Ponds as experimental arenas for studying animal movement: current research and future prospects.

Animal movement is a multifaceted process that occurs for multiple reasons with powerful consequences for food web and ecosystem dynamics. New paradigms and technical innovations have recently pervaded the field, providing increasingly powerful means to deliver fine-scale movement data, attracting renewed interest. Specifically in the aquatic environment, tracking with acoustic telemetry now provides integral spatiotemporal information to follow individual movements in the wild. Yet, this technology also holds great promise for experimental studies, enhancing our ability to truly establish cause-and-effect relationships. Here, we argue that ponds with well-defined borders (i.e. "islands in a sea of land") are particularly well suited for this purpose. To support our argument, we also discuss recent experiences from studies conducted in an innovative experimental infrastructure, composed of replicated ponds equipped with modern aquatic telemetry systems that allow for unparalleled insights into the movement patterns of individual animals.

Timing is everything; operational changes at a pumping station with a gravity sluice to provide safe downstream passage for silver European eels and deliver considerable financial savings.

Catadromous European eel (Anguilla anguilla) are a critically endangered fish species due in part to in-river anthropogenic barriers (e.g., pumping stations, weirs, hydropower facilities). European legislation stipulates that safe downstream passage must be provided at hazardous intakes. Where present, gravity sluices have the potential to act as safe and low-cost downstream passage for seaward migrating silver eels at pumping station, but operational changes are required. This study used catchment-wide and fine-scale acoustic telemetry to investigate if operational changes (OC) at a pumping station (PS) with a co-located gravity sluice (GS) facilitated safe downstream passage for silver European eels. Specifically, night-time pump operations were ceased, river levels prior to sluicing were elevated and the GS was opened during key eel migration windows, i.e., at night during the new moon phase in autumn. No tagged eels passed through any pumps and the majority (2018 = 87.5%, 2020 = 88.9%) that approached the PS during OC passed downstream through the GS. Most eels approached during the first period of night sluicing after release (2018 = 73.9% and 2020 = 76.5%) and passed downstream during the first sluice event they experienced at the PS (2018 = 66.7% and 2020 = 75.0%). During the final approach prior to passage, very few retreats back upstream occurred at a median (IQR) distance of 34 (7.25) m from the GS and were predominantly a short distance (1-8 m). Overall, OC at a PS with a GS are considered a win-win-win, despite opening the sluice for <3% of the study period, given safe downstream passage was maximised, the financial benefits of sluicing water (∼£14,670 in direct operational costs over two years) and the relative ease of implementation.

Three-dimensional migratory behaviour of European silver eels (Anguilla anguilla) approaching a hydropower plant.

The global population of European eel (Anguilla anguilla) is rapidly declining, and migration barriers in rivers are believed to be one of several key causes. While progress has been made in the development of bypass solutions, they are often constructed based on a limited knowledge of swimming behaviour. A bypass close to the stream bed is often recommended at fish passage facilities to accommodate downstream eel migration. The results of this recommendation are poorly studied, and the few studies that exist show varying bypass efficiencies. The current study used acoustic telemetry with depth sensors to explore the three-dimensional migratory behaviour of downstream-migrating silver eels. The eels were tracked as they approached a hydropower plant with a state-of-the-art angled bar rack and full-depth bypass. Downstream and upstream swimming differed in preferred vertical and lateral positions. During periods of local downstream movement, the density of observations was largest in the upper middle section, away from the river boundaries and in higher velocities. Conversely, when moving upstream, eels tended to avoid the upper layers of the middle part of the river, swimming closer to the riverbed and using the bank areas to a greater extent. Downstream-moving fish swam higher in the water column during night and in turbid conditions (high discharge). When approaching the impassable bar rack and the full-depth bypass, the eels searched most intensely but not exclusively along the bottom third of the rack, often exploring at new depths after changing direction. The impediment passage efficiency was 100% when both bypass solutions were considered. The study provides knowledge of the swimming behaviour of silver eels, which is relevant for the design of bypass solutions for eels at migration barriers.

First tagging data on large Atlantic bluefin tuna returning to Nordic waters suggest repeated behaviour and skipped spawning.

