Honors & Awards
Rolex Award for Enterprise, Rolex (2012)
Walter B. Cannon Award, American Physiological Society (2008)
Pew Marine Conservation Fellow, Pew Foundation (1997)
MacArthur Fellow, MacArthur Foundation (1996)
Presidents Medal, Society for Experimental Biology, London (1994)
Presidential Young Investigator Award, National Science Foundation (1989)
B.A., University of Vermont, Zoology (1980)
Ph.D, Duke University, Zoology (1986)
Current Research and Scholarly Interests
Thermal physiology, open ocean predators, ecological physiology and tuna biology
- Comparative Animal Physiology
BIOHOPK 162H, BIOHOPK 262H (Win)
BIOHOPK 84 (Spr)
Independent Studies (16)
- Advanced Research Laboratory in Experimental Biology
BIO 199 (Aut, Win, Spr, Sum)
- Directed Individual Study in Earth Systems
EARTHSYS 297 (Aut, Win, Spr, Sum)
- Directed Instruction or Reading
BIOHOPK 198H (Aut, Win, Spr, Sum)
- Directed Reading in Biology
BIO 198 (Aut, Win, Spr, Sum)
- Directed Reading in Environment and Resources
ENVRES 398 (Aut, Win, Spr, Sum)
- Directed Research
EARTHSYS 250 (Aut, Win, Spr, Sum)
- Directed Research in Environment and Resources
ENVRES 399 (Aut, Win, Spr, Sum)
- Graduate Research
BIO 300 (Aut, Win, Spr, Sum)
- Honors Program in Earth Systems
EARTHSYS 199 (Aut, Win, Spr, Sum)
- Out-of-Department Advanced Research Laboratory in Experimental Biology
BIO 199X (Sum)
- Out-of-Department Directed Reading
BIO 198X (Aut, Win, Spr, Sum)
- Out-of-Department Graduate Research
BIO 300X (Win, Spr, Sum)
BIOHOPK 300H (Aut, Win, Spr, Sum)
- Teaching of Biological Science
BIOHOPK 290H (Win, Spr, Sum)
- Teaching of Biology
BIO 290 (Aut, Win, Spr)
- Undergraduate Research
BIOHOPK 199H (Aut, Win, Spr, Sum)
- Advanced Research Laboratory in Experimental Biology
- Prior Year Courses
Biomonitoring of marine vertebrates in Monterey Bay using eDNA metabarcoding
2017; 12 (4)
Molecular analysis of environmental DNA (eDNA) can be used to assess vertebrate biodiversity in aquatic systems, but limited work has applied eDNA technologies to marine waters. Further, there is limited understanding of the spatial distribution of vertebrate eDNA in marine waters. Here, we use an eDNA metabarcoding approach to target and amplify a hypervariable region of the mitochondrial 12S rRNA gene to characterize vertebrate communities at 10 oceanographic stations spanning 45 km within the Monterey Bay National Marine Sanctuary (MBNMS). In this study, we collected three biological replicates of small volume water samples (1 L) at 2 depths at each of the 10 stations. We amplified fish mitochondrial DNA using a universal primer set. We obtained 5,644,299 high quality Illumina sequence reads from the environmental samples. The sequence reads were annotated to the lowest taxonomic assignment using a bioinformatics pipeline. The eDNA survey identified, to the lowest taxonomic rank, 7 families, 3 subfamilies, 10 genera, and 72 species of vertebrates at the study sites. These 92 distinct taxa come from 33 unique marine vertebrate families. We observed significantly different vertebrate community composition between sampling depths (0 m and 20/40 m deep) across all stations and significantly different communities at stations located on the continental shelf (<200 m bottom depth) versus in the deeper waters of the canyons of Monterey Bay (>200 m bottom depth). All but 1 family identified using eDNA metabarcoding is known to occur in MBNMS. The study informs the implementation of eDNA metabarcoding for vertebrate biomonitoring.
View details for DOI 10.1371/journal.pone.0176343
View details for Web of Science ID 000400308800048
View details for PubMedID 28441466
- Assessing the effectiveness of a large marine protected area for reef shark conservation BIOLOGICAL CONSERVATION 2017; 207: 64-71
- Bioenergetics of captive yellowfin tuna (Thunnus albacares) AQUACULTURE 2017; 468: 71-79
A Novel Cardiotoxic Mechanism for a Pervasive Global Pollutant
The Deepwater Horizon disaster drew global attention to the toxicity of crude oil and the potential for adverse health effects amongst marine life and spill responders in the northern Gulf of Mexico. The blowout released complex mixtures of polycyclic aromatic hydrocarbons (PAHs) into critical pelagic spawning habitats for tunas, billfishes, and other ecologically important top predators. Crude oil disrupts cardiac function and has been associated with heart malformations in developing fish. However, the precise identity of cardiotoxic PAHs, and the mechanisms underlying contractile dysfunction are not known. Here we show that phenanthrene, a PAH with a benzene 3-ring structure, is the key moiety disrupting the physiology of heart muscle cells. Phenanthrene is a ubiquitous pollutant in water and air, and the cellular targets for this compound are highly conserved across vertebrates. Our findings therefore suggest that phenanthrene may be a major worldwide cause of vertebrate cardiac dysfunction.
View details for DOI 10.1038/srep41476
View details for Web of Science ID 000392958700001
View details for PubMedID 28139666
View details for PubMedCentralID PMC5282528
- Influence of temperature and oxygen on the distribution of blue marlin (Makaira nigricans) in the Central Pacific FISHERIES OCEANOGRAPHY 2017; 26 (1): 34-48
A novel application of multi-event modeling to estimate class segregation in a highly migratory oceanic vertebrate
2016; 97 (12): 3494-3502
Spatial segregation of animals by class (i.e., maturity or sex) within a population due to differential rates of temporary emigration (TE) from study sites can be an important life history feature to consider in population assessment and management. However, such rates are poorly known; new quantitative approaches to address these knowledge gaps are needed. We present a novel application of multi-event models that takes advantage of two sources of detections to differentiate temporary emigration from apparent absence to quantify class segregation within a study population of double-marked (photo-identified and tagged with coded acoustic transmitters) white sharks (Carcharodon carcharias) in central California. We use this model to test if sex-specific patterns in TE result in disparate apparent capture probabilities (p(o) ) between male and female white sharks, which can affect the observed sex ratio. The best-supported model showed a contrasting pattern of Pr(TE) from coastal aggregation sites between sexes (for males Pr[TE] = 0.015 [95% CI = 0.00, 0.31] and Pr[TE]= 0.57 [0.40, 0.72] for females), but not maturity classes. Additionally, by accounting for Pr(TE) and imperfect detection, we were able to estimate class-specific values of true capture probability (p(*) ) for tagged and untagged sharks. The best-supported model identified differences between maturity classes but no difference between sexes or tagging impacts (tagged mature sharks p(* ) = 0.55 (0.46-0.63) and sub-adult sharks p*( ) = 0.36 (0.25, 0.50); and untagged mature sharks p(* ) = 0.50 (0.39-0.61) and sub-adults p(* ) = 0.18 (0.10, 0.31). Estimated sex-based differences in p(o) were linked to sex-specific differences in Pr(TE) but not in p(*) ; once the Pr(TE) is accounted for, the p(*) between sexes was not different. These results indicate that the observed sex ratio is not a consequence of unequal detectability and sex-specific values of Pr(TE) are important drivers of the observed male-dominated sex ratio. Our modeling approach reveals complex class-specific patterns in Pr(TE) and p(*) in a mark-recapture data set, and highlights challenges for the population modeling and conservation of white sharks in central California. The model we develop here can be used to estimate rates of temporary emigration and class segregation when two detection methods are used.
