Buoyancy control of four species of eleotrid fishes during aquatic surface respiration

Synopsis Four species of Australian Eleotridae from hypoxic habitats were examined in the laboratory to study buoyancy control in hypoxic water (<10 torr) when performing aquatic surface respiration (ASR; irrigating gills with upper millimeter of surface water). A conflict can arise here because O₂ can be reabsorbed from the swimbladder (reducing buoyancy) at a time when additional lift may be required to perform ASR. Three species were negatively buoyant and initially performed ASR while resting on the bottom in shallow water. After 24 h swimbladder lift increased to nearly neutral and ASR was performed while fish were pelagic. The fourth species remained pelagic at near neutral buoyancy in hypoxic water. With sudden exposure to hypoxia these physoclists reabsorbed between 5–27% (depending on species) of swimbladder volume (standard pressure) during the initial 30–90 min exposure to hypoxia. Additional experiments on one species (Hypseleotris galii) showed such loss to occur at O₂ tensions below 68 torr and when O₂ declined rapidly (2.17 torr min^-1). Secretion of gas compensated for losses under slower, natural rates of nocturnal O₂ decline. Eleotrids appear to reduce the conflict between respiration and buoyancy control in hypoxia by restricting gas reabsorbtion from the swimbladder and by rapidly secreting gases into the swimbladder.     

The influence of aquatic surface respiration (ASR) on cardio-respiratory function of the serrasalmid fish Piaractus mesopotamicus

When exposed to severely hypoxic water, many teleosts skim the better oxygenated surface layer (aquatic surface respiration, ASR). Information is scarce concerning the thresholds triggering ASR and its cardio-respiratory consequences. To assess the ambient conditions leading to ASR and to evaluate its effects on cardio-respiratory function, we exposed specimens of Piaractus mesopotamicus to gradual hypoxia (water oxygen tension ranging from 120 to 10 torr) with or, alternatively, without access to the surface. Concurrently, ASR, cardiac and respiratory frequencies, O₂ uptake and gill ventilation were monitored. With surface access, ASR developed below the critical tension for O₂ uptake (34 torr) by normal gill ventilation. Moreover, the time spent in ASR increased with prolonged hypoxic exposure to a maximum of 95% of total time. Without surface access, the species exhibited hypoxic bradycardia, that had not occurred in the group with fully developed ASR. Even without ASR, P. mesopotamicus recovered readily from hypoxic exposure, showing that this species possesses a number of mechanisms to cope with environmental hypoxia.     

Variation in thermal tolerances of native freshwater fishes in South Africa's Cape Fold Ecoregion: examining the east–west gradient in species' sensitivity to climate warming

The Cape Fold Ecoregion (CFE) is a biodiversity hotspot with high levels of endemism in its freshwater fish fauna. This study examined inter and intra-specific variation in critical thermal maxima (T_Cmax) for eight native species of freshwater fish from the CFE. Cape galaxias Galaxias zebratus, Breede River redfin Pseudobarbus burchelli, Berg River redfin Pseudobarbus burgi, Clanwilliam redfin Pseudobarbus calidus and fiery redfin Pseudobarbus phlegethon were the most thermally sensitive (T_Cmax = 29.8–32.8°C). Clanwilliam rock-catfish Austroglanis gilli, Eastern Cape redfin Pseudobarbus afer and Cape kurper Sandelia capensis were moderately sensitive (T_Cmax = 33.0–36.8°C). An increase in intra-specific thermal sensitivity of S. capensis was observed from east to west. The results were related to in situ water temperature, which influenced T_Cmax for all species, suggesting that thermal history is a major driver of variation in thermal tolerance amongst populations. These thermal tolerance data for freshwater fishes in the CFE demonstrate that resilience to climate warming follows a geographical cline and that the more sensitive western species and regions are conservation priorities.     

