Osmoregulatory Costs Research Articles

Metabolic cost of osmoregulation by the gastro-intestinal tract in marine teleost fish.

Introduction: Although dozens of studies have attempted to determine the metabolic cost of osmoregulation, mainly by comparing standard metabolic rates (SMR) in fish acclimated to different salinities, consensus is still lacking. Methods: In the present study, using the Gulf toadfish, Opsanus beta, we aimed to determine the metabolic cost of esophageal and intestinal osmoregulatory processes by estimating ATP consumption from known ion transport rates and pathways and comparing these estimates with measurements on isolated tissues. Further, we performed whole animal respirometry on fish acclimated to 9, 34 and 60ppt. Results and Discussion: Our theoretical estimates of esophageal and intestinal osmoregulatory costs were in close agreement with direct measurements on isolated tissues and suggest that osmoregulation by these tissues amounts to ∼2.5% of SMR. This value agrees well with an earlier attempt to estimate osmoregulation cost from ion transport rates and combined with published measurements of gill osmoregulatory costs suggests that whole animal costs of osmoregulation in marine teleosts is ∼7.5% of SMR. As in many previous studies, our whole animal measurements were variable between fish and did not seem suited to determine osmoregulatory costs. While the esophagus showed constant metabolic rate regardless of acclimation salinity, the intestine of fish acclimated to higher salinities showed elevated metabolic rates. The esophagus and the intestine had 2.1 and 3.2-fold higher metabolic rates than corresponding whole animal mass specific rates, respectively. The intestinal tissue displays at least four different Cl- uptake pathways of which the Na+:Cl-:2K+ (NKCC) pathway accounts for 95% of the Cl- uptake and is the most energy efficient. The remaining pathways are via apical anion exchange and seem to primarily serve luminal alkalinization and the formation of intestinal CaCO3 which is essential for water absorption.

Metabolic costs associated with seawater acclimation in a euryhaline teleost, the fourspine stickleback (Apeltes quadracus).

The cost of osmoregulation in teleosts has been debated for decades, with estimates ranging from one to 30 % of routine metabolic rate. The variation in the energy budget appears to be greater for euryhaline fish due to their ability to withstand dynamic salinity levels. In this study, a time course of metabolic and physiological responses of the euryhaline fourspine stickleback (Apeltes quadracus) acclimated to freshwater (FW) and then exposed to seawater (SW) was examined. There was 18% mortality in the first 3 days following exposure to SW, with no mortalities in the FW control group. Gill Na+/K+-ATPase (NKA) activity, an index of osmoregulatory capacity, increased 2.6-fold in SW fish peaking on days 7 and 14. Gill citrate synthase activity, an index of aerobic capacity, was 50-62% greater in SW than FW fish and peaked on day 7. Tissue water content was significantly lower in the SW fish on day 1 only, returning to FW levels by day 3. Routine metabolic rate was decreased within 24h of SW exposure and was maintained slightly (8-22%) but significantly lower in SW compared to FW water controls throughout the 2-week experiment. These results indicate that elevated salinity resulted in increased SW osmoregulatory and aerobic capacity in the gill, but with a reduced whole animal metabolic rate to this euryhaline species.

Kingfish (Seriola lalandi) adjust to low salinity with only subtle effects to cardiorespiratory and growth performance

