Tissue Respiration in Invertebrates

TISSUE RESPIRATION IN INVERTEBRATES

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TISSUE RESPIRATION IN INVERTEBRATES

DOROTHY E. BLISS Associate Curator

Department of Living Invertebrates The American Museum of Natural History and Research Assistant Professor Department of Anatomy The Albert Einstein College of Medicine

DOROTHY M. SKINNER

Assistant Professor Department of Physiology and Biophysics New York University School of Medicine

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THE AMERICAN MUSEUM OF NATURAL HISTORY NEW YORK: 1963

PREFACE

May we introduce this work with an explan- to tissues derived from invertebrates of many ation of its general organization and its species, the section includes no information

contents? In Section 1, Introduction, we have regarding the respiration of protozoans, nor traced the historical development of the study does it deal with respiratory rates of sperms of invertebrate tissue respiration from its be- and of fertilized or unfertilized eggs. ginnings late in the nineteenth century up to the Many types of tissue preparations are men- present time. In doing so, we have placed par- tioned in Section 2. These include whole organs, ticular emphasis on the influence exerted by slices, teased tissues, minces, cell suspensions, new apparatus and techniques. We have pre- homogenates, and fractions (nuclear fraction, sented graphically the distribution of studies mitochondria, microsomes, or soluble fraction). among various phyla and classes of inverte- The arrangement of data in Section 2 is phy- brate animals. From this initial survey it logenetic, according to the classification ad- should be apparent to the reader how rapidly vocated by Hyman (1940-1959, vol. 1). Since the field of invertebrate tissue respiration is phylum and class are the categories most fre- developing and how broad and active it remains quently selected for mention by biochemists today. and experimental biologists, we have not in- While scanning the literature, we found a cluded references to other higher categories. wealth of usable data. Section 2, the principal The valid scientific name of each animal and portion of this volume, contains these data, ar- at least one of its common names appear in ranged to indicate the variation in respiratory this section. In a Systematic Index (see Section rate with animal and type of tissue, with amount 9) a scientific name, if no longer valid, can be of tissue, with concentration and type of sub- traced to the presently correct one. strate, with sex of the animal, with season of In order to tabulate the data on invertebrate the year in which the assay was made, and with tissue respiration, we found it necessary to many other factors. convert figoires on oxygen uptake from the Owing to such an abundance of material, we units employed by a given investigator into one found it necessary to limit our coverage as re- of several selected expressions of metabolic gards specific enzymes and enzyme systems. rate. Thus in Section 2, data appear as the Thus, while Section 2 includes many examples mean number of microliters of oxygen per hour of endogenous respiration, for the most part it per milligram of nitrogen, protein, wet weight, omits reference to enzymes other than those or dry weight, or alternatively as '^^ enzymatic of the citric acid cycle and the electron trans- activity," with footnotes indicating the units in port system. Furthermore, whereas data from which enzymatic activity is given. The complete an original paper containing few entries usu- list of footnotes, which are arranged in an ar- ally appear in their entirety, those from a bitrary, not sequential, order, is repeated on more extensive study have been selected (1) to each page of Section 2, although a reference afford representative sampling and (2) to illus- to every footnote may not appear on every page trate principles and hypotheses. Footnote su- within the body of the table. perscript "t" appears after any bibliographi- Wherever we have converted our units, we cal reference in Section 2 if there are more have indicated this fact by the footnote super- data in an original paper than appear in Sec- script "a" after the data. When possible, we tion 2. have changed all expressions for concentration Although the data contained in Section 2 refer of reactants into molarity and have noted this VI TISSUE RESPIRATION IN INVERTEBRATES also by the superscript "a." We have omitted formation contained within an original paper all reference to standard deviation and stand- but not included in Section 2. ard error. A discussion (Section 4) follows the analysis Within the table comprising Section 2 is a of data. It is concerned not only with the mate- column bearing the title "Remarks." It con- rial presented in tabular form in Section 2 and tains miscellaneous information about the analyzed in the subsequent section but also with salt solutions and inhibitors used, the methods broad principles and hypotheses suggested in the employed for determining nitrogen content, various original papers. This discussion seeks the composition of various gas phases, and so to examine selected data in terms of the light on. In this column we have noted, for example, that they may shed upon these principles and that during an assay cytochrome c was present hypotheses. in the complete system, that P/O ratios ap- A list of abbreviations and symbols used in pear in an original paper, or that specimens Section 2 appears in Section 5. Wherever pos- used in a particular study were collected dur- sible, abbreviations are identical with those ing winter and spring. In other words, items given in Webster's New International Dictionary, that we consider vital for proper evaluation of second edition, unabridged, 1958. the data appear in this column. Section 6 consists of the Glossary, which is There are many unfilled spaces in Section intended to give in a cursory way some under- 2. The reader should clearly understand their standing of the many technical terms used in significance. The scientific name and common this work. For the most part, this glossary does name of an animal appear only once for each not include terms that appear in Webster's New work. Such usage is also true for temperature, International Dictionary, second edition, un- providing there is no change in this factor abridged, 1958. during a given study, and also for apparatus, In Section 7 (Guide to Literature), we have when only one type is used throughout the study. made suggestions for supplementary reading The author or authors and the date of publica- on tissue metabolism and other pertinent fields. tion are given once for each work. Thus, an Here we have listed books and articles that deal unfilled space in the first, second, third, and with such topics as cell structure, electron last columns signifies that the same animal microscopy, intermediary metabolism, and man- was used by the same author at the same ometric methods, to name a few. Popular, semi- temperature and with the same apparatus as popular, and semi -technical references bear an previously noted. asterisk. The complete citation for each book Quite a different meaning should be read and article appears in the Bibliography (Section into an unfilled space in columns 4 through 15. 8). In these coluntms such a blank space usually Section 9 consists of three indexes. In the indicates that no information regarding the first, designated the Systematic Index, there is point in question appears in the original a page reference for every mention of a given paper. In a few instances, however, an un- animal in this volume. Insofar as we are aware, filled space in columns 4 through 15 relates the generic and specific names appearing in this to data or descriptive material which, in our work are valid. Occasionally an author has used opinion, is either unsuitable for inclusion or an invalid name in an original paper. By use of of questionable interpretation. the Systematic Index, the reader can trace the In Section 3 we have analyzed the data on invalid name to the presently correct one. Also invertebrate tissue respiration, giving em- indexed here are common names of animals phasis to principles and relationships that the cited in the present work. data illustrate. We have noted particularly the In the Author Index, there is a reference for effects of metabolic inhibitors and the influ- every citation in this volume (exclusive of the ence of sex, age, composition of the suspending Bibliography). medium, surgery, injury, and stage in the The third and last index deals with the vari- molt cycle or life cycle on tissue respiration ous subjects of which there is mention in this in various invertebrates. In some instances work. we have based our analysis in part upon in- No paper on invertebrate tissue respiration PREFACE Vll

