Fish mortality in the Amazonian drought of 2023: the role of experimental biology in our response to climate change.

Higher temperatures exacerbate drought conditions by increasing evaporation rates, reducing soil moisture and altering precipitation patterns. As global temperatures rise as a result of climate change, these effects intensify, leading to more frequent and severe droughts. This link between higher temperatures and drought is particularly evident in sensitive ecosystems like the Amazon rainforest, where reduced rainfall and higher evaporation rates result in significantly lower water levels, threatening biodiversity and human livelihoods. As an example, the serious drought experienced in the Amazon basin in 2023 resulted in a significant decline in fish populations. Elevated water temperatures, reaching up to 38°C, led to mass mortality events, because these temperatures surpass the thermal tolerance of many Amazonian fish species. We know this because our group has collected data on critical thermal maxima (CTmax) for various fish species over multiple years. Additionally, warmer waters can cause hypoxia, further exacerbating fish mortality. Thus, even Amazon fish species, which have relatively high thermal tolerance, are being impacted by climate change. The Amazon drought experienced in 2023 underscores the urgent need for climate action to mitigate the devastating effects on Amazonian biodiversity. The fact that we have been able to link fish mortality events to data on the thermal tolerance of fishes emphasizes the important role of experimental biology in elucidating the mechanisms behind these events, a link that we aim to highlight in this Perspective.

Predator exposure early in life shapes behavioral development and individual variation in a clonal fish.

Predation risk is one of the most important factors generating behavioral differences among populations. In addition, recent attention focusses on predation as a potential driver of patterns of individual behavioral variation within prey populations. Previous studies provide mixed results, reporting either increased or decreased among-individual variation in response to risk. Here, we take an explicit developmental approach to documenting how among-individual variation develops over time in response to predator exposure, controlling for both genetic and experiential differences among individuals. We reared juveniles of naturally clonal Amazon mollies, Poecilia formosa, either with or without a predator visible during feedings over 4 weeks and analyzed activity during feedings, time spent feeding and number of visits to the feeding spot. (I) Predator-exposed fish did not differ from control fish in average feeding behavior, but they were less active during feeding trials. (II) In the absence of the predator, substantial changes in among-individual variation over time were detected: among-individual differences in feeding duration increased whereas differences in activity decreased, but there were no changes in feeder visits. In contrast, in the presence of a predator, among-individual variation in all three behaviors was stable over time and often lower compared to control conditions. Our work suggests that predation risk may have an overall stabilizing effect on the development of individual variation and that differences in predation risk may well lead to population-wide differences in among-individual behavioral variation.

Two-year assessment of the effects of controlled sediment flushing on stream habitats and biota at reach scale.

Controlled sediment flushing operations (CSFOs) allow to recover reservoirs storage loss while rebalancing the sediment flux interrupted by dams but, at the same time, may cause unacceptable ecological impact. In this study, we investigated the responses of the food web of an upland stream to a CSFO, focusing on the effects of fine sediment deposition detected in three different mesohabitats, i.e., a pool, a riffle, and a step-pool. The field campaign lasted two years and included repeated measurements of fine sediment deposits, and sampling of periphyton, benthic macroinvertebrates and fishes. A moderate and patchy deposition occurred due to the CSFO with short and medium-term ecological impact on the lower trophic levels of the food web, which may affect the whole ecosystem functioning. The monitoring of all available mesohabitats in the investigated stream allowed to detect variations in the ecological response to CSFO, providing a more adequate assessment of the impact. As expected, sedimentation was larger in the pool but, in contrast to our hypotheses, the impact was lower and the recovery was longer for the benthic organisms inhabiting the riffle. In the case of fishes, no lethal impact of both brown trout and bullhead was recorded in the short term but the occurrence of longer lasting effects could not be excluded. To date, this is one of the few studies dealing with a detailed integrative assessment of the downstream impact of sediment management from reservoir on both abiotic and biotic components of stream ecosystem.

Bat consumption by holostean fishes in the Eocene Lake Messel: insights into the trophic adaptability of extinct gars and bowfins.