Atlantic bluefin tuna (Thunnus thynnus; ABFT) is one of the most iconic fish species in the world. Recently, after being very rare for more than half a century, large bluefin tunas have returned to Nordic waters in late summer and autumn, marking the return of the largest predatory fish in Nordic waters. By tagging 18 bluefin tunas with electronic tags (pop-up satellite archival tags), we show that bluefin tuna observed in Nordic waters undertake different migration routes, with individuals migrating into the western Atlantic Ocean, while others stay exclusively in the eastern Atlantic and enter the Mediterranean Sea to spawn. We additionally present evidence of possible skipped spawning inferred from behavioural analyses. In Nordic waters, ABFT are primarily using the upper water column, likely reflecting feeding activity. The results support the hypothesis that ABFT migrating to Nordic waters return to the same general feeding area within the region on an annual basis. These observations may have important implications for management because (1) tunas that come into Nordic waters might represent only a few year classes (as evidenced by a narrow size range), and thus may be particularly vulnerable to area-specific exploitation, and (2) challenge the assumption of consecutive spawning in adult Atlantic bluefin tuna, as used in current stock assessment models. Without careful management and limited exploitation of this part of the ABFT population, the species' return to Nordic waters could be short-lived.

Big-data approaches lead to an increased understanding of the ecology of animal movement.

Understanding animal movement is essential to elucidate how animals interact, survive, and thrive in a changing world. Recent technological advances in data collection and management have transformed our understanding of animal "movement ecology" (the integrated study of organismal movement), creating a big-data discipline that benefits from rapid, cost-effective generation of large amounts of data on movements of animals in the wild. These high-throughput wildlife tracking systems now allow more thorough investigation of variation among individuals and species across space and time, the nature of biological interactions, and behavioral responses to the environment. Movement ecology is rapidly expanding scientific frontiers through large interdisciplinary and collaborative frameworks, providing improved opportunities for conservation and insights into the movements of wild animals, and their causes and consequences.

Contrasting structural complexity differentiate hunting strategy in an ambush apex predator.

Structural complexity is known to influence prey behaviour, mortality and population structure, but the effects on predators have received less attention. We tested whether contrasting structural complexity in two newly colonised lakes (low structural complexity lake-LSC; high structural complexity-HSC) was associated with contrasting behaviour in an aquatic apex predator, Northern pike (Esox lucius; hereafter pike) present in the lakes. Behaviour of pike was studied with whole-lake acoustic telemetry tracking, supplemented by stable isotope analysis of pike prey utilization and survey fishing data on the prey fish community. Pike displayed increased activity, space use, individual growth as well as behavioural differentiation and spent more time in open waters in the LSC lake. Despite observed differences between lakes, stable isotopes analyses indicated a high dependency on littoral food sources in both lakes. We concluded that pike in the HSC lake displayed a behaviour consistent with a prevalent ambush predation behaviour, whereas the higher activity and larger space use in the LSC lake indicated a transition to more active search behaviour. It could lead to increased prey encounter and cause better growth in the LSC lake. Our study demonstrated how differences in structural complexity mediated prominent changes in the foraging behaviour of an apex predator, which in turn may have effects on the prey community.

A role for lakes in revealing the nature of animal movement using high dimensional telemetry systems.

Movement ecology is increasingly relying on experimental approaches and hypothesis testing to reveal how, when, where, why, and which animals move. Movement of megafauna is inherently interesting but many of the fundamental questions of movement ecology can be efficiently tested in study systems with high degrees of control. Lakes can be seen as microcosms for studying ecological processes and the use of high-resolution positioning systems to triangulate exact coordinates of fish, along with sensors that relay information about depth, temperature, acceleration, predation, and more, can be used to answer some of movement ecology's most pressing questions. We describe how key questions in animal movement have been approached and how experiments can be designed to gather information about movement processes to answer questions about the physiological, genetic, and environmental drivers of movement using lakes. We submit that whole lake telemetry studies have a key role to play not only in movement ecology but more broadly in biology as key scientific arenas for knowledge advancement. New hardware for tracking aquatic animals and statistical tools for understanding the processes underlying detection data will continue to advance the potential for revealing the paradigms that govern movement and biological phenomena not just within lakes but in other realms spanning lands and oceans.

Redefining the oceanic distribution of Atlantic salmon.

Determining the mechanisms driving range-wide reductions in Atlantic salmon marine survival is hindered by an insufficient understanding of their oceanic ecology and distribution. We attached 204 pop-up satellite archival tags to post-spawned salmon when they migrated to the ocean from seven European areas and maiden North American salmon captured at sea at West Greenland. Individuals migrated further north and east than previously reported and displayed increased diving activity near oceanographic fronts, emphasizing the importance of these regions as feeding areas. The oceanic distribution differed among individuals and populations, but overlapped more between geographically proximate than distant populations. Dissimilarities in distribution likely contribute to variation in growth and survival within and among populations due to spatio-temporal differences in environmental conditions. Climate-induced changes in oceanographic conditions will alter the location of frontal areas and may have stock-specific effects on Atlantic salmon population dynamics, likely having the largest impacts on southern populations.

