The Society for Integrative and Comparative Biology
Biotelemetry of New World thrushes during migration: Physiology, energetics and orientation in the wild1
1 Department of Ecology and Evolutionary Biology, 102 Guyot Hall, Princeton University, Princeton, New Jersey 08540
2 Illinois Natural History Survey, 607 East Peabody Drive, Champaign, Illinois 61820 USA
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Billions of songbirds migrate between continents each year, but we have yet to obtain enough information on in-flight physiology and energetics to fully understand the migratory behavior of any one species. New World Catharus thrushes are common nocturnal migrants amenable to biotelemetry, allowing us to measure physiological parameters during migratory flight in the wild. Here, we review work by the authors on Catharus thrush in-flight physiology during spring migration in continental North America and present new data on individual variation in energy use during migratory flight. Previous work demonstrated that (1) a number of simple behavioral rules are sufficient to explain the initiation of individual migratory flights made by Catharus thrushes, (2) the thrushes used a magnetic compass to orient during the night rather than celestial cues and that they calibrated this magnetic compass each day using cues associated with the setting sun, (3) in total, Catharus thrushes used approximately twice as much energy during stopovers than they used during migratory flight, and (4) thrushes may use more energy when thermoregulating on cold days than on days when they make short migratory flights. Recently, we built upon this work and used newly-developed transmitters to measure heart rate, wingbeat frequency and respiration rate of free-flying Swainson's Thrushes (C. ustulatus). We found a large amount of between-individual variation in average heart rate after ascent (range 12.06–14.81 Hz, mean ± SD, 13.48 ± 0.75, n = 10), average wingbeat frequency after ascent (10.25–11.75 Hz, 10.82 ± 0.49, n = 10), and the difference between the two variables (1.5–3.84 Hz, 2.53 ± 0.76, n = 8). Both heart rate and wingbeat frequency were significantly higher during ascent than later in the flight. We propose biotelemetry as a means to understand energetic trade-offs and decisions during natural migratory flight in songbirds. To further our knowledge of intercontinental songbird migration and the connectivity between wintering and breeding sites, we outline plans for a satellite-based global tracking system for <1 g transmitters.
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INTRODUCTION |
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Every year, billions of individuals representing thousands of species of animals make migratory journeys. An estimated 50 billion of the 200–400 billion birds on the earth make predictable seasonal movements between the temperate zone and the tropics (Berthold, 2001
). In eastern North America, over two-thirds of breeding bird species migrate (Moore, 2000). Migratory songbirds play an important role in their environment and can for example be important disease vectors (Jackson, 1979; Otvos, 1979; Rappole et al., 2000; Malkinson et al., 2002; but see Rappole and Hubalek, 2003). Migrants may be more vulnerable to extinction than non-migrants as they depend on three different habitats (wintering, stopover and breeding) each year rather than a single one (Terborgh, 1974; Rappole, 1995).
Because of their importance and possible vulnerability, it is essential that we learn more about the behavioral and physiological constraints migrant songbirds face while flying across continents. Advancing our knowledge of in-flight physiology is an excellent way to understand the mechanisms that underlie behavioral decisions of migrant songbirds; thus, we use biotelemetry (Cooke et al., 2004) to directly quantify physiological parameters during flight.
Much is already known about the behavior, ecology and physiology of migratory birds. In particular, much progress has been made in understanding stopover ecology, habitat use and selection, competition, diet selection and foraging (e.g., Bairlein, 2002; Biebach, 1995; Hume and Biebach, 1996; Jenni-Eiermann and Jenni, 2001; Baker et al., 2004; Yong and Moore, 1994; McWilliams and Karasov 2001; Rodewald and Brittingham 2002). Here we focus on a new methodology that we hope will complement these studies. Methods employed previously to study migratory behavior include direct observations of diurnal birds, collections of birds either in flight or after being killed at migratory obstacles, recordings of calls of nocturnal migrants, tracking birds by radar or radio telemetry, observations of captive birds during the migratory season, and, most prominently, the marking of birds with bands or paint and later recapture/resighting (Berthold, 2001). However, barring exceptional luck, of all of these methods only radio telemetry allows individual free-living nocturnal migrants to be examined immediately before, during, and immediately after migratory flights, in different habitats hundreds of kilometers apart (Wikelski et al., 2003). In fact, an individual songbird can even be followed during multiple migratory flights (e.g. Cochran, 1987; Cochran et al., 2004). Perhaps most importantly, radio transmitters allow researchers to study physiological parameters of birds in the wild rather than under laboratory conditions. Because of its many advantages, we have made extensive use of radio telemetry in our work on the migratory behavior of New World Catharus thrushes.
