Winter ecology of specialist and generalist morphs of European whitefish, Coregonus lavaretus, in subarctic Northern Europe

European whitefish is a model species for adaptive radiation of fishes in temperate and subarctic lakes. In northern Europe the most commonly observed morphotypes are a generalist (LSR) morph and a pelagic specialist (DR) morph. The evolution of a pelagic specialist morph is something of an enigma, however, as this region is characterized by long, dark winters with pelagic primary production limited to a brief window in late summer. We conducted the first winter-based study of polymorphic whitefish populations to determine the winter ecology of both morphs, and we combined seasonal diet and stable isotope analysis with several proxies of condition in three polymorphic whitefish populations. The generalist LSR morph fed on benthic and pelagic prey in summer but was solely reliant on benthic prey in winter. This was associated with a noticeable but moderate reduction in condition, lipid content and stomach fullness in winter relative to summer. In contrast, the DR whitefish occupied a strict pelagic niche in both seasons. A significant reduction in pelagic prey during winter resulted in severe decrease in condition, lipid content and stomach fullness in DR whitefish in winter relative to summer, with the pelagic morph apparently approaching starvation in winter. We suggest that this divergent approach to seasonal foraging is associated with the divergent life-history traits of both morphs.Peer reviewe

Allopatric origin of sympatric whitefish morphs with insights on the genetic basis of their reproductive isolation

The European whitefish (Coregonus lavaretus) species complex is a classic example of recent adaptive radiation. Here, we examine a whitefish population introduced to northern Finnish Lake Tsahkal in the late 1960s, where three divergent morphs (viz. littoral, pelagic, and profundal feeders) were found 10 generations after. Using demographic modeling based on genomic data, we show that whitefish morphs evolved during a phase of strict isolation, refuting a rapid sympatric divergence scenario. The lake is now an artificial hybrid zone between morphs originated in allopatry. Despite their current syntopy, clear genetic differentiation remains between two of the three morphs. Using admixture mapping, we identify five SNPs associated with gonad weight variation, a proxy for sexual maturity and spawning time. We suggest that ecological adaptations in spawning time evolved in allopatry are currently maintaining partial reproductive isolation in the absence of other barriers to gene flow.Peer reviewe

The role of predation risk in structuring life-history traits of crucian carp (Carassius carassius) in a series of small boreal lakes

Predation is a major evolutionary force determining life-history traits in prey by directand indirect mechanisms. This study focuses on life-history trait variation in cruciancarp (Carassius carassius), a species well known for developing a deep body as aninducible morphological defence against predation risk. Here, the authors tested vari-ation in growth and reproductive traits in 15 crucian carp populations in lakes along apredation risk gradient represented by increasingly efficient predator communities.Lakes were located in south-eastern Norway and were sampled in summer 2018 and2019. The authors expected crucian carp to attain higher growth rate, larger size, andlater age at maturity with increasing predation risk. In the absence of predators, theyexpected high adult mortality, early maturity and increased reproductive effortcaused by strong intraspecific competition. They found that the life-history traits ofcrucian carp were clearly related to the presence of piscivores: with increasing preda-tion risk, fish grew in body length and depth and attained larger asymptotic lengthand size at maturity. This growth was evident at young age, especially in productivelakes with pike, and it suggests that fish quickly outgrew the predation window byreaching a size refuge. Contrary to the authors’predictions, populations had similarage at maturity. High-predation lakes also presented low density of crucian carp. Thissuggests that fish from predator lakes may experience high levels of resource avail-ability due to reduced intraspecific competition. Predation regulated life-history traitsin crucian carp populations, where larger size, higher longevity and size at maturitywere observed in lakes with large gaped predators.publishedVersio

Climate and productivity affect total mercury concentration and bioaccumulation rate of fish along a spatial gradient of subarctic lakes

