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ABSTRACT. Altitudinal migration is the seasonal altitudinal movement of birds from breeding areas to non-breeding or wintering areas at different elevations.

J. Field Ornithol. 88(4):321–335, 2017

DOI: 10.1111/jofo.12234

Altitudinal migration by birds: a review of the literature and a comprehensive list of species Luciana Barcßante,1,3,4 Mariana M. Vale,2 and Maria Alice S. Alves3 Programa de Po s-graduacß~a o em Ecologia e Evolucß~a o, Instituto de Biologia Roberto Alcantara Gomes (IBRAG), Universidade do Estado do Rio de Janeiro (UERJ), Rua S~ a o Francisco Xavier, 524. Bairro Maracan~ a , CEP 20550-011, Rio de Janeiro, Brazil 2 Laborato rio de Vertebrados, Departamento de Ecologia, Instituto de Biologia, Universidade Federal do Rio de Janeiro (UFRJ), Ilha do Fund~a o, C.P. 68020, Rio de Janeiro, Brazil 3 Departamento de Ecologia, IBRAG, Universidade do Estado do Rio de Janeiro (UERJ), Rua S~ a o Francisco Xavier, 524. Bairro Maracan~a , CEP 20550-011, Rio de Janeiro, Brazil 1

Received 14 June 2014; accepted 17 August 2017 ABSTRACT. Altitudinal migration is the seasonal altitudinal movement of birds from breeding areas to non-breeding or wintering areas at different elevations. Although this type of migration is widely reported, questions remain concerning the number of species that perform altitudinal migration, possible variation among different taxa and geographic locations in the extent of altitudinal migration, and the foraging guilds of altitudinal migrants. We conducted an extensive bibliographic survey and compiled a list of altitudinal migrant birds worldwide. We characterized species in terms of their foraging guilds because the spatial distribution of food resources along altitudinal gradients is often evoked as a driver of bird altitudinal migration. We identified 1238 species of altitudinal migrants, ~10% of the ~10,000 extant species of birds. We found a strong geographic bias in publications focusing on avian altitudinal migration toward the United States and Costa Rica, and a paucity of studies in megadiverse regions such as the Afrotropical and Indomalayan realms, and areas in the Neotropics other than Costa Rica. We also found that most species of altitudinal migrants were invertivores rather than frugivores or nectarivores. This general pattern held true for all zoogeographic realms except the Neotropics, where nectarivores and frugivores predominated among altitudinal migrants. The prevalence of invertivore birds among altitudinal migrants is not unexpected because this is the most common foraging guild among birds worldwide. Overall, we found no prevalence of any specific foraging guild among altitudinal migrants across zoogeographic regions. The results of studies to date suggest that altitudinal migration by birds may be driven by a number of factors, including access to increased food resources for breeding or molting, weather conditions, and mating and nesting opportunities. However, to better understand the mechanisms underlying altitudinal migration, broadening the geographic scope of studies is paramount, with additional study of altitudinal migration especially needed in the megadiverse tropical regions of sub-Saharan Africa, Southeast Asia, and South America. RESUMEN. Migraci on altitudinal por aves: una revisi on de la literatura y una lista completa de especies La migracion altitudinal es el movimiento altitudinal estacional de las aves desde las areas de reproducci on a las areas no reproductivas o de invernada a diferentes elevaciones. Aunque este tipo de migracion es ampliamente reportado, quedan preguntas sobre el n umero de especies que realizan migracion altitudinal, la posible variacion entre diferentes taxones y ubicaciones geograficas en el grado de migracion altitudinal, y los gremios de forrajeo de migrantes altitudinales. Realizamos una extensa encuesta bibliografica y compilamos una lista de aves migratorias altitudinales en todo el mundo. Caracterizamos a las especies en terminos de sus gremios de forrajeo porque la distribucion espacial, y por los gradientes altitudinales, de los recursos de alimentacion muchas veces se evoca como un impulsor de la migracion altitudinal de las aves. Identificamos 1238 especies de migrantes altitudinales, ~ 10% de las ~ 10,000 especies de aves existentes. Encontramos un fuerte sesgo geografico en las publicaciones que se enfoque en la migracion altitudinal de las aves en los Estados Unidos y Costa Rica, y una escasez de estudios en regiones megadiversas como los regiones de Afrotropical e Indomalayan, y areas en el Neotropico ademas de Costa Rica. Tambien encontramos que la mayorıa de las especies de migrantes altitudinales eran invertıvoros en vez de frugıvoros o nectarıvoros. Este patron general se mantuvo para todas las regiones zoogeograficos, excepto el Neotropico, donde los nectarıvoros y frugıvoros predominaron entre los migrantes altitudinales. La prevalencia de aves invertıvoras entre los migrantes altitudinales no es inesperada, ya que es el gremio de forrajeo mas com un entre las aves en todo el mundo. En general, no encontramos prevalencia de ning un gremio de forrajeo especıfico entre todos los migrantes altitudinales en las regiones zoogeograficas. Los resultados de los estudios hasta ahora sugieren que la migracion altitudinal de las aves puede estar impulsada por una serie de factores, incluido el acceso a mayores recursos alimentarios durante la crıa o muda, las condiciones climaticas y las oportunidades de apareamiento y anidacion. Sin embargo, para comprender mejor los mecanismos subyacentes a la migracion altitudinal, es primordial a ampliar el alcance geografico de los estudios, con estudios de la migracion

