Introduction

From early observation of planets through telescopes by Galileo and Kepler, the development of time measurement methods which allowed navigation, the discovery of the elemental parts of cells through microscopes, the use of x-ray diffraction to discover DNA structure, chromatography, spectroscopy or DNA sequencing, to modern use of fast computational tools in the Internet era, technological innovations have led to exciting fast-moving developments in science. Many philosophers and science historians have long debated whether scientific advances are driven mostly by novel ideas or by new tools and, although there is no clear response to this question, no-one doubts that technology has played a fundamental role in scientific progress (Dyson, 2012).

Today, we are living in a technologydriven era of biological discovery where extremely large datasets are routinely used in biology (Ropert-Coudert and Wilson, 2005; Shade and Teal, 2015). In this sense, the fields of ecology, ethology, zoology and ultimately, ornithology, have not been unaware of these technological innovations, thus allowing the generation of large amounts of data owing to the increasingly extensive use of remote tracking technologies (Benson, in press). As happened some decades ago with genomics, proteomics, metabolomics and other “-omics”, ecology has entered the so called era of “big data” (Hampton et al., 2013). The study of animal movement, an important aspect of ecology, is no exception.

Animal movement, and particularly bird movement, has long caught the attention of naturalists and scientists since the time of Aristotle. As a consequence, there is a vast amount of information gathered across different taxa and geographic regions that has been the subject of analysis of many scientific disciplines. In order to provide a conceptual framework to integrate all this information, some scientists proposed the foundation of a new scientific discipline called “movement ecology” eight years ago (Nathan et al., 2008). As their proposers claim, the aim of the movement ecology concept is “proposing a new scientific paradigm that places movement itself as the focal theme, and promoting the development of an integrative theory of organism movement for better understanding the causes, mechanisms, patterns, and consequences of all movement phenomena” (Nathan, 2008). Accordingly, individual tracking technologies are the link between the emerging field of movement ecology and the vast body of knowledge gathered in traditional scientific disciplines.

This paper is particularly addressed to undergraduate students in their final years, to recent graduates in the fields of biology or environmental sciences and especially to young scientists wishing to start their careers in the emerging field of movement ecology. It reflects my personal point of view of the state of the art of individual-based tracking methods for birds and the most important challenges that, as a personal user, I consider we should address in the future. First, I provide a brief overview of individual tracking systems for birds. I then discuss current challenges for tracking birds with remote telemetry, including technological and scientific challenges. I also highlight future prospects for this research field including a set of scientific questions that have been answered by means of remote telemetry data or are expected to be answered in the future. Finally, I discuss some ethical aspects of animal tracking with particular focus on bird trapping, attachment methods, tag mass to body mass ratios and the behaviour of the species subject to individual tracking.

Individual tracking in Ornithology: a brief overview

Individual tracking, or simply tracking sensu lato (see Box 1), involves methodological techniques aimed at following and determining where an animal is located spatially on Earth. Individual tracking has a long tradition in ornithology, principally in the form of bird ringing (Newton, 2014). Since the first metal rings were attached to birds by Hans Christian Cornelius Mortensen in 1899, the individual identification of birds by means of metal rings and wing tags has provided many of the most significant advances in many fields of animal ecology, which reach far beyond the field of ornithology. Basically, ringing has facilitated dramatic advances in the fundamental understanding of ecology, animal behaviour, bird conservation and even evolution. Primarily focused on the fascinating study of bird migration, individual tracking of birds by using metal rings has provided valuable insight into other aspects of bird biology, such as population monitoring, population dynamics, dispersal, biometrics, breeding and moult phenology, orientation and navigation mechanisms, mating systems, genetics, territoriality, feeding behaviour, physiology, disease transmission and, more recently, the study of global climate change (Spina, 1999; Baillie, 2001; Newton, 2014; EURING, 2015; Hays et al., in press), to give a few examples. A comprehensive description of major achievements in animal ecology attributable to bird ringing is, however, beyond the scope of this paper. I would kindly ask the reader to excuse me for this omission.