At reduced salinities nearing isosmotic conditions, marine fishes experience reduced osmotic gradients between body fluids and the surrounding water, which should lower energetic costs of osmoregulation. Such energy savings on osmoregulation can potentially be directed to other processes such as growth, suggesting the possibility that rearing euryhaline fishes under reduced salinity in aquaculture may be a beneficial practice. The yellowtail kingfish (Seriola lalandi) is one such aquaculture species that appears to benefit from low salinity, as juveniles display faster growth when reared at salinities approaching isosmotic conditions. Here, we tested the hypothesis that, due to reduced osmoregulatory costs, growth is improved in sub-adult kingfish reared at low salinity, and this is associated with a down-regulation of resting cardiorespiratory activity reflecting energetic savings. Furthermore, to gain a more complete picture of how low salinity impacts cardiorespiratory function in kingfish, we also assessed maximal cardiorespiratory responses to enforced exercise. Two experiments were carried out. The first assessed resting and maximum cardiac and respiratory performance of kingfish acclimated to seawater (35 ppt), and after ~20 h (acute) or > 4 weeks (chronic) exposure to brackish water (17 ppt). Acute 17 ppt exposure reduced standard metabolic rate (i.e. resting O2 consumption rate; 179.4 mg O2∙h−1∙kg−1) relative to fish maintained in seawater (198.3 mg O2∙h−1∙kg−1), but this difference was no longer apparent following chronic acclimation to 17 ppt (191.3 mg O2∙h−1∙kg−1). While maximum metabolic rate was not affected by salinity, kingfish both acutely transferred and acclimated to 17 ppt had a reduced excess post-exercise O2 consumption compared to fish in 35 ppt. Acclimation to 17 ppt was also associated with a reduced proportion of ventricle compact myocardium. In a second experiment, we analyzed growth rate and feed conversion efficiency of kingfish acclimated to seawater (35 ppt) or brackish water (24 and 12 ppt) for 8 weeks. Contrary to our initial hypothesis, growth rate and feed conversion efficiency were slightly deteriorated (by ~5 and ~ 6% for growth rate and feed conversion efficiency, respectively) after 4 weeks acclimation to 12 ppt; however, these differences were no longer apparent after 8 weeks acclimation. This study shows neither substantial benefits nor costs of brackish water exposure to cardiorespiratory and growth performance in sub-adult kingfish, suggesting this species can be reared at salinities as low as 12 ppt.

Distribution of adult fish and spawning nests of estuarine-dependent amphidromous goby (

Adults of the marine-originated amphidromous goby (Gymnogobius petschiliensis) inhabit both freshwater and brackish-water areas, unlike many other amphidromous species, which spend their entire lives, except the larval stage, in freshwater. Furthermore, adult G. petschiliensis individuals incur higher osmoregulatory costs in freshwater than those in hypertonic brackish water under laboratory conditions, suggesting that the ecology of the species is largely dependent on high-salinity (ancestral) environments. Therefore, a detailed information on the ecology of G. petschiliensis will help elucidate the diversity and evolution of amphidromy. Here, this study assessed the habitat use and freshwater dependency of G. petschiliensis in two streams in central Japan. Year-round surveys showed that adult density was higher in freshwater than in brackish water during the non-spawning season. This implies that adults chose salinity habitats according to ecological conditions (e.g. inter- and intraspecific competition, and predation risk) without being bound by physiological preferences. Conversely, most egg clutches were found in brackish water. Furthermore, adult density in brackish water increased with the increase in spawning events, suggesting that the adults migrated downstream for spawning. This preference for spawning in brackish water rather than in freshwater may be attributed to the constraints of their reproductive physiology.

Alternative reproductive tactics are associated with sperm performance in invasive round goby from two different salinity environments.

During male–male competition, evolution can favor alternative reproductive tactics. This often results in a dominant morph that holds a resource, such as a nest for egg laying, which competes with a smaller sneaker morph that reproduces by stealing fertilizations. The salinity environment can influence male growth rates, for example, via osmoregulatory costs, which in turn may influence the use of sneaker tactics for small males competing for mating opportunities. Salinity can also affect sperm directly; however, little is known of how salinity influences sneaker tactics through sperm performance. We sampled males of the invasive round goby (Neogobius melanostomus) from two environments, a freshwater river and a brackish estuary. This fish has two male morphs: nest‐holding dark males and non‐nest‐holding light males. We examined the role of water salinity of 0, 8, and 16 on sperm performance and found that for estuarine males, a salinity of 0 reduced sperm velocity compared to a salinity of 8 and 16. Riverine males had low velocity in all salinities. Sperm viability also decreased by over 30% in 0 salinity, compared to 8 and 16, for fish from both environments. Gobies produce ejaculate contents in specialized glands that could in theory shield sperm in an adverse environment. However, gland contents did not improve sperm performance in our tests. Body mass and age estimates indicate that riverine males invested more in somatic growth compared to estuarine males. Estuarine light morph males had a high enough gonadosomatic index to indicate sneaker tactics. We propose that when sperm performance is low, such as for the riverine males, sneaker tactics are ineffective and will be selected against or phenotypically suppressed. Instead, we interpret the increased investment in somatic growth found in riverine males as a life‐history decision that is advantageous when defending a nest in the next reproductive season.

