Minimal Dissolved Oxygen Requirements of Aquatic Life With

Minimal DissolvedOxygen Requirementsof Aquatic Life with Emphasis on Canadian Species:a Review

JoHN C. D,q.vrs

Department of the Environmen'r;,::;';;:;:#!Y;:';'ifii'i;Pacific EnvironmentInstitute'

Contents

2295 Preface Respiratorydependence in invertebrates 2296 Abstract Oxygen requirementsof some freshwater 2296 R6sum6 in verte brates 2291 lntroduction,Rationale, and Objectives Oxygen requirementsof some intertidal 2297 PhysicalConsiderations marineinvertebrates 2299 Natural O, Regimesin the Aquatic Environ- Oxygenrequirements of benthicmarine or- ment ganismsand communities Oxygen tolerances and requirements of marineplanktonic and pelagic or- 2301 OxygenRequirements of Fish ganisms Bloodoxygen dissociation curves Ventilation, circulation,and respiratoryde- 2318 Summaryof OxygenRequirements of pendence rA.quatic Invertebrates Energeticsand low oxygen 2320 Developmentof Oxygen Criteria for Fish Behavioral responsesto hypoxia Populations Growthin reducedoxygen StatisticalTreatment of Data for Devia- Acclimationto low oxygen tion of Criteria Interactionof low oxygenand toxic agents 2325 Guidelines for Low Oxygen Tolerance of Eggand larval development in low oxygen AquaticInvertebrates 2326 Relationshipof ProposedCriteria to Other For personal use only. 2310 Summaryof OxygenRequirements of Fish Documents 2327 Suggestionsfor Implementationof Criteria 2321 Acknowledgments 2311 Oxygen Requirementsof Aquatic Inverte- 2127Glossary of Terms brates 2328 List of Symbols Aerobicand anaerobic metabolism 2328 References

Preface

Originally, some of the material in this report was prepared for the National Research Council of Canada Environmental Secretariat under the title "Waterborne Dissolved Oxygen Requirements and Criteria With Particular Emphasis on the Canadian Environ- ment." That document was published n 1975 as part of N.R.C.'s special publication series under the auspicesof the Associate Committee on Scientific Criteria for Environ- mental Quality. The emphasis in the N.R.C. document was on development of oxygen criteria which were defined as cause and efiect interrelations based on a scientific evaluation of environmental harm caused by low oxygen in water. The content of tle N.R.C. report was, of necessity, limited to matters considered the mandate of the N.R.C. environmental secretariat. This report, although similar in many ways to the N.R.C. report, is intended to serve more as a review document to persons interested in oxygen requirements of Canadian aquatic species. Where criteria are discussed, suggestions are made as to how criteria

J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 might be implemented. It must be stressedthat the suggestionsherein are the author's opinions and are not the opinions of N.R.C. whose mandate does not include recommendations on criteria implementation. Readers should be very careful to distinguish between the content and positions taken when making reference to these two reports. Printed in Canada (13915) Imprim6 au Canada (J3915) 2295 2296 J. FISH. RES. BOARD CAN.' VOL. 32(t2)' 1975

Abstract Drvrs, J. C. 1975.Minimal dissolvedoxygen requirementsof aquaticlife with emphasison Canadianspecies: a review.J. Fish.Res. Board Can.32:2295-2312. This articlereviews the sensitivity,responses, response thresholds, and minimumoxygen requirementsof marineand freshwaterorganisms with strongemphasis on Canadianspecies. Th-eanalysis attempts to definelow dissolvedoxygen thresholds which produce some physiological, behavioral,or otherresponse in differentspecies. Oxygenavailability is discussedwith referenceto seasonal,geographical, or spatialvariation in dissolvedoxygen. Factors affectingavailability of dissolvedoxygen include atmospheric exchange,mixing ofwater masses,upwelling, respiration, photosynthesis, ice cover,and physical factorssuch is temperatureand salinity.Dissolved oxygen terminology is summarizedand tablesare includedfor both fresh and saltwaterO, solubility at different temperatures. IncipientO, responsethresholds are used in a statisticalanalysis to developoxygen criteria for safeguardingvarious groups of freshwaterand marine fish. These include mixed freshwater fish populationiincluding or excludingsalmonids, freshwater salmonid populations, salmonid larvie or maturesalmonid eggs, marine anadromous and nonanadromousspecies. Criteria are basedon threshold oxygen levels which influencefish behavior, blood O, saturation, metabolic rate, swimmingability, viabilityand normal development of eggsand larvae, growth, circulatory dynamics,veniilation, gaseous exchange, and sensitivityto toxic stresses.The criteriaprovide three levels of protection for eachfish group and are expressedas percentageoxygen saturatlon for a rangeofseasonal temperature maxima. Oxygentolerances and responsesofaquatic invertebratesto low oxygenare reviewedfor freshwaterand marine species according to habitat.No inverlebratecriteria are proposed owing to the capacityfor many invertebratespecies to adopt anaerobicmetabolism during low Ot stress. It is suggestedthat the criteriaproposed for fish specieswill providea reasonablesafeguard to_ most ini-ertebratespecies. It appearslikely, however,that a changein oxygenregime to one of increasedO, scarcitywill probablyinfluence invertebrate community structure. It is suggestedthat iriteria for protectionof aquaticlife be implementedby groups of experienced-individuals.The group shouldconsider the naturaloxygen regimefor a specific waler body and its natural variability, the aquatic life therein and its value, importance,relative O, sensitivity,and the possibilityof interactionswith toxicants and other factors that may compoundthe stressproduced by low O, on aquaticlife. Each water body and its aquaticlife shouldbe consideredas a uniquesituation and criteria application should not encompassdiverse areas,habitats, or biologicalassociations as if they wereidentical.

For personal use only. R6sum6 Davrs, J. C. 1975.Minimal dissolvedoxygen requirementsof aquaticlife with emphasison Canadianspecies: a review.J. Fish.Res. Board Can. 3;2:2295-2332' Danscet article,I'auteur passe en revuela sensibilit6,les r6ponses, les seuilsde r6ponseet les exigencesminimales en oxygEned'organismes marins et dulgaquicoles,avec accentpar- ticuliei sur les espdcescanadiennes. Il y d6finit les seuilsminimums d'oxygbne dissous qui d6clenchentdes r6ponses physiologiques, de comporlementou autreschez diff6rentes espdces' I1analyse |a diiponibiiit6d'oxygdne en relation avec la variationg6ographique ou spatialede I'oxygbne.Les factiurs affectantla disponibilit6de I'oxygbnedissous sont, entre autres,les 6changesavec I'atmosphbre,le m6langedes massesd'eau, la remont6ed'eaux profondes,la respirition, la photosynthdse,la couverturede glace et des facteurs physiquestels que la temp6ratureet la salinit6.Il donneun 16sum6de la terminologiede I'oxygdne dissous et destables de solubilit6 de I'oxygbne, tant en eau douce qu'en eau sal6e,ir differentestemp€ratures. Il utiliseles seuils de d6butde r6ponse)r I'oxygbne dans une analyse visant ir mettreau point des critdresde sauvegardedes divers gloupesde poissonsde mer et d'eau douce.Ces groupes comprennentdes populationsmixtes de poissonsd'eau douce, incluant ou excluant les salmonid6s,des populationsde salmonid6sd'eau douce, des larves ou des ceufsmfirs de salmonid6s,et desespbces marines anadromes et nonanadromes. Ces critbres sont fond6s sur les niveaux de seuil d'oxygdne affectant le comportementdes poissons,la saturationdu sangen O, , le taux m6tabolique,I'aptitude i la nage,la survivanceet le ddveloppementnormal des ceufset deslarves, la croissance,la dynamiquede la circulation,les 6changes gazeux et la sensibilit6aux stresstoxiques. Les critbresfournissent trois paliers de protectionpour chaquegroupe de poissonsetiont exprim6sen pourcentagede saturationd'oxygbne sur une gamme de maximums J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 saisonniersde temp6rature. L'auteur passLen revuela tol6ranceir I'oxygbneet lesr6ponses d'invert6br6s aquatiques ir de bas niveaux d'oxygbne, pour des espbcesdulEaquicoles et marines, selon l'habitat' Il ne proposeaucun critdre pour les invert6br6sir causede I'aptitude de plusieursespbces ir adopterun m6tabolismean6robie au moment d'un stresscaus6 par un basniveau d'Or. Les critEressugg6r6s pour lesespdces de poissonfourniraient une sauvegarderaisonnable pour la plupartdes espbces DAVIS:REVIEW OF OXYGENREQUIREMENTS oF AQUATICLIFE 2297

d'invert6br6s.Il est probable,cependant, qu'un changementde r6gimed'O, en directiond'une plusgrande raret6 d'Or, affectela strxcturedes communaut6s d'invert6br6s. L'auteur suggEreque les critEresde protectionde la vie aquatiquesoient appliqu6s par des groupesd'individus exp6riment6s. Ces groupes devraient 6tudier le r6gimenaturel d'O, d'un plan d'eau particulier et sa variabilit6 naturelle, la sensibilit6relative ir I'O2 et la possibilit6 d'interactionsavec les toxiques et autresfacteurs qui peuvents'ajouter au stress caus6 par un bas niveaud'O, sur la vie aquatique.Chaque plan d'eauet la vie aquatiquequ'il contientdevraient Otreconsid6r6s comme situation unique, et I'applicationdes critEres ne devraitpas englober des r6gions,des associations biologiques et deshabitats diff6rents comme s'ils 6taientidentiques.

ReceivedJuly 21, 1975 Regule 2l I ,tlllet197 5 AcceptedJuly 30,1975 Accept6le 30juillet 1975

Introduction, Rationale, and Obiectives be exhibited by the test species,and the response varies with the severity of hypoxia. Attempts to Tne purpose of this paper is to review available arrive at critical oxygen levels, based on data information on the oxygen requirementsof aquatic gathered under differing experimental conditions organismsas a basis for formulating water oxygen and with varying approaches and experimental quality criteria that provide a reasonable assess- criteria, are bound to be frustrating. ment of hazard for Canadian aquatic resources. The present approach has been to scan the large A body of literature exists on the general literature and extract information on dissolved subject and some excellent reviews have appeared oxygen levels where sublethal responses to hy- (Doudoroff and Shumway l97O; Wanen and poxia first became apparent (i.e. the incipient Shumway 1964; Warren et al. 1973). This paper sublethal threshold). By extracting this sort of attempts to arrive at a consensusof opinion on information one becomes aware of the oxygen low oxygen sensitivity of fish and invertebrates. level where some physiological, behavioral, or Results of this review are used to develop water other stress-inducedresponse occurs. It is then quality criteria based on the best available cause that the animal indicates at what point energy and effect information relating to aquatic life. must be expendedor adjustmentsmade to counter- In preparing paper this it was not intended to act hypoxia. When such a stress is a chronic reiterate much of the information summarized by occurrence, it is an important determinant factor other reviewers. Instead, this report attempts to in the long-term survival of an organism. concentrate mainly on aquatic organisms found Some readers may take exception to the above in Canadian waters, relying on the reader to

For personal use only. approach, citing the ability of animals to adjust consult other sources geographic relevant to areas or regulate to altered condit.ons. A later section outside Canada. Some considerable attention has will deal with acclimationphenomena, and other been given to defining low oxygen effects on sections will explain the significance of observed aquatic organisms, identifying oxygen response sublethalresponses. It is my belief that we should thresholds, and physiological examining responses look for "no-effect" levels in setting water quality to low oxygen under different conditions. criteria that assure the long-term survival of In reviewing the literature it was evident that aquatic organisms.Any departurefrom this level numerous and often contradictory results have assumesa degreeof risk which increaseswith the been reported for critical oxygen levels for the severity of hypoxia present. The degree of risk same aquatic organisms. This lack of clarity has acceptedbecomes a matter of judgement based made it extremely difficult for reviewers to de- on the economic value of an individual aquatic cide the levels of oxygen that are critical as a population or an entire aquatic community, basis for criteria recommendations. Part of the assessedagainst such factors as industrial needs problem appears to be one of definition. Much or the aestheticsof unpolluted waters - none of of the literature deals with determining lethal which can be satisfied by scientific criteria. levels of dissolved oxygen (see table 1 in Doudoroff and Shumway l97O). In contrast, Physical Considerations some workers have defined critical oxygen levels as that point when fish lost equilibrium (e.g. At 19 C fresh water contains 7.93 ml/liter Townsend et al. 1938; Townsend and Earnest oxygen, roughly O.8% of its volume, when ex-

J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 1940; Townsend and.Cheyne 1944) or exhibited posed to air at sea level. Air at the same tem- "respiratory distress" (Wilding 1939). It should perature and pressure,in contrast,holds approxi- be recognizedthat each of these responsesreflects mately 2A9 ml/liter oxygen, roughly 26 times as some degree to which the animal responds to much oxygen as water. Aquatic organisms have low oxygen. Thus there is an entire range of re- evolved within the physical constraints of their sponsesto hypoxia (lowered oxygen) which may relatively oxygen-scarce environment and many 2298 J. FISH. RES. BOARD CAN,, VOL, 32(12),1975

possesshigh specializedgas exchange systems Tasrn 1. Saturated water vapor pressure and oxygen in water which permit maximal utilization of available partial pressuresin relation to water temperature air at 760 mm Hg air oxygen supplies. ixposed to fully oxygen-saturated pressure. Aerobic organismsutilize the process of diffusion to move oxygen into their systems by Oxygen partial for means of an internal-external 02 pressure gra- Pressure Saturatedwater l0O%'air saturation at process often facilitated dient. The exchange is Temp vapor pressure 760 mm Hg pressurein water (e.g. and opercu- by a delivery system branchial (6 Gnmm Hd Gnmm He) lar pumps in fish) and a transport system (e.g. internal circulatory system) to distribute oxygen -5 3.0 158.6 within the body. In all aerobic organisms,move- t 3.4 158.5 -3 ment of oxygen to the tissuesfor metabolisrnis 5.1 158.4 -2 158.4 fundamentally via tension gradients, both within 4.0 -1 4.3 158.3 without the body. Thus, it is the oxygen and 0 4.6 158.3 tension gradient between tissues and the external medium that is critical to the gas exchange +l 4.9 158.2 158.1 process. 5.3 -L? 5.7 158.0 Air at sea level contains about 20.9Vo oxygen. +4 6.1 157.9 Under standard conditions dry air exerts a pres- 6.5 157.9 sure equivalentto 760 mm Hg. The oxygen ten- +6 7.0 157.8 sion can be calculated: 7.5 r57.6 PO, : (Atmos.Press - H2Ovap. press.) x %O, (1) +8 8.0 157.5 8.6 1s7.4 : +9 where:Atmos. Press. Atmosphericpressure in milli- 9.2 157.3 metersHg +10 HrO vap.press. : watervapor pressure in millimeters +ll 9.8 157.2 Hg at testtemperature +12 10.5 157.O 7,Oz : percentageoxygen in atmosphere +13 rt.2 156.9 PO2: oxygenpartial pressure, millimeters Hg +14 t2.o 1s6.7 +15 t2.8 156.5 the aboveexample at l0 C (assumingAtmos' For 13.6 156.4 = +16 Press. 760 mm Hg): +17 14.5 t56.2 PO2: Q6O- 9.2) x 20.946%: 157.3mm Hg (2) +18 15.5 156.0

For personal use only. 16.s 155.8 at sea +19 Water equilibratedwith atmosphericair +20 t7.5 155.6 level usually has an oxygen partial pressure of r8.6 155.3 Hg. Thus organismsexposed +21 about 154-158 mm 19.8 155.r to fully saturated water under those conditions 21.0 154.8 exist with an external oxygen pressure of 154- I ai 22.4 154.5 158 mm Hg. In fish the internal oxygen tension rt< 23.7 t54.3 (ca. external tension. 5G-110) is lower than the 25.2 153.9 gills into +26 Oxygen therefore diffuses across the ta1 26.7 153.6 the blood down an 02 gradientof 4G-100 mm Hg +28 28.3 153.3 (Randall 1970). A drop of externalPO2 reduces +29 30.0 152.9 this gradient or depressesarterial PO2 levels. If +30 31.8 152.6 the oxygen depression is severe, insufficient 02 tension will occur at the tissue level. For practical purposesthe PO2 of water can be 7.93 ml O2lliter (1 mg Oz:0.7 ml 02) and calculated from the above cited equation (1)' from (2) has a partial pressureof 157.3mm Hg' when the barometric pressure is known. Water If that sample were only 507o satvated, it would - = vapor pressurecan be obtained from tables (e.g. have11.33/2 5.67mg O2lliter,7.93/2 3'82 Table 1) for purposesof calculation. ml Orlliter, and a PO2 of 157.3/2 = 78.65 It is more conventional for water quality or mm Hg. oceanographicpurposes to expresswater oxygen As temperature and salinity increase, oxygen (Tables J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 levels in terms of their concentration rather than content decreases.Tabulated values 2 partial pressure.Thus one speaks of oxygen in and 3) and well-known formulae (Gamesonand terms of milliliters Or/liter or mg O2lliter (parts Robertson 1955; Truesdaleand Gameson 1957) per million). All the terms can be interrelated enable easy calculation of oxygen content of such that a sample of air-equilibrated fresh water water at different temperatures and salinities. As at 10 C at sealevel has 11.33mg Orlliter (ppm), temperature increases, oxygen content drops DAVIS:REVIEW OF OXYGENREQUIREMENTS OF AQUATICLIFE

Tnsrr 2. Solubility of oxygen in fresh water at different temperatureswhen water is exposedto an atmospherecontaining 20.9ftoxygen at a pressureof 760 mm Hg (including water vapor pressure)(derived from Whipple 1914).

