i. sabbatical leave report - cover page - miracosta.cc.ca.us leave... · collaborative research...

J. Sepulveda Sabbatical Report

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I. Sabbatical Leave Report - Cover Page

(to be completed upon return from sabbatical leave and submitted with your report)

Attached is my comprehensive Sabbatical Leave Report. I certify that I have fulfilled the objectives of my sabbatical leave and will render the amount of

service required by District Policy – Administrative Procedure 7341. NAME: Jeanine Sepulveda DATE SUBMITTED: 2/3/12 ACADEMIC SCHOOL YEAR IN WHICH LEAVE WAS TAKEN: 2011-2012 SEMESTER IN WHICH LEAVE WAS TAKEN: Fall (NOTE: If this was a full-year leave or a variable leave, please indicate this. Do not include any unbanking as part of a sabbatical leave) CHECK (X) TYPE OF SABBATICAL LEAVE: _____ Advanced Academic Studies, or ___X__Non-Traditional Activities SIGNATURE : ______________________________________________________ (hard copy must include your actual signature on line above) Applicant should not write below this line.

APPROVALS

Title Approved? (Y/N)

Signature Date

SLC Chair

Academic Senate President

Superintendent/ President


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II. Restatement of Abstract of Sabbatical Leave Proposal

The purpose of the proposed sabbatical leave is to conduct scholarly research in the field of marine biology and to produce one or more professional presentations of the results. Upon completion of the sabbatical the results of this project will be written into a scientific manuscript to be submitted for publication. Specifically, I will participate in a collaborative research project investigating locomotor muscle function in a high-performance marine fish species, the swordfish (Xiphias gladius).

This research endeavor will quantify muscle performance in a species that tolerates extreme environmental conditions, regularly transitioning from warm surface waters of the ocean to depths greater than 1000m and temperatures below 4°C. The proposed work will provide valuable information that will help scientists better understand how physiological adaptations influence the distribution of marine species. The goal of this sabbatical is to perform field and laboratory research that will enhance my current knowledge base of the biology and ecology of marine organisms as well as that of vertebrate muscle function. Information gained from this research will be incorporated into my courses (Marine Biology and Marine Ecology), presented at professional meetings, and ultimately written into a scientific manuscript.

III. Completion of Objectives, Description of Activities

The activities performed during my sabbatical period were consistent with that described in the proposal. Documentation of the number of hours that I spent on each respective activity as well as photographs taken and the PowerPoint presentation produced are included with this report.

General overview of sabbatical project The project was separated into two objectives: the first was geared towards designing and conducting experiments which test hypotheses about swordfish muscle performance. The second phase of the project was data analysis and production of a PowerPoint presentation. In total, 21 experiments were performed successfully. Due to the opportunistic capture of a few bigeye thresher shark specimens (similar to swordfish but little is known about many aspects of their physiology), the project was expanded beyond swordfish to incorporate findings from this species as well. Although locating, capturing and working with large pelagic fishes is historically a difficult set of tasks to complete, this project was an outstanding success producing enough data to provide several preliminary conclusions about the functional mechanical design in these species. Many thanks to the PIER research team for their collaborative effort and support of this endeavor.


