Gill ventilation and respiratory efficiency of Sacramento blackfish, Orthodon microlepidotus Ayres, in hypoxic environments

Respiratory and gill ventilatory responses of Sacramento blackfish to three environmental temperatures (12, 20 and 28°C) and four environmental dissolved oxygen concentrations (130, 90, 65 and 40 torr P_O2) were examined to determine physiological strategies of survival in eutrophic lakes and suitibility for culture conditions. Situated in van Dam-type respirometers, experimental blackfish showed increased gill ventilatory flows from increased ventilatory frequencies and stroke volumes to meet higher respiratory oxygen demands at increased temperatures. Ventilation volumes also increased at reduced environmental dissolved oxygen levels by increased ventilatory stroke volumes alone, except at 28°C where frequency increases were also measured. Oxygen consumption rates remained essentially constant with declining dissolved oxygen, except at 28°C where excitement elevated respiratory metabolism at 65 and 40 torr. Percentage utilization of oxygen increased with temperature from 12°C, but levels at 20 and 28°C were insignificantly different. Contrary to most studies on other species, there was no change in percentage utilization under hypoxic conditions even with 4.7-fold increases in ventilation volume in excited fish at 28°C. The ability of blackfish to survive in hypoxic waters is quantitatively compared with other species by calculation of a respiratory efficiency index (I), which includes the relationship between ventilation volume and percentage utilization of oxygen under normoxic and hypoxic conditions as well as the half-saturation value (P₅₀) of the species' blood with oxygen.     

Making a master filterer: Ontogeny of specialized filtering plates in silver carp (Hypophthalmichthys molitrix)

Filter feeding fishes possess several morphological adaptations necessary to capture and concentrate small particulate matter from the water column. Filter feeding teleosts typically employ elongated and tightly packed gill rakers with secondary bony or epithelial modifications that increase filtering efficiency. The gill rakers of Hypophthalmichthys molitrix, silver carp, are anatomically distinct from and more complex than the filtering apparatus of other teleostean fishes. The silver carp filtering apparatus is composed of biserial, fused filtering plates used to capture particles ranging in size from 4 to 80 μm. Early in ontogeny, at 15–25 mm standard length (SL), silver carp gill rakers are reminiscent of other more stereotypical teleostean rakers, characterized by individual lanceolate rakers that are tightly packed along the entirety of the branchial arches. At 30 mm SL, secondary epithelial projections and concomitant dermal ossification begin to stitch together individual gill rakers. During later juvenile stages, dermal bone further modifies the individual gill rakers and creates a bony scaffold that supports the now fully fused and porous epithelium. By adulthood, the stitching of bone and complete fusion of the overlying epithelium creates rigid filtering plates with morphologically distinct faces. The inner face of the plates is organized into a net‐like matrix while the outer face has a sponge‐like appearance comprised of differently sized pores. Here, we present morphological data from an ontogenetic series of the filtering apparatus within silver carp. These data inform hypotheses regarding both how these gill raker plates may have evolved from a more basal condition, as well as how this novel architecture allows this species to feed on exceedingly small phytoplankton, particles that represent a greater filtering challenge to the typical anatomy of the gill rakers of fishes.     

Responses of the teleost Hoplias malabaricus to hypoxia

Synopsis Oxygen uptake (VO₂) during graded hypoxia, rate of hypoxia acclimation, breathing frequency (f_R), breath volume (V_{S, R}) and gill ventilation (V_G) were measured in Hoplias malabaricus. Normoxia and hypoxia acclimated fish had similar and constant VO₂ and V_G in a range of water PO₂ from 150 to 25 mmHg. Hypoxia acclimated fish showed significantly higher VO₂ in severe hypoxia (PO₂ <15 mmHg). Normoxia acclimated fish showed symptoms similar to hypoxic coma after 1 h of exposure to water PO₂ of 10 mmHg whereas the same symptoms were observed only at PO₂ of 5 mmHg for fish acclimated to hypoxia. Fish required 14 days to achieve full acclimation to hypoxia (PO₂ ≥25 mmHg). Lowering of water PO₂ from 150 to 25 mmHg resulted in normoxic fish showing a 3–2 fold increase in V_G. The increase was the result of an elevation in V_{S, R} rather than f_R. Among normoxia acclimated specimens, small fish showed a higher V_G per unit weight than the large ones in both normoxia (PO₂ =150 mmHg) and hypoxia (PO₂ = 15 mmHg). A decrease in the ventilatory requirement (V_G/VO₂) with increased body weight was recorded in hypoxia (PO₂ = 15 mmHg).     

