Effects of acute hypoxia exposure and acclimation on the thermal tolerance of an imperiled Canadian minnow.

Elevated water temperatures and low dissolved oxygen (hypoxia) are pervasive stressors in aquatic systems that can be exacerbated by climate change and anthropogenic activities, and there is growing interest in their interactive effects. To explore this interaction, we quantified the effects of acute and long-term hypoxia exposure on the critical thermal maximum (CTmax) of Redside Dace (Clinostomus elongatus), a small-bodied freshwater minnow with sparse populations in the Great Lakes Basin of Canada and designated as Endangered under Canada's Species at Risk Act. Fish were held at 18°C and acclimated to four levels of dissolved oxygen (>90%, 60%, 40%, and 20% air saturation). CTmax was measured after 2 and 10 weeks of acclimation and after 3.5 weeks of reoxygenation, and agitation behavior was quantified during CTmax trials. Aquatic surface respiration behavior was also quantified at 14 weeks of acclimation to oxygen treatments. Acute hypoxia exposure decreased CTmax in fish acclimated to normoxia (>90% air saturation), but acclimation to hypoxia reduced this effect. There was no effect of acclimation oxygen level on CTmax when measured in normoxia, and there was no effect of exposure time to hypoxia on CTmax. Residual effects of hypoxia acclimation on CTmax were not seen after reoxygenation. Agitation behavior varied greatly among individuals and was not affected by oxygen conditions. Fish performed aquatic surface respiration with low frequency, but performed it earlier when acclimated to higher levels of oxygen. Overall, this work sheds light on the vulnerability of fish experiencing acute hypoxia and heat waves concurrently.

Counter-gradient variation in gene expression between fish populations facilitates colonization of low-dissolved oxygen environments.

The role of phenotypic plasticity during colonization remains unclear due to the shifting importance of plasticity across timescales. In the early stages of colonization, plasticity can facilitate persistence in a novel environment; but over evolutionary time, processes such as genetic assimilation may reduce variation in plastic traits such that species with a longer evolutionary history in an environment can show lower levels of plasticity than recent invaders. Therefore, comparing species in the early stages of colonization to long-established species provides a powerful approach for uncovering the role of phenotypic plasticity during different stages of colonization. We compared gene expression between low-dissolved oxygen (DO) and high-DO populations of two cyprinid fish: Enteromius apleurogramma, a species that has undergone a recent range expansion, and E. neumayeri, a long-established native species in the same region. We sampled tissue either immediately after capture from the field or after a 2-week acclimation under high-DO conditions, allowing us to test for both evolved and plastic differences in low-DO vs high-DO populations of each species. We found that most genes showing candidate-evolved differences in gene expression did not overlap with those showing plastic differences in gene expression. However, in the genes that did overlap, there was counter-gradient variation such that plastic and evolved gene expression responses were in opposite directions in both species. Additionally, E. apleurogramma had higher levels of plasticity and evolved divergence in gene expression between field populations. We suggest that the higher level of plasticity and counter-gradient variation may have allowed rapid genetic adaptation in E. apleurogramma and facilitated colonization. This study shows how counter-gradient variation may impact the colonization of divergent oxygen environments.

Turbidity drives plasticity in the eyes and brains of an African cichlid.

Natural variation in environmental turbidity correlates with variation in the visual sensory system of many fishes, suggesting that turbidity may act as a strong selective agent on visual systems. Since many aquatic systems experience increased turbidity due to anthropogenic perturbations, it is important to understand the degree to which fish can respond to rapid shifts in their visual environment, and whether such responses can occur within the lifetime of an individual. We examined whether developmental exposure to turbidity (clear, <5 NTU; turbid, ∼9 NTU) influenced the size of morphological structures associated with vision in the African blue-lip cichlid Pseudocrenilabrus multicolor. Parental fish were collected from two sites (clear swamp, turbid river) in western Uganda. F1 broods from each population were split and reared under clear and turbid rearing treatments until maturity. We measured morphological traits associated with the visual sensory system (eye diameter, pupil diameter, axial length, brain mass, optic tectum volume) over the course of development. Age was significant in explaining variation in visual traits even when standardized for body size, suggesting an ontogenetic shift in the relative size of eyes and brains. When age groups were analyzed separately, young fish reared in turbid water grew larger eyes than fish reared in clear conditions. Population was important in the older age category, with swamp-origin fish having relatively larger eyes and optic lobes relative to river-origin fish. Plastic responses during development may be important for coping with a more variable visual environment associated with anthropogenically induced turbidity.

