Migratory-derived resources induce elongated food chains through middle-up food web effects.

BACKGROUND: Seasonal movements of animals often result in the transfer of large amounts of energy and nutrients across ecosystem boundaries, which may have large consequences on local food webs through various pathways. While this is known for both terrestrial- and aquatic organisms, quantitative estimates on its effects on food web structure and identification of key pathways are scarce, due to the difficulty in obtaining replication on ecosystem level with negative control, i.e. comparable systems without migration. METHODS: In this study, we estimate the impact of Arctic charr (Salvelinus alpinus) migration on riverine ecosystem structure, by comparing multiple streams with strictly resident populations above natural migration barriers with streams below those barriers harboring partially migratory populations. We compared density estimates and size structure between above and below populations. Diet differences were examined through the analysis of stomach contents, changes in trophic position were examined by using stable isotopes. To infer growth rate of resident individuals, back-growth calculation was performed using otoliths. RESULTS: We find higher densities of small juveniles in partially migratory populations, where juvenile Arctic charr show initially lower growth, likely due to higher intraspecific competition. After reaching a size, where they can start feeding on eggs and smaller juveniles, which are both more frequent in partially migratory populations, growth surpasses that of resident populations. Cannibalism induced by high juvenile densities occurred almost exclusively in populations with migration and represents an altered energy pathway to the food web. The presence of large cannibalistic charr feeding on smaller ones that have a similar trophic level as charr from strictly resident populations (based on stomach content) coupled with steeper δ15N-size regression slopes illustrate the general increase of food chain length in systems with migration. CONCLUSIONS: Our results thus suggest that the consumption of migration-derived resources may result in longer food chains through middle-up rather than bottom-up effects. Furthermore, by occupying the apex of the food chain and feeding on juvenile conspecifics, resident individuals experience reduced competition with their young counterparts, which potentially balances their fitness with migratory individuals.

Neglecting biodiversity baselines in longitudinal river connectivity restoration impacts priority setting.

River habitats are fragmented by barriers which impede the movement and dispersal of aquatic organisms. Restoring habitat connectivity is a primary objective of nature conservation plans with multiple efforts to strategically restore connectivity at local, regional, and global scales. However, current approaches to prioritize connectivity restoration do not typically consider how barriers spatially fragment species' populations. Additionally, we lack knowledge on biodiversity baselines to predict which species would find suitable habitat after restoring connectivity. In this paper, we asked how neglecting these biodiversity baselines in river barrier removals impacts priority setting for conservation planning. We applied a novel modelling approach combining predictions of species distributions with network connectivity models to prioritize conservation actions in rivers of the Rhine-Aare system in Switzerland. Our results show that the high number and density of barriers has reduced structural and functional connectivity across representative catchments within the system. We show that fragmentation decreases habitat suitability for species and that using expected distributions as biodiversity baselines significantly affects priority settings for connectivity restorations compared to species-agnostic metrics based on river length. This indicates that priorities for barrier removals are ranked higher within the expected distributions of species to maximize functional connectivity while barriers in unsuitable regions are given lower importance scores. Our work highlights that the joint consideration of existing barriers and species past and current distributions are critical for restoration plans to ensure the recovery and persistence of riverine fish diversity.

Warming underpins community turnover in temperate freshwater and terrestrial communities.

Rising temperatures are leading to increased prevalence of warm-affinity species in ecosystems, known as thermophilisation. However, factors influencing variation in thermophilisation rates among taxa and ecosystems, particularly freshwater communities with high diversity and high population decline, remain unclear. We analysed compositional change over time in 7123 freshwater and 6201 terrestrial, mostly temperate communities from multiple taxonomic groups. Overall, temperature change was positively linked to thermophilisation in both realms. Extirpated species had lower thermal affinities in terrestrial communities but higher affinities in freshwater communities compared to those persisting over time. Temperature change's impact on thermophilisation varied with community body size, thermal niche breadth, species richness and baseline temperature; these interactive effects were idiosyncratic in the direction and magnitude of their impacts on thermophilisation, both across realms and taxonomic groups. While our findings emphasise the challenges in predicting the consequences of temperature change across communities, conservation strategies should consider these variable responses when attempting to mitigate climate-induced biodiversity loss.

