Migration encompasses a persistent, directed, often seasonal, redistribution of individuals beyond or between their home ranges, but is often incorrectly used to describe a wide range of other movement behaviours in several animal groups, including birds. Flamingos (Phoenicopteridae) are birds that are frequently, but not universally, classified as migratory. Nevertheless, movements performed by flamingos do not seem to match the scientific and ecological concept of migration sensu stricto. We discuss different bird movements and their correct typology. Based on available information concerning flamingo movements, we recommend that they be considered irruptive or nomadic species, and that correct classification is important to avoid wrongly interpreting these birds' ecology in the media and scientific works. Despite that they are not truly migratory, conservation action plans for flamingos still need to take into account their movement behaviour.
All major animal groups, including arthropods, fishes, mammals, birds and reptiles engage in long-distance movements (Hobson et al. 2019, Senner et al. 2020). Usually, animals move seasonally between discrete regions to avoid unfavourable climatic conditions, to find better feeding grounds, or to breed (Newton 2003, Milner-Gulland et al. 2011). Long-distance movements are commonly, but not always accurately, referred to as ‘migration’ (Dingle & Drake 2007). The term ‘migration’ evokes four different yet overlapping ideas: (1) a persistent directed movement, (2) redistribution of individuals over much greater spatial and temporal scales than during normal daily activities, (3) seasonal to-and-fro of populations between regions where conditions are alternately favourable and unfavourable, and (4) movement leading to individual redistribution within a population with a large range (Dingle & Drake 2007). These ideas mix individual movements with population-level patterns, often leading to mistakes in the characterisation of movement patterns (Dingle 2006, Dingle & Drake 2007). In recent decades, scientists have developed a more precise definition for ‘migration’ and a suite of new concepts and terms has been introduced, e.g., ‘restricted migration’, ‘dispersive behaviour’, etc. (Chapman et al. 2014, Lohmann 2018).
Birds are perhaps the most conspicuous and easily observed group of ‘migratory’ animals, especially in subtropical and temperate regions (Newton 2003). For example, >80% of bird species from temperate and high latitudes exhibit migratory behaviour (Winger et al. 2014). The orders Anseriformes (ducks, geese and swans), Charadriiformes (gulls, terns and shorebirds) and Ciconiiformes (storks and allies) include species often referred to as migratory (Alerstam 1993, Bairlein 2003). Another order frequently considered migratory is the Phoenicopteriformes (e.g. McCulloch et al. 2003, IUCN 2018, Somenzari et al. 2018, Wijesundara et al. 2018), which comprises six extant species of flamingos in three genera: Phoenicopterus, Phoeniconaias and Phoenicoparrus (Winkler et al. 2020, Gill et al. 2021). Four species occur in the Americas: Caribbean (American) Flamingo Phoenicopterus ruber, Chilean Flamingo P. chilensis, Andean Flamingo Phoenicoparrus andinus and Puna (James’s) Flamingo P. jamesi, whereas Greater Flamingo Phoenicopterus roseus and Lesser Flamingo Phoeniconaias minor occur in Eurasia and Africa (Winkler et al. 2020).
Flamingos are large, long-legged waterbirds with unique down-curved bills adapted to filter feeding, and pinkish or reddish plumage (Winkler et al. 2020). They inhabit wetlands such as shallow inland lakes, lagoons and coastal marine areas (del Hoyo 1992, Anderson 2016, Winkler et al. 2020), and move between wetlands to exploit different food resources throughout the year, but mainly in the non-breeding season (e.g. McCulloch et al. 2003, Balkiz et al. 2007, Zaccara et al. 2011). These movements have been frequently characterised as migration (McCulloch et al. 2003, Somenzari et al. 2018, Wijesundara et al. 2018). Nevertheless, movements performed by flamingos do not seem to match the scientific and ecological concept of migration (del Hoyo 1992, Béchet 2016) and various authors have proposed terms to refer to these movements. Here, we review the definitions and concepts related to migratory birds and discuss the movements of flamingos to determine if they fit the definition of migration. We also discuss the importance of this status in conservation policies.