Cycles of fusion and fission enabled rapid parallel adaptive radiations in African cichlids.

Although some lineages of animals and plants have made impressive adaptive radiations when provided with ecological opportunity, the propensities to radiate vary profoundly among lineages for unknown reasons. In Africa's Lake Victoria region, one cichlid lineage radiated in every lake, with the largest radiation taking place in a lake less than 16,000 years old. We show that all of its ecological guilds evolved in situ. Cycles of lineage fusion through admixture and lineage fission through speciation characterize the history of the radiation. It was jump-started when several swamp-dwelling refugial populations, each of which were of older hybrid descent, met in the newly forming lake, where they fused into a single population, resuspending old admixture variation. Each population contributed a different set of ancient alleles from which a new adaptive radiation assembled in record time, involving additional fusion-fission cycles. We argue that repeated fusion-fission cycles in the history of a lineage make adaptive radiation fast and predictable.

Behavioural responses of a cold-water benthivore to loss of oxythermal habitat.

Climate-driven declines in oxythermal habitat in freshwater lakes can impose prolonged constraints on cold-water fishes sensitive to hypoxia. How fish cope with severe habitat limitations is not well understood, yet has implications for their persistence. Here, we use acoustic-positioning telemetry to assess seasonal habitat occupancy and activity patterns of lake whitefish (Coregonus clupeaformis), a cold-water benthivore, in a small boreal lake that regularly faces severe oxythermal constraints during summer stratification. During this stratified period, they rarely (< 15% of detections) occupied depths with water temperatures > 10 °C (interquartile range = 5.3-7.9 °C), which resulted in extensive use (> 90% of detections) of water with < 4 mg L-1 dissolved oxygen (DO; interquartile range = 0.3-5.3 mg L-1). Lake whitefish were least active in winter and spring, but much more active in summer, when only a small portion of the lake (1-10%) contained optimal oxythermal habitat (< 10 °C and > 4 mg L-1 DO), showing frequent vertical forays into low DO environments concurrent with extensive lateral movement (7649 m d-1). High rates of lateral movement (8392 m d-1) persisted in the complete absence of optimal oxythermal habitat, but without high rates of vertical forays. We found evidence that lake whitefish are more tolerant of hypoxia (< 2 mg L-1) than previously understood, with some individuals routinely occupying hypoxic habitat in winter (up to 93% of detections) despite the availability of higher DO habitat. The changes in movement patterns across the gradient of habitat availability indicate that the behavioural responses of lake whitefish to unfavourable conditions may lead to changes in foraging efficiency and exposure to physiological stress, with detrimental effects on their persistence. Supplementary Information: The online version contains supplementary material available at 10.1007/s10641-022-01335-4.

Take time to look at the fish: Behavioral response to acute thermal challenge in two Amazonian cichlids.

Critical thermal maximum (CTmax ) is often used as an index of upper thermal tolerance in fishes; however, recent studies have shown that some fishes exhibit agitation or avoidance behavior well before the CTmax is reached. In this study, we quantified behavioral changes during CTmax trials in two Amazonian cichlids, Apistogramma agassizii and Mesonauta insignis. The thermal agitation temperature (Tag ) was recorded as the temperature at which fish left cover and began swimming in an agitated manner, and four behaviors (duration of sheltering, digging, activity, and aquatic surface respiration [ASR]) were compared before and after Tag . Both A. agassizii and M. insignis exhibited high critical thermal maxima, 40.8°C and 41.3°C, respectively. Agitation temperature was higher in M. insignis (37.3°C) than in A. agassizii (35.4°C), indicating that A. agassizii has a lower temperature threshold at which avoidance behavior is initiated. Activity level increased and shelter use decreased with increased temperatures, and patterns were similar between the two species. Digging behavior increased after Tag in both species, but was higher in A. agassazii and may reflect its substrate-oriented ecology. ASR (ventilating water at the surface film) was extremely rare before Tag , but increased in both cichlid species after Tag and was greater in M. insignis than in A. agassizii. This suggests that fish were experiencing physiological hypoxia at water temperatures approaching CTmax . These results demonstrate that acute thermal challenge can induce a suite of behavioral changes in fishes that may provide additional, ecologically relevant information on thermal tolerance.