Climate change is resulting in increased temperatures and precipitation in subarctic regions of Europe. These changes are extending tree lines to higher altitudes and latitudes, and enhancing tree growth enabling intensification of forestry into previously inhospitable subarctic regions. The combined effects of climate change and land-use intensification extend the warm, open-water season in subarctic lakes and increase lake productivity and may also increase leaching andmethylation activity of mercury within the lakes. To assess the joint effects of climate and productivity on total mercury (THg) bioaccumulation in fish, we conducted a space-for-time substitution study in 18 tributary lakes of a subarcticwatercourse forming a gradient fromcold pristine oligotrophic lakes in the northern headwaters to warmer and increasingly human-altered mesotrophic and eutrophic systems in the southern lower reaches. Increasing temperature, precipitation, and lake productivity were predicted to elevate length-and age-adjusted THg concentrations, as well as THg bioaccumulation rate (the rate of THg bioaccumulation relative to length or age) in muscle tissue of European whitefish (Coregonus lavaretus), vendace (Coregonus albula), perch (Perca fluviatilis), pike (Esox lucius), roach (Rutilus rutilus) and ruffe (Gymnocephalus cernua). A significant positive relationship was observed between age-adjusted THg concentration and lake climateproductivity in vendace (r(2) = 0.50), perch (r(2) = 0.51), pike (r(2) = 0.55) and roach (r(2) = 0.61). Higher climate-productivity values of the lakes also had a positive linear (pike; r(2) = 0.40 and whitefish; r(2)= 0.72) or u-shaped (perch; r(2) = 0.64 and ruffe; r(2) = 0.50) relationship with THg bioaccumulation rate. Our findings of increased adjusted THg concentrations in planktivores and piscivores reveal adverse effects of warming climate and increasing productivity on these subarctic fishes, whereas less distinct trends in THg bioaccumulation rate suggest more complex underlying processes. Joint environmental stressors such as climate and productivity should be considered in ongoing and future monitoring of mercury concentrations. (C) 2018 Elsevier B.V. All rights reserved.Peer reviewe

Simulated eutrophication and browning alters zooplankton nutritional quality and determines juvenile fish growth and survival

The first few months of life is the most vulnerable period for fish and their optimal hatching time with zooplankton prey is favored by natural selection. Traditionally, however, prey abundance (i.e., zooplankton density) has been considered important, whereas prey nutritional composition has been largely neglected in natural settings. High-quality zooplankton, rich in both essential amino acids (EAAs) and fatty acids (FAs), are required as starting prey to initiate development and fast juvenile growth. Prey quality is dependent on environmental conditions, and, for example, eutrophication and browning are two major factors defining primary producer community structures that will directly determine the nutritional quality of the basal food sources (algae, bacteria, terrestrial matter) for zooplankton. We experimentally tested how eutrophication and browning affect the growth and survival of juvenile rainbow trout (Oncorhynchus mykiss) by changing the quality of basal resources. We fed the fish on herbivorous zooplankton (Daphnia) grown with foods of different nutritional quality (algae, bacteria, terrestrial matter), and used GC-MS, stable isotope labeling as well as bulk and compound-specific stable isotope analyses for detecting the effects of different diets on the nutritional status of fish. The content of EAAs and omega-3 (ω-3) polyunsaturated FAs (PUFAs) in basal foods and zooplankton decreased in both eutrophication and browning treatments. The decrease in ω-3 PUFA and especially docosahexaenoic acid (DHA) was reflected to fish juveniles, but they were able to compensate for low availability of EAAs in their food. Therefore, the reduced growth and survival of the juvenile fish was linked to the low availability of DHA. Fish showed very low ability to convert alpha-linolenic acid (ALA) to DHA. We conclude that eutrophication and browning decrease the availability of the originally phytoplankton-derived DHA for zooplankton and juvenile fish, suggesting bottom-up regulation of food web quality.Peer reviewe

Ecological speciation in a generalist consumer expands the trophic niche of a dominant predator

Ecological speciation - whereby an ancestral founder species diversifies to fill vacant niches - is a phenomenon characteristic of newly formed ecosystems. Despite such ubiquity, ecosystem-level effects of such divergence remain poorly understood. Here, we compared the trophic niche of European whitefish (Coregonus lavaretus) and their predators in a series of contrasting subarctic lakes where this species had either diversified into four ecomorphologically distinct morphs or instead formed monomorphic populations. We found that the trophic niche of whitefish was almost three times larger in the polymorphic than in the monomorphic lakes, due to an increase in intraspecific specialisation. This trophic niche expansion was mirrored in brown trout (Salmo trutta), a major predator of whitefish. This represents amongst the first evidence for ecological speciation directly altering the trophic niche of a predator. We suggest such mechanisms may be a common and important - though presently overlooked - factor regulating trophic interactions in diverse ecosystems globally.Peer reviewe

A brain and a head for a different habitat : Size variation in four morphs of Arctic charr (Salvelinus alpinus(L.)) in a deep oligotrophic lake