Morphological plasticity associated with environmental hypoxia in characiform fishes from neotropical floodplain lakes

The ability to develop reversible dermal extensions on the lower jaw in some South American characiform fishes has been proposed as a way to optimize the performance of aquatic surface respiration (ASR) during hypoxic conditions. These structures are formed by edema of the hypodermal tissues and can develop in a large proportion of individuals inhabiting a lake within a few hours following daily changes in dissolved oxygen. Our study report the development of dermal lip protuberances in eleven species of characiform fishes associated with periods of strong environmental hypoxia in floodplain lakes of Salado River, Argentina. Protuberances occurred in different basic forms in fishes with divergent head morphology (genera Astyanax, Ctenobrycon, Aphyocharax, Brycon, Mylossoma, Triportheus, Oligosarcus and Acestrorhynchus). The discovery of dermal projections on the anterior border of maxillary bone extends the known range of structures affected by lip protuberances. Dermal structures began to develop simultaneously in both jaws below dissolved oxygen (DO) concentrations of 1.20–1.75 mgl⁻¹ and rose in a steep manner as oxygen level decreased. The degree of morphological plasticity differed among traits and species. The shape of response of morphology to DO was similar to that previously reported on ASR, providing additional evidence about the functional link between these traits. Our results suggests that dermal lip protuberances are widely spread among characiform fishes, affecting several mouth structures. The different types of protuberances would make up for the limitations imposed by body size and mouth shape and position on the performance of ASR in fishes with divergent morphology.     

Intracellular pH in rice and wheat root tips under hypoxic and anoxic conditions

The influence of anoxia and hypoxia on dynamic of intracellurar pH and ATP content in rice and wheat root tips was investigated with ³¹P-NMR spectroscopy. Both cereals responded to hypoxia similarly, by rapid cytoplasmic acidification (from pH 7.6–7.7 to 7.1), which was followed by slow partial recovery (0.3 units). Anoxia led to a dramatic pH_cyt drop in tissues of both species (from pH 7.6–7.7 to less than 7.0) and partial recovery took place in rice only. In wheat, the acidification continued to pH 6.8 after 6 h of exposure. Anoxic wheat root tips were deficient in ADH induction, whereas increased activity of alcoholic fermentation enzymes took place in anoxic rice root tips, as well as in both species after hypoxic treatment. In both plants, NTP content followed the dynamics of pH_cyt. There was a strong correlation between NTP content and cytoplasmic H⁺ activity ([H⁺]_cyt = 10^−pHcyt) for both hypoxic and anoxic conditions. In this addendum we want to focus the reader''s attention on the importance of adequate experimental design when hypoxia is under investigation and on some further perspectives of intracellular pH regulation in plants under anaerobic conditions.Key words: anoxia, hypoxia, rice, wheat, cytoplasmic pH regulation     

1H-NMR study of the metabolome of a moderately hypoxia-tolerant fish, the common carp (Cyprinus carpio)

All 20.000 different fish species vary greatly in their ability to tolerate and survive fluctuating oxygen concentrations in the water. Especially fish of the genus Carassius, e.g. the crucian carp and the goldfish, exhibit a remarkable tolerance to limited/absent oxygen concentrations. The metabolic changes of anoxia-tolerant crucian carp were recently studied and published. Contrary to crucian carp, the hypoxia-tolerant common carp cannot survive a complete lack of oxygen (anoxia). Therefore, we studied the ¹H-NMR-based metabolomics of brain, heart, liver and white muscle extracts of common carp, subjected to anoxia (0 mg O₂ l^?1) and hypoxia (0.9 mg O₂ l^?1) at 5 °C. Specifically, fish were exposed to normoxia (i.e. 9 mg O₂ l^?1; controls 24 h, 1 week and 2 weeks), acute hypoxia (24 h), chronic hypoxia (1 week) and chronic hypoxia (1 week) with normoxic reoxygenation (1 week). Additionally, we also investigated the metabolic responses of fish to anoxia for 2 h. Both anoxia and hypoxia significantly changed the tissue levels of standard energy metabolites as lactate, glycogen, ATP/ADP and phosphocreatine. Remarkably, anoxia induced increased lactate levels in all tissues except for the heart whereas hypoxia resulted in decreased lactate concentrations in all tissues except for brains. Furthermore, hypoxia and anoxia influenced amino acids (alanine, valine/(iso)leucine) and neurotransmitters levels (GABA, glutamate). Lastly, we also detected ‘other’ i.e. previously not reported compounds to play a role in the present context. Scyllo-inositol levels changed significantly in heart, liver and muscle, providing novel insights into the anoxia/hypoxic responses of the common carp.     