For present purposes, hereafter I refer to the study of individual tracking using remote telemetry methods (Box 1). After ringing, one of the most significant advances in the study of bird movements was the development of the first radio transmitters in the late 1950s (Lemunyan et al., 1959; Cochran and Lord, 1963; White and Garrott, 1990). Due to the low cost of equipment and its basic technology, very high frequency (VHF) radio tracking has been the conventional tracking system used for decades (Kenward, 2001). Like bird ringing, conventional ground-tracking is still a very useful (and in some cases the only) system available to track small organisms, including most bird species (fig. 1). Later, one of the major advances in individual tracking was the development of the first satellite transmitters in the 1980s (Fuller et al., 1984; Jouventin and Weimerskirch, 1990; Nowak et al., 1990). Satellite transmitters allowed tracking animals remotely across the globe without the researcher needing to locate the signal (Börger, 2016). Hence, questions that so far had remained unsolved, such as where longdistance migrants spent their winters, and concerning important aspects of migratory connectivity began to be answered. With the incorporation of GPS receivers, data transmission through the Argos system and the increase of data storage and battery capacity (firstly in on-board batteries and afterward by using solar-powered rechargeable panels), satellite transmitters have definitely revolutionised the study of animal movement. Furthermore, new technological innovations such as the development of light-level geolocators, which allowed estimating geographical position by calculating the times of sunrise and sunset, were made available in the 1990s (Wilson, 1992), helping to address major research and conservation questions in avian ecology (Bridge et al., 2013). Their main advantage is that they provide a relatively lightweight, low-cost alternative to traditional tracking technologies and, consequently, have allowed significant advances in the study of small bird species (Stutchbury et al., 2009). Unfortunately, their main disadvantages are that geolocators must be retrieved to download data, and so are only useful for easily recaptured species exhibiting high site-fidelity, and that their location accuracy, ranging from 50 km up to 200 km, is low (particularly close to the Poles, the equator, and during equinoxes). Finally, archival data loggers (or dataloggers, see box 1) were first available in the late 1990s and have become more popular in recent years mainly due to their capability to incorporate new sensors along with GPS location, these including accelerometers and temperature, heart rate, conductivity or even video recording sensors (Cooke et al., 2004; Ropert-Coudert and Wilson, 2005; Tomkiewicz et al., 2010; Brown et al., 2013; Hays, 2015). This fact, combined with improved remote data download capabilities through the mobile communications GSM network and the possibility of duty cycle reconfiguration based on users' requests, has made near-real-time monitoring of animals possible. Currently available commercial dataloggers allow the collection of up to several thousand locations per day due to their high frequency of data acquisition (1 Hz = 1 location/second) and larger internal memory storage capacity. In addition, the current dataloggers also have increased accuracy of location estimation. As a consequence of these major technological improvements, many researchers claim that animal movement ecology has entered a “golden age” during which the current generation of scientists will witness unprecedented exciting discoveries (Wilcove and Wikelski, 2008; Kays et al., 2015).

Bird tracking in the context of scientific publishing

Bird movements have long held great interest for ornithologists. Consequently, the number of published papers using individualbased tracking technologies for birds has increased considerably in recent years (Holyoak et al., 2008). For example, according to a literature survey for the period 1950–2015, the first papers about satellite tracking, dataloggers, geolocators and accelerometry were published in 1990, 1991, 2002 and 2002, and have increased by an average of 42.7%, 27.7%, 79.5%, 51.5% per year in the last 25 years, respectively (fig. 2). In parallel, scientific publishing has experienced an exponential increase in the last decades (Bornmann and Mutz, 2015). However, whereas ecology papers have increased on average by 7.0% per year, those involving individual-based tracking technologies for birds have increased on average by 17.6% per year (i.e., by 2.52 times over the same period) (fig. 2). This clearly shows that modern individualbased tracking technologies have made significant contributions to many important topics in ornithology, or are expected to do so in the future (table 1), building on knowledge gained by other methods, such as ringing and conventional radio-tracking.

Fig. 1.

Histogram of bird body masses and possible tracking devices according to the 3%-body-weight rule. This figure has been adapted and updated from Bridge et al. (2011) and Kays et al. (2015). Note that body mass (g) on the X-axis is shown in log₂ scale. Bird body masses of 8,654 species were obtained from Dunning (2007).

[Histograma de los pesos corporales y posibles dispositivos de seguimiento que se pueden utilizar de acuerdo con la regla del 3% del peso corporal. La figura ha sido adaptada y actualizada a partir de Bridge et al. (2011) y Kays et al. (2015). Nótese que la masa corporal (g) en el eje X se muestra en escala log². El peso corporal de 8.654 especies de aves fue obtenido de Dunning (2007).]