Cm3 per liter Cm3 per liter Temp Parts per (at 0 C and Temp Parts per (at 0 C and (c) million 760 mm) (C) million 760 mm)

0 14.62 r0.23 16 9.9s 6.96 1 l+.zJ 9.96 l7 9.74 6.82 ) 13.84 9.68 l8 9.s4 6.68 J 13.48 9.43 19 9.35 6.54 4 13.13 9.19 20 9.17 6.42 5 12.80 8.96 21 8.99 6.29 6 12.48 8.73 22 8.83 6.I8 7 12.17 8.52 ZJ 8.68 6.07 8 11.87 8.31 a1 8.53 5.97 9 11.s9 8.11 25 8.38 5.86 10 11.33 7.93 26 8.22 5.75 ll 1I.08 7.7s 27 8.07 5.65 12 10.83 7.58 28 7.92 5.54 13 10.60 t.+z 29 7.77 5.44 t4 ro.37 7.26 30 7.63 5.34 15 10.15 7.10

owing to reduced solubility, while oxygen partial as 364.5Voin the upper portion of a Wisconsin pressure drops only slightly owing to increased lake. Tarzwell and Gaufin (1953) described a molecular activity. Thus a fish breathing warm location in a southern Ohio creek polluted with water must pump more water over the gills than sewage where dissolved oxygen was 19.4 mg in cold water to deliver a given volume of Or/liter one afternoon and 0.7 mg Orlliter the oxygen/unit time, becauseof the reduced oxygen next morning. Oxygen concentrations in ponds content of inspired water. This is necessaryeven and lakes exceeding30 mg Orlliter have been though the 02 tension gradient between blood reported (Wiebe 1933; Woodbvry 1942). Servizi For personal use only. and water is little changed at high temperatures. and Burkhalter (1970) reported oxygen levels Severe respiratory problems can result from a close to saturation on the surface of the Thompson combination of high temperature (low O, con- and Fraser rivers in 1963 and 1966, prior to tent) and reduced oxygen tension (water not operation of pulp mills on the upper reachesof fully saturated) as both availability and the gra- the rivers. Seasonallylow levels of oxygen in dient for oxygen diffusion are reduced. Associated freshwater bodies can lead to "winter kills" re- with this phenomenon is the fact that higher sulting from decay of organic rnaterials under ice temperatures usually increase the metabolic de- cover without replenishment of oxygen from the mand for oxygen. It is likely that the stimulatory atmosphere.Summer kills can result from high effect of increased temDeratureon metabolism is water temperatures, reduced water oxygen solu- the most important of all these factors owing to bility, and large oxygen demandsfrom planktonic the magnitude of its effect. It is largely for tf,ese and bacterial respiration. reasonsthat fish kills relatedto low oxygenlevels In the sea, oxygen levels in the photic zone often occur in warmwater periods. Obviously, may rise to 130% saturationor higher, owing to meaningful oxygen criteria should consider the photosyntheticprocesses (Fairbridge 1966). As critical oxygen content and oxygen tension as well as the contribution from photosynthesis, well as temperature effects on metabolism in oxygen enrichment occurs in water by atmospheric order to provide a full measure of protection. exchange.The rate of enrichment is dependenton the rate of "turnover" of the system. In deep Natural ()2 Regimes in the Aquatic marine waters, oxygen levels are generally lower

J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 Enyironment than at the surface owing to reduced atmospheric exchange and to oonditions where respiration ex- Bodies of fresh water often show larse varia- ceedsphotosynthesis. Fairbridge (1966) reported tions in dissolved oxygen, both season-allyand that Atlantic bottom water generally does not fall geographically.Welch (1952) attributedto photo- below 6OVo saturation, while oxygen levels in synthesisvalues of oxygen supersaturationas high deep Pacific water may be somewhat lower. In 2300 J. FISH. RES. BOARD CAN., VOL. 32(.12),t9'15

T,cslr 3. Solubility of oxygen in seawater of salinity 35%",inmilligrams per liter, from a normal atmospheresaturat- ed with *ut", uupoi at a io-tal pressureof 760 mm of -ir.rrty from -2 to +40 C' AC, is the changein solubility for a changeof tfl"insalinity (from Truesdaleand Gameson1957). (This tablecan be usedto calculateoxygen content of water at various temperaturesand salinities.) : Temp (c) .e .8 .7 .6 .5 -+ .J .. .1 .0 AC, -2 11.86 -0.088 - .72 11.69 tl .66 1.1.63 11. 59 11.56 11.53 1 11.82 t1.79 11.76 11 - -0 11.50 11.4't 11.44 11.41 11.37 lt .34 1l .31 1l .28 1,1.25 11.22 0.085

Temp .3 .4 .6 .6 .7 .8 .9 AC, (c) .0 .r .2 -0.083 +0 11.22 11.19 11.16 11.13 11.10 11.07 1l .04 11.01 10.98 r0.95 10.80 10.78 10.75 10.72 10.69 10.66 -0.080 | 10.92 10.89 10.86 10.83 -0.078 10.52 10.50 10.47 10.44 10.41 10.39 2 10.64 10.61 10.58 10.55 -0.076 10.26 10.23 10.20 10.18 10.15 10.12 3 10.36 10.33 10.31 10.28 -O.073 4 10.10 10.07 10.05 10.02 10.00 9.97 9.95 9 .92 9.90 9.87 9.75 9.73 9.70 9.68 9.66 9.63 -0.071 5 9.85 9.82 9.80 9.78 -0.069 6 9.61 9.58 9.56 9.54 9.52 9.49 9.47 9.45 9.42 9.40 9.29 9.27 9.25 9.22 9.20 9.18 -0.067 7 9.38 9.36 9.33 9.3r - l0 9.O7 9.05 9.03 9.01 8.99 8.97 0.065 8 9.16 9.14 9.12 9. - 9 8.95 8.93 8.91 8.89 8.87 8.85 8.83 8.81 8.79 8.77 0.063 8.67 8.65 8.63 8.61 8.59 8.58 -0.061 10 8.7s 8.73 8.71 8.69 -0.059 11 8.56 8.54 8.52 8.50 8.48 8.46 8.45 8.43 8.4r 8.39 8.30 8.29 8.27 8.25 8.23 8.22 -0.058 12 8.37 8.36 8.34 8.32 -0.056 t3 8.20 8.18 8.17 8.15 8.13 8.12 8.10 8.08 8.06 8.05 .98 7 .97 7 .95 7.94 1.92 7.90 7.89 -0.055 14 8.03 8.02 8.00 7 - 7.83 8.81 7.80 7.78 7.76 7.75 7.73 0.053 15 7.87 7.86 7.84 -0.052 7.70 7.69 7.67 7.66 7.65 7.63 7.62 7.60 7.59 t6 7.72 -0.051 7.56 7.54 7.53 7.52 7.50 7.49 7.48 7.46 7.45 t7 7.57 -0.049 18 7.43 7.42 7.41 7.39 7.38 7.37 7.35 7.34 7.33 7.31 '7 '.r7, -0.048 19 7.30 7.29 7.27 7.26 1 )< 1 )) 7.21 7.20 7.18 7 7.12 7.11 7.09 7.08 7 .O7 7.06 -0.047 20 7.17 7.16 .ls 7.13 -0.046 21 7.O5 7.03 7.02 7.01 7.00 6,99 6 .97 6.96 6.95 6.94 -0.045 22 6.93 6.92 6.90 6.89 6.88 6.87 6.86 6.85 6.84 6.82

For personal use only. -0.044 23 6.81 6.80 6.70 6.78 6.77 6.76 6.75 6.73 6.72 6.71 -0.044 24 6.70 6.69 6.68 6.67 6.66 6.65 6.64 6.63 6.62 6.61 -0.043 25 6.60 6.59 6.57 6.56 6.55 6.s4 6.53 6.52 6.51 6.50 26 6.48 6.47 6.46 6.45 6.44 6.43 6.42 6.41 6.40 -0.042 6.49 -0.042 27 6.39 6.38 6.37 6.36 6.3s 6.34 6.33 6.32 6.31 6.30 28 6.29 6.28 6.27 6.26 6.25 6.24 6.23 6.22 6.21 6.20 -0.041 -0.041 29 6.19 6.18 6.17 6.16 6.15 6.14 6.13 6.12 6.12 6.11 30 6.10 6.09 6.08 6.07 6.06 6.05 6.04 6.03 6.02 6.01 -0.041 31 6.00 5.99 5.98 5.97 5.97 5.96 5.95 5.94 5.93 5.92 - 0.040 32 s .91 5.90 5.89 5.88 5.87 5.86 5.85 5.84 5.83 5.82 -0.040 33 s.82 5.81 5.80 5.79 5.78 5.77 s.76 5.75 5.74 5.73 - 0.040 34 5.72 5.71, 5.70 5.69 5.68 5.68 5.67 5.66 5.65 s.64 -0.040 35 5.63 5.62 5.61 5.60 5.59 5.58 5.57 5.56 5.55 5.s4 -0.040 36 5.53 5.52 5.51 5.51 5.50 s .49 5.48 5.47 5.46 5.45 -0.040 37 s.44 5.43 5.42 5.4r 5.40 5.39 5.38 5.37 5.36 5.35 - 0.041 38 5.34 5.33 5.32 5.31 5.30 5.29 s.28 s.27 5.26 s.25 - 0.041 39 5.24 5.23 s.22 5.21 5.20 5.1.9 5.18 5.17 5.16 5.15 -0.041 40 5.14

coastal Atlantic inlets such as Bedford Basrn sive study of the oceanographic characteristics of (Krauel 1969) and Petpeswick Inlet (Platt and a number of mainland British Columbia and Van-

J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 Irwin 1972), surface water is close to saturation couver Island inlets. These areas are important to on a year-round basis while bottom water can commercial and recreational fisheries. They are have seasonally low oxygen levels of 4O and OVo also attractive as sites for location of oxygen- saturation in the two areas, respectively. depleting industries such as pulp mills. In general, Pickard (1961, 1963) provided a comprehen- oxygen levels are high in the surface waters of DAVIS: REVIEW OF OXYGEN REQUIREMENTS OF AQUATIC LIFE 2301

these inlets, whereasthe deep inlet water is often via the gills (Randall l97O). In the tissues, higher low in oxygen. CO, levels shift the blood curve to the right In Vancouver Island inlet studies.Pickard en- causing release of oxygen. countered considerable variability in dissolved The oxygen tension where the blood ceases to oxygen. He found vertical stratification related to be fully oxygen saturated is indicative of a limit- temperature and salinity variance. Horizontal ing oxygen condition for fish. Under these con- oxygen stratification was due to pockets of photo- ditions more circulatory and ventilatory work synthesis,or respiration and decay or organics. must be done to meet the oxygen requirements of At depths greater than 100 m, oxygen levels were the tissues. Indeed, even at PO2's above the point usually lessthan 4 ml O2/liter (5.7 mglliter) and where arterial blood ceases to be saturated as in many instancesthey were below 1 ml Orlliter PO, drops, a critical point is reached owing to ( 1.4 mglliter) . the need to maintain a gradient between water Mainland B.C. inletsreceive considerable fresh- and blood to drive oxygen into the blood. Jones water runoff of varying volume flow, chiefly from et al. ( l97O), on the basis of data for rainbow glaciers.On this topic, Pickard (1961) has stated: trout at 5 C, suggestedthat a PO2 of 118 mm Hg "Generally the large-runoff inlets show less was necessary to maintain a proper gradient for variable dissolvedoxygen values along an inlet at oxygen uptake. Randall (1970) calculated that any depth than do small runoff inlets. Super- the internal-external gradient for trout should be saturation of the upper layers is common and 20 mm Hg PO2. C. M. Wood (unpublished data) there is often an oxygen maximum just below the noted physiological signs of hypoxia 20 mm Hg halocline of the larger-runoffinlets. A few small- PO, above the point where the blood ceased to runoff inlets have a mid-depth oxygen minimum be fully saturated. This relationship was related in which the lowest values are at the inlet head. to the shape of the blood curve such that when it Dissolvedoxygen values of less than 2 ml/l are shifted with temperature so did the PO2 threshold not common in any mainland inlets and zero for hypoxia responses. valueshave not been definitely recorded." Useful dissolvedoxygen profiles for B.C. inlets are shownin Pickard (1961, 1963). VBNtIretlrou, CncuretIoN, AND Resprneronv DepeNpBNce Oxygen Requirements Fish of Ventilatory and circulatory changes have been A summary of literature values of incipient observed in a number of fish species in response to hypoxia. Rainbow trout (Holeton and Randall For personal use only. oxygen responsethresholds for Canadian aquatic life appearsin Table 4A-D. A detailed descrip- 1967a, b) and carp (Garey 1967) show eleva- tion of the summarizedresponses and the rationale tions in both rate and amplitude of breathing for includingeach of themfollows. and decreased heart rate in response to low oxygen. In trout the stroke volume output of the cardiac Br-oon OxycBN DrssocrelroNCunves heart also increases, thus maintaining output as heart rate decreases. The gill transfer The process of diffusion of oxygen into the factor for oxygen (a measure of the ability of blood dependson a partial pressure difference, the gills to transfer oxygen per unit gradient) describing a gradient between blood and water. increases, gill water flow goes up, and venous In many fish the respiratorypigment hemoglobin oxygen tension drops. All these factors operate has a high affinity for oxygen which enablesit to to maintain oxygen uptake in the face of reduced act as an oxygentransport mechanism. The blood oxygen availability. oxygen dissociation curve for fish relates the In understanding effects of low oxygen on percentagesaturation of the blood to the oxygen metabolism, it is useful to refer to Fig. 2 which partial pressure (PO2) applied. The hemoglobin embodies the classical concepts of Fry G951). curve maintains the gradient betweenwater and Metabolic rate (oxygen uptake rate) is shown blood, and blood and tissues,and therefore pro- plotted against oxygen tension. Standard met- motesa high rate of gas ransfer. abolic rate was defined by Brett (1962) as the Figure 1 illustrates that rainbow trout blood minimal metabolic rate accompanying the energy remains nearly LOOVosaturated with oxygen until cost of maintenance, measured under laboratory

J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 PO, drops below 80 mm Hg. These data also conditions. It is close to, but slightly higher than, indicate how an increase in either temperature the term "basal metabolic rate" used by other or CO2 tension shifts the curve to the right. workers. The point at which available oxygen Arterial blood in fish has a low PCO, owing to the level coincides with the oxygen needs for bare high water solubility of Ca, and easeof CO2 loss maintenance of bodily functions is termed the 2302 J. FISH. RES. BOARD CAN,. VOL, 32(IZ), 1975

Tanre 4. The incipient oxygen responsethresholds for various fish groups and habitats gatheredfrom the literature with emphasison Canadian species.The rationalesfor choosing the reported responseand its significanceare reported in the following pages 2301-2311.In most instances,oxygen responsethresholds were found in only one form of terminology (e.g. column 6 - mg Ozlliter and the others in the table were calculated. Calculations for freshwater fish made use of the reported temperatureand the O, solubility data in Tables 1 and 2 while those for nonanadromous fish in sea water used the data in Table 3 and an assumedsalinity of 28"1o.It is stressedthat the responselevels reported are incipient oxygen levels where effectsfirst becomeapparent thus providing a "biological indication" of the onset of hypoxic stress.A) Freshwater species,B) Marine nonanadromous species,C) Anadromous species,D) Eggs and larvae (freshwaterand marine species).