that has come to our attention since February 1, out her, this volume would never have reached 1960, have we analyzed for inclusion in this work. its final stages. On the other hand, we have cited without analysis For giving freely of their time and still re- some papers that have appeared since that time. taining their patience despite the trying nature The closing date does not apply to entries in Sec- of their tasks, we thank Miss Ana Uscocovich, tions 7 and 8, which we have continually revised Mrs. Phyllis Fish, and Miss Joan Ruff, typists. to include pertinent recent publications. For considerable assistance in the initial stages May we request that any reader who finds of the work, when references had to be tracked errors or omissions in this volume bring them down and unwanted ones eliminated, we acknowl- to our attention? Should usage justify such ac- eged particularly the help of Mrs. Patricia tion, we may eventually assemble and publish Cannon Sprague. For other assistance of vari- any data appearing in new studies or in those ous sorts during the course of compilation, we inadvertently omitted from the present work. are grateful to Mrs. Jane Rouillion Boyer, Persons to whom we owe a debt of gratitude are Mr. William F. Mussig, Mr. Frederick V. Weir, many. In the first place, we thank Dr. William R. and Mrs. Mary Weitzman. For their competent Harvey, Dr. Melvin V. Simpson, and Dr. Heinrich help in the tedious task of preparing the indexes, Waelsch, all of whom offered valuable advice re- we thank Mr. Arnold Ross and Miss Susan E. garding the content and format of certain entries. Bliss. For verifying scientific names and making We have a special word of thanks for mem- suggestions regarding generally accepted com- bers of the staff of the Library of the American mon names, we thank Dr. Elisabeth Deichmann, Museum of Natural History, who furthered in Dr. William K. Emerson, Dr. G. E. Gates, Dr. no small way the progress of our work. Willard D. Hartman, Dr. Libbie H. Hyman, Mr. We also express our gratitude to Dr. Charles Morris K. Jacobson, and Mr. John C. Pallister. M. Breder, Jr., and to members of the Publica- Valid names of Crustacea came from the sys- tions Committee of the Council of the Scientific tematic index included in Waterman (1960). Ac- Staff of the American Museum of Natural His- cording to the preface, Dr. Fenner A. Chace, tory for making possible the preparation and Jr., acted as referee on all taxonomic citations printing of this volume. pertaining to the Crustacea. Hence, for their Lastly, we gratefully acknowledge the sup- indirect assistance, we are grateful to Dr. port of the National Science Foundation through Chace and Dr. Waterman. grants (NSF G-4006 and NSF G-11254) to one For suggesting or verifying definitions of of us (D.E.B.), and also the support of both the terms included within the glossary we thank Dr. National Institute of Neurological Diseases and H. E. Coomans, Dr. Emerson, Dr. Henry Har- Blindness and the National Cancer Institute of bury. Dr. Hyman, Dr. Mary Ellen Jones, Dr. the United States Public Health Service through Sam Katz, Dr. Sasha Malamed, Dr. Berta predoctoral and postdoctoral fellowships to Scharrer, and Dr. Simpson. the other (D.M.S.) while she was at Radcliffe For permitting inclusion of unpublished mate- College, Brandeis University, and Yale Uni- rial, we thank Dr. Rose Robyns Coelho and Dr. versity. Harvey. The unpublished data submitted by Dr. We have tried to produce an accurate refer- Harvey appear in his thesis for the Ph.D. de- ence on tissue respiration in invertebrates. gree, Harvard University. For all errors that remain, we accept full re- For permission to quote a passage from Cancer sponsibility. Research, we thank the University of Chicago. For her patient, experienced editorial advice DOROTHY E. BLISS and guidance, we express appreciation to Miss DOROTHY M. SKINNER Ruth Tyler, Editor of Scientific F>ublications of the American Museum of Natural History. With- December 15, 1961