The weakly electric fish, Apteronotus albifrons, actively avoids experimentally induced hypoxia.

Anthropogenic environmental degradation has led to an increase in the frequency and prevalence of aquatic hypoxia (low dissolved oxygen concentration, DO), which may affect habitat quality for water-breathing fishes. The weakly electric black ghost knifefish, Apteronotus albifrons, is typically found in well-oxygenated freshwater habitats in South America. Using a shuttle-box design, we exposed juvenile A. albifrons to a stepwise decline in DO from normoxia (> 95% air saturation) to extreme hypoxia (10% air saturation) in one compartment and chronic normoxia in the other. On average, A. albifrons actively avoided the hypoxic compartment below 22% air saturation. Hypoxia avoidance was correlated with upregulated swimming activity. Following avoidance, fish regularly ventured back briefly into deep hypoxia. Hypoxia did not affect the frequency of their electric organ discharges. Our results show that A. albifrons is able to sense hypoxia at non-lethal levels and uses active avoidance to mitigate its adverse effects.

Divergence in aerobic scope and thermal tolerance is related to local thermal regime in two populations of introduced Nile perch (Lates niloticus).

We tested whether thermal tolerance and aerobic performance differed between two populations of Nile perch (Lates niloticus) originating from the same source population six decades after their introduction into two lakes in the Lake Victoria basin in East Africa. We used short-term acclimation of juvenile fish to a range of temperatures from ambient to +6°C, and performed critical thermal maximum (CTmax ) and respirometry tests to measure upper thermal tolerance, resting and maximum metabolic rates, and aerobic scope (AS). Across acclimation temperatures, Nile perch from the cooler lake (Lake Nabugabo, Uganda) tended to have lower thermal tolerance (i.e., CTmax ) and lower aerobic performance (i.e., AS) than Nile perch from the warmer waters of Lake Victoria (Bugonga region, Uganda). Effects of temperature acclimation were more pronounced in the Lake Victoria population, with the Lake Nabugabo fish showing less thermal plasticity in most metabolic traits. Our results suggest phenotypic divergence in thermal tolerance between these two introduced populations in a direction consistent with an adaptive response to local thermal regimes.

The effect of normoxia exposure on hypoxia tolerance and sensory sampling in a swamp-dwelling mormyrid fish.

Effects of energetic limitations on the performance of sensory systems are generally difficult to quantify. Weakly electric fishes provide an ideal model system to quantify the effects of metabolic stressors on sensory information acquisition, because they use an active-sensing strategy that permits easy measurement of the sensing effort. These fishes discharge an electric signal and sense perturbations of the resulting electric field. We used the mormyrid Petrocephalus degeni to quantify the relationship between routine metabolic rate and the rate of sensory sampling (rate of electric organ discharge, EOD) while under progressive hypoxia by quantifying the critical oxygen tension (PC-MR) and the critical electric organ discharge threshold (PC-EOD). PC-MR was significantly higher in fish acclimated to normoxia for over 40 days compared to animals tested within 1-5 days of capture from a hypoxic swamp, which suggests high costs of maintaining hypoxia tolerance; however, there was no acclimation effect on PC-EOD. All P. degeni reached their PC-EOD prior to their PC-MR. However, below the respective critical tension value, EOD rate decreased more gradually than the metabolic rate suggesting that the fish were increasing the proportion of their energy budget allocated to acquiring sensory information as dissolved-oxygen levels dropped. Trade-offs between sensory sampling and other physiological functions are also suggested by the increase in routine EOD rate with long-term normoxia acclimation, in contrast to metabolic rate, which showed no significant changes. These results highlight the relationship between sensory sampling and metabolic rate in response to progressive hypoxia and the plasticity of hypoxia tolerance.

Effects of hypoxia on aerobic metabolism and active electrosensory acquisition in the African weakly electric fish Marcusenius victoriae.