Adaptive radiation is the diversification of species to different ecological niches and has repeatedly occurred in different salmonid fish of postglacial lakes. In Lake Tinnsjoen, one of the largest and deepest lakes in Norway, the salmonid fish, Arctic charr (Salvelinus alpinus(L.)), has likely radiated within 9,700 years after deglaciation into ecologically and genetically segregated Piscivore, Planktivore, Dwarf, and Abyssal morphs in the pelagial, littoral, shallow-moderate profundal, and deep-profundal habitats. We compared trait variation in the size of the head, the eye and olfactory organs, as well as the volumes of five brain regions of these four Arctic charr morphs. We hypothesised that specific habitat characteristics have promoted divergent body, head, and brain sizes related to utilized depth differing in environmental constraints (e.g., light, oxygen, pressure, temperature, and food quality). The most important ecomorphological variables differentiating morphs were eye area, habitat, and number of lamellae. The Abyssal morph living in the deepest areas of the lake had the smallest brain region volumes, head, and eye size. Comparing the olfactory bulb with the optic tectum in size, it was larger in the Abyssal morph than in the Piscivore morph. The Piscivore and Planktivore morphs that use more illuminated habitats have the largest optic tectum volume, followed by the Dwarf. The observed differences in body size and sensory capacities in terms of vision and olfaction in shallow and deepwater morphs likely relates to foraging and mating habitats in Lake Tinnsjoen. Further seasonal and experimental studies of brain volume in polymorphic species are needed to test the role of plasticity and adaptive evolution behind the observed differences.Peer reviewe

Predator community and resource use jointly modulate the inducible defense response in body height of crucian carp

Phenotypic plasticity can be expressed as changes in body shape in response to environmental variability. Crucian carp (Carassius carassius), a widespread cyprinid, displays remarkable plasticity in body morphology and increases body depth when exposed to cues from predators, suggesting the triggering of an antipredator defense mechanism. However, these morphological changes could also be related to resource use and foraging behavior, as an indirect effect of predator presence. In order to de-termine whether phenotypic plasticity in crucian carp is driven by a direct or indirect response to predation threat, we compared twelve fish communities inhabiting small lakes in southeast Norway grouped by four categories of predation regimes: no predator fish, or brown trout (Salmo trutta), perch (Perca fluviatilis), or pike (Esox lucius) as main piscivores. We predicted the body shape of crucian carp to be associated with the species composition of predator communities and that the presence of efficient piscivores would result in a deeper body shape. We use stable isotope analyses to test whether this variation in body shape was related to a shift in individual resource use- that is, littoral rather than pelagic resource use would favor the development of a specific body shape- or other environmental characteristics. The results showed that increasingly efficient predator communities induced progressively deeper body shape, larger body size, and lower population densities. Predator maximum gape size and individual trophic position were the best variables explaining crucian carp variation in body depth among predation categories, while littoral resource use did not have a clear effect. The gradient in predation pressure also corresponded to a shift in lake productivity. These results indicate that crucian carp have a fine-tuned morpho-logical defense mechanism against predation risk, triggered by the combined effect of predator presence and resource availabilitypublishedVersio

Total mercury concentrations in liver and muscle of European whitefish (Coregonus lavaretus (L.)) in a subarctic lake - Assessing the factors driving year-round variation

Subarctic lakes are characterised by extreme seasonal variation in light and temperature which influences growth, maturation, condition and resource use of fishes. However, our understanding of how seasonal changes affect mercury concentrations of fishes is limited. We conducted a year-round study (3 ice-covered months, 3 open-water months) with open-water inter-annual aspect (3 years: samples from August/September), focusing on total mercury (THg) concentrations and ecological characteristics of a common freshwater fish, European whitefish (Coregonus lavaretus (L.)) from a subarctic lake. We measured THg concentrations from tissues with fast (liver, n = 164) and moderate (muscle, n = 225) turnover rates, providing information on THg dynamics over different temporal scales. In both tissues, lipid-corrected THg concentrations were highest in winter (liver: 1.70 +/- 0.88 mu g/g, muscle: 0.24 +/- 0.05 mu g/g) and lowest in summer (liver: 0.87 +/- 0.72 mu g/g, muscle: 0.19 +/- 0.04 mu g/g). THg concentrations increased in winter following the summer-autumn dietary shift to pelagic zooplankton and starvation after spawning. Whitefish THg concentrations decreased towards summer, and were associated with consumption of benthic macroinvertebrates and subsequent growth dilution. Mercury bio-accumulated in both tissues with age, both showing the strongest regression slopes in winter and lowest in summer. THg concentrations in liver and muscle tissue were correlated throughout the year, however the correlation was lowest in summer, indicating high metabolism during somatic growing season in summer and growth dilution. Multiple linear regression models explained 50% and 55% of the THg variation in liver and muscle both models dominated by seasonally-variable factors i.e. sexual maturity, delta C-13, and condition factor. Seasonally varying bioaccumulation slopes and the higher level of intra-annual variation (21%) in whitefish THg concentration in muscle than the inter-annual accumulation (8%) highlight the importance of including seasonal factors in future THg studies. (C) 2017 Elsevier Ltd. All rights reserved.Peer reviewe