CONTENTS

Preface v

Section 1: Introduction 1

Section 2: Presentation of Data: A Table of Respiratory Rates of Invertebrate Tissues 7 Porifera 9 Demospongiae 9 Coelenterata 11 Hydrozoa 11 Scyphozoa 11 Anthozoa 11 Aschelminthes 11 Nematoda 11 Mollusca 15 Gastropoda 15 Pelecypoda 21 Cephalopoda 33 Annelida 39 Polychaeta 39 Clitellata 41 Arthropoda 43 Merostomata 43 Crustacea 45 Insecta 55 Echinodermata 73 Holothuroidea 73

Section 3: Analysis of Data 75 Effects of Certain Inhibitors on Respiratory Rate 75

2, 4-Dinitrophenol (DNP) 75 Carbon Monoxide (CO) 75 Cyanide 75 Antimycin A 76 Comparison of Respiratory Rates of Various Tissues 76 Sex Differences in Respiratory Rate 77 Variation in Respiratory Rate with Age 78 Variation in Respiratory Rate During Crustacean Molt Cycle 78 Variation in Respiratory Rate During Insect Life Cycle 78 Variation in Respiratory Rate with Season 79 Variation in Respiratory Rate with Salinity 79 Effects of Various Ions on Respiratory Rate 79 Gradient of Respiratory Rate Along Long Axis of Body 79 Gradient of Respiratory Rate Along a Nerve 79 Respiratory Rate After Removal of Endocrine Organs 80 Respiratory Rate Following Injury 80