Recent technological developments have led to <1 g radio transmitters that can measure heart rate, wingbeat frequency, and respiration rate in addition to simply providing a method of locating the bird (Cochran and Wikelski, 2005). With these transmitters, researchers can potentially obtain detailed information about energy use during migration if careful calibrations are performed (for large birds, see Nolet et al., 1992; Bevan et al., 1995; Butler et al., 1998; Ward et al., 2002). In this paper, we summarize recent results from prior work on the energetics and orientation of migrating Catharus thrushes to present an ecological framework for our in-flight physiological measurements and then present new data on interspecific variation in energy use during migratory flight obtained using the physiological transmitters.
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MODEL MIGRATORY ORGANISMS: NEW WORLD THRUSHES |
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Catharus thrushes that breed in the northern United States and Canada are long-distance migrants, with the exception of the Hermit Thrush (C. guttatus, 31.2 g adults during migration in southern Ontario [Jones and Donovan, 1996
]), which is a short-distance migrant. The New World thrushes include the Veery (C. fuscescens, mean 32.4 g for all birds [Moskoff, 1995]), Gray-Cheeked Thrush (C. minimus, 32.6 g adult males, 30.6 g adult females in Illinois during migration, [Lowther et al., 2001]), Bicknell's Thrush (C. bicknelli, 29.2 g adult males, 28.9 g adult females during the breeding season, [Rimmer et al., 2001]), Swainson's Thrush (C. ustulatus, 32.7 g adult males, 30.3 g adult females in Illinois during migration [Mack and Yong, 2000]), and Hermit Thrush. Migratory behavior appears to have evolved multiple times in Catharus, so the species mentioned above do not constitute a monophyletic clade (Outlaw et al., 2003). Like a number of other passerines (songbirds) in both the Old and New Worlds, Catharus thrushes are nocturnal migrants. Thus, some of the conclusions drawn about the migratory behavior of these species may hold true for other small migratory birds.
One of the authors (W.W.C.) has studied the migration of Catharus thrushes since the late 1960s via radio telemetry (Cochran et al., 1967; Cochran, 1972, 1987; Cochran and Kjos, 1985; Cochran and Wikelski, 2005). Prior to 1970, the smallest radio transmitters weighed approximately 2.5 grams, 8% of a 30 g bird's body weight (Cochran et al., 1967). The transmitters we currently use (Sparrow Systems, Dewey, IL) are 0.6 to 1 gram (2–3% of 30 g). While having a radio transmitter attached to the back almost certainly influences a bird's behavior to some degree (Cochran et al., 1967), Cochran (1972) found that Catharus thrushes paid little attention to transmitters and seemed to resume normal behavior within a few hours. Similarly, Powell et al. (1998) found that Wood Thrushes (Hylocichla mustelina, 53.7 g males, 51.1 g females during migration in Illinois [Roth et al., 1996]) carrying 1.6 g transmitters (approximately 4% of body weight in their study) for up to two years bred and migrated normally and did not lose mass between years, suggesting that transmitters weighing <4% of body mass have no discernable effects on small birds when attached properly. We used a different attachment method (Raim, 1978) than Powell and colleagues, but since we put a smaller transmitter (2–3% of body weight) in approximately the same location, our method should have had similar negligible effects on the birds' fitness.
Recently, Cochran and Wikelski (2005) summarized available Catharus spp. migratory behavioral data. Most of these data were obtained from spring migrant Catharus thrushes captured in mist nets at stopover areas near Champaign-Urbana, Illinois, equipped with radio transmitters, monitored until they migrated, and then followed using a radio-tracking vehicle. From these data, Cochran and Wikelski (2005) concluded that spring migrant Catharus thrushes followed simple departure rules of thumb (Fig. 1): thrushes initiated migratory flight only when the daily high temperature exceeded 21°C and only when surface wind during the departure period was less than 
10 km/hr (cf. Åkesson and Hedenström 2000). When these favorable conditions were present and a thrush was also physiologically ready (e.g., had sufficient subcutaneous fat, Table 1), it departed on a migratory flight that continued until morning twilight, unless terminated earlier when a cold front or adverse weather was encountered or when energy reserves built up during stopover were depleted (Table 1). The birds then remained at the new stopover site until the above conditions favored the next flight. Presumably, this cycle would repeat until the breeding area or latitude was reached, where thrushes might switch to a different mode of movement (W.W.C., unpublished data).
