Senior Fellow (By courtesy), Stanford Woods Institute for the Environment
Thermal physiology, open ocean predators, ecological physiology and tuna biology
The white shark (Carcharodon carcharias) is a wide-ranging apex predator in the northeastern Pacific (NEP). Electronic tagging has demonstrated that white sharks exhibit a regular migratory pattern, occurring at coastal sites during the late summer, autumn and early winter and moving offshore to oceanic habitats during the remainder of the year, although the purpose of these migrations remains unclear. The purpose of this study was to use stable isotope analysis (SIA) to provide insight into the trophic ecology and migratory behaviors of white sharks in the NEP. Between 2006 and 2009, 53 white sharks were biopsied in central California to obtain dermal and muscle tissues, which were analyzed for stable isotope values of carbon (?(13)C) and nitrogen (?(15)N). We developed a mixing model that directly incorporates movement data and tissue incorporation (turnover) rates to better estimate the relative importance of different focal areas to white shark diet and elucidate their migratory behavior. Mixing model results for muscle showed a relatively equal dietary contribution from coastal and offshore regions, indicating that white sharks forage in both areas. However, model results indicated that sharks foraged at a higher relative rate in coastal habitats. There was a negative relationship between shark length and muscle ?(13)C and ?(15)N values, which may indicate ontogenetic changes in habitat use related to onset of maturity. The isotopic composition of dermal tissue was consistent with a more rapid incorporation rate than muscle and may represent more recent foraging. Low offshore consumption rates suggest that it is unlikely that foraging is the primary purpose of the offshore migrations. These results demonstrate how SIA can provide insight into the trophic ecology and migratory behavior of marine predators, especially when coupled with electronic tagging data.
View details for DOI 10.1371/journal.pone.0030492
View details for Web of Science ID 000302741300013
View details for PubMedID 22355313
In this work, the temperature dependence of the sarco-endoplasmic reticulum Ca(2+) -ATPase (SERCA2) activity from rainbow trout Oncorhynchus mykiss cardiac ventricles was measured and compared with the mammalian SERCA2 isoform. The rate of ATP-dependent Ca(2+) transport catalysed by O. mykiss vesicles was totally abolished by thapsigargin and the Ca(2+) ionophore A(23187) . At warm temperatures (25 and 30° C), the SERCA2 from O. mykiss ventricles displayed the same rate of Ca(2+) uptake. At 35° C, the activity of the O. mykiss enzyme decreased after 20 min of reaction time. The rate of Ca(2+) uptake catalysed by the mammalian SERCA2 was temperature dependent exhibiting its maximal activity at 35° C. In contrast to the rate of Ca(2+) uptake, the rate of ATP hydrolysis catalysed by O. mykiss SERCA2 was not significantly different at 25 and 35° C, but the rate of ATP hydrolysis catalysed by the rat Rattus norvegicus SERCA2 isoform at 35° C was two-fold higher than at 25° C. At low temperatures (5 to 20° C), the rate of Ca(2+) uptake from O. mykiss SR was less temperature dependent than the R. norvegicus isoform, being able to sustain a high activity even at 5° C. The mean ±s.e. Q(10) values calculated from 25 to 35° C for ATP hydrolysis were 1·112 ± 0·026 (n = 3) and 2·759 ± 0·240 (n = 5) for O. mykiss and R. norvegicus, respectively. Taken together, the results show that the O. mykiss SERCA2 was not temperature dependent over the 10 to 25° C temperature interval commonly experienced by the animal in vivo. The Q(10) value of SERCA2 was significantly lower in O. mykiss than R. norvegicus which may be key for cardiac function over the wide environmental temperatures experienced in this eurythermal fish.
View details for DOI 10.1111/j.1095-8649.2011.03076.x
View details for Web of Science ID 000294598300014
View details for PubMedID 21884113
Pelagic marine predators face unprecedented challenges and uncertain futures. Overexploitation and climate variability impact the abundance and distribution of top predators in ocean ecosystems. Improved understanding of ecological patterns, evolutionary constraints and ecosystem function is critical for preventing extinctions, loss of biodiversity and disruption of ecosystem services. Recent advances in electronic tagging techniques have provided the capacity to observe the movements and long-distance migrations of animals in relation to ocean processes across a range of ecological scales. Tagging of Pacific Predators, a field programme of the Census of Marine Life, deployed 4,306 tags on 23 species in the North Pacific Ocean, resulting in a tracking data set of unprecedented scale and species diversity that covers 265,386 tracking days from 2000 to 2009. Here we report migration pathways, link ocean features to multispecies hotspots and illustrate niche partitioning within and among congener guilds. Our results indicate that the California Current large marine ecosystem and the North Pacific transition zone attract and retain a diverse assemblage of marine vertebrates. Within the California Current large marine ecosystem, several predator guilds seasonally undertake north-south migrations that may be driven by oceanic processes, species-specific thermal tolerances and shifts in prey distributions. We identify critical habitats across multinational boundaries and show that top predators exploit their environment in predictable ways, providing the foundation for spatial management of large marine ecosystems.