Direct evidence of trophic interactions between extinct species is rarely available in the fossil record. Here, we describe fish-mammal associations from the middle Eocene of Messel (Germany), consisting of three specimens of holosteans (one Atractosteus messelensis (Lepisosteidae) and two Cyclurus kehreri (Amiidae)) each preserved with a bat specimen (Palaeochiropteryx tupaiodon) lying in close contact with its jaws. This suggests that these fishes probably died after failed swallowing attempts, with the bat wing membrane entangled in their jaws resulting in a fatal handicap. Based on data from modern gars and bowfins, A. messelensis and C. kehreri may have opportunistically attacked drowning and dying individuals or scavenged on floating/sinking carcasses. This hypothesis is also supported by the unusually high number of bat specimens preserved in the deposits of the Eocene Lake Messel, suggesting that this group of small mammals may have represented a substantial food source for generalist feeders. This is the earliest case of chiropterophagy and the first known evidence of bat consumption by lepisosteid and amiid fishes, emphasizing the high trophic variability and adaptability of these groups throughout their evolutionary histories. The newly described associations provide important information for reconstructing the Eocene Lake Messel palaeoecosystem and its trophic web.

Cleaner fish with mirror self-recognition capacity precisely realize their body size based on their mental image.

Animals exhibiting mirror self-recognition (MSR) are considered self-aware; however, studies on their level of self-awareness remain inconclusive. Recent research has indicated the potential for cleaner fish (Labroides dimidiatus) to possess a sophisticated level of private self-awareness. However, as this study revealed only an aspect of private self-awareness, further investigation into other elements is essential to substantiate this hypothesis. Here, we show that cleaner fish, having attained MSR, construct a mental image of their bodies by investigating their ability to recall body size. A size-based hierarchy governs the outcomes of their confrontations. The mirror-naïve fish behaved aggressively when presented with photographs of two unfamiliar conspecifics that were 10% larger and 10% smaller than their body sizes. After passing the MSR test, they refrained from aggression toward the larger photographs but still behaved aggressively toward the smaller ones without re-examining their mirror images. These findings suggest that cleaner fish accurately recognize their body size based on mental images of their bodies formed through MSR. Additionally, mirror-experienced fish frequently revisited the mirror when presented with an intimidating larger photograph, implying the potential use of mirrors for assessing body size. Our study established cleaner fish as the first non-human animal to be demonstrated to possess private self-awareness.

Delta wing design in earliest nektonic vertebrates.

The colonization of the pelagic realm by the vertebrates represents one of the major transitions in the evolutionary success of the group and in the establishment of modern complex marine ecosystem. It has been traditionally related with the Devonian rise of jawed vertebrates, but new evidences indicate that first active swimmers, invading the water column, occurred within earlier armoured jawless fishes ("ostracoderms"). These "primitive" fishes lacked conventional fish control surfaces and the precise mechanism used to generate lift and stabilizing forces still remains unclear. We show that, because of their shape, the rigid cephalic shield of Pteraspidiformes, a group of Silurian-Devonian "ostracoderms", generate significant forces for hydrodynamic lift. Particle Image Velocimetry and force measurements in a water channel shows that the flow over real-sized Pteraspidiformes models is similar to that over delta wings, dominated by the formation of leading-edge vortices resulting in enhanced vortex lift forces and delayed stall angles of attack. Additionally, experiments simulating ground effect show that Pteraspidiformes present better hydrodynamic performance under fully pelagic conditions than in a benthic scenario. This suggests that, lacking movable appendages other than the caudal fin, leading-edge vortices were exploited by earliest vertebrates to colonize the water column more than 400 Mya.

Otolith reliability is context-dependent for estimating warming and CO2 acidification impacts on fish growth.

