Thresholds for Reduction in Fish Growth and Consumption Due to Hypoxia: Implications for Water Quality Guidelines to Protect Aquatic Life.

Control of hypoxia is a key element of water quality management, and guidelines are usually based on qualitative reviews of hypoxia impacts. In this study we use segmented regression to identify both thresholds for growth reduction and rate of decline of fish growth and food consumption under hypoxia; and then evaluate whether current freshwater guidelines for dissolved oxygen based on qualitative reviews are consistent with the quantitative analysis of hypoxia thresholds. Segmented regressions were fit to data from published growth-hypoxia studies for freshwater (N = 17) and marine fishes (N = 13). To understand potential drivers of hypoxia tolerance, we also modelled thresholds as simple functions of environmental and ecological covariates for each species including trophic level, marine vs. freshwater environment, maximum fish length, fish weight, and maximum temperature tolerance. The average threshold for growth reduction (Gcrit; 5.1 mg·l-1 DO) and decreased food consumption (Ccrit = 5.6 mg·l-1 DO) were not significantly different, and did not differ between marine and freshwater taxa. However, salmonids showed a significantly steeper decline in growth with increasing hypoxia relative to other taxa. Growth declined by 22% for every mg·l-1 reduction in DO below average Gcrit, and significant regressions indicate that warmwater (R2 = 0.25) and smaller-bodied (R2 = 0.44) species are more likely to be hypoxia tolerant. Observed mean Gcrit and Ccrit in the range of 5-6 mg·l-1 broadly match minimum water quality guidelines for the protection of aquatic life in freshwater in representative industrialized countries. However, this is much higher than the definition of hypoxia typically used in marine systems (2-2.5 mg·l-1), indicating a need to reconcile definition of hypoxia in the marine environment with empirical data. The principal challenge in freshwater hypoxia management is now translating discretionary guidelines into effective regulatory frameworks to reduce the incidence and severity of hypoxia.

Behavioural variation between piscivore and insectivore rainbow trout Oncorhynchus mykiss.

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.

Adaptive differentiation of growth, energetics and behaviour between piscivore and insectivore juvenile rainbow trout along the Pace-of-Life continuum.

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.

The energetic consequences of habitat structure for forest stream salmonids.

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.

Relationship between growth and standard metabolic rate: measurement artefacts and implications for habitat use and life-history adaptation in salmonids.

Mass-specific standard metabolic rate (SMR, or maintenance metabolism) varies greatly among individuals. Metabolism is particularly sensitive to variation in food consumption and growth creating the potential for significant bias in measured SMR for animals that are growing (e.g. juveniles) or of uncertain nutritional status. Consequently, interpreting individual variation in metabolism requires a sound understanding of the potentially confounding role of growth and the relative importance of fixed (genetic) vs. environmental drivers of SMR variation. We review the role of growth in measured SMR variation in juvenile salmonids, with the goals of (i) understanding the contribution of growth (and food consumption) to SMR variation through ontogeny, (ii) understanding the relative contributions of tissue maintenance and biosynthesis (overhead costs of growth) to apparent SMR variation, and (iii) using intrinsic growth effects on SMR to model how alternate life-history strategies may influence growth and measured SMR in juvenile salmonids. SMR measures on juveniles, even when post-absorptive, may be inflated by delayed growth-associated overhead costs, unless juveniles are on a maintenance ration (i.e. not growing). Empirical measurements of apparent SMR in food restricted vs. satiated 2-5 g juvenile salmon demonstrate that estimates may be inflated by as much as 67% due to delayed overhead costs of growth, even when SMR measurements are taken 35 h post-feeding. These results indicate that a substantial component of variation in apparent SMR among juvenile salmonids may be associated with (i) environmentally driven variation in ration (where elevated SMR measurements are an artefact of delayed growth overhead costs), (ii) intrinsic (genetic) or plastic organ-system trade-offs related to increasing investment in metabolically expensive digestive tissue responsible for processing food and (iii) intrinsic (genetic) variation in maximum body size and growth among individuals or life-history types. We suggest that selection for differences in adult body size among resident and anadromous forms leading to differences in juvenile growth trajectories may contribute to both SMR variation and habitat segregation in freshwater, where juveniles with higher growth are constrained to foraging in high velocity habitats to meet their greater consumption needs.

Effects of food ration on SMR: influence of food consumption on individual variation in metabolic rate in juvenile coho salmon (Onchorhynchus kisutch).

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.

Divergence in digestive and metabolic strategies matches habitat differentiation in juvenile salmonids.

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.

Stressor-response functions as a generalizable model for context dependence.

Defining the context dependence of ecological states or processes is a fundamental goal of ecology. Stressor-response functions are the quantitative representation of context dependence, where the context (environmental contingency) is defined by location on the stressor (x) axis, and represents a unifying concept in biological science.

Adaptive trade-offs in juvenile salmonid metabolism associated with habitat partitioning between coho salmon and steelhead trout in coastal streams.

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.

Contrasting landscape influences on sediment supply and stream restoration priorities in northern Fennoscandia (Sweden and Finland) and coastal British Columbia.

Sediment size and supply exert a dominant control on channel structure. We review the role of sediment supply in channel structure, and how regional differences in sediment supply and land use affect stream restoration priorities. We show how stream restoration goals are best understood within a common fluvial geomorphology framework defined by sediment supply, storage, and transport. Land-use impacts in geologically young landscapes with high sediment yields (e.g., coastal British Columbia) typically result in loss of in-stream wood and accelerated sediment inputs from bank erosion, logging roads, hillslopes and gullies. In contrast, northern Sweden and Finland are landscapes with naturally low sediment yields caused by low relief, resistant bedrock, and abundant mainstem lakes that act as sediment traps. Land-use impacts involved extensive channel narrowing, removal of obstructions, and bank armouring with boulders to facilitate timber floating, thereby reducing sediment supply from bank erosion while increasing export through higher channel velocities. These contrasting land-use impacts have pushed stream channels in opposite directions (aggradation versus degradation) within a phase-space defined by sediment transport and supply. Restoration in coastal British Columbia has focused on reducing sediment supply (through bank and hillslope stabilization) and restoring wood inputs. In contrast, restoration in northern Fennoscandia (Sweden and Finland) has focused on channel widening and removal of bank-armouring boulders to increase sediment supply and retention. These contrasting restoration priorities illustrate the consequences of divergent regional land-use impacts on sediment supply, and the utility of planning restoration activities within a mechanistic sediment supply-transport framework.

Sensitivity analyses of spatial population viability analysis models for species at risk and habitat conservation planning.

Population viability analysis (PVA) is an effective framework for modeling species- and habitat-recovery efforts, but uncertainty in parameter estimates and model structure can lead to unreliable predictions. Integrating complex and often uncertain information into spatial PVA models requires that comprehensive sensitivity analyses be applied to explore the influence of spatial and nonspatial parameters on model predictions. We reviewed 87 analyses of spatial demographic PVA models of plants and animals to identify common approaches to sensitivity analysis in recent publications. In contrast to best practices recommended in the broader modeling community, sensitivity analyses of spatial PVAs were typically ad hoc, inconsistent, and difficult to compare. Most studies applied local approaches to sensitivity analyses, but few varied multiple parameters simultaneously. A lack of standards for sensitivity analysis and reporting in spatial PVAs has the potential to compromise the ability to learn collectively from PVA results, accurately interpret results in cases where model relationships include nonlinearities and interactions, prioritize monitoring and management actions, and ensure conservation-planning decisions are robust to uncertainties in spatial and nonspatial parameters. Our review underscores the need to develop tools for global sensitivity analysis and apply these to spatial PVA.