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Completion of Objective I - Description of activities a. Restatement of Objective I and description of the means by which objective was accomplished Obj I. Design and conduct experiments which investigate the effects of reduced temperature and oxygen availability on the in vitro contractile properties of swordfish red muscle. Activities performed to accomplish objective I comprised the bulk of my time during the sabbatical period. Activities completed fell into several categories: designing experiments, constructing and executing a sample collection protocol, preliminary dissections (prep. for experimentation) and conducting the experiments. First came the design phase. This involved coordinating the logistics of everything from specimen collection, to how the experimental equipment would be assembled, to how I would control the temperature of isolated muscle samples once dissected. I also worked closely with the PIER research team during these initial stages of design to determine how, where, when, and at what frequency swordfish samples would be collected and to devise a way to transport muscle biopsies back to the lab. Once a plan was developed for sample collection I turned my attention to assembling the apparatus that would be used to assess muscle mechanical properties. This apparatus included, among other minor equipment, a servo motor for controlling the length of muscle cells, a strain gauge force transducer, two 12V batteries placed in series, platinum electrodes, a stimulator, several voltage regulators and routers as well as a computer, oxygen tank, thermistor, set of Peltier plates for controlling the temperature of the experimental chamber, and an auxiliary cooling system for the plates (images shown in section V. of this report). To give those of you reading this report an idea of why assembling this apparatus proved to be time-consuming; I’ll offer one example of a hurdle that I needed to overcome in this process. An unpredicted voltage surge blew a transistor within a key voltage regulator in the system during set up. Diagnosing this problem took several days. While it manifested in a lack of charge being pulled from the batteries, it could have been attributed to any number of issues. Not knowing that the transistor was faulty I tried recharging the batteries, changing their connections in series, resoldering all connections to the electrodes before finally replacing the transistor and repairing the problem. Since I had difficulty identifying such problems without live tissue to work with, I performed all of these diagnostic tests using chub mackerel red muscle. The specimens used in these initial equipment tests were collected locally offshore and subsequently dissected down to small bundles of cells before being placed within the experimental chamber. Once the apparatus was set-up and working properly the next task was to design and build a cooling system for the Peltier plates that could maintain their temperature within about +/- 10 C across a range of voltages. Care was taken to properly design this system, because if the Peltier plates overheated they would no longer be operational compromising my ability to precisely control the temperature of the experimental chamber. Diagnostic tests were performed on this system as well. The implementation phase of this objective, actually conducting experiments on swordfish, began with sample collection. Sample collection entailed several trips aboard the R/V Malolo as well as time spent getting the ringers solution and gear necessary for

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sample extraction prepared for each trip. Fishing took place locally, within 30 miles off the coast of Oceanside, Ca. and used a combination of traditional harpooning and a newly PIER-developed NOAA-sanctioned deep set buoy gear to collect the specimens. Because catching fish was unpredictable, several more trips were taken than those that actually produced a specimen. Typical days at sea lasted about 10 to 12 hours each. Upon successful capture of a specimen, a muscle block was brought back to the lab for the fine-scale dissections (this is part of the “preparation for experimentation” portion of objective I in the sabbatical proposal). The goal of these dissections was to whittle each muscle block down to a bundle of about 100 to 150 cells in preparation for placement in the experimental chamber. Similar to the design phase of objective I, this activity proved to be time-consuming; each experimental bundle took between four and six hours to prepare. The first step of this activity was to determine the orientation of the muscle fibers relative to the myosepta (connective tissue). Next, to produce a bundle of viable cells with limited damage throughout, I carefully removed the exterior cells leaving the interior of the bundle intact and untouched. Even minor contact between the microdissection tools and the cells located peripherally would lead to their rupture, which would contribute to error in measurements or perhaps a nonviable bundle altogether. Lastly, I attached surgical grade silk to the myosepta on either end of each bundle. The temperature and oxygen experiments comprised a major portion of the time devoted to completion of objective I. Briefly; these experiments involved using the work loop technique to determine the optimal in vitro stimulus parameters as well as the effects of temperature and reduced oxygen on isolated muscle cell function. To do this I tethered each small muscle bundle to the lever arm of the servo motor and to the force transducer. The muscle bundle was then stimulated to contract under varying conditions of stimulus duration, strain and phase at a series of cycle frequencies at each of three temperatures (8, 16 and 24C) and under normal versus reduced oxygen. Contractile performance was quantified using the data collected in Acknowledge, a software program which records in real-time. Data from each experiment was recorded in a lab notebook. Additionally, to verify my methods as well as to gain insight into the design aspects of these experiments, I spent time performing a literature review and built a library of relevant sources. b. Description of materials produced in fulfillment of objective I: Materials produced during the completion of objective I include (1) a laboratory notebook logging details of experimental design and summary data, (2) photo-documentation of all aspects of the research from sample collection to the fine-scale dissections and work loop experiments, (3) a digital log of all hours spent on each respective activity, and (4) excel spreadsheets containing muscle performance data for all experiments performed. Additionally, my literature research resulted in the production of a library of scientific manuscripts on muscle performance and swordfish ecology. c. Total number of hours dedicated in the accomplishment of objective I: 470


