Future opportunities: addressing the challenges
With a more unified definition that includes both terrestrial and
aquatic species of divergent animal lineages, we have outlined an
improved conceptual framework for the study of altitudinal migration,
but multiple challenges and questions still exist:
- What is the full taxonomic extent of altitudinal migration? Whether or
not many taxa undertake altitudinal migration remains unknown,
especially in the global south (i.e
Rappole et al.,
2011; Maicher et
al., 2020; Guaraldo et al., 2022). Many studies and sources on
altitudinal migration have lacked scientific rigor, are descriptive,
or are from “gray” literature and are not easily found
(Schunck et al.,
2023), all of which hampers our knowledge of the true extent of
altitudinal migration. Combining macroevolutionary analyses in a
phylogenetic comparative framework with population-level studies will
reveal how altitudinal migration contributes to diversification at
different taxonomic scales. A deeper understanding of the taxonomic
diversity of altitudinal migration will also clarify how ecological
and evolutionary drivers may overlap and contrast with latitudinal
migrants
(Barçante et
al., 2017; Hobson et al., 2019; Hsiung et al., 2018; Pageau et al.,
2020).
- How do the drivers of altitudinal migration differ among regions? Each
mountain range has a unique geological history and evolutionary
pressures driving the gain and loss of altitudinal migration may vary
substantially among mountains that vary in latitude or their
surrounding biome (Rahbek et al., 2019). The distinct age and origin
of each mountain or bathymetric feature can contribute to differences
in elevational zonation, climate, and the potential for altitudinal
migration to evolve. Studies of altitudinal migration have been highly
concentrated in a few select biogeographic realms and counties,
especially in North America (Hsiung et al., 2018; Pageau et al., 2020,
Schunck et al.,
2023). Expanding the geographic scope of altitudinal migration
studies will undoubtedly reveal novel patterns and comparisons among
regions with altitudinal migrants.
- What impacts does altitudinal migration have on diversification?
Various studies have considered how the evolution of different
migratory states may impact speciation, both empirically at the
population level
(Gómez-Bahamón et
al., 2020) and through a more theoretical lens
(Winker, 2010).
However, little is known regarding how altitudinal migration may
impact rates of speciation or diversification. One might hypothesize
that changes in altitudinal migration may lead to a reduction in gene
flow—as is seen in latitudinal migration—but there are few
empirical papers that have explicitly tested this hypothesis (but see
Tigano & Russello,
2022). Future studies could clarify how changes in altitudinal
migration impact patterns of gene flow and whether there are
generalizable or idiosyncratic patterns across lineages regarding
whether altitudinal migration character states or transition rates are
associated with speciation rates.
- How is anthropogenic change impacting altitudinal migration and
migrants? Migrants and especially altitudinal migrants experience such
a wide breadth of environmental conditions, they are severely impacted
by anthropogenic change at different elevations and may be more
subjected to declines caused by forest fragmentation
(Loiselle & Blake,
1992, Runge et al. 2014). For example, many altitudinal migrants are
reliant on high-elevation habitat, which is rapidly shifting upslope
as our planet warms
(Chen et al., 2011;
Maicher et al., 2020). Changes in the elevational distributions of
ecosystems and their constituents may induce new ecological
interactions, such as the introduction of avian malaria to the
Hawaiian Honeycreepers, many of which are altitudinal migrants and
become infected with malaria during their non-breeding season at lower
elevations (Eggert
et al., 2008). Anthropogenic change has also induced various
phenological shifts, which can harm altitudinal and latitudinal
migrants due to a mismatch in the timing of resource availability
(Green, 2010; Inouye
et al., 2000). Despite the potentially pernicious impacts of land use
and climate change on altitudinal migrants, empirical studies that
address this harm and our general understanding of anthropogenic
impacts on altitudinal migrants are still sorely lacking
(but see Adams,
2018).
- What comparisons can we draw between altitudinal and latitudinal
migration? Migration is taxonomically widespread, and a broader
definition of altitudinal migration allows for more nuanced
comparisons of animal movement (Dingle & Drake, 2007). As in
latitudinal migration, subcategories of altitudinal migration can be
differentiated and compared, such as partial versus complete
altitudinal migration, or short- versus long-distance altitudinal
migration. How do these different categories compare to latitudinal
migrants? Are certain types of altitudinal migration more common among
certain lineages or biogeographic regions? Are there shared paths of
altitudinal migration (i.e., “flyways”) as there are in latitudinal
migrants? Do barriers to movement impact altitudinal migrants in a
similar or different way to that observed in latitudinal migrants?
