simulated human diving and heart rate - swarthmore college

27:130-145, 2003. doi:10.1152/advan.00045.2002 Advan Physiol EducSara M. Hiebert and Elliot Burch RESPONSE AS A LABORATORY EXERCISE RATE: MAKING THE MOST OF THE DIVING SIMULATED HUMAN DIVING AND HEART

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SIMULATED HUMAN DIVING AND HEART RATE:MAKING THE MOST OF THE DIVING RESPONSE

AS A LABORATORY EXERCISE

Sara M. Hiebert1 and Elliot Burch2

1Biology Department, Swarthmore College, Swarthmore, Pennsylvania 19081; and2Science Department, The Putney School, Putney, Vermont 05346

Laboratory exercises in which students examine the human diving response are

widely used in high school and college biology courses despite the experience

of some instructors that the response is unreliably produced in the classroom.

Our experience with this exercise demonstrates that the bradycardia associated with

the diving response is a robust effect that can easily be measured by students without

any sophisticated measurement technology. We discuss measures that maximize the

success of the exercise by reducing individual variation, designing experiments that

are minimally affected by change in the response over time, collecting data in

appropriate time increments, and applying the most powerful statistical analysis.

Emphasis is placed on pedagogical opportunities for using this exercise to teach

general principles of physiology, experimental design, and data analysis. Data col-

lected by students, background information for instructors, a discussion of the

relevance of the diving reflex to humans, suggestions for additional experiments, and

thought questions with sample answers are included.

ADV PHYSIOL EDUC 27: 130–145, 2003;10.1152/advan.00045.2002.

Key words: diving reflex; bradycardia; experimental design

When mammals dive, they must cope with the prob-lem of being denied an external source of oxygen.Consummate divers such as the remarkable Weddellseal may remain submerged for up to two hours. Todo so, they rely on anatomical features and physiolog-ical responses that increase oxygen storage whilereducing the use of oxygen for nonessential activitiesduring a dive. Blood vessels supplying nonessentialorgans are constricted, redirecting blood to the oxy-gen-requiring brain and heart. Because it is supplyingfewer organs with blood, the heart can beat moreslowly (a condition known as bradycardia) whilemaintaining adequate blood pressure to the brain, themost metabolically sensitive organ; a further benefitof bradycardia is that the heart requires less oxygen as

well. Diving bradycardia is an easily measured com-ponent of a group of reflexes that also include holdingthe breath (apnea) and peripheral vasoconstriction.Together these reflexes constitute the “diving re-sponse.”

In comparison with diving mammals, humans arepoorly adapted to life in the water. In 2002, free-diving champion Mandy-Rae Cruikshank set a wom-en’s world record for static apnea of 6 minutes 13seconds (the men’s record, set in 2001 by Scott Camp-bell, is 6 minutes 45 seconds), but most of us arecomfortable holding our breaths for less than aminute. The first part of this laboratory exercise isdesigned to demonstrate that, despite our terrestrial

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nature, humans experience bradycardia when simu-lating a dive by holding the breath and immersing theface in cold water. The second part of this investiga-tory exercise asks students to consider the cues thatstimulate the bradycardia reflex. In common par-lance, this question might be phrased “how does thebody ’know’ that it is diving?” As biologists, we mightrestate this question as “what are the proximate sig-nals that trigger diving bradycardia?” The simulateddive holds several potential proximate cues: 1) apneaand 2) exposure of the face to cold water, which maybe further broken down into several componentsincluding cold, wetness, and pressure. The goal of thesecond part of the exercise is to determine which ofthese cues triggers diving bradycardia.

Human diving experiments have been used widely inthe classroom (5, 6) and have gained popularity as aninvestigative laboratory activity, although some in-structors have found that the diving response is un-reliably replicated in the classroom. On the basis ofeight years of experience with this exercise, we sug-gest ways to improve student success and elaborateon ways of expanding the pedagogical potential ofthis exercise, which can be used successfully at avariety of levels of biology instruction. Instructorsmay wish to use it primarily as a means of teachingthe scientific method of inquiry, with relatively littleattention to the details of diving physiology or theintricacies of statistical analysis. The exercise can alsobe rendered suitable for more advanced students byincorporating more physiological information and us-ing formal statistical analysis. In all contexts, we rec-ommend that the instructor demonstrate the simu-lated dive to the class before beginning the exercise.In our experience, a dripping instructor is the singlebest introduction to this activity, inviting students toparticipate and letting them know that everyone inthe classroom is engaged in discovery together.

METHODS

Equipment and Supplies

1 plastic basin per student1 towel per studenttap waterice1 thermometer per groupface masks

1 snorkel per student (can use large diameter plastictubing)1-pint plastic storage bags or gel packs that have beenkept in the freezerbleach for sterilizing basins between uses by differentstudentsstatistical analysis softwareIf measuring pulse manually:1 stopwatch per groupIf using computer-aided heart rate monitoring system:1 monitoring device per groupsoftware set up to collect average heart rates overintervals of 15 s

Procedures

Basic protocol for all tests. All tests are conductedin the same posture: leaning over the lab bench withelbows resting on the lab bench and the head down.

Students should work in groups of three. Each stu-dent takes a turn being the experimental subject,taking the pulse (or operating the data collectionsoftware if using an electronic heart rate monitor),and watching the time.

To measure the radial pulse manually: with the sub-ject’s palm facing upward, follow the thumb to itsbase and continue 2.5 cm (1 in.) beyond the wrist.Use the index and middle fingers to locate the groovebetween the radial bone (the long bone on the sameside as the thumb) and the tendon that runs parallel tothe radial bone. Press the fingers gently, slidingslightly up or down in the groove to locate the pulsein the radial artery. Fat deposits in the wrist may makeit more difficult to find the pulse in some individuals.

Each test lasts 30 s. Most students will be able to holdtheir breath this long without too much trouble butshould always stop anytime they experience discom-fort. Test subjects will appreciate being tapped on theback every 10 s by the timer, particularly when beingasked to hold their breath, because it is easy forsubjects to lose track of time during the test. In ourclassroom, tapping helped students to remain calmduring the test because they had a better idea of whenthe 30-s test period would end.