View details for DOI 10.1038/nature10082
View details for Web of Science ID 000292461300050
View details for PubMedID 21697831
Specialisations in excitation-contraction coupling may have played an important role in the evolution of endothermy and high cardiac performance in scombrid fishes. We examined aspects of Ca(2+) handling in cardiomyocytes from Pacific bonito (Sarda chiliensis), Pacific mackerel (Scomber japonicus), yellowfin tuna (Thunnus albacares) and Pacific bluefin tuna (Thunnus orientalis). The whole-cell voltage-clamp technique was used to measure the temperature sensitivity of the L-type Ca(2+) channel current (I(Ca)), density, and steady-state and maximal sarcoplasmic reticulum (SR) Ca(2+) content (ssSR(load) and maxSR(load)). Current-voltage relations, peak I(Ca) density and charge density of I(Ca) were greatest in mackerel and yellowfin at all temperatures tested. I(Ca) density and kinetics were temperature sensitive in all species studied, and the magnitude of this response was not related to the thermal preference of the species. SR(load) was greater in atrial than in ventricular myocytes in the Pacific bluefin tuna, and in species that are more cold tolerant (bluefin tuna and mackerel). I(Ca) and SR(load) were particularly small in bonito, suggesting the Na(+)/Ca(2+) exchanger plays a more pivotal role in Ca(2+) entry into cardiomyocytes of this species. Our comparative approach reveals that the SR of cold-tolerant scombrid fishes has a greater capacity for Ca(2+) storage. This specialisation may contribute to the temperature tolerance and thermal niche expansion of the bluefin tuna and mackerel.
View details for DOI 10.1242/jeb.048231
View details for Web of Science ID 000288155200011
View details for PubMedID 21389190
Tuna long distance migrations and exposure to wide range of ambient water temperatures facilitate infections with several parasitic groups. This is reflected in the remarkable diversity of tuna parasite communities, especially members of Didymozoidae superfamily (Poche, 1907) (Trematoda, Digenea). Didymocystis wedli is the most frequent species encountered in bluefin tuna parasitizing gill filaments, therefore suggested as a biological marker to differentiate between discrete tuna Atlantic stocks. Because of its high occurrence in gill tissue and inflammatory reaction as the consequence, the aim of our study was to asses if inflammatory madiation through expression of IL-1beta and TNF-alpha is present locally at the site of D. wedli encystment, as well as if the systematic expression of cytokines can be detected in different tissues of infected versus uninfected fish. Quantification of localized cytokine expression was done on paraffine embedded gill sections by in situ hybridization, while quantitative PCR was used to mesured cytokine transcripts in skin mucus, kidney, spleen, gills and liver. Our results suggest that tuna constitutive expression of IL-1beta and TNF-alpha in gills and skin implies a well-adapted innate immunity present at the barrier between the organism and environment. Upregulation of both cytokines in Didymocystis-infected gills not followed by a systematic response evidences the ongoing of an inflammatory process specific for the parasitation site. However, the lack of intensive cytokines response to D. wedli observed by molecular and histological data that fails to eliminate the parasite, could be related to the "old" age of the parasitic process.
View details for DOI 10.1016/j.fsi.2010.05.008
View details for Web of Science ID 000280513700014
View details for PubMedID 20580835
Specific dynamic action (SDA) is defined as the energy expended during ingestion, digestion, absorption and assimilation of a meal. This study presents the first data on the SDA response of individual tunas of any species. Juvenile Pacific bluefin tunas (Thunnus orientalis; body mass 9.7-11.0 kg; N=7) were individually fed known quantities of food consisting primarily of squid and sardine (meal energy range 1680-8749 kJ, approximately 4-13% of tuna body mass). Oxygen consumption rates (M(O2)) were measured in a swim tunnel respirometer during the postprandial period at a swimming speed of 1 body length (BL) s(-1) and a water temperature of 20 degrees C. was markedly elevated above routine levels in all fish following meal consumption [routine metabolic rate (RMR)=174+/-9 mg kg(-1) h(-1)]. The peak M(O2) during the SDA process ranged from 250 to 440 mg kg(-1) h(-1) (1.5-2.3 times RMR) and was linearly related to meal energy content. The duration of the postprandial increment in M(O2) ranged from 21 h to 33 h depending upon meal energy content. Consequently, the total energy used in SDA increased linearly with meal energy and ranged from 170 kJ to 688 kJ, such that the SDA process accounted for 9.2+/-0.7% of ingested energy across all experiments. These values suggest rapid and efficient food conversion in T. orientalis in comparison with most other fishes. Implanted archival temperature tags recorded the increment in visceral temperature (T(V)) in association with SDA. M(O2) returned to routine levels at the end of the digestive period 2-3 h earlier than T(V). The qualitative patterns in M(O2) and T(V) during digestion were similar, strengthening the possibility that archival measurements of T(V) can provide new insight into the energetics and habitat utilization of free-swimming bluefin in the natural environment. Despite efficient food conversion, SDA is likely to represent a significant component of the daily energy budget of wild bluefin tunas due to a regular and high ingestion of forage.