View details for DOI 10.1002/ecy.1589
View details for Web of Science ID 000389444800026
View details for PubMedID 27912002
Quantification of Environmental DNA (eDNA) Shedding and Decay Rates for Three Marine Fish
ENVIRONMENTAL SCIENCE & TECHNOLOGY
2016; 50 (19): 10456-10464
Analysis of environmental DNA (eDNA) to identify macroorganisms and biodiversity has the potential to significantly augment spatial and temporal biological monitoring in aquatic ecosystems. Current monitoring methods relying on the physical identification of organisms can be time consuming, expensive, and invasive. Measuring eDNA shed from organisms provides detailed information on the presence and abundance of communities of organisms. However, little is known about eDNA shedding and decay in aquatic environments. In the present study, we designed novel Taqman qPCR assays for three ecologically and economically important marine fish-Engraulis mordax (Northern Anchovy), Sardinops sagax (Pacific Sardine), and Scomber japonicas (Pacific Chub Mackerel). We subsequently measured fish eDNA shedding and decay rates in seawater mesocosms. eDNA shedding rates ranged from 165 to 3368 pg of DNA per hour per gram of biomass. First-order decay rate constants ranged from 0.055 to 0.101 per hour. We also examined the size fractionation of eDNA and concluded eDNA is both intra- and extracellular. Finally, we derived a simple mass-balance model to estimate fish abundance from eDNA concentration. The mesocosm-derived shedding and decay rates inform the interpretation of eDNA concentrations measured in environmental samples and future use of eDNA as a monitoring tool.
View details for DOI 10.1021/acs.est.6b03114
View details for Web of Science ID 000384841900019
View details for PubMedID 27580258
- Quantifying overlap between the Deepwater Horizon oil spill and predicted bluefin tuna spawning habitat in the Gulf of Mexico SCIENTIFIC REPORTS 2016; 6
The effect of temperature on postprandial metabolism of yellowfin tuna (Thunnus albacares)
COMPARATIVE BIOCHEMISTRY AND PHYSIOLOGY A-MOLECULAR & INTEGRATIVE PHYSIOLOGY
2016; 195: 32-38
Specific dynamic action (SDA), the increase in metabolic expenditure associated with consumption of a meal, represents a substantial portion of fish energy budgets and is highly influenced by ambient temperature. The effect of temperature on SDA has not been studied in yellowfin tuna (Thunnus albacares, Bonnaterre 1788), an active pelagic predator that occupies temperate and subtropical waters. The energetic cost and duration of SDA were calculated by comparing routine and post-prandial oxygen consumption rates. Mean routine metabolic rates in yellowfin tuna increased with temperature, from 136mgO2kg(-1)h(-1) at 20°C to 211mgO2kg(-1)h at 24°C. The mean duration of SDA decreased from 40.2h at 20°C to 33.1h at 24°C, while mean SDA coefficient, the percentage of energy in a meal that is consumed during digestion, increased from 5.9% at 20°C to 12.7% at 24°C. Digestion in yellowfin tuna is faster at a higher temperature but requires additional oxidative energy. Enhanced characterization of the role of temperature in SDA of yellowfin tuna deepens our understanding of tuna physiology and can help improve management of aquaculture and fisheries.
View details for DOI 10.1016/j.cbpa.2016.01.005
View details for Web of Science ID 000373410500005
View details for PubMedID 26794613
- Tracking the fidelity of Atlantic bluefin tuna released in Canadian waters to the Gulf of Mexico spawning grounds CANADIAN JOURNAL OF FISHERIES AND AQUATIC SCIENCES 2015; 72 (11): 1700-1717
Exposure to Deepwater Horizon weathered crude oil increases routine metabolic demand in chub mackerel, Scomber japonicus.
Marine pollution bulletin
2015; 98 (1-2): 259-266
During the 2010 Deepwater Horizon incident, the continuous release of crude oil from the damaged Macondo 252 wellhead on the ocean floor contaminated surface water habitats for pelagic fish for more than 12weeks. The spill occurred across pelagic, neritic and benthic waters, impacting a variety of ecosystems. Chemical components of crude oil are known to disrupt cardiac function in juvenile fish, and here we investigate the effects of oil on the routine metabolic rate of chub mackerel, Scomber japonicus. Mackerel were exposed to artificially weathered Macondo 252 crude oil, prepared as a Water Accommodated Fraction (WAF), for 72 or 96h. Routine metabolic rates were determined pre- and post-exposure using an intermittent-flow, swim tunnel respirometer. Routine energetic demand increased in all mackerels in response to crude oil and reached statistical significance relative to unexposed controls at 96h. Chemical analyses of bile from exposed fish revealed elevated levels of fluorescent metabolites, confirming the bioavailability of polycyclic aromatic hydrocarbons (PAHs) in the exposure WAF. The observed increase in metabolic demand is likely attributable to the bioenergetic costs of contaminant detoxification. These results indicate that short-term exposure (i.e. days) to oil has sub-lethal toxicity to mackerel and results in physiological stress during the active spill phase of the incident.
View details for DOI 10.1016/j.marpolbul.2015.06.039
View details for PubMedID 26210587
Direct quantification of energy intake in an apex marine predator suggests physiology is a key driver of migrations.
2015; 1 (8)
Pacific bluefin tuna (Thunnus orientalis) are highly migratory apex marine predators that inhabit a broad thermal niche. The energy needed for migration must be garnered by foraging, but measuring energy intake in the marine environment is challenging. We quantified the energy intake of Pacific bluefin tuna in the California Current using a laboratory-validated model, the first such measurement in a wild marine predator. Mean daily energy intake was highest off the coast of Baja California, Mexico in summer (mean ± SD, 1034 ± 669 kcal), followed by autumn when Pacific bluefin achieve their northernmost range in waters off northern California (944 ± 579 kcal). Movements were not always consistent with maximizing energy intake: the Pacific bluefin move out of energy rich waters both in late summer and winter, coincident with rising and falling water temperatures, respectively. We hypothesize that temperature-related physiological constraints drive migration and that Pacific bluefin tuna optimize energy intake within a range of optimal aerobic performance.
View details for DOI 10.1126/sciadv.1400270
View details for PubMedID 26601248
Assessing niche width of endothermic fish from genes to ecosystem.
Proceedings of the National Academy of Sciences of the United States of America
2015; 112 (27): 8350-8355
Endothermy in vertebrates has been postulated to confer physiological and ecological advantages. In endothermic fish, niche expansion into cooler waters is correlated with specific physiological traits and is hypothesized to lead to greater foraging success and increased fitness. Using the seasonal co-occurrence of three tuna species in the eastern Pacific Ocean as a model system, we used cardiac gene expression data (as a proxy for thermal tolerance to low temperatures), archival tag data, and diet analyses to examine the vertical niche expansion hypothesis for endothermy in situ. Yellowfin, albacore, and Pacific bluefin tuna (PBFT) in the California Current system used more surface, mesopelagic, and deep waters, respectively. Expression of cardiac genes for calcium cycling increased in PBFT and coincided with broader vertical and thermal niche utilization. However, the PBFT diet was less diverse and focused on energy-rich forage fishes but did not show the greatest energy gains. Ecosystem-based management strategies for tunas should thus consider species-specific differences in physiology and foraging specialization.
