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.     

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.     

The Effect of Gestational State on Oxygen Consumption and Response to Hypoxia in the Sailfin Molly, Poecilia latipinna

Metabolic activity in livebearing fishes increases with embryonic development so that embryos prior to parturition may have a higher mass-specific oxygen requirement than maternal tissues, temporarily increasing the total routine oxygen requirement of the female. We examined whether females of the livebearing poeciliid Poecilia latipinna (sailfin molly) increase their routine metabolic oxygen consumption during development of their broods. We also quantified effects of gestation on time allocation to aquatic surface respiration (ASR) under hypoxic conditions. Mass-adjusted routine metabolic rate (RMR) of female mollies showed a significant increase during late gestation. The RMR of males did not differ from females that were in their early or mid stage of gestation, but was lower than females in late gestation. Gestating females spent approximately 27% more time conducting ASR than non-gestating females when exposed to chronic hypoxia (1mgl^–1), further supporting a brood-related increase in oxygen demand. Increased time allocation to ASR may directly affect maternal predation risk in low-oxygen conditions.     

Brood protection at a cost: mouth brooding under hypoxia in an African cichlid

This study quantifies the behavioral response of the widespread mouth brooding African cichlid Pseudocrenilabrus multicolor victoriae to progressive hypoxia. We exposed four gender/stage classes of P. multicolor (males, brooding females, females that had just released young, and non-brooding females) to progressive hypoxia and recorded the percent time spent using aquatic surface respiration (surface skimming, ASR) and gill ventilation rates. This was done for fish collected from three sites in Uganda (lake, swamp, and river) after long-term acclimation to normoxia. There was no effect of site of origin on response to hypoxia, but ASR thresholds did differ between gender/stage classes. The oxygen level (threshold) at which spent 10, 50, and 90% of their time at the surface using ASR was much higher for brooding females than for males, whereas ASR thresholds did not differ between non-brooding females and males. Similarly, the level at which ASR was initiated was much higher in brooding females than males, but did not differ between males and non-brooders, or between males and females than had just released young. The rate of gill ventilation dropped significantly in males and all stages of females after initiation of ASR, suggesting that surface skimming increases efficiency of oxygen acquisition. These results suggest that mouth brooding in female P. multicolor ASR improves oxygen uptake but imposes a cost in terms of time spent at the water surface, and this may affect maternal predation risk in low-oxygen habitats.     

Air Breathing and Gill Ventilation Frequencies in Juvenile Tarpon, Megalops atlanticus: Responses to Changes in Dissolved Oxygen, Temperature, Hydrogen Sulfide, and PH

This study quantified the air-breathing frequency (ABf in breaths h^–1) and gill ventilation frequency (Vf in ventilations min^–1) of tarpon Megalops atlanticusas a function of PO₂, temperature, pH, and sulphide concentration. Ten tarpon held at normoxia at 22–33°C without access to atmospheric oxygen survived for eight days, and seven survived for 14 days (at which point the experiment was terminated) suggesting that the species is a facultative, rather than an obligate, air breather. At temperatures of 29°C and below ABf was highest and Vf was lowest at low oxygen partial pressures. Tarpon appear to switch from aquatic respiration to air breathing at PO₂levels of roughly 40 torr. The gills were the primary organ for oxygen uptake in normoxia, and the air-breathing organ the primary mechanism for oxygen uptake in hypoxia. At 33°C, both ABf and Vf were elevated but highly variable, regardless of PO₂. There were no mortalities in tarpon exposed to total H₂S concentrations of 0–232µM (0–150.9µM H₂S); however, high sulfide concentrations resulted in very high ABf and Vf near zero. Vf was reduced when pH was acidic. We conclude that air breathing provides an effective means of coping with the environmental conditions that characterize the eutrophic ponds and sloughs that juvenile tarpon typically inhabit.     

The effect of visual density on the fecundity of the guppy,Poecilia reticulata

Synopsis This paper examines the effect of visual density on the brood size of female guppies,Poecilia reticulata. Previous laboratory studies of guppies showed that the fecundity of females decreases as density increases. In the present study, the effect of visual density was examined under conditions where detrimental factors such as interaction of individuals, waste substances, and dissolved oxygen were constant. The brood size of females at visual densities of 4 or more individuals was significantly larger than at zero visual density. There was a significant positive correlation between brood size and visual density. Sex ratio did not significantly affect brood size. Guppies can recognize surrounding densities and change their own fecundity in response to changes in density.     

