Phenotype flexibility in wild fish: Dolly Varden regulate assimilative capacity to capitalize on annual pulsed subsidies

Abstract

Summary 1.Large digestive organs increase rates of energy gain when food is plentiful but are costly to maintain and increase rates of energy loss when food is scarce. The physiological adaptations to this trade-off differ depending on the scale and predictability of variation in food abundance. 2. Currently, there is little understanding of how animals balance trade-offs between the cost and capacity of the digestive system in response to resource pulses: rare, ephemeral periods of resource superabundance. We investigated the physiological and behavioural tactics of the fish Dolly Varden (Salvelinus malma) that rear in watersheds with low in situ productivity, but experience annual resource pulses from the spawning migrations of Pacific salmon. The eggs of Pacific salmon provide high-energy food for Dolly Varden. 3. Dolly Varden sampled 6 weeks prior to the resource pulse exhibited atrophy of the stomach, pyloric caeca, intestine and liver. Throughout the portion of the growing season prior to the resource pulse, fish exhibited empty stomachs, low indices of energy condition and muscle isotope signatures reflecting the previous resource pulse. 4. During the resource pulse, Dolly Varden exhibited large digestive machinery, gorged on salmon eggs and rapidly stored energy in fat reserves, somatic growth and gonad development. Dolly Varden appeared to achieve nearly their entire annual energy surplus during the ∼5-week period when sockeye salmon spawn. 5. Digestive flexibility provides Dolly Varden the energy efficiency required to survive and reproduce when resource abundance is concentrated into an annual pulse that is predictable, yet highly ephemeral. Although fish are known to incur extremely variable energy budgets, our study is one of the first to document digestive flexibility in wild fish. Our study emphasizes that fish can rely heavily on rare, high-magnitude foraging opportunities. Human actions that attenuate spikes in food abundance may have stronger than anticipated effects on consumer energy budgets.

Flexibility in metabolic rate confers a growth advantage under changing food availability

“…If the latter were true, then we would expect a positive relationship between SMR and growth regardless of food level rather than the negative one we observed at low food levels. Indeed, shifts in SMR are thought to reflect underlying changes in digestive and assimilative processes (Armstrong & Bond 2013), mitochondrial efficiency (Monternier et al . 2014) and/or respiratory substrate use (McCue 2010) that may be critical for growth and explain observed relationships between metabolic rates and growth across the spectrum of food availability.…”

Resource subsidies from adfluvial fishes increase stream productivity

“…The digestive flexibility of Dolly Varden (Salvelinus malma) suggests an adaptability to rely on an annual pulse of eggs that is predictable (Armstrong & Schindler, 2011;Armstrong & Bond, 2013). The importance of an annual subsidy may have stronger and unanticipated impacts on fish growth and overwintering survival (Ward & Slaney, 1988;Shuter & Post, 1990;Biro et al, 2004).…”

“…Nutrients from salmon are incorporated into all trophic levels in streams, including riparian vegetation, algae, invertebrates and fish, directly through the consumption of salmon eggs and carcasses and indirectly through excretory products and the decomposition of carcasses (Willson, Gende & Marston, 1998;Gende et al, 2002;Hicks et al, 2005;Helfield & Naiman, 2006). The flow of energy from salmon subsidies can greatly enhance stream productivity resulting in increased density, growth rate, condition, overwintering survival, and ultimately, better marine survival of juvenile salmon than would be expected without migratory salmon subsidies Bentley et al, 2012;Armstrong & Bond, 2013).…”

“…In Alaska, eggs may provide resident stream fishes much of their annual energy surplus (Moore, Schindler & Ruff, 2008;Armstrong & Bond, 2013). eggs and carcasses) have influenced community dynamics and productivity in connected stream systems.…”

Divergent growth patterns between juveniles of two sympatric Arctic charr morphs with contrasting depth gradient niche preferences

“…The LO-morph, on the other hand, displayed clear seasonal variations in growth with negative SGR during late autumn-early winter, low but positive growth during spring and markedly elevated SGR-values with higher temperatures during summer. This seems to be a common adaptation to take advantage of the seasonal variations in water temperature and food resource availability generally seen for northern freshwater fishes and Arctic charr in particular (Johnson 1980;Klemetsen et al 2003a;Armstrong and Bond 2013). The difference in growth between the LO-and the PB-morph was most evident at the constant low temperature regime, where almost 50 % of the LOmorph displayed negative SGR-values during the polar night period in late autumn-early winter, despite having unlimited access to feed during this period.…”