Current Biology Magazine recording of local environmental Primer past century, particularly with the parameters offer to provide advent of tracking technologies. complementary streams of extremely Conservation of However, there remains much to valuable information that will allow discover about migration. Even the researchers to obtain an increasingly migratory species movement patterns of Earth’s largest accurate picture of how migrating animal, the blue whale (Balaenoptera animals make movement decisions, musculus), remain poorly understood. 1 and to do so across species Joshua J. Horns Unfortunately, just as we are 1,2, boundaries. It is vital, therefore, that and Çag˘an H. S¸ekerciog˘lu * coming to appreciate the scale and we bring together researchers from signifi cance of animal migrations, diverse disciplines to gather and Were you to fi nd yourself somehow many migratory species are integrate the knowledge that will transported to the American Midwest experiencing substantial population prove essential if we are to conserve in the 18th century, one feature that declines as a result of habitat loss, migratory populations in the face of might strike you would be a curiously overexploitation, climate change and increasing anthropogenic pressures. shifting cloud approaching from the other anthropogenic stressors. Some northeast. As it drew closer, you might conservation strategies give hope for FURTHER READING begin to discern some sound, “[like] optimism, but far more conservation an army of horses laden with sleigh work is necessary to protect Earth’s Bazazi, S., Buhl, J., Hale, J.J., Anstey, M.L., bells” in the words of a Potawatomi great travelers. Sword, G.A., Simpson, S.J., and Couzin, I.D. (2008). Collective motion and cannibalism Native American. However, not in locust migratory bands. Curr. Biol. 18, until it was nearly upon you would The migratory lifestyle 735–739. Berdahl, A., Torney, C.J., Ioannou, C.C., Faria, J., it become apparent that this cloud Migration is a temporally repeated and Couzin, I.D. (2013). Emergent sensing was made up of billions of individual movement undertaken by part or all of complex environments by mobile animal birds. This was the autumn migration of a species’ population. It differs groups. Science 339, 574–576. Berdahl, A., Kao, A., Flack, A., Westley, P., of the passenger pigeon (Ectopistes from other forms of movement in Codling, E., Couzin, I.D., Dell, A., and Biro, D. migratorius), the most abundant bird several important aspects. Unlike (2018). Collective animal navigation and migratory culture: from theoretical models to to ever be found in North America nomadic movement patterns, empirical evidence. Philos. Trans. R. Soc. B and perhaps in the world (Figure 1). migration is repeated over a 373, 20170009. By some estimates, the number of regular time interval, at least at the Bolger, D.T., Newmark, W.D., Morrison, T.A., and Doak, D.F. (2008). The need for integrative passenger pigeons in North America population level, and is often linked approaches to understand and conserve at the time of European colonization to seasonal patterns in temperature migratory species. Ecol. Lett. 11, 63–77. Flack, A., Nagy, M., Fiedler, W., Couzin, I.D., and was greater than the combined or precipitation. Additionally, while Wikelski, M. (2018). From local collective number of all birds of all species many non-migratory species may behavior to global migratory patterns in white found on the continent today. Yet, move substantially over the course storks. Science 360, 911–914. th Guttal, V., and Couzin, I.D. (2010). Social by the beginning of the 20 century, of days or weeks within a well- interactions, information use and the evolution passenger pigeons had effectively defi ned home range, migration of collective migration. Proc. Natl. Acad. Sci. USA 107, 16172–16177. been eradicated, in large part due represents a purposeful departure Holdo, R.M., Holt, R.D., and Fryxell, J.M. (2009). to the extraordinary keenness with from an established territory. The Opposing rainfall and plant nutritional which they were hunted. By 1914, 5 abandonment of familiar surroundings gradients best explain the wildebeest migration in the Serengeti. Am. Nat. 173, billion birds were gone and the last and the greatly amplifi ed energetic 431–445. passenger pigeon, Martha, died in the cost mean that migration is often Larkin, R.P., and Szafoni, R.E. (2008). Evidence for widely dispersed birds migrating together at Cincinnati Zoo. Passenger pigeons risky and marked by higher rates of night. Int. Comp. Biol. 48, 40–49. represented an extraordinary example mortality. Milner-Gulland, E.J., Fryxell, J.M., and of one of Earth’s great natural Migratory behavior is found across Sinclair, A.R.A. (2011). Animal Migration: A Synthesis. (Oxford University Press: Oxford, phenomena: the annual migration of all types of animal and comes in a UK.) organisms. They also highlight the number of different forms. Migratory Portugal, S.J., Hubel, T.Y., Fritz, J., Heese, S., Trobe, D., Voelkl, B., Hailes, S., Wilson, A.M., potential vulnerability of migratory distances, for example, can vary and Usherwood, J.R. (2014). Upwash species. These seasonal movements enormously. The most substantial exploitation and downwash avoidance by fl ap are not only awe-inspiring; they are migration yet recorded is that of phasing in ibis formation fl ight. Nature 505, 399–402. also critical for the health of countless Arctic terns (Sterna paradisaea), Sasaki, T., and Biro, D. (2017). Cumulative culture species and ecosystems. with some individuals travelling over can emerge from collective intelligence in animal groups. Nat. Commun. 