Level of dissolved oxygen Temp Response to oxygen Species Size (c) PO2-mm Hg ml O2lliter mg Ozlliter %Satn. level Reference

A. Freshwater species Arctic char, t+ nS 25 1. 53 2.18 15.8 "signs ofasphyxia Holeton Ssluelinus and loss of equilibrium" (1973) alpinus brown bullhead, 43-127 9-10 4.874.76 6.95-6.80 38 .0 onset of oxygen - Grigg Ictalurus nebulosus depe_ndentoxygen (1969) uptake Rainbow trout, 682-1t36 20 78 3.20 4.59 50 below this level blood Irving et al. Salmo gairdneri is not fully saturated (1941) with oxygen 120-250 8.5-15 80-100 3 .63-5.14 5 .18-7 .34 50.7-63 .7 circulatory changes Rmdall occur, including a and Smith slowing of heart (1967) cafp, 77-350 e 10 50 2.51 3 .59 31.7 standard oxygen up- Beamish Cyprinus carpio take elevated (de- (1964) 30-600 g 20 80 1to 4.71 51 .3 pressedat lower levels) 235-?85g t3.3-25 80 2.74-3.O4 5.394.34 50.9-51 . 6 blood ceased to be ltazawa fully saturatedwith (1970) 0: below this level Walleye, 2yr-old 22 3s.2-70.4 2.8-1.4 4-2.O 45.3-22.7 loss ofnegative pho- Scherer Stizostedion uitreum totaxis (light avoid- (1971) ance behaYior) 70.4-96.8 3 .85-2.8 5.54.0 45.3-62.3 increasedmobility, "darting" behavior Largemouth bass, 5-9 3.15 4.5 some indication of Whitnore Micropterus 9m avoidancebehavior etal. salmonides 1.1 1.5 narked avoidance (1960) Brook trout 682-1136 20 77.95 3.21 4.59 50 blood ceasesto be Irving et al, For personal use only. (speckled trout) g fully satd. with 02 (1941) Saluelinus below this leYel fontinalis 17-65 5 100 s .66 8.09 05,z onsetofO2-dependent Graham metabolism (1949) 8 80 4.19 5.99 50.7 reduced cruising speed 20 154 6.34 9.06 98.8 onset of 02 dependent metabolism 5J0 116.9-118.7 6.724.82 9.G6.88 75 reduced activity, all temps. 56-140 10,15 80 4.03-3.63 5.75-5.18 50.?-51.0 standard oxygen up- Beamish g take reduced below (1964) this level Brown trout, 682-1136 20 7'1.95 3.21 4.s9 50 blood ceasesto b€ Irving et al. Salmo ffuttq g fully satd. with Oz 0941) below this level Rainbow trout, 13.3+1.4 17!.5 l)o.o 6.82 9.74 100 any reduction in DDwning Salmo gairdneri cm oxygen led to more (1954) rapid death in cyanide 20 mos old 8-10 78.85-79.95 4.16-3.97 s .94-5.67 50 43f .redtctior in . Jones maximumswimming (l97lb) speed 2t_23 77 .85-77 .6 3.15-3.04 4.5M.34 50 3O%.reduction in . maxrmum swmmrng speed 235-5I0 2.3-13 100 6.114.71 8.73-6.74 63.1-63.6 blood is not fully ltazawa satd. with oxygen (1970) below this level

l) 78.45 3.55 5 .08 50 altered respiratory Kutty quotient, little capacity (1968a) J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 for anaerobic metabolism below this level 80-100 3.634.53 5.18-6.47 5I.0-63.7 changesinoxygen Ratrdall transfer factor and er al. (1967) efectiveness of Ou oxchange occur DAVIS: REVIEW OF OXYGEN REQUIREMENTS OF AQUATIC LIFE 2303

T,qsrs 4. (Continued)

Level of dissolved oxygen TempTemn RgsDonseResDonseto oxygen Species Size (C) PO2-mm Hg ml O2lliter mg Ozlliter 7, Satr. level Reference

400-600 13.5 80 3 .74 5 . 35 51 .0 breathing amplitude Hughes and b,;gcarnressure r?Bro8i. Itt " approx.30O 10,15, 80 3.3O-4.03 4.?1-5.75 50.7-51-3belowthislevelblood Cameron g 20 is not fully satd. with (1971) oxygen 17.5 93.8 4. 05 5 .78 60 toxicity of zinc, lead, Llovd copper_,phenols.in- (1961) creasedmarKeoly below this level Largemouthbass, juvenile 25 92.3-110.7 3.54.2 5-6 59.7-71.6 final (maximum sus- Dahlberg, Micropterus tained) swimming et al' (1968) salmoides speed reduced below this level Bluegill, 5-9 2.1 3.0 some avoidance Whitmore Lepomis cm behavior et al. (1960) macrochirus 1.1 1.5 strong aYoidance B. Marine nonanadromous species Pile perch, adults l1 80 3.19 4.56 50. 8 blood ceasesto be Webb and Rhacochilus aacca fully 02 saturated Brett below this level (1972) Dogfish, 2.5-6.0 It5 4.68 6.69 72.92 blood ceasesto be Lenfant and Squalus suckleyi kg fullv O' saturated Johansen bel6w this level (1966) Dogfish, 150-600 t2-14 80 3.12-2.95 4.464.20 50.8-51.0 Oxygen-dependent Hughesand Scyliothinus g metabolism begins Umezawa canicula' below this level (1968a) Dragonet, 7O-14O 1t-12 125 4 .98-4.88 7 .12-6.9.'7 79.4 Oxygen-dependent Hughes and Callioq)mus b,ra^ g metabolism below Ijmezawa this level (1968b) 100 3.97-3.90 5.67-5.58 63.5 altered heart rate Dragonet, 80-120 80 increased ventilatory Hughes and Callioqlmus lJ)raa muscle activity below Ballintijn this level (1968) Ratfish, 11 150 5 .98 8 .54 95.2 blood ceasesto be llanson Hydrolagus colliei fully 02 saturated (1967) below this level Atlmtic cod. | .14-2.33 5 158.2 7.14 10.20 100 anv reduction in Saunders Gadus morhua kg anibient 02 level (1963)

For personal use only. -tilatoryDroduces rise in ven- water flow C. Anadromous species Steelhead. Salmo gairdneri - seefreshwater species Sockeyesalmon, 50 g 20-24 155.9-154.9 6.42-5.9'1 9.17-8.53 100 available oxygen level Brett Oncorhvnchus nerka appears to limit active (1964) metabolism and muimum swimming speed 1579 e 100 4.72 6.74 63.6 blood ceasesto be Davis fully 02 saturated (1973) below this level | .5-l .7 15 78.45 3.55 5.O7 50 eleYated blood and Randall kg buccal pressure and and Smith breathing rate increased (1967) Coho salmon, 6 .3-11 "summer 3.15 4.5 erratic aYoidance Whitnore Oncorhynchus cm tempera- behavior et al. (1960) kisutch tures" 5. 1-14.8 12!1 130.8 6.3 9.0 83.1 below this level acute Hicks and cm mortality in kraft Dewitt pulpnill effluent (1971) increased Juvenile 10-20 157.7-155.9 7.93-6.42 11.33-9.17 100 reduction ofOz below Davis et al. saturationproduced (1963) some lowering of maximum sustained swimming speed 155.9 6.42 9.17 100 as above Dahlberg J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 et al. (1968) 13G67.9 5.6-2.8 8.M.0 87 .243 .6 growth rate propor- Ilermann tional to oxygen level (t958) with best growth at 8 .0 mg/liter, lowest at 4.0 mg/liter 2304 J. FrSH. RES. BOARD CAN., VOL. 32(12),197s

TAsr-r 4. (Concluded)

Level of dissolved oxygen Temp Response to oxygen Speci€s (c) PO:-mm Hg ml Or/liter mg Oz/liter 7, Satn. level Referenca

Chinook salmon, 6.3-11 "summer 3.15 4.5 marked avoidance of Whitmore Oncorhynchus cm temps" this level in summer et al. (1960) tshawltscha "fall little avoidance of temps" this level in fall Juveniles 10-20 157.7-155.9 7.93-6.42 11.33-9.17 100 reduction of 02 Davis et al. below saturation pro- (1963) duced some lowering of maximal sustained swimming sp€ed Atlantic salmon, 87-135 15 69.6 3.15 4.5 44.33 Salmon stop swimming Kutty md Salmo sclar g at a speed of 55 Saunders cm/s at Oz Ievels (L973) below this. Faster swimming tequirs more oxygen American shad, 1.75-2.1 2.5-3.0 threshold for nigra- Chittenden Alosa sapidissima tion through (1973) polluted ileas 2.8 4.0 necessary for spawilng areas D. Eggsand larvae Rainbow trout, I +8 10+r 100 5.03 7.18 63.4 elevated heart and Holeton larvae, day breathing rates below (1971) Salmo gairdneri old this level. Brady- larvae cardia (heart rate slow$ sts in at lower 02 levels Chum salmon eggs, early 10 13.9 8.8 retardeddeyelopment, Alderdice Oncorhynchusketa stage deformities, mortal- et al. (t958) eggs ity, respiratory 02- deoendence pre-hatch 10 >97.4 > 4.9 >7 .0 > 61.8 oxygen level required eggs for normal deYelop- ment and non 02- dependent metabolism 5 day 8.0-8.2 22.2 14 .O7 critical oxygen level wickett eggs for supply of oxygen (1954) demand and non 02- dependent metabolism (eyed) 3.A.9 > 60.3b >3.5b >5.0 > 38.lb 85 day eggs For personal use only. Atlantic salmon, early 5.5 9.62 .53 0.76 6.09 As above Lindroth Salmo salar eggs (r942) near (from hatching s 71.7 4.06 5.80 45.31 Wickett hatching t7 160.8 7.O .100 102.67 19s4) Atlantic salmon, eyed 10 43.14 2.17 3.r 27 .36 critical 02 level for Hayes et al. Salmo salar hatching l0 98.83 4.97 7.1 62.67 supply of02 demand (1951)(from and non O2-depen- Wickett, dent metabolism t9s4) Northern pike, from 15,19 >5.18-5.66 >2.16-2.35 > 3.35-3.09 > 33.0 necessary02 level for Siefert Esox lucius fertilization Proper hatching, et al. to survival and (r973) feeding development larvae Mummichog," fertilization 20 101.2 3.15 4.5 64.9 reduced hatching at Voyer and Fundulus to this level compared Hennekey heteroclitus hatching to 7.5 mg/liter O2 (r972) Pacific cod, fertilization 3-5 >2-3 oxygen level required Alderdice Gadus to for optimal hatching and macrocephalus hatching at 15%" salinity Forrester (r971)

.European species- representatives of this family found in Canadian Atlantic waters. bCalculations based on 4 C. "Estuarine fish - calculations based on salinity of 30%" .

"incipient lethal tension." Below this level orga- Tables 4A-D as the "no-effect oxygen threshold" nisms resist for a time but eventually die. The that affords good protection for fish species.This point at which metabolic rate ceasesto be de- relationshipseems to hold for a variety of species, J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 pendent on available oxygen is termed the "in- from fish eggs to invertebrates, and will be fre- cipient limiting tension." It is identical with the quently referred to in this paper. In animals critical oxygen tension of Prosser and Brown tolerant of low oxygen, the curve in Fig. 2 is (1962), termed Pc, and is frequently given in pushed to the left, while in animals requiring DAVIS: REVIEW OF OXYGEN REQUIREMENTS OF AQUATIC LIFE 2305

severe enough to provoke the above responses -a occur at oxygen levels well above those acutely z80 6./- o lethal to fish. The responsesof fish to hypoxia representsome F '(u", 860 form of compensationor adjustment of bodily f F processes. Fish can resist or tolerate reduced 640 levels of oxygen for short periods. The successof I tolerance depends on species,the oxygen levels, *zo and on environmental factors, particularly temperature. Use of regulatory or compensatory o mechanismsrequires energy expenditure and will 20 .lO @ consequently reduce energy reserves for swim- POz mmH9 AT IOC ming, feeding, avoiding predators,and other activities.

ENBncBrrcs ANDLow Oxvceu 280 o Considerablework has been done on the oxy- F gen requirements of quiescent flsh under labora- ro 60 the earlier work on f tory conditions. Much of F harmful or lethal oxygen levels is of this nature. 340 Fry (1957) recognizedthat the respiratory de- Szo pendencephenomenon should be studied in rela- / tion to active metabolism,i.e. the level of oxygen uptake accompanyingmaximal swimming activity. 20 40 60 80 Brett (1964) studied oxygen uptake and swim- PO. mm Hg AT 15C ming performance of young sockeye salrnon and obtained evidence that available oxygen levels may limit active metabolic rate above 15 C roo (Fig. 3). Brett (1970) also determinedthe oxygen requirements for fingerling sockeye salmon z80 at 20 C during various important activities: o tr

For personal use only. Oz Costof energy /. active E, .f Activity expenditure metabolicrate F 840 feeding - 450 mg/kg per h ss.4% max. ration Szo feeding- main- 300 mg/kg per h 37.3 ,/ tenanceration o migrating up 625 mg/kg per h 75.0 o20406080 vigorous river tO, mm Hg A1 2O C aggression 180 mg/kg per h 22.9 In light of the abovedata, examinationof Fig. Frc. 1. Blood for rain- oxygen dissociation curves 3 indicates that a reduction in oxygen to 5O% bow trout (Salmo gairdneri) blood, plotted as Oz tension vs. percentage oxygen saturation in the blood at saturation would severely limit energy expendi- three temperatures. COz tensions accompanying each ture for migrating or maximum feeding at the curve are indicated below it in parentheses (from higher temperatures.Fry (1957) stated: Cameron1971). "Any reduction of the oxygen content below the level where the active metabolic rate begins considerable oxygen the curve shifts right. Thus to be restricted is probably unfavorable to the the oxygen tension that produces respiratory de- speciesconcerned. From the ecologicalpoint of 'incipient pendence varies with species. view this limiting level' (the critical Different species of teleosts (bony fish) vary in level under conditions of activity) can be taken ability to regulate oxygen uptake over a range of as the point where oxygen content becomes un- J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 available oxygen tensions. Elasmobranchs (car- suitable." tilaginous fish) are apparently less able to regu- In a theoretical analysis,Jones (1971a) pro- late oxygen uptake in this way (Randall 1970). posed that for salmonid fish at low temperatures It should be remembered that levels of hvpoxia (5 C) the oxygencost of the cardiac pump limits 2306 J. FISH. RES. BOARD CAN., VOL. 32(12),1975

zol'lE oF ZOI{EOF RESPIRATOiY DE PENDEiEE RESPIRATORYRESUL ATIO lt| zo||E oF RESISTAXCE I ZOilE OF TOLSRAilCE

LI t

F lilctPtExr uilTt1{G TExsloil A f z (,U x o

l! o U HETAAOLIC RATE F lr9TA!{DARD E

IT{CIPIEIIT LETHALTETSIO'{

EWIROT{ET{TAL'O,

Frc. 2. Relation between standard and active (maximum) oxygen uptake rates at different environmental oxygen concentrations (from Hoar 1966).

maximal oxygen uptake during swimming; but at high temperatures (25 C) the oxygen cost of the branchial pump becomes limiting. Reductions of For personal use only. maximal swimming speed in rainbow trout of 30 and 43Vo resulted when environmental oxygen fell to 5O% of saturation at 2I-23 C and 8-10 C, respectively(Jones 1971b). o r It should be emphasized that swimming ability z in reduced oxygen may be affected by season and

I o temperature. For example, Katz et al. (1959), z z 9 r reported that 6-cm largemouth bass, Micropterus z F salmoides, could resist a water current of 25 cmls E ! f even at 02 levels of 2.O z = at 25 C in September o z mglliter. However, in December at 15-17 C o I z they were apparently unable to do so even when B oxygen content was 5.0 mg/liter. In contrast, o Davis et al. (1963) reported that any reduction from ambient oxygen at 1O-2O C usually reduced maximum sustained swimming speed in coho and chinook salmon.

ACCLIMATION TEMPERATURE_ C Bsrtavroner Rr,spoNsns ro HypoxIA Frc. 3. Active metabolism of yearling Sockeye J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 salmon (Oncorhynchus nerka) (heavy line) tested at Literature records of altered behavior of fish air-saturatedoxygen levels (dotted line). Mean t 2 sE in low oxygen are often contradictory owillg metabolic rate for elevatedoxygen (13.9 ppm) deter- perhaps, in part, to varying experimental con- mined at 20 C (circled points) (from Brett 1964). ditions and methods applied in studying fish DAVIS: REVIEW OF OXYGEN REQUIREMENTS OF AQUATIC LIFE

t I

60 j z =50

lrJ k+o G.

F tBo rlrl 20

o 20 40 60 80 too t20 t40 t60 t80 Pg. mm Hg

FIc. 4. Onset of bradycardia (slowing of heart beat rate) in rainbow trout in response to water oxygen tension. Solid line was fitted fotrlowing a statisticalanalysis of the data (from Randall and Smith 1967).

behavior. It has often been stated that fish gen- at 02 levels slightly above incipient lethal levels erally become more active in hypoxic water and (1.'75-1.9mg O2lliter) "were sluggishin their attempt to move away from the low oxygen movements,fed poorly and were susceptibleto region (Randall 1970). Avoidance behavior has disease." For personal use only. been reported for a number of species, although It is not clear whether avoidance behavior in the reported O, threshold for a given response responseto low oxygen constitutesa highly di- often varies considerably. For example, Whit- rected form of behavior. It may result simply more et al. (1960) observed that juvenile chinook from increasedlocomotor activity with more ran- salmon (Oncorhynchus tshawytscha) showed dom movement, which is satisfiedby discovery of marked avoidance of 1.5-4.5 mg Orlliter in the improved oxygen conditions.It seemslikely that summer at high temperatures but showed little avoidance behavior in low oxygen would have avoidance of 4.5 mg Orlliter in the fall. As survival value and that the presenceof this be- described earlier, problems of hypoxia may de- havior pattern suggeststhat fish periodicallymay velop at high temperatures where reduced water benefit from it. O, content and elevated metabolic rates would Implicit in a behavioralresponse to low oxygen prevail. Thus a seasonal variability in behavioral would be some means of detecting low oxygen sensitivity to dissolved oxygen does not seem water. The physiological responses to hypoxia unreasonable. are rapid, consistingof circulatory and ventilatory A number of other behavioral responses to changesin trout and tench within a few seconds hypoxia have been reported. Scherer (1971) de- of the onsetof hypoxia (Eclancher 1972; Randall scribed loss of normal avoidance of high light and Smith 1967; Fig. 4). Such rapid responses intensities (negative phototaxis) in walleye suggestthe presenceof an oxygenreceptor system (Stizostedion vitreum) when 02 fell to 24 on or near the gills. The precise location of this mgr'liter. Shepard ( 1955), studying speckled is not yet clear. The responseis rapid enoughto trout, Salvelinus "a J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 t'ontinahs, reported violent suggestthat a reflex mechanismis involved (De- burst of activity involving all the individuals in jours 1973). a sample" with evident "attempts to surface" It is also possiblethat behavioralresponses to when oxygen deficient water was introduced to low oxygen are triggered by the circulatory and test chambers. He further reported that fish held ventilatory changesnecessary to compensatefor J. FrSH. RES. BOARD CAN., VOL. 32(12),1975

-F (9 UJ = 120 gJ F z

Fz 1rJ r00 o E UJ (L if::-*;1--'-r.,-'o'-l-1--^.-lro'7-s'r ior-..r-''.. -i-_-*---n"

WEEKS Frc. 5. Growth rate in yearling eastern brook trout (Salvelinus fontinalis) in constant high (solid lines - controls) and various daily fluctuat- ing levels of oxygen (broken lines with O: range in mg O,/liter) (frorn Fry r97O).

hypoxia. Such a mechanism would help to ex- mum oxygen level for growth of young sturgeon plain the varied behavioral thresholds reported fry as 5.0-5.5mg O2lliter.Davison et al. (1959) for hypoxia, since the response might be trig- observedthat juvenilecoho salmonat 2OC or less gered at a higher 02 level when metabolic needs in the summer or fall fed well and gained weight are large (for swimming, feeding, high tempera- at 2.9 mg/liter, but concluded that their fish tures, etc.) but not when they are minimal. were "probably somewhat affected."