Otoliths are frequently used as proxies to examine the impacts of climate change on fish growth in marine and freshwater ecosystems worldwide. However, the large sensitivity differences in otolith growth responses to typical changing environmental factors (i.e., temperature and CO2 concentration), coupled with unclear drivers and potential inconsistencies with fish body growth, fundamentally challenge the reliability of such otolith applications. Here, we performed a global meta-analysis of experiments investigating the direct effects of warming (297 cases) and CO2 acidification (293 cases) on fish otolith growth and compared them with fish body growth responses. Hierarchical models were used to assess the overall effect and quantify the influence of nine explanatory factors (e.g., fish feeding habit, life history stage, habitat type, and experimental amplitude and duration). The overall effects of warming and acidification on otolith growth were positive and significant, and the effect size of warming (effect size = 0.4003, otolith size of the treatment group increased by 49.23% compared to that of the control group) was larger than that of acidification (0.0724, 7.51%). All factors examined contributed to the heterogeneity of effect sizes, with larger responses commonly observed in carnivorous fish, marine species, and young individuals. Warming amplitudes and durations and acidification amplitudes increased the effect sizes, while acidification durations decreased the effect sizes. Otolith growth responses were consistent with, but greater than, fish body growth responses under warming. In contrast, fish body growth responses were not significant under acidification (effect size = -0.0051, p = .6185) and thus cannot be estimated using otoliths. Therefore, our study highlights that the reliability of applying otoliths to examine climate change impacts is likely varied, as the sensitivity of otolith growth responses and the consistency between the growth responses of otoliths and fish bodies are context-dependent.

Behavioural changes of native freshwater prawn in the presence of a predator fish.

Predation pressure influences animal behaviour in relation to feeding, exposure to predators and habitat use. In the presence of a predator, prey usually decreases feeding and activity, avoiding predation-risk areas. This study evaluated the visual effects of a predator fish (red-bellied piranha Pygocentrus nattereri) on the behaviour and habitat use of Macrobrachium jelskii prawn. It was hypothesized that prawns would modify their behaviour in the presence of a predator, decreasing their general activity (foraging and locomotion) and seeking shelter more frequently. Twenty behavioural tests were carried out without and with the presence of a predator using five different M. jelskii individuals per trial. Behavioural data were collected using scan sampling with instantaneous recording of behaviours every 15 s during 5 min in each trial. The presence of the predator caused prawns to decrease their locomotion and feeding and increase environment exploration and predator inspection. Prawns used the shelter more frequently when the predator was present. Red-bellied piranha elicited anti-predator behaviour in M. jelskii. The patterns observed suggested that the most common anti-predatory behaviours exhibited by M. jelskii are beneficial as they reduce vigilance and active anti-predation strategies, such as escape.

Fisheries shocks provide an opportunity to reveal multiple recruitment sources of sardine in the Sea of Japan.

The abrupt decline in sardine catches in the Sea of Japan and the East China Sea (SJ-ECS) in 2014 and 2019 and the recovery in the following years call into question the current assumption that sardines in the SJ-ECS form a self-recruiting subpopulation. To test this hypothesis, we analysed otolith stable oxygen and carbon isotope profiles (δ18O, δ13C) of age-0 and age-1 sardines from 2010 and 2013-2015 year-classes captured in the SJ-ECS, as geographic markers for nursery areas. Age-0 sardines generally showed a significant ontogenetic decrease in otolith δ18O from larval to juvenile stages. However, the majority of age-1 captured in spring 2011, 2015 and 2016 showed non-decreasing otolith δ18O profiles, suggesting that the age-0 off the Japanese coast were not the main source of recruitment. Different migration groups were thus indicated: the "locals" growing up off the Japanese coast and the migrating "nonlocals". The isotope profiles of the "nonlocals" overlapped with those of age-0 captured in the subarctic North Pacific, suggesting that they may be migrants from the Pacific, or perhaps an unobserved northward migration group in the SJ-ECS. Our results highlight the considerable uncertainty in the population structure assumed in current stock assessment models for Japanese sardine.

Flooding and dam operations facilitate rapid upstream migrations of native and invasive fish species on a regulated large river.