Temperature regime during embryogenesis alters subsequent behavioural phenotypes of juvenile brown trout.

Climate warming imposes a serious threat, especially to freshwater ecosystems in temperate and (sub)polar regions, which are often dominated by cold-adapted ectotherms. Although relatively intense warming during winter is common across the climatic regions, comparably little focus has been put on the organismal impacts of winter warming. Embryonic development, which is exceptionally susceptible to ambient temperature, occurs during winter in various freshwater ectotherms. Yet, our knowledge of the effects of increased temperature during embryogenesis on later life stages is limited. Using brown trout (Salmo trutta), we examined how a 1.5°C temperature increase from fertilization to hatching affects various traits at the onset of the free-swimming stage (i.e. a comparison between 3.5 and 5.0°C treatments). Although all hatchlings were kept at the same temperature (7.0°C) from hatching to the onset of the free-swimming stage for about two months, the temperature increase during embryogenesis substantially reduced key ecological behaviours, i.e. activity and exploration levels, at the onset of the free-swimming stage despite only marginal temperature effects on morphological and physiological traits at this stage. Given the importance of behavioural traits in early growth and survival, our study suggests a likely pathway through which subtle changes in mean winter temperature affect early fitness.

Blue and green food webs respond differently to elevation and land use.

While aquatic (blue) and terrestrial (green) food webs are parts of the same landscape, it remains unclear whether they respond similarly to shared environmental gradients. We use empirical community data from hundreds of sites across Switzerland and a synthesis of interaction information in the form of a metaweb to show that inferred blue and green food webs have different structural and ecological properties along elevation and among various land-use types. Specifically, in green food webs, their modular structure increases with elevation and the overlap of consumers' diet niche decreases, while the opposite pattern is observed in blue food webs. Such differences between blue and green food webs are particularly pronounced in farmland-dominated habitats, indicating that anthropogenic habitat modification modulates the climatic effects on food webs but differently in blue versus green systems. These findings indicate general structural differences between blue and green food webs and suggest their potential divergent future alterations through land-use or climatic changes.

Climate, immigration and speciation shape terrestrial and aquatic biodiversity in the European Alps.

Quaternary climate fluctuations can affect speciation in regional biodiversity assembly in two non-mutually exclusive ways: a glacial species pump, where isolation in glacial refugia accelerates allopatric speciation, and adaptive radiation in underused adaptive zones during ice-free periods. We detected biogeographic and genetic signatures associated with both mechanisms in the assembly of the biota of the European Alps. Age distributions of endemic and widespread species within aquatic and terrestrial taxa (amphipods, fishes, amphibians, butterflies and flowering plants) revealed that endemic fish evolved only in lakes, are highly sympatric, and mainly of Holocene age, consistent with adaptive radiation. Endemic amphipods are ancient, suggesting preglacial radiation with limited range expansion and local Pleistocene survival, perhaps facilitated by a groundwater-dwelling lifestyle. Terrestrial endemics are mostly of Pleistocene age and are thus more consistent with the glacial species pump. The lack of evidence for Holocene adaptive radiation in the terrestrial biome is consistent with faster recolonization through range expansion of these taxa after glacial retreats. More stable and less seasonal ecological conditions in lakes during the Holocene may also have contributed to Holocene speciation in lakes. The high proportion of young, endemic species makes the Alpine biota vulnerable to climate change, but the mechanisms and consequences of species loss will likely differ between biomes because of their distinct evolutionary histories.

Timing and synchrony of migration in a freshwater fish: Consequences for survival.