A comparison of oxygen,nitrate, and sulfate respiration in coastal marine sediments

Aerobic respiration with oxygen and anaerobic respiration with nitrate (denitrification) and sulfate (sulfate reduction) were measured during winter and summer in two coastal marine sediments (Denmark). Both aerobic respiration and denitrification took place in the oxidized surface layer, whereas sulfate reduction was most significant in the deeper, reduced sediment. The low availability of nitrate apparently limited the activity of denitrification during summer to less than 0.2 mmoles NO ₃ ^– m^–2 day^–1, whereas activities of 1.0–3.0 mmoles NO ₃ ^– m^–2 day^–1 were measured during winter. Sulfate reduction, on the contrary, increased from 2.6–7.6 mmoles SO ₄ ^2– m^–2 day^–1 during winter to 9.8–15.1 mmoles SO ₄ ^2– m^–2 day^–1 during summer. The aerobic respiration was high during summer, 135–140 mmoles O₂ m^–2 day^–1, as compared to estimated winter activities of about 30 mmoles O₂ m^–2 day^–1. The little importance of denitrification relative to aerobic respiration and sulfate reduction is discussed in relation to the availability and distribution of oxygen, nitrate, and sulfate in the sediments and to the detritus mineralization.     

The effect of hypoxia on the vulnerability of guppies (Poecilia reticulata,Poeciliidae) to an aquatic predator (Astronotus ocellatus,Cichlidae)

Synopsis When dissolved oxygen concentration was near saturation in a laboratory experiment, guppies that spent (a) more time at the surface and (b) more time moving had a higher probability of being captured by a predatory cichlid fish. With decreasing oxygen concentration surface time and percent time moving increased, but prey risk decreased. In addition, the qualitative correlates of risk changed; under hypoxic conditions, predation risk was lower for prey which spent more time at the surface and in motion. Thus, dissolved oxygen concentration influences both quantitative and qualitative aspects of risk from water-breathing predators.Author to whom reprint requests should be addressed.     

Zonation and seasonality of benthic primary production and community respiration in tropical mangrove forests

Benthic oxygen consumption and primary production were measured using the bell jar technique in deltaic and fringing mangrove forests of tropical northeastern Australia. In a deltaic forest, rates of sediment respiration ranged from 197 to 1645 mol O₂ m^–2 h^–1 (mean=836), but did not vary significantly with season or intertidal zone. Gross primary production varied among intertidal zones and seasons, ranging from –281 to 1413 mol O₂ m^–2 h^–1 (mean=258). Upon tidal exposure, rates of gross primary production increased, but respiration rates did not change significantly. In a fringing mangrove forest, benthic respiration and gross primary production exhibited strong seasonality. In both forests, rates of oxygen consumption and production were low compared to salt marshes, but equivalent to rates in other mangrove forests. The production:respiration (P/R) ratio varied greatly over space and time (range:–0.61 to 1.76), but most values were «1 with a mean of 0.15, indicating net heterotrophy. On a bare creek bank and a sandflat, rates of gross primary production and P/R ratios were generally higher than in the adjacent mangroves. Low microalgal standing stocks, low light intensity under the canopy, and differences in gross primary production between mangroves and tidal flats, and with tidal status, indicate that benthic microalgae are light-limited and a minor contributor to primary productivity in these tropical mangrove forests.     

Observations on microbial percent respiration values in arctic and subarctic marine waters and sediments

