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Divergent energy acquisition and processing strategies associated with using different microhabitats may allow phenotypes to specialize and coexist at small spatial scales. To understand how ecological specialization affects differentiation in energy acquisition and processing strategies, we examined relationships among digestive physiology, growth, and energetics by performing captive experiments on juveniles of wild coho salmon (Oncorhynchus kisutch) and steelhead trout (O. mykiss) that exploit adjacent habitats along natural low-to-high energy flux gradients (i.e., pools versus riffles) in coastal streams. We predicted that: (i) the specialization of steelhead trout to high-velocity, high-energy habitats would result in elevated food intake and growth at the cost of lower growth efficiency relative to coho salmon; (ii) the two species would differentiate along a rate-maximizing (steelhead trout) versus efficiency-maximizing (coho salmon) axis of digestive strategies matching their ecological lifestyle; and (iii) the higher postprandial metabolic demand (i.e., specific dynamic action, SDA) associated with elevated food intake would occupy a greater fraction of the steelhead trout aerobic budget. Relative to coho salmon, steelhead trout presented a pattern of faster growth and higher food intake but lower growth efficiency, supporting the existence of a major growth versus growth efficiency trade-off between species. After accounting for differences in ration size between species, steelhead trout also presented higher SDA than coho salmon, but similar intestinal transit time and lower assimilation efficiency. Both species presented similar aerobic budgets since the elevated SDA of steelhead trout was largely compensated by their higher aerobic scope relative to coho salmon. Our results illustrate the key contribution of digestive physiology to the adaptive differentiation of juvenile growth, energetics, and overall performance of taxa with divergent habitat specializations along a natural productivity gradient.

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A proactive-reactive continuum integrating multiple (i.e., 3+) dimensions of animal behaviour has been reported as a major axis of behavioural differentiation, but its stability along a biological hierarchy from individuals to populations remains speculative. Piscivore and insectivore rainbow trout (Oncorhynchus mykiss) represent closely related ecotypes with strong ecological divergence driven by selection for a large-bodied piscivorous lifestyle with fast juvenile growth vs. selection for smaller adult body size and lower growth associated with an insectivorous diet. To evaluate whether differences in behaviour between ecotypes are consistent with a proactive-reactive axis and consistent along a biological hierarchy, the authors examined variation in emergence time from a shelter, exploration, activity and predator inspection among individuals, populations and ecotypes of juvenile piscivore and insectivore rainbow trout O. mykiss. As expected, the faster-growing piscivore ecotype was more proactive (i.e., shorter emergence time, exploration and predator inspection) than the more reactive insectivore ecotype. This behavioural contrast was partly maintained across populations, although activity differences were most pronounced among populations, rather than emergence time. Insectivore fry showed substantial variation in behavioural expression among individuals within populations; by contrast, piscivores showed highly similar proactive behaviours with significantly lower inter-individual variation in behavioural expression, suggesting intense selection on behaviour supporting their faster growth. This work suggests that piscivore and insectivore O. mykiss broadly differ in behaviour along a proactive vs. reactive continuum, and highlights the greater multidimensionality of behavioural expression within the insectivore ecotype. Contrasting behaviours between ecotypes may result from differential selection for slow vs. fast juvenile growth and associated metabolism, and may contribute to adult trophic specialization.

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Adaptive trade-offs are fundamental mechanisms underlying phenotypic diversity, but the presence of generalizable patterns in multivariate adaptation and their mapping onto environmental gradients remain unclear. To understand how life history affects multivariate trait associations, we examined relationships among growth, metabolism, anatomy and behaviour in rainbow trout juveniles from piscivore versus insectivore ecotypes along an experimental gradient of food availability. We hypothesized that (a) selection for larger size in piscivorous adults would select for higher juvenile growth at the cost of lower active metabolism; (b) elevated growth of piscivores would be supported by a greater productivity of their natal stream and more proactive foraging behaviours and (c) general patterns of multivariate trait associations would match the predictions of the Pace-Of-Life Syndrome. Relative to insectivores, piscivorous fry showed a pattern of higher growth (+63%), maximum food intake (+33%), growth efficiency (+41%) and standard metabolic rate (SMR; +47%), but lower active metabolic capacity (maximum metabolic rate [MMR; -17%], aerobic scope [AS; -48%]), suggesting that faster piscivore growth is supported by greater food intake and digestive capacity but is traded-off against lower scope for active metabolism. A similar trade-off appeared among organ systems, with piscivorous fry exhibiting an 83% greater investment in average mass of organs associated with food consumption and processing (i.e. stomach and intestine), but an apparently smaller relative investment in organs involved in cardiovascular or cognitive activities (heart and brain, respectively). Higher invertebrate drift in their natal rearing habitat, quicker behavioural transition to a novel food source and lower anxiety after a frightening event in piscivorous fry suggest that faster growth requires both proactive foraging behaviours and higher prey availability in the environment. Finally, the sampling of replicate insectivore populations confirmed their lower juvenile growth (-73% on average) and reduced environmental productivity of their natal streams (-45% lower drift abundance) relative to the piscivore ecotype. Our results suggest that selection for large adult body size influences selection on high juvenile growth, high basal metabolism and proactive behaviours, and that the intense phenotypic divergence between piscivorous and insectivorous rainbow trout may be constrained by environmental productivity.