The interplay between ambient temperature and salt intake affects oxidative status and immune responses in a ubiquitous Neotropical passerine, the rufous-collared sparrow

Physiological traits associated with maintenance, growth, and reproduction demand a large amount of energy and thus directly influence an animal's energy budget, which is also regulated by environmental conditions. In this study, we evaluated the interplay between ambient temperature and salinity of drinking water on energy budgets and physiological responses in adult Rufous-collared sparrow (Zonotrichia capensis), an omnivorous passerine that is ubiquitous in Chile and inhabits a wide range of environments. We acclimated birds to 30 days at two ambient temperatures (27 °C and 17 °C) and drinking water salinity (200 mM NaCl and fresh water) conditions. We evaluated: 1) the aerobic scope and the activities of mitochondrial metabolic enzymes, 2) osmoregulatory parameters, 3) the skin-swelling immune response to an antigen, 4) oxidative status, and 5) the length of telomeres of red blood cells. Our results confirm that Z. capensis tolerates the chronic consumption of moderate levels of salt, maintaining body mass but increasing their basal metabolic rates consistent with expected osmoregulatory costs. Additionally, the factorial aerobic scope was higher in birds acclimated to fresh (tap) water at both 17° and 27 °C. Drinking water salinity and low ambient temperatures negatively impacted inflammatory response, and we observed an increase in lipid peroxidation and high levels of circulating antioxidants at low temperatures. Finally, telomere length was not affected by osmo- and thermoregulatory stress. Our results did not support the existence of an interplay between environmental temperature and drinking water salinity on most physiological and biochemical traits in Z. capensis, but the negative effect of these two factors on the inflammatory immune response suggests the existence of an energetic trade-off between biological functions that act in parallel to control immune function.

Effects of salinity on swimming performance and oxygen consumption rate of shiner perch Cymatogaster aggregata

Environmental factors add constraints to organismal performance at their extremes, but support optimal performance at energetically beneficial conditions. In aquatic environments, salinity adds costs for ion transportation to the energetic budgets of osmoregulating animals, such as teleost fishes. These additional costs may limit the available energy for important ecological traits of fishes, including maximal and optimal swimming performance, which are required for successful foraging and migration in the wild. Here, we hypothesize that swimming performance, and its related costs, will be optimized at near-isoosmotic salinity, and decline under more saline conditions. Using the euryhaline shiner perch (Cymatogaster aggregata) as a model for coastal fishes, we determined critical swimming speeds and oxygen consumption rates during swimming at salinities of 12 g kg−1 (near-isoosmotic, brackish, S12) and 31 g kg−1 (hyperosmotic, marine, S31). Most tested metrics were unaffected by salinity, including aerobic scope, active metabolic rate and optimal swimming speed. Likewise, critical swimming speed (in body lengths per second, BL s−1) was not significantly different between fishes acclimated to S12 (4.8 ± 0.6 BL s−1) or S31 (5.1 ± 0.5 BL s−1, means ± SD, n = 5) suggesting that the fish could swim and hunt for prey equally well regardless of salinity. However, S31 conditions did cause comparatively higher oxygen consumption rates at swimming speeds from 0.5 to 1.5 BL s−1, and a 20% increase in the extrapolated standard metabolic rate (i.e. cost of maintaining bodily functions). Our results confirm that there is an added energetic cost of salinity, but highlight that the cost of osmoregulation appears minimal relative to the energetic demands of swimming, and consequently has no effect on the maximal swimming performance of adult shiner perch. Given the strong salinity gradients naturally encountered in many coastal ecosystems, these data provide an explanation for the capacity of a coastal roaming species to move in an out of coastal habitat zones without significantly compromising their ability to hunt prey, avoid predation and migrate. As climate change locally affects environmental salinity, our results offer valuable insight towards the effects of environmental perturbations on fishes in coastal marine and estuarine habitats.