View details for DOI 10.1242/jeb.043455
View details for Web of Science ID 000279180700009
View details for PubMedID 20581267
Parasite communities of wild and reared bluefin tuna display remarkable diversity. Among these, the most prevalent and abundant are the Didymozoidae (Monticelli, 1888) (Trematoda, Digenea), considered one of the most taxonomically complex digenean families. The aim of this study was to evaluate phylogenetic structure of Didymozoidae occurring in Pacific (Thunnus orientalis) and Atlantic bluefin tuna (T. thynnus) in order to increase our knowledge of didymozoid zoogeography and identify species that could successfully be employed as biological tags for stock assessment studies. For the present analyses we used 2 nuclear ribosomal DNA loci, part of the 28S gene and the second internal transcribed spacer (ITS-2) as well as a portion of the mitochondrial cytochrome c oxidase subunit 1 gene (cox1). In most parasitic groups, morphology is the primary factor in the structuring of phylogenetic relationships. In rare examples, however, habitat has been suggested as a primary factor affecting parasite evolution. During their evolution, didymozoids have spread and inhabited a remarkable number of different sites in their hosts, colonizing exterior as well as strictly interior niches. Our data suggest that habitat selection has been the leading force in shaping didymozoid phylogenetic relationships. For 2 didymozoid species (D. wedli and D. palati), cox1 sequences indicate intraspecific differences between Mexican and Adriatic populations.
View details for DOI 10.1017/S0031182009991703
View details for Web of Science ID 000278673600012
View details for PubMedID 20028607
Advances in electronic tagging and genetic research are making it possible to discern population structure for pelagic marine predators once thought to be panmictic. However, reconciling migration patterns and gene flow to define the resolution of discrete population management units remains a major challenge, and a vital conservation priority for threatened species such as oceanic sharks. Many such species have been flagged for international protection, yet effective population assessments and management actions are hindered by lack of knowledge about the geographical extent and size of distinct populations. Combining satellite tagging, passive acoustic monitoring and genetics, we reveal how eastern Pacific white sharks (Carcharodon carcharias) adhere to a highly predictable migratory cycle. Individuals persistently return to the same network of coastal hotspots following distant oceanic migrations and comprise a population genetically distinct from previously identified phylogenetic clades. We hypothesize that this strong homing behaviour has maintained the separation of a northeastern Pacific population following a historical introduction from Australia/New Zealand migrants during the Late Pleistocene. Concordance between contemporary movement and genetic divergence based on mitochondrial DNA demonstrates a demographically independent management unit not previously recognized. This population's fidelity to discrete and predictable locations offers clear population assessment, monitoring and management options.
View details for DOI 10.1098/rspb.2009.1155
View details for Web of Science ID 000273882800004
View details for PubMedID 19889703
To sustain cardiac muscle contractility relatively independent of temperature, some fish species are capable of temporarily altering excitation-contraction coupling processes to meet the demands of their environment. The Pacific bluefin tuna, Thunnus orientalis, is a partially endothermic fish that inhabits a wide range of thermal niches. The present study examined the effects of temperature and thermal acclimation on sarcolemmal K(+) currents and their role in action potential (AP) generation in bluefin tuna cardiomyocytes. Atrial and ventricular myocytes were enzymatically isolated from cold (14 degrees C)- and warm (24 degrees C)-acclimated bluefin tuna. APs and current-voltage relations of K(+) channels were measured using the whole cell current and voltage clamp techniques, respectively. Data were collected either at the cardiomyocytes' respective acclimation temperature of 14 or 24 degrees C or at a common test temperature of 19 degrees C (to reveal the effects of acclimation). AP duration (APD) was prolonged in cold-acclimated (CA) cardiomyocytes tested at 14 degrees C compared with 19 degrees C and in warm-acclimated (WA) cardiomyocytes tested at 19 degrees C compared with 24 degrees C. This effect was mirrored by a decrease in the density of the delayed-rectifier current (I(Kr)), whereas the density of the background inward-rectifier current (I(K1)) was unchanged. When CA and WA cardiomyocytes were tested at a common temperature of 19 degrees C, no significant effects of temperature acclimation on AP shape or duration were observed, whereas I(Kr) density was markedly increased in CA cardiomyocytes. I(K1) density was unaffected in CA ventricular myocytes but was significantly reduced in CA atrial myocytes, resulting in a depolarization of atrial resting membrane potential. Our results indicate the bluefin AP is relatively short compared with other teleosts, which may allow the bluefin heart to function at cold temperatures without the necessity for thermal compensation of APD.
View details for DOI 10.1152/ajpregu.90810.2008
View details for Web of Science ID 000268187100031
View details for PubMedID 19515982
Electronic tags were used to examine the seasonal movements, aggregations and diving behaviors of Atlantic bluefin tuna (Thunnus thynnus) to better understand their migration ecology and oceanic habitat utilization. Implantable archival tags (n = 561) were deployed in bluefin tuna from 1996 to 2005 and 106 tags were recovered. Movement paths of the fish were reconstructed using light level and sea-surface-temperature-based geolocation estimates. To quantify habitat utilization we employed a weighted kernel estimation technique that removed the biases of deployment location and track length. Throughout the North Atlantic, high residence times (167+/-33 days) were identified in four spatially confined regions on a seasonal scale. Within each region, bluefin tuna experienced distinct temperature regimes and displayed different diving behaviors. The mean diving depths within the high-use areas were significantly shallower and the dive frequency and the variance in internal temperature significantly higher than during transit movements between the high-use areas. Residence time in the more northern latitude high-use areas was significantly correlated with levels of primary productivity. The regions of aggregation are associated with areas of abundant prey and potentially represent critical foraging habitats that have seasonally abundant prey. Throughout the North Atlantic mean diving depth was significantly correlated with the depth of the thermocline, and dive behavior changed in relation to the stratification of the water column. In this study, with numerous multi-year tracks, there appear to be repeatable patterns of clear aggregation areas that potentially are changing with environmental conditions. The high concentrations of bluefin tuna in predictable locations indicate that Atlantic bluefin tuna are vulnerable to concentrated fishing efforts in the regions of foraging aggregations.
