Definitions and nuances:
A shared language for discussing altitudinal migration has not been used
consistently in the literature. Both the term used and the definition of
the phenomenon itself lack a standardized definition (Barçante et al.,
2017), which makes it difficult to find and compare studies across
disciplines and taxonomic groups. In fact, the patterns and processes
that constitute altitudinal migration and the taxa considered
altitudinal migrants have differed widely among studies, with most
definitions focused heavily on birds (Burgess & Mlingwa, 2000, Boyle,
2017; Hsiung et al., 2018; Tsai et al., 2021; Williamson & Witt, 2021).
A conceptual framework for studying altitudinal migrations needs to
start with a standardized definition and understanding of the use of the
term. Here, we suggest a revised definition for altitudinal migration asa seasonal round trip between breeding and non-breeding ranges
for part or all of a population along an elevational or bathymetric
gradient that results in a biologically relevant shift in distribution .
But then what do we mean by “biologically relevant”?
We believe biological relevance depends on the taxon in question and
whether the vertical movement directly impacts an organism’s
fitness—either by ensuring successful migration and subsequent
reproduction, or by harming their chances for survival. Challenges to an
organism’s fitness can fall under two, non-mutually exclusive
categories: seasonal elevational movements that impart (1) physiological
and/or (2) ecological changes on migrants. Physiological challenges can
occur when individuals move across extreme elevational gradients (i. e.
Bar-headed Geese; Scott et al., 2015), which requires adaptations for
the extreme differences in partial oxygen pressure (Williamson & Witt,
2021). Vertical physical barriers, such as waterfalls or mountains, or
dams, can also impose physiological challenges to survival by blocking
migratory routes or requiring physical exertion to cross
(Cosgrove et al.,
2018). Physical barriers may present different strengths of
physiological or ecological change; in some instances, certain taxa may
move across a given physical barrier daily, while other taxa may only do
so once a season or only once in their lifetime. Ecological challenges
may include changes in habitat, intraspecific competition, predation
risk, climatic changes, trophic interactions and/or resource
availability (Alerstam
& Bäckman, 2018). The distance covered by altitudinal migrants varies
among taxa, but the migration event typically involves movement between
breeding and non-breeding ranges that extend far beyond the organism’s
home range in either site
(Teitelbaum et al.,
2015). On one extreme, more vagile species may move more than 2000 m in
elevation and thousands of kilometers in latitude, which presents clear
physiological challenges for survival in dramatically different
environments across their annual cycle (Williamson & Witt, 2021). In
contrast, some snails undertake amphidromous migrations from saltwater
to freshwater habitats that cover less than a hundred meters of
elevational change (Villeneuve et al., 2019), while some terrestrial
species only move a few hundred meters in elevation (i.e. some
Drosophila; Mitsui et al. 2010 or Trochilidae; Tinoco et al., 2009).
These may seem like trivial elevational changes for more vagile taxa,
yet represent dramatic shifts in ecology and physiological conditions
between breeding and non-breeding sites. Thus, although physiological
and ecological changes are difficult to quantify and observe directly,
they are nevertheless more important than changes in elevation that meet
a numerical or statistical threshold between breeding and non-breeding
territories. Imposing a strictly numerical definition to identify
altitudinal migrants without considering the biological relevance of the
migration event may erroneously include or omit altitudinal migrants and
bias the inferences drawn from such studies.
Even with a revised definition grounded in biological relevance and
scale, there are still many nuances and potential points of confusion
when discussing and classifying altitudinal migrants. For instance,
animals can move both latitudinally and vertically during seasonal
movements, as exhibited by monarch butterflies (Danaus
plexippus ), which migrate over the course of multiple generations from
high-elevation mountains in the Transvolcanic Belt of central Mexico to
breed at low-elevation sites in the eastern United States and Canada
during warmer spring and summer months (Kimura, 2021). There is not
widespread agreement in the literature if altitudinal migration is
strictly a short-distance migration phenomenon or if it encompasses such
long-distance migration events as well. Some comparative studies or
syntheses either do not address this explicitly, or allow for some but
not all latitudinal migrants that also move in elevation to be
classified as altitudinal migrants
(Boyle, 2017; McGuire
& Boyle, 2013; Pageau et al., 2020). Other studies state it is
strictly a short-distance phenomenon
(Hsiung et al.,
2018), or may encompass long-distance latitudinal migration as well
(Barçante et al.,
2017a; Rappole, 2013; Williamson & Witt, 2021). Migrants that move
across large latitudinal expanses while also changing elevations
experience similar or greater physiological and ecological changes as
short-distance altitudinal migrants. As such, we feel that work on
altitudinal migration should encompass both long- and short-distance
migrants, and that authors should explicitly state their criteria and
rationale for classifying altitudinal migration.