Animal migration is one of the most spectacular and visible behavioural phenomena in nature with profound implications for a range of ecological and evolutionary processes. Successful migration hinges on the ability to exploit temporary resources (e.g. food) and evade threats (e.g. predators) as they arise, and thus the timing of migration is often regarded as a dominant predictor of individual migratory success. However, with the exception of intensively studied taxa (mainly birds), relatively few studies have investigated inter-individual annual and seasonal variation in migratory timing and performance, or tested predictions on how migration across high and low predation-risk habitats may exert selection on migratory timing. In particular, studies that assess the survival consequences of variation in migratory timing remain rare, which is most likely due to the logistical challenges associated with monitoring survival success and population-level characteristics simultaneously. Here, we address the above-mentioned questions using roach Rutilus rutilus, a fish that migrates from lakes characterised by high predation risk into low-risk streams during winter. Specifically, we used individual-based tracking of roach in two European lake systems over multiple migration periods (9 and 7 years respectively), to obtain highly detailed (year-round scheduling, repeat journeys and the fate of individuals) data on the variability/synchrony of migratory timing in spring and autumn respectively. We report seasonal differences in the variability of migratory timing, with lower variance and higher migration synchrony in spring lake arrival timing as compared to autumn lake departure timing. Furthermore, the timing of autumn migration is more variable across years than the timing of spring migration. Second, we find that later arrival to the lake habitat is positively associated with apparent survival from 1 year to the next, whereas we found no effect of lake departure timing on survival probability. These findings represent rare evidence showing how intraspecific variation in timing in migratory fish differs across years and seasons, and how variation in timing can translate into survival consequences for prey in systems characterised by high predation risk.

The influence of predator community composition on photoprotective traits of copepods.

Trait expression of natural populations often jointly depends on prevailing abiotic environmental conditions and predation risk. Copepods, for example, can vary their expression of compounds that confer protection against ultraviolet radiation (UVR), such as astaxanthin and mycosporine-like amino acids (MAAs), in relation to predation risk. Despite ample evidence that copepods accumulate less astaxanthin in the presence of predators, little is known about how the community composition of planktivorous fish can affect the overall expression of photoprotective compounds. Here, we investigate how the (co-)occurrence of Arctic charr (Salvelinus alpinus) and threespine stickleback (Gasterosteus aculeatus) affects the photoprotective phenotype of the copepod Leptodiaptomus minutus in lake ecosystems in southern Greenland. We found that average astaxanthin and MAA contents were lowest in lakes with stickleback, but we found no evidence that these photoprotective compounds were affected by the presence of charr. Furthermore, variance in astaxanthin among individual copepods was greatest in the presence of stickleback and the astaxanthin content of copepods was negatively correlated with increasing stickleback density. Overall, we show that the presence and density of stickleback jointly affect the content of photoprotective compounds by copepods, illustrating how the community composition of predators in an ecosystem can determine the expression of prey traits that are also influenced by abiotic stressors.

Conspecific migration and environmental setting determine parasite infracommunities of non-migratory individual fish.

Parasite infracommunities tend to be stochastic in nature, although environmental characteristics such as the type of water source in streams and host traits can have an effect on the biotic assemblages and by extension the parasite fauna. We examined the effect of water source and the rate of adult fish migration on the metazoan parasite infracommunities of conspecific juvenile brown trout, Salmo trutta L. among streams flowing into Lake Lucerne (Switzerland). Juvenile (1 to 2-year old) fish harboured higher parasite species richness in groundwater-fed than in surface water-fed streams, whereas the rate of fish migration did not affect infracommunity richness. Heteroxenous species were more common in groundwater-fed streams with high and medium rates of trout migration, whereas infracommunities in surface water-fed streams and streams with low rates of fish migration were dominated by one monoxenous parasite or lacked infections. Similarity in the parasite infracommunity composition of juvenile trout across streams was explained by the interaction between type of water source and adult migration rates. Our conclusions support that similarity in the parasite composition of resident freshwater conspecifics can be predicted by the local environmental settings and host migratory behaviour, whereas parasite richness is mainly influenced by the environmental characteristics.

Using PIT-tags and portable antennas for quantification of fish movement and survival in streams under different environmental conditions.