Environmental hypoxia has effected numerous and well-documented anatomical, physiological and behavioural adaptations in fishes. Comparatively little is known about hypoxia's impacts on sensing because it is difficult to quantify sensory acquisition in vivo. Weakly electric fishes, however, rely heavily on an easily-measurable sensory modality-active electric sensing-whereby individuals emit and detect electric organ discharges (EODs). In this study, hypoxia tolerance of a mormyrid weakly electric fish, Marcusenius victoriae, was assessed by examining both its metabolic and EOD rates using a critical threshold (pcrit ) paradigm. The routine metabolic rate was 1.42 mg O2 h-1 , and the associated critical oxygen tension was 14.34 mmHg. Routine EOD rate was 5.68 Hz with an associated critical tension of 15.14 mmHg. These metabolic indicators of hypoxia tolerance measured in this study were consistent with those in previous studies on M. victoriae and other weakly electric fishes. Furthermore, our results suggest that some aerobic processes may be reduced in favour of maintaining the EOD rate under extreme hypoxia. These findings underscore the importance of the active electrosensory modality to these hypoxia-tolerant fish.

Conservation through the lens of (mal)adaptation: Concepts and meta-analysis.

Evolutionary approaches are gaining popularity in conservation science, with diverse strategies applied in efforts to support adaptive population outcomes. Yet conservation strategies differ in the type of adaptive outcomes they promote as conservation goals. For instance, strategies based on genetic or demographic rescue implicitly target adaptive population states whereas strategies utilizing transgenerational plasticity or evolutionary rescue implicitly target adaptive processes. These two goals are somewhat polar: adaptive state strategies optimize current population fitness, which should reduce phenotypic and/or genetic variance, reducing adaptability in changing or uncertain environments; adaptive process strategies increase genetic variance, causing maladaptation in the short term, but increase adaptability over the long term. Maladaptation refers to suboptimal population fitness, adaptation refers to optimal population fitness, and (mal)adaptation refers to the continuum of fitness variation from maladaptation to adaptation. Here, we present a conceptual classification for conservation that implicitly considers (mal)adaptation in the short-term and long-term outcomes of conservation strategies. We describe cases of how (mal)adaptation is implicated in traditional conservation strategies, as well as strategies that have potential as a conservation tool but are relatively underutilized. We use a meta-analysis of a small number of available studies to evaluate whether the different conservation strategies employed are better suited toward increasing population fitness across multiple generations. We found weakly increasing adaptation over time for transgenerational plasticity, genetic rescue, and evolutionary rescue. Demographic rescue was generally maladaptive, both immediately after conservation intervention and after several generations. Interspecific hybridization was adaptive only in the F1 generation, but then rapidly leads to maladaptation. Management decisions that are made to support the process of adaptation must adequately account for (mal)adaptation as a potential outcome and even as a tool to bolster adaptive capacity to changing conditions.

Independent and Interactive Effects of Long-Term Exposure to Hypoxia and Elevated Water Temperature on Behavior and Thermal Tolerance of an Equatorial Cichlid.

Hypoxia and climate warming are pervasive stressors in aquatic systems that may have interactive effects on fishes because both affect aerobic metabolism. We explored independent and interactive effects of dissolved oxygen (DO) and temperature on thermal tolerance, behavior, and fitness-related traits of juvenile F1 offspring of the African cichlid Pseudocrenilabrus multicolor. Fish were reared in a split-brood design with four treatments (low or high DO, cool or hot temperature); thermal tolerance, growth, and condition were measured after 1 mo in the rearing treatments, following which behavioral traits were measured over 3.6 mo. Critical thermal maximum was higher in fish reared under hot conditions but was not affected by hypoxia. There was an interactive effect of DO and temperature on agitation temperature (temperature at which fish show behavioral signs of thermal stress) and the thermal agitation window (°C between the onset of agitation and final loss of equilibrium). Fish reared and tested under hot, normoxic conditions showed a higher agitation temperature, while fish reared and tested under hot, hypoxic conditions showed the largest thermal agitation window. Fish grew more quickly in length under hot than cool conditions and more quickly under normoxic than hypoxic conditions. Fish reared under cool, normoxic conditions were characterized by higher condition than other groups. Both cool and hypoxic rearing conditions reduced activity and aggression. These results highlight the importance of integrating physiological tolerance measures with sublethal behavioral effects of hypoxia and high temperature to gain a fuller understanding of species responses to multiple stressors.

Predicted impacts of climate warming on aerobic performance and upper thermal tolerance of six tropical freshwater fishes spanning three continents.