8, 15049. Human understanding of animal 80,000 kilometers in a single year. On Wilcove, D.S., and Wikelski, M. (2008). Going, migration has been developing the more modest end of the spectrum going, gone: is animal migration disappearing? remarkably slowly. As late as the is the cricket frog (Acris crepitans), PLoS Biol. 6, e188. 17th century, many hypotheses about which may venture only a dozen migration, such as the belief that meters or so from its native pond Department of Collective Behaviour, birds undertook yearly migrations to before returning to breed. Max Planck Institute for Ornithology, the moon, refl ected human creativity The number of times one individual and Department of Biology, University of Konstanz, Universitätsstraße 10, 78464 more than any empirical evidence. in a given species migrates varies Konstanz, Germany. Our understanding of migration has as well. Most avian or mammalian E-mail: [email protected] improved substantially over the migrants will travel twice per year,

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as well. In addition to ecosystem services, such as pollination and pest control, the rise of ecotourism, often with the express purpose of seeing migratory animals, has grown into a multi-billion-dollar industry. In 2008, for instance, 13 million tourists took whale-watching trips, spending a collective $2.1 billion. In many developing nations, ecotourism is the fastest growing sector of the economy. In some cases, a migratory lifestyle may help buffer a species against negative anthropogenic factors. Migratory species often have a greater dispersal capability than sedentary species and this can allow them to fi nd new habitats should their previous home range become degraded or lost altogether. For example, approximately 17% of Figure 1. A taxidermied passenger pigeon. migratory bird species are extinct, Passenger pigeons (Ectopistes migratorius) were once abundant migrant birds, but were hunted threatened or near threatened with to extinction in the early 20th century. Photo: © Jim, the Photographer/Flickr. extinction, compared to 28% for once in the spring and once in the vectors for seeds, fungal spores sedentary and resident bird species fall, and they will continue this pattern and other less mobile organisms. (Figure 2). However, migratory annually throughout their lives. Other Some species of bird consume species can face unique challenges taxa, like spawning salmon, will only higher-than-normal levels of seeds as a result of traveling. The most migrate once during their life in order during migration, and many species notable is the migrants’ reliance on to reproduce. In some migratory of plant respond by timing their multiple, often geographically distant species, no single individual will live seed production to coincide with habitats. This means successful to complete the entire journey. For bird migrations. Lindera plants in conservation of migrant species example, monarch butterfl ies (Danaus North America, for example, time must include the protection of all plexippus) in North America depart their fall fruiting to when many parts of a species’ migratory range. from the mountains of Mexico in opportunistically frugivorous birds, Some areas may only be used for February, spend the summer in the such as hermit thrushes, are passing a brief period during migration as United States and Canada, and return through. The long-distance transport a temporary resting spot to fi nd to Mexico the next winter. During this of seeds by migrating animals allows time, 3–4 generations of monarchs plants to disperse across latitudinal 0.30

will come and go, each completing ranges, helping them to cope with a 0.25 one segment of the journey before warming climate. Animal migrations producing offspring to take up the can also act to move vital nutrients 0.20 next leg in a grand international, from one habitat to another. Millions 0.15 inter-generational relay (for more on of salmon leave the ocean each year monarch migration, see the review by and travel up freshwater streams 0.10 Reppert and colleagues in this special to breed. In doing so, they act as 0.05 issue). a vitally important food source for Proportion of species extinction–prone

For many animal species, migration many upland species of animals. 0.00 All species Altitudinal Migrant Irregular Dispersal Sedentary is essential for survival. Oceanic fi sh Additionally, after the salmon spawn 11503 1122 1954 1202 742 7252 Type of long–distance movement that spawn in inland rivers hatch and die, their decaying carcasses Current Biology physiologically adapted to fresh water deposit hundreds of millions of tons and would not survive if their eggs of nutrients, which are taken up by Figure 2. Proportion of world’s bird species were laid in a marine environment. plants and invertebrates throughout extinct, threatened or near threatened with However, the conservation of the rivers and surrounding forests. extinction based on pattern of movement. migratory species is of importance More than 6000 wildebeest dying Numbers below movement types indicate total beyond the species’ own well-being. during their migration every year number of species in that group based on the Because they often travel great contribute even more biomass and taxonomy of the IOC World Bird List (www.world- birdnames.org). To compare the increases in the distances and interact with many nutrients to the Mara River. numbers and proportions of extinction-prone different habitats along the way, Many migratory species have species in the past decade, see S¸ ekerciog˘lu migrants are excellent dispersal important functions for human society (2007) Curr. Biol. 17, R283–R286.