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Cochran and Kjos (1985)
and Cochran (1987) found that individual Catharus thrushes maintained a nearly constant heading throughout a night's flight, but that they changed their heading slightly each night in relation to the change in perceived sunset direction (the sun sets successively further northward as one moves north in latitude, Fig. 1c). The suggestion that Catharus thrushes oriented by a magnetic compass calibrated each day using sunset cues was recently supported with further experiments (Cochran et al., 2004). Although constant-heading behavior was overwhelmingly predominant during migratory flight, there were occasional departures from this behavior; for example, thrushes preferentially flew toward thunderstorms (Cochran and Wikelski, 2005).
Cochran and Wikelski's (2005) simulation of constant-heading flights from the Gulf of Mexico coast into Canada, with the aforementioned flight rules applied to temperature and wind data from 1965–1966 April–June weather maps, resulted in arrivals at suitable breeding habitat in Canada at approximately the same time that Swainson's thrushes arrive at these breeding areas. We here reproduce these simulation data to show isochronal lines of advance (Fig. 2).
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The simulations show a rate of northward movement similar to that recorded for the species (Stevenson, 1957
). Also, the effects of lateral wind drift, although showing day to day lateral displacements as great as ca. 400 km, tend to average out over the many flights to produce an end displacement much smaller than the largest off-heading displacements along the route. The availability of this information on basic migratory behavior is what makes Catharus thrushes ideal species in which to continue investigating avian migration. Much of the recent work we have done would be impossible without, for example, being able to reasonably predict whether or not a focal bird would initiate a migratory flight on a particular night.
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THE ENERGETICS OF MIGRATION |
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Prior to biotelemetry, the migration energetics of Swainson's thrushes and other small passerines could not be measured directly and had to be estimated (e.g., Odum et al., 1961
; Raveling and LeFebvre, 1967). Using biotelemetry, Wikelski et al. (2003) quantified the energy expenditure of three Hermit and three Swainson's Thrushes during their nocturnal migratory flights and of 7 Hermit and 19 Swainson's Thrushes during stopover using doubly-labeled water (Fig. 3). For this, individual thrushes were injected <18 hours prior to a nocturnal flight, followed during a flight, and then recaptured in their new stopover habitats dozens to hundreds of kilometers away. Using theoretical optimal migration models, Hedenström and Alerstam (1997) predicted that, in total, birds should use twice as much energy during stopovers than they do during migratory flight; flight is costlier in terms of energy on a per-time basis, but birds spend much more time foraging during migration than they do flying. Wikelski et al.'s (2003) data confirmed this relationship: if conditions in Illinois in 2001 were similar to the average conditions experienced by the thrushes during the 2001 spring migration, approximately 29% of the total energy these birds used during spring migration was spent on flight; the remaining 71% was spent on stopover behavior, including foraging and thermoregulation.
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Surprisingly, the rate of energy expenditure during migratory flight was lower than is generally assumed (cf., Utter and LeFebvre, 1970
)—4–5 times resting metabolic rate rather than 8–12 times resting metabolic rate. As a result, Catharus thrushes that migrated for 2–3 hr expended approximately the same amount of energy per day as birds that did not migrate on days with low average temperatures. Thus, a short migratory flight on a cold night may be less costly than remaining and thermoregulating at that location (Wikelski et al., 2003). However, with few exceptions, birds did not appear to take advantage of this fact: during spring migration thrushes were less likely to initiate migratory flights when it was cold (Fig. 1, Cochran and Wikelski, 2005; W.W. Cochran, unpublished data).
The results of studies that estimate energy expenditure during natural migratory flight (e.g., Butler et al., 1998; Wikelski et al., 2003) are only the beginning of a thorough understanding of avian in-flight migratory physiology and need to be supplemented with both larger sample sizes and different species to permit generalizations to be made. Our study would not have been possible without the ability to continuously monitor small birds via biotelemetry before and during migratory flights and to recapture individuals after migratory flights.