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Completion of Objective II - Description of activities a. Restatement of Objective II and description of the means by which objective was accomplished Obj II. Complete the investigation by analyzing the data collected, construct an ecological model for swordfish habitat utilization based upon the locomotor implications, and build a presentation of the research for delivery at a scientific conference. Completion of objective II comprised that latter portion of my sabbatical period. First, all data files were organized into an Excel spreadsheet. Data required filtering and reorganization from its original form recorded in the Acknowledge program before it could be analyzed. Additionally, I transferred the summary data recorded in the lab notebook into Excel. Data analysis involved calculating multiple parameters related to muscle performance. The most important of these parameters included absolute and relative power outputs and the cycle frequencies at which optimal work and power resulted at each temperature. Absolute power output (measured in joules s-1) was quantified as work (force per unit length; measured in joules) as a function of cycle frequency (cyclical length changes per second; measured in Hz). Relative power output was quantified as power relative to that obtained at 1Hz cycle frequency and 16 C. To determine the optimal cycle frequencies for work and power production, both values (work and power output) calculated for each temperature of each muscle bundle were plotted as a function of cycle frequency. Finally, statistical tests were performed. Combining information gathered through experimentation with that gained from conversations with PIER researchers about swordfish movements and the local commercial swordfish industry, as well as from my literature review, I was able to construct a preliminary eco-physiological model for swordfish deep diving. In a “nut shell” what this entailed was using all of the facts gathered about swordfish movements and muscle performance to describe how they are capable of sustained and prolonged activity in the cold, oxygen-poor waters of the deep ocean. What I needed to learn before I could construct this model was (1) for what duration of time and at what frequency this species visits the cold, deep ocean, (2) whether swordfish red muscle likely maintained warmth while at depth, and (3) whether their red muscle performs positive work and power over a wide range of temperatures. What I discovered in this process of inquiry is that swordfish spend a significant amount of time (10 or more hours per day) within the cold, oxygen-poor region of the ocean. Studies of swordfish tagged with pop-off satellite archival transmitters have identified several distinct diving behaviors in this species and have shown consistency in this prolonged deep diving behavior. Additionally, swordfish are likely maintaining warmth in their red muscle for a brief period of time (relative to that spent at depth) due simply to thermal inertia as their rete is not thought to be developed enough to sustain muscle temperatures above ambient as seen in regional RM endotherms. This meant that swordfish RM does likely experience a broad temperature range while diving leading me to question whether their red muscle performs positive work and power over a wide range of temperatures. The preliminary data collected in this study suggests several consistencies between swordfish and other similarly active species. First, similar to both

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the common and bigeye thresher (regional RM endotherm and ectotherm, respectively), optimal cycle frequencies for work and power increase with temperature in swordfish RM. Second, the optimal cycle frequencies for swimming performance fell within the range of frequencies observed in other species (which ranged from 0.25 to 2.5 Hz). What was unexpected was the observation that at cold temperatures (8 C) optimal cycle frequency in swordfish was lower (at 0.25 Hz) than that seen in either the common or bigeye thresher. The significance of this finding, albeit preliminary, is that it suggests that swordfish RM does not produce significant positive work or power at this cold temperature. Furthermore, it also suggests that this species likely swims slowly at 8 C (less than a body length per second). Gut content assessments of captured swordfish have shown that they hunt squid at depth and it is assumed that they would require significant speed to do so. If future data confirms these preliminary findings, then it may be the case that swordfish hunt during the early portion of a dive during which time their muscle may still be warm enough from the heat absorbed at the surface to produce sufficient speed and power. This model for habitat utilization adds to our understanding of the unrivalled deep diving behavior of this fish species and will be incorporated into a joint scientific publication with the PIER research team in the future. In addition, because I collected bigeye thresher data as well, preliminary conclusions about their muscle performance were also made. Lastly, to communicate findings from this work a PowerPoint presentation was constructed. b. Description of materials produced in fulfillment of objective II Materials produced in the completion of objective II include (1) excel spreadsheets containing the data collected in the experiments and statistical analyses performed and (2) a PowerPoint presentation of the results of this project. c. Total number of hours dedicated in the accomplishment of objective II: 108 Total number of hours dedicated to completion of all objectives for sabbatical period: 578