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 altitudinal especialmente necesario en las regiones tropicales y megadiversas del Africa subsahariana, el sudeste asiatico y Sudamerica. Key words: bird migration, elevational movements, foraging guilds, landbird movements, short-distance migration

Migration is a common response of birds to environmental periodicity (Berthold 2001) and altitudinal migration is, for most species that exhibit such behavior, the seasonal movement of individuals in a population from non-breeding (or wintering) areas at lower elevations to breeding areas at higher elevations (Hayes 1995, Dingle and Drake 2007, Rappole 2013, but see Cade and Hoffman 1993 and Norbu et al. 2013 for examples of migration to lower elevations to breed). There is no standard terminology for bird movements between different elevations, and several terms have been used to describe these movements, including regional, altitudinal (Boyle 2010), elevational (Blake and Loiselle 2000, Katuwal et al. 2016), and vertical migration or movements (Hobson et al. 2003, Cordeiro et al. 2006). Here, we use the term altitudinal migration for the seasonal altitudinal movement of individuals from breeding areas to non-breeding or wintering areas, including both short- or long-distance movements. We do not consider high-elevation mountain crossings, such as trans-Himalayan migrations (e.g., Harter et al. 2015), to be altitudinal migration. Altitudinal migration has been reported at both temperate (e.g., Rabenold and Rabenold 1985, Laymon 1989, Boyle and Martin 2015) and tropical latitudes (e.g., Loiselle and Blake 1991, Powell and Bjork 1995, Boyle et al. 2010a,b, Norbu et al. 2013). In the tropics, altitudinal migration appears to be especially common (Blake and Loiselle 1991, Loiselle and Blake 1991, Hobson et al. 2003, Boyle 2010), and plays an important role in the seasonal distribution of birds (Fraser et al. 2008) and community structure (Loiselle and Blake 1991, Blake and Loiselle 2000). Differences in the altitudes of breeding and wintering areas vary among regions and species (Loiselle and Blake 1991, Hayes 1995, Berthold 2001, Hobson et al. 2003, Boyle 2008b, 2010), and some species may use stopover 4 Corresponding gmail.com

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sites during their altitudinal migrations (Leopold and Hess 2014). We reviewed the altitudinal migration literature with four main objectives. First, we compiled a comprehensive list of species that perform altitudinal migration to determine if there has been a taxonomic or geographic bias in the study of avian altitudinal migration. Second, we identified the foraging guilds of altitudinal migrants, given that several hypotheses proposed to explain altitudinal migration based are on access to food resources. Third, we examined the methods used to study altitudinal migrants in the field, given that different methods may target a specific portion of the bird community and, therefore, can bias our understanding of bird altitudinal migration. Finally, we summarized the different hypotheses proposed to explain altitudinal migration, discussing their generality in light of zoogeographic distributions, foraging guilds, and geographic bias in the literature on bird altitudinal migration. METHODS

We performed a bibliographic survey on the Web of Science database (Thompson Institute for Scientific Information – ISI; http://isiwebofknowledge.com), following the guidelines of Preferred Reporting Items for Systematic Reviews and Meta-Analysis – PRISMA (http://www.prisma-statement.org) for bibliographic surveys (Moher et al. 2009) (Fig. S1). We searched the database for articles published in English, Spanish, French, Portuguese, and German from January 1946 through March 2017, using a combination of the words bird, altitud*, elevat*, local, regional, short distance, slope*, vertical, migra*, and movement to search parts of titles, abstracts, or key words (see Appendix S1 for the combinations of words used). We also selected additional papers from the references cited in the papers retrieved with our systematic survey, either when the title of a paper suggested it had information about altitudinal migration, and/or the context in which the