For personal use only. Exposure to cycling oxygen levels appeared to juveniles at Gnowrn rN REDUcED OxyceN reduce growth of largemouth bass 26 C (Stewart et al. 1967). Food conversion High environmental oxygen levels seem to en- efficiency was reduced at oxygen concentrations courage growth rates in experimental fish. Stewart below a constantO, level of 4.0 mg/liter. Simi- et al. 1967) reported that growth rate and food larly, Whitworth (1968) observedloss of weight consumption in juvenile largemouth bass, Mi- in brook trout exposedto daily fluctuations in cropterus salmoides, at 26 C increased markedly oxygen(Fig. 5). as oxygen increased to near air-saturation levels and then decreased above those levels. Herrmann AccrrvetroN ro Low OxvceN (1958) obtained similar results for juvenile coho are a number of indications that fish can salmon at 20 C as follows: There acclimate, to some degree, to lowered oxygen 2l-27 d,ay levels. Shepard (1955) showed that the lethal constant 02 level - mg O, liter weight gain O, level for brook trottt, Salvelinus fontinalis, 4 s6% could be reduced with low oxygen acclimation. s 68% He suggestedthat adjustmentsmight be made in 6 88% the oxygen carrying capacity of the blood, thus 8 92% increasing the ability to extract 02 from the He concluded that at temperatures around 20 C water. Macleod and Smith (1966) showed that the "minimal oxygen concentrations to which fatheadminnows, Pimephales promelas, increased juvenile hematocrit (packedvolume of red blood cells) in J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 coho salmon may be exposedfor relatively long periods without markedly affecting responseto low oxygen,thus making more hemo- growth, feeding, food conversion, and general globin available for 02 transport in the blood. activity, lie within the range of four to six milli- However, Cameron (1970), in assessinghemato- grams per liter." Lozinov (1956) gave the opti- logical responsesof pinfish,Lagodon rhomboides, DAVIS: REVIEW OF OXYGEN REQUIREMENTS OF AQUATIC LIFE 2309 () lrl U' o - 4 oF z 5 t F E o lr. lr- trl (9 z

=(n

AMBIENT O\YGEN mg/L

Frc. 6. Swimming ability vs. oxygen availability in goldfish (Carassius auratus). Open circles denote fish acclimated to air-saturation O, levels; closed circles indicate fish acclimated to 15Vo oxygen saturation. Acclima- tion to low oxygen did not appear to enhance swimming ability in low oxygen water under theseconditions (from Kutty 1968).

and striped mullet, Mugil cephalas, concluded low oxygen regime is slow enough to enable that changes in blood oxygen capacity induced acclimation to occur without severe physiological by low oxygen acclimation were small and of stress.However, the mechanism would be of little slight significance to respiration, rather than the help to fish suddenly encountering low-oxygen

For personal use only. extensive compensatory hemoglobin production water. Acclimation ability can be considered as previously proposed for goldfish (Prosser et al. a built-in safety factor for some speciesencounter- 19s7) . ing low oxygen conditions. I consider that there As well as resulting in blood oxygen capacity is insufficient evidence to warrant modiflcation changes, acclimation could be behavioral in of oxygen criteria to include acclimatory ability nature. It is possible that considerable energy of fish. could be expended by a nonacclimated fish reacting behaviorally to low oxygen conditions. Ac- INrr,necrroN op Low OxvcsN AND Toxrc climation could lower the magnitude of these AcBNts reactions and might thus enable conservation of energy under oxygen stress. Areas polluted with industrial waste, sewage, Acclimation that enhances survival at near- and other contaminants frequently have both a lethal conditions may not always aid active pro- low oxygen and a toxicity problem. Often a cesses. Kutty ( 1968b) found no difference in number of different wastes are discharged into a swimming speed at limiting oxygen levels in gold- body of water from various sources. The effects fish acclimated to both low and air-saturation of these discharges can be additive. Alderdice oxygen levels (Fig. 6). In addition, he observed and Brett (1957) observed an apparent increase that reduced oxygen consumption existed in low in toxicity of kraft pulpmill waste to young O2-adapted fish at a given swimming speed com- sockeye salmon in the presence of low oxygen. pared to fish held at high oxygen levels. Townsend and Cheyne (1944) reported a similar There is a scarcity of field data to show that toxic interaction of low oxygen and elevated J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 ability to acclimate to low O, markedly improves hydrogen ion concentrations to coho salmon. survival chances of fish populations. Any such Markedly increased toxicity of ammonia solu- ability to adapt to low oxygen should be useful tions, salts of zinc, lead, and copper and a mix- to some degree, especially if the transition to a ture of monohydric phenols, was evident in 23l0 J. FrSH. RES. BOARD CAN., VOL. 32(12),t91s

rainbow trout when oxygen levels fell below 6O7o absorption and better growth in S-day-old Salmo saturation aI 17.5 C (I-loyd 196l). Lloyd felt salar larvae reared for 25 days at 6.8-7.5 mg that toxicant delivery to the gills, and its rate of O2lliter, compared to those reared at 4.5-5.0 mg uptake, was enhancedby the increasedrespira- O2/liter. The latter group weighed less than one tory flow necessary to counteract hypoxic con- half of the high-oxygen reared group and had ditions. Presumably high water temperatures, one third of the yolk sac unabsorbed. hyperactivity,or some other metabolism-stimulat- Circulatory and ventilatory responses of fish ing condition elevatingrespiratory activity, would larvae to low oxygen have been described. Holeton producea similarresult. (1971) observed that oxygen tensions below 100 mm Hg stimulated heart rate and breathing rate Ecc eNo Lenver- DEvrropN4ptrr rN Low OxycEN in l-day-old rainbow trout larvae. Similar, but more marked responses, were seen in 8-day-old There are several studies on the dissolved larvae. In these older larvae, POt levels of 45-50 oxygen requirementsof developingfish eggs and mm Hg produced reduced breathing rate and in- larvae. Like fish, eggs also show respiratory decreased depth (amplitude) of breathing. pendence(Fry 1957) (Fig. 7). Alderdiceet al. There is very little information on the dissolved (1957) reported a gradual increase in the dis- oxygen requirements of marine fish eggs. It seems solvedoxygen requirements of chum salmon eggs, likely that marine eggs, when close to hatching, Oncorhynchusketa, as developmentprogressed. require fairly high oxygen levels similar to eggs Eggs at early stagesof incubation required about of freshwater species. Conceivably, an oxygen 1 mg O2lliter, while those about to hatch re- level acceptable to adult marine flsh may be un- quired over 7 mg Or/liter. Eggs held at low suitable for marine eggs - a factor that could oxygen tensionsshowed reduced growth and re- easily be overlooked! tarded development.Deformities in embryos exposed to hypoxia were observed,with mortality occurring at the stagewhen the circulatory system Summaryof OxygenRequirements of Fish develops. Other workers report similar increased Reduction in the level of available oxygen has oxygen requirementsof eggsas developmentpro- a marked effect on many physiological, biochemi- ceeds (Guilidov 1969; Hayes 1949; Lindroth cal, and behavioral processes in fish. The oxygen I 942;Wickett 1954). Ievel where such effects first become apparent - Larval fish, like eggs, are affected by reduced i.e. the incipient oxygen response threshold, has oxygen. The oxygen demand of larval flsh in- been used throughout this report in the derivation creasesmarkedly with age (Sharmardina 1954). For personal use only. of oxygen criteria selected to assessadverse efiects Nikiforov (1952) reported complete yolk sac on fish. Restriction in the supply of oxygen available for metabolic processes including swimming, migrating, and feeding are likely caused by hypoxia. Adequate oxygen levels for such activities are tr necessary for survival of healthy fish populations. I fish are noticeably in- @ Oxygen requirements of (9 fluenced by season, temperature, and activity. The lrJ oxygen tension where respiratory dependence begins is considered an important lower limit for E tolerable available oxygen. Effects of hypoxia E as d on metabolic processes and swimming ability, a well as O, levels causing the onset of respiratory l dependence, are thus considered good indicators of the incipient suble,thal effect threshold for low oxygen. The blood oxygen dissociation curve delineates the water oxygen tension where the blood ceases to be fully oxygen saturated. For optimal gas ex- pg.mm H0 change, water PO2's, preferably 20 mm Hg above J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 Frc. 7. Oxygen uptake rates in eggs and larvae of that saturation point are required in trout to Atlantic salmon, Salmo salar, at 10 C, illustrating maintain the necessary oxygen gradient at the respiratory dependence and the influence of the egg gills. Oxygen dissociation curves, therefore, pro- capsule(from Fry 1957). vide an indication of the point where available DAVIS: REVIEW OF OXYGEN REQUIREMENTS OF AQUATIC LIFE 23tl

oxygen limits or influences respiratory and circu- dependence, retarded growth, reduced yolk sac latory functions. The shape of the blood curve absorption, developmental deformities, and mor- and position of the lirniting O, tension are in- tality. As development proceeds, the oxygen re- fluenced by temperature and CO2, such that quirements of both eggs and larvae increase. increases in these factors elevate the PO2 required Trout larvae exhibit circulatory and respiratory to fully saturate the blood. Limiting oxygen ten- effects of low oxygen. Most data on the effect of sions. therefore. can be derived from blood curves low oxygen on fish eggs and larvae are confined and are useful for defining low oxygen effects on to freshwater species, particularly salmonids, and fish. In addition, oxygen response thresholds for there is little informatiton for marine eggs and circulatory and ventilatory systems have been larvae. described. It is particularly evident that much of our Low oxygen levels have been shown to influ- knowledge of low 02 effects on fish tends to be ence growth rate, food conversion efficiency, and confined to freshwater species, particularly salm- feeding in some species. In some cases, cycling onids. There is a great lack of knowledge available oxygen levels appear to adversely affect growth on the oxygen requirements and tolerances of under laboratory conditions. As growth is an nonsalmonid species and their eggs and larvae. expression of the net product of metabolic func- The need for more research in this area is strongly tions, it is a good indicator of an overall effect emphasized. of low oxygen. Therefore, adverse effects of low 02 on growth constitute a useful criterion for Oxygen Requirements of Aquatic Invertebrates permissibly low oxygen levels. There is extensive literature pertaining to mea- Avoidance behavior has been reported for a surement of metabolic rate (oxygen uptake) of number of species in response to low oxygen, al- aquatic invertebrates under various environmental though reports of O, thresholds to initiate this conditions such as temperature, salinity, pH, CO2 behavior vary considerably. Observed behavior tension, etc. Indeed, a considerable body of patterns in low 02 include increased activity, poor knowledge is available on the interaction of en- feeding behavior, and altered phototaxis. Avoid- vironmental oxygen availability, oxygen uptake, ance behavior is likely a useful protective mecha- and ventilation rates for many freshwater, marine, nism that enhances the survival of some species. and estuarine organisms. The following is an It is apparent that low oxygen in the presence attempt to summarize some of the general findings of some toxicants enhances the lethal effect of of this rather extensive literature. Unlike the fish those toxicants on some fish. Low oxygen levels section of this report, this section is not mainly producing metabolic stress could lower the ability For personal use only. confined to a discussion of purely Canadian of fish to resist toxicants as well as increase toxi- species. Wherever possible, however, attention is cant uptake rate via elevated ventilatory water given to reporting results from work with Cana- flow. For these reasons the need for sound scien- dian species.In my opinion, knowledge of inverte- tific dissolved oxygen criteria should be obvious, brate community oxygen requirements is too in- especially in geographical areas polluted by dis- complete to warrant the setting of definite "eco- charges toxic to fish. for invertebrate Some fish show ability to acclimate to lowered logically safe" oxygen criteria discussion was de- ambient oxygen. However, the degree of advan- communities. The following general knowledge and tage gained is not clear. Acclimation can enhance signed to review current general recommenda- blood oxygen capacity and oxygen utilization attempts to arrive at some by those attempting to somewhat but may not aid active swimming per- tions that can be followed levels for prolonged survival formance. This acclimation phenomenon may be define safe oxygen useful to fish subjected to gradual reductions in of invertebrate communities. oxygen levels, but would be of little advantage Aenosrc eNo ANeenoBIc METABoLISM when encountering reduced oxygen levels for the first time, especially if the O, depression was Most aquatic organisms can utilize several severe. For these reasons, the application of metabolic pathways as a means of obtaining acclimation phenomena to water oxygen criteria energy. These processes can be aerobic (utilizing for fish protection has not been attempted in a oxygen) or anaerobic. Anaerobic processes yield subsequent section of this report and can be con- energy in the absence of oxygen. An excellent

J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 sidered only as a possible safety factor enhancing discussion of the various metabolic pathways, the flsh's resistance to low oxygen. their evolution, and relationship to oxygen avail- Developing fish eggs and larvae show a number ability can be found in Hochachka and Somero of responses to low oxygen including respiratory ( 1973) . 2312 J. FrSH. RES. BOARD CAN., VOL. 32(12),1975

Tasrr 5. Summary of A) oxygen independent (regulated Oz uptake) and B) oxygen dependent (O2 conforming) groups of organisms(from Prosserand Brown 1962).

A) Oxygen independent Most protozoa - Tetrahymera,Paramecium, Trypanosoma Coelenterates- Hydra between 10 and 100f. 02 in the gasephase Annelids - TubiJbx,Lumbricus, the leechesGlossiphonia and Hirudo,larvae of some polychaetes,Pc : 40 to 50 mm Echinoderm eggs- Arbacia, unfertilized, Pc : 40; fertilized, Pc : 50 mm Hg A few parasitic worms -Trichinella, Pc: 8 mm; Nematodirus, Haemonchus,Rhabdilis elegans,Pc: I21 mm; Rhabditis strongloides,Pc : 58.5 mm Molluscs-clam Mya,Pc: 40 to 50 mm; oyster,Pc: 100 mm; snail Ancylus,Pc: 80 mm; snail Australabrus, Pc : 30 mm; Mytilus,Pc: 50'Z air saturation Crustacea- copepod Calanus, Pc : 204 ml Or/liter; crayfish, Pc : 40 mm; crab Pugettia, Pc : 70 mml Uca pugilator and Uca pugnax, Pc : 4 mm Insects- termite termopsrs,Pc : 38 mm; diapausingcecropia pupae, Pc : 23 to 28 mm; severalchironomid larvae, Pc:55to68mm Most aquatic vertebrates,Pc : 30 mm Hg Crucian carp - 30 mm Hg at 5 C A11terrestrial vertebrates;probably all terrestrial insects B) Oxygen dependent Protozoa - Spirostomum Numerous coelenterates- actinians, Cas siopea FreeJiving worms - Sipunculus,Urechis, leeches Prscrco Ia and Erpobdella,Nereis Most parastic worms - trematodes- Fasciola,Schistosoma, cestode Diphyllobothriun, nematodesAscaris, Litomo- soides,Limax, strongyleslarvae Some molluscs and crustaceans- Limes, Limulus, Homarus, series of marine crustaceansdaphnid Simocephalus fifth instar conforms over environmental range 14.6 to 1.1 cms O2/liter Echinoderm adults - starfish, sea urchins Some aquatic insects- Ephemera,Anatopynia, Tanytarsus Few vertebrates- toadfish, Triturus pynhogasler, cutaneousrespiration

The degree to which organisrns can utilize It should be emphasized that anaerobic pro- anaerobic processes varies considerably and thus cessesyield less energy per unit glucose metab- determines aerobic processes(Lehninger For personal use only. the tolerance of individual species to olized comparedto low oxygen conditions. Anaerobiosis is common 1965). The utilization of anaerobicpathways is in parasites and some, such as the intestinal therefore accompanied by some reduction of flagellates of termites, may be poisoned by small availableenergy. This is likely not a seriouscon- amounts of oxygen (Prosser and Brown 1.962). sequencefor small, relatively inactive speciesbut Others such as mud-dwelling tubificid worms can would be problematical to larger, active species. live for long periods in water nearly devoid of A reduction in available oxygen would therefore oxygen. Many organisms are normally aerobic most seriously affect the more active, high-energy but can survive many hours without oxygen (e.g. utilizing members of a community. These gen- frogs, earthworms, cockroaches, aquatic snails) eralizations will be discussedin the following by utilizing anaerobic means of energy produc- sections on animals inhabitine different environ- tion. In contrast, many aerobic animals are highly ments. dependent on oxygen. Typically, these animals (accumu- can build up only a brief oxygen debt REsprneronvDrpnNonNcn rN INvERTEBRATEs lated metabolic products of anaerobic metabolism, such as lactic acid, or other compounds, which Earlier it was pointed out that the phenomenon must be later oxidized), particularly in their of respiratory dependence(a correspondenceof muscles. Examples of these organisms are birds, the rate of oxygen uptake with availableoxygen mammals, many adult insects, and cephalopod level) occursin many fish as well as in their eggs molluscs (Prosser and Brown 1962). In general, and larvae. Often there is a critical oxygen ten- animals with high metabolic rates are less tolerant sion for invertebratesas well (Pc - Prosserand