Dams commonly restrict fish movements in large rivers but can also help curtail the spread of invasive species, such as invasive bigheaded carps (Hypophthalmichthys spp). To determine how dams in the upper Mississippi River (UMR) affect large-scale invasive and native fish migrations, we tracked American paddlefish (Polyodon spathula) and bigheaded carp across > 600 river km (rkm) and 16 navigation locks and dams (LD) of the UMR during 2 years with contrasting water levels. In 2022, a low-water year, both native paddlefish and invasive bigheaded carp had low passage rates (4% and 0.6% respectively) through LD15, a movement bottleneck being studied for invasive carp control. In contrast, flooding in 2023 led to open-river conditions across multiple dams simultaneously, allowing 53% of paddlefish and 46% of bigheaded carp detected in Pool 16 to move upstream through LD15. Bigheaded carp passed upstream through LD15 rapidly (µ = 32 rkm per day) a maximum of 381 rkm, whereas paddlefish moved an average of 9 upstream rkm per day (maximum of 337 rkm). Our results can inform managers examining trade-offs between actions that enhance native fish passage or deter movements of invasive species. This understanding is critical because current climate change models project increases in flooding events like that observed during 2023.

Hidden rivals: the negative impacts of dolphinfish on seabird foraging behaviour.

Marine predators often aggregate at the air-sea boundary layer to pursue shared prey. In such scenarios, seabirds are likely to benefit from underwater predators herding fish schools into tight clusters thereby enhancing seabirds' prey detectability and capture potential. However, this coexistence can lead to competition, affecting not only immediate foraging strategies but also their distribution and interspecies dynamics. We investigated both the longitudinal relationships and instantaneous interactions between streaked shearwaters (Calonectris leucomelas) and common dolphinfish (Coryphaena hippurus), both preying on Japanese anchovy (Engraulis japonicus). Using GPS data from 2011 to 2021, we calculated behavioural parameters for streaked shearwaters as an index of time spent and distance travelled. Despite the abundance of Japanese anchovies, we found that streaked shearwaters might increase their foraging time in the presence of underwater predators. Moreover, video loggers provided direct evidence of streaked shearwaters and common dolphinfish attacking the same fish schools, potentially interfering with bird foraging by dolphinfish. Our results suggest that the presence of underwater predators in a given patch might increase the time spent by seabirds foraging without affecting the distance travelled. This highlights the need for future studies that consider the potential adverse effects of other top predators on seabird prey availability.

Cardiac arrhythmias in fish induced by natural and anthropogenic changes in environmental conditions.

A regular heartbeat is essential for maintaining the homeostasis of the vertebrate body. However, environmental pollutants, oxygen deficiency and extreme temperatures can impair heart function in fish. In this Review, we provide an integrative view of the molecular origins of cardiac arrhythmias and their functional consequences, from the level of ion channels to cardiac electrical activity in living fish. First, we describe the current knowledge of the cardiac excitation-contraction coupling of fish, as the electrical activity of the heart and intracellular Ca2+ regulation act as a platform for cardiac arrhythmias. Then, we compile findings on cardiac arrhythmias in fish. Although fish can experience several types of cardiac arrhythmia under stressful conditions, the most typical arrhythmia in fish - both under heat stress and in the presence of toxic substances - is atrioventricular block, which is the inability of the action potential to progress from the atrium to the ventricle. Early and delayed afterdepolarizations are less common in fish hearts than in the hearts of endotherms, perhaps owing to the excitation-contraction coupling properties of the fish heart. In fish hearts, Ca2+-induced Ca2+ release from the sarcoplasmic reticulum plays a smaller role than Ca2+ influx through the sarcolemma. Environmental changes and ion channel toxins can induce arrhythmias in fish and weaken their tolerance to environmental stresses. Although different from endotherm hearts in many respects, fish hearts can serve as a translational model for studying human cardiac arrhythmias, especially for human neonates.

Effect of local and regional factors on the structure of the fish communities associated with aquatic macrophyte stands in oxbow lakes on the Amazon floodplain.

The Amazon floodplain is home to an extremely high diversity of fish, with lakes playing an important role in the establishment of this biological richness. These lacustrine environments are subject to constant fluctuations caused by the annual flood pulse, with local factors and other regional patterns also contributing to the variation in fish community structure. The present study verified how local (depth and transparency of the water, the size and species composition of the macrophyte stands) and regional factors (spatial distribution of the stands and the hydrological phase) influence the structure of the fish community of the floodplain lakes of the Môa River, in northern Brazil. Fish species richness was influenced by the depth of the water and the spatial distribution of the macrophyte stands. Fish species composition was influenced by local environmental variables, spatial structure, and the hydrological phase. However, variation partitioning indicated that only the hydrological phase explained the variation in fish composition. These findings indicate that the local environment, the spatial structure, and the hydrological phase drive changes in the structure of the fish communities associated with aquatic macrophytes in the floodplain lakes of the Amazon basin.