Body size influences energetic and osmoregulatory costs in frogs infected with Batrachochytrium dendrobatidis

Sloughing maintains the skins integrity and critical functionality in amphibians. Given the behavioural, morphological and osmoregulatory changes that accompany sloughing, this process is likely to be physiologically costly. Chytridiomycosis, a cutaneous disease of amphibians caused by the fungus Batrachochytrium dendrobatidis (Bd), disrupts skin function and increases sloughing rates. Moreover, mortality rates from chytridiomycosis are significantly higher in juveniles and so we hypothesised that smaller individuals maybe more susceptible to chytridiomycosis because of allometric scaling effects on the energetic and osmoregulatory costs of sloughing. We measured in-vivo cutaneous ion loss rates and whole animal metabolic rate (MR) of Green tree frogs, Litoria caerulea, over a range of body sizes both infected and uninfected frogs during sloughing. Infected animals had a greater rate of ion loss and mass-specific MR during non-sloughing periods but there were no additional effects of sloughing on either of these parameters. There were also significant interactions with body size and Bd load indicating that smaller animals with higher Bd loads have greater rates of ion loss and higher energetic demands. Our results shed light on why smaller Bd-infected anurans often exhibit greater physiological disruption than larger individuals.

Moving Forward in a Reverse Estuary: Habitat Use and Movement Patterns of Black Drum (Pogonias cromis) Under Distinct Hydrological Regimes

Understanding the effects of freshwater inflow on estuarine fish habitat use is critical to the sustainable management of many coastal fisheries. The Baffin Bay Complex (BBC) of south Texas is typically a reverse estuary (i.e., salinity increases upstream) that has supported many recreational and commercial fisheries. In 2012, a large proportion of black drum (Pogonias cromis) landed by fishers were emaciated, leading to concerns about the health of this estuary. In response to this event and lacking data on black drum spatial dynamics, a 2-year acoustic telemetry study was implemented to monitor individual-based movement and seasonal distribution patterns. Coupled with simultaneous water quality monitoring, the relationship between environmental variables and fish movement was assessed under reverse and “classical” estuary conditions. Acoustic monitoring data suggested that the BBC represents an important habitat for black drum; individuals exhibited site fidelity to the system and were present for much of the year. However, under reverse estuary conditions, fish summertime distribution was constrained to the interior of the BBC, where food resources are limited (based on recent benthic sampling), with little evidence of movement across the system. Out of eight environmental variables used to model fish movement using multiple linear regression, the only significant variable was salinity, which exhibited a negative relationship with movement rate. These findings suggest that prolonged periods of hypersalinity, which are detrimental to other euryhaline species due to increased osmoregulatory costs, reduce black drum distribution patterns and can limit the species’ access to benthic habitats supporting abundant prey resources.

Plasma osmolality and oxygen consumption of perch Perca fluviatilis in response to different salinities and temperatures

The present study determined the blood plasma osmolality and oxygen consumption of the perch Perca fluviatilis at different salinities (0, 10 and 15) and temperatures (5, 10 and 20° C). Blood plasma osmolality increased with salinity at all temperatures. Standard metabolic rate (SMR) increased with salinity at 10 and 20° C. Maximum metabolic rate (MMR) and aerobic scope was lowest at salinity of 15 at 5° C, yet at 20° C, they were lowest at a salinity of 0. A cost of osmoregulation (SMR at a salinity of 0 and 15 compared with SMR at a salinity of 10) could only be detected at a salinity of 15 at 20° C, where it was 28%. The results show that P. fluviatilis have capacity to osmoregulate in hyper-osmotic environments. This contradicts previous studies and indicates intraspecific variability in osmoregulatory capabilities among P. fluviatilis populations or habitat origins. An apparent cost of osmoregulation (28%) at a salinity of 15 at 20° C indicates that the cost of osmoregulation in P. fluviatilis increases with temperature under hyperosmotic conditions and a power analysis showed that the cost of osmoregulation could be lower than 12·5% under other environmental conditions. The effect of salinity on MMR is possibly due to a reduction in gill permeability, initiated to reduce osmotic stress. An interaction between salinity and temperature on aerobic scope shows that high salinity habitats are energetically beneficial during warm periods (summer), whereas low salinity habitats are energetically beneficial during cold periods (winter). It is suggested, therefore, that the seasonal migrations of P. fluviatilis between brackish and fresh water is to select an environment that is optimal for metabolism and aerobic scope.