J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 of low 02 than sluggish forms; early eggs and Brown 1962) below which respiratory dependence cysts and small organisms are often tolerant of begins. Prosser and Brown describe organisms low oxygen, as are hibernating or behaviorally- whoseoxygen uptake rate is independentof avail- inactive organisms. able 02 level abovethe Pc level (Table 5,A.)and DAVIS: REVIEW OF OXYGEN REQUIREMENTS OF AQUATIC LIFE z5 t5

others (Table 5B) whose 02 uptake rate con- Moshiri et al. ( 1970) reported dependent forms to the available O, level. respiration in the crayfish, Pacilastacus leniuscu- It can be seen from Table 5 that many aquatic lus. At 20 C over a range of 2-7 ml O2lliter invertebrates possess the ability to regulate oxy- oxygen utilization was elevated below 4.0 ml gen uptake over a range of oxygen tensions, while O2/liter (=5.7 mglliter) and ventilation de- many others show conforrnity (dependence). Fur- pressedbelow 2.5 ml O2/liter (=3.6 mglliter). thermore, the level of Pc varies considerably, Larimer and Gold (1961) found similar respira- sometimes even between closely related forms. tory dependence in the crayfish, Procambarus Nicol (1967) suggested that a number of factors simulaus,and a stimulation of ventilation when determine whether an animal is dependent or oxygen levels dropped. Hoglund (196I) showed independent of the environmental oxygen level. that the crayfish, Astacus fluviatilus, responded These factors include size, existence of a circula- to oxygen gradientsby moving from low to high tory system, diffusion distances, temperature, de- 02 concentration.Berg (1952) comparedrelated gree of locomotor activity, ability to regulate freshwater snails,Ancylus fluviatilus, and Acro- external respiration, and the existence of respira- loxus lacustns, and noted that Acroloxus could tory pigments. survive much longer anaerobic exposure than Examples of respiratory dependence and inde- Ancylus. Berg suggestedthis difierencecould be pendence will be discussed in the following related to Acroloxu,s' preference for stagnant sections. conditions. Various responsesof freshwater organisms to OxvceN RneurntvnNrs on SovrB FnesHwerBn low or declining oxygen levels have been de- INvrnrpnn,qtss scribed.Chironomid larvae and the leech,Erpob- The oxygen-sensitivity and oxygen uptake rates della testacea,are able to regulate oxygen uptake of many freshwater organisms appear to reflect and lower their Pc following acclimation to low the habitat in which they live. For example, Fox oxygen. Daphnia produce hemoglobin and turn et al. (1937) reported the following results with red after stimulation with low oxygen for about mayfly nymphs: 10 days (Prosser and Brown 1962). Donacia larvae become inactive in low oxygen water and 02 uptake (Hoffman at resumeactivity when oxygenlevels rise air satn. Pc Pc 1940). Daphnia magna show a preference for (meOrl (ml Ozl (ms O,/ fully saturated water over that only l5Vo sat- Genus Habitat c/h) liter) liter) urated, although more than an hour is required for the responseto develop (Fig. 8) (Ganning

For personal use only. Baetis swift 2.8 1.2.0 17.00 streams and Wulff 1966). Gammaruspulex (Costa 1967) Leptophlebia lake 2.1 2.5 3.60 increasesits pleopod movement in low oxygen Cloean pond 1.3 2,0 2.86 and moves out of low oxygen water. A slowly developingavoidance reaction to oxygen contents Von Brand et al. (1950) reported that Lym- up to 7 mg Orlliter was demonstrated(Fig. 9). naeidae and Physidae groups of freshwater snails Freshwater snails, Ancylus climb to- could withstand 6 h of anaerobiosis, while Planor- fluviatilus, bidae and Operculate snails survived at least 24 h. Donacia larvae (Chrysomelidae: Coleoptera) survived 168 h in closed bottles that had only = @z 0.26 ml Or/liter (0.37 mg O2/liter) at the start *9 =E of the test (Hoffman 1940). Also, Cole (1926) ze <= reported that freshwater clams, Anadontoides fer- russacianus, could live for several days in the dz absence of oxygen. These species inhabit muddy tx bottoms where oxygen may be periodically low. zo Sprague (1963) observed 5OVo mortality in 24 h JS in the isopod Asellus intermedius at 0.03 mg O2/liter, and mortality thresholds of 0.7, 22, and r020504050@7a60 4.3 mg O2lliter for the amphipods, Hyalella TIME IN MINUTES azteca, Gammarus pseudolimnaeus, and Gam-

J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 Ftc. 8. Oxygen preference test with Daphnia magna mants fascialas, respectively. Of these, A. inter- taken from a laboratory culture kept in 80Vo O,- medius is often found in polluted and deoxygen- saturated water. Dotted line refers to a 50-50% dis- ated water, whereas records of G. fasciatus tribution of animals in the two choice O, saturations inhabiting deoxygenated water are scarce. (from Ganning and Wulff 1966). 2314 J. FISH. RES. BOARD CAN., VOL. 37(12),T975

30 Uca pugnax and U. pugilator, show respiratory I independence down to a PO, of 40-50 mm Hg, o lrj and can withstand anaerobic conditions for at 525 least 1 wk (Teal and Carey 1967). = = Pacific sea urchins provide a good example of utilization of various degrees and modes of res- =20 piration related to 02 availability and demands lr, of metabolism. Strongylocentrotus drobachiensis, =15 S. franciscamzs, and S. purpuratu,s show respira- 2 tory dependence below 60-70 mm Hg PO2 (Fig. tr10 10), and below that level, oxygen tensions in C' water and coelomic fluid show close correspon- trj E- dence (Fig. 11). Indeed, these urchins appear -.2' able to reduce their internal coelomic fluid PO2 .4' even in well-aerated water, possibly utilizing energy-saving mechanisms in doing so (Johansen 12345678 and Vadas 1967). Furthermore, urchins can sur- o' mg/t vive up to 15 h exposure to moist air. The gas exchange occurring under these conditions is Flc. 9. Time for the onset of avoidance behavior to enough to support an oxygen uPtake rate 1L-1/sof low oxygen water by Gammarus pulex at 14-15 C (from Costa1967). the maximum rate observed in aerated water. Some amphipods, frequently found under rocks, logs, and algae on Pacific shores can tolerate low wards the surface of the water when dissolved oxygen. Waldichuk and Bousfield (1962) ob- oxygen drops (Berg 1952). Chironomids suspend served numerots Allorchestes angustu.t and some feeding when oxygen drops to 5-7.5Vo of satura- Anisogammarus pugettensls in surface water con- tion (Prosser and Brown 1962). taining 0.3-0.89 mg Or/liter (near a Sulphite pulp mill). C. D. Levings (unpublished cruise OxvcpN RrqurnrtmNTs oF SoME IhlrnnrroeL report - Ocean Falls Harbour, B.C.) lowered ManrNr INvBnrrsnatEs baskets of Anisogammarus confervicolus into a low oxygen layer 40 m deep. All the amphipods During the night at tide, oxygen levels in low survived 24 h exposure to O.52-1.25 ml Orlliter pools and animal may burrows drop substantially, (0.74-1.8 mg O2lliter) but died after 36 h. For personal use only. depending on community respiration rates, population density, organic decomposition, and other Oxvcpr.t RseurneNlnNTs oF BnNrrnc MenrNs factors. The lugworm, Arenicola marina, cannot OnceNrsvrs AND CoMMUNTTTES tolerate oxygen in water above 4Vo of saturation. Fully Or-saturated water is slowly toxic, reflecting Marine benthos are often exposed to low oxy- this species' tolerance and specialization for peri- gen conditions due to oxidative processes occur- odic anoxic conditions. In contrast, Sabella ring in or near the sediments that deplete water pavonina, a tubicolus polychaete normally dwelling of oxygen. The severity of the depletion depends in well-aerated water, tolerates 10% 02 saturation upon many factors including geographical posi- but dies in 4 days at 4Vo (Nicol 1967). The tion, depth, tides and currents, population struc- polychaete Nereis diversicolor reduces its rate of ture, settlement rate of organic matter, and aerobic water pumping in low 02, as does Arenicola, pos- respiration of organisms. sibly to conserve energy. Gammarus oceanicus In many instances the oxygen level most suit- from Nova Scotia tide pools avoid experimental able for benthic dwellers can be related to their anoxic conditions and become more active (Cook life habits. The amphipod Corophium arenarium and Boyd 1965). Oysters, Ostrea virginica, survive inhabits aerobic sediments, while Corophium exposure for at least a week to water containing volutator is found in anaerobic sediments. Be- less than 0.5 mg O2/liter (Mitchell 1912). Simi- havior experiments showed that C. arenarium has larly, the mussel, Mytilus edulis, can survive a significant preference for oxygenated water, several weeks without oxygen (Moore 1964). while C. volutator is indifferent (Gamble l97l). Nematodes and mites, inhabiting large coastal Numerous responses of benthic invertebrates to J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 sea weeds (Fucus, Ascophyllum) which collapse declining oxygen levels have been reported. The at low tide and consume oxygen from tide pools, octopus, Octopus dofleini, exhibits lowered arletial can survive anaerobic conditions for 16 h at blood oxygen levels and elevated cardiac output 25 C (Wieser and Kanwisher 1959). Marsh crabs, when 02 partial pressure falls below 120 mm Hg DAVIS: REVIEW OF OXYGEN REQUIREMENTS OF AQUATIC LIFE 2315

o G I STRoNoYr,ocENrRorus too I @EE!! ': E q OVO2 . \ OXYGENUPTAKE t 90o OPoz coELoMlc FLUID O 5 z. 8 8O ur n O vA F OOO " a c o 6 "d 70= = Qoo ono f - J o e o 3o-o 6 o o z 6 o . 605 o pr o o 502 z !J 900 z 4 400 :o. X uao a ? o 306 a,O ?o2 o9! U )- rK- r ,vxrn- b-

?o 40 60 I0 loo 120 140 OXYGENTENSION IN WATER FIc. 10. Oxygen uptake (left ordinate, open circles) and coelomic fluid PO, (right ordinate, closed circles) vs. partial pressureof ambient water in the Pacific sea urchin Strongylocentrotus purpuralzs (from Johansen and Vadas 1967),

Slrmgyloccnlrolus purpurofu! o Po2 WATER

a Po coELoMtc FLUID z For personal use only.

z 9 z U Slrongylocanlrolusd.oebachiensis z O I P^v2 WA'TER

o . Po2 COELOMICFLUID

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J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 tz!456 TIME - HOURS Frc. 11. Oxygen tension in water and coelomic fluid to two species of Pacific urchins observed when the urchins were in a closedrespiration chamber (from Johnsenand Vadas 1967). 23t6 J. FISH. RES. BOARD CAN., VOL. 32(IZ),T975

E oo7 50 o.o8 - z = ; U o07 F P o 45? G 0.o6 o IE co 006 F 2 X J S 4Ot F z U 0.o4 U o o U E o.o3 I oo5 3sd U i Y o.o2 Fs L 30s o.ol z z oo4 U / ^\ O U \AI 2345678 zcu DISSOLVEOOXYGEN lN mq,/L oX G o.ll 003 0.r0 L. lrigrnctolo (22- 25 C) 23456 OXYGENCONCENTRATION mllL o.09

Frc. 12. Efiect of water oxygen content on oxygen o.08 L.lignorum(19-2OC) percentage by the gills uptake, and oxygen extracted = o.o7 of a 332-9 European lobster, Homarus vulgaris. U < Solid line depicts oxygen uptake and the dotted line E 0,06 denotes percentageextraction (from Thomas 1954). z o oo5 q U o.o4 PO2 (Johansen and Lenfant 1966). Some tendency U 0.o3 for oxygen-dependent respiration is evident in l the lobster, Homarus vulgaris (Fig. 12) and crab, o o.o2 Cancer productus, especially at high temperatures o.0l when oxygen availability falls (Belman and Chil- o dress 1973). Burrowing activity in wood of three (B) 12345678 marine isopods, Limnoria lignorum, L. quadri- DISSoLVEoOXYGEN lN mglL punctata, and L. tripunctata, (Fig. 13) appears di- Frc. 13. Daily egestion rates of three species of rectly related to available oxygen tension (Ander- Limnoria at different dissolved oxygen concentrations For personal use only. at A) 15 C and B) the temperaturesindicated (from son and Reish 1967). Twenty-eight days MTL's Anderson and Reish 1967). for survival of these three species tested at three temperatures range from 0.6 to 1.18 mg O2lliter. The calcareous tube-building polychaete, Hy- vulgaris shows increased oxygen utilization and droides norvegica, may show reduced larval settle- respiratory dependence at 15 C, in response to ment in low oxygen conditions (Reish 1961) as declining oxygen levels. Atlantic lobster kills are well as in low temperatures. Estuarine shrimps, suspectedto be sometimes related to low dissolved Crangon vulgaris, are asphyxiated below 2O7o air oxygen (Young 1973), although Mcleese (1956) saturation (21 C,23'1, salinity), and are stimulated reported survival of American lobsters for 48 h to swim vertically at dissolved oxygen levels be- in 1.1 mg/liter of oxygen. Crustacea often show tween 22 and 357o of saturation (Huddard and elevated respiratory movements in low oxygen, as Arthur 1971). The authors suggestthat this vertical seen in the stomatopod, Squilla mantis, the prawn, swimming response may allow the shrimps to be Pandalus borealis and the crab Carcinus maenas horizontally displaced by currents and so reach (Johnston1936). areas of improved oxygen conditions where they The respiratory dependence phenomenon, ex- passively sink to the bottom. The anemonae hibited by many invertebrates, can be demon- Actinia moves to the surface when 02 falls below strated for benthic communities. The log of sedi- 2 ml O2/liter (2.8 mg O2/liter), but if this movement oxygen uptake from a variety of benthic ment is prevented it closes up and "enters a latent communities appears correlated significantly with period of life," (Nicol 1967). temperature (Fig. 14A). Thus, in terms of their oxygen requirements, benthic communities of di- J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 Ventilatory activity is often affected by Oz level. Arenicola and Nereis diversicolor reduce verse geographical location appear similar. When their rate of water pumping in burrows, while oxygen levels fall below 6.0 mg O2/litet, the rate another polychaete, Choetopterus variopedatus, of sedinrent-community 02 uptake may decline increases its pumping rate. The lobster Homarus (Fig. laB). The sediment community appears to- DAVIS: REVIEW OF OXYGEN REQUIREMENTS OF AQUATIC LIFE 21t7

A comprehensive documentation of the effect 2OO of periodic anaerobic conditions on benthic com- .- munity structure was made by Hoos (1973)' Her E N with Inlet, Nova Scotia, o too study dealt Petpeswick becomes anoxic in late Eeo where the deeper water '60 fall. Hoos found that species diver- z summer and 940 sity of benthos decreased with depth, and varied F seasonally according to the available dissolved oxygen level. Below 15 m, Nephtys incisa, Mytilus a?o 2 edulis, Mya arenaria, Capitella capitata, and co- o'^ pepods were the dominant organisms when suffi- z8 cient oxygen was present to support life. In the U6 I' deep basin, species diversity declined to zero in September-November, 1971. When basin turnover o4 : LOG"y 1.74LOO"(x)-l.30 adult F occurred, the major recolonizers included z u2 r O.85 Yoldia limatuloides, Nephtys incisa, Polydora t- phyllodocid poly- o quadrilobata, Corophium sp., U ol chaetes, and nematode worms. Hoos reports that ? 4 6 810 20 30 her findings are similar to those of several authors, TEMPERATURE- C working elsewhere, who listed organisms best able to survive periods of deoxygenation that included Nephys sp., Nereis sp., Scoloplos sp., Capitella ru' zo capitata, Mytilus edulis, Mya arenaria, Corophium OJ and nematodes. o volutator, harpacticoid copepods, = Similar studies and reports of sensitivity of benthos to low oxygen in other parts of the world 3a were made by Emery and Hulsemann (1962), ao (1944), Morse (1971), E Heegaard Rhoads and c" and Tulkki (1965\. U Substantial benthic communities often exist E LOG y = 0.66 LOG (x) + F under low oxygen conditions. For example, C. D- z U^ r : 0.79 Levings (unpublished data) examined the oxygen >1 6 content and community structure below 150 m For personal use only. 6 depth in two areas in the north end of Howe Sound near Vancouver, B.C. Seasonal oxygen IR\ 4 6 8lO levels at these two sample areas taken 5 m above nl 02/L the bottom were: variety of benthic FIc. 14. A, Oxygen uptake by a Basin station Woodfibre station communities, both marine and fresh water, in rela- given tion to temperature. Values are as individual (x, range,n) (x, range,n) permit, point or points or as ranges if the data each Date ml Ozlliter ml Ozlliter B, Relationship range signifying a different study; June1972 2.24,2.10-2.57,4 2.25,1.87-2'63,2 rate and the between the sediment oxygen uptake $ept.1.972 5.65,4.08-7.16,3 5.86,(identical), 2 oxygen content of overlying water at 15 C in Marion 2.79,2.32-3.11,42.54,2.22-2.86,2 in the Nov.1973 Lake, B.C. Open circles are not included 3.03,2.30-3.32,7 2.42,2.41'-2'43,2 (from Jan.1973 regression calculation Hargrave 1969). Feb.1973 2.84,2.71-2.93,42.71,2.57-2.86,2

exhibit the respiratory dependence phenomenon, likely because of the response of the individuals Summaries of the polychaete worm species composing the community. It follows that the retained on a 0.5-mm sieve at each station are degree of hypoxia tolerated by a community will presentedin Table 6. It can be seenthat a variety depend on the ability of individuals within the of taxa exist in deep water where only 2-3 ml community to withstand low oxygen. Thus, if a O"/liter (2.9-4.3 mglliter) is commonly found. prolonged low oxygen regime is imposed on a The large differencesin number of taxa between J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 community, the tolerant members will survive the two communitiesmay be related to the pres- while the less resistant will die off and may be ence of wood waste and/ or chemical contamina- replaced by more tolerant forms from within or tion at Woodfibre station,or other factors, as yet outside the community. unknown. 2318 J. F]SH. RES. BOARD CAN., VOL. 32(12).1975