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study was cited indicated that the paper included information about altitudinal migration. Papers were categorized based on how altitudinal migration was approached: (1) papers that mentioned or discussed altitudinal migration without naming any species, including review papers, (2) studies that mention that one or more species were altitudinal migrants without providing evidence, (3) studies or syntheses that identified that birds (either single species or communities) are altitudinal migrants and provided supporting data, and (4) studies that used known altitudinal migrants to test hypotheses about altitudinal migration. We compiled a preliminary list of species of altitudinal migrants based on our bibliographic survey. In addition, we consulted ~10,000 bird species of the world listed in the Handbook of the Birds of the World (HBW) (del Hoyo et al. 1992, 1994, 1996, 1997, 1999, 2001, 2002, 2003, 2004, 2005, 2006, 2007, 2008, 2009, 2010, 2011, 2017), searching under the heading “Movements” for species described as performing some seasonal altitudinal movement. In our final list of species of altitudinal migrants, we included species reported to be altitudinal migrants and species reported as “probably” performing altitudinal migration according to HBW or the papers we retrieved. We characterized altitudinal migrants based on their taxonomic family, zoogeographic realm of occurrence, and foraging guild. Species were assigned to all zoogeographic realms where they are known to occur based on their geographic ranges. We followed the IOC World Bird List (Gill and Donsker 2017) for taxonomy, used HBW’s information to assign species to Newton and Dale’s (2001) zoogeographic realms, and used Wilman et al.’s (2014) classification of species into five foraging guilds: (1) frugivores/nectarivores (birds that consume mainly fruits and/or nectar), (2) invertivores (birds that consume mainly invertebrates, including insects), (3) omnivores (birds that consume both animal and plant matter), (4) plantivores (birds that consume mainly plant material other than fruit or nectar, e.g., granivores and folivores), and (5) carnivores (birds that consume mainly vertebrates and/or carrion) (Appendix S2). We also gathered information about the feeding habits of different species

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of birds from the HBW (del Hoyo et al. 1992, 1994, 1996, 1997, 1999, 2001, 2002, 2003, 2004, 2005, 2006, 2007, 2008, 2009, 2010, 2011, 2017). For 10 species where Wilman et al. (2014) and the HBW placed species in different foraging guilds, we used the guild assigned by the HBW. Finally, we used a chi-square test of independence to compare the observed proportion of species in guilds among altitudinal migrant birds in each zoogeographic realm with the expected proportion, i.e., the proportions reported by Wilman et al. (2014) for birds worldwide: 0.50 invertivores, 0.17 omnivores, 0.16 frugivores/nectavirores, 0.11 plantivores, and 0.06 carnivores. RESULTS AND DISCUSSION

We compiled a list of 1238 altitudinal migrant birds, including 618 species identified in 136 scientific papers and 620 species from the HBW (Appendix S2). We also identified 291 species from the HBW that perform some type of altitudinal movement, but that were not included in our analysis because the seasonality of their movements was unclear (Appendix S2). Geographic distribution of species and studies. The 1238 species of altitudinal

migrants represented 130 families (Appendix S2). Six families had the greatest proportion of species that are altitudinal migrants and, together, these families, including Trochilidae, Muscicapidae, Fringillidae, Thraupidae, Turdidae, and Tyrannidae, comprised ~34% of all altitudinal migrants recorded. All other families had < 40 species of altitudinal migrants (Appendix S2). Most altitudinal migrants are in the Neotropical zoogeographic realm (44% of all altitudinal migrants), followed by the Palearctic (29%) and Indomalayan (29%) realms (Fig. 1, Table 1). Fewer altitudinal migrants are found in the Nearctic (16%), Afrotropical (16%), Australasian (6%), and Oceanian (< 1%) realms (Fig. 1, Table 1; because species were assigned to all zoogeographic realms where they are known to occur, these percentages add up to more than 100%). Because the number of altitudinal migrants in the Oceanian zoogeographic realm was so low (N = 10), this realm was not included in further analyses.

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Fig. 1. Distribution of (A) the number of studies reporting bird altitudinal migration and (B) foraging guilds of altitudinal migrants in different zoogeographic realms. I, invertivore birds; F/N, frugivores/nectarivores; O, omnivores; P, plantivores; and V, carnivores that consume mainly vertebrates and/or carrion. Because species were assigned to all zoogeographic realms where they are known to occur, the sum of species per realm adds up to a larger number than the 1238 altitudinal migrant species identified in our study. [Color figure can be viewed at wileyonlinelibrary.com]

We found 54 papers where investigators studied altitudinal migration in the Neotropical zoogeographical realm, with most studies conducted in Costa Rica (48%; Fig. 1A). For the Nearctic, we found 34 papers, with most studies conducted in the United States (82%). Although only seven papers focused on altitudinal migration in the Afrotropical realm, one single review paper (Johnson and Maclean 1994) documented 72 species of altitudinal migrants. Although more papers about altitudinal migration have focused on birds in the Neotropical realm than any other realm, our understanding of altitudinal migration in

South America remains limited (Alves 2007). Because the Andes are such a large mountain range with a wide range of elevations, patterns of altitudinal migration by birds in the Andes might be more complex than elsewhere (Faaborg et al. 2010). In addition, our knowledge of most species of birds in tropical regions is limited (Fig. 1A) so our estimate of the total number of species that are altitudinal migrants (1238) is probably lower than the actual number. For example, the list of 291 species we identified as exhibiting some altitudinal movement (Appendix S2) likely includes some species that are actually altitudinal migrants.

