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Going wild: what a global small-animal tracking system could do for experimental biologists

Going wild: what a global small-animal tracking system could do for experimental biologists The Journal of Experimental Biology 210, 181-186 Published by The Company of Biologists 2007 doi:10.1242/jeb.02629 Commentary Going wild: what a global small-animal tracking system could do for experimental biologists 1, 2 3 4 5 Martin Wikelski *, Roland W. Kays , N. Jeremy Kasdin , Kasper Thorup , James A. Smith and George W. Swenson, Jr 1 2 Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544, USA, Mammal Lab, New York State Museum, CEC 3140, Albany, NY 12230, USA, Department of Mechanical and Aerospace Engineering, Princeton University, Princeton, NJ 08544, USA, Copenhagen Bird Ringing Centre, Zoological Museum, University of Copenhagen, DK-2100 Denmark, Goddard Space Flight Center, NASA, Greenbelt, MD 20771, USA and Department of Electrical and Computer Engineering and Department of Astronomy, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA *Author for correspondence (e-mail: wikelski@princeton.edu) Accepted 26 October 2006 Summary Tracking animals over large temporal and spatial scales extinctions and invasions. Experimental biologists may find has revealed invaluable and spectacular biological a global small-animal tracking system helpful in testing, information, particularly when the paths and fates of validating and expanding laboratory-derived discoveries in individuals can be monitored on a global scale. However, wild, natural populations. We suggest that the relatively only large animals (greater than ~300·g) currently can be modest investment into a global small-animal tracking followed globally because of power and size constraints on system will pay off by providing unprecedented insights the tracking devices. And yet the vast majority of animals is into both basic and applied nature. small. Tracking small animals is important because they Tracking small animals over large spatial and temporal are often part of evolutionary and ecological experiments, scales could prove to be one of the most powerful they provide important ecosystem services and they are of techniques of the early 21st century, offering potential conservation concern or pose harm to human health. Here, solutions to a wide range of biological and societal we propose a small-animal satellite tracking system that questions that date back two millennia to the Greek would enable the global monitoring of animals down to the philosopher Aristotle’s enigma about songbird migration. size of the smallest birds, mammals (bats), marine life and Several of the more recent Grand Challenges in eventually large insects. To create the scientific framework Environmental Sciences, such as the regulation and necessary for such a global project, we formed the ICARUS functional consequences of biological diversity or the initiative (www.IcarusInitiative.org), the International surveillance of the population ecology of zoonotic hosts, Cooperation for Animal Research Using Space. ICARUS pathogens or vectors, could also be addressed by a global also highlights how small-animal tracking could address small-animal tracking system. some of the ‘Grand Challenges in Environmental Sciences’ Our discussion is intended to contribute to an emerging identified by the US National Academy of Sciences, such as groundswell of scientific support to make such a new the spread of infectious diseases or the relationship between technological system happen. biological diversity and ecosystem functioning. Small- animal tracking would allow the quantitative assessment of Key words: small animal, ICARUS initiative, migration pattern, dispersal and migration in natural populations and thus migratory bird orientation, satellite, field experiments, tracking help solve enigmas regarding population dynamics, technology, telemetry, songbird, bat, insect. abundant birds and have a breeding population in excess of Applications of a global small animal tracking system Songbird movements as an example 1.5·billion. Single colonies can contain up to 30·million birds Imagine tracking the individual movements of red-billed and these large individual colonies can destroy up to 5% of queleas (Quelea quelea) across the African continent (Ward, grain crops in the Sahel zone of Africa (Bruggers and Elliott, 1971; Dallimer and Jones, 2002). Queleas are the world’s most 1989). Queleas can migrate long distances, sometimes more THE JOURNAL OF EXPERIMENTAL BIOLOGY 182 M. Wikelski and others than 2000·km, to seek appropriate breeding areas or to avoid validate lab-derived hypotheses and to generate new food shortage (Ward, 1971). Beyond the obvious applied hypotheses about physiological, behavioral and life-history benefit of planning for human health emergencies such as adaptations of animals that cannot be expressed in a laboratory widespread famines in the present and projected paths of these setting (Bartholomew, 1986). Invaluable progress will be made ‘feathered locusts’ (Manikowski, 