Juvenile winter flounder (Pseudopleuronectes americanus) and summer flounder (Paralichthys dentatus) utilization of Southern New England nurseries: Comparisons among estuarine, tidal river, and coastal lagoon shallow-water habitats.

This study evaluated the relative importance of the N arragansett Bay estuary (RI and MA, USA), and associated tidal rivers and coastal lagoons, as nurseries for juvenile winter flounder, Pseudopleuronectes americanus, and summer flounder, Paralichthys dentatus. Winter flounder (WF) and summer flounder (SF) abundance and growth were measured from May to October (2009-2013) and served as indicators for the use and quality of shallow-water habitats (water depth < 1.5-3.0 m). These bioindicators were then analyzed with respect to physiochemical conditions to determine the mechanisms underlying intra-specific habitat selection. WF and SF abundances were greatest in late May and June (maximum monthly mean = 4.9 and 0.55 flounder/m2 for WF and SF, respectively), and were significantly higher in the tidal rivers relative to the bay and lagoons. Habitat-related patterns in WF and SF abundance were primarily governed by their preferences for oligohaline (0.1-5 ppt) and mesohaline (6-18 ppt) waters, but also their respective avoidance of hypoxic conditions (< 4 mg DO/L) and warm water temperatures (> 25 °C). Flounder habitat usage was also positively related to sediment organic content, which may be due to these substrates having sufficiently high prey densities. WF growth rates (mean = 0.25 ± 0.14 mm/d) were negatively correlated with the abundance of conspecifics, whereas SF growth (mean = 1.39 ± 0.46 mm/d) was positively related to temperature and salinity. Also, contrary to expectations, flounder occupied habitats that offered no ostensible advantage in intra-specific growth rates. WF and SF exposed to low salinities in certain rivers likely experienced increased osmoregulatory costs, thereby reducing energy for somatic growth. Low-salinity habitats, however, may benefit flounder by providing refugia from predation or reduced competition with other estuarine fishes and macro-invertebrates. Examining WF and SF abundance and growth across each species' broader geographic distribution revealed that southern New England habitats may constitute functionally significant nurseries. These results also indicated that juvenile SF have a geographic range extending further north than previously recognized.

Hyperventilation and blood acid-base balance in hypercapnia exposed red drum (Sciaenops ocellatus).

Hyperventilation is a common response in fish exposed to elevated water CO2. It is believed to lessen the respiratory acidosis associated with hypercapnia by lowering arterial PCO2, but the contribution of hyperventilation to blood acid-base compensation has yet to be quantified. Hyperventilation may also increase the flux of irons across the gill epithelium and the cost of osmoregulation, owing to the osmo-respiratory compromise. Therefore, hypercapnia exposed fish may increase standard metabolic rate (SMR) leaving less energy for physiological functions such as foraging, migration, growth and reproduction. Here we show that gill ventilation, blood PCO2 and total blood [CO2] increased in red drum (Sciaenops ocellatus) exposed to 1000 and 5000 µatm water CO2, and that blood PCO2 and total blood [CO2] decrease in fish during hypoxia induced hyperventilation. Based on these results we estimate the ventilatory contributions to total acid-base compensation in 1000 and 5000 µatm water CO2. We find that S. ocellatus only utilize a portion of its ventilatory capacity to reduce the acid-base disturbance in 1000 µatm water CO2. SMR was unaffected by both salinity and hypercapnia exposure indicating that the cost of osmoregulation is small relative to SMR, and that the lack of increased ventilation in 1000 µatm water CO2 despite the capacity to do so is not due to an energetic tradeoff between acid-base balance and osmoregulation. Therefore, while ocean acidification may impact ventilatory parameters, there will be little impact on the overall energy budget of S. ocellatus.