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Table 1. Comparison of the observed proportion of foraging guilds among altitudinal migrant birds in each zoogeographic realm, with the proportion found in birds worldwide, using a chi-square test of independence (df = 4).

Percent deviation from expected Zoogeographic realm Afrotropical Australasian Indomalayan Nearctic Neotropical Palearctic

N

v2

198 81 355 201 543 361

10.3 7.3 43.6 30.9 209.3 80.2

P

< < <
50% lower than expected for the Palearctic, Indomalayan, and Nearctic realms. The proportion of species of altitudinal migrants that are plantivores in these realms, however, was particularly high. A more consistent result

was the low number of altitudinal migrant carnivores across zoogeographic realms (Fig. 1B). The results of several studies suggest that frugivores and nectarivores are the main guilds of altitudinal migrant birds (Blake and Loiselle 1991, 2000, Levey and Stiles 1992, Hobson et al. 2003, Alves 2007, Boyle 2010). Our results, however, suggest that frugivores and nectarivores are not the main foraging guilds of altitudinal migrants worldwide. This apparent disagreement can be partially explained by historical contingency because an influential paper by Levey and Stiles (1992) might have convinced researchers about the logic of fruit and nectar availability as the explanation for bird altitudinal migration. In addition, most studies of altitudinal migration (including Levey and Stiles 1992) have been conducted in the Neotropics where, in fact, we found that more altitudinal migrants were frugivores and nectarivores rather than invertivores (Fig. 1B, Table 1). In Costa Rica, more than 70% of reported species of altitudinal migrants were either frugivores (~50%) or nectarivores (~25%) (Loiselle and Blake 1991, Blake and Loiselle 2000). A similar pattern was reported in Brazil, with most altitudinal migrants being frugivores and nectarivores (Sick 1997, Alves 2007). Our analysis of species occurrence by country, however, shows that frugivores and nectarivores together represent only 38% of the species of altitudinal migrants in

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Costa Rica (60 of 159 species) and 31% in Brazil (33 of 106 species) (Appendix S2). The smaller proportion of frugivores/nectarivores in our survey than reported in the literature for Costa Rica is likely due to the broader geographic scope of our study. We covered all species of birds in Costa Rica, recording 159 altitudinal migrants, whereas studies conducted at La Selva Biological Station and in the contiguous Braulio Carrillo National Park, recorded 75 and 56 altitudinal migrant species, respectively (Loiselle and Blake 1991, Blake and Loiselle 2000). We found 26 papers focusing on altitudinal migration in Costa Rica, but only three focused on altitudinal migration in Brazil (Fig. 1A) and none provided a quantitative assessment of the proportions of different foraging guilds (Alves 2007). Although we found smaller proportions of frugivores and nectarivores in Costa Rica and Brazil than previously reported in the literature, overall we found more frugivores/nectarivores in the Neotropics than expected. In the other zoogeographic realms, we found that the number of invertivores was always greater than the number of frugivores and nectarivores combined (Fig. 1B). In addition, Johnson and Maclean (1994) reported that most altitudinal migrants in South Africa were insectivores. Therefore, well-established patterns and processes known for bird altitudinal migration in the Neotropics cannot be generalized to other regions of the world. Sampling techniques. Authors of the 136 papers retrieved used various sampling techniques to record and/or evaluate altitudinal migration (Appendix S3), with direct observations (67 studies) and capture-mark-recapture (51 studies) being the most common. These techniques, however, have limitations. Direct observation, e.g., is highly dependent on a researcher’s experience, and detection probability can be hampered by vegetation and/or weather conditions (Blake and Loiselle 2000). In addition, bird captures are spatially limited (Betts et al. 2008), provide a biased survey of bird communities (Remsen and Good 1996, Blake and Loiselle 2000), and are inefficient in differentiating altitudinal migration from other bird movements or from seasonal variation in bird abundance (Fraser et al. 2008).

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Studies of animal movements require that individuals or populations be followed throughout the year (Webster et al. 2002), which may be difficult to do. However, recent technological advancements such as GPS/accelerometer tags (Norbu et al. 2013) and miniature video-loggers (Rutz and Troscianko 2013) may make it easier for investigators to monitor bird movements. Analysis of stable isotopes also holds promise for the study of bird altitudinal migration (Webster et al. 2002, Inger and Bearhop 2008, Perez et al. 2008). Although widely used in studies of animal movements, use of stable isotopes in studies of altitudinal migration has been limited (Graves et al. 2002, Hobson et al. 2003, Chang et al. 2010, Newsome et al. 2015). However, values of stable hydrogen isotope (deuterium) in the feathers, claws, and blood of birds have been used by some investigators to study altitudinal migration (Hobson et al. 2003, Fraser et al. 2008, Bridge et al. 2010, Hardesty and Fraser 2010, Boyle et al. 2011, Newsome et al. 2015, Villegas et al. 2016). Stable isotope analysis can also refine our knowledge of bird movements (Webster et al. 2002, Inger and Bearhop 2008, Perez et al. 2008) by revealing, with only one captured bird, the isotopes incorporated into the bird’s tissue and whether they come from lower or higher altitudes (Hardesty and Fraser 2010). Why do birds migrate altitudinally? We evaluated a number of variables that have been suggested as possible drivers of bird altitudinal migration. Although many studies have revealed some form of altitudinal migration by target species (88 studies), hypotheses that might explain that migration were empirically tested in only 10 studies (see Appendix S3 for references). Hypotheses most often tested have focused on (1) food resources, (2) climatic conditions, and (3) mating and nesting opportunities (Table 2). Food resources. Food resources as a driver of bird altitudinal migration have been investigated primarily in Neotropical systems (e.g., Levey and Stiles 1992). A number of related hypotheses attempt to explain bird movements to higher and lower elevations. Seasonal resource availability has frequently been proposed as the main driver of bird migration in general (Somveille et al. 2015) and as the primary explanation for seasonal