View details for DOI 10.1371/journal.pone.0006151
View details for Web of Science ID 000267806400007
View details for PubMedID 19582150
The temperature stress that pelagic fishes experience can induce physiological and behavioural changes that leave a signature in gene expression profiles. We used a functional genomics approach to identify genes that were up- or down-regulated following thermal stress in the Pacific bluefin tuna. Following the acclimation period, 113, 81 and 196 genes were found to be differentially expressed between the control (20 degrees C) and cold (15 degrees) treatment groups, in ventricle, red muscle and white muscle, respectively. The genes whose expression levels were responsive to thermal acclimation varied according to muscle fibre type, perhaps reflecting the tissue-specific degrees of endothermy characteristic of this species.
View details for DOI 10.1111/j.1365-294X.2009.04174.x
View details for Web of Science ID 000265774300005
View details for PubMedID 19389180
Effective transboundary conservation of highly migratory marine animals requires international management cooperation as well as clear scientific information about habitat use by these species. Populations of leatherback turtles (Dermochelys coriacea) in the eastern Pacific have declined by >90% during the past two decades, primarily due to unsustainable egg harvest and fisheries bycatch mortality. While research and conservation efforts on nesting beaches are ongoing, relatively little is known about this population of leatherbacks' oceanic habitat use and migration pathways. We present the largest multi-year (2004-2005, 2005-2006, and 2007) satellite tracking dataset (12,095 cumulative satellite tracking days) collected for leatherback turtles. Forty-six females were electronically tagged during three field seasons at Playa Grande, Costa Rica, the largest extant nesting colony in the eastern Pacific. After completing nesting, the turtles headed southward, traversing the dynamic equatorial currents with rapid, directed movements. In contrast to the highly varied dispersal patterns seen in many other sea turtle populations, leatherbacks from Playa Grande traveled within a persistent migration corridor from Costa Rica, past the equator, and into the South Pacific Gyre, a vast, low-energy, low-productivity region. We describe the predictable effects of ocean currents on a leatherback migration corridor and characterize long-distance movements by the turtles in the eastern South Pacific. These data from high seas habitats will also elucidate potential areas for mitigating fisheries bycatch interactions. These findings directly inform existing multinational conservation frameworks and provide immediate regions in the migration corridor where conservation can be implemented. We identify high seas locations for focusing future conservation efforts within the leatherback dispersal zone in the South Pacific Gyre.
View details for DOI 10.1371/journal.pbio.0060171
View details for Web of Science ID 000257971100013
View details for PubMedID 18630987
Pacific bluefin tuna inhabit a wide range of thermal environments across the Pacific ocean. To examine how metabolism varies across this thermal range, we studied the effect of ambient water temperature on metabolic rate of juvenile Pacific bluefin tuna, Thunnus thynnus, swimming in a swim tunnel. Rate of oxygen consumption (MO2) was measured at ambient temperatures of 8-25 degrees C and swimming speeds of 0.75-1.75 body lengths (BL) s(-1). Pacific bluefin swimming at 1 BL s(-1) per second exhibited a U-shaped curve of metabolic rate vs ambient temperature, with a thermal minimum zone between 15 degrees C to 20 degrees C. Minimum MO2 of 175+/-29 mg kg(-1) h(-1) was recorded at 15 degrees C, while both cold and warm temperatures resulted in increased metabolic rates of 331+/-62 mg kg(-1) h(-1) at 8 degrees C and 256+/-19 mg kg(-1) h(-1) at 25 degrees C. Tailbeat frequencies were negatively correlated with ambient temperature. Additional experiments indicated that the increase in MO2 at low temperature occurred only at low swimming speeds. Ambient water temperature data from electronic tags implanted in wild fish indicate that Pacific bluefin of similar size to the experimental fish used in the swim tunnel spend most of their time in ambient temperatures in the metabolic thermal minimum zone.
View details for DOI 10.1242/jeb.005835
View details for Web of Science ID 000251108300025
View details for PubMedID 18025023
Tunas have an extraordinary physiology including elevated metabolic rates and high cardiac performance. In some species, retention of metabolic heat warms the slow oxidative swimming muscles and visceral tissues. In all tunas, the heart functions at ambient temperature. Enhanced rates of calcium transport in tuna myocytes are associated with increased expression of proteins involved in the contraction-relaxation cycle. The cardiac SR Ca2+-ATPase (SERCA2) plays a major role during cardiac excitation-contraction (E-C) coupling. Measurements of oxalate-supported Ca2+-uptake in atrial SR vesicles isolated from four species of tunas indicate that bluefin have at least two fold higher Ca2+-uptake than all other tunas examined between 5 and 30 degrees C. The highest atrial Ca2+-uptake was measured in bluefin tuna at 30 degrees C (23.32+/-1.58 nmol Ca2+/mg/min). Differences among tunas in the temperature dependency of Ca2+-uptake were similar for ATP hydrolysis. Western blot analysis revealed a significant increase in SERCA2 content associated with higher Ca2+ uptake rates in the atrial tissues of bluefin tuna and similar RyR expression across species. We propose that the expression of EC coupling proteins in cardiac myocytes, and the higher rates of SERCA2 activity are an important evolutionary step for the maintenance of higher heart rates and endothermy in bluefin tuna.