View details for DOI 10.1073/pnas.1500524112
View details for PubMedID 26100889
Hearing thresholds of swimming Pacific bluefin tuna Thunnus orientalis
JOURNAL OF COMPARATIVE PHYSIOLOGY A-NEUROETHOLOGY SENSORY NEURAL AND BEHAVIORAL PHYSIOLOGY
2015; 201 (5): 441-454
Pacific bluefin tuna (Thunnus orientalis) is a highly migratory, commercially valuable species potentially vulnerable to acoustic noise generated from human activities which could impact behavior and fitness. Although significant efforts have been made to understand hearing abilities of fishes, the large size and need to continuously swim for respiration have hindered investigations with tuna and other large pelagic species. In this study, Pacific bluefin tuna were trained to respond to a pure tone sound stimulus ranging 325-800 Hz and their hearing abilities quantified using a staircase psychophysical technique. Hearing was most sensitive from 400 to 500 Hz in terms of particle motion (radial acceleration -88 dB re 1 m s(-2); vertical acceleration -86 dB re 1 m s(-2)) and sound pressure (83 dB re 1 μPa). Compared to yellowfin tuna (Thunnus albacares) and kawakawa (Euthynnus affinis), Pacific bluefin tuna has a similar bandwidth of hearing and best frequency, but greater sensitivity overall. Careful calibration of the sound stimulus and experimental tank environment, as well as the adoption of behavioral methodology, demonstrates an experimental approach highly effective for the study of large fish species in the laboratory.
View details for DOI 10.1007/s00359-015-0991-x
View details for Web of Science ID 000353353700002
View details for PubMedID 25732931
- Reconstructing habitat use by juvenile salmon sharks links upwelling to strandings in the California Current MARINE ECOLOGY PROGRESS SERIES 2015; 525: 217-228
Effect of temperature acclimation on red blood cell oxygen affinity in Pacific bluefin tuna (Thunnus orientalis) and yellowfin tuna (Thunnus albacares)
COMPARATIVE BIOCHEMISTRY AND PHYSIOLOGY A-MOLECULAR & INTEGRATIVE PHYSIOLOGY
2015; 181: 36-44
Hemoglobin-oxygen (Hb-O2) binding properties are central to aerobic physiology, and must be optimized for an animal's aerobic requirements and environmental conditions, both of which can vary widely with seasonal changes or acutely with diving. In the case of tunas, the matter is further complicated by large regional temperature differences between tissues within the same animal. This study investigates the effects of thermal acclimation on red blood cell Hb-O2 binding in Pacific bluefin tuna (T. orientalis) and yellowfin tuna (T. albacares) maintained in captive tanks at acclimation temperatures of 17°, 20° and 24 °C. Oxygen binding properties of acclimated tuna isolated red blood cells were examined under varying experimental temperatures (15°-35 °C) and CO2 levels (0%, 0.5% and 1.5%). Results for Pacific bluefin tuna produced temperature-independence at 17 °C- and 20 °C-acclimation temperatures and significant reverse temperature-dependence at 24 °C-acclimation in the absence of CO2, with instances of reverse temperature-dependence in 17 °C- and 24 °C-acclimations at 0.5% and 1.5% CO2. In contrast, yellowfin tuna produced normal temperature-dependence at each acclimation temperature at 0% CO2, temperature-independence at 0.5% and 1.5% CO2, and significant reverse temperature-dependence at 17 °C-acclimation and 0.5% CO2. Thermal acclimation of Pacific bluefin tuna increased O2 binding affinity of the 17 °C-acclimation group, and produced a significantly steeper oxygen equilibrium curve slope (nH) at 24 °C-acclimation compared to the other acclimation temperatures. We discuss the potential implications of these findings below.
View details for DOI 10.1016/j.cbpa.2014.11.014
View details for Web of Science ID 000350081400005
View details for PubMedID 25434601
Electronic Tagging of Atlantic Bluefin Tuna (Thunnus thynnus, L.) Reveals Habitat Use and Behaviors in the Mediterranean Sea
2015; 10 (2)
We analyzed the movements of Atlantic tuna (Thunnus thynnus L.) in the Mediterranean Sea using data from 2 archival tags and 37 pop-up satellite archival tags (PAT). Bluefin tuna ranging in size from 12 to 248 kg were tagged on board recreational boats in the western Mediterranean and the Adriatic Sea between May and September during two different periods (2000 to 2001 and 2008 to 2012). Although tuna migrations between the Mediterranean Sea and the Atlantic Ocean have been well reported, our results indicate that part of the bluefin tuna population remains in the Mediterranean basin for much of the year, revealing a more complex population structure. In this study we demonstrate links between the western Mediterranean, the Adriatic and the Gulf of Sidra (Libya) using over 4336 recorded days of location and behavior data from tagged bluefin tuna with a maximum track length of 394 days. We described the oceanographic preferences and horizontal behaviors during the spawning season for 4 adult bluefin tuna. We also analyzed the time series data that reveals the vertical behavior of one pop-up satellite tag recovered, which was attached to a 43.9 kg tuna. This fish displayed a unique diving pattern within 16 days of the spawning season, suggesting a use of the thermocline as a thermoregulatory mechanism compatible with spawning. The results obtained hereby confirm that the Mediterranean is clearly an important habitat for this species, not only as spawning ground, but also as an overwintering foraging ground.
View details for DOI 10.1371/journal.pone.0116638
View details for Web of Science ID 000349545300022
View details for PubMedID 25671316
Stable isotope analysis of vertebrae reveals ontogenetic changes in habitat in an endothermic pelagic shark
PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES
2015; 282 (1799)
Ontogenetic changes in habitat are driven by shifting life-history requirements and play an important role in population dynamics. However, large portions of the life history of many pelagic species are still poorly understood or unknown. We used a novel combination of stable isotope analysis of vertebral annuli, Bayesian mixing models, isoscapes and electronic tag data to reconstruct ontogenetic patterns of habitat and resource use in a pelagic apex predator, the salmon shark (Lamna ditropis). Results identified the North Pacific Transition Zone as the major nursery area for salmon sharks and revealed an ontogenetic shift around the age of maturity from oceanic to increased use of neritic habitats. The nursery habitat may reflect trade-offs between prey availability, predation pressure and thermal constraints on juvenile endothermic sharks. The ontogenetic shift in habitat coincided with a reduction of isotopic niche, possibly reflecting specialization upon particular prey or habitats. Using tagging data to inform Bayesian isotopic mixing models revealed that adult sharks primarily use neritic habitats of Alaska yet receive a trophic subsidy from oceanic habitats. Integrating the multiple methods used here provides a powerful approach to retrospectively study the ecology and life history of migratory species throughout their ontogeny.