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Table 2. Variables associated with altitudinal migration by birds, with explanations of hypotheses and citations.

Variable Food resources

Climatic conditions Mating and nesting opportunities

Explanation During the breeding season, birds migrate to higher altitudes following food resources. This pattern has been reported primarily in the Neotropics (Levey 1988, Blake and Loiselle 1991, 2000, 2002, Loiselle and Blake 1991, Levey and Stiles 1992, Rosselli 1994, Solorzano et al. 2000, Kimura et al. 2001, Chaves-Campos et al. 2003, Chaves-Campos 2004, Boyle 2008b, 2010, 2011, Boyle et al. 2010a, Bridge et al. 2010, Faaborg et al. 2010). Migrant frugivorous species can explore food sources available in young and old second-growth forest in the Neotropics (Blake and Loiselle 2000). Some birds can experience limited opportunities for foraging in the highlands due to storm events. These limited opportunities for foraging are associated with poorer physical condition and, in the Neotropical realm, leads frugivorous males (that are at greater risk of mortality at high altitudes due to their smaller size) to leave breeding areas and migrate to lower elevations (Boyle 2008b, 2011, Boyle et al. 2010b). Birds migrate to higher altitudes, following food resources required for molting (Butler et al. 2002, Rohwer et al. 2008, Fraser et al. 2010). Birds migrate in response to climatic conditions. Individuals in poorer physical condition will migrate to lower elevations where extreme conditions (frequency and duration of storms) are rarer. This pattern has only been reported in the Neotropics (Boyle 2008b, 2011, Boyle et al. 2010b, 2011). Birds migrate to higher altitudes (1650–2780 m) where nest predation is lower. This pattern was found in one study in the Neotropics (Boyle 2008a). Birds that are poor competitors migrate altitudinally to areas less suitable for breeding (Gillis et al. 2008, Mackas et al. 2010). Some large male Dark-eyed Juncos remain resident in breeding areas (higher altitudes) throughout the year and compete for food, driving subordinate individuals to lower elevations (Rabenold and Rabenold 1985). Some male White-ruffed Manakins migrate to lower elevations after the breeding season to survive, causing a reduction in their social status and mating success in the next breeding season (Boyle et al. 2011).

altitudinal migration by Neotropical forest birds (Stiles 1988, Loiselle and Blake 1991, Levey and Stiles 1992), particularly species that feed on seasonally distributed resources such as flowers and fruits (Stiles 1988, Loiselle and Blake 1991). Loiselle and Blake (1991) were among the first to study bird altitudinal migration in Costa Rica, examining both the bird community and the availability of fruit along an altitudinal gradient and showing that birds migrate following seasonal and spatial fluctuations of resources. Thus, the food availability hypothesis became widely accepted and has been cited as a general explanation for altitudinal migration, especially for frugivorous and nectarivorous species of birds (e.g., Alcock 2015, Newton 2008). However, our review of the literature suggests that the predominance of frugivores

and nectarivores in the altitudinal migrant community appears to be exclusive to the Neotropics. Other investigators have suggested that competitive exclusion may explain bird altitudinal migration (Rabenold and Rabenold 1985, Loiselle and Blake 1991), with less competitive species migrating to avoid competition for food, particularly for fruit, with more competitive (non-migrating) species. Boyle et al. (2010a) tested this hypothesis in Costa Rica, comparing phylogenetically close migrating and non-migrating pairs of species. Migrant species were found to have a more frugivorous diet and were competitively superior (rather than inferior) foragers for fruit than their resident counterparts. This suggests that, at least in this system, competitive exclusion is not a satisfactory explanation for