View details for DOI 10.1016/j.cbpa.2007.03.033
View details for Web of Science ID 000249103900014
View details for PubMedID 17566775
Bluefin tuna are endothermic and have higher temperatures, heart rates, and cardiac outputs than tropical tuna. We hypothesized that the increased cardiovascular capacity to deliver oxygen in bluefin may be associated with the evolution of higher metabolic rates. This study measured the oxygen consumption of juvenile Pacific bluefin Thunnus orientalis and yellowfin tuna Thunnus albacares swimming in a swim-tunnel respirometer at 20 degrees C. Oxygen consumption (Mo2) of bluefin (7.1-9.4 kg) ranged from 235+/-38 mg kg(-1) h(-1) at 0.85 body length (BL) s(-1) to 498+/-55 mg kg(-1) h(-1) at 1.80 BL s(-1). Minimal metabolic rates of swimming bluefin were 222+/-24 mg O(2) kg(-1) h(-1) at speeds of 0.75 to 1.0 BL s(-1). Mo2 of T. albacares (3.7-7.4 kg) ranged from 164+/-18 mg kg(-1) h(-1) at 0.65 BL s(-1) to 405+/-105 mg kg(-1) h(-1) at 1.8 BL s(-1). Bluefin tuna had higher metabolic rates than yellowfin tuna at all swimming speeds tested. At a given speed, bluefin had higher metabolic rates and swam with higher tailbeat frequencies and shorter stride lengths than yellowfin. The higher M dot o2 recorded in Pacific bluefin tuna is consistent with the elevated cardiac performance and enhanced capacity for excitation-contraction coupling in cardiac myocytes of these fish. These physiological traits may underlie thermal-niche expansion of bluefin tuna relative to tropical tuna species.
View details for Web of Science ID 000243966400001
View details for PubMedID 17252513
Shark populations are declining globally, yet the movements and habitats of most species are unknown. We used a satellite tag attached to the dorsal fin to track salmon sharks (Lamna ditropis) for up to 3.2 years. Here we show that salmon sharks have a subarctic-to-subtropical niche, ranging from 2 degrees to 24 degrees C, and they spend winter periods in waters as cold as 2 degrees to 8 degrees C. Functional assays and protein gels reveal that the expression of excitation-contraction coupling proteins is enhanced in salmon shark hearts, which may underlie the shark's ability to maintain heart function at cold temperatures and their niche expansion into subarctic seas.
View details for DOI 10.1126/science.1114616
View details for Web of Science ID 000232477000047
View details for PubMedID 16210538
Electronic tags that archive or transmit stored data to satellites have advanced the mapping of habitats used by highly migratory fish in pelagic ecosystems. Here we report on the electronic tagging of 772 Atlantic bluefin tuna in the western Atlantic Ocean in an effort to identify population structure. Reporting electronic tags provided accurate location data that show the extensive migrations of individual fish (n = 330). Geoposition data delineate two populations, one using spawning grounds in the Gulf of Mexico and another from the Mediterranean Sea. Transatlantic movements of western-tagged bluefin tuna reveal site fidelity to known spawning areas in the Mediterranean Sea. Bluefin tuna that occupy western spawning grounds move to central and eastern Atlantic foraging grounds. Our results are consistent with two populations of bluefin tuna with distinct spawning areas that overlap on North Atlantic foraging grounds. Electronic tagging locations, when combined with US pelagic longline observer and logbook catch data, identify hot spots for spawning bluefin tuna in the northern slope waters of the Gulf of Mexico. Restrictions on the time and area where longlining occurs would reduce incidental catch mortalities on western spawning grounds.
View details for DOI 10.1038/nature03463
View details for Web of Science ID 000228693300041
View details for PubMedID 15858572
Tunas are capable of exceptionally high maximum metabolic rates; such capability requires rapid delivery of oxygen and metabolic substrate to the tissues. This requirement is met, in part, by exceptionally high maximum cardiac outputs, opening the possibility that myocardial Ca(2+) delivery is enhanced in myocytes from tuna compared with those from other fish. In this study, we investigated the electrophysiological properties of the cardiac L-type Ca(2+) channel current (I(Ca)) to test the hypothesis that Ca(2+) influx would be large and have faster kinetics in cardiomyocytes from Pacific bluefin tuna (Thunnus orientalis) than in those from its sister taxon, the Pacific mackerel (Scombe japonicus). In accordance with this hypothesis, I(Ca) in atrial myocytes from bluefin tuna had significantly greater peak current amplitudes and faster fast inactivation kinetics (-4.4 +/- 0.2 pA/pF and 25.9 +/- 1.6 ms, respectively) than those from mackerel (-2.7 +/- 0.5 pA/pF and 32.3 +/- 3.8 ms, respectively). Steady-state activation, inactivation, and recovery from inactivation were also faster in atrial myocytes from tuna than from mackerel. In ventricular myocytes, current amplitude and activation and inactivation rates were similar in both species but elevated compared with those of other teleosts. These results indicate enhanced I(Ca) in atrial myocytes from bluefin tuna compared with Pacific mackerel; this enhanced I(Ca) may be associated with elevated cardiac performance, because I(Ca) delivers the majority of Ca(2+) involved in excitation-contraction coupling in most fish hearts. Similarly, I(Ca) is enhanced in the ventricle of both species compared with other teleosts and may play a role in the robust cardiac performance of fishes of the family Scombridae.