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.

The effects of hydrodynamics on the three-dimensional downstream migratory movement of Atlantic salmon.

Anthropogenic structures in rivers are major threats for fish migration and effective mitigation is imperative given the worldwide expansion of such structures. Fish behaviour is strongly influenced by hydrodynamics, but little is known on the relation between hydraulics and fish fine scale-movement. We combined 3D Computational fluid dynamics modelling (CFD) with 2D and 3D fish positioning to investigate the relation between hydrodynamics and the downstream movement of Atlantic salmon smolts (Salmo salar). We show that fish use fine-scale flow velocity and turbulence as navigation cues of fine-scale movement behaviour. Tri-dimensional swimming speed and swimming direction can be explained by adjustments of fish to flow motion, which are linked to fish swimming mode. Fish diverge from the flow by swimming at speeds within or higher than their prolonged speeds (0.38-0.73 m s-1). Flow direction plays a pivotal role on fish swimming performance, with high upstream and downwards velocities impacting swimming the most. Turbulence is also influential, by benefiting swimming performance at low TKE (< 0.03 m2 s-2) or constraining it at higher levels. We show that fish behaviour is affected by interactions of several hydraulic variables that should be considered jointly.

The influence of initial developmental status on the life-history of sea trout (Salmo trutta).

Spring migrating sea trout juveniles can be classified as parr, pre-smolt or smolt based on body morphology and osmoregulatory capacity. In this respect, parr are assumed to be less prepared for a marine life and to have lower survival at sea than pre-smolts and smolts. However, the behaviour and survival of these trout phenotypes upon entering the sea is not well known. Using passive integrated transponder telemetry, this study found that the return rate from the sea to the natal river was higher for parr compared to pre-smolts and smolts. Additionally, trout classified as parr generally migrated earlier to the sea and a larger proportion returned to the river after less than one year at sea. The daily mortality rate at sea was comparable among the different phenotypes of trout, suggesting that the higher proportion of returning parr to the river was linked to their shorter duration at sea. These results provide evidence of different life-history strategies for seaward-migrating juvenile sea trout, ultimately affecting their return rate to the natal river. Investigations failing to consider downstream migrating parr and pre-smolts risks neglecting a large part of the anadromous population and may result in inaccurate assessments of sea trout stocks in rivers.

Genetic analyses reveal complex dynamics within a marine fish management area.

Genetic data have great potential for improving fisheries management by identifying the fundamental management units-that is, the biological populations-and their mixing. However, so far, the number of practical cases of marine fisheries management using genetics has been limited. Here, we used Atlantic cod in the Baltic Sea to demonstrate the applicability of genetics to a complex management scenario involving mixing of two genetically divergent populations. Specifically, we addressed several assumptions used in the current assessment of the two populations. Through analysis of 483 single nucleotide polymorphisms (SNPs) distributed across the Atlantic cod genome, we confirmed that a model of mechanical mixing, rather than hybridization and introgression, best explained the pattern of genetic differentiation. Thus, the fishery is best monitored as a mixed-stock fishery. Next, we developed a targeted panel of 39 SNPs with high statistical power for identifying population of origin and analyzed more than 2,000 tissue samples collected between 2011 and 2015 as well as 260 otoliths collected in 2003/2004. These data provided high spatial resolution and allowed us to investigate geographical trends in mixing, to compare patterns for different life stages and to investigate temporal trends in mixing. We found similar geographical trends for the two time points represented by tissue and otolith samples and that a recently implemented geographical management separation of the two populations provided a relatively close match to their distributions. In contrast to the current assumption, we found that patterns of mixing differed between juveniles and adults, a signal likely linked to the different reproductive dynamics of the two populations. Collectively, our data confirm that genetics is an operational tool for complex fisheries management applications. We recommend focussing on developing population assessment models and fisheries management frameworks to capitalize fully on the additional information offered by genetically assisted fisheries monitoring.

Artificial lakes delay the migration of brown trout Salmo trutta smolts: a comparison of migratory behaviour in a stream and through an artificial lake.

Juvenile salmonids experience high mortality when negotiating lentic waters during their downstream migration to the sea. The development of artificial lakes and wetlands in streams has become a widely used management tool to reduce nutrient load to coastal areas. Such wetlands may threaten anadromous populations. In this study we quantify net ground speed of downstream migrating brown trout Salmo trutta smolts in equally long stream and lake sections in a Danish lowland stream and artificial lake. This was done by passive integrated transponder telemetry in 2016 and 2017. Mean net ground speed in the stream section was 36.58 and 0.8 km day-1 in the lake section. This decrease of net ground speed through the lake may lead to prolonged exposure to predators and probably contributes to high mortalities threatening anadromous populations.