Effect of anoxia and hypoxia on brain lipid metabolism

Lipid metabolism in rat brain was investigated in mild hypoxia (5–7% O₂ in nitrogen), which is associated with no apparent change in energy metabolism, and in severe anoxic conditions (ischemic anoxia), which are associated with a rapid decrease in ATP and oxygen content in brain. When brain slices were incubated with labeled glucose or acetate, the amount of labeled CO₂ produced was no different in experimental and control conditions, but the incorporation of radioactivity into brain lipids was decreased in all hypoxic and anoxic conditions. Interestingly, the incorporation of label from [¹⁴C]glucose into phosphatidylinositols was specifically inhibited by both hypoxic conditions but not by conditions associated with anoxia. The incorporation of the same labeled precursor, i.e., [¹⁴C]glucose, into fatty acids was elevated in ischemic anoxia but reduced after mild hypoxia. Because of the obvious differences in oxygen utilization in brain in anoxic and hypoxic conditions, we believe that the observed disturbances in lipid metabolism may be due to factors other than those that arise from oxygen deficiency alone.     

Diurnal distribution and behavioral responses of fishes to extreme hypoxia in an Amazon floodplain lake

Synopsis Because of the need for surface access for aquatic surface respiration (ASR), fish density increases were demonstrated for the open water of a floodplain lake during severe hypoxia. This indicates an O₂-induced diurnal pattern of horizontal migrations between the zone of macrophyte cover and open water. Supplemental experimental investigations seem to suggest that species such as characoids,Colossoma macropomum andSchizodon fasciatum, deviate from this pattern. During long periods of oxygen depletion, they return to the region of macrophyte growth and survive there without displaying the usual kind of ASR. Mortality studies in net cages exposed in natural water bodies confirmed that only these two species are able to survive severe hypoxia beneath macrophyte cover. The possibility of an O₂-input through the root system of plants is discussed. The O₂-concentration has a significant influence on the locomotory behavior and the frequency of opercular movement in characoids. There is significantly less locomotory activity beneath the macrophytes during periods of oxygen depletion among those species not forced to migrate than among those in the open water regions, where normal ASR behavior is possible.     

Aquatic surface respiration,a widespread adaptation to hypoxia in tropical freshwater fishes

Synopsis Use of the surface water for aquatic respiration (aquatic surface respiration, ASR) is one of the few alternatives to aerial respiration which allow fish to survive extreme hypoxia, yet it has received very little attention. This report examines three generalizations concerning ASR on a phylogenetically and geographically diverse range of tropical freshwater fishes. It demonstrates that ASR greatly enhances survival in hypoxic water, even in fish not morphologically specialized to use the surface film, that ASR is initiated at a distinct threshold oxygen concentration, with time spent at the surface increasing rapidly as O₂ declines, and that with extreme deoxygenation fish perform ASR over 90% of the time. Ninety-four percent of the 31 species of non-air breathing fish tested showed ASR., with the threshold oxygen concentration ranging from 6 to 40 torr.Present address correspondence and reprint requests to D.L. Kramer.     

Estimation of minimum area requirement of river‐connected lakes for fish diversity conservation in the Yangtze River floodplain

Aim Hydrological disconnection of floodplains from rivers is among the top factors threatening river‐floodplain ecosystems. To keep enough floodplain area is of great importance to biodiversity conservation. In the Yangtze River floodplain, most lakes were disconnected from the mainstream by dams in 1950–1970s. By analysing fish diversity data, we aim at determining the effects of river‐lake disconnection on fish diversity, at estimating the minimum protected area of river‐connected lakes and at proposing a holistic strategy for fish conservation in the mid‐lower reaches of the river. Location The Yangtze River floodplain, China. Methods We collected recorded data of fish diversity of 30 Yangtze floodplain lakes. Species–area relationships were analysed and compared between river‐connected and river‐disconnected lakes. Cumulative species–area models were constructed to estimate the minimum protected area of river‐connected lakes. Results River‐lake disconnection reduced fish diversity of Yangtze lakes by 38.1%, so that the river‐connected lakes play an important role in maintaining the floodplain biodiversity. The minimum protected area of river‐connected lakes was estimated to be 14,400 km². Therefore, we should not only protect the existent connected lakes of 5500 km², but also reconnect disconnected lakes of at least 8900 km² in the Yangtze basin. Main conclusions Species–area relationships are of importance in reserve design. We suggest that cumulative species–area model might be more suitable for ecosystems with high connectivity among regions such as floodplains. As the Yangtze River floodplain is an integrative ecosystem, we suggest establishing a holistic nature reserve in the mid‐lower basin for effective conservation of biodiversity.     