IV. Contribution to District a. How this sabbatical project contributed to my professional development: Original statement:

This sabbatical leave offers me the opportunity to produce original scholarly research within my area of expertise, as well as the prospect of learning from the intellectual exchange with colleagues that are currently active in marine research. Due to the amount of time that must be devoted to this endeavor, I would otherwise not be able to participate without the block of time afforded by this sabbatical. With respect to professional development there are several areas in which this project contributes to


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instructional improvement: (1) enhancement of my discipline-specific knowledge base, (2) maintenance of my involvement in the scientific community, and (3) revitalizing my excitement for original research. First, enhancement of my discipline-specific knowledge base directly translates into instructional improvement. For example, concepts presented in marine biology often center around the physiological adaptations that enable animals to live and function in their respective niche. The swordfish offers a captivating example to illustrate how an animal has evolved to survive in extreme environmental conditions. Second, because the process of science is so heavily engrained in my courses, maintenance of my involvement in the scientific community leads to instructional improvement by offering examples based upon personal experiences and direct communication with colleagues. Lastly, refreshing my excitement for learning and engaging in science will directly translate into a renewed sense of enthusiasm for designing and implementing new investigative laboratory exercises in marine biology. I am ready and looking forward to diving into this project which directly relates to concepts taught within my discipline. Conclusions: As stated above there are several ways in which this sabbatical project contributed to my professional development. Improvement of my knowledge of the subject matter was accomplished through conversations with PIER marine biologists, through reading an extensive collection of scientific articles, and of course by way of performing the experiments. The collaborative nature of the project also allowed for the development of relationships with fellow researchers. The reciprocal exchange of ideas that took place as well as my personal experiences throughout the semester have broadened my perspectives of the biology of pelagic fishes and the impact they have on our coastal ecology. b. Short- and long-term impacts of my sabbatical leave activities on: 1) students 2) department 3) college 4) community: 1. Students:

Original statement:

I currently teach marine biology, marine ecology, and serve as an instructor for Biology 292 internship studies. What I enjoy most about my faculty position here at MiraCosta is the opportunity to encourage students to become aware of and excited about science. Thus, a major theme in all of the courses that I teach is the emphasis on knowledge gained from recent marine biological research studies, especially those conducted locally. My goals in teaching about local researchers are to convey both the methods and importance of scientific inquiry to our society as well as to get students interested and engaged in science. In order to continue to achieve these goals I feel it is necessary for me to remain an active participant in the scientific community. As such I can involve my students in the process of science by diving into the details of the study. My students will learn about the methods, challenges, and logistics of field research and gain a more realistic understanding of science than can be conveyed by reading a journal article or performing a lab exercise.

Aside from teaching my courses, I have continued throughout my time here at MiraCosta


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to seek out connections with local educational and research facilities with the goal of increasing the internship opportunities for students interested in marine biology. Participating in this collaborative project will forge new relationships that will contribute to internship opportunities in the future.

Conclusions:

As mentioned above I commonly highlight local research in my classes, the goals of which are to convey a sense of the methods used and importance of scientific inquiry to our society. Being an active part of a local research study on an economically important California marine resource has helped me to effectively achieve these goals. I have recent experiences, updated knowledge, relevant pictures to share with students as well as current literature resources to draw from to build a story that may perhaps encourage students to want to learn more about marine biology and about science in general. Furthermore, a student from the University of Massachusetts Dartmouth accompanied me throughout most of the experiments this past semester to learn about the work loop technique and its application to understanding functional mechanical design. Our journey together afforded me the added benefit of a mentorship role in this sabbatical project, one that I have learned from and view as a wonderful opportunity for personal and professional growth.