A thriving mixed invertebrate community was (Prosserand Brown 1962), and observationsof described by Levings and McDaniel (1974) who other planktonicspecies' availability in low oxygen examined benthos attached to an undersea cable conditions are recorded. For example, Hoos spanning the Strait of Georgia, B.C. The cable (1970) observeda variety of speciesinhabiting was retrieved from deep water where the oxygen an oxygen-minimum deep layer (approximately levels are between 2 and 4 mI O2/liter (2.9 and 0.4 ml O2/liter = .57 mg/liter) in a B.C. inlet 5.7 mg/liter). Levings and McDaniel observed (Table 7). Hoos found that some vertically mi- "a wide variety of epifaunal invertebrates includ- grating speciessuch as Euphasia pacifica did not rng sponges, anemones, gorgonians, polychaetes, enter the oxygen-minimum layer, while others and starfish attached to the cable retrieved frorn such as Calanus plumchrus tended to remain water 300-350 m deep." there. In contrast, Marshall et al. (1935) concluded: OxvcnN Tor-nReNcns AND REeuTREMENTS oF "Calanus are unaffectedby an increasein the Menrur PLaNxroNrc aNo Ppt.tcrc OnceNtsvs oxygen content of the water, but are sensitive to low oxygen tensions.Below a concentrationof Organisms that swim freely in the sea, float, or about 3 m|ll the respiration decreases.At con- are passively transported in some way, could en- centrationsbetween 1 & 2 ml/l they are killed. counter a variety of oxygen conditions. Generally, They are more resistant at 5oC than 15o and surface waters are well oxygenated while deeper stage V are more resistant than adults at both layers tend to be lower in oxygen content, al- thesetemperatures." (Fig. 15) though there are numerous exceptions due to upwelling, river outflows, decomposition, respiration, Summary of Oxygen Requirements of Aquatic photosynthesis, and pollution influences. fnvertebrates The oxygen requirements, oxygen-related behavior and physiology of pelagic flsh have been From the foregoingdiscussion it is obviousthat reviewed previously. Pelagic invertebrates in many a greatrange of tolerances,responses, and require- instances show some similar responses.The squid ments for oxygen exist amongst aquatic inverte- Loligo is reported to avoid oxygen-deficient water brates. Separate aquatic communities are also likely to differ in sensitivity to oxygen, and a range of susceptibility to low O, is often found amongstthe individualsof a community. Oxygen tolerancetends to be correlatedwith habitat, so Tesrr 6. Polychaete taxa retained on a 0.5-mm seive that individualsnormally living in well-oxygenated from benthic samplestaken at two Howe Sound, B.C. For personal use only. stations in 1972by C. D. Levings (unpublished data). water are less tolerant of low dissolvedoxygen than those encounteringit periodically. Further- more, there is some evidence that oxygen-depen- Taxa at basin stations Taxa at woodfi ber stations dent respiration may apply to oxygen uptake Polychaeta(Families) Polychaeta (Families) relationsof communities,as well as to individuals. Ampharetidae Capitellidae Difficulty is encountered in determining safe Capitellidae Cirratulidae levels of dissolved oxygen for aquatic inverte- Cirratulidae Nereidae bratesbecause of i) the wide range of responses Flabelligeridae Nephytidae reported, ii) the ability of many organisms to Glyceridae Paraonidae inhabit low oxygen regimes and obtain energy Lumbrineridae anaerobically,and iii) by a lack of understanding Maldanidae E 5 taxa of the physiologicaleffects of low 02. Survival in Nephytidae continuous levels of low oxygen depends on Nereidae ability to produce energy Opheliidae continuously anaer- Oweniidae obically, or the capacity to extract oxygen from Paraonidae an environmentlow in oxygen. Also, the ability Pectinariidae of organisms to cope with oscillating oxygen Phyllodocidae levels is very poorly known or understood.Ob- Polynoidae viously, the tolerance of the speciesinvolved and Sabellidae the duration of low oxygencondition are of prime Spoinidae importance to survival. Utilization of anaerobic J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 Syllidae metabolism could satisfy the energy needs of Sternaspidae Terebellidae many aquatic invertebratesfor long periods,par- E 20 Taxa ticularly the smaller, sluggishforms with a typically low oxygendemand. The larger,more active DAVIS:REVIEW OF OXYGENREQUIREMENTS OF AQUATICLIFE 2319

-ltsrn7. Pelagic invertebrate speciesinhabiting an oxygen minimum.layer (approx.0.4 ml-Oz/liter : 0.57mg/liter) in SaanichInlet, B.C. (from Hoos 1970).

Phylum Species Abundance'

Cnidaria Aglantha digitals seasonallyabundant Aequorea aequorea tate Phialidium gregarium common Aegina rosea tate Ctneophora Pleurobrachiia pileus seasonallyabundant Beroe cucumis rare Annelida Tomopteris renata rare Chaetognatha Sagitta elegans rare Mollusca Pteropoda Clione limacina rare Limacina helicina common Arthropoda Copepoda Calanus plumchrus very abundant Calanus cristatus rate Pseudocalanus minutus abundant Eucalanus bungii bungii common Euchaeta japonica abundant Metridia lucens abundant Mysidacea Neomysis rayii rare Amphipoda Parathemisto pacifica abundant Euprimno abyssalis rare Cyphocaris challengeri abundant Orchomenella obtusa abundant Euphausiaceae Euphausia pacifica abundant Thysanoessa longipes common Thysanoessa raschii common Thysanoessa spinifer rare Decapoda Spirontocaris sica rare Munida quadrispina common For personal use only. uTermsdescribed by Fulton (1968).

F EIiIALE ' sraerv O o.7

v.o

f \.)4 o-' o na

c \.)a

o. I J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 024681012t416 OXYGENCONTENT_ MIlL Frc. 15. Eftect of oxygen content on the oxygen consumption of female and stage Y Calanus, at 15 C (from Marshall et al. 1935)' 2320 J. FISH. RES. BOARD CAN., VOL. 32(12),r97s

forms are likely to be more affected by low 02 2. Oxygen response thresholds for marine and thus may be the most sensitive members of fishes, including both anadromous and nonana- the community. Thus, a change from an adequate dromousspecies. All the speciesof salmon (except oxygen regime to one of relative O, scarcity may rainbow trout and steelhead) are included in this result in loss of the more sensitive organisms and section although they spend some portion of their a restructuring of the community. New speoies, life in fresh water. tolerant to low oxygen, could move into the com- 3. Thresholdsof oxygenresponse for salmonid munity; or those already present in the community eggs and lawae at various stagesof deVelopment. could become more numerous to replace the in- These groupings can be further broken down tolerant species. Alternatively, no replacement by including or excludingthe salmonids,to ther€- could take place, leading to a net reduction in by derive criteria for nonsalmonid freshwater or biomass and/ or alteration of species composition marine species. of the community. In conclusion, and on a common-sense basis alone, it seems likely that any depression of natural oxygen conditions can result in a change Sretrstrcar TnnerraeNt oF DATAFoR DEvIATIoN in an aquatic invertebrate community. The severity oF CRITERIA of this change will be related to the species com- The data of Table 4A-D were analyzed by position, the species sensitivity of low oxygen, the averagingthe incipient threshold levels of PO2, degree of oxygen depression, and other factors millili'ters 02 per liter, milligrams O, per liter, acting on the community, such as temperature. and percent saturation for various fish groups Whether a change in an invertebrate community within the tables.The data-groupsanalyzed appear is necessarily bad from an point ecological of in Table 8. For each group, the mean averagein- view may be very difficult to determine. It may cipient threshold oxygen level was calculated and be that a change from one type of community to reported with its standard deviation, standard another may not be necessarily deleterious. On the error, and number of observations.Averaging the other hand, if major food chain constituents drop data in this way assumes that results will be out, the change could be considered deleterious. unaffected by different experimental conditions, Insufficient evidence presently exists to formu- fish tested,and factorssuch as temperature.Varia- late definite dissolved oxygen criteria concerning tions due to differing experimental conditions aquatic invertebrate communities. However, d should be minimized by the large sample size in reasonable will probably basis be assured by fol- most instances. lowing the recommendations for fish populations For personal use only. The effect of temperature on the incipient given here, particularly as many invertebrates are oxygen threshold was examined to test the validity able to temporarily periods withstand of low of the averaging procedure. For the largest body oxygen. It must be remembered, however, that of data (Table 4A), all results showing the in- any change in dissolved oxygen will likely affect cipient oxygen level in milligrams 02 per liter invertebrate communities in some way. Ideally, (Fig. 16) and percent saturation (Fig. 17) were we need a good knowledge of community struc- plotted in relation to temperature. From these ture in areas threatened by pollution so that im- figures it can be seen that the oxygen content portant sensitive species are pro- identified and threshold,in milligrams 02 per liter, is relatively tected. In addition, knowledge of the seasonal unaffected by temperature; although, higher per- oxygen minima for specific areas is required to centage saturation levels are required at higher identify periods when further oxygen depression temperatures. This is logical since the oxygen poses a hazard to aquatic life. content drops as temperature increases. Thus, progressivelyhigher percentagesaturation is required at high temperatures to fulfil the oxygen requirementsof fish. For the analysisthen, oxygen Developrnent of Oxygen for Criteria Fish content data (milligrams per liter) rather than Populations percentagesaturation data were used in the deri- The incipient oxygen response levels for flsh vation of criteria. populations \Merepresented in Tables 4A-D. These From the data in Table 8, major fish groups tablesyield: (only thosewith a large number of observations) J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 1 Oxygen response thresholds for freshwater were selected (Table 9) for criteria purposes. flshes including nonanadromous salmonids (as These groups encompassboth salmonid and non- the steelheadis a variant of the rainbow trout, it salmonid speciesin fresh and salt water, as well was considered a nonanadromous sDeciesfor the as larvae and mature eggs of salmon. Owing to purpose of this paper) the fact that oxygen levels often fluctuate in DAVIS:REVIEW OF OXYGENREQUIREMENTS OF AQUATICLIFE 2321

Tesrn 8. Mean thresholds of incipient oxygen responsethresholds listed in Table 4A-D. Values are means (x) shown with + I standard deviation (so), * standard error (sE),and the number of observations(r).

Averaged Group PO2-mmHg Mg Oz/liter %,Satn.

Freshwater species x 85.56 5.26 s4.62 including salmonids SD 27.37 2.0r 17.53 SE 5.37 0.37 3.44 n 26 30 26 Freshwater species x 72.56 3.98 46.53 excluding salmonids SD 18.83 l.6s 12.34 SE 7.12 0.50 4.66 1 1t a Freshwatersalmonids 7 90.35 6.00 57.60 SD 28.84 1.84 18.47 SE 6.62 0.42 4.24 n t9 19 19 Marine, nonanadromous x 1r1.03 6.72 73.25 SD 31.54 2.12 19.72 SE 11.15 0.80 7.45 n 8 Marine anadromous x t22.86 6.43 78.49 species,including SD 35.86 2.57 23.03 salmonids SE ll.95 0.69 7.68 9 l4 9 Marine anadromous x 3.38 species,excluding SD salmonids SE n L Marine anadromous x 122.86 6.94 n.qg salmonids SD 35.86 2.39 23.03 SE 11.95 0.69 7.67 n 9 t2 9 For personal use only. Early eggs,freshwater X 15.24 1.14 9.65 salmonids SD 6.40 0.47 4.06 SE 3.69 0.27 2.34 n J J Mature eggs, x 76.47 5.93 48.40 prehatching salmonids SD 1,9.00 1.01 12.15 SE 10.97 0.58 7.O1 J 3 3 Hatching eggsand x I 19.88 8.09 76.26 larval salmonids SD 35.45 l.6s 22.88 SE 20.46 0.95 13.21 fa J 3 3 Eggs, fertilization x 'ltt 3.86 orjt to hatching, non- SD salmonids SE ; n 2 ; z

natural waters, the levels of protection selected average incipient oxygen response level for the were defined as MINIMUM oxygen levels in a group. The rationale is that few members of a J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 body of water SEASONALLY (fall, winter, fish population, or fish community, will likely spring, and summer). Three levels of protection exhibit effests of low oxygen at or above this were devised to provide flexibility in interpreta- level. Level A representsmore or less ideal con- tion: ditions and permits little depression of oxygen Level A - This level is I so above the mean from full saturation. It represents a level that 2322 J. FISH. RES. BOARD CAN.. VOL. 32(12).1975

OXYGENCONTENT RESPOilSE IHRESHOLDS Iil RELATIONTO TEMPERATUREFOR MESHWATERFISH

| 5377| O|SX

4 I 16 20 24 28 rrmpel2mune- c

Ftc. 16. Incipient sublethal oxygen response thresholds vs. temperature for all the freshwater fish data in Table 4, plotted in terms of oxygen content. The plot is similar to Fig. 77 and shows that the relationship between response threshold is not as clearly related to temperature as when plotted in terms of percentagesaturation.

OXYGEN O/o SATURATIoN THREsrus II RELATIoN To TEMPSATURE FoR A MIXEO GROUP OF FRESHWATER FISH For personal use only.

s I

at2162024A TEMPERATURE_ C Frc. 17. Incipient sublethal response thresholds vs. temperature for all the freshwater fish data from Table 4, plotted as percentage oxygen saturation. The linear regressionline and equation are given. This graph illus-

J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 trates the effect of temperature on the response threshold expressed in percentagesaturation O:. (Note - {s lsglg5sion of percentile data is a questionable statistical procedure, the regression analysis was repeated following arcsine transformation according to Snedecor (1965). This analysis reduced the slope of the regression line somewhat; however, more slopewas presentthan for the data of Fig. 16.) DAVIS:REVIEW OF OXYGENREQUIREMENTS OF AQUATICLIFE zil)

Tanle 9. Incipient dissolvedoxygen response thresholds selected from Table 8 for derivation of oxygen criteria. These selectionswere made to give a good representationof fish groups in both fresh and salt water for criteria purposes. Levels of protection A, B, or C (seetext) are given. The ayeragetemperature, extracted from Tables 4A-D, which corresponds with the average incipient oxygen threshold (in mm Hg POz) is indicated in parentheses.

Protection Group Ievel PO, mg O2lliter

Mixed freshwaterfish A 113 7.27 population including B 86(15 C) 5.26 salmonids C 58 3.25 Mixed freshwaterfish A 92 5.63 population with no B 73(18 C) 3.98 salmonids C 54 Freshwater salmonids A 119 7.84 (including steelhead) B e0 (15c) 6.00 c 6l 4.16 Salmonid larvae and A 155 9.74 mature eggs B 120(9 C) 8.09 C 85 6.44 Marine, nonanadromous A 143 8.84 species B 1r1(r1 C) 6.72 C 80 4.60 Marine, anadromous A 159 9.00 species,including B 123(17 C) 6.43 salmonids c 87 3.86 Anadromous salmonids A 159 9.33 in sea water B 1,23(r7 C) 6.94 c 87 A << For personal use only. assures a high degree of safety for very important the mean. Thus, the recommended levels span fish stocks in prime areas. the range of responses that include both sensitive Level B - This level represents the oxygen and insensitive animals, both within and between value where the average member of a species in species.l Analysis of the data for the freshwater a fish community starts to exhibit symptoms of fish group, including salmonids, indicates ,that oxygen distress. These values are der,ved from these data are normally distributed about the the class mean averages from Table 8. Some mean and yields a typical cumulative frequency degree of risk to a portion of fish populations curve about the mean (Fig. 18). exists at this level if the oxygen minimum period The criteria values of Table 9 based on oxygen is prolonged beyond a few hours. content in milligrams 02 per liter and PO2 were Level C - At this level a large portion of a rounded ofl and entered in Table 10. This table given fish population or fish community may be constitutes the final derivation of the recom- affected by low oxygen. This deleterious effect mended criteria. Oxygen content values in milli- may be severe, especially if the oxygen minimum li'ters 02 per liter were calculated from the values is prolonged beyond a very few hours. The values for milligrams Oz per liter in Table 10, and per- are 1 so below the B level, or class average, for 'A the group. This level should be applied only if weaker form of these criteria could be adopted fish populations in an area are judged hardy or of by setting the value of A or B level as the average marginal significance, or of marginal economic 24-h O, value and the minimum O, concentration 24 the next criteria level. importance and, as such, are dispensible (i.e. in over any h eqral to lower

J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 For example, the value of A would represent the the socioeconomic sense). average 24-h O, level and at no time should it be The use of standard deviations to recommend allowed to fall below the value of B. Adoption of levels of protection is based on the statistical this scheme could risk serious damage to fish popula- concept that, in normally distributed data, ap- tions at level B. Objections to the use of average proximately 68% of the values lie with + I sD of values are discussedin Warren et al. (1973\. L' L+ J. FISH. RES. BOARD CAN., VOL. 32(12),1975

ne Oz/ L

Frc. 18. Frequency distribution of oxygen response thresholds for the largest data group - that for the freshwater fish in Table 4, illustrating that the thresholds follow a more-or-less normal distribution.

cent saturation was calculated for a range of that they are heavily biased towards the oxygen 0-25 C from the desirable PO2 and content data. requirements of salmonids, which tend to be

For personal use only. Calculations of percent saturation in sea water higher than some other species.This results from were based on a salinity of 28%" (this detailed much key work beingconfined to salmonids.With account of procedures used to derive criteria is this possiblecriticism in mind, the criteria recom- given so that others may use the same data to mended in Table 10 for nonsalmonid speciesin derive their own criteria in another way, if so fresh and salt water are lower than for salrnonids; desired). however, they are based on fewer data. It must It must be emphasized that, as pointed out be stressedtherefore, that although these criteria earlier in this report, fish require both the correct are based on best-availableknowledge to date, oxygen tension gradient to move 02 into the they are tentative and should be subject to re- blood and sufncient oxygen (per unit volume of vision when new information arises. water breathed) to fulfill the requirements of A key point in application of the criteria pre- metabolism. Therefore, the criteria have been sented above is that daily, seasonal,or periodic derived to provide both these essential require- low oxygen levels may occur naturally in many ments of flsh. They are expressed as percentage water bodies. These natural levels may be near saturation values over a range of temperatures. At or below recommendedcriteria levelsA, B, or C. the lower temperatures where water solubility of In such cases, judgernent and caution must be oxygen is high, the criteria were set using the exercised in applying criteria to these naturally PO2 values in Table 10 to ensure 'that a percent- oxygen-deficientwaters. A standardcould be im- age saturation value consistent with the required posedwhich would be impossibleto meet owing PO, gradient was present. At the higher tempera- to natural fluctuationsin dissolvedoxygen. Also, tures, higher percentage saturation values were if natural depressionof oxygen occurs in waters J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 necessary to provide the oxygen content require- that are to receive wastes with a significant ments dictated by the milligrams O, per liter oxygen demand, even a relatively small discharge values in Table 10. could reduce oxygen below critical levels. One A major criticism of these criteria might be method of assessingthe severityof hazard would DAVIS: REVIEW OF OXYGEN REQUIREMENTS OF AQUATIC LIFE 2325