Proteomic changes in the brain of the western painted turtle (Chrysemys picta bellii) during exposure to anoxia

During anoxia, overall protein synthesis is almost undetectable in the brain of the western painted turtle. The aim of this investigation was to address the question of whether there are alterations to specific proteins by comparing the normoxic and anoxic brain proteomes. Reductions in creatine kinase, hexokinase, glyceraldehyde‐3‐phosphate dehydrogenase, and pyruvate kinase reflected the reduced production of adenosine triphosphate (ATP) during anoxia while the reduction in transitional endoplasmic reticulum ATPase reflected the conservation of ATP or possibly a decrease in intracellular Ca²⁺. In terms of neural protection programed cell death 6 interacting protein (PDCD6IP; a protein associated with apoptosis), dihydropyrimidinase‐like protein, t‐complex protein, and guanine nucleotide protein G_(o) subunit alpha (G_o alpha; proteins associated with neural degradation and impaired cognitive function) also declined. A decline in actin, gelsolin, and PDCD6IP, together with an increase in tubulin, also provided evidence for the induction of a neurological repair response. Although these proteomic alterations show some similarities with the crucian carp (another anoxia‐tolerant species), there are species‐specific responses, which supports the theory of no single strategy for anoxia tolerance. These findings also suggest the anoxic turtle brain could be an etiological model for investigating mammalian hypoxic damage and clinical neurological disorders.     

Quantifying Hypoxia Impacts on an Estuarine Demersal Community Using a Hierarchical Ensemble Approach

In coastal marine ecosystems, hypoxia and anoxia are emerging as growing threats whose ecological impacts are difficult to ascertain because of the frequent lack of adequate references for comparison. We applied conventional and hierarchical ensemble analyses to evaluate the weight of evidence in support of hypoxia impacts on local densities of individual and groups of demersal fish and invertebrate species in Hood Canal, WA, which is subject to seasonal hypoxia in its southern reaches. Central to our approach was a sample design and analysis scheme that was designed specifically to consider multiple alternative hypotheses regarding factors that dictate local species’ densities. We anticipated persistent effects of hypoxia (felt even when seasonal hypoxia was absent) on species densities would be most pronounced for sessile species, but that immediate effects (felt only when seasonal hypoxia was present) would dominate for mobile species. Conventional analysis provided strong evidence that densities of sessile species were persistently reduced in the hypoxic-impacted site, but did not indicate widespread immediate density responses during hypoxic events among mobile species. The absence of strong weights of evidence for hypoxia effects was partly a consequence of alternative hypotheses that better explained spatial-temporal variation in species’ densities. The hierarchical ensemble analysis improved the precision of species-specific effect sizes, and also allowed us to make inferences about the response of aggregated groups of species. The estimated mean density reductions during hypoxic events (dissolved oxygen ~2 mg/l) ranged from 73 to 98% among mobile invertebrates, benthic, and benthopelagic fishes. The large reduction in benthic and benthopelagic species suggests substantial effects of hypoxia in Hood Canal even at oxygen levels that were marginally hypoxic. Understanding the full ecological consequence of hypoxia will require a greater knowledge on the spatial extent of distributional shifts and their effects on competitive and predator–prey interactions.     