While PIT-tag tracking using mobile antennas is being increasingly used to study fish movement and survival in streams, little is known about the limitations of the method, especially over longer periods of time and under different environmental settings. We used 6 years of data combining tagging, mobile antenna tracking and recaptures of Salmo trutta in multiple small streams in the Lake Lucerne drainage area in Switzerland to evaluate the relative importance of different environmental and intrinsic factors affecting the efficiency of the method. Our study system and experimental design allowed us to accurately verify the continuous presence and survival of recaptured fish in the stream after tracking, which meant that we could estimate detection probability with high confidence. The mean detection probability of tagged trout was 43%, but we found that fish length had a strong negative effect on detection probability, especially in males. Multivariate axes of stream environmental features did not predict efficiency but stream width alone was significantly positively correlated with efficiency. Additionally, stream temperature when tracking had a positive effect on fish detectability. Tag loss at recapture was globally rare (<8%) but common in large postspawn females (>30%). Based on the escape response of fish after detection, we could estimate the proportion of ghost tags, which reached a plateau of around 80% 2 years after tagging. We finally showed that our models of tag loss, fish detection and escape response are needed to interpret detection events. Our results highlight that individual variation in detection probability and tag loss is high and has to be considered for analysis.

Maladaptive migration behaviour in hybrids links to predator-mediated ecological selection.

Different migratory species have evolved distinct migratory characteristics that improve fitness in their particular ecological niches. However, when such species hybridize, migratory traits from parental species can combine maladaptively and cause hybrids to fall between parental fitness peaks, with potential consequences for hybrid viability and species integrity. Here, we take advantage of a natural cross-breeding incident to study migratory behaviour in naturally occurring hybrids as well as in their parental species and explore links between migratory traits and predation risk. To achieve this, we used electronic tags and passive telemetry to record detailed individual migration patterns (timing and number of migratory trips) in two common freshwater fish species, roach Rutilus rutilus, common bream Abramis brama as well as their hybrids. Next, we scanned for tags regurgitated by a key avian predator (great cormorant Phalacrocorax carbo) at nearby roosting sites, allowing us to directly link migratory behaviour to predation risk in the wild. We found that hybrid individuals showed a higher number of short, multi-trip movements between lake and stream habitats as compared to both parental species. The mean date of first lake departure differed between bream and roach by more than 10 days, while hybrids departed in two distinct peaks that overlapped with the parental species' averages. Moreover, the probability of cormorant predation increased with multi-trip movement frequency across species and was higher for hybrids. Our data provide novel insights into hybrid viability, with links to predator-mediated ecological selection. Increased exposure to predators via maladaptive migratory behaviour reduces hybrid survival and can thereby reinforce species integrity.

A field evaluation of long-term effects of PIT tagging.

Passive integrated transponder (PIT)-tagging is commonly used in behavioural studies of fish, although long-term evaluations of effects from tagging under natural conditions are scarce. We PIT-tagged common bream Abramis brama, European perch Perca fluviatilis, pike Esox lucius and roach Rutilus rutilus, released them in their lakes of origin and recaptured them after 103-3269 days. Overall, tagged fish did not differ in condition from non-tagged fish, except for small R. rutilus that had a lower length-specific body mass in one lake in 1 year. We conclude that PIT-tagging in general has negligible long-term effects on fish condition.

Ecological opportunity shapes a large Arctic charr species radiation.

Ecological opportunity is considered a crucial factor for adaptive radiation. Here, we combine genetic, morphological and ecological data to assess species and ecomorphological diversity of Artic charr in six lakes of a catchment in southernmost Greenland, where only charr and stickleback occur. Because the diversity of habitats and resources increases with lake size, we predict a positive association between lake size and the extent of ecomorphological diversity. The largest lake of the catchment harbours the largest Arctic charr assemblage known today. It consists of six genetically differentiated species belonging to five ecomorphs (anadromous, littoral benthic, profundal dwarf, planktivorous, piscivorous), of which the latter comprises two ecomorphologically extremely similar species. Lakes of intermediate size contain two ecomorphologically and genetically distinct species. Small lakes harbour one genetically homogeneous, yet sometimes ecomorphologically variable population. Supporting our prediction, lake size is positively correlated with the extent of ecomorphological specialization towards profundal, pelagic and piscivorous lifestyle. Furthermore, assemblage-wide morphospace increases sharply when more than one genetic cluster is present. Our data suggest that ecological opportunity and speciation jointly determine phenotypic expansion in this charr radiation.