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At the beginning of a test that requires holding thebreath, students should take a deep but not maximalbreath and then hold it. Students should not hyper-ventilate before holding their breath.

Before conducting any test using water, studentsshould measure the temperature of the water andadjust it by adding warm tap water or ice. Temp-erature should be 15°C for the initial simulateddive.

For immersion tests, subjects should immerse the faceup to the temples.

Allow several minutes for heart rate to return to nor-mal between tests.

Student-designed experiments: pairs of test con-ditions for evaluating proximate cues. Havingdemonstrated that diving bradycardia exists in hu-mans, students are asked to discover what proximate

Table 1Experiments for testing the effect of major components of a simulated dive on HR

Test(Independent)

Variable

Exp.no.

Compare These Test Conditionsa Difference in HR Between TheseTwo Test Conditions Indicates

Comparisons Between Experiments

Simulated dive 1 Breathing in air vs.holding breath in cold waterb

Effect of all components of simulateddive on HR

Apnea(holdingbreath)

2 Breathing in air vs.holding breath in air

Effect of apnea alone on HR Apnea in presence of cold watershould result in lower HR thanapnea alone. Difference in HRreduction between experiments 2and 3 indicates additive effect ofcold water on HR reduction byapnea.

3 Breathing in water with snorkel vs.holding breath in cold waterb

Effect of apnea in presence of coldwater on HR

Facialimmersion

4 Breathing through snorkel in air vs.breathing through snorkel inwaterb

Effect of cold water submersion onHR

Cold water submersion in presence ofapnea should result in lower HRthan cold water submersion whilebreathing. Difference in HRreduction between experiments 4and 5 indicates additive effect ofapnea on HR reduction by coldwater submersion.

5 Holding breath in air vs.holding breath in cold waterb

Effect of cold water submersion inpresence of apnea on HR

Temperature 6 Warm pack on foreheadc vs.cold pack on foreheadc

Effect of temperature on HR. Notethat this set of treatments fails toremove any additive effects thatpressure might have on HRreduction by exposure to cold

Difference in HR reduction betweenexperiments 6 and 7 indicatesadditive effect of wetness on HRreduction by cold.

7 Breathing in warmd water withsnorkel vs. breathing in coldd

water with snorkel

Effect of temperature on HR inpresence of water (wetness andpressure)

Difference in HR reduction betweenexperiments 7 and 8 indicatesadditive effect of apnea on HRreduction by cold.

8 Holding breath in warmd water vs.holding breath in coldd water

Effect of temperatue on HR inpresence of both water (wetnessand pressure) and apnea

HR, heart rate. aEach pair of conditions constitutes a separate experiment. bWater at 15°C. cSee ADDITIONAL EXPERIMENTS for other ideas ontesting the role of the forehead. dWater at temperature students wish to test. Note that, in very warm water, students may find difficultyholding their breath.




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cues stimulate the decrease in heart rate. Potentialproximate cues can be evaluated with a series ofpaired experiments (Table 1). Note that some vari-ables can be investigated with more than one set oftest conditions; each of these tests yields slightly dif-ferent information, and consideration of several ex-periments together can yield further information notrevealed by tests considered separately.

Large diameter flexible plastic tubing may be used asan inexpensive snorkel. For temperature tests in air,use a frozen gel pack or plastic freezer bag filled withwater of !5°C [Below this temperature, cold on theface may cause an increase in heart rate (1); gel packsare usually coated with cloth, so they don’t feel ascold even if they have been stored in the freezer].Between use by different students, basins and snor-kels should be disinfected with a mild bleach solution(5 ml bleach/liter of water) to prevent the spread ofinfection. In a 3-h laboratory session that includestime for discussion and experiment design, collegestudents are typically able to carry out a total of fourexperiments—the initial demonstration that the bra-dycardia reflex exists plus three student-designedtests of proximate cues.

General considerations for conducting maxi-mally effective experiments. The basic testing pro-cedure (above) and the additional recommendationsbelow maximize the success of the exercise by con-trolling for 1) individual variation in basal heart rate,2) learning or habituation during the exercise, and 3)other changes that might take place in an individual’sheart rate over the course of several hours [or be-tween days, if the exercise occupies more than onelaboratory period (21)].

The exercise should consist of a series of experi-ments, each comprising two test conditions (Table 1).Identical tests in different experiments (e.g., apneawith immersion in experiments 1, 3, 5, and 8 or apneain air in experiments 2, 5, and 6) may yield variableresults, even within the same individual. Several stud-ies have shown that the response of heart rate tosimulated diving can change over time as the subjectbecomes habituated to the procedure (21, 24, 26).This is one of the reasons that pairs of tests, con-ducted close to each other in time and in randomized

order, are the best controls and yield the strongestand most easily interpreted results. Although compar-ing several test conditions with a single control mayappear to save time in the classroom, this approachwould require a more complex statistical tool (analy-sis of variance, or ANOVA) and would require that theorder of all tests, including the control, be random-ized among subjects to control for time-dependenteffects such as habituation.

A single paired t-test should be used to compare heartrates from the two test conditions in the 15- to 30-smeasurement period (Fig. 1). Data from experiments2–8 (see Table 2) illustrate the importance of thispoint. Making more than one comparison within anexperiment requires more advanced statistical tools—ANOVA or Bonferroni-corrected t-tests—which areinappropriate for the beginning student. In the eventthat the distribution of the data is significantly non-normal, the nonparametric Wilcoxon matched pairstest, which makes no assumptions about the distribu-tion of the data, should be substituted for the pairedt-test.

To make use of paired t-tests, each student mustcomplete both test conditions in each experiment,and data must be compiled so that pairs of resultsfrom each student are kept together (for instructionson how to format data, see instructions accompany-ing your statistical analysis software).

Order effects should be controlled for within eachexperiment by instructing one-half of the groups inthe class to perform the test conditions in one orderand the remaining groups in the reverse order.

Throughout, remind students that they should remainas quiet as possible. Published studies are usuallyconducted on subjects who have been resting quietlyfor up to 30 min, often in a prone position (e.g.,Refs. 21 and 24). Additional studies have shownthat distraction may reduce or eliminate diving bra-dycardia (reviewed in Ref. 14). In our experience,boisterous students tend to generate data that fail toshow some of the expected features of the divingresponse.