Fig. 2.

Number of papers published per year referring to individual tracking systems for birds. Information is based on a literature survey by using the ISI Web of Science database. The purple line shows the number of published papers on individual tracking as a percentage of all papers published in the field of ecology. Search terms are available in Supplementary Electronic Material:  Table S2 (Art5Lopez63.1_SupplementaryMaterial).

[Número de artículos publicados por año referentes a sistemas de seguimiento individual en aves. La información fite obtenida a partir de una búsqueda bibliográfica en la base de datos del ISI Web of Science. La línea morada muestra el porcentaje de artículos publicados sobre seguimiento individual con respecto al número total de artículos publicados en el campo de la ecología. Los términos de búsqueda están disponibles en el Material Suplementario Electrónico:  Tabla S2 (Art5Lopez63.1_SupplementaryMaterial).]

Current challenges of bird tracking

Technological challenges

Since Gordon E. Moore, co-founder of Intel Corporation, stated his famous law in 1965 based on the observation that the number of transistors in a dense integrated circuit doubles approximately every two years (i.e., Moore's law) (Moore, 1965), electronic devices have undergone a dramatic miniaturisation process during the last five decades. Like mobile phones and computers, animal tracking technologies have downsized by three or four orders of magnitude, from the first radio-transmitters weighing as much as one or two kilograms to small geolocators lighter than 0.5 g (fig. 1;  Supplementary Electronic Material: table S1 (Art5Lopez63.1_SupplementaryMaterial)). Obviously, there is a trade-off between the operational life of tracking devices, maximum number locations recorded per day, temporal and spatial resolution, battery size and weight. Thus, engineers are struggling to get the most from current technologies, developing new smaller components and installing more energy-efficient microprocessors in tracking devices. For example, just a decade ago, Platform Transmitters Terminals (PTTs) attached to resident and migratory birds provided one or two locations per day based on Argos Doppler shift (e.g., Cadahia et al., 2005; Thorup et al., 2006), whereas the best Argos/GPS transmitters were able to get one fix every 2–3 hours in the most demanding duty cycle configuration (e.g., Soutullo et al., 2007, 2008; Cadahia et al., 2008). In contrast, modern dataloggers are able to provide up to one location per second (fig. 3), also including additional information from other activity sensors, and are able to send data packages through the GSM network (e.g., Lanzone et al., 2012) or by automatic downloading to a base station (e.g., Holland et al., 2009; Kays et al., 2011; Bouten et al., 2013; Pfeiffer and Meyburg, 2015).

Table 1

Main topics to which individual-based tracking methods have made significant contributions in ornithology (or are expected to do so in the future). The reference list shows some examples to illustrate addressed topics and only includes information on birds tracked by remote telemetry (examples using radio-tracking and ringing methods are not shown).

[Principales temas en los que los métodos de seguimiento individual han contribuido a realizar importantes aportaciones en ornitología (o se espera que así lo hagan en el futuro). La lista de referencias muestra algunos ejemplos para ilustrar los temas tratados e incluye información solo de aves seguidas mediante telemetría remota (se han excluido ejemplos en los que se hubiera utilizado radio-seguimiento o anillamiento científico).]

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More sensors in smaller tags

The current technological challenge is to continue shrinking transmitter size together with increasing the number of incorporated bio-logging sensors (Cooke et al., 2004; Rutz and Hays, 2009). Cutting-edge tracking devices, unlike traditional tracking methods such as metal rings or conventional radiotracking, are very expensive: from several hundred to several thousand euros. There is thus an enormous commercial market behind tracking technologies, leading companies to strive vigorously to develop ever-smaller transmitters with higher capacities at competitive prices ( see some examples in table S1 (Art5Lopez63.1_SupplementaryMaterial)). Future transmitters will have higher internal storage capacities and longer battery lifetimes (i.e., more charge/discharge cycles). In addition, it is expected that remotely downloadable dataloggers (i.e., transmitters using radio link for wireless communication) will have shorter processing times for data retrieval from multiple tags. Interesting en 2D terprises, such as the promising ICARUS project (see box 1), which is aimed at observing global migratory movements of small animals through a satellite system installed in the International Space Station (ISS), are under development (Wikelski et al., 2007). This initiative aims to revolutionise current tracking systems, mimicking conventional radio-tracking by pointing antennas towards Earth from near-Earth orbit in the ISS. This will permit radio transmitters attached to small animals, from birds to insects, to be located anywhere on Earth. The scientific community has great interest on this initiative and, although several questions still remain unanswered (e.g., how much will transmitters weigh, how much will they cost, or who will be the final users?), if it succeeds, this could facilitate a quantum leap in our knowledge of animal movement.