View details for DOI 10.1098/rspb.2014.1446
View details for Web of Science ID 000354866500003
View details for PubMedID 25621332
- Bioenergetics of captive Pacific bluefin tuna (Thunnus orientalis) AQUACULTURE 2014; 434: 137-144
Reconstructing transoceanic migration patterns of Pacific bluefin tuna using a chemical tracer toolbox
2014; 95 (6): 1674-1683
View details for Web of Science ID 000337218500025
Deepwater Horizon crude oil impacts the developing hearts of large predatory pelagic fish
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
2014; 111 (15): E1510-E1518
The Deepwater Horizon disaster released more than 636 million L of crude oil into the northern Gulf of Mexico. The spill oiled upper surface water spawning habitats for many commercially and ecologically important pelagic fish species. Consequently, the developing spawn (embryos and larvae) of tunas, swordfish, and other large predators were potentially exposed to crude oil-derived polycyclic aromatic hydrocarbons (PAHs). Fish embryos are generally very sensitive to PAH-induced cardiotoxicity, and adverse changes in heart physiology and morphology can cause both acute and delayed mortality. Cardiac function is particularly important for fast-swimming pelagic predators with high aerobic demand. Offspring for these species develop rapidly at relatively high temperatures, and their vulnerability to crude oil toxicity is unknown. We assessed the impacts of field-collected Deepwater Horizon (MC252) oil samples on embryos of three pelagic fish: bluefin tuna, yellowfin tuna, and an amberjack. We show that environmentally realistic exposures (1-15 µg/L total PAH) cause specific dose-dependent defects in cardiac function in all three species, with circulatory disruption culminating in pericardial edema and other secondary malformations. Each species displayed an irregular atrial arrhythmia following oil exposure, indicating a highly conserved response to oil toxicity. A considerable portion of Gulf water samples collected during the spill had PAH concentrations exceeding toxicity thresholds observed here, indicating the potential for losses of pelagic fish larvae. Vulnerability assessments in other ocean habitats, including the Arctic, should focus on the developing heart of resident fish species as an exceptionally sensitive and consistent indicator of crude oil impacts.
View details for DOI 10.1073/pnas.1320950111
View details for Web of Science ID 000334288600012
View details for PubMedID 24706825
Predicting bycatch hotspots for endangered leatherback turtles on longlines in the Pacific Ocean
PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES
2014; 281 (1777)
Fisheries bycatch is a critical source of mortality for rapidly declining populations of leatherback turtles, Dermochelys coriacea. We integrated use-intensity distributions for 135 satellite-tracked adult turtles with longline fishing effort to estimate predicted bycatch risk over space and time in the Pacific Ocean. Areas of predicted bycatch risk did not overlap for eastern and western Pacific nesting populations, warranting their consideration as distinct management units with respect to fisheries bycatch. For western Pacific nesting populations, we identified several areas of high risk in the north and central Pacific, but greatest risk was adjacent to primary nesting beaches in tropical seas of Indo-Pacific islands, largely confined to several exclusive economic zones under the jurisdiction of national authorities. For eastern Pacific nesting populations, we identified moderate risk associated with migrations to nesting beaches, but the greatest risk was in the South Pacific Gyre, a broad pelagic zone outside national waters where management is currently lacking and may prove difficult to implement. Efforts should focus on these predicted hotspots to develop more targeted management approaches to alleviate leatherback bycatch.
View details for DOI 10.1098/rspb.2013.2559
View details for Web of Science ID 000332382000013
View details for PubMedID 24403331
Crude Oil Impairs Cardiac Excitation-Contraction Coupling in Fish
2014; 343 (6172): 772-776
Crude oil is known to disrupt cardiac function in fish embryos. Large oil spills, such as the Deepwater Horizon (DWH) disaster that occurred in 2010 in the Gulf of Mexico, could severely affect fish at impacted spawning sites. The physiological mechanisms underlying such potential cardiotoxic effects remain unclear. Here, we show that crude oil samples collected from the DWH spill prolonged the action potential of isolated cardiomyocytes from juvenile bluefin and yellowfin tunas, through the blocking of the delayed rectifier potassium current (I(Kr)). Crude oil exposure also decreased calcium current (I(Ca)) and calcium cycling, which disrupted excitation-contraction coupling in cardiomyocytes. Our findings demonstrate a cardiotoxic mechanism by which crude oil affects the regulation of cellular excitability, with implications for life-threatening arrhythmias in vertebrates.
View details for DOI 10.1126/science.1242747
View details for Web of Science ID 000331557800040
View details for PubMedID 24531969
Amino Acid Isotope Incorporation and Enrichment Factors in Pacific Bluefin Tuna, Thunnus orientalis
2014; 9 (1)
Compound specific isotopic analysis (CSIA) of amino acids has received increasing attention in ecological studies in recent years due to its ability to evaluate trophic positions and elucidate baseline nutrient sources. However, the incorporation rates of individual amino acids into protein and specific trophic discrimination factors (TDFs) are largely unknown, limiting the application of CSIA to trophic studies. We determined nitrogen turnover rates of individual amino acids from a long-term (up to 1054 days) laboratory experiment using captive Pacific bluefin tuna, Thunnus orientalis (PBFT), a large endothermic pelagic fish fed a controlled diet. Small PBFT (white muscle δ(15)N∼11.5‰) were collected in San Diego, CA and transported to the Tuna Research and Conservation Center (TRCC) where they were fed a controlled diet with high δ(15)N values relative to PBFT white muscle (diet δ(15)N∼13.9‰). Half-lives of trophic and source amino acids ranged from 28.6 to 305.4 days and 67.5 to 136.2 days, respectively. The TDF for the weighted mean values of amino acids was 3.0 ‰, ranging from 2.2 to 15.8 ‰ for individual combinations of 6 trophic and 5 source amino acids. Changes in the δ(15)N values of amino acids across trophic levels are the underlying drivers of the trophic (15)N enrichment. Nearly all amino acid δ(15)N values in this experiment changed exponentially and could be described by a single compartment model. Significant differences in the rate of (15)N incorporation were found for source and trophic amino acids both within and between these groups. Varying half-lives of individual amino acids can be applied to migratory organisms as isotopic clocks, determining the length of time an individual has spent in a new environment. These results greatly enhance the ability to interpret compound specific isotope analyses in trophic studies.
View details for DOI 10.1371/journal.pone.0085818
View details for Web of Science ID 000330283100078
View details for PubMedID 24465724
Effects of temperature acclimation on Pacific bluefin tuna (Thunnus orientalis) cardiac transcriptome
AMERICAN JOURNAL OF PHYSIOLOGY-REGULATORY INTEGRATIVE AND COMPARATIVE PHYSIOLOGY
2013; 305 (9): R1010-R1020
Little is known about the mechanisms underpinning thermal plasticity of vertebrate hearts. Bluefin tuna hearts offer a unique model to investigate processes underlying thermal acclimation. Their hearts, while supporting an endothermic physiology, operate at ambient temperature, and are presented with a thermal challenge when migrating to different thermal regimes. Here, we examined the molecular responses in atrial and ventricular tissues of Pacific bluefin tuna acclimated to 14°C, 20°C, and 25°C. Quantitative PCR studies showed an increase in sarcoplasmic reticulum Ca(2+) ATPase gene expression with cold acclimation and an induction of Na(+)/Ca(2+)-exchanger gene at both cold and warm temperatures. These data provide evidence for thermal plasticity of excitation-contraction coupling gene expression in bluefin tunas and indicate an increased capacity for internal Ca(2+) storage in cardiac myocytes at 14°C. Transcriptomic analysis showed profound changes in cardiac tissues with acclimation. A principal component analysis revealed that temperature effect was greatest on gene expression in warm-acclimated atrium. Overall data showed an increase in cardiac energy metabolism at 14°C, potentially compensating for cold temperature to optimize bluefin tuna performance in colder oceans. In contrast, metabolic enzyme activity and gene expression data suggest a decrease in ATP production at 25°C. Expression of genes involved in protein turnover and molecular chaperones was also decreased at 25°C. Expression of genes involved in oxidative stress response and programmed cell death suggest an increase in oxidative damage and apoptosis at 25°C, particularly in the atrium. These findings provide insights into molecular processes that may characterize cardiac phenotypes at upper thermal limits of teleosts.