Effects of temperature and dissolved oxygen on heart rate,ventilation rate and oxygen consumption of spangled perch,Leiopotherapon unicolor (Günther 1859), (Percoidei,Teraponidae)

Summary Heart, ventilation and oxygen consumption rates ofLeiopotherapon unicolor were studied at temperatures ranging from 5 to 35°C, and during progressive hypoxia from 100% to 5% oxygen saturation. Biopotentials recorded from the water surrounding the fish corresponded to ventilation movements, and are thought to originate from the ventilatory musculature. Cardio-respiratory responses to temperature and dissolved oxygen follow the typical teleost pattern, with bradycardia, increased ventilation rate and reduced oxygen consumption occurring during hypoxia. However, ventilation rate did not increase at 15°C and below. Ventilation rate showed a slower response to increasing temperature (normoxic Q₁₀=1.39) than heart rate and oxygen consumption (normoxic Q₁₀=2.85 and 2.38).L. unicolor is unable to survive prolonged hypoxia by utilising anaerobic metabolism, but has a large gill surface area which presumably facilitates oxygen uptake in hypoxic environments. Periodic ventilation during normoxia in restingL. unicolor may improve ventilation efficiency by increasing the oxygen diffusion gradient across the gills.Abbreviations EBG electrobranchiogram - ECG electrocardiogram     

The filter pads and filtration mechanisms of the devil rays: Variation at macro and microscopic scales

Three lineages of cartilaginous fishes have independently evolved filter feeding (Lamniformes: Megachasma and Cetorhinus, Orectolobiformes: Rhincodon, and Mobulidae: Manta and Mobula); and the structure of the branchial filters is different in each group. The filter in Rhincodon typus has been described; species within the Lamniformes have simple filamentous filters, but the anatomy and ultrastructure of the branchial filter in the mobulid rays varies and is of functional interest. In most fishes, branchial gill rakers are elongated structures located along the anterior ceratobranchial and/or epibranchial arches; however, mobulid gill rakers are highly modified, flattened, lobe‐like structures located on the anterior and posterior epibranchial elements as well as the ceratobranchials. The ultrastructure of the filter lobes can be smooth or covered by a layer of microcilia, and some are denticulated along the dorsal and ventral lobe surface. Flow through the mobulid oropharyngeal cavity differs from other filter‐feeding fishes in that water must rapidly deviate from the free stream direction. There is an abrupt 90° turn from the initial inflowing path to move through the laterally directed branchial filter pores, over the gill tissue, and out the ventrally located gill slits. The deviation in the flow must result in tangential shearing stress across the filter surface. This implies that mobulids can use cross‐flow filtration in which this shearing force serves as a mechanism to resuspend food particles initially caught by sieving or another capture mode. These particles will be transported by the cross filter flow toward the esophagus. We propose that species with cilia on the rakers augment the shear mediated movement of particles along the filter with ciliary transport. J. Morphol. 274:1026–1043, 2013. © 2013 Wiley Periodicals, Inc.     

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.     

Confocal microscopy as a useful approach to describe gill rakers of Asian species of carp and native filter‐feeding fishes of the upper Mississippi River system

To better understand potential diet overlap among exotic Asian species of carp and native species of filter‐feeding fishes of the upper Mississippi River system, microscopy was used to document morphological differences in the gill rakers. Analysing samples first with light microscopy and subsequently with confocal microscopy, the three‐dimensional structure of gill rakers in Hypophthalmichthys molitrix, Hypophthalmichthys nobilis and Dorosoma cepedianum was more thoroughly described and illustrated than previous work with traditional microscopy techniques. The three‐dimensional structure of gill rakers in Ictiobus cyprinellus was described and illustrated for the first time.     