1988; Malthus, 1995; Mullie in integrative and experimental biology once we are able to et al., 1999), researchers could also test whether our track the whereabouts of small animals across the globe mechanistic, lab-derived understanding of migratory drivers (Lawton and May, 1983; National Academy of Sciences, truly reflects migratory decisions of individuals that join the 2001). For example, lab-based findings demonstrate that swarming herds in fields and deserts (Marshall and Disney, navigation in laboratory conditions is altered or impaired by 1956; Desdisney et al., 1959; Wolfson and Winchester, 1959; hippocampal lesions (Sherry and Vaccarino, 1989; Strasser and Jones and Ward, 1976). Although it remains unclear whether a Bingman, 1997) and that trigeminal nerve section prevents mechanistic knowledge of quelea movement would enable pigeons from sensing the magnetic field. However, studies on agricultural managers to prevent major devastations from the free-flying birds show that in both cases pigeons are outset (Manikowski, 1988), tracking individuals might at least nevertheless able to home (Gagliardo et al., 1999; Gagliardo et allow for a predictive forecast of pattern, similar to a tornado al., 2006). Furthermore, whatever the magnetic manipulation or hurricane warning system (Malthus, 1995). imposed on pigeons, only vanishing bearings are affected; the pigeons are always able to home (Wallraff, 1999). In the field of migratory bird orientation, Perdeck’s classic field The power of combined laboratory and field experiments experiment testing songbird orientation mechanisms in nature In general, we suggest that a true understanding of natural (Perdeck, 1958) is still cited as providing unparalleled insight phenomena, and the attendant applications that such an into changes in orientation mechanisms between young and understanding enables, hinges upon our ability to translate and adult birds. Furthermore, Muheim et al.’s review (Muheim et test mechanistic, laboratory-based findings in the real world al., 2006) suggests that a field-based test of cue-conflicts during (Table·1). Ideally, previous lab-based experiments conducted songbird orientation (Cochran et al., 2004) provided data that under controlled conditions would be repeated in the wild to helped resolve long-standing disputes over results of lab-based Table·1. Examples of studies using a system for tracking small animals from space that could greatly enhance existing knowledge Scientific question Basis of current knowledge Possibilities in the ICARUS project Experimental approaches The migratory orientation program Simple experiment using ring recoveries of New model species (marsh warbler, in birds displaced common starlings(Perdeck, 1958) Swainson’s thrush). Has been tried on larger species Cue use in orientation of migratory With few exceptions (e.g. Cochran et al., 2004), Certainty of studying the behavior at large birds decades of orientation tests in Emlen funnels scales in the wild on many continents Non-experimental approaches Basic migration patterns, e.g.route Band recoveries and observations Identifying wintering areas for endangered and wintering areas of long- species, e.g.aquatic warbler ranging animals Dispersal Observations of dispersal distances or recaptures Unbiased tracking of dispersal movements of marked individuals, both of which are typically spatially biased Mortality Mortality at different parts of the life cycle are Spatially unbiased quantification of deaths extremely difficult to obtain in populations at different stages of the life cycle, i.e. where individuals cannot be followed on migration and in wintering areas Maximum flight distance Mostly based on wind tunnel studies and theory Observations of migrations by wild birds suggest that much longer distances than the ones estimated from tunnel studies are possible Effects of climate and land use Observations The detailed paths obtained will make it changes on migration patterns possible to measure these effects in real time Direct tracking of radio-tagged seeds Seed dispersal Genetic and morphological studies around the world THE JOURNAL OF EXPERIMENTAL BIOLOGY 10 000 000 1000 000 100 000 10 000 A global tracking system for small animals 183 orientation studies. Given this clear importance of tracking be observed. Similarly, for many experimental studies, large small migrating animals, it is remarkable that even after a animals are not ideally suited as they are either endangered and century of songbird migration research, one 6-day track of a protected, not numerous enough, again too long-lived or simply single Swainson’s thrush (Catharus ustulatus) conducted too difficult to keep in any numbers to study selection on 32·years ago (in 1973) by Bill Cochran (Cochran, 1987) remains certain traits. our globally best data set describing the individual decisions of The most limiting factor of modern satellite tracking an estimated forty billion songbirds migrating annually among methods is the size of the tag. The smallest commercially continents. All other data on individual songbird migration are available satellite