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PHYSIOLOGICAL TELEMETRY: A NEW METHOD TO STUDY IN-FLIGHT BEHAVIOR AND ENERGETICS IN SMALL SONGBIRDS |
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While the doubly-labeled water method can provide valuable insights into energy expenditure during migration, it has a number of limitations (e.g., Nagy, 1980
; Butler et al., 2004). In particular, unexplained variance in the measurements makes it impossible to correlate estimates of energy expenditure with individual-level traits. Furthermore, doubly-labeled water per se (without behavioral observations) cannot provide information on short-term changes in energy use, as it integrates energy use over the entire measurement period. Finally, animals must be recaptured so a blood sample can be taken at the conclusion of the experiment. Even with the added advantage of having radio transmitters on a bird, it can occasionally prove difficult or impossible to recapture them, particularly if birds cross large lakes or international borders during a migratory flight (Wikelski et al., 2003).
Alternatively, one can estimate the energy use of birds using the heart rate method which, while not without shortcomings, is more useful for work on small free-flying birds in the wild. The heart rate method has been used to measure energy expenditure during flight in larger birds such as gulls, albatrosses, and geese (e.g., Kanwisher et al., 1978; Bevan et al., 1995; Ward et al., 2002), but recently also in small birds such as the 17 g Spotted Antbird (Hylophylax naevioides) from the rainforest in Panama (Steiger et al., in review). Cochran and Wikelski (2005) developed a heart rate transmitter that weighs as little as 0.6 grams for use with Catharus thrushes. The devices (Sparrow Systems, Dewey, Illinois) transmit a continuous signal amplitude modulated (AM) by an approximately 1,800 Hz sub-carrier oscillator. The 1,800 Hz subcarrier is frequency modulated (FM) by heart and respiration muscle potentials from electrodes placed just under the skin and by up-down movement of the transmitter and its attached 9 cm antenna as the bird beats its wings. The subcarrier, from the receiver audio output, was recorded on a DAT tape recorder (Sony digital audio tape-corder, model TCD-D7) and later converted to a computer sound file. The FM modulation was recovered from the sound file by a program that detected zero crossings, converted them into corresponding frequencies, and saved the result to a final sound file viewable with a spectrum analysis program or processed by an autocorrelation program written for the purpose. The latter program enabled the many hours of heart and wingbeat frequencies to be extracted in temporal detail (1 second resolution) with little manual effort.
Heart rate can be used to measure energy expenditure because it is proportional to oxygen consumption, although not directly. The oxygen consumption of a vertebrate also depends on the stroke volume of the heart and the difference in the oxygenation levels of incoming and outgoing blood (collectively termed the oxygen pulse). Previous studies have shown that these variables are largely constant for a species performing a given activity (see Butler et al., 2004; and references therein). Thus, a species- and activity-specific correlation of energy use (measured via respirometry or doubly-labeled water) and heart rate can be used to calculate a bird's energy expenditure from its heart rate. Temporal resolution of energy use estimates can then in principle be as fine as a few seconds (but see Butler et al., 2004 for cautionary notes), whereas resolution of doubly-labeled water estimates are a matter of >6 hours or one to two days for small birds.
Cochran and Wikelski (2005) performed a preliminary calibration between heart rate and oxygen consumption on resting Swainson's Thrushes. Using this calibration to predict energy expenditure from the heart rate of flying thrushes yields values lower than those obtained by Wikelski et al. (2003). This indicates that the thrushes increase their oxygen pulse while flying, and underscores the need for activity-specific calibrations when measuring energy consumption with the heart rate method (sensu Ward et al., 2002).