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When individual classes are small or there is consid-erable variability among the responses of students,pooling data from several classes or laboratory sec-tions can provide sufficient data to show the effectsthat are described in this report and in the literature.

If possible, practice the immersion procedure in ad-vance of the diving exercise to reduce anxiety and theconsequent tachycardia that can obscure the brady-cardia reflex (10, 26).

SAMPLE RESULTS

For sample results, see Table 2.

DISCUSSION: INTERPRETING THE SAMPLERESULTS

What the Results Tell Us About the BradycardiaReflex

All numerical analyses refer to data shown in Table 2for the 15- to 30-s measurement period unless other-wise noted.

Experiment 1: simulated dive. Experiment 1 dem-onstrates that the full bradycardia reflex exists inhumans, with an average heart rate reduction of 20beats/min (76 beats/min at rest to 56 beats/min dur-

FIG. 1.Use of controls and statistical tests. Schematic representation of what each sta-tistical comparison can tell us about the effect of an independent variable (e.g.,apnea, facial immersion, or cold on the face) on the dependent variable, heartrate (HR). The same principles apply to measurements taken in successive timeperiods or taken before and after a treatment (sometimes referred to as “baseline”and “experimental” measurements, respectively). Control and test groups ofmeasurements must be compared at the same time period in the experiment,because the control may change over time (because of learning, habituation,circadian rhythms, or other time-dependent effects). The purpose of the controlis to allow us to subtract these purely time-dependent effects from the totalchange to reveal the effect of the independent variable itself. Thus only compar-ison C answers the question of whether the independent variable influences heartrate in the second measurement period.




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ing the dive; Fig. 2B). This result matches that ofReyners et al. (21) for apneic subjects with a coldpack pressed against the face, which suggests thatapnea and cold facial stimulation are sufficient to

elicit the full diving response. This experiment alsoshows that diving bradycardia does not develop im-mediately, but becomes more pronounced with time(10, 20, 24) (Fig. 2, A and B).

Table 2HRs pooled from diving reflex experiments conducted by 5 laboratory sections of introductory college biology students

measuring radial pulse manually. Students had had no prior experience with the lab procedurebefore beginning experiment 1

Test (Independent) VariableExp.no.

Measurement Period

n

0–15 s 15–30 s Averaged over 0–30 s

AvgHR

Avgdecr

inHR

Significance/type of t-test

AvgHR

Avgdecr

inHR


AvgHR

Avgdecr

inHR


Simulated dive (breathing in air vs.apnea in cold water)

1 79.85.8

‡2-samp. 76.019.9

§2-samp. 77.912.9

§2-samp.101

74.0 ‡paired 56.1 §paired 65.0 §paired

Apnea In air (breathing in airvs. apnea in air)

2 73.01.6 NS

70.14.9

*2-samp. 71.63.3 †paired 60

71.3 65.2 ‡paired 68.3

In water (snorkel inwatervs. apnea in coldwater)

3 68.5

2.5 NS

65.3

10.3

*2-samp. 66.9

6.4

*2-samp

3466.0 54.9 §paired 60.5 ‡paired

Facialimmersion

Breathing (snorkel inairvs. snorkel in coldwater)

4 74.8

4.2 ‡paired

71.2

4.9 *paired

73.0

4.6 ‡paired 4671.1 66.9 68.0

With apnea (apnea inairvs. apnea in coldwater)

5 71.7

2.7 *paired

69.6

8.2

§2-samp. 70.7

5.4

‡2-samp.

6469.0 61.5 §paired 65.2 §paired

With apnea (apnea inairvs. apnea in RTwater)

6 71.7

3.1 NS

70.5

9.8 *paired

71.1

6.5 NS 1368.6 60.6 64.6

Temperature In air (RT pack onforeheadvs. cold pack onforehead)

7 71.8

2.4 NS

69.7

2.8 *paired

70.7

2.6 *paired 4469.3 67.0 68.1

In water (apnea inwarm watervs. apnea in coldwater)

8 70.1

0.9 NS

65.5

7.1

†2-samp. 67.8

4.0 §paired 3969.2 58.5 §paired 63.8

Average HRs (beats/min) are shown for the 2 treatments described for each experiment in column 2; n ! no. of students participating in eachexperiment. RT, room temperature, 23°C. *P " 0.05; †P " 0.01; ‡P " 0.005; §P " 0.0001. Only tests with statistically significant results areshown.




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Experiments 2 and 3: effect of apnea. Experi-ments 2 and 3 demonstrate that apnea itself can causebradycardia, even in the absence of immersion (simi-lar results in Ref. 26). Experiment 3 demonstrates thatthe degree of bradycardia caused by apnea is approx-imately doubled when the subject’s face is immersed[a similar result was obtained by Gross et al. (15)andZbrozyna and Westwood (26)]. Note that this exper-iment isolates the effect of apnea because in bothtests the subject is immersed. In this experiment, one

of the test conditions is actually the simulated dive-apnea in cold water, and the result of this test is aheart rate that closely matches the heart rate mea-sured during the simulated dive in experiment 1, #55beats/min. According to experiment 3, approxi-mately one-half of the heart rate reduction during thesimulated dive in experiment 1 is caused by apneaenhanced by the additive effect of immersion in coldwater. This result implies that the remainder of the 20beats/min decrease in heart rate during the simulateddive is due to the effect of being immersed in coldwater (a separate effect from the enhancing effect ofimmersion on apnea); this explains why facial immer-sion in cold water while breathing through a snorkelreduces heart rate to 65 beats/min, #10 beats/minbelow the resting control in experiment 1. This con-clusion is also addressed by experiment 5 and dis-cussed in that section.