Different concepts of bird movements
Bird movements can be divided into three general categories: station-keeping, ranging, and migration. These categories and their corresponding activities are defined based on the purpose, frequency, pattern, and temporal and spatial scales of the movements involved (Kennedy 1985, Dingle 1996). Station-keeping consists of movements performed within the animal's territory or home range to find food, shelter and mates (Dingle 1996). Home range is defined as the continuous area, usually around a home site, which an animal normally explores to find different resources (Burt 1943), sometimes defending this area against other individuals (Noble 1939, Nice 1941). Station-keeping movements have no fixed pattern in time and space; animals occasionally move from one place to another and are driven by short-term environmental and physiological stimuli like the weather or hunger (Alerstam 1993, Dingle 2006). These movements cease whenever resources are found, or the stimuli cease, e.g., when a vulture perches after locating a carcass or a male initiates courtship after finding a female (Dingle 2006). Sometimes, birds make movements driven by short-term stimuli but outside their home range, finding and colonising new environments. These are ranging movements and cease when the animal finds the resources sought, e.g. when young birds locate new territories (Jander 1975, Kennedy 1985, Dingle 1996). Ranging is therefore defined as a variety of movements that facilitate expanding and exploring a new home range or territory (Dingle & Drake 2007).
Migration stricto sensu is a more complex movement that extends beyond the home-range limits and involves physiological, behavioural and population aspects linked to long-distance displacements (Newton 2003, Rappole 2013). Variables such as day length (photoperiod) over the year and life-cycle stage (age class) may promote behavioural and physical changes that result in migratory movements (Newton 2003, Dingle 2006).
Long-distance movements in birds can be described based on four attributes: distance, time, site fidelity, and physiology (Dingle 1996, 2006, Newton 2003). The first of these is related to their scale: long-distance movements take an animal beyond its home range, as noted above (Newton 2003). For some birds, this type of movement is easily recognisable and delimited, as they cover remarkable distances during migration, whereas they usually move shorter distances within their home range, e.g., Buff-breasted Sandpiper Calidris subruficollis, which flies 7,600 km between breeding and non-breeding sites, but moves only a few km within either (Aldabe 2016). In some species, however, movements performed within the home range and so-called migratory distances are confused by a large continuous home range or by the short distances between each ‘migration’ site, like for example in Western Gull Larus occidentalis (Coulter 1975, Shaffer et al. 2017).
The second descriptor of migratory movements is periodicity and seasonality, both related to time. Migration involves a displacement from one site to another at regular time intervals, generally coinciding with the end /start of a climatic season, and that animals do so with a certain periodicity, usually annually (Newton 2003). These movements occur mainly because of environmental changes over the seasons of the year, e.g., temperature and photoperiod changes that can serve as an indication of fluctuations in food availability (Newton 2003, Dingle 2006). Persistence of movement patterns is extremely important for a species' ecology and is intrinsically related to the ecological process both in foraging and breeding areas (Newton 2010, Chapman et al. 2011). Several species of terns, e.g. Arctic Tern Sterna paradisaea, migrate every year in autumn to escape the Northern Hemisphere winter, instead spending the non-breeding period in the Southern Hemisphere and returning to their breeding sites in spring (Egevang et al. 2010). For other species, periodicity and seasonality of these movements are not fixed, with no clear pattern to their movements or a fixed timescale, like in Gouldian Finch Chloebia gouldiae and Grey-backed Sparrow-Lark Eremopterix verticalis (Dean 1997). In other cases, despite existence of a temporal pattern, the behaviour varies among populations and years, like in Snowy Owl Bubo scandiacus (Doyle et al. 2017).
Site fidelity, or philopatry, is another fundamental characteristic of true migrants. Migrant birds generally fly from a place where the environment is no longer favourable to another where they can find more food or better conditions to breed and feed offspring. They return to the original place or colony when the season and local conditions change again, making this seasonal to-and-fro movement to the same places, creating a route that is usually well established in the population and is followed rigorously between years (Ketterson & Nolan 1990, Newton 2003, Dingle 2006). Many ‘true migrants’, like Calidris subruficollis (Aldabe 2016) and Magellanic Penguin Spheniscus magellanicus (Pütz et al. 2007) possess high fidelity to breeding and non-breeding areas, but usually also pause at the same stopover sites during migration. For other species, these places tend to change between years and colonies, with no or very low site fidelity, as is the case in Cliff Swallow Petrochelidon pyrrhonota (Brown et al. 2017).
Based on the above three attributes, scientists have elaborated a typology to describe the different movements that are important to differentiate the wide variety of patterns in birds (Table 1; adapted from Newton 2010 and Cottee-Jones et al. 2015).