View details for DOI 10.1152/ajpregu.00254.2013
View details for Web of Science ID 000326584200005
View details for PubMedID 24005253
Quantifying energy intake in Pacific bluefin tuna (Thunnus orientalis) using the heat increment of feeding
JOURNAL OF EXPERIMENTAL BIOLOGY
2013; 216 (21): 4109-4123
Using implanted archival tags, we examined the effects of meal caloric value, food type (sardine or squid) and ambient temperature on the magnitude and duration of the heat increment of feeding in three captive juvenile Pacific bluefin tuna. The objective of our study was to develop a model that can be used to estimate energy intake in wild fish of similar body mass. Both the magnitude and duration of the heat increment of feeding (measured by visceral warming) showed a strong positive correlation with the caloric value of the ingested meal. Controlling for meal caloric value, the extent of visceral warming was significantly greater at lower ambient temperature. The extent of visceral warming was also significantly higher for squid meals compared with sardine meals. By using a hierarchical Bayesian model to analyze our data and treating individuals as random effects, we demonstrate how increases in visceral temperature can be used to estimate the energy intake of wild Pacific bluefin tuna of similar body mass to the individuals used in our study.
View details for DOI 10.1242/jeb.084335
View details for Web of Science ID 000325806300027
View details for PubMedID 24133153
- Cumulative human impacts on marine predators. Nature communications 2013; 4: 2688-?
- Exxon Valdez to Deepwater Horizon: Comparable toxicity of both crude oils to fish early life stages AQUATIC TOXICOLOGY 2013; 142: 303-316
Heart rate responses to temperature in free-swimming Pacific bluefin tuna (Thunnus orientalis)
JOURNAL OF EXPERIMENTAL BIOLOGY
2013; 216 (17): 3208-3214
The bluefin tuna heart remains at ambient water temperature (Ta) but must supply blood to warm regions of the body served by countercurrent vascular heat exchangers. Despite this unusual physiology, inherent difficulties have precluded an understanding of the cardiovascular responses to Ta in free-swimming bluefin tunas. We measured the heart rate (f(H)) responses of two captive Pacific bluefin tunas (Thunnus orientalis; 9.7 and 13.3 kg) over a cumulative period of 40 days. Routine f(H) during fasting in the holding tank at a Ta of 20°C was 45.1±8.0 and 40.7±6.5 beats min(-1) for Tuna 1 and Tuna 2, respectively. f(H) decreased in each fish with a Q10 temperature coefficient of 2.6 (Tuna 1) and 3.1 (Tuna 2) as Ta in the tank was slowly decreased to 15°C (~0.4°C h(-1)), despite a gradual increase in swimming speed. The same thermal challenge during digestion revealed similar thermal dependence of f(H) and indicated that the rate of visceral cooling is not buffered by the heat increment of feeding. Acutely decreasing Ta from 20 to 10°C while Tuna 1 swam in a tunnel respirometer caused a progressive increase in tail-beat frequency and oxygen consumption rate (M(O2)). f(H) of this fish decreased with a Q10 of 2.7 as Ta decreased between 20 and 15°C, while further cooling to 10°C saw a general plateau in f(H) around 35 beats min(-1) with a Q10 of 1.3. A discussion of the relationships between f(H), and haemoglobin-oxygen binding sheds further light on how bluefin cardiorespiratory systems function in a changing thermal environment.
View details for DOI 10.1242/jeb.086546
View details for Web of Science ID 000322955200014
View details for PubMedID 23661777
Influence of Ambient Temperature on Specific Dynamic Action in Bluefin Tuna
Annual Meeting of the Society-for-Integrative-and-Comparative-Biology (SICB)
OXFORD UNIV PRESS INC. 2013: E289–E289
View details for Web of Science ID 000316991402213
- Predicted habitat shifts of Pacific top predators in a changing climate NATURE CLIMATE CHANGE 2013; 3 (3): 234-238
- Archival and acoustic tags reveal the post-spawning migrations, diving behavior, and thermal habitat of hatchery-origin Sacramento River steelhead kelts (Oncorhynchus mykiss) ENVIRONMENTAL BIOLOGY OF FISHES 2013; 96 (2-3): 175-187
Travelling light: white sharks (Carcharodon carcharias) rely on body lipid stores to power ocean-basin scale migration.
Proceedings. Biological sciences / The Royal Society
2013; 280 (1766): 20130836-?
Many species undertake long-distance annual migrations between foraging and reproductive areas. Such migrants depend on the efficient packaging, storage and utilization of energy to succeed. A diverse assemblage of organisms accomplishes this through the use of lipid reserves; yet, it remains unclear whether the migrations of elasmobranchs, which include the largest gill breathers on Earth, depend on such a mechanism. We examine depth records from pop-up satellite archival tags to discern changes in buoyancy as a proxy for energy storage in Eastern Pacific white sharks, and assess whether lipid depletion fuels long-distance (approx. 4000 km) migrations. We develop new algorithms to assess body condition, buoyancy and drift rate during drift dives and validate the techniques using a captive white shark. In the wild, we document a consistent increase in drift rate over the course of all migrations, indicating a decrease in buoyancy caused by the depletion of lipid reserves. These results comprise, to our knowledge, the first assessment of energy storage and budgeting in migrating sharks. The methods provide a basis for further insights into using electronic tags to reveal the energetic strategies of a wide range of elasmobranchs.
View details for DOI 10.1098/rspb.2013.0836
View details for PubMedID 23864595
Eating or Meeting? Cluster Analysis Reveals Intricacies of White Shark (Carcharodon carcharias) Migration and Offshore Behavior
2012; 7 (10)
Elucidating how mobile ocean predators utilize the pelagic environment is vital to understanding the dynamics of oceanic species and ecosystems. Pop-up archival transmitting (PAT) tags have emerged as an important tool to describe animal migrations in oceanic environments where direct observation is not feasible. Available PAT tag data, however, are for the most part limited to geographic position, swimming depth and environmental temperature, making effective behavioral observation challenging. However, novel analysis approaches have the potential to extend the interpretive power of these limited observations. Here we developed an approach based on clustering analysis of PAT daily time-at-depth histogram records to distinguish behavioral modes in white sharks (Carcharodon carcharias). We found four dominant and distinctive behavioral clusters matching previously described behavioral patterns, including two distinctive offshore diving modes. Once validated, we mapped behavior mode occurrence in space and time. Our results demonstrate spatial, temporal and sex-based structure in the diving behavior of white sharks in the northeastern Pacific previously unrecognized including behavioral and migratory patterns resembling those of species with lek mating systems. We discuss our findings, in combination with available life history and environmental data, and propose specific testable hypotheses to distinguish between mating and foraging in northeastern Pacific white sharks that can provide a framework for future work. Our methodology can be applied to similar datasets from other species to further define behaviors during unobservable phases.