Experiments 4, 5, and 6: effect of immersion inwater. Experiments 4, 5, and 6 are designed to testthe effect of immersing the face in water. Experiment4, which controls for the effect of apnea by allowingthe subject to breathe in both test conditions, showsthat facial immersion alone significantly decreasesheart rate, by #5 beats/min. Experiment 5 also con-trols for apnea, this time requiring the subject to holdhis/her breath both in air and when the face is im-mersed in cold water. The interesting result of thisexperiment is that immersion is found to decreaseheart rate significantly and, furthermore, that apneaincreases the bradycardia due to immersion. Just asimmersion has an additive effect on heart rate reduc-tion by apnea (experiment 3), so too does apnea havean additive effect on heart rate reduction by immer-sion in cold water. The decrease in heart rate due toimmersion in the presence of apnea is 8 beats/min,which, when added to the 10 beats/min reductioncaused by apnea in the presence of immersion, isclose to the total reduction of 20 beats/min caused bythe simulated dive. To resolve the appearance thateffects are being “double counted” in this reckoning,it is important to recognize that, for each experiment,we are primarily interested in the difference in heartrate between the two treatments. In experiment 5,the difference of 8 beats/min is that caused by immer-sion in cold water with apnea; the control condition,apnea in air, already shows a lower heart rate (#70beats/min) than breathing in air (76 beats/min), be-

FIG. 2.Mean HRs in beats/min [bpm; !95% confidence inter-val (CI)] in college students of both sexes during asimulated dive (apnea with facial immersion in 15°Cwater) compared with control condition of breathingin air. A: data from 1 laboratory section, showing thatsignificant differences were present only in 15- to 30-smeasurement. B: pooled data from 5 laboratory sec-tions showing that, when sample size is increased,smaller but nevertheless significant differences mayalso be present in 0- to 15-s measurement. CI indicates95% certainty that population mean lies within thisrange; thus, if two 95% CIs do not overlap, a 2-samplet-test would show a significant difference, with P <0.05 (similarly, if two 99% CIs do not overlap, there isa significant difference, with P < 0.01). This type ofgraph is an effective visual representation of how the2-sample t-test works. Note, however, that P valuesshown here are for a paired, rather than 2-sample,t-test, because the paired t-test is better suited for thepaired data the students collected. This graphic pre-sentation is therefore good for showing mean HRsand how they change during the experiment, but stu-dents should be aware that it does not correspondconceptually with the paired t-test. See Fig. 3 forgraphic representation of how the paired t-test works.




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cause apnea itself depresses heart rate as previouslydemonstrated in experiment 2. The additional de-crease of 8 beats/min beyond the reduction in heartrate already shown by the control tells us that thisadditional effect is due to immersion. The same logicmay be applied to experiment 3, in which the 10beats/min reduction in heart rate relative to the con-trol (i.e., the reduction due to apnea) is above andbeyond the reduction already shown by the water-immersed control (65.3 beats/min pm) relative tobreathing in air (76 beats/min, experiment 1).

One laboratory section wished to isolate the effects ofwater (wetness, greater pressure than air) as separatefrom the effects of the water’s temperature (experiment6). Noting that the temperatures of air and water inexperiment 1 were different, they attempted to controlfor temperature by comparing apnea in air and in waterof the same temperature (23°C). Although their inten-tions were good, they failed to consider the fact thatwater and air of the same temperature usually havedifferent thermal effects on an organism. Heat is lost towater at 23°C more rapidly than to air at 23°C, becausewater has a higher conductance than air (in addition,water colder than the skin ultimately extracts more heatthan air because of its higher specific heat). These dif-ferences in conductance and specific heat are reflectedin the well-known experience that 23°C water feelscooler than 23°C air. Experiment 6 showed that immer-sion in 23°C water resulted in about the same reductionin heart rate as immersion in cold water, a result thatcontradicts the findings of experiments 7 and 8. Note,however, that the sample size in this experiment wassmall; even though the qualitative result that watercauses bradycardia is unlikely to change, a larger groupof subjects would give us greater confidence in themagnitude of the temperature effect.

Experiments 7 and 8: effect of temperature. Aswith apnea and water, there are several ways of test-ing for the effect of temperature. Experiment 7 teststhe effect of temperature on the forehead (the loca-tion of the ophthalmic branch of the trigeminalnerve) in the absence of the other qualities of water(e.g., wetness, pressure). Although the reduction inheart rate due to an ice pack is not large (3 beats/min),it is weakly significant [similar to results of Allen et al.(1)]. We have noted in past years, however, that thisexperiment often does not yield significant results ex-

cept when data from several laboratory sections arepooled. Some studies indicate that forehead cooling mayresult in a transient (or at very low temperatures con-stant) tachycardia (6, 10, 26). Like experiment 3, exper-iment 8 demonstrates that the effect of temperature ispotentiated by the presence of water to result, in thiscase, in a 7 beats/min reduction in heart rate over awater temperature range of 8°C (15–23°C), consistentwith findings summarized by Gooden (14). In light ofthe discussion regarding experiment 6, it might be use-ful to test 15°C water against water in the thermoneutralzone, 34–35°C (14, 19), to attempt to isolate tempera-ture from wetness and pressure.

ADDITIONAL EXPERIMENTS

Below are listed some additional avenues along whichstudents might wish to investigate diving bradycardia.Or, instead of actually performing the experiments,students might be asked to design experiments, as athought exercise, to test these ideas.

Water as a cue. What are the critical components ofwater immersion for the bradycardia reflex, otherthan temperature (e.g., pressure, wetness)? Althoughsome authors have concluded that temperature is theonly relevant component of facial immersion stimu-lating diving bradycardia, other studies suggest thatwetness may be a factor (14). One laboratory sectionat Swarthmore College designed the following exper-iment. Heart rate during immersion with apnea wascompared with heart rate during immersion with ap-nea when a plastic-wrap barrier separated the facefrom the water. The experiment proved too difficultto execute with manual pulse measurement but mightbe possible with electronic pulse monitors.

Location of skin sensors. Is the forehead critical insensing the presence of cold water? Students mightaddress this question by comparing immersion with andwithout a face mask or by comparing full-face immer-sion with immersion of only the mouth and nose. Theymight also compare immersion of the face with immer-sion of some other body part, such as a hand or foot.

Sex differences. Do males and females have differ-ences in heart rate, and do they respond differently tofacial immersion?