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Increasing habitat availability (i.e. habitat suitable for occupancy) is often assumed to elevate the abundance or production of mobile consumers; however, this relationship is often nonlinear (threshold or unimodal). Identifying the mechanisms underlying these nonlinearities is essential for predicting the ecological impacts of habitat change, yet the functional forms and ultimate causation of consumer-habitat relationships are often poorly understood. Nonlinear effects of habitat on animal abundance may manifest through physical constraints on foraging that restrict consumers from accessing their resources. Subsequent spatial incongruence between consumers and resources should lead to unimodal or saturating effects of habitat availability on consumer production if increasing the area of habitat suitable for consumer occupancy comes at the expense of habitats that generate resources. However, the shape of this relationship could be sensitive to cross-ecosystem prey subsidies, which may be unrelated to recipient habitat structure and result in more linear habitat effects on consumer production. We investigated habitat-production relationships for juveniles of stream-rearing Pacific salmon and trout (Oncorhynchus spp.), which typically forage in low-velocity pool habitats, while their prey (drifting benthic invertebrates) are produced upstream in high-velocity riffles. However, juvenile salmonids also consume subsidies of terrestrial invertebrates that may be independent of pool-riffle structure. We measured salmonid biomass production in 13 experimental enclosures each containing a downstream pool and upstream riffle, spanning a gradient of relative pool area (14%-80% pool). Increasing pool relative to riffle habitat area decreased prey abundance, leading to a nonlinear saturating effect on fish production. We then used bioenergetics model simulations to examine how the relationship between pool area and salmonid biomass is affected by varying levels of terrestrial subsidy. Simulations indicated that increasing terrestrial prey inputs linearized the effect of habitat availability on salmonid biomass, while decreasing terrestrial inputs exaggerated a "hump-shaped" effect. Our results imply that nonlinear effects of habitat availability on consumer production can arise from trade-offs between habitat suitable for consumer occupancy and habitat that generates prey. However, cross-ecosystem prey subsidies can effectively decouple this trade-off and modify consumer-habitat relationships in recipient systems.

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1. Consistency of differences in standard metabolic rate (SMR) between individual juvenile salmonids and the apparently limited ability of individuals to regulate their SMR has led many researchers to conclude that differences in individual SMR are fixed (i.e. genetic). 2. To test for the effects of food ration on individual performance and metabolism, SMR was estimated by measuring oxygen consumption using flow-through respirometry on individually separated young of the year coho salmon (Oncorhynchus kisutch) placed on varying food rations over a period of 44 days. 3. Results demonstrate that the quantity of food consumed directly affects SMR of juvenile coho salmon, independent of specific dynamic action (SDA, an elevation in metabolic rate from the increased energy demands associated with digestion immediately following a meal) and indicates that higher food consumption is a cause of elevated SMR rather than a consequence of it. Juvenile coho salmon therefore demonstrated an ability to regulate their SMR according to food availability and ultimately food consumption. 4. This study indicates that food consumption may play a pivotal role in understanding individual variation in SMR independent of inherent genetic differences. We suggest that studies involving SMR need to be cautious about the effects of intra-individual differences in food consumption in communal tanks or in different microhabitats in the wild as disproportionate food consumption may contribute more to variation in SMR than intrinsic (genetic) factors. 5. In general, our results suggest that evolutionary changes in SMR are likely a response to selection on food consumption and growth, rather than SMR itself.

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1. Adaptive trade-offs are fundamental to the evolution of diversity and the coexistence of similar taxa and occur when complimentary combinations of traits maximize efficiency of resource exploitation or survival at different points on environmental gradients. 2. Standard metabolic rate (SMR) is a key physiological trait that reflects adaptations to baseline metabolic performance, whereas active metabolism reflects adaptations to variable metabolic output associated with performance related to foraging, predator avoidance, aggressive interactions or migratory movements. Benefits of high SMR and active metabolism may change along a resource (productivity) gradient, indicating that a trade-off exists among active metabolism, resting metabolism and energy intake. 3. We measured and compared SMR, maximal metabolic rate (MMR), aerobic scope (AS), swim performance (UCrit) and growth of juvenile hatchery and wild steelhead and coho salmon held on high- and low-food rations in order to better understand the potential significance of variation in SMR to growth, differentiation between species, and patterns of habitat use along a productivity gradient. 4. We found that differences in SMR, MMR, AS, swim performance and growth rate between steelhead trout and coho salmon were reduced in hatchery-reared fish compared with wild fish. Wild steelhead had a higher MMR, AS, swim performance and growth rate than wild coho, but adaptations between species do not appear to involve differences in SMR or to trade-off increased growth rate against lower swim performance, as commonly observed for high-growth strains. Instead, we hypothesize that wild steelhead may be trading off higher growth rate for lower food consumption efficiency, similar to strategies adopted by anadromous vs. resident brook trout and Atlantic salmon vs. brook trout. This highlights potential differences in food consumption and digestion strategies as cryptic adaptations ecologically differentiating salmonid species. 5. We hypothesize that divergent digestive strategies, which are common and well documented among terrestrial vertebrates, may be an important but overlooked aspect of adaptive strategies of juvenile salmonids, and fish in general.

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