View details for DOI 10.1371/journal.pone.0047819
View details for Web of Science ID 000310705300018
View details for PubMedID 23144707
View details for PubMedCentralID PMC3483152
Microarray gene expression profiles from mature gonad tissues of Atlantic bluefin tuna, Thunnus thynnus in the Gulf of Mexico
Bluefin tunas are highly prized pelagic fish species representing a significant economic resource to fisheries throughout the world. Atlantic bluefin tuna (Thunnus thynnus) populations have significantly declined due to overexploitation. As a consequence of their value and population decline, T. thynnus has been the focus of considerable research effort concerning many aspects of their life history. However, in-depth understanding of T. thynnus reproductive biology is still lacking. Knowledge of reproductive physiology is a very important tool for determining effective fisheries and aquaculture management. Transcriptome techniques are proving powerful and provide novel insights into physiological processes. Construction of a microarray from T. thynnus ESTs sourced from reproductive tissues has provided an ideal platform to study the reproductive physiology of bluefin tunas. The aim of this investigation was to compare transcription profiles from the ovaries and testes of mature T. thynnus to establish sex specific variations underlying their reproductive physiology.Male and females T. thynnus gonad tissues were collected from the wild and histologically staged. Sub-samples of sexually mature tissues were also measured for their mRNA differential expression among the sexes using the custom microarray design BFT 4X44K. A total of 7068 ESTs were assessed for differential expression of which 1273 ESTs were significantly different (p<0.05) with >2 fold change in expression according to sex. Differential expression for 13 of these ESTs was validated with quantitative PCR. These include genes involved in egg envelope formation, hydration, and lipid transport/accumulation more highly expressed in ovaries compared with testis, while genes involved in meiosis, sperm motility and lipid metabolism were more highly expressed in testis compared with ovaries.This investigation has furthered our knowledge of bluefin tunas reproductive biology by using a contemporary transcriptome approach. Gene expression profiles in T. thynnus sexually mature testes and ovaries were characterized with reference to gametogenesis and potential alternative functions. This report is the first application of microarray technology for bluefin tunas and demonstrates the efficacy by which this technique may be used for further characterization of specific biological aspects for this valuable teleost fish.
View details for DOI 10.1186/1471-2164-13-530
View details for Web of Science ID 000310085500001
View details for PubMedID 23036107
Stable Isotope Analysis Challenges Wasp-Waist Food Web Assumptions in an Upwelling Pelagic Ecosystem
Eastern boundary currents are often described as 'wasp-waist' ecosystems in which one or few mid-level forage species support a high diversity of larger predators that are highly susceptible to fluctuations in prey biomass. The assumption of wasp-waist control has not been empirically tested in all such ecosystems. This study used stable isotope analysis to test the hypothesis of wasp-waist control in the southern California Current large marine ecosystem (CCLME). We analyzed prey and predator tissue for δ¹³C and δ¹⁵N and used Bayesian mixing models to provide estimates of CCLME trophic dynamics from 2007-2010. Our results show high omnivory, planktivory by some predators, and a higher degree of trophic connectivity than that suggested by the wasp-waist model. Based on this study period, wasp-waist models oversimplify trophic dynamics within the CCLME and potentially other upwelling, pelagic ecosystems. Higher trophic connectivity in the CCLME likely increases ecosystem stability and resilience to perturbations.
View details for DOI 10.1038/srep00654
View details for Web of Science ID 000308807000002
View details for PubMedID 22977729
Movement Patterns for a Critically Endangered Species, the Leatherback Turtle (Dermochelys coriacea), Linked to Foraging Success and Population Status
2012; 7 (5)
Foraging success for pelagic vertebrates may be revealed by horizontal and vertical movement patterns. We show markedly different patterns for leatherback turtles in the North Atlantic versus Eastern Pacific, which feed on gelatinous zooplankton that are only occasionally found in high densities. In the Atlantic, travel speed was characterized by two modes, indicative of high foraging success at low speeds (<15 km d(-1)) and transit at high speeds (20-45 km d(-1)). Only a single mode was evident in the Pacific, which occurred at speeds of 21 km d(-1) indicative of transit. The mean dive depth was more variable in relation to latitude but closer to the mean annual depth of the thermocline and nutricline for North Atlantic than Eastern Pacific turtles. The most parsimonious explanation for these findings is that Eastern Pacific turtles rarely achieve high foraging success. This is the first support for foraging behaviour differences between populations of this critically endangered species and suggests that longer periods searching for prey may be hindering population recovery in the Pacific while aiding population maintenance in the Atlantic.
View details for DOI 10.1371/journal.pone.0036401
View details for Web of Science ID 000305341300016
View details for PubMedID 22615767
- Thermal dependence of cardiac SR Ca2+-ATPase from fish and mammals JOURNAL OF THERMAL BIOLOGY 2012; 37 (3): 217-223
Identification of distinct movement patterns in Pacific leatherback turtle populations influenced by ocean conditions
2012; 22 (3): 735-747
Interactions with fisheries are believed to be a major cause of mortality for adult leatherback turtles (Dermochelys coriacea), which is of particular concern in the Pacific Ocean, where they have been rapidly declining. In order to identify where these interactions are occurring and how they may be reduced, it is essential first to understand the movements and behavior of leatherback turtles. There are two regional nesting populations in the East Pacific (EP) and West Pacific (WP), comprising multiple nesting sites. We synthesized tracking data from the two populations and compared their movement patterns. A switching state-space model was applied to 135 Argos satellite tracks to account for observation error, and to distinguish between migratory and area-restricted search behaviors. The tracking data, from the largest leatherback data set ever assembled, indicated that there was a high degree of spatial segregation between EP and WP leatherbacks. Area-restricted search behavior mainly occurred in the southeast Pacific for the EP leatherbacks, whereas the WP leatherbacks had several different search areas in the California Current, central North Pacific, South China Sea, off eastern Indonesia, and off southeastern Australia. We also extracted remotely sensed oceanographic data and applied a generalized linear mixed model to determine if leatherbacks exhibited different behavior in relation to environmental variables. For the WP population, the probability of area-restricted search behavior was positively correlated with chlorophyll-a concentration. This response was less strong in the EP population, but these turtles had a higher probability of search behavior where there was greater Ekman upwelling, which may increase the transport of nutrients and consequently prey availability. These divergent responses to oceanographic conditions have implications for leatherback vulnerability to fisheries interactions and to the effects of climate change. The occurrence of leatherback turtles within both coastal and pelagic areas means they have a high risk of exposure to many different fisheries, which may be very distant from their nesting sites. The EP leatherbacks have more limited foraging grounds than the WP leatherbacks, which could make them more susceptible to any temperature or prey changes that occur in response to climate change.