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Training effect. Trained divers report that trainingextends their breath hold time and deepens the divingresponse, resulting in greater bradycardia during adive. Students may wish to compare bradycardiaachieved by trained swimmers/divers with thatachieved by others in the class in response to simu-lated diving. Students may also wish to determinewhether individuals can achieve greater bradycardiaby habituation or “short-term training” [try five 30-simmersions, 2 min apart (24)] or by training overlonger periods of time (days or weeks). They may alsowish to determine whether repeated immersionshave a greater effect on trained athletes than on otherstudents; some authors suggest that the increase inbreath-holding ability and bradycardia after short-termtraining can be used as a general indicator of cardio-vascular health (reviewed in Ref. 24). In interpretingthe results of this experiment, students should beaware that any changes that occur after repeatedimmersions may have both physiological and psycho-logical components [e.g., reduced anxiety (26)].

Anticipatory effects. Diving mammals may begin acardiovascular diving response just before they actu-ally dive (8), and their response while diving may alsochange depending on when they anticipate resurfac-ing. Diving bradycardia may begin to disappear as theanimal rises toward the surface at the end of a dive. Inhumans, however, the anticipatory response before adive begins may be tachycardia rather than bradycar-dia (24). To examine anticipatory effects, the subjectshould first rest for some period of time (2 min)without knowing what the next test condition will be(order of test conditions is randomized so that sub-jects cannot predict what they will experience next).The test condition is then announced and another30 s allowed to elapse before the subject undergoesthe announced test condition. Heart rates during the30-s anticipation period are then compared betweenthe test conditions.

Psychological control. Diving heart rate in divingmammals is a function of whether or not the subjectknows it can resurface (see BACKGROUND INFORMATION FOR

INSTRUCTORS). In humans, a sense of control, or lackthereof, can also affect the development of divingbradycardia (12). Students might compare heart ratesnear the end of a simulated dive between subjectswho are given no time cues (never tapped on the

back during the dive or told the time) and those whoknow when the dive will end because they receivecontinual verbal or tactile cues from a group member.

Lung volume. Does the size of the breath taken beforeimmersion affect 1) how long the breath can be heldduring a simulated dive and 2) bradycardia during asimulated dive? Andersson and Schagatay (2) found thata breath of 100% lung volume (i.e., the deepest breathpossible) produced the longest dives but the least divingbradycardia, whereas a breath of 60% lung volume pro-duced the shortest dives but the most pronounced bra-dycardia. Note: We recommend against student investi-gations on the effect of hyperventilation becausehyperventilation may result in black-out.

Mental effects. Does performing mental arithmeticduring a simulated dive reduce bradycardia, as re-ported in one study (11)?

PRECAUTIONS IN STUDIES USING HUMANSUBJECTS

Experiments using human subjects should be clearedwith your institution’s research committee, whichmay include a separate human subjects section, be-fore using the exercise in your classroom. Studentsneed to know that their participation in the exerciseis optional and that the exercise is in no way anendurance contest (6). Students should not try to holdtheir breath longer than is comfortable, and anyonewith a heart arrhythmia disorder should not partici-pate (19). Note that, because some of the experi-ments do not involve apnea or immersion, studentshaving difficulty with this portion of the exercise canstill participate in some experiments and contributeto data collection by the class. In our experience, thepercentage of students unwilling or unable to partic-ipate is typically low. We have found, however, thatstudents who have little swimming experience mayfind facial immersion challenging.

GENERAL PRINCIPLES THAT CAN BE TAUGHTWITH THIS LABORATORY EXERCISE

Transferable general principles are arguably the mostvaluable, and best remembered, content of any labo-ratory exercise. Instructors are encouraged to drawattention to the following general principles, demon-strated by the diving bradycardia exercise, and to




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remind students when they recur in later lectures orlaboratory exercises.

A physiological response is the product of bothultimate and proximate factors. Ultimate factorsare those that lead to positive natural selection for atrait, whereas proximate factors refer to the mecha-nism by which the response is brought about withinan individual. The difference between these two kindsof causation represents a central concept in biologicalthought, articulated by an unidentified author when heposed the question “Why is a house?” and recognizedthat there are two classes of answers: 1) “because manneeds shelter” (ultimate cause) and 2) “because man laidbrick on brick” (proximate cause).

Biological data are inherently messy, even whenmeasurement is precise. Individuals vary in theirresponses to any given perturbation, as may be shownby asking students to plot the data from individuals inthe class (Fig. 3). Statistical analysis was invented so thatwe can see beyond this individual variation to significantpopulation trends. It is worth noting that this variation,if heritable, is the variation on which natural selectionacts; without it, there would be no evolution.

A control for any test condition is the test con-dition minus the independent variable you areinterested in testing. Many students (and many sci-ence teachers!) erroneously believe that a control isthe subject, in their words, “with nothing” or “doingnothing.” On the contrary, the control treatmentshould match every feature of the test conditionexcept for the independent variable being tested. Forexample, each of the three experiments that test theeffect of immersion in water (experiments 4, 5, and 6;Table 2) has two test conditions that are identical exceptthat one includes immersion in water and the other doesnot. Although breathing in air (which might be consid-ered the subject “doing nothing”) is the appropriatecontrol for experiments 1 and 2 (Table 2), it is not agood control for the other experiments (not even ex-periment 4, which is better controlled by having thesubject breathe through a snorkel in air).

Experiments can be properly controlled withouthaving a particular test condition or group ofsubjects designated as the control. Experimentstesting the effect of temperature always simply com-

pare two or more temperatures, because there is nosuch condition as “no temperature.” As long as thetest conditions being compared are identical to oneanother except for the temperature chosen, the ex-periment is well controlled. As the experiments inthis exercise demonstrate, it is also not necessary forone group of subjects to be the control group; if allsubjects undergo all test conditions and the order inwhich they experience the test conditions is random-ized, then the experiment is controlled.