Heritable morphological differentiation in salmonids from two distinct stream types.

We tested for phenotype-to-habitat associations in brown trout Salmo trutta populations from two ecologically different habitat types; i.e., groundwater and surface-water-fed streams. Additionally, we raised captive offspring from two such populations under standardised conditions to test whether potential phenotypic differentiation would be passed on to offspring. We found analogous differentiation by habitat in multiple wild populations. Some of these morphological differences were at least partially inherited by offspring. We suggest that this could have implications for both scientists and fisheries authorities studying or managing trout populations.

Size-dependent tradeoffs in seasonal freshwater environments facilitate differential salmonid migration.

BACKGROUND: Seasonal spatio-temporal variation in habitat quality and abiotic conditions leads to animals migrating between different environments around the world. Whereas mean population timing of migration is often fairly well understood, explanations for variation in migratory timing within populations are often lacking. Condition-dependent tradeoffs may be an understudied mechanism that can explain this differential migration. While fixed condition-specific thresholds have been identified in earlier work on ontogenetic niche shifts, they are rare in differential migration, suggesting that thresholds in such systems can shift based on temporally variable environmental conditions. METHODS: We introduced a model based on size-specific tradeoffs between migration and growth in seasonal environments. We focused on optimal migratory timing for first-time migrants with no knowledge of an alternative habitat, which is a crucial stage in the life history of migratory salmonids. We predicted that optimal timing would occur when individuals move from their natal habitats based on a seasonally variable ratio of predation and growth. When the ratio becomes slightly more favorable in the alternative habitat, migratory movement can occur. As it keeps shifting throughout the season, the threshold for migration is variable, allowing smaller individuals to move at later dates. We compared our model predictions to empirical data on 3 years of migratory movement of more than 800 juvenile trout of varying size from natal to feeding habitat. RESULTS: Both our model and empirical data showed that large individuals, which are assumed to have a lower predation risk in the migratory habitat, move earlier in the season than smaller individuals, whose predicted predation-to-growth ratio shifted to being favorable only later in the migratory season. Our model also predicted that the observed difference in migratory timing between large and small migrants occurred most often at low values of growth differential between the two habitats, suggesting that it was not merely high growth potential but rather the tradeoff between predation and growth that shaped differential migration patterns. CONCLUSIONS: We showed the importance of considering condition-specific tradeoffs for understanding temporal population dynamics in spatially structured landscapes. Rather than assuming a fixed threshold, which appears to be absent based on previous work on salmonids, we showed that the body-size threshold for migration changed temporally throughout the season. This allowed increasingly smaller individuals to migrate when growth conditions peaked in the migratory habitat. Our model illuminates an understudied aspect of predation as part of a condition-dependent tradeoff that shapes migratory patterns, and our empirical data back patterns predicted by this model.

Upward Adaptive Radiation Cascades: Predator Diversification Induced by Prey Diversification.

The value of biodiversity is widely appreciated, but we are only beginning to understand the interplay of processes that generate biodiversity and their consequences for coevolutionary interactions. Whereas predator-prey coevolution is most often analyzed in the context of evolutionary arms races, much less has been written about how predators are affected by, and respond to, evolutionary diversification in their prey. We hypothesize here that adaptive radiation of prey may lead to diversification and potentially speciation in predators, a process that we call an upwards adaptive radiation cascade. In this paper we lay out the conceptual basis for upwards adaptive radiation cascades, explore evidence for such cascades, and finally advocate for intensified research.

Species integrity enhanced by a predation cost to hybrids in the wild.