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game will be. In addition, migration may carry a population out of a protected area and into regions where hunting pressures are far greater. Many migratory species are under extreme threat from habitat loss, particularly those that congregate in small areas. In China, thousands of Siberian cranes (Leucogeranus leucogeranus), the vast majority of the global population, spend the winter at or near Poyang Lake. Drought and water management in the region have already degraded the cranes’ critical riparian habitat, forcing them to forage in suboptimal areas. Now, a proposed dam at the outlet of the lake threatens to further diminish the quality of the restricted area these birds rely on. While habitat loss can negatively affect migratory species by Figure 3. Migrating zombie crabs. eliminating important areas on which Migrating zombie crabs (Gecarcinus ruricola) in Cuba must cross several roads during the course the animals depend, migratory of their short migrations and millions are killed each year. animals also face an additional and food and shelter. Because of this the same as for sedentary species, unique threat: the impediment of brevity, conservation of these areas especially over-exploitation, habitat movement along migratory routes. has been traditionally overlooked. loss and climate change. However, Roads, fences, dams and urban However, without these sources of the mechanisms by which these sprawl can create insurmountable food and rest, many species would be stressors imperil migrants differ obstacles for migrating animals unable to complete their epic treks. between species and they can often that are already under severe Additionally, the different habitats interact to exacerbate conservation energetic pressure as a result of that migrants require often span issues. their lifestyle. Runs of Pacifi c salmon several political entities. This means In the past, overexploitation has (Oncorhynchus sp.) are about 5% of inter-governmental cooperation is been the largest driver of wildlife loss, their historic levels due in large part an important, but often challenging, for migrants and non-migrants alike. to widespread damming of rivers aspect of migrant conservation. The Passenger pigeons, as noted earlier, in the western U.S. Similarly, crabs protection of just one population of disappeared completely in early 20th on Christmas Island and Cuba must great reed warblers (Acrocephalus century due in part to uncontrolled cross several roads during the course arundinaceus), for instance, can entail hunting. Even some extant migratory of their short migrations and millions coordinated efforts between the species are only a shadow of their are killed each year (Figure 3). This governments of at least 17 nations, former populations. Before European has been enough to cause some including Turkey, Syria, Iran, Iraq, settlers hunted their way across North breeding populations to vanish. Saudi Arabia, Yemen, Sudan, South America, there were perhaps as many Climate change is becoming Sudan, Eritrea, Ethiopia, and Somalia, as 35 million pronghorn (Antilocapra increasingly threatening. Climate and across many confl ict zones. In americana) and 50 million American change imperils migrants in a number order to address the principal threats bison in the wild. These species of different ways. First, as many faced by migratory animals, these used to make long journeys across species change their phenology hurdles of geographic distance and the prairies and served a key role in in response to a rapidly changing international coordination must be the health of prairie habitat. By the climate, mismatches in ecological overcome. In fact, the catastrophic mid 19th century, both populations synchronization are all but inevitable. level of hunting of migratory birds, had dwindled to only a few thousand For instance, pied fl ycatchers including millions of songbirds, across individuals. Today these species (Ficedula hypoleuca), which winter the Mediterranean basin, North Africa have recovered somewhat but they in sub-Saharan Africa and breed in and the Middle East is one of the no longer engage in long-distance Europe, have been unable to advance biggest threats to migratory species migration. Migratory animals are their spring migratory schedule at worldwide. at a particular disadvantage when the same pace at which their insect it comes to hunting. Because they prey have begun hatching earlier in Threats to migratory species repeatedly use the same migratory northern latitudes. The result has On a broad scale, the principal routes, it is much easier for hunters, been a dramatic decline in pied threats facing migratory animals are both legal and illegal, to predict where fl ycatcher populations.