2. Department of Biological Sciences: Original statement: By updating my knowledge base within my discipline as well as gaining hands-on experience with research, I will better serve my department. With the changing field of science, keeping up to date with innovations in biological research is a key part of my contribution to the department, one that I am happy to share via presentation or collegial discussion. Additionally, our department regularly hosts guest speakers: scientists as well as members of the allied health community. Maintaining ties to the scientific community will allow me to broaden the potential speaker pool. Conclusions: I think my most valuable contribution to the biology department is in the depth and currency of knowledge within my particular area of expertise. My colleagues and I all bring to the department an understanding of general biological principles, but each of us also brings our own particular strengths; mine is marine biology. Updating and enhancing my discipline-specific knowledge base therefore adds to the collective strengths of the department. 3. College: Original statement: The experiences that our students have and the enthusiasm for learning that they develop in the classroom does not end once they leave the room. Rather, those experiences are retained and fuel inquiry in other fields and classes. I believe the college community benefits when one of its faculty members shares a renewed sense of enthusiasm for their discipline as well as an updated knowledge base.


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Conclusions: As indicated above my sabbatical experiences indeed renewed my enthusiasm for and updated my knowledge of current issues in marine biology. These experiences have also rejuvenated my passion for learning and teaching, characteristics which will benefit the college community. 4. Community: Original statement: This sabbatical project is a collaborative endeavor. As such it brings together members of the community from various institutions of higher learning. This work will offer an opportunity for intellectual exchange of ideas and teaching methodologies amongst the researchers and educators involved. Furthermore, it is my hope that by forging new relationships with local biologists/institutions, they may gain a connection to the college which may enable active participation in the mentoring and development of our students through involvement in the Internship Program. Conclusions:

Participation in this sabbatical project did indeed lead to the reciprocal exchange of ideas with colleagues from both academic and scientific institutions, thereby strengthening my ties to these communities. In addition to the impacts described in the original statement above, future, longer-term impacts on the community will be made through the eventual communication of our research findings through participation in scientific meetings and by publishing peer reviewed manuscripts.


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V. Documentation As a supplement to the documentation described below, the PowerPoint presentation constructed during completion of objective II was sent electronically to Louise McDermott, SLC Administrative Assistant along with the electronic version of this report. All hours documented below are my own invested and do not include those invested by collaborators on this project. Weekly Log of hours dedicated to each objective:

Week Obj I hours

completed

Obj II hours

completed

Description of activities

8/14/11 35 Specimen collection at-sea gear test; logistical design w/ PIER team; began assembly of exp apparatus

8/21/11 40

Chemical and dissection station prep; continued assembly of exp apparatus; troubleshoot apparatus function using mack; specimen collection trip for mack

8/28/11 41

Tested composition & O2 saturation of ringers using live tissue; more troubleshooting with mack; solved issues with exp apparatus; sword dissections using specimen caught by PIER team

9/4/11 32 Ringers & gear prep; sample collection trip; literature search; met with PIER team to reevaluate logistics

9/11/11 34 Ringers & gear prep; cooling system design; literature search; sample collection trip; caught BET & released

9/18/11 39 Bait collection trip; mack dissections; ran 3 exps using mack RM to eliminate sources of error in equipment and to verify thermal control

9/25/11 36 Ringers & gear prep; sample collection trip; BET dissections & thermal and O2 exps

10/2/11 40 Sword dissections; sword thermal and O2 exps

10/9/11 37 Ringers & gear prep; 2 sample collection trips; BET dissections & thermal and O2 exps

10/16/11 22 11 BET exps cont.; organized and transferred initial data to digital format

10/23/11 32 Ringers & gear prep; sample collection trip; literature review

10/30/11 20 12 Literature review; preliminary data analysis

11/6/11 41 Ringers & gear prep; sample collection trip; sword dissections & thermal and O2 exps

11/13/11 21 6 Finished sword exps; organized and transferred data from most recent exps to digital format

11/20/11 27 Statistical analysis and data reorganization


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11/27/11 35 Organized photo documentation; constructed ecological model; finished statistical analysis

12/4/11 17 Created PowerPoint presentation; produced figures

12/11/11 Wrapped up all "loose ends" with PIER team; cleaned up experimental equipment (none of these hours were counted in sabbatical log).