Respiratory responses of the striped mullet,Mugil cephalus (L.) to hypoxic conditions*

Ventilation volume, ventilatory frequency, ventilatory stroke volume, percentage utilization of oxygen and respiratory metabolism were measured on unanaesthetized striped mullet, Mugil cephalus L., under ambient and hypoxic conditions with a modified van Dam respiration chamber. Hypoxia caused a statistically significant increase in ventilation volume, ventilatory frequency, and ventilatory stroke volume and a significant decrease in percentage utilization of oxygen. The routine rate of respiratory metabolism was not significantly altered by hypoxia. These responses probably represent ventilatory adjustments which serve to maintain a constant oxygen supply to the gills under conditions of oxygen depletion.     

Cardiorespiratory responses of the woodchuck and porcupine to CO2 and hypoxia

Summary The burrow-dwelling woodchuck (Marmota monax) (mean body wt.=4.45±1 kg) was compared to a similar-sized (5.87±1.5 kg) but arboreal rodent, the porcupine (Erithrizon dorsatum), in terms of its ventilatory and heart rate responses to hypoxia and hypercapnia, and its blood characteristics.V _T,f,T _I andT _E were measured by whole-body plethysmography in four awake individuals of each species. The woodchuck has a longerT _E/T _TOT (0.76±0.03) than the porcupine (0.61±0.03). The woodchuck had a higher threshold and significantly smaller slope to its CO₂ ventilatory response compared to the porcupine, but showed no difference in its hypoxic ventilatory response. The woodchuck P₅₀ of 27.8 was hardly different from the porcupine value of 30.7, but the Bohr factor, –0.72, was greater than the porcupine's, –0.413. The woodchuck breathing air has PaCO₂=48 (±2) torr, PaO₂=72 (±6), pHa=7.357 (±0.01); the porcupine blood gases are PaCO₂=34.6 (±2.8), PaO₂=94.9 (±5), pHa=7.419 (±0.03), suggesting a difference in PaCO₂/pH set points. The woodchuck exhibited no reduction in heart rate with hypoxia, nor did it have the low normoxic heart rate observed in other burrowing mammals.     

Specific features of structure and functioning of gill-jaw apparatus of whitefish <Emphasis Type="Italic">Coregonus lavaretus pravdinellus</Emphasis>

The food spectrum of multirakered whitefish Coregonus lavaretus pravdinellus was studied. It was shown that C. lavaretus pravdinellus feeds mainly on large zooplankton; however, it also consumes nauplii whose average sizes are considerably smaller than the intergill distance. This fact counts in favor of the view of the active functioning of gill rakers. The type of feeding of C. lavaretus is related to a set of morphological characters of the gill-jaw apparatus and the head, such as the number of gill rakers, the length of the upper and lower jaws, mouth position, and the shape and slope of the snout tip area. A great number of gill rakers allows coregonids to use as food a wider size range of prey.     

Effects of fatty acid provision during severe hypoxia on routine and maximal performance of the in situ tilapia heart

The ability to maintain stable cardiac function during environmental hypoxia exposure is crucial for hypoxia tolerance in animals and depends upon the maintenance of cardiac energy balance as well as the state of the heart’s extracellular environment (e.g., availability of metabolic fuels). Hypoxic depression of plasma [non-esterified fatty acids] (NEFA), an important cardiac aerobic fuel, is a common response in many species of hypoxia-tolerant fishes, including tilapia. We tested the hypothesis that decreased plasma [NEFA] is important for maintaining stable cardiac function during and following hypoxia exposure, based on the premise that continued reliance upon cardiac fatty acid metabolism under such conditions could impair cardiac function. We examined the effect of severe hypoxia exposure (PO₂ < 0.2 kPa) on routine and maximum performance of the in situ perfused tilapia heart under conditions of routine (400 μmol L^?1) and low (75 μmol L^?1) [palmitate], which mimicked the in vivo levels of plasma [NEFA] found in normoxic and hypoxic tilapia, respectively. Under both concentrations of palmitate, the in situ tilapia heart showed exceptional hypoxic performance as a result of a high maximum glycolytic potential, confirming our previous results using a perfusate without fatty acids. We additionally provide evidence suggesting that non-contractile ATP demand is depressed in tilapia heart during hypoxia exposure. Cardiac performance during and following severe hypoxia exposure was unaffected by the level of palmitate. Thus, we conclude that hypoxic depression of plasma [NEFA] in fishes does not play a role in cardiac hypoxia tolerance.     

