The importance of rare phenotypes and life history diversity
Otolith isotope profiles revealed three distinct juvenile life-history types (hereon referred to as “early”, “intermediate” and “late” migrants; Figure 1 right panel, Supplementary Results S1), concordant with the three emigration modes observed in the juvenile trapping data (Supplementary Results S2). The three life-history types were characterized by significant differences in the age and size at which they exited the natal tributary (Figures 1 right panel and 2a, Supplementary Results S2). Despite leaving the natal stream considerably smaller, early migrants entered the ocean at a similar size and age to intermediate migrants, after rearing for multiple months in non-natal freshwater habitats. Late migrants emigrated out to the ocean significantly later and larger than either other phenotype (Figure 2b, Supplementary Results S2), having reared in the natal stream over the summer (mean natal rearing period = 194 days ± 32 days SD). Late migrants may thus experience very different freshwater, and estuarine and nearshore marine conditions, potentially resulting in differential feeding, growth and survival opportunities31,32.
While late migrants were the least commonly observed phenotype in juvenile monitoring traps33 (Supplementary Figure S2a), they represented the majority of the returning adults (mean across years = 60%; Figure 2a). Conversely, on average, 19% of surviving adults were represented by intermediate migrants (mean natal rearing period = 84 days ± 27 days SD) and 21% by early migrants (mean natal rearing period = 15 days ± 14 days SD). Importantly, the contribution rate of each life history type varied considerably among years (Figure 3). Half of the return years (2007, 2008, 2013) were represented by similar contributions of each life history type and bimodal freshwater exit sizes while during multi-year droughts and ocean heatwaves (returning 2012, 2014, 2018) the late migrants that left the freshwater during cooler fall conditions were functionally the only strategy to survive to adulthood (Figure 3; Supplementary Table S2).
Early-life freshwater growth rates were inversely correlated with emigration timing, with faster growing individuals tending to leave the natal tributary earlier, and slower growing individuals remaining for longer before migrating downstream (Figure 4a and Supplementary Results S3). Early migrant growth over the first 15 days was faster on average (mean cumulative width of first 15 increments = 37 µm) than intermediate (32 µm) and late migrants (30 µm; Figure 4b). It is interesting to note that the fastest growth rates were typically observed among the juveniles that left the natal stream earliest (within 15 days after emergence; open circle dots in Figure 4a), and thus reared in both natal and non-natal habitats. Those results are consistent with previous studies showing differential salmon juvenile growth rates and sizes across multiple migratory pathways29,34,35.
Thermally suitable habitat in a warming climate
Temperature strongly influences salmonid physiology, growth and survival36. Thus populations with access to diverse water temperatures during incubation and natal rearing are predicted to exhibit increased phenotypic and phenological diversity37. To support late migrants, stream temperatures need to remain suitably cool over the summer to accommodate the extended rearing period. Mill and Deer Creek watersheds, along with upstream reaches of the Battle and Clear Creeks and the Yuba River, are among the few accessible and populated spring-run streams in the system that still provide suitable rearing temperatures to support all three phenotypes (Figure 5 top panels). In accessible stream reaches where spring run were historically present but are now extirpated, only the Stanislaus River has temperatures that could support the late migrating phenotype. Importantly, increases in spring and summer stream temperatures by 2040 (Figure 5 bottom panels) and 2080 (Supplementary Results S4) are predicted to further contract the amount of thermally suitable rearing habitat, especially along the downstream reaches of spring-run streams and the mainstem Sacramento River. Without intervention, late-migrants may only have access to 76 km of suitable summer rearing habitat by 2080, around half of the accessible suitable habitat during our study period (i.e., 2005-2015; Supplementary Table S3). However, suitable rearing habitat for late-migrants could be approximately tripled (201 km; Supplementary Table S3) if spring run were provided access above the dams on the Sacramento, Feather, Yuba, American and Tuolumne Rivers (Figure 5). Here we used a fixed temperature threshold of 15°C after Richter and Kolmes38, yet we acknowledge that there is likely some variation in this threshold according to local water quality and food availability39.