transmitter in 2006 (9.5·g; limited to one or two nights of migratory flight (Cochran et al., www.microwavetelemetry.com) is still too large for ~81% of 2004; Diehl and Larkin, 1998; Wikelski et al., 2003; Cochran all bird species [6106 bird species of 7514 species for which and Wikelski, 2005; Bowlin et al., 2004) or banding studies body weights are available weigh less than 240·g (Bennett and connecting dots across continents (Thorup and Rahbek, 2004). Owens, 2002); following the <5% body weight rule (Murray We know even less about migration in small mammals such as and Fuller, 2000)]. Similarly, ~66.8% of the world’s mammal bats (Tuttle and Stevenson, 1977; Cryan et al., 2004). Even so, fauna cannot be tracked over long distances, i.e. from space, this lack of knowledge of individual migration pattern should again because of body weight constraints on transmitter size not conceal the fact that major progress in small-animal [Fig.·1; 3763 of 5630 species for which body weights are migration continues to be made, with spectacular insights being available (Smith et al., 2003)]. published in rapid succession (Alerstam and Hedenström, 1998; Berthold, 2001). Beyond Aristotle’s migration enigma: tracking small animals globally A global challenge for experimental biologists: dispersal We suggest here that tracking small mobile animals will and long-distance migration solve some of the longest-standing biological enigmas across a Migrating animals pose the most extreme challenge in range of disciplines and provide a much sought-after tool for animal tracking (Cochran, 1972), but even repeatedly locating experimental biologists of all fields (e.g. Pennycuick, 1969; resident study animals is rarely easy (Winkler et al., 2004). Hedenström and Alerstam, 1997; Klaassen et al., 2000). Many animal species are cryptic, shy and faster than the field Aristotle wondered about 2000·years ago where songbirds biologists chasing after them. Nevertheless, there are many disappeared to in winter (Peck, 1968). For many of the species situations in nature where this is not true, and experimental that the famous natural philosopher was concerned about, we biologists have taken advantage of this. The bonanza of are still rather ignorant – even in Europe, where scientific bird knowledge that these situations have produced illustrates the banding started more than 100·years ago (Berthold, 2001). For scientific potential of a global tracking system. The Galapagos most of the species wintering in tropical areas, our knowledge are one such example where animal dispersal is limited. The about wintering homes and migration routes is limited to less extraordinary success of Rosemary and Peter Grant’s long-term than a handful of recoveries in the presumed wintering areas investigation on Darwin’s finches (Grant and Grant, 1996) and the information contained in the recordings of observers relies on the ability to reliably relocate individuals, enabled (Thorup and Rahbek, 2004). because they work on birds living on a small, desolate crater Cannot be island 1000·km off the Pacific coast of South America. In most tracked other ‘open’ study systems, the demonstration of micro- globally evolutionary processes would have been much more equivocal. Can be tracked globally The only reliable approach for animal tracking with with ARGOS-type transmitters guaranteed global coverage and constant access is via satellite. Present satellite technology allows us to track large (>300·g) animals globally and has led to spectacular insights. Weimerskirch et al. tracked wandering albatrosses (Diomedea exulans) around the South Pole and through the Indian Ocean and related their wanderings to feeding rates and food distribution (Weimerskirch et al., 1993). Fuller and colleagues found a breeding snowy owl in Alaska one year, then in Canada and in Siberia in subsequent years (Fuller et al., 2003), Body size (g) presumably also breeding at these locations. Block and coworkers tracked bluefin tuna across the entire Atlantic and Fig.·1. The body weight distribution of the world’s mammals into the Mediterranean Sea (Block et al., 2005). Although all demonstrates that most mammals are small. Approximately 66% of of these studies are remarkable, many large animals such as the world’s mammals cannot be followed over large distances (i.e. be petrels or albatrosses may outlive their researchers (Clapp and tracked from space) because mammals smaller than ~240·g cannot Sibley, 1966) and thus do not allow for evolutionary trends to carry satellite transmitters (from Smith et al., 2003). THE JOURNAL OF EXPERIMENTAL BIOLOGY Frequency (N) 184 M. Wikelski and others Other questions for biologists that such new satellite tracking positions and they still remain too large for most animals. GPS methods could address are natal dispersal (Winkler et al., tags with a communication network to transmit data are even 2004), a mechanism critical to our understanding and modeling heavier (30·g; www.microwavetelemetry.com). Miniaturizing of animal demography (Lawton and May, 1983), cell-phone technology holds high promises but also