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altitudinal migration. For other systems, however, competition for food resources remains a working hypothesis that needs to be tested. For example, Rabenold and Rabenold (1985) suggested that the partial altitudinal segregation of male and female Dark-eyed Juncos (Junco hyemalis carolinensis) in the Appalachian Mountains of the United States was likely due to competition, with males more common at higher elevations and remaining closer to breeding areas than females. In addition, larger males remained resident in breeding areas throughout the year, whereas other males migrated throughout the entire available altitudinal range. Rabenold and Rabenold (1985) suggested that individual variation in altitudinal migration behavior was influenced by social dominance in competition for food during the winter. This is consistent with the dominance hypothesis, with larger individuals dominant over smaller ones (Fretwell 1969, Ketterson and Nolan 1976) and subordinate females leaving breeding areas to avoid competition with dominant males (Balph 1975, Ketterson and Nolan 1976). The results of studies of captive Darkeyed Juncos also lend support to this dominance hypothesis (Millikan et al. 1985, Wiedenmann and Rabenold 1987). In addition to studies that explain migration to higher altitudes as a way to gain access to increased food resources for breeding, the results of some studies suggest that these movements may be associated with molting (although not explicitly linking it to energy requirements and thus availability of food resources). Migrating to higher altitudes to molt has been reported for three species of birds, including Blue-tailed Hummingbirds (Amazilia cyanura) in Nicaragua (Fraser et al. 2010), Western Tanagers (Piranga ludoviciana) in southwestern North America (Butler et al. 2002), and Cassin’s Vireos (Vireo cassinii) in the northwestern United States (Rohwer et al. 2008). Altitudinal molt migration may be common in the Neotropics, but investigators have not focused on the possible link between the energy required for molting and the phenology of food resources (Fraser et al. 2010). Climatic conditions. Although a relationship between food availability and movement of frugivorous birds to higher elevations has been well-established in the Neotropics

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(Loiselle and Blake 1991, Alcock 2015, Boyle 2010, 2011), less is known about factors responsible for migration to lower elevations. Indeed, the results of a number of studies suggest that migration to lower altitudes can only be partially explained by altitudinal variation in food availability (Kimura et al. 2001, Chaves-Campos et al. 2003, Chaves-Campos 2004), and some studies have even revealed complete asynchrony between peak fruiting periods at higher elevations and altitudinal migration to lower elevations (Rosselli 1994, Solorzano et al. 2000, Boyle 2010). Skutch (1969) suggested that adverse weather conditions in the highlands, such as long continuous storms, was a factor in migration to lower elevations among some birds in Central America. As an example, Skutch (1969) proposed that altitudinal migration by Three-wattled Bellbirds (Procnias tricarunculatus) was explained in part by altitudinal variation in availability of fruit as well as by long periods of rain in the highlands during the wettest months of the year. The possible role of weather in altitudinal migration was tested decades later in a study of White-ruffed Manakins (Corapipo altera) in Costa Rica (Boyle 2008b). Male Whiteruffed Manakins are smaller than females and also more likely to migrate to lower altitudes even though food availability is greater at higher altitudes (Boyle 2008b). Storms, however, are more frequent at higher elevations and can last for several consecutive days, potentially reducing the time available for foraging and increasing mortality risk for some individuals (Boyle 2008b, Boyle et al. 2010b). Boyle (2011) predicted that birds most likely to leave breeding areas and move to lower elevations would be the most metabolically challenged, specifically small birds with higher metabolic rates, frugivorous and nectarivorous birds that rely on food with low nutritional content, and individuals physically compromised by pathogens, molting, or reproductive stress (Boyle 2011). Boyle (2008b) found that, as expected, smaller males were more likely to migrate to lower elevations than females. In addition, the abundance of altitudinal migrant species increased in the lowlands after major storms, and resident males at high elevations exhibited greater physiological stress associated with storm events than did males in the lowlands.

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Therefore, although food is more available at higher elevations, the reduction in foraging time due to frequent storms threatens the survival of smaller individuals, promoting migration of some individuals to lower elevations. The results of a community-level study in lowland areas in the same location in Costa Rica also provided support for the link between weather and the limited foraging opportunity hypothesis (Boyle 2011). The bird community showed a positive relationship between rainfall intensity at high elevations and the abundance of altitudinal migrants in the lowlands during the wet season. This relationship was stronger for smaller species and for frugivorous and nectarivorous birds. Responses to rainfall may vary among species of altitudinal migrants, suggesting that the threshold of rainfall intensity that triggers migration is species-specific (Boyle 2011). Despite important advances in Costa Rica (Boyle et al. 2010b, Boyle 2011), the possible effect of weather on bird altitudinal migration remains a major gap in our knowledge in other parts of the world. Even the effect of temperature during the winter, an important factor influencing long-distance migration by birds (Sparks et al. 2005, Saino et al. 2007, Somveille et al. 2015), has not been examined in the context of altitudinal migration. Some investigators have suggested a link between snow at higher elevation and altitudinal migration to lower elevations, but no one has actually tested this hypothesis (King and Wales 1964, O’Neil and Parker 1978, Tomback 1978, Hendricks and Swenson 1983, Dixit et al. 2016). The general assumption is that snow represents a challenge for birds, with the results of some studies suggesting the inability to recover seeds stored in the ground as the specific mechanism (King and Wales 1964, Tomback 1978, Hendricks and Swenson 1983). In any case, predictions concerning body size and limited foraging opportunity hypotheses seem perfectly plausible for other mountainous regions of the world and should be tested to evaluate their generality. Mating and nesting opportunities. Reproduction may play a role in bird altitudinal migration, with reports of migratory movements associated with nest predation and a trade-off between survival and reproductive success in Costa Rica and competition for nesting