The complex migratory patterns of monarch butterflies illustrate another
nuance of altitudinal migration: partial altitudinal migration. Not all
monarch populations are migratory (Chowdhury et al., 2021), as opposed
to obligate migrants where all populations within a species are
migratory. Here, we follow the broader definition of partial migration
(Terrill & Able, 1988), where partial altitudinal migration (including
differential migration; Dingle & Drake, 2007) not only includes
distinct migratory and non-migratory populations, but also encompasses
within-population variation in migration strategies, including taxa
wherein only certain ages, sexes, or other demographic subunits of a
population migrate
(e.g.
White-ruffed manakin Corapipo altera, Boyle et al., 2011). The
majority of altitudinal migrants are also partial migrants (Hsiung et
al., 2018), such that some subpopulation or demographic group does not
participate in each annual migration event. Conversely, many
long-distance latitudinal migrants undertake ‘obligate’ or complete
migration, in which each demographic class of each population
participates in seasonal movements
(Newton, 2012).
Although altitudinal migration is a specific type of and part of the
broader study of animal movement, ‘movement’ is not synonymous with
‘migration’. Rather, migration is a specific form of animal movement.
Importantly, altitudinal migration is seasonal and cyclic with
individuals and populations moving between distinct breeding and
non-breeding areas at different elevations, which distinguishes it from
other forms of movement where populations may shift their elevational
distribution, but do so non-annually (i.e., dispersal, irruptions). Some
cyclic daily movements may occur across vertical gradients, such as
“hilltopping” in some insects, in which they form daily leks on top of
hills or mountains (Kimura, 2021), and aquatic animals undergoing “diel
vertical migration”, in which individuals change water depth between
night and day (Chapman et al., 2012). However, these are daily rather
than seasonal movements at different elevations or depths, and therefore
do not fall under our working definition of altitudinal migration.
Migration and movement exist along a behavioral and ecological
continuum, and distinguishing migration from the broader study of
movement is not always straightforward (e.g. some flies in the family
Calliphoridae; Kimura 2021). For example, two polar breeding
birds—Ivory Gull Pagophila eburnea in the Arctic, and Snow
Petrel Pagodroma nivea in the Antarctic—both breed on high
remote rocky outcrops (up to 2000 m and 2500 m, respectively) and make
regular foraging trips to the ocean (Carboneras et al., 2020; Mallory et
al., 2020). Under our definition, these daily behaviors of adults are
best categorized as ‘movements’. However, the young that are born at
high-elevation nesting sites and return to breed after spending the
non-breeding season at sea level could be considered altitudinal
migrants. Despite the similar movement ecology of these two species,
only the Ivory Gull is considered an altitudinal migrant, whereas no
Antarctic birds—including the Snow Petrel—are considered altitudinal
migrants (Barçante et
al., 2017a; Hsiung et al., 2018). The study of migration is embedded
within the broader study of animal movement, but determining where the
narrower study begins is sometimes difficult due to complex life
histories involving seasonal and/or ontological changes in elevation. A
unified conceptual framework for altitudinal migration will help
unpackage these complexities and alleviate this confusion. One can
envision a multivariate space to describe the how organisms vary in
their migratory behavior; for example, it may be helpful to place
organisms along continua that describe variation whether organisms
exhibit latitudinal migration, altitudinal migration, or both in
conjunction with whether or not those taxa are complete or partial
migrants (Figure 2).
Finally, establishing a consistent language for the field is important
to help improve the visibility and searchability of the primary
literature involved. Though “vertical” or “elevational” migration
may be seen as more accurate descriptors of this type of seasonal
movement across biomes and taxonomic groups, the term “altitudinal
migration” has historical precedence
(i. e. Todd and
Carriker 1922; Presnall, 1935) and is more frequently used in the
literature (2840 Google Scholar search hits for “altitudinal
migration” compared to 464 for “elevational migration”; searches done
on 15 August 2023). We used the program Publish or Perish (Harzing 2007)
to quantify temporal trends in Google Scholar hits for publications that
use the terms “altitudinal migration” and “elevational migration”,
finding that altitudinal migration was established as a term far earlier
and is used far more often than “elevational migration” (Figure 3).
Thus, although these terms have often been used interchangeably,we
recommend using the more commonly used term altitudinal migration. We do
not just advocate for its use because it is the more commonly used and
historical term, but also because it better encompasses terrestrial and
aquatic migrations. In that regard, “vertical migration” is perhaps a
more accurate term, but is used predominantly in aquatic systems (over
141,000 Google Scholar search hits on 15 August 2023) to describe a
different phenomenon of daily movement across multiple trophic levels up
and down the water column rather than the seasonal movements we focus on
here (Chapman et al., 2012). Use of a single term not commonly used
elsewhere in the literature will aid researchers and search engines in
identifying information on this phenomenon rather than often-conflated
terms (Leeming 2023). ’Altitudinal migration’ may seem a misnomer due to
the definition of altitude in aviation as the distance above the Earth’s
surface as opposed to above sea level, yet we nonetheless recommend its
use to promote a consistent vocabulary to facilitate dialogue across
disciplines and taxonomic groups.