high metapopulation dynamics (Robinson et al., 1995), life-history hurdles. The hardware and software (including >1·million lines evolution (Sillett and Holmes, 2002) and extinction (Jackson, of code) are advanced and inexpensive to purchase but very 1979; Webster et al., 2002). For example, it is unknown customized to commercial applications. It is unclear to what whether the fragmented landscapes of the North American degree a small market such as experimental biology can Midwest are population sinks for wood thrushes or whether capitalize on this technology. Furthermore, network coverage these long-distance migratory songbirds sustain healthy remains limited on a global scale and locational accuracy is low populations amidst the corn and soybean fields, despite high (Stokely, 2005). Radar technology, either passive or active, nest predation (Robinson et al., 1995). Long-term tracking over also holds many promises but, because of the immobility of large spatial scales could be used to discover when and where most radar installations, will not resolve long-distance free-ranging animals die, helping to improve our understanding migration of individuals (passive radar) (Gauthreaux and of the ecology of the different life-cycle stages that are Belser, 2003). Active radar, such as the cross-band transponder otherwise very difficult to investigate (Rubenstein et al., 2002). technology, faces similar power and detection problems as the Furthermore, the paths of birds, bats, rodents and insects ARGOS satellite tags (www.earthspan.org). carrying diseases could be followed (Rappole et al., 2000; Malkinson et al., 2002). A global solution to track small animals What is needed to address these problems is a system that can track hundreds of small animals down to the size of a 6·g All long-distance tracking problems boil down to constraints hummingbird or large insects (Naef-Daenzer et al., 2005; in the emitted signal power of animal-borne tags and the Wikelski et al., 2006) over large, continental distances and over detection of these weak signals against background noise long periods of time. Individuals should be tracked over at least (Cochran and Wikelski, 2005). These problems are not unique one entire year to solve pressing scientific and conservation to animal tracking. Another scientific discipline has already questions, such as where individuals die and what stopover addressed similar, albeit inverse, problems. As radio sites are most important (Moore and Simons, 1992; McNamara astronomers cannot increase the power emitted by distant et al., 1998; Moore, 2000; Sillett and Holmes, 2002). galaxies or control the nature of the radio emissions, they were forced to build sensitive receivers with sophisticated antennae and to develop elaborate signal processing algorithms (e.g. Why current technology is not sufficient Kraus, 1986; Thompson et al., 1986). We suggest that the best Various new technologies or combinations of already technical solution for experimental biologists involves a similar existing technologies could theoretically provide the means to solution (Cochran and Wikelski, 2005; Cochran and Wikelski, fulfill these science requirements, although each has its own 2005). Radio astronomers point antennas into space to locate series of hurdles to overcome before meeting our scientific faint radio sources against background noise tens of thousands needs. For example, to understand the connectivity between of times stronger. Wildlife biologists could point antennas breeding and wintering grounds, a combination of genetic, towards earth from near-earth orbit to locate small radio isotopic and banding studies could provide significant insights transmitters attached to animals. Radio telemetry receivers and (Rubenstein et al., 2002). However, the spatial precision of antennas mounted on satellites have global reach and are a these methods is inherently limited (Rubenstein and Hobson, natural extension of the ground and aerial radio techniques that 2004) and the actual routes that animals take during migration have been the mainstay of animal tracking for the past 45·years would remain unknown. Satellite tracking systems such as (Lord et al., 1962). Extending this space technology to ARGOS (www.argosinc.com) have produced spectacular accommodate much smaller animals than can be served by the global location data for large animals, for example albatrosses ARGOS program will have very great benefits to the study of (Weimerskirch et al., 1993). ARGOS instruments are housed dispersal and migration. on board different satellites from the US National Oceanic and The physics of this scenario has been modeled and shown to Atmospheric Administration, The Japanese Space Agency and provide a workable solution using presently available radio the European Meteorological Satellite organization. Two technology. Satellite-mounted radio receivers could track satellites are operational at any time in ~850 radio-tags with a radiated power as low as 1·mW with an ·km orbits. The accuracy of a few km under favorable conditions. 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Going wild: what a global small-animal tracking system could do for experimental biologists