Environmental calcium and variation in yolk sac size influence swimming performance in larval lake sturgeon (Acipenser fulvescens).

In many animal species, performance in the early life stages strongly affects recruitment to the adult population; however, factors that influence early life history stages are often the least understood. This is particularly relevant for lake sturgeon, Acipenser fulvescens, living in areas where environmental calcium concentrations are declining, partly due to anthropogenic activity. As calcium is important for muscle contraction and fatigue resistance, declining calcium levels could constrain swimming performance. Similarly, swimming performance could be influenced by variation in yolk sac volume, because the yolk sac is likely to affect drag forces during swimming. Testing swimming performance of larval A. fulvescens reared in four different calcium treatments spanning the range of 4-132 mg l-1 [Ca2+], this study found no treatment effects on the sprint swimming speed. A novel test of volitional swimming performance, however, revealed reduced swimming performance in the low calcium environment. Specifically, volitionally swimming larvae covered a shorter distance before swimming cessation in the low calcium environment compared with the other treatments. Moreover, sprint swimming speed in larvae with a large yolk sac was significantly slower than in larvae with a small yolk sac, regardless of body length variation. Thus, elevated maternal allocation (i.e. more yolk) was associated with reduced swimming performance. Data suggest that larvae in low calcium environments or with a large yolk sac exhibit reduced swimming performance and could be more susceptible to predation or premature downstream drift. Our study reveals how environmental factors and phenotypic variation influence locomotor performance in a larval fish.

Positioning of aquatic animals based on time-of-arrival and random walk models using YAPS (Yet Another Positioning Solver).

Aquatic positional telemetry offers vast opportunities to study in vivo behaviour of wild animals, but there is room for improvement in the data quality provided by current procedures for estimating positions. Here we present a novel positioning method called YAPS (Yet Another Positioning Solver), involving Maximum Likelihood analysis of a state-space model applied directly to time of arrival (TOA) data in combination with a movement model. YAPS avoids the sequential positioning-filtering-approach applied in alternative tools by using all available data in a single model, and offers better accuracy and error control. Feasibility and performance of YAPS was rigorously tested in a simulation study and by applying YAPS to data from an acoustic transmitter towed in a receiver array. Performance was compared to an alternative positioning model and proprietary software. The simulation study and field test revealed that YAPS performance was better and more consistent than alternatives. We conclude that YAPS outperformed the compared alternative methods, and that YAPS constitute a vast improvement to currently available positioning software in acoustic telemetry. Additionally, in contrast to vendor-supplied solutions, YAPS is transparent, flexible and can easily be adapted and extended for further improvements or to meet study specific requirements such as three-dimensional positioning.

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.

Phenotypic variation in metabolism and morphology correlating with animal swimming activity in the wild: relevance for the OCLTT (oxygen- and capacity-limitation of thermal tolerance), allocation and performance models.

Ongoing climate change is affecting animal physiology in many parts of the world. Using metabolism, the oxygen- and capacity-limitation of thermal tolerance (OCLTT) hypothesis provides a tool to predict the responses of ectothermic animals to variation in temperature, oxygen availability and pH in the aquatic environment. The hypothesis remains controversial, however, and has been questioned in several studies. A positive relationship between aerobic metabolic scope and animal activity would be consistent with the OCLTT but has rarely been tested. Moreover, the performance model and the allocation model predict positive and negative relationships, respectively, between standard metabolic rate and activity. Finally, animal activity could be affected by individual morphology because of covariation with cost of transport. Therefore, we hypothesized that individual variation in activity is correlated with variation in metabolism and morphology. To test this prediction, we captured 23 wild European perch (Perca fluviatilis) in a lake, tagged them with telemetry transmitters, measured standard and maximal metabolic rates, aerobic metabolic scope and fineness ratio and returned the fish to the lake to quantify individual in situ activity levels. Metabolic rates were measured using intermittent flow respirometry, whereas the activity assay involved high-resolution telemetry providing positions every 30 s over 12 days. We found no correlation between individual metabolic traits and activity, whereas individual fineness ratio correlated with activity. Independent of body length, and consistent with physics theory, slender fish maintained faster mean and maximal swimming speeds, but this variation did not result in a larger area (in square metres) explored per 24 h. Testing assumptions and predictions of recent conceptual models, our study indicates that individual metabolism is not a strong determinant of animal activity, in contrast to individual morphology, which is correlated with in situ activity patterns.

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.