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INDIVIDUAL ENERGY USE DURING MIGRATION |
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We used the heart rate transmitters to examine the heart rate and wingbeat frequency of 12 Swainson's Thrushes during spring migratory flights. Figure 4 shows these variables (plus respiration rate) for one thrush during a 4.5-hour flight from Champaign-Urbana, Illinois to Rockford, Illinois. The pattern shown in Figure 4 is a general one: The heart rate of the thrushes (and thus, presumably, their energy expenditure) increased dramatically at take-off relative to pre-flight levels, decreased rapidly for a time, and then remained more or less constant or slowly decreased for several hours (depending on the length of the flight). During descent, the heart rate of this bird and that of two others we were able to obtain data for during the last few minutes prior to landing decreased sharply for a few minutes before increasing right before the thrushes landed. Average heart rate during the presumed ascent portion of the flights (as indicated by changes in both heart rate and groundspeed) was significantly higher (paired two-tailed t-test, t9 = 6.96, P < 0.001, n = 10) than average heart rate during the cruise portion of the flights (the period after presumed ascent but prior to descent). Wingbeat frequency was also higher during ascent (paired two-tailed t-test, t8 = 12.32, P < 0.001, n = 9) (Fig. 5). Despite the general correlation between wingbeat frequency and heart rate (Fig. 4), we found many short-term changes in each of these that were not mirrored by the other. These and other exceptions to the general correlations that appear in temporal detail are currently under investigation (Bowlin et al., unpublished data; Cochran et al., unpublished data). We hypothesize that the within-individual variation in wingbeat frequency and heart rate (and most likely, energy expenditure) reflected changes in the bird's flying effort as it gained or lost altitude as well as physiological changes, possibly due to changes in metabolic substrate (switching from using carbohydrates as the primary fuel to using fat, for example).
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Figure 6a shows typical examples of patterns seen in wingbeat frequency during daytime (foraging) flights as well as takeoff, cruising and landing during migratory flight. During daytime flights, both amplitude and frequency of wingbeats varied within the few seconds duration of such flights and wingbeats were often interspersed with pauses. During takeoff, both frequency and amplitude were very high with no pausing (Fig. 6a, second line). Once the Swainson's thrushes began cruising flight, wingbeats were of lower amplitude at lowered frequencies with few or no pauses (Fig. 6a, third line). Once the Swainson's thrushes got into cruising flight, they used a low amplitude but high frequency wingbeat with few or no pauses. Towards the end of long flights (Fig. 6b), periods with wingbeat pauses became more frequent with flap-pause ratios sometimes dropping to 3:1 (Fig. 6a, fourth line; contrary to Diehl and Larkin, 1998
who suggested Swainson's thrushes do not pause during migratory flight). During the landing phase (Fig. 6c), pauses and wingbeat frequency increased and wingbeats became shallow. Several recurring patterns of wingbeat frequency during long flights are yet unexplained (Diehl and Larkin, 1998). For example, in many thrushes we found a periodic increase and decrease of wingbeat frequency between about 10 to 11 Hz on a time scale of about 30 minutes (Fig. 6b). Similarly unexplained is the relationship between wingbeat frequency and wingbeat pauses. Fig. 6c highlights a typical example of a landing phase after a long (670 minute) flight. Wingbeat frequency increased in a rhythmic pattern about 15 minutes before the end of the flight, whereas wingbeat pauses increased in frequency about 30 minutes before the thrush landed. Shortly before landing, about every second wingbeat was skipped. We suggest that such patterns likely have biological and/or aerodynamic relevance and can now be investigated further with the help of biotelemetry. Similarly, heart rate, wingbeat frequency, and respiration of birds flying in wind tunnels can now be compared to that of birds migrating in the wild.
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Tolksdorf (2003)
found that the heart rate of a Swainson's Thrush flying in a German wind tunnel declined during the first hour of two separate six-hour flights (Fig. 7). Nachtigall (1990) observed similar declines in metabolic rate in pigeons flying for >3 hours in a wind tunnel. His pigeons first metabolized primarily carbohydrates, then gradually switched to fat reserves. In general, as in Fig. 7, the declines in heart rates following the periods of ascent were larger and steeper in naturally-migrating Swainson's thrushes than in the two wind-tunnel flights. The more pronounced declines in naturally-migrating birds suggest that even if they were changing their metabolic substrate in the wild, they had to expend additional energy (relative to level flight) to gain altitude.
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The reason why the thrushes increased their heart rate just prior to landing is unknown. It is unlikely that such large changes would be due to the effects of variation in altitudinal air density on flight performance. Air density at the birds' flight altitude (hundreds to possibly two thousand meters over IL, USA) is only marginally lower than the air density at sea level. Furthermore, the effects of air density on wingbeat frequency (presumably one of the primary determinants of energy expenditure) are predicted to scale with air density raised to the –3/8 power (Pennycuick, 1996
), further reducing the effects of an increase in air density with decreasing altitude. We postulate that the thrushes' heart rates increased just before landing as the birds changed their flight style to search for a good stopover site. Theoretical models of optimal migration strategies have generally ignored descent as it is thought to be relatively inexpensive (e.g., Hedenström and Alerstam, 1994). We suggest that these models might be re-examined in light of these results. In addition to within-individual variation in heart rate and wingbeat frequency, we have found substantial between-individual variation in average heart rate and wingbeat frequency during the cruise phase of migratory flights in Swainson's Thrushes (Fig. 8). We are currently investigating the sources of between-individual variation in heart rate and wingbeat frequency, but suspect that much of it will be explained by the atmospheric conditions birds encounter while aloft as well as various individual morphological characteristics, particularly wingloading.