Equatorial fishes, and the critically important fisheries based on them, are thought to be at-risk from climate warming because the fishes have evolved in a relatively aseasonal environment and possess narrow thermal tolerance windows that are close to upper thermal limits. We assessed survival, growth, aerobic performance and critical thermal maxima (CTmax) following acute and 21 d exposures to temperatures up to 4°C higher than current maxima for six species of freshwater fishes indigenous to tropical countries and of importance for human consumption. All six species showed 1.3-1.7°C increases in CTmax with a 4°C rise in acclimation temperature, values which match up well with fishes from other climatic regions, and five species had survival >87% at all temperatures over the treatment period. Specific growth rates varied among and within each species in response to temperature treatments. For all species, the response of resting metabolic rate (RMR) was consistently more dynamic than for maximum metabolic rate, but in general both acute temperature exposure and thermal acclimation had only modest effects on aerobic scope (AS). However, RMR increased after warm acclimation in 5 of 6 species, suggesting incomplete metabolic compensation. Taken in total, our results show that each species had some ability to perform at temperatures up to 4°C above current maxima, yet also displayed certain areas of concern for their long-term welfare. We therefore suggest caution against the overly broad generalization that all tropical freshwater fish species will face severe challenges from warming temperatures in the coming decades and that future vulnerability assessments should integrate multiple performance metrics as opposed to relying on a single response metric. Given the societal significance of inland fisheries in many parts of the tropics, our results clearly demonstrate the need for more species-specific studies of adaptive capacity to climate change-related challenges.

Effects of hypoxia on swimming and sensing in a weakly electric fish.

Low dissolved oxygen (hypoxia) can severely limit fish performance, especially aerobically expensive behaviours including swimming and acquisition of sensory information. Fishes can reduce oxygen requirements by altering these behaviours under hypoxia, but the underlying mechanisms can be difficult to quantify. We used a weakly electric fish as a model system to explore potential effects of hypoxia on swim performance and sensory information acquisition, which enabled us to non-invasively record electric signalling activity used for active acquisition of sensory information during swimming. To quantify potential effects of hypoxia, we measured critical swim speed (Ucrit) and concurrent electric signalling activity under high- and low-dissolved oxygen concentrations in a hypoxia-tolerant African mormyrid fish, Marcusenius victoriae Fish were maintained under normoxia for 6 months prior to experimental treatments, and then acclimated for 8 weeks to normoxia or hypoxia and tested under both conditions (acute: 4 h exposure). Acute hypoxia exposure resulted in a significant reduction in both Ucrit and electric signalling activity in fish not acclimated to hypoxia. However, individuals acclimated to chronic hypoxia were characterized by a higher Ucrit under both hypoxia and normoxia than fish acclimated to normoxia. Following a 6 month re-introduction to normoxia, hypoxia-acclimated individuals still showed increased performance under acute hypoxic test conditions, but not under normoxia. Our results highlight the detrimental effects of hypoxia on aerobic swim performance and sensory information acquisition, and the ability of fish to heighten aerobic performance through acclimation processes that can still influence performance even months after initial exposure.

Cardiac plasticity influences aerobic performance and thermal tolerance in a tropical, freshwater fish at elevated temperatures.

Fishes faced with novel thermal conditions often modify physiological functioning to compensate for elevated temperatures. This physiological plasticity (thermal acclimation) has been shown to improve metabolic performance and extend thermal limits in many species. Adjustments in cardiorespiratory function are often invoked as mechanisms underlying thermal plasticity because limitations in oxygen supply have been predicted to define thermal optima in fishes; however, few studies have explicitly linked cardiorespiratory plasticity to metabolic compensation. Here, we quantified thermal acclimation capacity in the commercially harvested Nile perch (Lates niloticus) of East Africa, and investigated mechanisms underlying observed changes. We reared juvenile Nile perch for 3 months under two temperature regimes, and then measured a series of metabolic traits (e.g. aerobic scope) and critical thermal maximum (CTmax) upon acute exposure to a range of experimental temperatures. We also measured morphological traits of heart ventricles, gills and brains to identify potential mechanisms for compensation. We found that long-term (3 month) exposure to elevated temperature induced compensation in upper thermal tolerance (CTmax) and metabolic performance (standard and maximum metabolic rate, and aerobic scope), and induced cardiac remodeling in Nile perch. Furthermore, variation in heart morphology influenced variations in metabolic function and thermal tolerance. These results indicate that plastic changes enacted over longer exposures lead to differences in metabolic flexibility when organisms are acutely exposed to temperature variation. Furthermore, we established functional links between cardiac plasticity, metabolic performance and thermal tolerance, providing evidence that plasticity in cardiac capacity may be one mechanism for coping with climate change.