Fig. 3.

Example of two individual tracks of a pair of Bonelli's eagles Aquila fasciata recorded by high-resolution GPS/GSM telemetry in Spain (López-López and Urios, unpubl. data). Each point corresponds to a GPS location and shows how male (red) and female (yellow) soar together a twohour time window. For this particular study, dataloggers were programmed to record one GPS location and tri-axial accelerometer measurements (sampling rate = 33.3 Hz for each axis) every five minutes according to a basic configuration throughout the year. Furthermore, dataloggers record a GPS location every second during certain time periods of 15 minutes in length called “super busts”. As a result, high-resolution GPS telemetry is allowing in-depth analysis of the behaviour of these birds within their territory.

[Ejemplo de dos “tracks” individuales de una pareja de águilas perdiceras Aquila fasciata en España gracias a telemetría GPS/GSM de alta resolución (López-López and Urios, datos inéditos). Cada punto corresponde a una localización GPS y muestra cómo el macho (rojo) y la hembra (amarillo) ciclean juntos en una ventana temporal de dos horas. En concreto, para este estudio los dataloggers fueron programados para obtener una posición GPS y medidas del acelerómetro tri-axial (frecuencia de muestreo = 33 Hz en cada eje) cada cinco minutos de acuerdo con la programación básica para todo el año. Además, los dataloggers recogen una localización GPS cada segundo durante determinados períodos de tiempo de 15 minutos de duración denominados “super ráfagas”. De este modo, la telemetría GPS de alta resolución está permitiendo llevar a cabo un análisis en profundidad del comportamiento de estas aves en su territorio.]

Data archiving and data processing

As a result of the improved characteristics of modern dataloggers, we have jumped from recording very few locations per animal to hundreds and thousands of locations per animal and per day. Until recently, raw data were accessed and downloaded directly by users at a relatively low frequency (e.g., usually every week or every ten days from the Argos system) and could easily be stored in conventional desktop computers. However, current dataloggers, especially those transmitting information through the GSM mobile network, transmit large amounts of raw data every day (fig. 2). Hence, storage and management of extremely large datasets can be overwhelming, especially for beginners. To improve this situation, several data repositories that are freely available on the Internet allow long-term data archiving in an off-site location. In addition, these repositories provide useful services such as automatic data download from transmitters, data parsing, data managing, data analysis and environmental annotation (see Box 1). Although data repositories are freely accessible on the Internet, it is important to emphasise that researchers retain ownership of their data and can choose between different levels of data accessibility to the public (e.g., data manager, project's collaborators, public at large). One of the most popular data repositories is Movebank (Wikelski and Kays, 2015), although others such as Satellite Tracking and Analysis Tool (Coyne and Godley, 2005) were pioneers in the field and have been used since early 2000s. Therefore, I recommend using external data repositories not only for data backup but also for data sharing with other members of the scientific community and citizens at large, which is probably the most important application (see, for example, seaturtle.org and seabirdtracking.org). This facilitates participation in collaborative work to help scientists to address wider scientific questions, and also attracts public interest. Finally, the information available in public repositories is a great tool for raising public awareness of conservation problems (e.g., for migratory species) and as a teaching tool at all academic levels.

Ethical aspects

Studies using individual-based tracking systems are based on an underlying basic assumption that bird behaviours are not altered (or are insignificantly altered) by the effect of transmitters. However, this basic assumption has rarely been tested and is arbitrary to a degree (Caccamise and Hedin, 1985; Barron et al., 2010; Constantini and Møller, 2013). There is a sizable literature on the effects of transmitters on birds, yet the results are inconclusive (Murray and Fuller, 2000). Whereas some authors report negative effects on birds, with an overall negative effect on fitness components (i.e., survival and breeding) (Constantini and Møller, 2013), other researchers have not found such effects (e.g., Igual et al., 2005) and argue that the sample sizes in most studies reporting deleterious effects are low (Sergio et al., 2015). The correct selection of the type of transmitter (i.e., PTTs, dataloggers, geolocators, etc.) in combination with an appropriate method of attachment (i.e., backpack harness, collar, glue, tailmount, leg rings, leg-loop backpack harness, anchor, and even implantable transmitters that need surgery) is critical in order to reduce potentially harmful effects on bird behaviour (e.g., Vandenabeele et al., 2013; Blackburn et al., 2016).