Species integrity can be challenged, and even eroded, if closely related species can hybridize and produce fertile offspring of comparable fitness to that of parental species. The maintenance of newly diverged or closely related species therefore hinges on the establishment and effectiveness of pre- and/or post-zygotic reproductive barriers. Ecological selection, including predation, is often presumed to contribute to reduced hybrid fitness, but field evidence for a predation cost to hybridization remains elusive. Here we provide proof-of-concept for predation on hybrids being a postzygotic barrier to gene flow in the wild. Cyprinid fishes commonly produce fertile, viable hybrid offspring and therefore make excellent study organisms to investigate ecological costs to hybrids. We electronically tagged two freshwater cyprinid fish species (roach Rutilus rutilus and bream Abramis brama) and their hybrids in 2005. Tagged fish were returned to their lake of origin, exposing them to natural predation risk from apex avian predators (great cormorant, Phalacrocorax carbo). Scanning for regurgitated tags under cormorant roosts 3-4 years later identified cormorant-killed individual fish and allowed us to directly test for a predation cost to hybrids in the wild. Hybrid individuals were found significantly more susceptible to cormorant predation than individuals from either parental species. Such ecological selection against hybrids contributes to species integrity, and can enhance species diversification.

A predation cost to bold fish in the wild.

Studies of predator-mediated selection on behaviour are critical for our understanding of the evolution and maintenance of behavioural diversity in natural populations. Consistent individual differences in prey behaviour, especially in the propensity to take risks ("boldness"), are widespread in the animal kingdom. Theory predicts that individual behavioural types differ in a cost-benefit trade-off where bolder individuals benefit from greater access to resources while paying higher predation-risk costs. However, explicitly linking predation events to individual behaviour under natural conditions is challenging and there is currently little data from the wild. We assayed individual behaviour and electronically tagged hundreds of fish (roach, Rutilus rutilus) before releasing them into their lake of origin, thereby exposing them to predation risk from avian apex predators (cormorants, Phalacrocorax carbo). Scanning for regurgitated tags at the cormorant roosting site provided data on individual predation events. We found that fish with higher boldness have a greater susceptibility to cormorant predation compared to relatively shy, risk-averse individuals. Our findings hereby provide unique and direct evidence of behavioural type-dependent predation vulnerability in the wild, i.e. that there is a predation cost to boldness, which is critical for our understanding of the evolution and maintenance of behavioural diversity in natural populations.

Emergence of a novel prey life history promotes contemporary sympatric diversification in a top predator.

Intraspecific phenotypic variation can strongly impact community and ecosystem dynamics. Effects of intraspecific variation in keystone species have been shown to propagate down through the food web by altering the adaptive landscape for other species and creating a cascade of ecological and evolutionary change. However, similar bottom-up eco-evolutionary effects are poorly described. Here we show that life history diversification in a keystone prey species, the alewife (Alosa pseudoharengus), propagates up through the food web to promote phenotypic diversification in its native top predator, the chain pickerel (Esox niger), on contemporary timescales. The landlocking of alewife by human dam construction has repeatedly created a stable open water prey resource, novel to coastal lakes, that has promoted the parallel emergence of a habitat polymorphism in chain pickerel. Understanding how strong interactions propagate through food webs to influence diversification across multiple trophic levels is critical to understand eco-evolutionary interactions in complex natural ecosystems.

Escaping peril: perceived predation risk affects migratory propensity.

Although migratory plasticity is increasingly documented, the ecological drivers of plasticity are not well understood. Predation risk can influence migratory dynamics, but whether seasonal migrants can adjust their migratory behaviour according to perceived risk is unknown. We used electronic tags to record the migration of individual roach (Rutilus rutilus), a partially migratory fish, in the wild following exposure to manipulation of direct (predator presence/absence) and indirect (high/low roach density) perceived predation risk in experimental mesocosms. Following exposure, we released fish in their lake summer habitat and monitored individual migration to connected streams over an entire season. Individuals exposed to increased perceived direct predation risk (i.e. a live predator) showed a higher migratory propensity but no change in migratory timing, while indirect risk (i.e. roach density) affected timing but not propensity showing that elevated risk carried over to alter migratory behaviour in the wild. Our key finding demonstrates predator-driven migratory plasticity, highlighting the powerful role of predation risk for migratory decision-making and dynamics.