View details for Web of Science ID 000303312000001
View details for PubMedID 22645807
- State-space framework for estimating measurement error from double-tagging telemetry experiments METHODS IN ECOLOGY AND EVOLUTION 2012; 3 (2): 291-302
Warm fish with cold hearts: Cardiac thermal plasticity of Pacific bluefin tuna Thunnus orientalis
Annual Meeting of the Society-for-Integrative-and-Comparative-Biology (SICB)/Symposium on New Frontiers from Marine Snakes to Marine Ecosystems
OXFORD UNIV PRESS INC. 2012: E86–E86
View details for Web of Science ID 000303165000345
Using Stable Isotope Analysis to Understand the Migration and Trophic Ecology of Northeastern Pacific White Sharks (Carcharodon carcharias)
2012; 7 (2)
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 (δ(13)C) and nitrogen (δ(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 δ(13)C and δ(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
View details for PubMedCentralID PMC3280240
- Seasonal changes in depth distribution of salmon sharks (Lamna ditropis) in Alaskan waters: implications for foraging ecology CANADIAN JOURNAL OF FISHERIES AND AQUATIC SCIENCES 2011; 68 (11): 1905-1921
- The role of discounting and dynamics in determining the economic efficiency of time-area closures for managing fishery bycatch THEORETICAL ECOLOGY 2011; 4 (4): 513-526
Temperature dependence of cardiac sarcoplasmic reticulum Ca2+-ATPase from rainbow trout Oncorhynchus mykiss
JOURNAL OF FISH BIOLOGY
2011; 79 (3): 789-800
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
A first estimate of white shark, Carcharodon carcharias, abundance off Central California
2011; 7 (4): 581-583
The decline of sharks in the global oceans underscores the need for careful assessment and monitoring of remaining populations. The northeastern Pacific is the home range for a genetically distinct clade of white sharks (Carcharodon carcharias). Little is known about the conservation status of this demographically isolated population, concentrated seasonally at two discrete aggregation sites: Central California (CCA) and Guadalupe Island, Mexico. We used photo-identification of dorsal fins in a sequential Bayesian mark-recapture algorithm to estimate white shark abundance off CCA. We collected 321 photographs identifying 130 unique individuals, and estimated the abundance off CCA to be 219 mature and sub-adult individuals ((130, 275) 95% credible intervals), substantially smaller than populations of other large marine predators. Our methods can be readily expanded to estimate shark population abundance at other locations, and over time, to monitor the status, population trends and protection needs of these globally distributed predators.
View details for DOI 10.1098/rsbl.2011.0124
View details for Web of Science ID 000292639100030
View details for PubMedID 21389017
View details for PubMedCentralID PMC3130246
Tracking apex marine predator movements in a dynamic ocean
2011; 475 (7354): 86-90
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
- Long-term individual identification and site fidelity of white sharks, Carcharodon carcharias, off California using dorsal fins MARINE BIOLOGY 2011; 158 (6): 1233-1237
Temperature effects on Ca2+ cycling in scombrid cardiomyocytes: a phylogenetic comparison
JOURNAL OF EXPERIMENTAL BIOLOGY
2011; 214 (7): 1068-1076
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
Warm fish with cold hearts: thermal plasticity of excitation-contraction coupling in bluefin tuna
PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES
2011; 278 (1702): 18-27
Bluefin tuna have a unique physiology. Elevated metabolic rates coupled with heat exchangers enable bluefin tunas to conserve heat in their locomotory muscle, viscera, eyes and brain, yet their hearts operate at ambient water temperature. This arrangement of a warm fish with a cold heart is unique among vertebrates and can result in a reduction in cardiac function in the cold despite the elevated metabolic demands of endothermic tissues. In this study, we used laser scanning confocal microscopy and electron microscopy to investigate how acute and chronic temperature change affects tuna cardiac function. We examined the temporal and spatial properties of the intracellular Ca2+ transient (Δ[Ca2+]i) in Pacific bluefin tuna (Thunnus orientalis) ventricular myocytes at the acclimation temperatures of 14°C and 24°C and at a common test temperature of 19°C. Acute (less than 5 min) warming and cooling accelerated and slowed the kinetics of Δ[Ca2+]i, indicating that temperature change limits cardiac myocyte performance. Importantly, we show that thermal acclimation offered partial compensation for these direct effects of temperature. Prolonged cold exposure (more than four weeks) increased the amplitude and kinetics of Δ[Ca2+]i by increasing intracellular Ca2+ cycling through the sarcoplasmic reticulum (SR). These functional findings are supported by electron microscopy, which revealed a greater volume fraction of ventricular SR in cold-acclimated tuna myocytes. The results indicate that SR function is crucial to the performance of the bluefin tuna heart in the cold. We suggest that SR Ca2+ cycling is the malleable unit of cellular Ca2+ flux, offering a mechanism for thermal plasticity in fish hearts. These findings have implications beyond endothermic fish and may help to delineate the key steps required to protect vertebrate cardiac function in the cold.
View details for DOI 10.1098/rspb.2010.1274
View details for Web of Science ID 000284554800004
View details for PubMedID 20667881
- Vertical and horizontal habitat preferences of post-nesting leatherback turtles in the South Pacific Ocean MARINE ECOLOGY PROGRESS SERIES 2011; 422: 275-289
- Movements and behaviors of swordfish in the Atlantic and Pacific Oceans examined using pop-up satellite archival tags FISHERIES OCEANOGRAPHY 2011; 20 (3): 219-241
Expression of cytokines IL-1 beta and TNF-alpha in tissues and cysts surrounding Didymocystis wedli (Digenea, Didymozoidae) in the Pacific bluefin tuna (Thunnus orientalis)
FISH & SHELLFISH IMMUNOLOGY
2010; 29 (3): 487-493
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
Postprandial metabolism of Pacific bluefin tuna (Thunnus orientalis)
JOURNAL OF EXPERIMENTAL BIOLOGY
2010; 213 (14): 2379-2385
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
- Movements of pacific bluefin tuna (Thunnus orientalis) in the Eastern North Pacific revealed with archival tags International Symposium on Climate Impacts on Oceanic Top Predators (CLIOTOP) PERGAMON-ELSEVIER SCIENCE LTD. 2010: 94–104
Comparative Influence of Ocean Conditions on Yellowfin and Atlantic Bluefin Tuna Catch from Longlines in the Gulf of Mexico
2010; 5 (5)
Directed fishing effort for Atlantic bluefin tuna in the Gulf of Mexico (GOM), their primary spawning grounds in the western Atlantic, has been prohibited since the 1980s due to a precipitous decline of the spawning stock biomass. However, pelagic longlines targeted at other species, primarily yellowfin tuna and swordfish, continue to catch Atlantic bluefin tuna in the GOM as bycatch. Spatial and temporal management measures minimizing bluefin tuna bycatch in the GOM will likely become important in rebuilding the western Atlantic bluefin stock. In order to help inform management policy and understand the relative distribution of target and bycatch species in the GOM, we compared the spatiotemporal variability and environmental influences on the catch per unit effort (CPUE) of yellowfin (target) and bluefin tuna (bycatch). Catch and effort data from pelagic longline fisheries observers (1993-2005) and scientific tagging cruises (1998-2002) were coupled with environmental and biological data. Negative binomial models were used to fit the data for both species and Akaike's Information Criterion (corrected for small sample size) was used to determine the best model. Our results indicate that bluefin CPUE had higher spatiotemporal variability as compared to yellowfin CPUE. Bluefin CPUE increased substantially during the breeding months (March-June) and peaked in April and May, while yellowfin CPUE remained relatively high throughout the year. In addition, bluefin CPUE was significantly higher in areas with negative sea surface height anomalies and cooler sea surface temperatures, which are characteristic of mesoscale cyclonic eddies. In contrast, yellowfin CPUE was less sensitive to environmental variability. These differences in seasonal variability and sensitivity to environmental influences suggest that bluefin tuna bycatch in the GOM can be reduced substantially by managing the spatial and temporal distribution of the pelagic longline effort without substantially impacting yellowfin tuna catches.