The interaction between warming and enrichment accelerates food-web simplification in freshwater systems.

Nutrient enrichment and climate warming threaten freshwater systems. Metabolic theory and the paradox of enrichment predict that both stressors independently can lead to simpler food-webs having fewer nodes, shorter food-chains and lower connectance, but cancel each other's effects when simultaneously present. Yet, these theoretical predictions remain untested in complex natural systems. We inferred the food-web structure of 256 lakes and 373 streams from standardized fish community samplings in France. Contrary to theoretical predictions, we found that warming shortens fish food-chain length and that this effect was magnified in enriched streams and lakes. Additionally, lakes experiencing enrichment exhibit lower connectance in their fish food-webs. Our study suggests that warming and enrichment interact to magnify food-web simplification in nature, raising further concerns about the fate of freshwater systems as climate change effects will dramatically increase in the coming decades.

Multiple climate change stressors reduce the emergence success of gravel-spawning fish species and alter temporal emergence patterns.

Climate change, with its profound effects on stream sediment, hydrological, and temperature dynamics, will exacerbate impacts on habitat conditions for many species, particularly those with vulnerable early life stages relying on the hyporheic zone, such as gravel-spawning fishes. Due to the complex and interactive nature of multiple stressor effects, we employed large-scale outdoor mesocosms to systemically test how the reproductive success of three gravel-spawning fish species brown trout (Salmo trutta), nase, (Chrondrostoma nasus) and Danube salmon (Hucho hucho) was affected by individual and combined effects of warming (+3-4 °C), fine sediment (increase in <0.85 mm by 22 %) and low-flow (eightfold discharge-reduction). Fine sediment had the most detrimental effect on emergence rate and fry length in all three species, reducing the emergence rate to zero in brown trout, 9 % in nase, and 4 % in Danube salmon. The emergence mortality caused by fine sediment surpassed that of hatching distinctly, suggesting that negative effects due to hypoxia were considerably exacerbated by entombment. Warming had only minor effects as a single stressor, but low flow reduced emergence rates of the spring spawning species nase and Danube salmon by 8 and 50 %, respectively. In combined treatments including fine sediment, however, the emergence success of all three species responded strongly negatively, even in the cyprinid species nase, which showed little interactive effects between stressors regarding hatching success. Warming and fine sediment also led to the earlier emergence of fry, implying a risk of asynchrony with available food resources. This study dramatically shows that climate change can have deleterious impacts on the reproductive success of gravel-spawning fish species, irrespective of taxonomic or ecological traits.

Cross-habitat utilization of fish in a tropical deltaic system as a function of climate variability and body size: Are mangroves fish nurseries in a tropical delta?

The temporal variability of fish habitat utilization is poorly understood in tropical deltaic systems due to high water turbidity, which limits visual censuses, and to the lack of long-term data incorporating climate variability events. We aimed to assess the influence of body size and El Niño Southern Oscillation (ENSO) variability on the cross-habitat utilization rate of 14 fish species of commercial relevance in the Ciénaga Grande de Santa Marta (CGSM). We estimated the utilization of mangroves and coastal lagoons based on relative catch frequencies from encircling gillnets used within a long-term catch monitoring program, and then tested for significant changes in each species' habitat utilization as a function of body size and climate variability. Six species showed a high dependence on mangroves and four on coastal lagoons for most body size classes (including juveniles) and ENSO conditions. One species (Elops smithi) showed a high utilization of mangroves in some ENSO phases and body size classes, while three species showed a high utilization of both mangroves and coastal lagoons. Mangrove utilization by six species (Megalops atlanticus, E. smithi, Centropomus undecimalis, Mugil incilis, Mugil liza, and Ariopsis canteri) increased in larger body sizes at low depths, which usually occurs under dry ENSO conditions, when predatory risk is higher in coastal lagoons. Another species (Caquetaia kraussi) increased its mangrove utilization from the body size at which its feeding habits change. Mangroves and coastal lagoons are important nurseries and habitats for adults of the main commercial fish species in the CGSM. Seascape habitats and fringe/riverine mangroves must be conserved in tropical deltas to promote not only nurseries but also fish lifecycles.