Osmoregulatory and metabolic costs of salt excretion in the Rufous-collared sparrow Zonotrichia capensis

Recent experiments on shorebirds have demonstrated that maintaining an active osmoregulatory machinery is energetically expensive. This may, in part, explain diet and habitat selection in birds with salt glands. However little is known about the osmoregulatory costs in birds lacking functional salt glands. In these birds, osmotic work is done almost exclusively by the kidneys. We investigated the osmoregulatory cost in a bird species lacking functional salt glands, the passerine Zonotrichia capensis. After 20days of acclimation to fresh water (FW) and salt water (200mM NaCl, SW), SW birds tended to be heavier than FW birds. However, this difference was not statistically significant. Total basal metabolic rate was higher in SW birds as compared with FW birds. Renal and heart masses were also higher in the SW group. We also found greater medullary development and an increase in urine osmolality in the SW group. In spite of Z. capensis' ability to tolerate a moderate salt load in the laboratory, we hypothesize that increased cost of maintenance produced by salt consumption may significantly affect energy budget, dietary, and habitat choices in the field.

Salinity selection and preference of the grey snapper Lutjanus griseus: field and laboratory observations

Field observations were supplemented with laboratory experiments to reveal patterns of salinity selection and preference for grey snapper Lutjanus griseus (c. 21 cm total length, L(T)), an ecologically and economically important species in the south-eastern U.S.A. Fish abundance data were examined from a long-term field survey conducted in the mangrove habitats of Biscayne Bay, Florida, where salinities ranged from <1 to 40. First, regression analyses indicated significant, positive linear relationships with salinity for both L. griseus frequency of occurrence and concentration (density when present). These patterns are inconsistent with physiological expectations of minimizing energetic osmoregulatory costs. Next, the salinity preference and swimming activity of 11 L. griseus (ranging from 18 to 23 cm L(T)) were investigated using a newly developed electronic shuttlebox system. In the laboratory, fish preferred intermediate salinities in the range of 9-23. Swimming activity (measured in terms of spontaneous swimming speed) followed a parabolic relationship with salinity, with reduced activity at salinity extremes perhaps reflecting compensation for higher osmoregulatory costs. It is suspected that the basis of the discrepancy between laboratory and field observations for size classes at or near maturity ultimately relates to the reproductive imperative to move towards offshore (high-salinity) coral-reef habitats, a necessity that probably overrides the strategy of minimizing osmoregulatory energetic costs.

Przewalski’s Naked Carp (Gymnocypris przewalskii): An Endangered Species Taking a Metabolic Holiday in Lake Qinghai, China

The naked carp is an endangered cyprinid that migrates annually between freshwater rivers, where it spawns, and Lake Qinghai, where it feeds and grows. Lake Qinghai is a high-altitude lake (3,200 m) in western China that currently exhibits the following composition (in mmol L(-1): [Na(+)] 200, [Cl(-)] 173, [Mg(2+)] 36, [Ca(2+)] 0.23, [K(+)] 5.3, total CO(2) 21, titration alkalinity 29; osmolality 375 mOsm kg(-1); pH 9.3), but concentrations are increasing because of water diversion and climate change. We studied the physiology of river water to lake water transfer. When river fish are transferred to lake water, there is a transitory metabolic acidosis followed by a slight respiratory alkalosis, and hemoconcentration occurs. All plasma electrolytes rise over the initial 48 h, and final levels in lake water-acclimated fish are very close to lake water concentrations for [Na(+)], [Cl(-)], [K(+)], and osmolality, whereas [Ca(2+)] continues to be regulated well above ambient levels. However, [Mg(2+)] rises to a much greater extent (fourfold in 48 h); final plasma levels in lake fish may reach 12 mmol L(-1) but are still much lower than in lake water (36 mmol L(-1)). At the same time, urine flow rate decreases drastically to <5% of river water values; only the renal excretion of Mg(2+) is maintained. Both gill and kidney Na(+),K(+)-ATPase rapidly decline, with final levels in lake water fish only 30% and 70%, respectively, of those in river water fish. Metabolic rate also quickly decreases on exposure to lake water, with O(2) consumption and ammonia-N excretion rates eventually falling to only 60% and 30%, respectively, of those in river fish, while plasma ammonia rises fivefold. The fish appear to be benefiting from a metabolic holiday at present because of decreases in iono- and osmoregulatory costs while in lake water; elevated plasma [Mg(2+)] and ammonia may be additional factors depressing metabolic rate. If the lake continues to dehydrate, these benefits may change to pathology.