TacrB 10' Oxygen criteria based on percentagesaturation values derived with three levels of protection as outlined in the text. PO2's and values of mg O2/liter were extracted from Table 9 and rounded otr foi use here. The values shown for milliliters Otlliter were calculatedfrom the values of milligrams Ozlliter in this table. The criteria essentialfor protection of aquatic fish populations are expressedas percentagesaturation values at various temperatures.They were derived from both PO, and mg O2/liter values, as both oxygen tension and oxygen content are critical factors. At the lower temperatures,the percentagesaturation value was determined using the PO, values essentialfor maintaining the necessaryoxygen tension gradient betweenwater and blood for proper gas exchange.Higher percentagesaturation values are necessaryat the higher temperaturesto provide sufficient oxygen content to meet the requirementsof respiration as defined by the mg O2/liter values. -Percentagesaturation values are defined as "oxygen minima" at each level of protection. Graphical presentation of the results is found in Fig. 19. The temperaturescorresponding to the perceniagesaturation iriterii are defined as "seasonaltemperature maxima."

fSatn. at C for criteria Protection Group level PO, ml O:/liter mg Ozlliter 0 l0 15 20 25 Freshwater mixed A 110 5.08 7.25 69 70 70 7t 79 87 fish population 885 3.68 5.25 s4 54 54 s7 54 63 including salmonids c60 2.28 3.25 38 38 38 38 39 39 Freshwater mixed fish A95 3.85 5.50 60 60 60 60 60 66 population with B75 2.80 4.00 47 47 47 47 47 48 no salmonids c55 1.75 2.50 35 35 35 35 35 36 Freshwater salmonid A 120 5.43 7.75 76 76 76 76 85 93 population (including 890 4.20 6.00 57 57 57 59 65 72 steelhead) c60 2.98 4.25 38 38 38 42 46 51 Salmonid larvae and A 155 6.83 9.75 98 98 98 98 100 100 mature eggsof B 120 5.60 8.00 76 76 76 79 87 95 salmonids c85 4.55 6.50 s4 54 57 64 71 78 Marine, nonanadromous A 140 6.13 8.75 88 88 9s 100 100 100 speciesu B 110 4.73 6.75 69 69 74 82 90 98 c80 3.15 4.50 50 51 51 55 60 65 Anadromous marine A 160 6.30 9.00 100 100 100 100 100 100 species,including B 125 4.55 6.50 79 79 79 79 87 94

For personal use only. salmonidsu c90 2.80 4.00 57 57 57 57 57 58 uPercentage saturation calculations based on salinity of 28%o.

be to calculate the expected oxygen depression Regarding aquatic invertebrates and aquatic eco- for the receiving water and then subtract this systemsgenerally, the following recommendations depressionfrom the naturally occurring 02 mini- are proposed: mum value(s). The severityof hazard could then 1. Any change in the dissolved oxygen regime be estimated by reference to Table 10, after con- will likely have some effect on the ecosystemand version of the data to percentagesaturation (see the magnitude of that effect will depend on the alsoFig. 19). severity and duration of the change. 2. A guide to sensitivity of the system could be basedon knowledgeand study of the area in Guidelines for Low Oxygen Tolerance of question. Open ocean coasts, swift-flowing fresh- Aquatic fnvertebrates water streams, or other well-aerated bodies of water are likely to contain more low oxygen- Owing to considerable lack of knowledge of intolerant species than poorly aerated water effectsof low oxygenon the physiologyof niarine bodies. Thus the habitat and its physical features invertebrates,oxygen criteria cannot be proposed would serve as an index of the degreeof sensi for these organismsat this time. It is reasonable tivity of the system. to assume, however, that the levels proposed in 3. Wherever possible,knowledge of the natural

J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 Table 10 for fish would provide good protection seasonal oxygen minima conditions should be for most aquatic invertebrates. Indeed. manv in- available as a guide to implementing criteria. ventebratescan withstand a much -or" ,"u"r" 4. Where seasonaloxygen minima are identi- oxygen lack for a longer period than can fish. fied, it is suggestedthat the potential depression 2326 J. FISH. RES. BOARD CAN., VOL. 32(12),1975

of water oxygen caused by a discharge be calculated. In this way, further reduction in oxygen level, imposed on the natural condition, could be predicted.

Relationshipof ProposedCriteria to Other Documents

Davis (1975) summarized the findings of other J oxygen criteria documents. The reader should E,- consult that reference for a detailed comparison of various points of view. A number of the other documents are based on the comprehensive review of Doudoroff and Shumway (1970). s This report was written entirely without con- sulting other criteria documents prior to deriva- 2 tion of the criteria, hopefully, to avoid bias. I 3o was generally aware, however, of the flndings of t5 20 25 50152023 -' - other reviewers and it was partly for this reason o .B t/'/t that the foregoing statistical methods were used t"-' -t "/ 8o to derive cause/effect criteria for the present re- -.-'/' port. I was also aware that Doudoroff and Shum- . -'/t " ." way (1970) had recommended various "levels of *.-'/ 40 protection" in compiling oxygen criteria and that

full acknowledgement must be given to their 20 sensible concepts.

In general, the 02 criteria formulated in this 20 25 5r0152025 report, and derived specifically for Canadian aquatic life, incorporate a number of considerations identifled as critical in o her oxygen criteria documents. The herein-presented criteria include the concept of seasonal oxygen minima, allow consideration of temperature, and contain three For personal use only. ::I::: levels for assessment of potential risk: Level A .-. provides a high safeguard for very important . c aquatic populations; with Level B, there is some 0 possibility of moderate risk to aquatic organisms, 3 because it allows some degree of oxygen depres- 2 6 possible large sion; with Level C, it is that a 5 o portion of a given fish population or fish com- \-\.-. munity may be severely affected by low oxygen, '--.-.-.-. especially on a "chronic exposure" basis. These criteria, unlike most others, present " oxygen levels as percentage saturation. This was

FIc. 19. A, Oxygen criteria, expressedas seasonatr flrz minima in percent saturation, at various seasonal temperature maxima. Three levels of protection, A, lo B, and C, are given as defined in the text. Values . \.__. used in derivation of the criteria are summarized in \\. Table 10; B, Oxygen criteria, expressed as oxygen ._._._..'...-: i minima in mg O,/liter (ppm), at various seasonal 6 temperature maxima. Three levels of protection, A, B, and C, are given as defined in the text. These J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 values were calculated from the percentage saturation values illustrated in (A) and summarized in Table 10. DAVIS: REVIEW OF OXYGEN REQUIREMENTS oF AQUATIC LIFE 2327

done partly because the concept is easily under- tic waste discharge, respiration, upwelling of deep stood and can be assessedconvenientlv. In addi- O2-deficient water, decomposition, etc. tion, the criteria, expressed as percentage satura- 5) Occurrence of toxicants in the water mass tion, incorporate both the necessary oxygen which, in combination with low oxygen, may content and partial pressure essential for fish lead to a potentiation stress responses on the part respiration over a range of temperatures. The of aquatic organisms. values can be easily converted to other units such If such a panel implements oxygen criteria in as milligrams O, per liter. keeping with the above considerations, there is Unlike other criteria, the present oxygen criteria considerable assurance that the criteria will be include consideration of marine fish, based on realistically applied to the area in question accord- actual data. These data are admittedly somewhat ing to the best current available knowledge. The scanty; thus, there is a need for more extensive proposed criteria should be considered subject to data on all aspects of pollution research with revision as new knowledge comes available. marine fish. Lacking current knowledge of oxygen require- Acknowledgments ments for aquatic invertebrates, oxygen requirements for assessmentof harm to these organisms I would like to thank Mr J. Marier and members of the N.R.C. Environmental Secretariat for have not been specifically proposed. For-protec- en- couragement to prepare much of this report. Those tion of aquatic invertebrates, adoption of ttre persons,as well as Drs I. B. Sprague,M. Waldichuk, criteria relating to fish populations is recom- C. Levings, G. Greer, D. Alderdice, J. R. Brett, and mended, for reasons given in this report. Much R. L. Saunders, provided useful advice, criticism, more work is needed in this particular area, to and information. The assistanceof Ms B. Mason and elucidate the effects of low oxygen on invertebrate Mr I. Shand in preparing the report is greatly appre- communities and ecosystems, especially those in ciated as is the untiring effort of Mrs D. Price. the sea. Glossaryof Terms - Suggestions Acclimation compensatory change or adjustment for fmplementationof Criteria of a bodily function (e.g. metabolism) in response to a single environmental factor, such as tempera- Criteriashoutd only be implementedin keeping ture, in the laboratory (Prosser and Brown 1962). with a thorough knowledge of the speciflc area in Aerobic - process that proceeds in the presence of question and the aquatic life inhabiting it. In my oxygen such as aerobic respiration (respiration opinion, use of a single oxygen level, group requiring and utilizing oxygen). For personal use only. or of oxygen levels, applied to all waters on a national Anaerobic - process that proceeds in the absence of basis is an unrealistic and potentially questionable oxygen, such as anaerobic respiration (energy production from metabolites without oxygen utiliza- practice. A sensible approach would be to form tion). regional panels, whose members have expertise Anadromous - term applied to an animal, usually a in diverse fields such as fisheries biology, ecblogy, fish, that spends part of its life in fresh water and oceanography, limnology, and industrial pollution. part in salt water, necessitating some movement The duty of the panels would be to review exist- (migration) from one media to the other. ing information, initiate studies to seek new Blood oxygen dissociation curye - experimentally knowledge and implement criteria (such as those derived curve describing the saturation kinetics of suggested here) once sufficient knowledge on the blood in relation to available oxygen tension. The curve indicates percentage saturation relevant area was amassed. The panel should trv of the blood at different and establish: oxygen tensions, illustrating the oxygen level required to saturate the blood and how the 1) What fish and invertebrates species reside blood carries oxygen and delivers it to the tissues. in or move through the area, their relative O, Criteria - set of rules or guidelines based strictly sensitivity, and what their economic, recreational, upon a scientific assessmentof environmental harm. or biological importance is. Oxygen criteria are derived from a study of cause 2)The seasonal natural oxygen regime for the and effect interrelations involving the responses of area. organisms to reduced oxygen. Food conversion efficiency - efficiency with 3) Physical factors that affect dissolved oxygen which a given quantity of food consumed levels such as emperature is converted to regimes, water circula- body mass. J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 tion patterns, and "turnover" of water masses. Hypoxia - a condition when oxygen availability is 4) Existing oxygen-depleting factors, either low. A fish reacting to low oxygen can be said to natural or man-made such as industrial or domes- be hypoxic. 2328 J. FrSH. RES. BOARD CAN., VOL. 32(12),1975

Incipient - just beginning. The incipient oxygen drawn from a paxent population - i.e. a measure response threshold can be defined as the oxygen of the reliability of the mean average. level where some organism just starts to respond Ventilation 12fs - breathing rate of an organism in some way to reduced oxygen availability. denoting the number of ventilatory movements per Metabolism - chemical process involving enzyme unit time. reactions in the body whereby energy is made available for bodily work. Metabolic reactions may be both oxidative and nonoxidative in nature. List of SYmbols Metabolic rate - rate at which metabolism proceeds, usually expressed as oxygen consumption rate, D.O. - abbreviation for dissolved oxygen level' caloric heat produced or rate of CO, liberation. In H,O vap. press. - water Yapor pressure' in milli- many instances, fish and aquatic invertebrate meta- meters Hg. bolic rate is measured in terms of oxygen uptake mg O"/liter - concentration of oxygen in milligrams rate. per liter of water (1 mg O,/liter = 1 ppm). Oxygen concentration (content) - the concentration, -f O,/lit". - concentration of oxygen in milliliters measured in terms of milligrams Oz present in a per liter of water (0.7 ml Oz/litet : 1.0 mg Ozl given body of water, usually I liter, at a specified liter = 1 ppm). temperature, pressure, and salinity. The amount of n - the number of individual data used in a compu- oxygen present per unit water breathed by an tation aquatic animal governs, in part, the oxygen avail- PCO, - partial pressure of carbon dioxide in milli- ability to the organism. metersHg. Oxygen partial pressure (PO) -oxygen tension mea- PO, - partial pressure of oxygen in millimeters Hg. sured in millimeters Hg, in a solution. Oxygen ppm - abbreviation for parts per million concentra- diffuses down a concentration gradient across the tion term. respiratory surface. The magnitude of the gradient so - standard deviation (statistical terminology). is conveniently determined by measuring oxygen sp - standard error of the mean (statistical termi- partial pressure on either side of the exchange sur- nology). face and considering solubility coefficients of MTL - median tolerance limit in terms of dosage oxygen in water and blood. or concentration of a substance that is lethal to Phototaxis - directed behavioral response of an half of the organisms in a bioassay test over a organism to light. Phototaxis may be positive specifiedtest time - usuallY 96 h. (directed towards) or negative (directed away) to %o- parts per thousand (used for expressing salinity the light stimulus. of water). Respiration - process of gaseous exchange across the respiratory surface via diffusion. Often respira- Ar-osnoIce.D. F.. eNo J. R. Bnsrr. 1957.Some effects of tion rate (gas exchange rate) is confused with kraft mill effluenton young Pacificsalmon. J. Fish. ventilation rate (rate of breathing movements). Res.Board Can. 14:783-795. For personal use only. Respiratory dependence - condition exhibited by Ar-opnprce,D. F. , nNo C, R. Fonnesrnn.1971. Effects of many animals where, under certain conditions of salinity,temperature, and dissolvedoxygen on early oxygen availability, respiration rate (and thus development of the Pacific cod (Gadus macro' aerobic metabolic rate) show a direct correspon- cephalus).J. Fish. Res.Board Can. 28: 883-902. dence to the available oxygen level. Animals whose Ar-onnorcE,D. F., W. P. Wrcrr,rr, aNo J. R. Bnprr. oxygen uptake rate increasesas oxygen availability 1958.Some effects oftemporary exposure to low dis- increasesare thus termed conformers. solvedoxygen levels on Pacificsalmon eggs. J. Fish. Respiratory independence - many animals maintain Res.Board Can. 15:229-249. their oxygen uptake rate independent of available ANoEnsoN,J. W., ,c.NoD. J. Relsn. 1967.The effectsof oxygen over a wide range of environmental oxygen varieddissolved oxygen concentrations and tempera- concentrations. These animals are said to exhibit ture on the wood-boringisopod gents Limnoria. Mat. respiratory independence and may, in some in- Biol. l: 56-59. stances,regulate their oxygen uptake rate. In most BEAMISH,F. W. H. 1964.Respiration of fisheswith special cases, however, when available oxygen declines to emphasison standardoxygen consumption. Can. J. a certain critical level, oxygen uptake rate declines Zool.42'.355-366. dramatically, indicating the presence of a limiting BELMAN,B. W., eNo J. J. CHtr-onrss.1973. Oxygen con- situation. Animals that maintain their metabolic sumptionof the larvaeof the lobsterPanulirusinter- rate independent of available oxygen are termed ruptus (Randall) and the crab Cancer productus regulators. (Randall).Comp. B iochem.Physiol. 44: 821 -828. Salinity - total salt content of water expressed in Benc, K. 1952.On the oxygenconsumption of Ancylidae parts per thousand (%,). (Gastropoda)from an ecologicalpoint of view. Hy- Standard deviation - statistical term that measures drobiologica4: 225-267. the spread, or deviation, of individual measure- voN BneNo.T., H. D. BlenNsrEIN,eNo B. MsnlveN. J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 ments from the center (usually the mean average) 1950.Studies on the anaerobicmetabolism and the of normally distributed data. aerobic carbohydrate consumption of some fresh Standard enlor - statistical term describing the watersnails. Biol. Bull. 98:266-276. standard deviation of sample means for samples Bnnrr, J. R. 1962.Some considerationsin the study of DAVIS: REVIEW OF OXYGEN REQUIREMENTS OF AQUATIC LIFE 2329