Extension of the Functional Range of Respiratory and Gas Exchange Responses in Repetitive Hypoxia

External respiration and gas exchange were studied in healthy volunteers during a session of intermittent normobaric hypoxia (INH) consisting of three cycles of breathing alternately a hypoxic mixture (10.7% O₂) for 5 min and normal air for 5 min. The ventilatory response increased in the successive cycles of hypoxia and gradually decreased during the normoxic intervals. These changes were accompanied by an increase in carbon dioxide in lung air, which was not eliminated by the increased pulmonary ventilation during the hypoxic intervals. However, the mean oxygen consumption did not change during the INH session because the ventilatory reactivity and breathing depth, as well as the efficiency of oxygen utilization, increased from cycle to cycle.__________Translated from Fiziologiya Cheloveka, Vol. 31, No. 3, 2005, pp. 100–107.Original Russian Text Copyright © 2005 by Krivoshchekov, G. Divert, V. Divert.     

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.     

Ecomorphology of the eyes and skull in zooplanktivorous labrid fishes

Zooplanktivory is one of the most distinct trophic niches in coral reef fishes, and a number of skull traits are widely recognized as being adaptations for feeding in midwater on small planktonic prey. Previous studies have concluded that zooplanktivores have larger eyes for sharper visual acuity, reduced mouth structures to match small prey sizes, and longer gill rakers to help retain captured prey. We tested these three traditional hypotheses plus two novel adaptive hypotheses in labrids, a clade of very diverse coral reef fishes that show multiple independent evolutionary origins of zooplanktivory. Using phylogenetic comparative methods with a data set from 21 species, we failed to find larger eyes in three independent transitions to zooplanktivory. Instead, an impression of large eyes may be caused by a size reduction of the anterior facial region. However, two zooplanktivores (Clepticus parrae and Halichoeres pictus) possess several features interpreted as adaptations to zooplankton feeding, namely large lens diameters relative to eye axial length, round pupil shape, and long gill rakers. The third zooplanktivore in our analysis, Cirrhilabrus solorensis, lacks all above features. It remains unclear whether Cirrhilabrus shows optical specializations for capturing planktonic prey. Our results support the prediction that increased visual acuity is adaptive for zooplanktivory, but in labrids increases in eye size are apparently not part of the evolutionary response.     

Combined ventilatory responses to aerial hypoxia and temperature in the South American lungfish Lepidosiren paradoxa

The control of pulmonary ventilation in South American lungfish Lepidosiren paradoxa is poorly understood. Interactions between temperature and hypoxia are particularly relevant due to large seasonal variations of its habitat. Therefore, we tested the hypothesis that the ventilatory responses to aerial hypoxia of Lepidosiren are highly dependent on ambient temperature. We used a pneumotachograph to measure pulmonary ventilation (V_E), tidal volume (V_T) and respiratory frequency (f_R) during normoxic (21% O₂) and hypoxic (12%, 10% and 7% O₂) conditions at two temperatures (25 and 35 °C). Blood gases, arterial PO₂ (PaO₂), arterial PCO₂ (PaCO₂) and arterial pH (pH_a) were also evaluated. At 25 °C, V_E increased significantly at 10% and 7% hypoxic levels when compared to the control value (21% O₂). At 35 °C, all hypoxic levels elicited a significant increase of V_E relative to control values. V_E is augmented mostly by increases of respiratory frequency (f_R), and there were significant interactions (p<0.001) between aerial hypoxia and temperature. PaCO₂ increased from ∼22 mmHg (normoxic value at 25 °C) to ∼32 mmHg (normoxic value at 35 °C). Concomitantly, the pH_a decreased from 7.51 (25 °C) to 7.38 (35 °C). Hypoxia-induced hyperventilation caused a reduction in PaCO₂ and an increase in pH_a, which were more pronounced at 35 °C than at 25 °C, reflecting an increased hyperventilation under the high temperature. In conclusion, the magnitude of ventilatory response is highly temperature-dependent in L. paradoxa, which is important for an animal experiencing large seasonal variations.     