Comparisons between strictly altitudinal migration and latitudinal
migration are lacking.
- What can we gain from comparisons of altitudinal migration patterns
across taxonomic groups? Comparative studies have been a fruitful area
of research in latitudinal migration research (i.e.
Soriano-Redondo et
al., 2020), however this topic has received little attention for
altitudinal migrants (Pageau et al., 2020). Questions such as how do
ectotherms address the challenges of traveling long distances across
elevational gradients compared to endotherms have yet to be addressed.
Though birds are comparatively well-studied in terms of altitudinal
migration, we have only scratched the surface of how they are
physiologically adapted to the changes in partial pressure and oxygen
levels (see
Williamson & Witt,
2021). How other organisms manage these changes, and if they have
physiological changes is largely unknown (but see
Jacobsen, 2020).
Comparative studies at different taxonomic scales will reveal how
ecological, physiological, and morphological variation among lineages
impacts how altitudinal migration has evolved in different animals.
Fortunately for our ability to address these challenges, the toolbox to
detect and study altitudinal migration is rapidly expanding and
improving. Here, we describe key advancements and resources that the
field can leverage toward a deeper understanding of the taxonomic
prevalence and nature of altitudinal migration. Rather than restricting
themselves to a single tool, future researchers will benefit from
integrating these tools to answer when, where, how, and why animals move
along elevational gradients across seasons
(i.e. Ruegg et
al., 2017).
- Community science is steadily growing, adding thousands of
observations that can be used to determine animal movements across
seasons (Tsai et al., 2021, Rueda-Uribe et al., 2023). Surveys and
observational data provide a simple yet powerful way to detect changes
in seasonal abundance across elevational gradients (Liang et al.,
2021, Cheng et al., 2022). However, because many altitudinal migrants
are partial migrants
(Hsiung et al.,
2018), sole reliance on presence and absence data may overlook some
potential altitudinal migrants. Using abundance in combination with
sex and/or age ratio data can provide information at the population
level rather than describing the movement of individuals.
- Tracking technologies are improving at a remarkable pace: biologgers
using satellite, radio, or acoustic transmitters are increasingly
smaller, cheaper, and easier to use (Börger et al., 2020; Holton et
al., 2021). This revolution in tracking technologies has led to new
discoveries in animal movement and migration (i. e. Satyr tragopan
Norbu et al., 2013). New multi-sensory tags that also record
atmospheric pressure are especially well-suited for short-distance
altitudinal migrants, and may help in our ability to distinguish diel-
or weather-related movements from seasonal migration across
elevational gradients
(Nussbaumer et al.,
2023; Rime et al., 2023). Parasites and other symbionts offer another
emerging framework to track populations as symbiont communities differ
strongly across elevational gradients (Williamson & Witt, 2021).
- Genomic data has long been used to study population connectivity among
latitudinal migrants (e.g. DeSaix, et al., 2019; DeSaix et al., 2023),
but has not been as extensively applied to altitudinal migrants.
Genomic data could be used to study gene flow among populations that
differ in altitudinal migration behavior and could also be used to
link populations between their breeding and non-breeding distributions
at different elevations, as has been done in many latitudinal migrants
(e.g., Battey and Klicka, 2017). Comparative and population genomics
have identified various loci associated with altitudinal migration (i.
e. Qu et al., 2015;
Tigano & Russello, 2022), yet similar studies of altitudinal
migration are lacking and the degree to which altitudinal migration is
an innate or learned behavior with a genetic component is unknown
(Merlin &
Liedvogel, 2019; Talla et al., 2020). Various studies have identified
genomic loci associated with adaptations to hypoxic conditions at
high-elevation, but our general understanding of the genetic
underpinnings of altitudinal migration lags behind that of latitudinal
migration (Moussy et al., 2013;
Merlin & Liedvogel,
2019; Toews et al., 2019; Justen & Delmore, 2022; Rougemont et al.,
2023; Sokolovskis et al., 2023).