Only by comparison with a control can we dem-onstrate that a change is due to the independentvariable. The importance of this point cannot be

FIG. 3.HRs of college students in 1 class (n " 13) performingsimulated dives with apnea in water at 2 temperatures.A: each line connecting 2 points (F) represents datafrom 1 subject; !, displaced right or left for clarity,represent mean HR of all subjects ! 95% CI. A 2-sam-ple t-test would compare these 2 means; because thereis overlap between the 95% CIs of the 2 means, onecould not conclude that there is a significant differencebetween them with P < 0.05. Note, however, that al-though absolute HRs varied widely among individuals,the HR of most individuals increased from 15 to 23°C. B:in this graphic representation of the data as viewed fromthe perspective of the paired t-test, the mean of all theindividual differences between the 2 temperatures isshown with its 95% CI. The null hypothesis, that there isno difference in HR between the 2 temperatures, wouldbe represented by a difference of 0. Thus, if the 95% CIdoes not overlap with 0, then there is a significant dif-ference between HRs at the 2 temperatures, with P <0.05 (likewise, if 99% CI does not overlap with 0, thenthere is a significant difference, with P < 0.01).




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overemphasized. Many published studies in the fieldof diving physiology do not make the statistical com-parisons that address the purpose of the experiment,either because they lack the appropriate controls orbecause they do not use the controls correctly in theirstatistical analysis. We therefore strongly urge instruc-tors to take the time to explain this important con-cept. A useful exercise for advanced students is toread a few primary papers on diving physiology todetermine whether the authors correctly designedtheir controls and statistical analysis.

Consider experiment 1, the comparison between thesimulated dive and the control of breathing in air.Students will be tempted to plot the change in heartrate from the first 15 s to the second 15 s, apply apaired t-test, and interpret the result as showing thata simulated dive causes a decrease in heart rate overtime. Drawing such a conclusion from this analysis,however, is completely invalid, because the compar-ison just described tells us nothing about the relativeroles of the dive and of separate time-dependent fac-tors in stimulating bradycardia. It may be, for exam-ple, that heart rate simply decreases over time duringthe test no matter what the test condition. Indeed, wefind that heart rate decreases over time even in sub-jects breathing in air (see experiments 1 and 2; Table2). This tells us that some of the decrease in heart rateover time in any of the test conditions (#4 beats/minin experiment 1) is due to some time-dependent fac-tor other than the test variable [such as the subjecthabituating to the test condition, as shown byZbrozyna and Westwood (26) and Reyners et al. (21)].The remainder of the decrease in heart rate, the por-tion that is due to the simulated dive conditions, is thedifference in heart rate between breathing in air andthe simulated dive during the same measurementperiod. The analysis must compare heart rates betweentest condition and control (or between two test condi-tions, if it is not possible to designate one of the condi-tions as the control) during the same measurement pe-riod, rather than comparing heart rates betweenmeasurement periods within the same test condition.These concepts are illustrated graphically in Fig. 1.

Paired analysis, which makes use of the fact thateach subject was tested in both test conditions,is more powerful than two-sample or unpairedanalysis, which simply compares the means of heart

rates between the two conditions without taking noteof how the data from each individual are paired.When combined with the concept of controls de-scribed in the preceding general principle, this con-cept states that, if each subject undergoes both testconditions, then the power of a paired statistical testcan be gained by comparing the subjects’ perfor-mance in the control and test conditions during thesame time period of the test (Fig. 3).

Increased sample size increases statistical signif-icance of differences where they exist. The moreindividuals we measure in our sample, the more certainwe can be about the mean heart rate for the wholepopulation under the conditions tested. This increasedcertainty is reflected in a lower P value. Students candemonstrate this principle by statistically analyzing thedata from their own laboratory section and then repeat-ing the analysis on data that have been pooled with oneor more other laboratory sections.

BACKGROUND INFORMATION FORINSTRUCTORS

Physiological Adaptations for Coping withHypoxia During Diving

Lung-breathing animals face two problems when theydive: a shortage of oxygen (hypoxia) and, if theyreach sufficient depth, abnormally high pressures (hy-perbaria). Here, we consider the problem of hypoxia,which may be solved in three general ways: by storingoxygen before the dive, by conserving oxygen duringthe dive, and by replenishing oxygen stores quicklybetween dives.

The animals best adapted for diving, the seals and sealions (pinnipeds), are able to remain submerged with-out resorting to anaerobic metabolism for up to 20min (7), during which time they rely heavily on oxy-gen bound to muscle myoglobin, present in suchlarge quantities that the muscles of diving mammalsappear nearly black when exposed to air (23, p. 28).Hemoglobin in red blood cells also stores oxygen.During a dive, the spleen of pinnipeds contracts,expelling the oxygen-rich red blood cells it stores intothe general circulation and increasing the hematocritfrom below 40 to near 70. During periods when sealsare hauled out on land, the spleen plays the equallyimportant role of storing these extra blood cells,




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which when circulating increase blood viscosity andrequire the heart to work harder, particularly at thehigher heart rates that prevail when the seal is notdiving (16). Peripheral vasoconstriction reduces cir-culation to the muscles and other tissues while main-taining blood flow (and hence oxygen delivery) to thebrain and heart. Lowering the oxygen demand of pe-ripheral tissues during a dive is accomplished mainly bymetabolic depression, which results when tissues arecooled or become hypoxic. The reduced blood circula-tion (hypoperfusion) caused by peripheral vasoconstric-tion seems to have two related functions: 1) reducingthe delivery of precious oxygen to the less needy pe-ripheral tissues, and 2) decreasing the need of periph-eral tissues for oxygen by denying them oxygen andallowing them to cool when circulation is restricted, aprocess that takes place especially quickly when theanimal is immersed in cold water (8, 14, 25).

