. & Hill, J. K. 2011. Convergent patterns of long-distance nocturnal migration in noctuid moths and passerine birds. Proceedings of the Royal Society B, 278, 3074e3080. published online 9 March 2011, doi:10.1098/rspb.2011.0058. Ayyalasomayajula, S., Gyfason, A., Collins, L. R., Bodenschatz, E. & Warhaft, Z. 2006. Lagrangian measurements of inertial particle accelerations in grid generated wind tunnel turbulence. Physical Review Letters, 97, 144507. Baird, E., Kreiss, E., Wcislo, W., Warrant, E. & Dacke, M. 2011. Nocturnal insects use optic flow for flight control. Biology Letters, 9, 499e501. Chapman, J. W. & Drake, V. A. 2010. Insect migration. In: Encyclopedia of Animal Behavior. Vol. 2 (Ed. by M. D. Breed & J. Moore), pp. 161e166. Oxford: Academic Press. Chapman, J. W., Reynolds, D. R. & Smith, A. D. 2003. Vertical-looking radar: a new tool for monitoring high-altitude insect migration. Bioscience, 53, 503e511. Chapman, J. W., Reynolds, D. R., Smith, A. D., Smith, E. T. & Woiwod, I. P. 2004. An aerial netting study of insects migrating at high-altitude over England. Bulletin of Entomological Research, 94, 123e136. Chapman, J. W., Reynolds, D. R., Mouritsen, H., Hill, J. K., Riley, J. R., Sivell, D., Smith, A. D. & Woiwod, I. P. 2008a. Wind selection and drift compensation optimize migratory pathways in a high-flying moth. Current Biology, 18, 514e518. Chapman, J. W., Reynolds, D. R., Hill, J. K., Sivell, D., Smith, A. D. & Woiwod, I. P. 2008b. A seasonal switch in compass orientation in a high-flying migrant moth. Current Biology, 18, R908eR909. Chapman, J. W., Nesbit, R. L., Burgin, L. E., Reynolds, D. R., Smith, A. D., Middleton, D. R. & Hill, J. K. 2010. Flight orientation behaviours promote optimal migration trajectories in high- flying insects. Science, 327, 682e685. Chapman, J. W., Drake, V. A. & Reynolds, D. R. 2011. Recent insights from radar studies of insect flight. Annual Review of Entomology, 56, 337e356.
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