resplratorymetabolism in fish,particularly salmon. J. EMsny, K. O., lNo J. Hur-sprraNN. 1962.The relatron- Fish.Res. Board Can. t9: 1025-1038. shipsof sediments,life and water in a marinebasin. 1964.The respiratorymetabolism and swimming Deep-SeaRes. 8: 165-180. performanceofyoung sockeyesalmon. J. Fish. Res. Flrnnmocr, R. W. 1966.The Encyclopediaof Oceanog- BoardCan. 2l: 1183-1226. raphy. Reinhold PublishingCo., New York, N.Y. 1970.Fish - the energycost of living,p.3j-52. 1021p. In W. J. McNeil [ed.] Marine aquaculture.Oregon Fox, H. M., C. A. WrNonrrr-o,AND B. G. SrulroNos. StateUniv. Press,Corvallis, Oreg. 1937.The oxygenconsumption ofephemerid nymphs Carr.tenoN,J. N. 1970.The influenceof environmental from flowing and from still waters in relationto the variables on the hematology of pinfish (Lagodon concentrationof oxygenin the water.J. Exp. Biol. 14: rhomboides) and striped rnullet (Mugil cephalus). 210-218. Comp.Brochem. Physiol. 32: 17 5-192. Fnv, F. 8. J. 1957.The aquaticrespiration of fish,p. 1-63. 1971.Oxygen dissociation characteristics of the In M. E. Brown [ed.] The Physiologyoffishes.Vol. l blood of rainbow trout, Salmo gairdneri. Comp. AcademicPress Inc., New York, N.Y. Biochem.Physiol. 38: 699-704. f970.Effect ofenvironmentalfactors, p. l-98. In CnrrreNorN, M. E. Jn. 1973.Effects of handling on W. S. Hoar and D. J. Randall[ed.] Fish physiology. oxygenrequirements of AmericanShad (Alosa sapi- Vol. VI. AcademicPress Inc., New York, N.Y. dissima).J. Fish.Res. Board Can. 30: 105-110. FUI-roN, J. 1968. A laboratory manual for the iden- Core, A. E. 1926.Physiological studies on fresh water tification of British Columbia marine zooplankton. clams.Carbon dioxide production in low oxygenten- Fish.Res. Board Can. Tech. Rep.55: 141 p. sions.J. Exp. Zool. 45:349-359. G,tunrr, J. C. 1971.The responsesof the marine am- Coor, R. H., aNo C. M. Boyo. 1965.The avoidanceby phipods Corphiunt arenarium and C. Volutator to Gammarus oceanicus Segerstrale (Amphiopoda: gradientsand to choicesof differentoxygen concen- Crusfagsn)sf anoxicregions. Can. J. Zool. 43 971- trationsJ. Exp. Biol. 54:275-290. 97s. GevrsoN, A. L. H., aNo K. G. RosenrsoN.1955. The Cosre, H. H. 1967.Responses of Gammaruspulex (L)to solubility of oxygenin pure water and sea-water.J. modifiedenvironment. III. Reactionsto low oxygen Appl.Chem. 5: 502p. tensions.Crustaceana l3: 175-189. GeNNrNc,B., aNo F. Wurpr. 1966.A chamberfor offer- DeuLrunc, M. L., D. L. Snuvwev, eNo p. Douoonor.r.. ing alternativeconditions to smallmotile aquaticani- 1968.Influence of dissolvedoxygen and carbondrox- mals.Ophelia 3: 151-160. ide on swimmingperformance of largemouthbass and Genrv, W. F. 1967.Gas exchange,cardiac output and cohosalmon. J. Fish.Res. Board Can. 25:49-70. blood pressure in free swimming carp (Cyprinus Davrs, G. E., J. Fosun, C. E. WannEN,AND p. carpio). Ph.D. Disserlation.Univ. New York, Buf- Douoonorr'. 1963.The influenceofoxygen concen- falo,N.Y. 123p, tratlon on the swimming performanceof juvenile GnnHeu, J. M. 1949.Some effectsof temperatureand Pacificsalmon at varioustemDeratures. Trans. Am. oxygenpressure on the metabolismand activity ofthe Fish.Soc.92: ttl-t24. speckledtrott, Salvelinusfontinalis. Can.J. Res.27: For personal use only. Davts, J. C. 1973.Sublethal effects of bleachedkraft 270-288. pulpmill effluent on respiration and circulation rn Gnr'cc,G. C.1969.The failureof oxygentransport in afish sockeyesalmon(Oncorhynchus nerka). J. Fish. Res. at low levels of ambient oxygen. Comp. Biochem. Board Can. 30: 369_37'7. Physiol.29: 1253-1257. 1975.Waterborne dissolved oxygen requirements Gurr-roov, M. V. 1969.Embryonic developmentof the and criteriawith particularemphasis on the Canadian plke, Esox lucius, when incubated under different envlronment.National ResearchCouncil of Canada, oxygenconditions. hobl. Ichthyol.9: 841-851. AssociateCommittee on ScientificCriteria For En_ HeNsor.t,D. 1967. Cardiovascular dynamics and aspects of vironmentalQuality, Report No. 13, NRCC 14100: gasexchange in Chondrichthyes.Ph.D. Dissertation. 111p. Univ. \\un5fii1gton,Seattle, Wash. 178 p. DevrsoN,R. C., W. p. Bnrnzr, C. E. WennEN,AND p. Hlncnevr, B. T. 1969.Similarity of oxygen uptakeby Douoonopr. 1959. Experimentson the dissolved benthiccommunities. Limnol. Oceanogr.l4: 801-805. oxygen requirementsof coldwater fishes. Sewage Havrs, F. R. 1949.The growth, generalchemistry and Ind. Wastes3l: 950-966. temperaturerelations of salmonideggs.Q.Rev. Biol. Drtouns, P. 1973.Problems of control of breathinein 24:281-308. fishes.Comparative physiology. locomotion. resfiru- Heves, F. R., L R. Wrr-rr.ror,AND D. A. LrvrNcsroNr. tion, transport. Int. Congr. Comp. physiol. Acus- 1951.The oxygenconsumption ofthe salmonegg in parta,Italy. p. 117-133. relationto developmentand activity. J. Exp. Zool. Douoononr, P., nNo D. L. Snuuw^y. 19i0.Dissolved 116:377-395. oxygen requlrementsof freshwater fishes. Food Hercenno, P. 1944.The bottom fauna of PraestFjord. Agric. Organ.U.N., FAO Tech.pap. 86:291p. Folia Geogr.Danica 3: 58-81. DowNtNc, K. M. 1954.The influenceof dissolvedoxygen HrnnuaNN, R. B. 1958.Growthofjuvenile salmonatvari- concentrationon the toxicity of potassiumcyanide to ous concentrationsof dissolvedoxygen. M.Sc. Dis- J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 rainbowtrout.J. Exp. Biol. 3l 16l-164. sertation.Oregon State Univ., Corvallis,Oreg. Ecr-eNcHEn,B. 1972.Aition deschangements de pO, de Hrcrs, D. B., aNo J. W. Dr,Wrrr. 1971.Effects of dissol- I'eau sur la ventilationde la truite et de la tanche.J. ved oxygen on kraft pulp mill effluent toxicity. Water Physiol.(Paris) 65: 397 A. Res.5: 693-701. 2330 J. FISH. RES. BOARD CAN,, VOL. 32(12),1975

'l966. anemia on the Holn, W. S. General and Comparative Physiology. 197lb. The effect of hypoxia and trolut (Salmo Prentice-HallInc., Englewood Cliffs, N.J. 815 p. swimming performance of rainbow HocnecHxn, P., W., a.NoG. N. Sorr.rEno.1973. Strategtes gairdneri). J. Exp. Biol. 55: 541-551. 1970.A of Biochemical Adaptation. W. B. Saunders and Co., JoNps,D. R., D. J. RnNoel-r-,eNo G. M. JenveN. in fish. Resp. Philadelphia,Pa. 358p. graphical analysis of oxygen transfer HorrnaN, C. E. 1940. The relation of Donacia larvae. Physiol. 10:285-298. 1959' (Chrysomelidae: Coleoptera) to dissolved oxygen. Klrz, M., A. PnrrcH.q.no,,lNn C' E. WanneN. to swim tn Ecology2l:176-183. Ability of some salmonids and a centrarchid Am. Fish. HocluNn, L. B. 1961.The reactionsof fish in concentra- water of reduced oxygen content. Trans. tion gradients. Rep. Inst. Freshwater Res. Drottning- Soc.88:88-95. Data Repoft. 1967' holm. 43: 1-147. Kn,,,usl. D. P. 1969. Bedford Basin HoleroN, G. F. 1971. Respiratory and circulatory re- Fish Res. Board Can. Tech. Rep. 120l.84p. quotients in goldfish and sponses of rainbow trout larvae to carbon monoxide Kurrv, M. N. 1968a.Respiratory 25: 1689- and to hypoxia. J. Exp. Biol. 55: 683-694. rainbow trout. J. Fish. Res' Board Can. 1973. Respiration of Arctic Char (Salvelinus 1728. on the swim- alpinus) from a high Arctic lake. J. Fish. Res. Board 1968b. Influence of ambient oxygen '117-723. and rainbow trout. Can. Can. 30: ming performance ofgoldfish -651 HoLr,roN, G. F., lNo D. J. RaNo.q.LL. 196'7a.Changes in J . Zool. 46: 64'1 . Swimming blood pressure in the rainbow trout during hypoxia. J. Kurrv, M. N., eNo R. L. Se.uNoBRS.1973. (Salmo salar) Exp. Biol. 46:297-3O5 performance of young Atlantic salmon concentration. 1967b. The effect of hypoxia upon the partial as alfectedby reducedambient oxygen pressure ofgases in the blood and water afferent and J. Fish. Res. Board Can. 30:223-227. Responsesof efferent to the gills of rainbow trout. J. Exp. Biol. 46: L.qnrrrasn,J. F., .tNo A. H. Gor-o. 1961. to respiratory 317-327. the crayfish, Procambarus simulans, Hoos, L. M. 1973. A study of the benthos of an anoxtc stress. Physiol. Zool. 34'.16'7 -17 6. marine basin and factors affecting its distribution. Ln.HNrNcsn, A. L. 1965. Bioenergetics: the molecular M.Sc. Thesis.Dalhousie Univ., N.S. 149 p. basis of energy transformations. W. A. Benjamin, Inc' Hoos, R. A. W. 1970. Distribution and physiology of zoo- New York, N.Y. 258P. plankton in an oxygen minimum layer. M.Sc. Disser- LrNr,tNr, C., e.No K. JoHeNssN. 1966.Respiratory func- tation. Univ. Victoria, Victoria, B.C. 113p. tion in the Elasmobranch Squalus suckleyi. G. Resp' Huooenr, R., e.NoD. R. Anrnun. 1971.Shrimps in rela- Physiol.l: 13-29. tion to oxygen depletion and its ecological significance LEvINGS, C. D., lNo N. G. McDaNtBt'. 1974. A untque in a polluted estuary.Environ. Pollut. 2: 13-35. collection of baseline biological data: benthic inver- HucHEs, G. M., ,q.r.roC. M. Belr-rNrrrN. 1968. Elec- tebrates from an undetwater cable across the Strait of tromyography of the respiratory muscles and gill Georgia.FishRes. BoardCan' Tech' Rep.441: 10p. water flow in the dragonet. J. Exp. Biol. 49: 583-602. LrNonorn, A. 1942. Sauerstoffverbrauch der Fische' I. HucnEs, G. M., eNo R. L. SnuNoens. 1970.Responses of Verschiendene Entwicklungs-und Altersstadien vom For personal use only. the respiratory pump to hypoxia in the rainbow trout Lachs und Hecht.Z. vertl. Physiol. 29t 583-594' (Salmo gairdneri). J. Exp. Biol' 53: 529-545. Llovo, R. 1961. Effect of dissolved oxygen concentra- HucHEs, G. M., aNo S. UMrzaw.c. 1968a.Oxygen con- tions on the toxicity of several poisons to rainbow sumption and gill water flow in the dogfish ScyLior- IrouI (Salmo gairdneri Richardson). J. Exp. Biol 38: hinus canicula l. J. Exp. Biol. 49: 554-564. 447-455. 1968b. On the respiration in the dragonet' Ca! LozrNov, A. B. 1956. The oxygen optimum of young lionymus lyra L. J . Exp. Biol. 49: 565-582. sturgeon. Doklady Akad. Nauk S.S.S.R. 10'l:33'7-9: InvrNc, L., E. C. Bl.qcx, AND V. Srepnonl. 1941' The Biol. Abstr. 32: Abstr. 30869. influence of temperature upon the combination of M.qcLBoo, J. C., aNo L. L. Slarrn. 1966.Effect of pulp- oxygen with the blood oftrout. Biol. Bull. 80: 1-17. wood fibre on oxygen consumption and swimming Ira.zewe, Y. 1970. Characteristics of respiration of fish endurance of the fathead minnow. Trans. Am. Fish. considered from the arterio-venous difference ofoxy- Soc.95:71-84. gen content. Bull. Jap. Soc. Sci. Fish. 36: 571-5"17. Mensner-L, S. M., A. G. Ntcnolls, eNo A. P. Onn' 1935. JoneusrN, K., .qNo C. LpNreNr. 1966. Gas exchange ln On the biology of Calanus finmarchicus. Part VI' the Cephalopod, Octopus dofleini. Am' J. Physiol' Oxygen consumption in relation to environmental 210:910-918. conditions. J. Mar. Biol. Assoc. U.K. 2O: l-28. Jon.qNsr,N. K., aNo R. L. V.c.o,A.s.1967. Oxygen uptake McLEesB, D. W. 1956.Effects of temperature, salinity and and responses to respiratory stress in sea urchins. oxygen on the survival of the American lobster. J. Biol. Bull. 132: 16-22. Fish. Res. Board Can. 3l:.24'7-272. JoHNsroN, L. M. 1936. The control of respiratory move- MrrcnELr-, P. H. 1912. The oxygen requirements of ments in crustacea by oxygen and carbon dioxide' II. shellfish. Bull. U.S. Bur. Fish. 32:209-222. J. Exp. Biol. 13:46'1-475. Moonn, H. B. 1964. Marine Ecology, 3rd ed. John Wiley JoNss, D. R. 1971a. Theoretical analysis of factors which and Sons, Inc., London.493 P. J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18 may limit the maximum oxygen uptake of fish: the Mosgrnt, G. A., C. R. Gor-ova.N, G. L. GoosHr.I-r, lNo oxygen cost of the cardiac and branchial pumps. J. D. R. Mur-1. 1970. The effects of variations in oxygen Theor. Biol. 32: 341-349. tension on certain aspects of respiratory metabolism DAVIS: REVIEW OF OXYGEN REQUIREMENTS oF AQUATIC LIFE 233r

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BnowN. 1962.Comparative of hydrogenion concentrationon theminimum dissol- animalphysiology, 2nd ed. W. B. Saundersand Co., ved oxygen tolerationof the silver salmon(Oncor_ London.688 n. hync hus kis ut c h). Ecology25: 461466. ReNoer-L,D. J. 1970.Gas exchange in fish,p. 253-292.In TowNseNo,L. P.,aNo D. EenNtsr. 1940.The effects of W. S. Hoar and D. J. Randall[ed.] Fish physiology. low oxygenand other extreme conditions on salmonid Vol. IV. Academichess Inc.,New york, N.y. fish.Proc. Sixth Pax. Sci. Congr. 3: 345-351. RnNoaLl, D. J., G. F. Horeror, er.roE. D. Srt,vrrs. TowNspNo,L. P., A. KnrxspN,AND D. Eantesr. 1938. 1967.The exchangeof oxygen and carbon dioxide Progressreport on field investigationsand research. acrossthe gills of rainbow trout. J. Exp. Biol. 6: Wash.State Pollut. Comm., Seattle, Wash. 47 p. 339-348. Tnuesoarr, G. A., eNo A. L. H. GeuesoN.1957. The ReNoaLl.D. J., eNo J. C. Surru. 1967.The reeulation of solubility of oxygen in salinewater. Extr. J. 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IN THIs REPoRT WHrruone, C. M., C. E. W.lnnnN, eNo P. Douoonorr. AooI.rtoNeL Rpnpnr,Ncns Nor INcLUDED 1960. Avoidance reactions of salmonids and centrar- AT TIME OF COMPILATION. chid fishes to low oxygen concentrations' Trans. Am' Fish. Soc. 89: 17-26. BovNp, B. L. 1973. The response of three species of Wnrrwonrn. W. R. 1968.Effectsof diurnalfluctuationsof bivalve mollusk to declining oxygen tension at re- dissolved oxygen on the growth ofbrook trout. J. Fish duced salinity. Comp. Biochem. Physiol. 45:'793-806. Res. Board Can.25: 5'79-584. Pan.nsaoe.R,lo, D. G. V., lNo P' N. GeNlparI. 1968' WrcKErr, P. 1954. The oxygen supply to salmon eggs in Respiration as a function of oxygen concentration in spawningbeds.J. Fish. Res. BoardCan. ll:933-953. iirtertidal barnacles. Mar. Biol' 1: 309-310. WtEsB, A. H. 1933.The effect of high concentrationsof dissolved oxygen on several species of pond fishes. S.qsseueN, C., eNo C. P. MlNcula. 1972. Adaptations to Ohio J. Sci.33: 110-126. environmental oxygen levels in infaunal and epifaunal WrpsEn, W., eNo J. KlNwIsnBr.. 1959.Respiration and sea anemones. Biol. Bull. 143:.657-678. anaerobic survival in some seaweed inhabiting inver- TnBsor,, J., A. PoNer, K. Htnorr, eNo C. ScnuEpBn. Biol. Bull. I 17:594-600. rebrates. 1969. Studies on the resistance of marine bottom in- L. 1939. The oxygen threshold for three WrrnrNc, J. vertebrates to oxygen deficiency and hydrogen 20: 253-263' species of fish. Ecology sulfide. Mar. Biol. 2: 325-337. WooDBURY, L. A. 1942. A sudden mortality of fishes ac- and companying a supersaturation of oxygen in Lake WonlscHI-ec, D. E. 1964. Respiratory metabolism in McMurdo Waubesa,Wisconsin. Trans. Am. Fish. Soc. 7l: 112- ecological characteristics of some fishes tt'7. Sound. Antarctica. In M. O. Lee [ed.] Biology of the YouNc. J. S. 1973.A marine kill in New Jersey coastal antarctic seas. Am. Geophys. Union, Washington' (Antarct. waters. Mar. Pollut. Bull. 4: 70 P. D.C. Res. Ser. l:33-62. For personal use only. J. Fish. Res. Bd. Can. Downloaded from www.nrcresearchpress.com by UNIV OF WASHINGTON LIBRARIES on 07/11/18