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The Journal of Experimental Biology 210, 181-186 Published by The Company of Biologists 2007 doi:10.1242/jeb.02629 Commentary Going wild: what a global small-animal tracking system could do for experimental biologists 1, 2 3 4 5 Martin Wikelski *, Roland W. Kays , N. Jeremy Kasdin , Kasper Thorup , James A. Smith and George W. Swenson, Jr 1 2 Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544, USA, Mammal Lab, New York State Museum, CEC 3140, Albany, NY 12230, USA, Department of Mechanical and Aerospace Engineering, Princeton University, Princeton, NJ 08544, USA, Copenhagen Bird Ringing Centre, Zoological Museum, University of Copenhagen, DK-2100 Denmark, Goddard Space Flight Center, NASA, Greenbelt, MD 20771, USA and Department of Electrical and Computer Engineering and Department of Astronomy, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA *Author for correspondence (e-mail: wikelski@princeton.edu) Accepted 26 October 2006 Summary Tracking animals over large temporal and spatial scales extinctions and invasions. Experimental biologists may find has revealed invaluable and spectacular biological a global small-animal tracking system helpful in testing, information, particularly when the paths and fates of validating and expanding laboratory-derived discoveries in individuals can be monitored on a global scale. However, wild, natural populations. We suggest that the relatively only large animals (greater than ~300·g) currently can be modest investment into a global small-animal tracking followed globally because of power and size constraints on system will pay off by providing unprecedented insights the tracking devices. And yet the vast majority of animals is into both basic and applied nature. small. Tracking small animals is important because they Tracking small animals over large spatial and temporal are often part of evolutionary and ecological experiments, scales could prove to be one of the most powerful they provide important ecosystem services and they are of techniques of the early 21st century, offering potential conservation concern or pose harm to human health. Here, solutions to a wide range of biological and societal we propose a small-animal satellite tracking system that questions that date back two millennia to the Greek would enable the global monitoring of animals down to the philosopher Aristotle’s enigma about songbird migration. size of the smallest birds, mammals (bats), marine life and Several of the more recent Grand Challenges in eventually large insects. To create the scientific framework Environmental Sciences, such as the regulation and necessary for such a global project, we formed the ICARUS functional consequences of biological diversity or the initiative (www.IcarusInitiative.org), the International surveillance of the population ecology of zoonotic hosts, Cooperation for Animal Research Using Space. ICARUS pathogens or vectors, could also be addressed by a global also highlights how small-animal tracking could address small-animal tracking system. some of the ‘Grand Challenges in Environmental Sciences’ Our discussion is intended to contribute to an emerging identified by the US National Academy of Sciences, such as groundswell of scientific support to make such a new the spread of infectious diseases or the relationship between technological system happen. biological diversity and ecosystem functioning. Small- animal tracking would allow the quantitative assessment of Key words: small animal, ICARUS initiative, migration pattern, dispersal and migration in natural populations and thus migratory bird orientation, satellite, field experiments, tracking help solve enigmas regarding population dynamics, technology, telemetry, songbird, bat, insect. abundant birds and have a breeding population in excess of Applications of a global small animal tracking system Songbird movements as an example 1.5·billion. Single colonies can contain up to 30·million birds Imagine tracking the individual movements of red-billed and these large individual colonies can destroy up to 5% of queleas (Quelea quelea) across the African continent (Ward, grain crops in the Sahel zone of Africa (Bruggers and Elliott, 1971; Dallimer and Jones, 2002). Queleas are the world’s most 1989). Queleas can migrate long distances, sometimes more THE JOURNAL OF EXPERIMENTAL BIOLOGY 182 M. Wikelski and others than 2000·km, to seek appropriate breeding areas or to avoid validate lab-derived hypotheses and to generate new food shortage (Ward, 1971). Beyond the obvious applied hypotheses about physiological, behavioral and life-history benefit of planning for human health emergencies such as adaptations of animals that cannot be expressed in a laboratory widespread famines in the present and projected paths of these setting (Bartholomew, 1986). Invaluable progress will be made ‘feathered locusts’ (Manikowski, 1988; Malthus, 1995; Mullie in integrative and experimental biology once we are able to et