View details for DOI 10.1152/ajpregu.00521.2003
View details for Web of Science ID 000220054100008
View details for PubMedID 14656768
This study reports the cardiovascular physiology of the Pacific bluefin tuna (Thunnus orientalis) in an in situ heart preparation. The performance of the Pacific bluefin tuna heart was examined at temperatures from 30 degrees C down to 2 degrees C. Heart rates ranged from 156 beats min(-1) at 30 degrees C to 13 beats min(-1) at 2 degrees C. Maximal stroke volumes were 1.1 ml x kg(-1) at 25 degrees C and 1.3 ml x kg(-1) at 2 degrees C. Maximal cardiac outputs were 18.1 ml x kg(-1) min(-1) at 2 degrees C and 106 ml x kg(-1) min(-1) at 25 degrees C. These data indicate that cardiovascular function in the Pacific bluefin tuna exhibits a strong temperature dependence, but cardiac function is retained at temperatures colder than those tolerated by tropical tunas. The Pacific bluefin tuna's cardiac performance in the cold may be a key adaptation supporting the broad thermal niche of the bluefin tuna group in the wild. In situ data from Pacific bluefin are compared to in situ measurements of cardiac performance in yellowfin tuna and preliminary results from albacore tuna.
View details for DOI 10.1242/jeb.00820
View details for Web of Science ID 000189349800023
View details for PubMedID 14747418
Recent physiological studies on the cardiovascular performance of tunas suggest that the elevated heart rates of these fish may rely on increased use of intracellular sarcoplasmic reticulum (SR) Ca2+ stores. In this study, we compare the cellular cardiac performance in endothermic tunas (bluefin, albacore, yellowfin) and their ectothermic sister taxa (mackerel) in response to acute temperature change. The cardiac sarco/endoplasmic reticulum Ca2+-ATPase (SERCA2) plays a major role during cardiac excitation-contraction (E-C) coupling, transporting Ca2+ from the cytosol into the lumen of the SR and thus promoting the relaxation of the muscle. Measurements of oxalate-supported Ca2+ uptake in SR-enriched ventricular vesicles indicated that tunas were capable of sustaining a rate of Ca2+ uptake that was significantly higher than the mackerel. Among tunas, the cold-tolerant bluefin had the highest rates of SR Ca2+ uptake and ATPase activity. The differences among Ca2+ uptake and ATP hydrolysis rates do not seem to result from intrinsic differences between the SERCA2 present in the different tunas, as shown by their similar temperature sensitivities and similar values for activation energy. Western blots reveal that increased SERCA2 protein content is associated with the higher Ca2+ uptake and ATPase activities seen in bluefin ventricles compared with albacore, yellowfin, and mackerel. We hypothesize that a key step in the evolution of high heart rate and high metabolic rate in tunas is increased activity of the SERCA2 enzyme. We also suggest that high levels of SERCA2 in bluefin tuna hearts may be important for retaining cardiac function at cold temperatures.
View details for DOI 10.1152/ajpregu.00392.2003
View details for Web of Science ID 000187791500022
View details for PubMedID 14604842
A thermogenic organ is found beneath the brain of billfishes (Istiophoridae), swordfish (Xiphiidae) and the butterfly mackerel (Scombridae). The heater organ has been shown to warm the brain and eyes up to 14 degrees C above ambient water temperature. Heater cells are derived from extraocular muscle fibers and express a modified muscle phenotype with an extensive transverse-tubule (T-tubule) network and sarcoplasmic reticulum (SR) enriched in Ca(2+)-ATPase (SERCA) pumps and ryanodine receptors (RyRs). Heater cells have a high mitochondria content but have lost most of the contractile myofilaments. Thermogenesis has been hypothesized to be associated with release and reuptake of Ca(2+). In this study, Ca(2+) fluxes in heater SR vesicles derived from blue marlin (Makaira nigricans) were measured using fura-2 fluorescence. Upon the addition of MgATP, heater SR vesicles rapidly sequestered Ca(2+). Uptake of Ca(2+) was thapsigargin sensitive, and maximum loading ranged between 0.8 micro mol Ca(2+) mg(-1) protein and 1.0 micro mol Ca(2+) mg(-1) protein. Upon the addition of 10 mmol l(-1) caffeine or 350 micro mol l(-1) ryanodine, heater SR vesicles released only a small fraction of the loaded Ca(2+). However, ryanodine could elicit a much larger Ca(2+) release event when the activity of the SERCA pumps was reduced. RNase protection assays revealed that heater tissue expresses an RyR isoform that is also expressed in fish slow-twitch skeletal muscle but is distinct from the RyR expressed in fish fast-twitch skeletal muscle. The heater and slow-twitch muscle RyR isoform has unique physiological properties. In the presence of adenine nucleotides, this RyR remains open even though cytoplasmic Ca(2+) is elevated, a condition that normally closes RyRs. The fast Ca(2+) sequestration by the heater SR, coupled with a physiologically unique RyR, is hypothesized to promote Ca(2+) cycling, ATP turnover and heat generation. A branch of the oculomotor nerve innervates heater organs, and, in this paper, we demonstrate that heater cells contain large 'endplate-like' clusters of acetylcholine receptors that appear to provide a mechanism for nervous control of thermogenesis.