Seasonal and interannual effects of hypoxia on fish habitat quality in central Lake Erie

1. Hypoxia occurs seasonally in many stratified coastal marine and freshwater ecosystems when bottom dissolved oxygen (DO) concentrations are depleted below 2–3 mg O₂ L^?1. 2. We evaluated the effects of hypoxia on fish habitat quality in the central basin of Lake Erie from 1987 to 2005, using bioenergetic growth rate potential (GRP) as a proxy for habitat quality. We compared the effect of hypoxia on habitat quality of (i) rainbow smelt, Osmerus mordax mordax Mitchill (young‐of‐year, YOY, and adult), a cold‐water planktivore, (ii) emerald shiner, Notropis atherinoides Rafinesque (adult), a warm‐water planktivore, (iii) yellow perch, Perca flavescens Mitchill (YOY and adult), a cool‐water benthopelagic omnivore and (iv) round goby Neogobius melanostomus Pallas (adult) a eurythermal benthivore. Annual thermal and DO profiles were generated from 1D thermal and DO hydrodynamics models developed for Lake Erie’s central basin. 3. Hypoxia occurred annually, typically from mid‐July to mid‐October, which spatially and temporally overlaps with otherwise high benthic habitat quality. Hypoxia reduced the habitat quality across fish species and life stages, but the magnitude of the reduction varied both among and within species because of the differences in tolerance to low DO levels and warm‐water temperatures. 4. Across years, trends in habitat quality mirrored trends in phosphorus concentration and water column oxygen demand in central Lake Erie. The per cent reduction in habitat quality owing to hypoxia was greatest for adult rainbow smelt and round goby (mean: ?35%), followed by adult emerald shiner (mean: ?12%), YOY rainbow smelt (mean: ?10%) and YOY and adult yellow perch (mean: ?8.5%). 5. Our results highlight the importance of differential spatiotemporally interactive effects of DO and temperature on relative fish habitat quality and quantity. These effects have the potential to influence the performance of individual fish species as well as population dynamics, trophic interactions and fish community structure.     

Establishing the condition of lowland floodplain rivers: a palaeo-ecological approach

1. Current approaches for determining river ‘health’ rely on the establishment of a ‘reference’ condition. This is often difficult to achieve for lowland floodplain river systems because of the lack of pristine or pre-impacted sites and process models capable of predicting the effect of natural and human disturbances. 2. Using examples from the River Murray, Australia, this paper highlights the benefits of using palaeo-ecological studies in deciding on benchmark or pre-European settlement conditions for lowland floodplain river systems. 3. Physical, chemical and biological analyses of sediment obtained from shallow cores (< 2 m) extracted from a variety of floodplain sites on the River Murray and its tributaries reveal the extent and timing of catchment disturbances on this lowland river. Rates of sedimentation have increased by an order of magnitude since settlement; sediments now being deposited are finer, having implications for the nutrient status of the floodplain and the accumulation of heavy metals associated with these sediments. There has also been a sustained drop in the macrophyte cover of billabongs in the area, as inferred by chydorid cladoceran assemblages. The pre-European settlement diatom assemblages do not resemble those presently accumulating in billabongs in the region. 4. Whilst initially developed for lentic studies, palaeo-ecological studies are relevant to the establishment of benchmark conditions for lowland floodplain rivers. They are relatively straightforward, incorporate both historical and contemporary ecological information and can be applied to any lowland system.     

Anoxia- and hypoxia-induced expression of LDH-A* in the Amazon Oscar, Astronotus crassipinis

Adaptation or acclimation to hypoxia occurs via the modulation of physiologically relevant genes, such as erythropoietin, transferrin, vascular endothelial growth factor, phosphofructokinase and lactate dehydrogenase A. In the present study, we have cloned, sequenced and examined the modulation of the LDH-A gene after an Amazonian fish species, Astronotus crassipinis (the Oscar), was exposed to hypoxia and anoxia. In earlier studies, we have discovered that adults of this species are extremely tolerant to hypoxia and anoxia, while the juveniles are less tolerant. Exposure of juveniles to acute hypoxia and anoxia resulted in increased LDH-A gene expression in skeletal and cardiac muscles. When exposed to graded hypoxia juveniles show decreased LDH-A expression. In adults, the levels of LDH-A mRNA did not increase in hypoxic or anoxic conditions. Our results demonstrate that, when given time for acclimation, fish at different life-stages are able to respond differently to survive hypoxic episodes.     