Percent respiration was measured in over 1,100 arctic and subarctic marine water and sediment samples using¹⁴C-labeled glucose and glutamate. These measurements were made at different times of the year in 4 regions. Percent respiration values were typically lower in regions where the waters of large rivers mixed with seawater. They were also lower in sediments and in waters collected near the bottom than in surface waters. They were higher in winter arctic waters than water samples collected in the summer; however, a similar seasonal trend was not observed in subarctic waters. There were a number of studies in which there were significant positive rank correlations between percent respiration and salinity and between percent respiration and temperature. From what is known about the range of temperature and salinity encountered in samples collected during these studies and the results of temperature and salinity effects experiments, it was concluded that changes in these 2 variables did not explain the variation observed in percent respiration. Correlations between percent respiration and the inorganic nutrients PO₄ ^–3, NH₄ ⁺ and NO₃ ^– showed that of the 3 variables, only NO₃ ^– showed relatively high correlations with all the same sign. From this it was concluded that there may be situations in which NO₃ ^– levels may influence percent respiration in nearshore marine waters. It is also likely that qualitative characteristics of the available organic nutrients may also influence percent respiration levels. Although no organic nutrient data is available for statistical analysis, the patterns of percent respiration near river plumes and the relatively strong negative correlation often observed between uptake rates (heterotrophic activity) and percent respiration suggests that organic nutrients may be a factor in controlling percent respiration. It is suggested that there are situations in which percent respiration measurements may be used to document stress in natural microbial populations due to nutrient deficiencies.     

Respiratory metabolism of mosquitofish,Gambusia affinis: effects of temperature,dissolved oxygen,and sex difference

Synopsis Routine respiratory metabolic rates of mosquitofish (0.2 g live weight) were determined at 10, 15, 20, 25, 30, and 35°C at normoxic, hypoxic (= 40 torr P_O2), and extreme hypoxic (= 25 torr P_O2) conditions. Rates generally increased with increases in temperature (overall Q₁₀ = 2.11 at normoxia). Significant depressions (P<0.05) in rates were measured at 30 and 35°C at extreme hypoxic conditions. Males exhibited higher mortality at extreme hypoxia than females, especially at 35°C. Metabolic rates were significantly elevated at hyperoxic conditions (= 300 torr P_O2) at 25 and 30°C, but not at 35°C. Resting routine rates of less-confined fish were determined at 20, 25, and 30°C at normoxia and were significantly lower than the routine rates at the same temperatures. Behavioral experiments showed that aquatic surface respiration is initiated by mosquitofish at 20–65 torr P_O2 and is obligatory below 20 torr at 20° C. Overall, respiratory metabolic rates provide a quantitative metabolic basis from which predation rates of mosquitofish in various environments can be estimated.     

Development of dependence on aerial respiration in Polypterus senegalus (Cuvier)

The respiratory behaviour and partitioning of O₂ uptake between air and water were investigated in Polypterus genegalus using continuous-flow and two-phase respirometers and lung gas replacement techniques P. senegalus rarely resorts to aerial respiration under normal conditions. Partitioning of O₂ consumption depends on the activity and age of fish and the availability of aquatic oxygen. Immature fish (12–22 g) cannot utilize aerial O₂ but older fish exhibit age-dependent reliance on aerial respiration in hypoxic and hypercarbic waters. Pulmonary respiration accounts for 50% of the total requirement at aquatic O₂ concentrations of about 3.5 mg · l^–1 (or CO₂ of about 5%) and fish rely exclusively on aerial respiration at O₂ concentrations of less than 2.5 mg · l^–1. Branchial respiration is initially stimulated by hypercarbia (CO₂: 0.5–0.8%) but increased hypercarbia (CO₂ – 1%) greatly depresses (by over 90%) brancial respiration and initiates (CO₂: 0.5%) and sustains pulmonary respiration.     

Soil carbon cycling in a temperate forest: radiocarbon-based estimates of residence times, sequestration rates and partitioning of fluxes