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Likewise, warming oceans may be causing declines in populations of plankton prey on which whales and other species rely. Gray whales (Eschrichtius robustus) migrating in the eastern Pacifi c have lower than normal fat reserves, imperiling their ability to undergo such arduous treks. Climate change also has the potential to severely alter precipitation patterns, diminishing the suitability of current migratory ranges. Gazelle, wildebeest and zebra in east Africa migrate in vast numbers, with millions of individuals traveling across the savanna (Figure 4). Their movements are tied to seasonal rainfalls and resulting vegetation. If precipitation patterns change such that this seasonal productivity is much reduced, then the great African ungulate migrations may disappear. Overexploitation, habitat loss, and Figure 4. A herd of Blue Wildebeest (Connochaetes taurinus) migrating through the climate change do not act in isolation Serengeti National Park, Tanzania. Every year, nearly two million Blue Wildebeest undergo massive migrations from southern to imperil migratory species. Often, Tanzania to southern Kenya. They appear to make these movements based on seasonal pat- they synergize in catastrophic ways. terns of rainfall and subsequent plant growth. These migrations are crucial to ensure that Many species of turtle, for instance, calving mothers have enough food for their offspring but fences, roads, and other barriers to are common victims of commercial movement make these journeys increasingly diffi cult. fi shing bycatch with hundreds of thousands of individuals inadvertently through developed areas, and wildlife FURTHER READING killed each year. Those that survive overpasses allow animals to cross Bauer, S., and Hoye, B.J. (2014). Migratory still have to deal with the beaches on highways safely. In Europe, volunteer animals couple biodiversity and ecosystem which they breed being threatened organizations even help shuttle functioning worldwide. Science 344, 6179. by development and rising sea levels. migrating common toads (Bufo bufo) Horns, J.J., Buechley, E., Aktay, L., Çoban, E., Kırpık, M.A., Herman, J.M., S¸ as¸maz, Y., and The increases in energy expenditure across roads. S¸ ekerciog˘ lu, Ç.H. (2016). Geolocator tracking during migration may make species Every year, billions of organisms of great reed warbler identifi es key regions of particularly vulnerable to these take to the air, to the sea and importance to migratory wetland specialists throughout the Middle East and Sub-Saharan threats. to waving grasslands on their Africa. Condor 118, 835–849. grand migrations. They travel over Robinson, R.A., Crick, H.Q., Learmonth, J.A., Reasons for optimism mountains and across deserts, from Maclean, I., Thomas, C.D., Bairlein, F., Forchhammer, M.C., Francis, C.M., Gill, Though the overall trajectory for wetland to scrubland to tundra. Some J.A., Godley, B.J., and Harwood, J. (2009). migratory populations has been will traverse oceans, and others, small Travelling through a warming world: climate discouraging, there are some hopeful mountain ponds. An Arctic tern may change and migratory species. Endanger. Species Res. 7, 87–99. examples of conservation success. see the North Pole in July and the S¸ ekerciog˘lu, Ç.H. (2010). Partial migration in Governmental regulation banning or South Pole in January, while a single tropical birds: the frontier of movement reducing hunting has allowed many Atlantic krill in the same period will ecology. J. Anim. Ecol. 79, 933–936. Subalusky, A.L., Dutton, C.L., Rosi, E.J. and once scarce species to rebound. In travel a few hundred feet up a water Post, D.M. (2017). Annual mass drownings of th the 19 century, whales were hunted column. Animal migration ties the the Serengeti wildebeest migration infl uence to the brink of extinction. After the world together in a way that no other nutrient cycling and storage in the Mara River. International Whaling Commission natural phenomenon does. In the last Proc. Natl. Acad. Sci. USA 114, 7647–7652. Wilcove, D.S., and Wikelski, M. (2008). Going, banned commercial whaling in the few centuries, humanity has increased going, gone: is animal migration disappearing. 1980s, many species have made a both the research and admiration of PLoS Biol. 6, e188. steady, if slow, recovery. these inspiring migrations, as well as Wilcove, D.S. (2007). No Way Home – The Decline of the World’s Great Animal Migrations. (Island Protected areas may help alleviate the rate at which we are threatening Press). the pressures of habitat loss, their populations. Coordinated efforts especially when designed to help between scientists, citizens, and facilitate movement. Increasing decision-makers can reverse negative 1University of Utah, Department of Biology. effort is being placed on habitat trends in migrant species. However, 257 South 1400 East, Salt Lake City, UT 84112, USA.2College of Sciences, Koç connectivity and reducing potential continually building pressures require University, Rumelifeneri, Istanbul 34450, migratory barriers. Connected urban much greater efforts and coordination Turkey. parks permit migrants to move to preserve Earth’s migrations. *E-mail: [email protected]

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