How does thermal heterogeneity mediate the potential for consumers to capitalize on seasonal resource pulses?
Every year tens of millions of sockeye salmon spawn in Bristol Bay watersheds and subsidize freshwater foodwebs with their energy-rich eggs. I’m interested in how spatial variation in water temperature among and within streams mediates the potential for resident salmonids to exploit seasonal pulses of eggs. Here is what my collaborators and I have found so far:
1. Thermal heterogeneity among streams dictates the population-level response of coho salmon fry to sockeye salmon subsidies.
Age-0 salmonids can’t fit an egg down their throat until they reach ~70 mm length. Water temperature mediates whether age-0 individuals can grow fast enough to reach this size threshold in time to exploit salmon eggs in their first summer of life. In cooler streams coho salmon fry did not grow large enough to consume eggs and showed no growth increase during the resource pulse. In contrast, coho salmon fry in warmer streams grew large enough to consume eggs and exhibited rapid growth during the resource pulse. This shows how ecological mechanisms (in this case the size threshold for consumption) can magnify the effects of water temperature on fish growth, generating non-linear responses that could not be predicted by physiological models alone.
Armstrong, J.B., D.E. Schindler, K.L. Omori, C.P. Ruff, and T.P. Quinn. 2010. Thermal heterogeneity mediates the effects of pulsed subsidies across a landscape. Ecology. 91: 1445-1454
2. Juvenile coho salmon and char actively exploit thermal heterogeneity through behavioral thermoregulation.
Salmonids require relatively warm water for their digestive systems to keep pace with high levels of foraging–such as gorging on salmon eggs. Water temperature and spawning salmon are heterogeneously distributed across aquatic ecosystems, which generates a mosaic of growth potential for juvenile coho salmon. We found that when sockeye salmon subsidies occur in cold water coho salmon can evade thermal constraints on growth by feeding in cool habitats with abundant food, and then moving to warmer habitats that accelerate metabolism. This behavioral thermoregulation can occur over surprisingly large spatial scales, with feeding forays exceeding 1km round trip. This shows how fish can benefit by actively exploiting habitat heterogeneity.
Armstrong, J.B., D.E. Schindler, C.P. Ruff, K. Bentley, G. Brooks, and C. Torgersen. 2013. Ecology 94: 2066–2075
3. Thermal heterogeneity generates spatio-temporal variation in the spawn timing of sockeye salmon, increasing the duration of the resource pulse for mobile consumers.
In general, sockeye salmon populations in colder habitats spawn earlier in the summer, while those in warmer habitats spawn later. While the duration of spawning in a single population lasts only ~2-4 weeks, a “portfolio” of salmon stocks in a thermally heterogeneous watershed may spawn over a much longer period (Lisi et al. 2013). We found that rainbow trout were able to move adaptively to track this shifting mosaic of foraging opportunity and extend the duration of the resource pulse. The spatial distribution of bears and gulls also also tracked population-level variation in salmon spawn-timing, suggesting they too “surf” the red wave of salmon as it shifts across the landscape. This phenomena is analogous to ungulates and other herbivores moving to track the “green wave” of plant phenology. I recently collaborated with Matt Kauffman’s research lab to explore the conservation implications of resource waves. I am also continuing field research on this subject, collaborating with Gordon Reeves and Daniel Schindler to conduct research in both Bristol Bay and the Copper River Delta. Will Deacy has joined my lab as a postdoctoral researcher, exploring how bears surf red waves of salmon on Kodiak Island.
Ruff, C.P., D.E. Schindler, J.B. Armstrong, K.T. Bentley, G.T. Brooks, G.W. Holtgrieve, M.T. McGlauflin, C.E. Torgersen, and J.E. Seeb. 2011 Temperature-associated population diversity in salmon confers benefits to mobile consumers. Ecology. 92: 2073-2084.
D.E. Schindler, J.B. Armstrong, et al. Riding the crimson tide: mobile terrestrial consumers track phenological variation in spawning of an anadromous fish. 2013. Biology Letters 9(3)
Schindler, D.E., J.B. Armstrong, and T.E. Reed. 2015. The Portfolio Concept in ecology and evolution. Frontiers in Ecology and the Environment.13: 257-263
Armstrong, J.B., G.T. Takimoto, D.E. Schindler, M.M. Hayes, and M.J. Kauffman. 2016. Resource waves: phenological diversity enhances foraging opportunities for mobile consumers. Ecology 97 1099-1122
Deacy, W., W. Leacock, J.B. Armstrong, and J.A. Stanford. 2016. Kodiak brown bears surf the red wave: direct evidence from GPS collared individuals. Ecology 97 1091-1098
Deacy, W., J.B. Armstrong, W. Leacock, C.T. Robbins, D.D. Gustine, J.A. Erlenbach, E.J. Ward, and J.A. Stanford. 2017. Phenological synchronization disrupts trophic interactions between Kodiak brown bears and salmon. Proceedings of the National Academy of Sciences 114 10432–10437
4. Juvenile coho salmon track shifting mosaics of water temperature
I’m interested in how the timing and magnitude of summer precipitation affects spatial patterns of water temperature in streams and in turn the physiological potential for juveniel coho salmon to capitalize on sockeye salmon eggs. I’ve found that episodic precipitation events homogenize water temperatures in the main-channel of streams, but also add heterogeneity by generating warm habitat in off-channel areas. Thus, as flow varies at annual and seasonal time-scales, the location of warm water habitats shifts across space.
In my focal stream, Bear Ck., I found that thermoregulatory behavior in juvenile coho salmon can track this shifting mosaic of water temperature. Individuals gorge on eggs and then move to warm water to accelerate metabolism. At high flows, we find juvenile coho salmon digesting their meals in warm off-channel habitats downstream, whereas at base flows, we find them in warm main-channel habitats upstream. This shows how an intact portfolio of stream habitats can allow fish to capitalize on resource pulses across a wide range of flow conditions. As an undergraduate researcher Jeff Baldock continued this work and discovered juvenile coho salmon also track shifting mosaics of temperature during early summer, prior to the sockeye salmon subsidy. Fish fed on benthic invertebrates in the main-channel at night and then moved back to off-channel habitats that provided warmer temperatures. As water levels receded and the spatial configuration of warm water habitats shifted, coho salmon tracked patches of warm water across the riverscape.
The above figure shows the spatial distribution of warm water and coho salmon in Bear Creek as water levels receded during the early summer (From Baldock et al. 2016). Parafluvial groundwater channels that are cold during mid to late summer provided warm water when high lake levels inundated them during the spring to early summer.
The above image shows juvenile coho salmon holding in a thin layer of warm water in a micro-stratified off-channel habitat.
J.B. Armstrong and D.E. Schindler. 2010. Going with the flow: spatial distributions of juvenile coho salmon track a shifting mosaic of water temperature. Ecosystems 16: 1429-1441
Baldock, J., J.B. Armstrong, and D.E. Schindler. 2016. Diel horizontal migrations of juvenile fish track intra-seasonal spatio-temporal variation in water temperature. Freshwater Biology 61: 1365–1609