Hypoxia acclimation increases novelty response strength during fast-starts in the African mormyrid, Marcusenius victoriae.

Many fishes perform quick and sudden swimming maneuvers known as fast-starts to escape when threatened. In pulse-type weakly electric fishes these responses are accompanied by transient increases in the rate of electric signal production known as novelty responses. While novelty responses may increase an individual's information about their surroundings, they are aerobically powered and may come at a high energetic cost when compared to fast-starts, which rely primarily on anaerobic muscle. The juxtaposition between two key aspects of fast-starts in these fishes - the aerobic novelty response and the anaerobic swimming performance - makes them an interesting model for studying effects of hypoxia on escape performance and sensory information acquisition. We acclimated the hypoxia-tolerant African mormyrid Marcusenius victoriae to either high or low dissolved oxygen (DO) levels for 8weeks, after which fast-starts and novelty responses were quantified under both high (normoxic) and low-DO (hypoxic) test conditions. Hypoxia-acclimated fish exhibited higher maximum curvature than normoxia-acclimated fish. Displacement of normoxia-acclimated fish was not reduced under acute hypoxic test conditions. Novelty responses were given upon each startle, whether or not the fish performed a fast-start; however, novelty responses associated with fast-starts were significantly stronger than those without, suggesting a functional link between fast-start initiation and the motor control of the novelty response. Overall, hypoxia-acclimated individuals produced significantly stronger novelty responses during fast-starts. We suggest that increased novelty response strength in hypoxia-acclimated fish corresponds to an increased rate of sensory sampling, which may compensate for potential negative effects of hypoxia on higher-level processing.

Elevated temperature and acclimation time affect metabolic performance in the heavily exploited Nile perch of Lake Victoria.

Increasing water temperatures owing to anthropogenic climate change are predicted to negatively impact the aerobic metabolic performance of aquatic ectotherms. Specifically, it has been hypothesized that thermal increases result in reductions in aerobic scope (AS), which lead to decreases in energy available for essential fitness and performance functions. Consequences of warming are anticipated to be especially severe for warm-adapted tropical species as they are thought to have narrow thermal windows and limited plasticity for coping with elevated temperatures. In this study we test how predicted warming may affect the aerobic performance of Nile perch (Lates niloticus), a commercially harvested fish species in the Lake Victoria basin of East Africa. We measured critical thermal maxima (CTmax) and key metabolic variables such as AS and excess post-exercise oxygen consumption (EPOC) across a range of temperatures, and compared responses between acute (3-day) exposures and 3-week acclimations. CTmax increased with acclimation temperature; however, 3-week-acclimated fish had higher overall CTmax than acutely exposed individuals. Nile perch also showed the capacity to increase or maintain high AS even at temperatures well beyond their current range; however, acclimated Nile perch had lower AS compared with acutely exposed fish. These changes were accompanied by lower EPOC, suggesting that drops in AS may reflect improved energy utilization after acclimation, a finding that is supported by improvements in growth at high temperatures over the acclimation period. Overall, the results challenge predictions that tropical species have limited thermal plasticity, and that high temperatures will be detrimental because of limitations in AS.

Agricultural expansion as risk to endangered wildlife: Pesticide exposure in wild chimpanzees and baboons displaying facial dysplasia.