al., 1999), researchers could also test whether our track the whereabouts of small animals across the globe mechanistic, lab-derived understanding of migratory drivers (Lawton and May, 1983; National Academy of Sciences, truly reflects migratory decisions of individuals that join the 2001). For example, lab-based findings demonstrate that swarming herds in fields and deserts (Marshall and Disney, navigation in laboratory conditions is altered or impaired by 1956; Desdisney et al., 1959; Wolfson and Winchester, 1959; hippocampal lesions (Sherry and Vaccarino, 1989; Strasser and Jones and Ward, 1976). Although it remains unclear whether a Bingman, 1997) and that trigeminal nerve section prevents mechanistic knowledge of quelea movement would enable pigeons from sensing the magnetic field. However, studies on agricultural managers to prevent major devastations from the free-flying birds show that in both cases pigeons are outset (Manikowski, 1988), tracking individuals might at least nevertheless able to home (Gagliardo et al., 1999; Gagliardo et allow for a predictive forecast of pattern, similar to a tornado al., 2006). Furthermore, whatever the magnetic manipulation or hurricane warning system (Malthus, 1995). imposed on pigeons, only vanishing bearings are affected; the pigeons are always able to home (Wallraff, 1999). In the field of migratory bird orientation, Perdeck’s classic field The power of combined laboratory and field experiments experiment testing songbird orientation mechanisms in nature In general, we suggest that a true understanding of natural (Perdeck, 1958) is still cited as providing unparalleled insight phenomena, and the attendant applications that such an into changes in orientation mechanisms between young and understanding enables, hinges upon our ability to translate and adult birds. Furthermore, Muheim et al.’s review (Muheim et test mechanistic, laboratory-based findings in the real world al., 2006) suggests that a field-based test of cue-conflicts during (Table·1). Ideally, previous lab-based experiments conducted songbird orientation (Cochran et al., 2004) provided data that under controlled conditions would be repeated in the wild to helped resolve long-standing disputes over results of lab-based Table·1. Examples of studies using a system for tracking small animals from space that could greatly enhance existing knowledge Scientific question Basis of current knowledge Possibilities in the ICARUS project Experimental approaches The migratory orientation program Simple experiment using ring recoveries of New model species (marsh warbler, in birds displaced common starlings(Perdeck, 1958) Swainson’s thrush). Has been tried on larger species Cue use in orientation of migratory With few exceptions (e.g. Cochran et al., 2004), Certainty of studying the behavior at large birds decades of orientation tests in Emlen funnels scales in the wild on many continents Non-experimental approaches Basic migration patterns, e.g.route Band recoveries and observations Identifying wintering areas for endangered and wintering areas of long- species, e.g.aquatic warbler ranging animals Dispersal Observations of dispersal distances or recaptures Unbiased tracking of dispersal movements of marked individuals, both of which are typically spatially biased Mortality Mortality at different parts of the life cycle are Spatially unbiased quantification of deaths extremely difficult to obtain in populations at different stages of the life cycle, i.e. where individuals cannot be followed on migration and in wintering areas Maximum flight distance Mostly based on wind tunnel studies and theory Observations of migrations by wild birds suggest that much longer distances than the ones estimated from tunnel studies are possible Effects of climate and land use Observations The detailed paths obtained will make it changes on migration patterns possible to measure these effects in real time Direct tracking of radio-tagged seeds Seed dispersal Genetic and morphological studies around the world THE JOURNAL OF EXPERIMENTAL BIOLOGY 10 000 000 1000 000 100 000 10 000 A global tracking system for small animals 183 orientation studies. Given this clear importance of tracking be observed. Similarly, for many experimental studies, large small migrating animals, it is remarkable that even after a animals are not ideally suited as they are either endangered and century of songbird migration research, one 6-day track of a protected, not numerous enough, again too long-lived or simply single Swainson’s thrush (Catharus ustulatus) conducted too difficult to keep in any numbers to study selection on 32·years ago (in 1973) by Bill Cochran (Cochran, 1987) remains certain traits. our globally best data set describing the individual decisions of The most limiting factor of modern satellite tracking an estimated forty billion songbirds migrating annually among methods is the size of the tag. The smallest commercially continents. All other data on individual songbird migration are available satellite transmitter in 2006 (9.5·g; limited to one or two nights of migratory flight (Cochran et al., www.microwavetelemetry.com) is still too large for ~81% of 2004; Diehl and Larkin, 1998; Wikelski et al., 2003; Cochran all bird species [6106 bird species of 7514 species for which and Wikelski, 2005; Bowlin et al., 2004) or banding studies body weights are available weigh less than 240·g (Bennett and connecting dots across continents (Thorup and Rahbek, 2004). Owens, 2002); following the <5% body weight rule (Murray We know even less about migration in small mammals such as and Fuller, 2000)]. Similarly, ~66.8% of the world’s mammal bats (Tuttle and Stevenson, 1977; Cryan et al., 2004). Even so, fauna cannot be tracked over long distances, i.e. from space, this lack of knowledge of individual migration pattern should again because of body weight constraints on transmitter size not conceal the fact that major progress in small-animal [Fig.·1; 3763 of 5630 species for which body weights are migration continues to be made, with spectacular insights being available (Smith et al., 2003)]. published in rapid succession (Alerstam and Hedenström, 1998; Berthold, 2001). Beyond Aristotle’s migration enigma: tracking small animals globally A global challenge for experimental biologists: dispersal We suggest here that tracking small mobile animals will and long-distance migration solve some of the longest-standing biological enigmas across a Migrating animals pose the most extreme challenge in range of disciplines and provide a much sought-after tool for animal tracking (Cochran, 1972), but even repeatedly locating experimental biologists of all fields (e.g. Pennycuick, 1969; resident study animals is rarely easy (Winkler et al., 2004). Hedenström and Alerstam, 1997; Klaassen et al., 2000). Many animal species are cryptic, shy and faster than the field Aristotle wondered about 2000·years ago where songbirds biologists chasing after them. Nevertheless, there are many disappeared to in winter (Peck, 1968). For many of the species situations in nature where this is not true, and experimental that the famous natural philosopher was concerned about, we biologists have taken advantage of this. The bonanza of are still rather ignorant – even in Europe, where scientific bird knowledge that these situations have produced illustrates the banding started more than 100·years ago (Berthold, 2001). For scientific potential of a global tracking system. The Galapagos most of the species wintering in tropical areas, our knowledge are one such example where animal dispersal is limited. The about wintering homes and migration routes is limited to less extraordinary success of Rosemary and Peter Grant’s long-term than a handful of recoveries in the presumed wintering areas investigation on Darwin’s finches (Grant and Grant, 1996) and the information contained in the recordings of observers relies on the ability to reliably relocate individuals, enabled (Thorup and Rahbek, 2004). because they work on birds living on a small, desolate crater Cannot be island 1000·km off the Pacific coast of South America. In most tracked other ‘open’ study systems, the demonstration of micro- globally evolutionary processes would have been much more equivocal. Can be tracked globally The only reliable approach for animal tracking with with ARGOS-type transmitters guaranteed global coverage and constant access is via satellite. Present satellite technology allows us to track large (>300·g) animals globally and has led to spectacular insights. Weimerskirch et al. tracked wandering albatrosses (Diomedea exulans) around the South Pole and through the Indian Ocean and related their wanderings to feeding rates and food distribution (Weimerskirch et al., 1993). Fuller and colleagues found a breeding snowy owl in Alaska one year, then in Canada and in Siberia in subsequent years (Fuller et al., 2003), Body size (g) presumably also breeding at these locations. Block and coworkers tracked bluefin tuna across the entire Atlantic and Fig.·1. The body weight distribution of the world’s mammals into the Mediterranean Sea (Block et al., 2005). Although all demonstrates that most mammals are small. Approximately 66% of of these studies are remarkable, many large animals such as the world’s mammals cannot be followed over large distances (i.e. be petrels or albatrosses may outlive their researchers (Clapp and tracked from space) because mammals smaller than ~240·g cannot Sibley, 1966) and thus do not allow for evolutionary trends to carry satellite transmitters (from Smith et al., 2003). THE JOURNAL OF EXPERIMENTAL BIOLOGY Frequency (N) 184 M. Wikelski and others Other questions for biologists that such new satellite tracking positions and they still remain too large for most animals. GPS methods could address are natal dispersal (Winkler et al., tags with a communication network to transmit data are even 2004), a mechanism critical to our understanding and modeling heavier (30·g; www.microwavetelemetry.com). Miniaturizing of animal demography (Lawton and May, 1983), cell-phone technology holds high promises but also high metapopulation dynamics (Robinson et al., 1995), life-history hurdles. The