- Bulk stable isotope analysis—primarily of Hydrogen but also
Oxygen—has been foundational in many recent studies of altitudinal
migration (Gadek et al., 2018; Newsome et al., 2015). However,
interpreting stable isotope data is sometimes difficult due to
potentially confounding factors of shifting isotopic baselines and the
influence of trophic cascades on isotope values (Hobson et al., 2012).
The use of trace element isotopes and microchemistry has been
suggested as a means to better detect altitudinal migration (Chapman
et al., 2012; Hobson et al., 2019), yet has seen few applications to
date in part due to high monetary costs and difficulty in obtaining
and analyzing samples. The advent of compound-specific stable isotope
analyses of amino acids (CSIA-AA), offers new possibilities and
increased power to detect altitudinal migration by more directly
connecting isotopes to the landscape rather than diet (McMahon and
Newsome 2019). For example, CSIA-AA was used to trace the
long-distance migration of Chum Salmon (Oncorhynchus keta)
between Okhotsk and Bering seas (Matsubayashi et al., 2020). In
particular, CSIA-AA of Hydrogen could provide improved spatial
resolution for tracking altitudinal migrants compared to bulk stable
isotope analyses (McMahon and Newsome 2019). However, ‘isoscapes’ that
describe spatial patterns of compound-specific isotopic variation are
not yet available due to the specialized instrumentation and expenses
required to process hundreds or thousands of samples at continental
scales. As the technologies underlying isotopic analyses continue to
improve, future studies of altitudinal migration incorporating CSIA-AA
will be better able to discriminate spatial from trophic signatures of
isotopic values underlying altitudinal migration.
- Natural history collections offer spatial and temporal series of
specimens that can be combined with aforementioned techniques to study
how altitudinal migration may have changed over time during the
Anthropocene
(Schmitt et
al., 2019). Many techniques used to estimate the geographic origin
from contemporary samples can be applied to museum specimens, such as
stable isotopes (Rocque and Winker, 2005) and historical DNA
sequencing (Wandeler et al., 2007), providing a potential way to
examine temporal shifts in altitudinal migration. However, differences
in preservation media—especially formalin—may impact stable
isotope values (Edwards et al., 2002) and our ability to accurately
sequence historical DNA (Do and Dobrovic, 2015) . As natural history
museums contribute specimens and metadata via continued collecting
efforts and online databases (Nachman et al., 2023), additional
studies of spatiotemporal change in altitudinal study will be
unlocked.
ConclusionHere, we have developed a taxonomically inclusive definition as a
starting point towards a conceptual framework for the study of
altitudinal migration that relies on the biological importance of
distribution shifts. We argue that the biological relevance of
altitudinal migration hinges on the movement capacity and physiology of
the taxon in question. In turn, these movements must be considered
alongside the strength and nature of ecological and physiological
changes imparted by movement along the vertical axis. A more unified
framework for studying altitudinal migration acknowledges the
complexities when classifying and comparing altitudinal migrants: many
altitudinal migrants are partial migrants, and there is also a continuum
between movement and migration that is sometimes difficult to partition.
There is still considerable work to be done to characterize the
taxonomic extent of altitudinal migration, understand regional
differences in patterns of altitudinal migration among biomes, and
mitigate Anthropogenic impacts on altitudinal migrants. Armed with an
expanding toolbox, researchers will benefit from a more unified
conceptual framework that enables comparisons across a wider breadth of
taxonomic groups, thereby revealing the evolutionary drivers, ecological
interactions, and conservation risks of altitudinal migrants across
aquatic and terrestrial biomes.
Authors Contributions DVP and NAM conceived of the ideas in this manuscript, wrote and
substantially edited the final paper.
Acknowledgements We thank Morgan Kelly, Maggie MacPherson, Samantha Rutledge, Subir
Shakya, and two anonymous reviewers for reviewing earlier versions of
this manuscript. We thank Ann Sanderson for providing the scientific
illustrations presented in Figure 1.
Conflict of Interest We report no conflict of interest.
Data Availability No original data was used for this paper
ORCID David Vander Pluym https://orcid.org/0000-0001-7975-5964
Nicholas A. Mason https://orcid.org/0000-0002-5266-463X