Effect of Brackish Salinities on Oxygen Consumption of Bat Rays (Myliobatis californica)

Abstract We measured resting routine oxygen consumption rates (MO2, in mg O2 · h−1 · kg−0.67) of bat rays (Myliobatis californica) under two seawater (33, 35 ppt) and two brackish (15, 25 ppt) salinity conditions. A significant increase in MO2 was observed for rays in 15 and 25 ppt brackish water, compared with those in 33 or 35 ppt, presumably due to increased osmoregulatory costs. Our results suggest that energetic factors associated with seasonal decreases in salinity may influence the out-migration of bat rays from Tomales Bay (California) during the winter months.

Differences in maintenance energy expenditure by two estuarine shrimp ( Palaemonetes pugio and P. vulgaris) that may permit partitioning of habitats by salinity

The estuarine shrimp Palaemonetes pugio and P. vulgaris co-occur across a broad range in salinity. Field surveys and laboratory lethality tests suggest that low salinity conditions favor P. pugio over P. vulgaris. This study compared energetic expenditures across a range in salinity (0.5–35 ppt) to test the hypothesis that P. pugio experiences lower maintenance-energy requirements than P. vulgaris in low-salinity habitats. Standard metabolic rate (SMR) was measured as the minimum oxygen consumption rate at 25 °C to estimate daily maintenance-energy expenditure. SMR was greatest at 0.5 and least at 10 ppt (irrespective of species), and greater for P. vulgaris than for P. pugio. At low salinity (1.5–3 ppt), SMR was lower for P. pugio than for P. vulgaris. Energy expenditure did not coincide with the pattern predicted based upon osmoregulatory costs alone; no reduction was observed near the reported hemolymph concentration for P. vulgaris, although a minimum was observed near the hemolymph isoionic concentration for P. pugio. A local minimum in SMR by P. pugio between 1.5 and 3 ppt contrasted with relatively high SMR of P. vulgaris across this range. It appears that low-salinity habitats are energetically more favorable for P. pugio than for P. vulgaris. The results suggest an adaptive mechanism allowing P. pugio to occupy environments that present its competitor, P. vulgaris, with greater energetic challenges. While long-term exposure to very low salinity may be detrimental to both species, energetic traits of P. pugio may confer it with greater success than P. vulgaris in habitats in which salinity periodically fluctuates to low values.

Gill and intestinal Na + -K + ATPase activity, and estimated maximal osmoregulatory costs, in three high-energy-demand teleosts: yellowfin tuna ( Thunnus albacares ), skipjack tuna ( Katsuwonus pelamis ), and dolphin fish ( Coryphaena hippurus )

We hypothesize that the morpho-physiological adaptations that permit tunas to achieve maximum metabolic rates (MMR) that are more than double those of other active fishes should result in high water and ion flux rates across the gills and concomitant high osmoregulatory costs. The high standard metabolic rates (SMR) of tunas and dolphin fish may, therefore, be due to the elevated rates of energy expenditure for osmoregulation (i.e. teleosts capable of achieving exceptionally high MMR necessarily have SMR). Previous investigators have suggested a link between activity patterns and osmoregulatory costs based on Na+-K+ ATPase activity in the gills of active epipelagic and sluggish deep-sea fishes. Based on these observations, we conclude that high-energy-demand fishes (i.e. tunas and dolphin fish) should have exceptionally elevated gill and intestinal Na+-K+ ATPase activity reflecting their elevated rates of salt and water transfer. To test this idea and estimate osmoregulatory costs, we measured Na+-K+ ATPase activity (V max) in homogenates of frozen samples taken from the gills and intestines of skipjack and yellowfin tunas, and the gills of dolphin fish. As a check of our procedures, we made similar measurements using tissues from hybrid red tilapia (Oreochromis mossambicus ×O. niloticus). Contrary to our supposition, we found no difference in Na+-K+ ATPase activity per unit mass of gill or intestine in these four species. We estimate the cost of osmoregulation to be at most 9% and 13% of the SMR in skipjack tuna and yellowfin tuna, respectively. Our results, therefore, do not support either of our original suppositions, and the cause(s) underlying the high SMR of tunas and dolphin fish remain unexplained.