The final attribute used in migration definitions are the physiological changes that the individuals go through before, during and after this process (Newton 2010). Often, true migrants gain weight and change behaviour to low calorific expenditure and promote better reserve accumulation weeks before migration starts, increasing flight muscle size and adjusting their hormonal organs to migrate and breed (Price et al. 2010, Ketterson et al. 2015). Some species, e.g. White-throated Sparrow Zonotrichia albicollis, can increase their mass by 50% and reduce the time spent sleeping (Ramenofsky et al. 2017), whilst others change the size and volume of digestive organs rapidly but reversibly, e.g., Red Knot Calidris canutus (van Gils et al. 2005). The energetic reserve and sleep deprivation alter the immune system and increase the tissue repair function of the body in these birds, important during the long flight periods that can sometimes last weeks (Newton 2010, Price et al. 2010). Some also change plumage, acquiring breeding feathers that are important in disputes between competing males and courtship rituals on the nesting grounds (Holmgren & Hedenström 1990, Leu & Thompson 2002).
Typology classifying the long-distance movements by different groups of birds, with the name, the definition and examples already established in the literature. Adapted from Newton (2010) and Cottee-Jones et al. (2015).
The six flamingo species have been frequently, but not unanimously (see below), considered migratory (Espino-Barros & Baldassarre 1989, McCulloch et al. 2003, Johnson & Cézilly 2007, Sanz-Aguilar et al. 2012, Béchet 2016, Wijesundara et al. 2018). Indeed, these birds appear to possess variable types of movements that do not match the above-mentioned attributes required to be considered strictly migratory (cf. Table 1). For example, distances covered by flamingos are very variable and can vary both individually and at population level. As they can fly >700 km in a single night (Johnson & Cézilly 2007), the so-called migratory distance is very similar to daily home-range distances (Béchet 2016).
The time attribute is also questionable. Flamingos show opportunistic behaviour, moving among nearby areas in response to food availability, without clear periodicity (Brown & King 2005, Ayache et al. 2006). Some individuals never really disperse from their colonies, whereas others relocate at different periods of the year from one place to another, and may never return to their natal breeding sites (del Hoyo 1992, Sanz-Aguilar et al. 2012, Béchet 2016). Although such variation is common among flamingos, it is especially pronounced in Caribbean, Greater and Lesser Flamingos, most of whose populations occur at tropical latitudes with more stable temperatures and rainfall (Espino-Barros & Baldassarre 1989, Balkiz et al. 2007, Zaccara et al. 2011, Sanz-Aguilar et al. 2012, Behrouzi-Rad 2013, Parasharya et al. 2014, Pretorius et al. 2020). Lesser Flamingos display irregular movement patterns in Africa, with individuals flying between alkaline lakes in response to environmental variables like rain and food (McCulloch et al. 2003), each one of which has its own population but with genetic flow between them due to this ‘nomadic’ type of movement (Zaccara et al. 2011). This phenomenon occurs because of the highly unpredictable environmental characters of these places (Newton 2006) and is important for the genetic structure of Lesser Flamingo populations on the continent, with direct impacts on their conservation (Zaccara et al. 2011). However, Pretorius et al. (2020) recently evidenced that Lesser Flamingos in central-southern Africa may be ‘partial migrants’, not true nomads, as some movements followed a regular, repeated pattern between just two locations.
Movements by temperate-breeding Chilean, Andean and Puna Flamingos appear more frequent and seasonal, but are flexible and vary between colonies (Caziani et al. 2007). For these species, movements are usually elevational, from high-altitude to lower altitude habitats, rather than longitudinal /latitudinal (Caziani et al. 2007, Derlindati 2008, Romano et al. 2011, Derlindati et al. 2014). Andean and Puna Flamingos, and some Chilean Flamingos, breed at high-elevation wetlands in north-central Argentina and Chile, but move to the lowlands of Chile, Peru, Uruguay and southern Brazil in the non-breeding season (Mascitti & Bonaventura 2002, Somenzari et al. 2018). Nevertheless, some individuals that remain at their breeding sites year-round do not return to these areas for several years, e.g., the resident population of Chilean Flamingos at Lagoa do Peixe, southern Brazil (Delfino & Aldana-Ardila 2020).
At least three movement patterns have been more frequently observed in flamingos (e.g. del Hoyo 1992, Sanz-Aguilar et al. 2012, Béchet 2016): (1) some individuals within a colony do perform typical migrations, respecting the same non-breeding and colony areas; (2) others, mainly young males, occasionally abandon the original colony and join other groups along the route; and (3) some choose to remain in the non-breeding or breeding areas for prolonged periods, sometimes not migrating at all. Behaviour is thus influenced by environmental conditions, age and sex, but social dynamics between colonies seem to affect individual choices as well (Sanz-Aguilar et al. 2012, Béchet 2016). Body condition can also directly affect dispersal capacity, with birds in poorer condition staying longer in areas whilst well-conditioned birds tend to fly more within and between colonies (Barbraud et al. 2003).