Time-course of the polycythemic response in normoxic and hypoxic mice with high blood oxygen affinity induced by cyanate administration

The Hb-O₂ affinity and the erythropoietic response as a function of time were studied in mice treated with sodium cyanate for up to 2 months. Cyanate increased the Hb-O₂ affinity in normoxic mice more than in chronically hypoxic mice. The hemoglobin concentration rose as a function of time both in normoxic and hypoxic conditions but reached higher levels in hypoxia. After 42 days of study (21 days of hypoxia) hemoglobin reached maximum levels and thereafter showed a plateau in both cyanate and control animals. It is concluded that a chronic left-shifted oxygen dissociation curve does not avoid the development of hypoxic polycythemia in mice. Moreover, prolonged cyanate administration potentiates the crythropoietic response to chronic hypoxia. Since polycythemia is an index of tissue hypoxia, the results show that the high hemoglobin affinity did not prevent tissue hypoxia in low PO₂ conditions. Results showing beneficial effects of high hemoglobin oxygen affinity induced by cyanate based on acute hypoxic expositions should be cautiously interpreted with regard to their adaptive value in animals chronically exposed to natural or simulated hypoxia.Abbreviations Hb hemoglobin - NaOCN sodium cyanate - ODC oxygen dissociation curve - P ₅₀ PO₂ at which hemoglobin is half saturated with O₂     

Hypoxia modifies the feeding preferences of <Emphasis Type="Italic">Drosophila</Emphasis>. Consequences for diet dependent hypoxic survival

Background  

Recent attention has been given to the relationships between diet, longevity, aging and resistance to various forms of stress. Flies do not simply ingest calories. They sense different concentrations of carbohydrate and protein macronutrients and they modify their feeding behavior in response to changes in dietary conditions. Chronic hypoxia is a major consequence of cardiovascular diseases. Dietary proteins have recently been shown to decrease the survival of chronically hypoxic Drosophila. Whether flies modify their feeding behavior in response to hypoxia is not currently known. This study uses the recently developed capillary feeding assay to analyze the feeding behavior of normoxic and chronically hypoxic Drosophila melanogaster.     

Effects of Hypoxic Exposure during Feeding on SDA and Postprandial Cardiovascular Physiology in the Atlantic Cod,Gadus morhua

Some Atlantic cod in the Bornholm Basin undertake vertical foraging migrations into severely hypoxic bottom water. Hypoxic conditions can reduce the postprandial increase in gastrointestinal blood flow (GBF). This could subsequently postpone or reduce the postprandial increase in oxygen consumption (MO₂), i.e. the SDA, leading to a disturbed digestion. Additionally, a restricted oxygen uptake could result in an oxygen debt that needs to be compensated for upon return to normoxic waters and this may also affect the ability to process the food. Long-term cardio-respiratory measurements were made on fed G. morhua in order to understand how the cardio-respiratory system of feeding fish respond to a period of hypoxia and a subsequent return to normoxia. These were exposed to 35% water oxygen saturation for 90 minutes, equivalent to the time and oxygen level cod voluntarily endure when searching for food in the Bornholm Basin. We found that i) gastric and intestinal blood flows, cardiac output and MO₂ increased after feeding, ii) gastric and intestinal blood flows were spared in hypoxia, and iii) there were no indications of an oxygen debt at the end of the hypoxic period. The magnitude and time course of the measured variables are similar to values obtained from fish not exposed to the hypoxic period. In conclusion, when cod in the field search for and ingest prey under moderate hypoxic conditions they appear to stay within safe limits of oxygen availability as we saw no indications of an oxygen debt, or negative influence on digestive capacity, when simulating field observations.     

Evidence for ram suspension feeding by the piscivore, Seriola dumerili (Carangidae)

Synopsis We have quantitatively analyzed a videotape of Seriola dumerili (Carangidae) displaying ram suspension-feeding behavior and ram ventilation in the field. This is the first report of facultative suspension feeding by a piscivorous carangid. The intraoral morphology of S. dumerili is not typical of ram suspension-feeding fishes in that closely-spaced, long gill rakers are lacking. While the mechanism of particle retention is not known for any ram suspension-feeding fish species, scanning electron microscopy revealed denticles on the branchial surfaces of S. dumerili that could play a role in particle entrapment.