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Testing aerodynamic theory
Quantitative aerodynamic theory predicts a number of effects of morphology, particularly wing shape and flight mass, on energy efficiency during steady, level flapping flight like that used during migration (e.g., Pennycuick, 1969
, 1972; Greenewalt, 1975; Norberg, 1990). For example, birds with relatively long and/or pointed wings are predicted to use less energy during migratory flight than birds with shorter and/or less pointed wings (reviewed in Lockwood et al., 1998). We can now begin to test some of the predictions of these theories using free-flying birds in their natural environment and combine atmospheric models with physiological measurements to understand behavioral decisions of birds during migration (Nathan et al. 2005).
Individual decision rules
Individual Catharus thrushes vary in their adherence to the behavioral rules described above (Fig. 1). As an example, juveniles migrating either northward or southward for their first time may respond differently to the same cues than adult birds (e.g., Perdeck, 1967). With biotelemetry, we will be able to examine the energetic consequences of individual behavior, especially the relative costs and benefits of initiating migratory flights given various weather conditions, stopover habitat quality or the bird's own energetic condition. The result should be a better understanding of why such rules have evolved. Physiological telemetry during migratory flight has great potential to contribute to our understanding of avian migratory behavior, particularly when combined with controlled wind tunnel experiments (cf., Lindström et al., 1999; Klaassen et al., 2000; Tolksdorf, 2003).
Global tracking of songbird migration from space
While it is in principle possible to follow individual birds as they migrate across the United States and Canada, it is much more difficult to determine what the thrushes do once they take off over the Gulf of Mexico, over other large ecological barriers, or when they land in inaccessible areas such as South American rainforests. Currently, we are unable to track the movements of small birds during migration beyond a few days (Cochran, 1987; Cochran et al., 2004). However, to understand the connectivity between breeding and wintering areas (Webster et al., 2002), the birds' intercontinental orientation capacities, the importance of circannual clocks and population cycles (Lawton and May, 1983), we will need to follow small birds for at least months at a time around the globe. One of the authors (M.W.) has started the "ICARUS"-Initiative (www.princeton.edu/~tracking) in collaboration with George Swenson (University of Illinois at Urbana-Champaign) and James A. Smith (NASA, Goddard Space Flight Center), aiming for the installation of a downward looking radio telescope in space, an Extraterrestrial Biological Observatory (EBO). Such a system would allow us to determine the daily locations of small (1 g) transmitters around the world with an accuracy of approximately ±1 km (Swenson et al., 2004).
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ACKNOWLEDGMENTS |
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This paper is dedicated to our late friend Ebo Gwinner who inspired much of this research and enthusiastically supported it. We are indebted to Arlo Raim for life-long help. We thank Elisa Tarlow, George Swenson, Nir Sapir, Angel Medina, Willie Cochran, Jim Cochran, Jamie Mandel and many other friends and assistants for help, support and understanding during these intensive projects. We would also like to thank the two anonymous reviewers who provided excellent feedback on a draft of this manuscript. Supported by the National Geographic Society (to MW), Princeton University (to MW) and The National Science Foundation (GB 3,155 and 6,680 to WWC).
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FOOTNOTES |
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1 From the Symposium Integrative Biology: A Symposium Honoring George A. Bartholomew presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 5–9 January 2004, at New Orleans, Louisiana.
2 Current address: 1204 W Union St., Champaign, IL 61821, USA
3 E-mail: wikelski{at}princeton.edu
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References |
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SYNOPSISINTRODUCTIONMODEL MIGRATORY ORGANISMS: NEW...THE ENERGETICS OF MIGRATIONPHYSIOLOGICAL TELEMETRY: A NEW...INDIVIDUAL ENERGY USE DURING...FUTURE DIRECTIONSReferences |
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