The principal sensory components and integrativepathways involved in the diving response are shownin Fig. 4. Trigeminal receptors on the face (and, tosome extent, glossopharyngeal receptors on the

tongue and upper airways) provide the first proxi-mate cue that a dive has begun (16). Subsequentsignals from arterial chemoreceptors reinforce anddeepen the diving response, which takes several min-utes to develop fully in a diving mammal; ultimately,heart rate may drop to as little as 5 beats/min (8). Inhumans, the response is also not immediate but de-velops more rapidly than in diving mammals, some-times to equally impressive levels [one human subjecthad heart rates as low as 6 beats/min (16)]. A princi-pal difference between the diving responses of hu-mans and diving mammals is that, in diving mammals,cardiac output (a product of heart rate and strokevolume) and peripheral vasoconstriction are balancedso that mean blood pressure does not increase duringa dive (in humans, blood pressure increases slightlyduring a dive because the effects of vasoconstrictionexceed the effects of reduced cardiac output). Duringa dive that exceeds the aerobic dive limit (ADL),peripheral vasoconstriction has the added advantageof preventing lactic acid (lactate) produced by musclecells from entering the general circulation where itwould have toxic effects. Blood lactate typically does

FIG. 4.Principal components of the diving response. Solid arrows indicate stimulation, dashed arrows inhibition. CNS,central nervous system.Inputs primarily from trigeminal receptors on the upper part of the face are integratedby the respiratory and cardiovascular centers in the medulla oblongata (in the brainstem), generating neuralsignals to the lung, heart, and arterioles that include both sympathetic and parasympathetic divisions of theautonomic nervous system. During longer dives, chemoreceptive inputs from aortic and carotid bodies help maintainthese effects. Bradycardia reduces cardiac output and therefore should reduce blood pressure, but in humans thiseffect is more than compensated for by the increase in blood pressure brought about by peripheral vasoconstriction,with the ultimate result that blood pressure increases during a dive in humans. Although arterial chemoreceptors mayrespond to pH and PCO2 as well as to PO2, during diving PO2 seems to be the more important in regulating cardiovas-cular center outputs (14). Based on figures from Gooden (14) and Hochachka and Somero (16).




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not rise until the animal surfaces, at which time it isflushed into the general circulation and detoxifiedaerobically (16). Postdive tachycardia speeds this pro-cess and reloads circulating red blood cells with ox-ygen before they are returned to the spleen for stor-age (16, 22). Spleen contraction has also beenobserved in human divers, suggesting that a similarmechanism might occur in nondiving mammals (18).

In addition to the principal sensory inputs describedabove, inputs from thoracic muscles as well as cogni-tive and emotional factors may modify the divingresponse as measured by the development of brady-cardia. As soon as a diving mammal becomes awarethat it cannot resurface (e.g., when being chased by apredator or when in a tank over which an investigatorhas just placed a cover), heart rate decreases further(8). In some cases, there may be anticipatory brady-cardia before the start of a dive and/or an anticipatoryreturn to nondiving heart rate as the animal begins toswim toward the surface (8). In humans, fear andfacial stimulation with very cold water may stimulatean initial transient tachycardia, which is later replacedby the more conventional bradycardia, either withinthe same dive (10), or in later dives after the subjecthas habituated to the test situation (26).

Bradycardia, peripheral vasoconstriction, and meta-bolic suppression occur in many mammalian taxa, notonly in response to diving but also in other hypoxicconditions. These responses occur during hibernationas well as during birth, when uterine contractionstemporarily occlude placental blood vessels that sup-ply the fetus with oxygen (22). Many vertebrates,including lizards and snakes, develop bradycardia in avariety of conditions in which oxygen is in limitedsupply, suggesting that this is an ancient responsewith a general function that has been put to specificuse during diving (16, 22). The fact that fish developbradycardia when taken out of water further supportsthe idea that hypoxia, rather than immersion per se, isthe ultimate cause of bradycardia (22).

Implications of the Diving Response forHumans

Diving bradycardia is a response to immersion. In theevent of involuntary immersion, when the subject hasnot had a chance to hold the breath voluntarily, the

apnea reflex stops breathing to prevent aspiration ofcold water (see Fig. 4 and Refs. 16 and 19). The momen-tary inability to breathe that we may experience when agust of very cold wind blows into our faces on a winterday is one manifestation of the apnea reflex; babies inthis situation can be at particular risk because they maybe unable to move out of the wind by themselves.Conversely, students may notice that it is more difficultto hold their breath when they immerse their faces inwarm water (personal observation), partly because thecue of cold on the face is absent. It is widely believedthat the evolutionary benefit of the diving response isthat it can improve survival not only in near-drowning(13, 19), but in any situation with reduced oxygen avail-ability (hypoxia) (16).

The professional breath-hold divers of Japan and Ko-rea, known as ama, depend on the diving responsefor increasing the time they can spend on the oceanfloor, but even they remain submerged on average foronly 30–60 s per dive (17). Clinically, plunging theface into cold water and/or holding the breath arerecommended for treating tachycardia or stimulatingthe vagus nerve (3, 4, 21). Dental examinations andmedical procedures that stimulate the glossopharyn-geal receptors on the back of the tongue or upperairway can sometimes trigger apnea and bradycardia(19). Some investigators have suggested that the div-ing response may be responsible for Sudden InfantDeath Syndrome (19), but this is only one of manyhypotheses under consideration. Others are studyingthe similarities between the diving response and sleepapnea, a sleep disorder in which hypoxia developswhen breathing is disrupted (22)

THOUGHT QUESTIONS

In a diving mammal, what would be the consequenceof constricting peripheral blood vessels without mak-ing any other circulatory adjustments? Why wouldthis be dangerous? What normally happens to preventthis from occurring? Peripheral vasoconstriction byitself would reduce the total volume of open bloodvessels, thus increasing blood pressure to organsthat continue to receive blood, such as the brain.The increase in pressure could cause arteries in thebrain to burst. Diving mammals compensate forperipheral vasoconstriction by lowering cardiac




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output (achieved at least partly by decreasing heartrate), thus keeping blood pressure roughly constant.

Arrange the following species in order of how welldeveloped you think the bradycardia reflex would be,from least developed to most developed, and explainyour reasoning: muskrat, tadpole, alligator, adult frog,human. State the general principles on which you arebasing your answers. General principles: 1) the bra-dycardia reflex develops in response to hypoxia; 2)the higher the metabolic rate, the faster hypoxiadevelops; 3) selection should favor development of amore robust diving response in air-breathing ani-mals that spend more time submerged. Answer: Atadpole should not require a bradycardia reflex be-cause it has gills. The adult frog breathes throughlungs but it can also absorb oxygen across the skin(in and out of water); furthermore, it has a very lowmetabolic rate because it is an ectotherm and hasreduced needs for oxygen at all times. Alligators arelarger and tend to have higher body temperaturesas a result, even though they are ectotherms; higherbody temperatures result in higher oxygen needs inthis animal, which spends much of its life in andnear water. Both humans and muskrats are endo-therms with high rates of oxygen consumption. Be-cause humans are larger, they have a lower rate ofoxygen consumption per gram body mass than domuskrats; the fact that muskrats live near waterand regularly dive further supports the conclusionthat the diving response of muskrats should be moredeveloped than that of humans.