There is a widely accepted 3–5% “rule of thumb” for the ratio of tag mass to body mass, which limits the tracking devices suitable for a given species (Brander and Cochran, 1969; Kenward, 2001) (fig. 1). However, some review studies suggest that there is no empirical support for this rule (Barron et al., 2010) and it is up to the researcher's arbitrary decision to follow the rule or not. Nowadays there is great pressure to push technologies to the limit in order to get better chances of final publication of results, and consequently some researchers succumb to the temptation of exceeding the 3–5% tag mass/body mass ratio in some cases. Nevertheless, the precautionary principle should be respected; i.e., the tracking project should not be permitted if the effects of the combination of a transmitter and method of attachment are unknown or are suspected of harmful effects in related or morphologically similar species. Hence, further research is needed to assess which tracking methods are appropriate, including not only the effects of tag mass, but also tag impact on the aerodynamics of different groups of species and the resulting possible drag effect (e.g., Pennycuick et al., 2012). Trial studies with common non-endangered species could be a good chance to check the transmitters' effects on birds under controlled conditions (e.g., using irrecoverable species in rehabilitation centres).

Finally, it would be desirable to regulate the use of individual-based tracking technologies in some way, including (for example) more stringent licensing criteria and enforcing attendance at training courses (Sergio et al., 2015). Fitting transmitters implies trapping birds, in some cases of vulnerable, rare or endangered species, and therefore a cost/benefit analysis should be done before starting a tracking project (Latham et al., 2015; Pimm et al., 2015). Trapping, handling and attaching tracking devices requires a set of skills that must be taught and constantly re-evaluated. Hence, I recommend creating special working groups, as well as open symposia and specific workshops for interested researchers. Public administration and financial entities should ask for strong ethical commitments before starting a tracking project. In addition, a scientist should clearly justify why tracking a given species is needed and should state the main goals of the project and how these goals are only achievable by using individualbased tracking technologies. Currently, the cost of transmitters is decreasing rapidly, making them more accessible to everyone. Consequently, some public administrations, NGOs, land managers, and amateur groups have found tracking birds an entertaining hobby that feeds numerous public profiles in social media (e.g., Facebook, project websites, etc.) without any intention of addressing clear questions supported by sound scientific projects. In my opinion, the simple curiosity to know where animals move does not itself justify trapping and tracking birds. Hence, collaboration among multidisciplinary groups and enhanced sharing of information should be promoted (Hampton et al., 2013; Pimm et al., 2015).

Concluding remarks

We are possibly experiencing the most productive time for the study of bird movements since the time of Aristotle. Fast-developing technologies are allowing cuttingedge studies that reveal an unprecedented level of detail about animal movements. Some have taken this opportunity to coin the term “movement ecology” as a scientific discipline in order to call attention to this emerging field. Although from my point of view movement does not itself constitute a separate scientific discipline, no-one doubts the importance of movement and its essential role in ecology and behaviour (Benson, in press). Individual tracking technologies are usually criticised for their elevated cost, which results in small sample sizes and thus a limited capacity for ecological inference (Hebblewhite and Haydon, 2010). Nevertheless, a promising future for the study of animal movement is assured by the continual improvements in current tracking technologies and the increasing number of companies commercializing remote-tracking devices. Current challenges include how to scale-up from individual fine-scale movements to coarse-scale resource selection and population-level dynamics (Hebblewhite and Haydon, 2010; Morales et al., 2010) and how to put the information derived from telemetry into the general framework of the theoretical body of ecological knowledge.

Finally, we should not forget that individual-based tracking systems are just methods and do not constitute an end in themselves (Sokolov, 2011). Trapping, handling and attaching transmitters entail disturbance (tolerable in most cases) and, accordingly, a great responsibility. Prior to starting a tracking project, researchers should carefully consider the main goals of the study, the convenience of tracking the species in question and whether remote tracking is the best methodology to this end (Latham et al., 2015). The key challenges ahead are to get the most out of data and to enhance a culture of multidisciplinary collaboration among research groups (Pimm et al., 2015). We have definitely entered a golden era in the study of animal movement and we should not miss this opportunity.