Twenty-five emerging questions when detecting, understanding, and predicting future fish distributions in a changing climate.

The 2023 Annual Symposium of the Fisheries Society of the British Isles hosted opportunities for researchers, scientists, and policy makers to reflect on the state of art of predicting fish distributions and consider the implications to the marine and aquatic environments of a changing climate. The outcome of one special interest group at the Symposium was a collection of questions, organized under five themes, which begin to capture the state of the field and identify priorities for research and management over the coming years. The five themes were Physiology, Mechanisms, Detect and Measure, Manage, and Wider Ecosystems. The questions, 25 of them, addressed concepts which remain poorly understood, are data deficient, and/or are likely to be impacted in measurable or profound ways by climate change. Moving from the first to the last theme, the questions expanded in the scope of their considerations, from specific processes within the individual to ecosystem-wide impacts, but no one question is bigger than any other: each is important in detecting, understanding, and predicting fish distributions, and each will be impacted by an aspect of climate change. In this way, our questions, particularly those concerning unknown mechanisms and data deficiencies, aimed to offer a guide to other researchers, managers, and policy makers in the prioritization of future work as a changing climate is expected to have complex and disperse impacts on fish populations and distributions that will require a coordinated effort to address.

Females increase reproductive investment when mated to less sexually attractive males in a serially monogamous fish.

Reproductive investment decision is an integral part of life-history theory. Differential allocation hypothesis predicts that females should increase investment when mated to high-quality males, conversely, reproductive compensation hypothesis predicts that females should increase investment when mated to low-quality males. Empirical research dominantly focuses on polygamous species and rarely on serially monogamous species. So, the question remains: which hypothesis does serially monogamous species fit? And if it fits reproductive compensation hypothesis, do females only compensate once or continuously for multiple times when mating to low-quality males? Here, we used a serially monogamous fish, the lined seahorse (Hippocampus erectus), to investigate the reproductive investment pattern of females in relation to male quality (measured by sexual attractiveness). We found that females allocated more resources into eggs when they mated to less-sexually-attractive males, indicating the investment pattern of lined seahorse falls in with the prediction of reproductive compensation hypothesis. This finding may imply that the sex role of seahorses is reversed, and female is the side imposed on a greater sexual selection pressure. On this basis, we compared the investment difference of females in two consecutive breeding events when mated to less-sexually-attractive males. We found that females allocated less resources into eggs in the second breeding than in the first one. Females reduced their reproductive compensation in the second breeding, which may be attributed to the improvement in the quality (e.g., paternal care ability) of their mates after the first breeding, thus eliminating the need for them to invest more in the second breeding.

Evaluation of fish habitat suitability based on stream hydrodynamics and water quality using SWAT and HEC-RAS linked simulation.

The objective of this study was to evaluate fish habitat suitability by simulating hydrodynamic and water quality factors using SWAT and HEC-RAS linked simulation considering time-series analysis. A 2.9 km reach of the Bokha stream was selected for the habitat evaluation of Zacco platypus, with hydrodynamic and water quality simulations performed using the SWAT and HEC-RAS linked approach. Based on simulated 10-year data, the aquatic habitat was assessed using the weighted usable area (WUA), and minimum ecological streamflow was proposed from continuous above threshold (CAT) analysis. High water temperature was identified as the most influential habitat indicator, with its impact being particularly pronounced in shallow streamflow areas during hot summer seasons. The time-series analysis identified a 28% threshold of WUA/WUAmax, equivalent to a streamflow of 0.48 m3/s, as the minimum ecological streamflow necessary to mitigate the impact of rising water temperatures. The proposed habitat modeling method, linking watershed-stream models, could serve as a useful tool for ecological stream management.