Flamingos' movements are clearly versatile and cannot be described as migratory sensu stricto. Some authors tried to provide new names for this type of displacement, terming them ‘irruptive migrants’, ‘partial migratory’, ‘restricted migratory’, or ‘nomadic species’, without explicitly defining the meaning of these concepts and sometimes using specific population variables (i.e. genetic patterns of population variation) to justify their nomenclature for the species or group (Hayes et al. 1994, Caziani & Derlindati 2000, Childress et al. 2004, Caziani et al. 2007, Rendón et al. 2011, Zaccara et al. 2011, Sanz-Aguilar et al. 2012, Deville et al. 2014, Pretorius et al. 2020). In these cases, use of different nomenclature or typology, with no consensus in the current literature or with outdated definitions, have complicated a broader and more comprehensive classification of the group with potential impacts for conservation. According to the typology presented here (cf. Table 1), flamingos seem to best fit the definition of nomadic and irruptive movements: they move between places but with much variation in temporal, spatial and population-level behaviour, and no fixed pattern. Teitelbaum & Mueller (2019) even considered irruptive movements to be a form of nomadism, wherein long-distance movements are unpredictable in time and direction but punctuated by periods of residency, i.e. irruptive nomadism. Considering flamingos as irruptive, nomadic, or irruptive-nomadic (sensu Teitelbaum & Mueller 2019) species helps to correctly define their movements, thereby avoiding confusion in both scientific literature and popular media, and differentiates their movements from true migrants, such as Calidris subruficollis and Spheniscus magellanicus, which fit the specific definition of migratory movement (cf. Table 1).
The importance of classification and further discussion
Considering a species to be migratory is more than just a biological classification. Currently, the concept includes an important political and practical side. Migratory species are protected by laws in many countries and continents (Runge et al. 2015b). There is also an international effort to protect these species and their habitats, as the effectiveness of conservation policies is low if countries that a species uses both for breeding and feeding do not work together (Dunn et al. 2019, Xu et al. 2019). The main global mechanism for the conservation of migrant species, the Convention on the Conservation of Migratory Species of Wild Animals (CMS), an international treaty signed by 108 different countries, prohibits the capture and apprehension of endangered species, including many migratory birds, and seeks to conserve their habitats. The treaty also regulates that the parties must seek agreements for conservation of migratory species, including less threatened taxa, and work at a continental level (CMS 1979).
Four species of flamingo are currently included in the CMS: James's and Andean Flamingos are protected by the convention itself, both being covered by a high-priority conservation act in South America to protect their colonies and habitats (CMS 1979, 2008). Lesser Flamingo has a single-species action plan for conservation that unites many African countries (Childress et al. 2008) whilst Greater Flamingo is protected under the African–Eurasian Waterbird Agreement (AEWA) (EU 2006). The other species, Chilean and American Flamingos, are not directly covered by any international agreement or treaty, despite their presence across country borders and in habitats subject to great human impact (Caziani et al. 2007, Derlindati 2008, Derlindati et al. 2014, Rose 2020). However, all flamingos are listed in Appendix II of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES 1963, 2021).
Although we argue that flamingos are not truly migratory, we support the various efforts to protect these species and their habitats in many countries. Their classification as irruptive or nomadic seeks merely to correctly identify and define their movements, and should not be taken as an argument to question their inclusion in agreements covering the conservation of migratory species. This classification is only in the biological and theoretical field, and should not affect efforts to monitor and protect flamingos. In fact, we support expanding protection programmes to other species that do not perform migration sensu stricto. Correctly defining different behaviours helps fulfil the movement shortfall in conservation policies and scientific studies, not only for flamingos but for other species with a similar movement pattern (Cottee-Jones et al. 2015). Flamingos, despite being geographically very widespread and popular, are impacted by many anthropogenic threats, such as pollution of lakes, human use of water, habitat destruction, tourism, and fishing near breeding sites, among others (Ugarte-Nuñes & Mosaurieta-Echegaray 2000, Moreno-Opo et al. 2012, Kumar & Rana 2021). Therefore, an international effort is needed to conserve these species and more studies are needed to better identify the many different and complex movements and displacement strategies of these birds, as well as to expand conservation efforts to include species that might not be considered strictly migratory but do frequent several sites across various international borders.
We thank our referees Felicity Arengo and Ignacio Barberis for carefully reading the manuscript and for their helpful comments. Our studies were supported by the Coordenação de Pessoal de Nível Superior (CAPES), Brazil.