Total hrs 470 108 Abbreviations: exp = experiment; mack = chub or Pacific mackerel; BET = bigeye thresher shark; sword = swordfish; O2 = oxygen

Total hrs completed

578


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Photo-documentation The photos presented here offer documentation of collaborating researchers, activities performed and equipment used during my Fall 2011 sabbatical.

PIER team Left: S.A. Aalbers, M.S. Right: C.A. Sepulveda PhD Bottom: Xiphias gladius

R/V Malolo used for sample collection

Sample collection: Top left: Buoy gear deployment. Each set of gear contains a single baited hook. Top right: Buoy down at surface, meaning that a fish is on the line at depth. Bottom left: Searching for swordfish on R/V Malolo. Bottom right: Swordfish finning at the surface (circled). This is what we looked for on days targeting them via harpoon.

A

B

C

D Dissection station at PIER lab facility in Oceanside,

Ca. where experiments were performed. Microscope (A), cold plate (B), stimulator with

electrodes (C) and light (D) are shown.


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Dissections: Top left shows red muscle blocks before being dissected down to a bundle of about 100 cells (shown on bottom right with silk attached). Top Right: Dissections lasted several hours and were performed immediately after returning from a sample collection trip. Bottom left: Ashley (student collaborator from University of Mass. Dartmouth) learning the dissection techniques.

0

A

B C

D

E

F

G H

I

J

Experimental apparatus: (A) microscope, (B) stimulator, (C) force transducer controller, (D) servo motor, (E) experimental chamber, (F) power supply, (G) Peltier plate cooling system, (H) oxygen supply, (I) voltage regulator, (J) platinum electrode within experimental chamber. Muscle bundle is attached to servo motor lever arm (left) and force transducer pin (right). Peltier plates are hidden beneath experimental chamber.

Data collection: real-time data acquisition software (left) and

in my lab notebook (right).


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Scientific literature reviewed during sabbatical period:

To refresh and update my knowledge of swordfish ecology and fish muscle physiology I performed a literature review during the sabbatical period. This review allowed me to gain insight into the design elements of the experiments performed for objective I and entailed researching, reading, and then writing a brief summary of key details of each article. The review was performed on days in which fishing and experimentation were not taking place and includes the following articles organized alphabetically by topic. Cartamil, D., N. C. Wegner, S. Aalbers, C. A. Sepulveda, A. Baquero, J. B. Graham (2010) Diel movement patterns and habitat preferences of the common thresher shark (Alopias vulpinus) in the Southern California Bight. Marine and Freshwater Research 61, 596-604. Dewar, H., E. Prince, M. K. Musyl, R. Brill, C. Sepulveda, J. Luo, D. Foley, E., Orbesen, M. Domeier, N. Nasby-Lucas, D. Snodgrass, R. M. Laurs, J. P. Hoolihan, B. A. Block, L. M. McNaughton (2011) Movements and behaviors of swordfish in the Atlantic and Pacific Oceans examined using pop-up satellite archival tags. Fisheries Oceanography 20, 219-241. Heberer, C., S.A. Aalbers, D. Bernal, S. Kohin, B. DiFiore, C.A. Sepulveda (2010) Insights into catch-and-release survivorship and stress-induced blood biochemistry of common thresher sharks (Alopias vulpinus) captured in the southern California recreational fishery. Fisheries Bulletin 106, 495-500. Nakano, H., H. Matsunaga, H. Okamoto, M. Okazaki, M. (2003) Acoustic tracking of bigeye thresher shark Alopias superciliosus in the eastern Pacific Ocean. Marine Ecology Progress Series 265, 255–261. Sepulveda, C.A., A. Knight, N. Nasby-Lucas, M. Domeier (2010) Fine-scale movements of the swordfish Xiphias gladius in the Southern California Bight. Fisheries Oceanography 19, 279-289. Weng, K. C., B. A. Block (2004) Diel vertical migration of the bigeye thresher shark (Alopias superciliosus), a species possessing orbital retia mirabilia. Fishery Bulletin 102, 221-229. Altringham, J. D., D. J. Ellerby (1999) Fish swimming: Patterns in muscle function. Journal of Experimental Biology 202, 3397-3403. Altringham, J. D., I. A. Johnston (1990) Scaling effects on muscle function: Power output of isolated fish muscle fibres performing oscillatory work, Journal of Experimental Biology 151, 453-467. Altringham, J. D., C. S. Wardle, C. I. Smith (1993) Myotomal muscle function at different locations in the body of a swimming fish. Journal of Experimental Biology 182, 191-206. Bernal, D., J. M. Donley, D. G. McGillivray, S. A. Aalbers, D. A. Syme, C. Sepulveda (2010) Function of the medial red muscle during sustained swimming in common thresher sharks: contrast and convergence with thunniform swimmers. Comparative Biochemistry and Physiology Part A 155, 454-463.