Influence of temperature, oxygen and salinity on the metabolism of the European sea bass

Standard (SMR) and routine (RMR) metabolic rates of groups (4 to 5 individuals) of European sea bass ( Dicentrarchus labrax) were measured at combinations of the following factors: temperature (10, 15, 20 and 25°C), oxygenation level (air saturation to 1.5 mg dm −3) and salinity (30, 20, 10 and 5‰). The influence of these environmental conditions on fish metabolic demand was then analysed through ANOVA. At 10, 15, 20 and 25°C, standard metabolic rates were 36, 65, 89, and 91 mg O 2 kg −1 h −1, respectively, while routine oxygen consumptions covered most of the metabolic range accessible. Osmoregulatory costs are linked to metabolic activity through ventilation. This relationship was highlighted by the observed interaction between environmental salinity and temperature. We were, however, unable to detect interactions between salinity and routine metabolic rate, or between salinity and oxygenation level. In order to delineate more precisely the restrictions imposed by water oxygenation on fish metabolic performance we determined the limiting oxygen concentration curves at each experimental temperature. We followed up by modelling the bass active metabolic rate (AMR) and metabolic scope (MS) as functions of both ambient temperature and oxygenation. These mathematical models allowed the characterisation of the controlling and limiting effects of water temperature and oxygen content on the metabolic capacity of the species. Thus, AMR at 10, 15 and 20°C were estimated at 65, 160 and 360 mg O 2 kg −1 h −1, respectively. However, at higher temperature (25°C) AMR dropped slightly (to 340 mg O 2 kg −1 h −1). Bass MS increased by a factor of 9 between 10 and 20°C, but diminished at higher temperatures. The present study contributes to our current understanding of the influences of environmental factors on the metabolism of sea bass and provides a bioenergetic basis for a study of how environmental constraints govern the spatial and temporal distribution pattern of this species.

High contents of trimethylamine oxide correlating with depth in deep-sea teleost fishes, skates, and decapod crustaceans.

In muscles of shallow-living marine animals, the osmolyte trimethylamine N-oxide (TMAO) is reportedly found (in millimoles of TMAO per kilogram of tissue wet weight) at 30-90 in shrimp, 5-50 in crabs, 61-181 in skates, and 10-70 in most teleost fish. Recently our laboratory reported higher levels (83-211 mmol/kg), correlating with habitat depth, in deep-sea gadiform teleosts. We now report the same trend in muscles of other animals, collected off the coast of Oregon from bathyal (1800-2000 m) and abyssal plain (2850 m) sites. TMAO contents (mmol/kg +/- SD) were as follows: zoarcid teleosts, 103 +/- 9 (bathyal) and 197 +/- 2 (abyssal); scorpaenid teleosts, 32 +/- 0 (shallow) and 141 +/- 16 (bathyal); rajid skates, 215 +/- 13 (bathyal) and 244 +/- 23 (abyssal); caridean shrimp, 76 +/- 16 (shallow), 203 +/- 35 (bathyal), and 299 +/- 28 (abyssal); Chionoecetes crabs, 22 +/- 2 (shallow) and 164 +/- 15 (bathyal). Deep squid, clams, and anemones also had higher contents than shallow species. Osmoconformers showed compensation between TMAO and other osmolytes. Urea contents (typically 300 mmol/kg in shallow elasmobranchs) in skates were 214 +/- 5 (bathyal) and 136 +/- 9 (abyssal). Glycine contents in shrimp were 188 +/- 17 (shallow) and 52 +/- 20 (abyssal). High TMAO contents may reflect diet, reduce osmoregulatory costs, increase buoyancy, or counteract destabilization of proteins by pressure.