Hypoxic blackwater event severely impacts Murray crayfish (Euastacus armatus) populations in the Murray River,Australia

Prolonged flooding in 2010/11 ended a decade of drought and produced a large‐scale hypoxic blackwater event across the southern Murray‐Darling Basin, Australia. The hypoxic conditions caused fish kills and Murray crayfish Euastacus armatus to emerge from the water onto the river banks to avoid the poor water quality. This study examined the medium‐term impact of this blackwater event on Murray crayfish populations in the Murray River, where approximately 1800 km of the main channel were affected by hypoxia. Murray crayfish populations were surveyed in July 2012, along a 1100‐km section of the Murray River at 10 sites affected by hypoxic blackwater and six sites that were not affected, and data were compared with surveys of the same sites undertaken in July 2010, four months before the hypoxic blackwater event (before‐after‐control‐impact experimental design). Murray crayfish abundance in 2012 (post‐blackwater) was significantly lower at blackwater affected sites (81% reduction from 2010), but not at non‐affected sites. The hypoxic blackwater impacted Murray crayfish of both sexes and all size‐classes in a similar manner. The results demonstrate that prolonged periods of hypoxia can markedly impact populations of the long‐lived and slow‐growing Murray crayfish despite the species ability to emerge from hypoxic water. The findings highlight important challenges for the management of both the recreational fishery for this species and riverine flows in relation to hypoxic blackwater events.     

Differences in in vitro cerebellar neuronal responses to hypoxia in eider ducks,chicken and rats

Ducks are well-known to be more tolerant to asphyxia than non-diving birds, but it is not known if their defences include enhanced neuronal hypoxia tolerance. To test this, we compared extracellular recordings of spontaneous activity in the Purkinje cell layer of 400 μm thick isolated cerebellar slices from eider ducks, chickens and rats, before, during and after 60 min hypoxia (95%N₂–5%CO₂) or chemical anoxia (hypoxia + 2 mM NaCN). Most slices rapidly lost activity in hypoxia, with or without recovery after rinse and return to normoxia (95%O₂–5%CO₂), but some maintained spontaneous activity throughout the insult. Proportions of ‘surviving’ (i.e. recovering or active) duck slices were significantly higher than for chickens in anoxia, and relative activity levels were higher for ducks than for chickens during hypoxia, anoxia and recovery. Survival of rat slices was significantly poorer than for birds under all conditions. Results suggest that (1) duck cerebellar neurons are intrinsically more hypoxia-tolerant than chicken neurons; (2) avian neurons are more hypoxia-tolerant than rat neurons, and (3) the enhanced hypoxic tolerance of duck neurons largely depended on efficient anaerobiosis since it mainly manifested itself in chemical anoxia. Mechanisms underlying the observed differences in neuronal hypoxic responses remain to be elucidated.     

The effect of oxygen tension on the physiology and distribution of Echinogammarus pirloti (Sexton & Spooner) and E. obtusatus (Dahl) (Crustacea:Amphipoda)

Echinogammarus pirloti (Sexton & Spooner) and E. obtusatus (Dahl) are two closely related gammarid amphipods that occupy vertically separated upper and lower zones, respectively, on boulder shores on Great Cumbrae Island (Firth of Clyde, Scotland). Measurement of the oxygen tension of small isolated pools under boulders showed that PO₂ was one of the most variable environmental factors to which amphipods were exposed, and that the major difference between upper and lower shore sites was in the duration of hypoxia or anoxia. When subjected to conditions of declining PO₂ in the laboratory, both species exhibited a high degree of respiratory independence and compensated for the low oxygen tension by increasing ventilatory effort. Critical PO₂ values were low (15–25 Torr) and showed an inverse relationship with the size of the animal. Under anoxic conditions both species accumulated lactate at similar rates (≈4 μmol · g wet wt⁻¹ · h⁻¹). On returning to normoxia, recovery time was longer for E. obtusatus than for E. pirloti. A model predicting the limits of distribution of the two species, based on the recovery times from varying periods of anoxia, appeared to agree with field data obtained between 1982 and 1983.