Edge thermal niche tracking
We estimated edge thermal niche tracking by testing whether the change in minimum or maximum temperature at the range edge over time was different from zero, based on 90% Bayesian credible intervals from Bayesian linear regressions of temperature on time. Of 153 species range edges, we found that 131 (86%) maintained at least one component of the edge thermal niche (warm or cold extreme temperature) during the study period. Further, for the majority of range edges—111, or 73%—both minimum and maximum temperatures were maintained over time. Of the 20 range edges consistent with only one temperature metric, 13 were consistent with cold extremes and 7 were consistent with warm extremes.
In the West Coast and the Eastern Bering Sea, almost all range edges tracked both temperature metrics (84% and 97%, respectively; Figure 3B, 3C). By contrast, only 34% of range edges in the Northeast tracked both temperature metrics, and the Northeast also contained 20 of the 22 range edges that did not track either warm or cold temperature extremes (Figure 3A). Lack of tracking arose for different reasons in poleward and equatorward edges: the poleward edges that did not maintain their edge thermal niches often did not shift as the oceans warmed, or even shifted south, while the equatorward edges that did not maintain their edge thermal niches often shifted north faster than expected, into cooler waters (Appendix 4).
DISCUSSION
We quantified temporal dynamics and thermal niche tracking over decades for more than 150 marine range edges while using a novel spatiotemporal modeling approach to standardize among the three study regions and their differing survey methodologies. Across diverse geographies, historical climates, and taxa, range edges of marine species were in general conserving their thermal niches through space and time. Edge thermal niche conservatism suggests that most species range edges are tracking temperature change, consistent with evidence that many species distributions are shifting through space (Pinsky et al. 2013, Hiddink et al. 2015, Day et al. 2018, Lenoir et al. 2020) and supported by theory from thermal ecophysiology (Sunday et al. 2012, Stuart-Smith et al. 2017, Pinsky et al. 2019). However, a non-negligible number of range edges did not shift as predicted—especially in the Northeast, the region with the greatest historical temperature increase—indicating that temperature alone does not explain range edge dynamics for all marine species. This study provides the first large-scale, multi-region analysis of thermal niche tracking at range edges and describes novel statistical approaches that are applicable to a wide range of taxa and systems.
Species ranges are shifting poleward around the globe, both on land and in the sea (Chen et al. 2011, Poloczanska et al. 2013). Local patterns in climate change have helped to explain distributional shifts of many species, especially those that did not shift directly toward the poles (Pinsky et al. 2013, Lenoir and Svenning 2015). These findings suggest that species’ range shifts can be at least partially explained by spatial shifts in their climatic niches (Loarie et al. 2009, Burrows et al. 2011). While many global change studies have not measured range edge displacement, those that have often report major poleward shifts in range edges, particularly at the poleward range edge (Parmesan et al. 1999, Hickling et al. 2005). However, most studies on range edges have used a small number of time points (e.g., Hickling et al. 2005)—and often just two—limiting inference about climatic niche tracking. Marine species are predicted to track their climatic niches more closely than terrestrial species: they have exhibited greater range shifts to date, and are more physiologically vulnerable to warming (Pinsky et al. 2019, 2020, Lenoir et al. 2020). Testing for climatic niche tracking is fundamentally related to measuring range edge dynamics, because—especially in the oceans—range edges are expected to coincide with climatic niche limits, specifically thermal limits (Sunday et al. 2012).
By measuring thermal niche conservatism at the range edge, we tested for a relationship between range edge position and the isotherms representing winter and summer temperatures over time (Sunday et al. 2015, Fredston‐Hermann et al. 2020). A finding that a range edge remained in the same winter or summer temperatures over time can have several interpretations. It does not necessarily imply that the isotherm moved: an edge may track its thermal niche either by shifting in the same direction and at the same rate as an isotherm, or by remaining in place when the isotherm is stationary. The two regions in our study with high levels of edge thermal niche tracking, the West Coast and the Eastern Bering Sea, both had relatively little temperature change when averaged over the study period; thus, range edges in those regions that did not move much were typically classified as tracking the edge thermal niche.