Chester (9) writes, “The diving reflex presumablyserved our amphibian ancestors well as an oxygenconserving technique with submersion, but serves noknown useful function now.” Do you agree withChester? Why or why not? See Background informa-tion for instructors. Even if near-drowning eventsoccur infrequently, they should be sufficient to selectfor a mechanism that improves survival. See alsothe answer to the previous question, which explainswhy an amphibian is less likely to show divingbradycardia than lung-breathing vertebrates.

If the function of bradycardia and the other adjust-ments in the body that take place during diving is toconserve oxygen use when oxygen supplies are low,why isn’t arterial oxygen the only proximate cue that

triggers the diving response? Use your thinking onthis question to make a general statement about prox-imate and ultimate causation in biology and why bothmay be necessary for survival. What is another exam-ple of ultimate and proximate mechanisms that illus-trates the general principle that you have identified(you may use an example from any area of biologythat you have studied)? The oxygen sensors in ourarteries do not respond immediately when the ani-mal stops breathing because it takes some time forarterial oxygen tension to decrease. A diving mam-mal, however, benefits from cardiovascular adjust-ments that take place early in the dive (or even inanticipation of it), because these adjustments re-duce the total oxygen requirement of the animaland increase dive time. Thus responding to a cuethat is immediate, such as cold on the face, is ad-vantageous. General principle: using a proximatecue (cold) that predicts the ultimate difficulty (lackof oxygen) allows the animal to prepare itself for thecoming change. Another example of this principle isthe timing of seasonal reproduction. The ultimategoal is to synchronize the birth of young with thetime at which food is most abundant, but animalsthat wait until food is abundant to begin theirreproductive effort (i.e., start regrowing their go-nads and mating) would be at a disadvantage com-pared with animals that are ready to give birthwhen food is abundant. Most animals living in sea-sonal environments use proximate cues that reli-ably predict the coming of abundant food (e.g., daylength), instead of food itself, to trigger the onset oftheir annual reproductive effort.

Given what you know from your results about whattriggers the diving response, what do you think wouldbe the response of heart rate, blood flow, and meta-bolic rate in a human if all body parts except the headwere immersed? When hypoxia is a limiting factor,the most important need for survival is to protectthe brain from injury, which is facilitated by pro-viding as much oxygen as possible to the brainwhile reducing the brain’s need for oxygen by al-lowing it to cool, an effect thought to be responsiblefor the survival of some extraordinary cases of near-drowning in cold water (13). When hypoxia is notlimiting, the most important need for survival is theprevention of overall hypothermia. The response to




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head-out immersion is a sharp increase in meta-bolic rate, heart rate and blood flow (13, 19).

After a harbor seal surfaces from a long dive, it expe-riences tachycardia (very high heart rate). Propose afunction for this tachycardia. As soon as oxygen be-comes available, circulation should increase toquickly remove lactic acid from the muscles andreoxygenate hemoglobin and myoglobin (23, p. 29).

When the forehead is cooled with a cold pack, it issometimes possible to observe an initial increase inheart rate, which is then followed by the bradycardiathat we are accustomed to observing in the diving re-sponse (10). Propose an adaptive function for this initialtachycardia. Does your hypothesis predict that theamount of tachycardia would be different at high or lowtemperatures? Tachycardia might be a response to pre-vent the brain from cooling by circulating warmblood to the head; in this case we would expect tachy-cardia to be more pronounced at lower temperatures.

Investigators of a published study wished to deter-mine whether the diving response could help chil-dren survive near-drowning in cold water. The chil-dren who were subjects in this study simulated dives(immersion with apnea) in 29°C water, but fewerthan 20% of the children were able to hold theirbreath to 25 s, which was the average time it took fordiving bradycardia to reach its maximum. The inves-tigators concluded that children have a weak brady-cardia reflex and that their ability to hold their breathwas not sufficient to improve their chances of surviv-ing near-drowning in cold water. Using examplesfrom your data, evaluate this experiment and its con-clusions. At 29°C, which is warmer than most bodiesof water in which a person might accidentally be-come submerged, diving bradycardia should be lesspronounced than at lower temperatures. If the div-ing response reduces oxygen requirements, then in-creased bradycardia could extend the survival timeof a child immersed in cold water.

APPENDIX

Definitions

Aerobic dive limit (ADL): the amount of time a diving animal canremain submerged while relying on aerobic metabolism

Bradycardia: lower than normal heart rate

Confidence interval: in statistics, an interval calculated fromsample data that has a stated percentage probability of containingthe population mean; e.g., the 95% confidence interval has a 95%probability of containing the population mean

Hematocrit: the percentage of blood volume consisting of redblood cells (RBCs), expressed as a whole number; e.g., humanhematocrit is normally #45 (45% RBC by volume)

Oxygen tension: a measure of the concentration of oxygen, ex-pressed as the partial pressure of oxygen in a fluid

Tachycardia: higher than normal heart rate

Thermoneutral zone: a range of ambient temperatures in whichheat is neither lost to nor gained from the environment; at thesetemperatures, the medium (e.g., air or water) should feel neitherwarm nor cool

Many thanks to our students in Biology at the Putney School and inPopulation and Organismal Biology at Swarthmore College, and toscience teachers in the Bryn Mawr Summer Institute, for collectingdata and testing our ideas. We also thank Paul Grobstein and LeeGass for helpful discussions about science pedagogy, and JudithSheridan at the Putney School for assistance in obtaining heart ratemonitors and computer software for use with this exercise in theclassroom.

Address for reprint requests and other correspondence: S. M.Hiebert, Biology Dept., Swarthmore College, Swarthmore, Pennsyl-vania 19081–1390 (E-mail: [email protected]).

Submitted 3 September 2002; accepted in final form 11 June 2003

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