hardware and software (including >1·million lines evolution (Sillett and Holmes, 2002) and extinction (Jackson, of code) are advanced and inexpensive to purchase but very 1979; Webster et al., 2002). For example, it is unknown customized to commercial applications. It is unclear to what whether the fragmented landscapes of the North American degree a small market such as experimental biology can Midwest are population sinks for wood thrushes or whether capitalize on this technology. Furthermore, network coverage these long-distance migratory songbirds sustain healthy remains limited on a global scale and locational accuracy is low populations amidst the corn and soybean fields, despite high (Stokely, 2005). Radar technology, either passive or active, nest predation (Robinson et al., 1995). Long-term tracking over also holds many promises but, because of the immobility of large spatial scales could be used to discover when and where most radar installations, will not resolve long-distance free-ranging animals die, helping to improve our understanding migration of individuals (passive radar) (Gauthreaux and of the ecology of the different life-cycle stages that are Belser, 2003). Active radar, such as the cross-band transponder otherwise very difficult to investigate (Rubenstein et al., 2002). technology, faces similar power and detection problems as the Furthermore, the paths of birds, bats, rodents and insects ARGOS satellite tags (www.earthspan.org). carrying diseases could be followed (Rappole et al., 2000; Malkinson et al., 2002). A global solution to track small animals What is needed to address these problems is a system that can track hundreds of small animals down to the size of a 6·g All long-distance tracking problems boil down to constraints hummingbird or large insects (Naef-Daenzer et al., 2005; in the emitted signal power of animal-borne tags and the Wikelski et al., 2006) over large, continental distances and over detection of these weak signals against background noise long periods of time. Individuals should be tracked over at least (Cochran and Wikelski, 2005). These problems are not unique one entire year to solve pressing scientific and conservation to animal tracking. Another scientific discipline has already questions, such as where individuals die and what stopover addressed similar, albeit inverse, problems. As radio sites are most important (Moore and Simons, 1992; McNamara astronomers cannot increase the power emitted by distant et al., 1998; Moore, 2000; Sillett and Holmes, 2002). galaxies or control the nature of the radio emissions, they were forced to build sensitive receivers with sophisticated antennae and to develop elaborate signal processing algorithms (e.g. Why current technology is not sufficient Kraus, 1986; Thompson et al., 1986). We suggest that the best Various new technologies or combinations of already technical solution for experimental biologists involves a similar existing technologies could theoretically provide the means to solution (Cochran and Wikelski, 2005; Cochran and Wikelski, fulfill these science requirements, although each has its own 2005). Radio astronomers point antennas into space to locate series of hurdles to overcome before meeting our scientific faint radio sources against background noise tens of thousands needs. For example, to understand the connectivity between of times stronger. Wildlife biologists could point antennas breeding and wintering grounds, a combination of genetic, towards earth from near-earth orbit to locate small radio isotopic and banding studies could provide significant insights transmitters attached to animals. Radio telemetry receivers and (Rubenstein et al., 2002). However, the spatial precision of antennas mounted on satellites have global reach and are a these methods is inherently limited (Rubenstein and Hobson, natural extension of the ground and aerial radio techniques that 2004) and the actual routes that animals take during migration have been the mainstay of animal tracking for the past 45·years would remain unknown. Satellite tracking systems such as (Lord et al., 1962). Extending this space technology to ARGOS (www.argosinc.com) have produced spectacular accommodate much smaller animals than can be served by the global location data for large animals, for example albatrosses ARGOS program will have very great benefits to the study of (Weimerskirch et al., 1993). ARGOS instruments are housed dispersal and migration. on board different satellites from the US National Oceanic and The physics of this scenario has been modeled and shown to Atmospheric Administration, The Japanese Space Agency and provide a workable solution using presently available radio the European Meteorological Satellite organization. Two technology. Satellite-mounted radio receivers could track satellites are operational at any time in ~850 radio-tags with a radiated power as low as 1·mW with an ·km orbits. The accuracy of a few km under favorable conditions. 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Published: Jan 15, 2007

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