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sites in Canada. Some investigators have suggested that higher rates of nest predation at lower elevations might stimulate migration to higher elevations during the breeding season (Loiselle and Blake 1991, Boyle 2008a, Faaborg et al. 2010). The only experimental test of this hypothesis was conducted with artificial nests along an altitudinal gradient in Costa Rica (Boyle 2008a). In Costa Rica, frugivorous birds breed at higher elevations where food resources are more abundant. However, nest predation may strengthen this pattern. Boyle (2008a) found that the highest risk of nest predation was at intermediate elevations (500–650 m), and that many species (but not all) migrated to higher (1650– 2780 m) elevations where the risk of nest predation was lowest. Altitudinal migration may also have a negative impact on reproductive success, in which case birds migrate for lack of a better option, e.g., male White-ruffed Manakins that remain in breeding areas at higher elevations can experience stress due to frequent storms (Boyle 2008b, Boyle et al. 2010b). Manakins exhibit lekking behavior, with dominant alpha males and subordinate males performing elaborate displays to attract females (Rosselli et al. 2002, Boyle et al. 2011). Males that migrate to lower elevations after the breeding season tend to experience both lower social status and reduced mating success in the following breeding season in a clear trade-off between survival and reproductive success (Boyle et al. 2011). Alpha males that are residents at higher elevations have longer courtship displays, vocalize more, have larger groups of subordinate males than do migrant alpha males, and have enhanced reproductive benefits in the following season (Boyle et al. 2011). Altitudinal migration reduces the reproductive success of American Dippers (Cinclus mexicanus) in Canada (Morrissey 2004, Morrissey et al. 2004, Gillis et al. 2008, Mackas et al. 2010). In contrast to White-ruffed Manakins, American Dippers find better breeding sites at lower elevations. For this species, altitudinal migration to higher areas seems to be a consequence of intraspecific competition for a limited number of nesting sites at lower elevations (Gillis et al. 2008, Mackas et al. 2010, Green et al. 2015), forcing many individuals to migrate to less

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suitable areas (Gillis et al. 2008). American Dippers that migrate to higher altitudes provide their young with food with lower energy content (i.e., fewer fish and more aquatic invertebrates; Mackas et al. 2010). Migrants also breed later in the season, reducing the chances of having a second brood (Morrissey et al. 2004, Gillis et al. 2008). Consequently, resident American Dippers have higher annual productivity and greater reproductive success during their lifespan than do migrants (Gillis et al. 2008), and migrants produce offspring with lower condition indices (Mackas et al. 2010) and reduced survival rates (Mackas et al. 2010, Green et al. 2015). Thus, bird altitudinal migration may be a response to both reproductive needs and survival needs, where birds either migrate to higher elevations where reproductive success is likely to be higher or to lower elevations where reproductive success is likely lower, but where mortality rates are lower or there is less competition for resources. Challenges and opportunities in the study of altitudinal migration. Altitudinal

migrants are expected to be of particular conservation concern. They make use of multiple habitats over a wide area, thus requiring conservation of an array of habitats along altitudinal gradients (Loiselle and Blake 1991, Blake and Loiselle 2002, Powell and Bjork 2004). In the Neotropics, e.g., some species of altitudinal migrants, as well as lowland species, are at higher risk of extinction (Stotz et al. 1996, Fogden and Fogden 1997, Alves 2007) due to deforestation in lowland areas more suitable for human activities (Stotz et al. 1996, Fogden and Fogden 1997, Powell and Bjork 2004, Pimm 2007, Papes et al. 2012). Habitat loss at lower elevations can reduce availability of food sources for altitudinal migrants during the non-breeding season, which may increase extinction risk (ChavesCampos et al. 2003). In Costa Rica, e.g., deforestation has dramatically changed the bird community, with altitudinal migrants disproportionately represented among species of birds that have disappeared (Biamonte et al. 2011). Another cause for concern is global climate change that can alter the distribution, abundance, and patterns of altitudinal migration by birds (Inouye et al. 2000, Faaborg et al. 2010, Green 2010, Boyle 2011, Sekercioglu