Recent work on marine heatwaves has underscored the need to move beyond means to measure climatic extremes and variability in studies of global change biology, including in the oceans (Smale et al. 2019). We quantified edge position in relation to temperature extremes precisely for this reason, especially given the marked recent increases in warm extreme (summer) temperatures in the Northeast and the Eastern Bering Sea. Yet our results revealed that range edges remained in the same cold extreme (winter) temperatures approximately as often as they did for summer temperatures, suggesting that winter temperatures may be an underappreciated covariate of range dynamics at both poleward and equatorward range edges (Dana 1853, Morley et al. 2017). Foundational biogeographic theory provides a hypothesis for this: poleward range edges could be influenced either by summer temperatures limiting reproduction and growth or by winter temperatures limiting survival; and equatorward range edges could be influenced either by summer temperatures limiting survival or by winter temperatures limiting growth and reproduction (Hutchins 1947). Further work could test whether this is a biologically plausible explanation for these temperate marine species. Longer time series, extensive analysis of different dimensions of temperature change, or additional oceanographic data products such as high-resolution hindcast sea bottom temperature data could be used in the future to tease apart more precisely which temperature metrics best explain range edge dynamics and why.
Our finding that the region with the greatest historical temperature increase exhibited the lowest frequency of edge thermal niche tracking underscores the critical importance of considering non-temperature and indirect processes that may influence species distributions. In the Northeast, we documented equatorward range edges that shifted much further north than expected based on temperature—into cooler waters—and poleward range edges that did not shift or shifted south (Appendices 3 and 4). This could arise due to density-dependent habitat selection if these species were declining in abundance, causing each range edge to collapse toward the range center (Blanchard et al. 2005). At the equatorward edge, competition or predation from the south could be driving edge retraction (Kordas et al. 2011); for example, the rapid contraction of the equatorward range edge of American lobster could be due to increased predation from species like black sea bass shifting up the coast (McMahan and Grabowski 2019) or increased mortality from a temperature-related disease (Groner et al. 2018). At the poleward edge, species interactions (HilleRisLambers et al. 2013), priority effects (Fukami 2015), dispersal limitation (Poloczanska et al. 2011), or a lack of non-thermal habitat (McHenry et al. 2019) could all inhibit northward shifts. Sessile invertebrates are particularly vulnerable to dispersal limitation if prevailing currents do not align with local climate velocities, as in the Northeast (Molinos et al. 2017, Fuchs et al. 2020). Changes in non-temperature abiotic drivers such as dissolved oxygen are likely to also influence range edge dynamics (Deutsch et al. 2015, Howard et al. 2020).
This study is the first to use a spatiotemporal modeling approach to estimate range edge dynamics and estimate a standard error around range edge positions, which we see as important methodological advances. Using the VAST model, we calculated rates of range edge shift that were similar in magnitude to those calculated from raw survey data in the Northeast (Fredston‐Hermann et al. 2020). Our results are not directly comparable to previous work, however, because—unlike analyses of raw distribution data—VAST attributes some variation in recorded observations and abundances to observation error. Continued extensions of VAST and similar models to distribution data will facilitate more rigorous evaluation of historical range edge dynamics, even for datasets with known inconsistencies and biases in sampling.
While we found that range edge positions almost always maintained their edge thermal niche, year-over-year temperatures at the range edge were often variable (Appendix 4), and near-term (i.e., annual, not multi-decadal) projections of a species’ edge thermal niche are unlikely to predict exactly where it will shift. Further, a non-negligible fraction of range edges did not shift at all, shifted opposite the predicted direction, or “overshot” temperature change and shifted into cooler waters. Our methods provide a blueprint for assessing whether range edges have tracked their thermal niches and for identifying species of concern that do not appear to be shifting as expected based on temperature alone. Classifying species by edge thermal niche tracking can inform management and conservation because different interventions are likely required for a species that shifts in response to warming (e.g., transboundary management) than for a species that remains stationary in the face of warming (e.g., assisted migration). To move beyond categorizing all results of no thermal niche tracking as “individualistic responses,” future research can test edge thermal niche conservatism against—or jointly with—other biogeographic hypotheses that integrate the influence of species interactions, population dynamics, eco-evolutionary processes, and other important abiotic and biotic drivers. Future progress on range edge dynamics will be accelerated by mechanistically testing predictions about which temperature and non-temperature processes should be limiting for which range edges against biogeographical data. Testing multiple contemporaneous processes (including density-dependent range expansion and contraction) and their net effects will provide insight into, and ultimately enable prediction of, range edge dynamics in a changing climate.
ACKNOWLEDGMENTS
We thank current and past NOAA staff for collecting, curating, and publishing the data used in this study. E. M. Howard and R. Mendelssohn provided expert advice regarding oceanographic and spatial data analysis. We also thank A. J. Allyn and D. Ovando for code review and feedback.
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