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Blake, R. W. (2004) Fish functional design and swimming performance. Journal of Fish Biology 65, 1193-1222. Coughlin, D. J. (2002) Aerobic muscle function during steady swimming in fish. Fish and Fisheries 3, 63-78. Dickinson, M. H., C. T. Farley, R. J. Full, M. A. R. Koehl, R. Kram, S. Lehman (2011) How animals move: An integrative view. Science 288, 100-106. Donley, J. M., R. E. Shadwick, C. A. Sepulveda, D. A. Syme (2007) Thermal dependence of contractile properties of the aerobic locomotor muscle in the leopard shark and shortfin mako shark. Journal of Experimental Biology 210, 1194-1203. Guderley, H. (2004) Metabolic responses to low temperature in fish muscle. Biological Review 79, 409-427. Johnston, I. A., G. K. Temple (2002) Thermal plasticity of skeletal muscle phenotype in ectothermic vertebrates and its significance for locomotory behavior. Journal of Experimental Biology 205, 2305-2322. Katz, S. L. (2002) Design of heterothermic muscle in fish. Journal of Experimental Biology 205, 2251-2266. Portner, H. O. (2002) Physiological basis of temperature-dependent biogeography: trade-off in muscle design and performance in polar ectotherms. Journal of Experimental Biology 205, 2217-2230. Rome, L. C., A. Sosnicki, I. Choi (1992) The influence of temperature on muscle function in fast swimming scup II. Mechanics of red muscle. Journal of Experimental Biology 163, 281-295. Rome, L. C., D. M. Swank, D. J. Coughlin (1999) The influence of temperature on power production during swimming II. Mechanics of red muscle fibres in vivo. Journal of Experimental Biology 202, 333-345. Bograd, S. J., C. G. Castro, E. D. Lorenzo, D. M. Palacios, H. Bailey, W. Gilly, F. P. Chavez (2008) Oxygen declines and the shoaling of the hypoxia boundary in the California Current. Geophysical Research Letters 35, L12607. Hoppeler, H., M. Vogt (2001) Muscle tissue adaptations to hypoxia. Journal of Experimental Biology 204, 3133-3139. Seibel, B. A. (2011) Critical oxygen levels and metabolic suppression in oceanic oxygen minimum zones. Journal of Experimental Biology 214, 326-336. Sepulveda, C. A., N. C. Wegner, D. Bernal, J. B. Graham (2005) The red muscle morphology of the thresher sharks (family Alopiidae). Journal of Experimental Biology 208, 4255-4261.


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N. C. Wegner, C. A. Sepulveda, J. B. Graham (2006) Gill specializations in high-performance teleosts, with reference to striped marlin (Tetrapturus audax) and wahoo (Acanthocybium solandri). Bulletin of Marine Science 79, 747-759. N. C. Wegner, C. A. Sepulveda, K. B. Bull, J. B. Graham (2010) Gill morphometics in relation to gas transfer and ram ventilation in high-energy demand teleosts: scombrids and billfishes. Journal of Morphology 271, 36-49.

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