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et al. 2012). Climate change may affect birds either directly through physiological stress or indirectly through changes that affect climatemediated altitudinal migration. Studies on the physiological tolerance to increased temperatures by birds worldwide shows a high climatic vulnerability, especially for tropical species (Ara ujo et al. 2013, Khaliq et al. 2014), but studies of altitudinal migrants in particular are missing. At the same time, the increased frequency, duration, and intensity of tropical storms caused by climate change may affect resource availability (Boyle 2008b, Moore 2011), leading to phenological mismatches, and a lack of resources during critical periods may cause birds that migrate to miss periods of peak food availability (Faaborg et al. 2010). This has already been observed in Australia, where an avian altitudinal migrant has responded to climate change by arriving earlier in its breeding area, but their main insect prey responded by appearing significantly later (Green 2010). Because altitudinal migrants are particularly susceptible, identifying them and determining where they live are necessary steps in developing conservation strategies for avian altitudinal migrants. Our analysis provides the most comprehensive list of altitudinal migrants to date, representing ~10% of the ~10,000 species of birds in the world. Our list, however, likely underestimates the actual number of altitudinal migrants because altitudinal migration is still understudied in most of the world. To broaden our understanding of altitudinal migration, we can adopt and adapt the procedures recommended by Alves (2007) for studies of bird migration in Brazil. These procedures include a systematic search for more information in several mountainous regions of the planet, creating a network of information among investigators working at different scales (intercontinental, regional, and local). Furthermore, we must combine the use of traditional techniques such as capture-markrecapture studies that provide information about the morphology and molting patterns of birds, with newer techniques such as miniaturized signal-transmitting tracking devices and stable isotopes. These new techniques have improved our ability to track small birds because the tracking devices are ever smaller (Webster et al. 2002, Bridge

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et al. 2011) and stable-isotope analysis has no mass or size limitations (Newsome et al. 2015). In addition, we must take into account the spatial and temporal variation in bird communities (Loiselle and Blake 1991, Alves 2007), as well as the demographics of migrating birds (Boyle 2010). Long-term studies will also be important for determining the causal mechanisms of bird migration (Levey and Stiles 1992, Sekercioglu 2010). Together with additional studies of altitudinal migrants, examination of the biotic and abiotic factors to which birds are exposed in different zoogeographical realms will allow a better understanding of the factors that cause birds to undertake these migrations. We need to evaluate the influence of environmental conditions at different elevations (Loiselle and Blake 1991), relating, e.g., resource availability (quantification of resources) to foraging guilds of birds at different altitudes. In doing so, we will be able to link environmental factors to the nutritional and physiological characteristics of individuals (Boyle 2010) and study altitudinal migration as a set of behavioral, ecological, and evolutionary phenomena (Dingle and Drake 2007). Finally, to achieve generality when testing hypotheses that attempt to explain the mechanisms underlying these migrations, broadening the geographic scope of studies on altitudinal migration is paramount, including in the megadiverse tropical regions of sub-Saharan Africa, Southeast Asia, and South America. In this way, we will be able to better understand the factors that shape bird altitudinal migrations and guide conservation efforts accordingly. ACKNOWLEDGMENTS

The authors have received support from Fundacß~ao Carlos Chagas Filho de Amparo a Pesquisa do Estado do Rio de Janeiro (FAPERJ), Coordenacß~ao de Aperfeicßoamento de Pessoal de Nıvel Superior (CAPES), and Conselho Nacional de Desenvolvimento Cientıfico e Tecnologico (CNPq). LB received a doctoral scholarship from FAPERJ (No. E-26/ 100.811/2009), CAPES (No. 31004016), and a postdoctoral scholarship from CNPq (No. 201297/ 2014-0). MMV received support from MCTI/CNPq/FAPs PELD (Grant No. 34/2012), CNPq PPBio/Rede BioM.A. (Grant No. 477524/ 2012-2), Brazilian Research Network on Global Climate Change - Rede CLIMA/MCTI (Grant No. 01.0405.01), FAPERJ APQ1 (Grant No. E-26/ 111.577/2014), and CNPq Universal (Grant No. 444704/2014). MASA received grants from CNPq (PQ Nos. 308792/2009-2 and 305798/2014-6) and

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FAPERJ (CNE Nos. E-26/102.837/2012 and E-26/ 203191/2015). This work was conceived during the doctorate of LB under MASA’ supervision at the Universidade do Estado do Rio de Janeiro. We thank M. Santana for help with data entry, and R. Macedo, M. Adeney, G. Ritchison, W. A. Boyle, C. L. Merkord, and an anonymous reviewer for valuable comments on earlier versions of our manuscript.

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Vol. 88, No. 4

Altitudinal Migration by Birds

Fig. S1. PRISMA flow diagram summarizing the systematic review. Appendix S1. Combinations of key words used to survey the literature on bird altitudinal migration in a publication database (Web of Science from Thompson Institute for Scientific Information).

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Appendix S2. List of bird species that perform altitudinal migration and their attributes. Appendix S3. Papers published between 1935 and March 2017, retrieved in the bibilographic survey, that reported bird altitudinal migration. Type of study and method used are provided.

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