Temperate forests of North America are thought to besignificant sinks of atmospheric CO₂. Wedeveloped a below-ground carbon (C) budget forwell-drained soils in Harvard Forest Massachusetts, anecosystem that is storing C. Measurements of carbonand radiocarbon (¹⁴C) inventory were used todetermine the turnover time and maximum rate ofCO₂ production from heterotrophic respiration ofthree fractions of soil organic matter (SOM):recognizable litter fragments (L), humified lowdensity material (H), and high density ormineral-associated organic matter (M). Turnover timesin all fractions increased with soil depth and were2–5 years for recognizable leaf litter, 5–10 years forroot litter, 40–100+ years for low density humifiedmaterial and >100 years for carbon associated withminerals. These turnover times represent the timecarbon resides in the plant + soil system, and mayunderestimate actual decomposition rates if carbonresides for several years in living root, plant orwoody material.Soil respiration was partitioned into two componentsusing ¹⁴C: recent photosynthate which ismetabolized by roots and microorganisms within a yearof initial fixation (Recent-C), and C that is respiredduring microbial decomposition of SOM that resides inthe soil for several years or longer (Reservoir-C).For the whole soil, we calculate that decomposition ofReservoir-C contributes approximately 41% of thetotal annual soil respiration. Of this 41%,recognizable leaf or root detritus accounts for 80%of the flux, and 20% is from the more humifiedfractions that dominate the soil carbon stocks.Measurements of CO₂ and ¹⁴CO₂ in thesoil atmosphere and in total soil respiration werecombined with surface CO₂ fluxes and a soil gasdiffusion model to determine the flux and isotopicsignature of C produced as a function of soil depth. 63% of soil respiration takes place in the top 15 cmof the soil (O + A + Ap horizons). The average residencetime of Reservoir-C in the plant + soil system is8±1 years and the average age of carbon in totalsoil respiration (Recent-C + Reservoir-C) is 4±1years.The O and A horizons have accumulated 4.4 kgC m^–2above the plow layer since abandonment by settlers inthe late-1800's. C pools contributing the most to soilrespiration have short enough turnover times that theyare likely in steady state. However, most C is storedas humified organic matter within both the O and Ahorizons and has turnover times from 40 to 100+ yearsrespectively. These reservoirs continue to accumulatecarbon at a combined rate of 10–30 gC m^{minus 2}yr^–1. This rate of accumulation is only 5–15% of the total ecosystem C sink measured in this stand using eddy covariance methods.     

Physiological adaptation to hypoxia of a neotropical characoid fish Colossoma macropomum,Serrasalmidae

Synopsis Investigations of seasonal changes in the hematological parameters of Colossoma macropomum revealed that during times of the year when they are exposed to low oxygen concentrations (< 0.5 mg 1^–1), there is an increase in the hemoglobin content of the blood and the erythrocyte count. Experiments to determine the influence of oxygen content on the routine oxygen consumption showed that the critical concentration is 2 mg 1^–1 at 30°C. At concentrations below 0.5 mg O₂ 1^–1, surface water is used for aquatic respiration. Above the critical concentration, short-term fluctuations in oxygen availability are compensated for by adjustment in the ventilation rate. Gas exchange is facilitated by the unusually large gill surface area (349 mm²g^–1 for a 200 g fish).     

Back to school: can antipredator behaviour in guppies be enhanced through social learning?

The ability to recognize and respond to predators often has a learned component, but few studies have examined the role of social learning in the development of antipredator behaviour. We investigated whether wild-caught juvenile guppies, Poecilia reticulata, from a low-predation river in Trinidad increase their response towards a novel predator through association with conspecifics from a high-predation river. We assigned fish to one of three treatment groups: (1) repeated exposure to a model accompanied by high-predation conspecifics; (2) repeated exposure to a model with low-predation conspecifics; (3) a control group in which focal fish interacted with high-predation fish in the absence of the model. Guppies trained with high-predation, but not low-predation, ‘demonstrators’ significantly improved their antipredator behaviour (spent more time schooling and inspected the model from further away). The guppies assigned to the control group showed no significant improvement in antipredator behaviour after the training period, suggesting that association with experienced conspecifics in the absence of the model is not sufficient to enhance the antipredator behaviour of na?ve fish. We conclude that guppies can improve their antipredator behaviour through association with more experienced conspecifics in the presence of visual cues simulating high predation risk. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.        

Feeding,growth, and particle-size-conversion efficiency in white sucker larvae and young common shiners

Synopsis Instantaneous feeding, assimilation, and growth rates for white sucker larvae and young common shiners and guppies (1–2 mg initial dry weight) were measured. Food consisted of natural zooplankton. Linear relationships were obtained between growth and feeding rates for instantaneous feeding rates up to 0.5 mg^-1 day^-1. Maximum gross conversion efficiencies (K₁) were 0.26, 0.31, and 0.24 for suckers, shiners, and guppies respectively. Particle-size-conversion efficiency (-log K₁ per log predator-prey size ratio) was 0.15 for suckers, 0.14 for shiners, and 0.18 for guppies. These values are lower than most available estimates of particle-size-conversion efficiency for carnivorous zooplankton and piscivorous fish, indicating that young planktivorous fish are among the most efficient predators at transferring biomass up the biomass size spectrum in aquatic ecosystems.     

