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:
  1. 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).
  2. 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.
  3. 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.
  4. 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).
  5. 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.
  6. 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).
  1. 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.
  2. 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).
  3. 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).
  4. 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.
  5. 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