Prenatal exposure to environmental endocrine disruptors can affect development and induce irreversible abnormalities in both humans and wildlife. The northern part of Kibale National Park, a mid-altitude rainforest in western Uganda, is largely surrounded by industrial tea plantations and wildlife using this area (Sebitoli) must cope with proximity to human populations and their activities. The chimpanzees and baboons in this area raid crops (primarily maize) in neighboring gardens. Sixteen young individuals of the 66 chimpanzees monitored (25%) exhibit abnormalities including reduced nostrils, cleft lip, limb deformities, reproductive problems and hypopigmentation. Each pathology could have a congenital component, potentially exacerbated by environmental factors. In addition, at least six of 35 photographed baboons from a Sebitoli troop (17%) have similar severe nasal deformities. Our inquiries in villages and tea factories near Sebitoli revealed use of eight pesticides (glyphosate, cypermethrin, profenofos, mancozeb, metalaxyl, dimethoate, chlorpyrifos and 2,4-D amine). Chemical analysis of samples collected from 2014 to 2016 showed that mean levels of pesticides in fresh maize stems and seeds, soils, and river sediments in the vicinity of the chimpanzee territory exceed recommended limits. Notably, excess levels were found for total DDT and its metabolite pp'-DDE and for chlorpyrifos in fresh maize seeds and in fish from Sebitoli. Imidacloprid was detected in coated maize seeds planted at the edge the forest and in fish samples from the Sebitoli area, while no pesticides were detected in fish from central park areas. Since some of these pesticides are thyroid hormone disruptors, we postulate that excessive pesticide use in the Sebitoli area may contribute to facial dysplasia in chimpanzees and baboons through this endocrine pathway. Chimpanzees are considered as endangered by IUCN and besides their intrinsic value and status as closely related to humans, they have major economic value in Uganda via ecotourism. Identifying and limiting potential threats to their survival such be a conservation priority.

Tropical fish in a warming world: thermal tolerance of Nile perch Lates niloticus (L.) in Lake Nabugabo, Uganda.

Key to predicting the response of fishes to climate change is quantifying how close fish are to their critical thermal limits in nature and their ability to adjust their thermal sensitivity to maintain performance. Here, we evaluated the effects of body size and habitat on aerobic scope (AS) and thermal tolerance of Nile perch Lates niloticus (L.), a fish of great economic and food security importance in East Africa, using respirometry and critical thermal maximum (CTmax) trials. Juvenile Nile perch from distinct habitats (high or low dissolved oxygen concentrations) of Lake Nabugabo, Uganda were exposed for 4.6 ± 0.55 days to a temperature treatment (25.5, 27.5, 29.5 or 31.5°C) prior to experimentation, with the lowest temperature corresponding to the mean annual daytime temperature in Lake Nabugabo and the highest temperature being 3°C higher than the maximal monthly average. As expected, metabolic rates increased with body mass. Although resting metabolic rate increased with temperature, maximal metabolic rate showed no change. Likewise, AS did not vary across treatments. The CTmax increased with acclimation temperature. There was no effect of habitat on maximal metabolic rate, AS or CTmax; however, there was a trend towards a lower resting metabolic rate for Nile perch captured in the low-dissolved oxygen habitat than in well-oxygenated waters. This study shows that juvenile Nile perch maintain a large AS at temperatures near the upper limit of their natural thermal range and provides evidence that Nile perch have physiological mechanisms to deal with acute exposure to thermal stress.

Limited variability in upper thermal tolerance among pure and hybrid populations of a cold-water fish.

As climate warming threatens the persistence of many species and populations, it is important to forecast their responses to warming thermal regimes. Climate warming often traps populations in smaller habitat fragments, not only changing biotic parameters, but potentially decreasing adaptive potential by decreasing genetic variability. We examined the ability of six genetically distinct and different-sized populations of a cold-water fish (brook trout, Salvelinus fontinalis) to tolerate acute thermal warming and whether this tolerance could be altered by hybridizing populations. Critical thermal maximum (CTmax) assays were conducted on juveniles from each population to assess thermal tolerance, and the agitation temperature was recorded for assessing behavioural changes to elevated temperatures. An additional metric, which we have called the 'CTmax-agitation window' (CTmax minus agitation temperature), was also assessed. The CTmax differed between five out of 15 population pairs, although the maximal CTmax difference was only 0.68°C (29.11-29.79°C). Hybridization between one large population and two small populations yielded no obvious heterosis in mean CTmax, and no differences in agitation temperature or CTmax-agitation window were detected among pure populations or hybrids. Summer variation in temperature within each stream was negatively correlated with mean CTmax and mean CTmax-agitation window, although the maximal difference was small. Despite being one of the most phenotypically divergent and plastic north temperate freshwater fishes, our results suggest that limited variability exists in CTmax among populations of brook trout, regardless of their population size, standing genetic variation and differing natural thermal regimes (temperature variation, minimum and maximum). This study highlights the level to which thermal tolerance is conserved between isolated populations of a vertebrate species, in the face of climate warming.