Annual and diel oxygen regime in two polder ditches

The oxygen regime of two polder ditches and two enclosures within these ditches was studied. Continous oxygen temperature and light measurements were performed for 24-hour periods each month during two and a half year in the ditches and one year in the enclosures. Oxygen concentrations between 0 and 23 ppm were found, with diurnal ranges as large as 18 ppm. Steep gradients between bottom and surface could develop, but mostly disappeared during nightly turnover. The 10-percentile of the surface water measured between 9 and 17 hours was above 3 ppm, fullfilling the Dutch standards for this type of ecosystems. The oxygen concentrations near the bottom, however, could drop to zero and during the night surface concentrations below 1 ppm were measured. Based on average oxygen saturation values it is concluded that in the open water of the ditches oxygen consumption prevailed while in the enclosures oxygen production was most important. Based on the mass balance equation gross primary production and respiration were calculated. Annual average respiration varied between 2.5 and 6.6 g O₂.m^–2.d^–1 and average gross primary production between 3.2 and 4.8 g O₂.m^–2.d^–1. Maximum daily production and respiration were 15.9 and 22.3 g O₂.m^–2.d^–1. These figures classify the polder ditches as highly productive aquatic ecosystems.     

Ecosystem respiration and organic carbon processing in a large,tidally influenced river: the Hudson River

We estimated whole-ecosystem rates of respiration over a 40-km stretch of the tidally influenced freshwater Hudson River every 2 to 3 weeks from May through November. We measured in situ concentrations of oxygen over depth at dusk and dawn at 10 stations spaced over this interval. The use of multiple stations allowed for the consideration of the influence of tidal advection of water masses. Respiration was estimated from the decrease in oxygen overnight with a correction for diffusive exchange of oxygen with the atmosphere. We estimated this flux of oxygen to or from the atmosphere using the measured oxygen gradient and a transfer velocity model which is a function of wind velocity.Integration of the data for the period of May through November yields an estimate of whole-ecosystem respiration of 591 g C m^–2 (S.E. = 66). That the standard error of this estimate is relatively low (11% of the estimate) indicates that the use of multiple stations adequately deals with error introduced through the advection of water between stations. The logarithm of average daily respiration rate was correlated with average daily temperature (p = 0.007;r ² = 0.62). We used this temperature-respiration relationship to derive an estimate of the annual respiration rate of 755 g C m^–2 yr^–1 (S.E. = 72). This estimate is moderately sensitive to the estimated flux of oxygen between the atmosphere and water; using the lower and upper 95% confidence limits of our model relating the transfer velocity of oxygen to wind speed gives a range of annual respiration estimates from 665 g C m^–2 yr^–1 to 984 g C m^–2 yr^–1.The river is strongly heterotrophic, with most respiration driven by allochthonous inputs of organic matter from terrestrial ecosystems. The majority of the allochthonous inputs to the river (over 60%) are apparently metabolized within the river. Any change in allochthonous inputs due to changes in land use or climate patterns would be expected to alter the oxygen dynamics and energy flow within this tidally influenced river.     

The influence of water velocity on the display behavior of male guppies, Poecilia reticulata

The objective of this experiment was to determine if differentwater velocities during ontogeny affect male physical condition,male signal intensity, and female mating preferences in theguppy (Poecilia reticulata). Guppies were raised in aquariain either high or low water velocities and fed in excess. Analysisof 72 males from four replicates indicated that high velocitymales had longer mean displays and spent more total time displayingthan low velocity males. These males also had significantlyfaster swimming speeds, wider caudal peduncles, and were moreattractive to females than low velocity males. There were nodifferences in display rates, body widths, standard lengths,or copulation attempts between high and low velocity males.These results indicate that water velocity conditions duringontogeny act as a proximal factor that influences the displaybehavior of guppies. Water velocity caused an indirect increasein the power of the male display to produce a female sexualresponse. The morpho-metric measurements suggest that the proximalmechanism behind the increased display intensity was the increasedmuscle development of males raised in high water velocities,which resulted in longer prolonged swimming speeds and moreintense displays. Therefore, display behavior of guppies maybe a general indicator of overall male physical condition.[BehavEcol07: 272–278 (1996)]