View details for DOI 10.1371/journal.pone.0010756
View details for Web of Science ID 000278222100001
View details for PubMedID 20526356
Multilocus phylogenetic analyses reveal that habitat selection drives the speciation of Didymozoidae (Digenea) parasitizing Pacific and Atlantic bluefin tunas
2010; 137 (6): 1013-1025
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
Philopatry and migration of Pacific white sharks
PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES
2010; 277 (1682): 679-688
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
View details for PubMedCentralID PMC2842735
- Movements and diving behavior of Atlantic bluefin tuna Thunnus thynnus in relation to water column structure in the northwestern Atlantic MARINE ECOLOGY PROGRESS SERIES 2010; 400: 245-265
- Resource partitioning by species but not sex in sympatric boobies in the central Pacific Ocean MARINE ECOLOGY PROGRESS SERIES 2010; 403: 291-301
Effect of thermal acclimation on action potentials and sarcolemmal K+ channels from Pacific bluefin tuna cardiomyocytes
AMERICAN JOURNAL OF PHYSIOLOGY-REGULATORY INTEGRATIVE AND COMPARATIVE PHYSIOLOGY
2009; 297 (2): R502-R509
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
Seasonal Movements, Aggregations and Diving Behavior of Atlantic Bluefin Tuna (Thunnus thynnus) Revealed with Archival Tags
2009; 4 (7)
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
- Expression of Hsp70, Na+/K+ ATP-ase, HIF-1 alpha, IL-1 beta and TNF-alpha in captive Pacific bluefin tuna (Thunnus orientalis) after chronic warm and cold exposure JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY 2009; 374 (1): 51-57
Heterologous hybridization to a complementary DNA microarray reveals the effect of thermal acclimation in the endothermic bluefin tuna (Thunnus orientalis)
2009; 18 (10): 2092-2102
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
A comparison of spatial and temporal habitat use by male and female migrating Great White Sharks (Carcharodon carcharias) in the eastern Pacific
Annual Meeting of the Society-for-Integrative-and-Comparative-Biology
OXFORD UNIV PRESS INC. 2009: E29–E29
View details for Web of Science ID 000268808800114
- Mitochondrial DNA and electronic tracking reveal population structure of Atlantic bluefin tuna (Thunnus thynnus) MARINE BIOLOGY 2008; 156 (1): 13-24
Persistent leatherback turtle migrations present opportunities for conservation
2008; 6 (7): 1408-1416
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
- Migration of an upper trophic level predator, the salmon shark Lamna ditropis, between distant ecoregions MARINE ECOLOGY PROGRESS SERIES 2008; 372: 253-264
Temperature effects on metabolic rate of juvenile Pacific bluefin tuna Thunnus orientalis
JOURNAL OF EXPERIMENTAL BIOLOGY
2007; 210 (23): 4254-4261
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
Elevated Ca2+ ATPase (SERCA2) activity in tuna hearts: Comparative aspects of temperature dependence
ELSEVIER SCIENCE INC. 2007: 124–32
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
- Migration and habitat of white sharks (Carcharodon carcharias) in the eastern Pacific Ocean MARINE BIOLOGY 2007; 152 (4): 877-894
- Results of satellite tagging of Atlantic bluefin tuna, Thunnus thynnus, off the coast of Ireland 6th Conference on Fish Telemetry SPRINGER. 2007: 91–97
Influence of swimming speed on metabolic rates of juvenile Pacific bluefin tuna and yellowfin tuna
PHYSIOLOGICAL AND BIOCHEMICAL ZOOLOGY
2007; 80 (2): 167-177
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
- Annual migrations, diving behavior, and thermal biology of Atlantic bluefin tuna, Thunnus thynnus, on their Gulf of Mexico breeding grounds MARINE BIOLOGY 2007; 151 (1): 1-18
- High apex predator biomass on remote Pacific islands CORAL REEFS 2007; 26 (1): 47-51
Satellite tagging and cardiac physiology reveal niche expansion in salmon sharks
2005; 310 (5745): 104-106
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 tagging and population structure of Atlantic bluefin tuna
2005; 434 (7037): 1121-1127
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
Physiological ecology in the 21st Century: Advancements in biologging Science
Symposium on Integrative Biology in Honor of George A Bartholomew held at the Annual Meeting of the Society-for-Integrative-and-Comparative-Biology
OXFORD UNIV PRESS INC. 2005: 305–20
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
Salmon shark (Lamna ditrops): An endothermic fish from polar area with higher SERCA2 activity
Annual Meeting of the Society-for-Integrative-and-Comparative-Biology
OXFORD UNIV PRESS INC. 2004: 534–34
View details for Web of Science ID 000226721400096
Electrophysiological properties of the L-type Ca2+ current in cardiomyocytes from bluefin tuna and Pacific mackerel
AMERICAN JOURNAL OF PHYSIOLOGY-REGULATORY INTEGRATIVE AND COMPARATIVE PHYSIOLOGY
2004; 286 (4): R659-R668
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
In situ cardiac performance of Pacific bluefin tuna hearts in response to acute temperature change
JOURNAL OF EXPERIMENTAL BIOLOGY
2004; 207 (5): 881-890
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
Temperature dependence of the Ca2+-ATPase (SERCA2) in the ventricles of tuna and mackerel
AMERICAN JOURNAL OF PHYSIOLOGY-REGULATORY INTEGRATIVE AND COMPARATIVE PHYSIOLOGY
2004; 286 (2): R398-R404
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
Characterization of ryanodine receptor and Ca2+-ATPase isoforms in the thermogenic heater organ of blue marlin (Makaira nigricans)
JOURNAL OF EXPERIMENTAL BIOLOGY
2003; 206 (5): 805-812
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
Effects of temperature, epinephrine and Ca2+ on the hearts of yellowfin tuna (Thunnus albacares)
JOURNAL OF EXPERIMENTAL BIOLOGY
2002; 205 (13): 1881-1888
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
Satellite tagging - Expanded niche for white sharks
2002; 415 (6867): 35-36
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 Web of Science ID 000173028800028
Migratory movements, depth preferences, and thermal biology of Atlantic bluefin tuna
2001; 293 (5533): 1310-1314
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
Oxygen affinity and amino acid sequence of myoglobins from endothermic and ectothermic fish
AMERICAN JOURNAL OF PHYSIOLOGY-REGULATORY INTEGRATIVE AND COMPARATIVE PHYSIOLOGY
2001; 280 (4): R1123-R1133
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
Characterization of RyR1-slow, a ryanodine receptor specific to slow-twitch skeletal muscle
AMERICAN JOURNAL OF PHYSIOLOGY-REGULATORY INTEGRATIVE AND COMPARATIVE PHYSIOLOGY
2000; 279 (5): R1889-R1898
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
The sarcoplasmic reticulum plays a major role in isometric contraction in atrial muscle of yellowfin tuna
The Journal of experimental biology
1999; 202 (Pt 7): 881–90
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
Characterization of Ryr1-slow, a ryanodine receptor specific to slow-twitch skeletal muscle.
CELL PRESS. 1999: A302–A302
View details for Web of Science ID 000081085901766
Development of an acoustic telemetry tag for monitoring electromyograms in free-swimming fish
The Journal of experimental biology
1999; 202 (Pt 19): 2693–99
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
A new satellite technology for tracking the movements of Atlantic bluefin tuna
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
1998; 95 (16): 9384-9389
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
Cloning and characterization of fiber type-specific ryanodine receptor isoforms in skeletal muscles of fish
AMERICAN JOURNAL OF PHYSIOLOGY-CELL PHYSIOLOGY
1998; 275 (2): C401-C415
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
- The role of ryanodine receptor isoforms in the structure and function of the vertebrate triad 49th Annual Symposium of the Society-of-General-Physiologists on Organellar Ion Channels and Transporters ROCKEFELLER UNIV PRESS. 1996: 47–65
- THERMOGENESIS IN MUSCLE ANNUAL REVIEW OF PHYSIOLOGY 1994; 56: 535-577