View details for DOI 10.1242/jeb.00158
View details for Web of Science ID 000181522300002
View details for PubMedID 12547935
Tuna are endothermic fish with high metabolic rates, cardiac outputs and aerobic capacities. While tuna warm their skeletal muscle, viscera, brain and eyes, their hearts remain near ambient temperature, raising the possibility that cardiac performance may limit their thermal niches. We used an in situ perfused heart preparation to investigate the effects of acute temperature change and the effects of epinephrine and extracellular Ca(2+) on cardiac function in yellowfin tuna (Thunnus albacares). Heart rate showed a strong temperature-dependence, ranging from 20 beats min(-1) at 10 degrees C to 109 beats min(-1) at 25 degrees C. Maximal stroke volume showed an inverse temperature-dependence, ranging from 1.4 ml kg(-1) at 15 degrees C to 0.9 ml kg(-1) at 25 degrees C. Maximal cardiac outputs were 27 ml kg(-1) min(-1) at 10 degrees C and 98 ml kg(-1) min(-1) at 25 degrees C. There were no significant effects of perfusate epinephrine concentrations between 1 and 100 nmol l(-1) at 20 degrees C. Increasing extracellular Ca(2+) concentration from 1.84 to 7.36 mmol l(-1) at 20 degrees C produced significant increases in maximal stroke volume, cardiac output and myocardial power output. These data demonstrate that changes in heart rate and stroke volume are involved in maintaining cardiac output during temperature changes in tuna and support the hypothesis that cardiac performance may limit the thermal niches of yellowfin tuna.
View details for Web of Science ID 000176960600006
View details for PubMedID 12077164
Until the advent of electronic tagging technology, the inherent difficulty of studying swift and powerful marine animals made ecological information about sharks of the family Lamnidae difficult to obtain. Here we report the tracking of movements of white sharks by using pop-up satellite archival tags, which reveal that their migratory movements, depth and ambient thermal ranges are wider than was previously thought.
View details for PubMedID 11780105
The deployment of electronic data storage tags that are surgically implanted or satellite-linked provides marine researchers with new ways to examine the movements, environmental preferences, and physiology of pelagic vertebrates. We report the results obtained from tagging of Atlantic bluefin tuna with implantable archival and pop-up satellite archival tags. The electronic tagging data provide insights into the seasonal movements and environmental preferences of this species. Bluefin tuna dive to depths of >1000 meters and maintain a warm body temperature. Western-tagged bluefin tuna make trans-Atlantic migrations and they frequent spawning grounds in the Gulf of Mexico and eastern Mediterranean. These data are critical for the future management and conservation of bluefin tuna in the Atlantic.
View details for Web of Science ID 000170492600038
View details for PubMedID 11509729
Myoglobin (Mb) buffers intracellular O2 and facilitates diffusion of O2 through the cell. These functions of Mb will be most effective when intracellular PO2 is near the partial pressure of oxygen at which Mb is half saturated (P50) of the molecule. We test the hypothesis that Mb oxygen affinity has evolved such that it is conserved when adjusted for body temperature among closely related animals. We measure oxygen P50s tonometrically and oxygen dissociation rate constants with stopped flow and generate amino acid sequence from cDNA of Mbs from fish with different body temperatures. P50s for the endothermic bluefin tuna, skipjack tuna, and blue marlin at 20 degrees C were 0.62 +/- 0.02, 0.59 +/- 0.01, 0.58 +/- 0.04 mmHg, respectively, and were significantly lower than those for ectothermic bonito (1.03 +/- 0.07 mmHg) and mackerel (1.39 +/- 0.03 mmHg). Because the oxygen affinity of Mb decreases with increasing temperature, the above differences in oxygen affinity between endothermic and ectothermic fish are reduced when adjusted for the in vivo muscle temperature of the animal. Oxygen dissociation rate constants at 20 degrees C for the endothermic species ranged from 34.1 to 49.3 s(-1), whereas those for mackerel and bonito were 102 and 62 s(-1), respectively. Correlated with the low oxygen affinity and fast dissociation kinetics of mackerel Mb is a substitution of alanine for proline that would likely result in a more flexible mackerel protein.
View details for Web of Science ID 000167445600026
View details for PubMedID 11247835
Two distinct skeletal muscle ryanodine receptors (RyR1s) are expressed in a fiber type-specific manner in fish skeletal muscle (11). In this study, we compare [(3)H]ryanodine binding and single channel activity of RyR1-slow from fish slow-twitch skeletal muscle with RyR1-fast and RyR3 isolated from fast-twitch skeletal muscle. Scatchard plots indicate that RyR1-slow has a lower affinity for [(3)H]ryanodine when compared with RyR1-fast. In single channel recordings, RyR1-slow and RyR1-fast had similar slope conductances. However, the maximum open probability (P(o)) of RyR1-slow was threefold less than the maximum P(o) of RyR1-fast. Single channel studies also revealed the presence of two populations of RyRs in tuna fast-twitch muscle (RyR1-fast and RyR3). RyR3 had the highest P(o) of all the RyR channels and displayed less inhibition at millimolar Ca(2+). The addition of 5 mM Mg-ATP or 2.5 mM beta, gamma-methyleneadenosine 5'-triphosphate (AMP-PCP) to the channels increased the P(o) and [(3)H]ryanodine binding of both RyR1s but also caused a shift in the Ca(2+) dependency curve of RyR1-slow such that Ca(2+)-dependent inactivation was attenuated. [(3)H]ryanodine binding data also showed that Mg(2+)-dependent inhibition of RyR1-slow was reduced in the presence of AMP-PCP. These results indicate differences in the physiological properties of RyRs in fish slow- and fast-twitch skeletal muscle, which may contribute to differences in the way intracellular Ca(2+) is regulated in these muscle types.
View details for Web of Science ID 000090003700045
View details for PubMedID 11049875
We used an isometric muscle preparation to test the hypothesis that yellowfin tuna Thunnus albacares utilize the intracellular Ca2+ storage sites of the sarcoplasmic reticulum (SR) during routine contractions. Ryanodine (a blocker of SR Ca2+ release) reduced the force of contraction by approximately 50 % and the rates of contraction and relaxation by 60 % in yellowfin tuna atrium. High levels of adrenaline were unable to ameliorate the effects of ryanodine. We conclude that the SR is active in contributing Ca2+ to force development at physiological contraction frequencies. Further, we suggest that, by using intracellular Ca2+ cycling, the yellowfin tuna is able to increase the maximum contraction frequency of its cardiac muscle beyond that of most other fishes.
View details for PubMedID 10069977
We report the development of an acoustic telemetry tag used to monitor electromyograms (EMGs) remotely from free-swimming marine fish. The device described amplifies and filters the EMG and then converts the electrical waveform into a frequency-modulated acoustic signal that is transmitted through water. The signal is then received, demodulated and recorded by the receiving system. The EMG tag described has been tested on a range of species, including toadfish Opsanus &tgr;, spiny dogfish Squalus acanthias, yellowfin tuna Thunnus albacares and eastern Pacific bonito Sarda chiliensis, in different tank environments. In certain tanks the fidelity with which the system replicates the EMG is sufficient to quantify accurately the onset, offset, duration, the integrated area under the absolute value of the signal and the number of signal zero crossings. This EMG tag will expand the scope of questions that can be addressed about the behavior and physiology of free-swimming fish.
View details for PubMedID 10482728
The movements of Atlantic bluefin tuna (Thunnus thynnus thynnus) have captured the interest of scientists and fishers since the time of Aristotle. This tuna is unique among bony fish for maintaining elevated body temperatures (21 degrees C above ambient) and attaining large size (up to 750 kg). We describe here the use of a pop-off satellite tag, for investigating the Atlantic-wide movements and potential stock overlap of western and eastern Atlantic bluefin tuna. The tag also archives data on water temperatures. The objectives of this study were to evaluate the effectiveness of the technology, study the movements of Atlantic bluefin tuna, examine their thermal niche, and assess survivorship of tagged fish. The pop-off satellite technology provides data independent of commercial fisheries that, when deployed in sufficient quantity, should permit a critical test of the stock structure hypotheses for Atlantic bluefin tuna.
View details for Web of Science ID 000075246600059
View details for PubMedID 9689089
We have cloned a group of cDNAs that encodes the skeletal ryanodine receptor isoform (RyR1) of fish from a blue marlin extraocular muscle library. The cDNAs encode a protein of 5,081 amino acids with a calculated molecular mass of 576,302 Da. The deduced amino acid sequence shows strong sequence identity to previously characterized RyR1 isoforms. An RNA probe derived from a clone of the full-length marlin RyR1 isoform hybridizes to RNA preparations from extraocular muscle and slow-twitch skeletal muscle but not to RNA preparations from fast-twitch skeletal or cardiac muscle. We have also isolated a partial RyR clone from marlin and toadfish fast-twitch muscles that shares 80% sequence identity with the corresponding region of the full-length RyR1 isoform, and a RNA probe derived from this clone hybridizes to RNA preparations from fast-twitch muscle but not to slow-twitch muscle preparations. Western blot analysis of slow-twitch muscles in fish indicates the presence of only a single high-molecular-mass RyR protein corresponding to RyR1. [3H]ryanodine binding assays revealed the fish slow-twitch muscle RyR1 had a greater sensitivity for Ca2+ than the fast-twitch muscle RyR1. The results indicate that, in fish muscle, fiber type-specific RyR1 isoforms are expressed and the two proteins are physiologically distinct.
View details for Web of Science ID 000075174400009
View details for PubMedID 9688594
Top pelagic predators such as tunas, sharks, marine turtles and mammals have historically been difficult to study due to their large body size and vast range over the oceanic habitat. In recent years the development of small microprocessor-based data storage tags that are surgically implanted or satellite-linked provide marine researchers a novel avenue for examining the movements, physiology and behaviors of pelagic animals in the wild. When biological and physical data obtained from the tags are combined with satellite derived sea surface temperature and ocean color data, the relationships between the movements, behaviors and physical ocean environment can be examined. Tag-bearing marine animals can function as autonomous ocean profilers providing oceanographic data wherever their long migrations take them. The biologging science is providing ecological physiologists with new insights into the seasonal movements, habitat utilization, breeding behaviors and population structures in of marine vertebrates. In addition, the data are revealing migration corridors, hot spots and physical oceanographic patterns that are key to understanding how organisms such as bluefin tunas use the open ocean environment. In the 21st century as ecosystem degradation and global warming continue to threaten the existence of species on Earth, the field of physiological ecology will play a more pivotal role in conservation biology.
View details for Web of Science ID 000229163400011
View details for PubMedID 21676774