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Section 4: Discussion 81 Enzymes of Citric Acid Cycle 81 Cytochrome System 81 Comparison of Respiratory Rates of Various Tissues 83 Sex Differences in Respiratory Rate 83 Variation in Respiratory Rate with Age 84 Variation in Respiratory Rate During Crustacean Molt Cycle 84 Variation in Respiratory Rate During Insect Life Cycle 86 Respiratory Rate Following Injury 86 Effect of Environment on Respiratory Rate 86 Effect of Various Ions on Respiratory Rate 86 Gradients in Respiratory Rate 86

Section 5: Abbreviations and Symbols 89 Section 6: Glossary 91 Section 7: Guide to Literature 95

Section 8: Bibliography 101 Section 9: Indexes 119 Systematic Index 119 Author Index 123 Subject Index 127 1^1 LI.

Section 1: INTRODUCTION

This introductory chapter traces the historical development of the study of invertebrate tissue respiration as a branch of experimental biology. Interest in its study has appeared relatively recently. It is only slightly more than 30 years since the first work to come to the attention of the authors appeared in print. Today tissue respiration of the invertebrates is an established domain of the experimental biologist. During the period 1929 through 1959, there occurred at least 114 studies on the respiration of invertebrate tissues as reported in 98 different papers. Other published accounts, not known

30 TISSUE RESPIRATION IN INVERTEBRATES

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01 INTRODUCTION

graph emphasizes the trend through the years towards the use of more and more finely divided tissue preparations. The vertical arrow indicates the approximate time when methods for the preparation of suspensions and homogenates first appeared. The use of homogenates and particulate fractions derived from homogenates in studies on invertebrate tissue respiration followed quickly upon this development. At no time during the 30-year period have whole organs or tissue slices fallen into dis- favor as subjects for respiratory studies. Indeed, in 1950 Krebs questioned the trend towards the disruption of cell structure in attempts to ex- plore certain aspects of cell physiology. He pointed out that one can attribute much of the conflicting data on the respiratory rates of A B C D E F G homologous tissues from different animals to PREPARATION the type of tissue preparation and the type of Fig. 3. Percentage distribution of various medium used. From his studies he concluded types of tissue preparations employed in studies that tissue slices suspended in particular syn- on invertebrate tissue respiration from 1929 thetic media comprise the type of preparation through 1959. Types of preparations indicated as follows: A. Whole organ. B. Pieces (including) most likely to yield meaningful results. fragments, strips, teased tissue, zones, parts). For the future, therefore, a reverse trend has C. Slices (including sheets, thin sections). something to recommend it. According to Green- D. Suspension (including cell suspension, ground stein (1956, p. 651): "It is possible that studies tissue, mince). E. Homogenate. F. Particulate of cellular metabolism, which began with obser- fraction (including mitochondria and microsomes). vation on the whole animal and then progressed G. Other fractions (nuclear, supernatant). successively through studies of isolated organs, ical aids. For a more complete treatment of tissue slices, homogenates, cell fractions, and work with tissue slices, see Field (1948) and finally highly purified individual metabolic fac- Robbie (1948). tors can with profit turn back to the whole ani- Soon a method was devised for fractionating mal. Studies of the effect of constitutional factors tissues into their finely ground or homogenized on metabolic reactions . ... in vitro provide a cellular components by centrifugation at differ- certain interest but, like all in vitro approaches, ent speeds for different lengths of time (see are at the mercy of the experimental conditions Claude, 1946a, 1946b: Schneider, 1946). Thence- which the investigator chooses to select." forth, workers directed much of their attention Just as methods of preparing tissues for study to characterizing these cell fractions. They of their respiratory rates have undergone studied the effects of various metabolites, ions, marked changes over a period of years, so also suspending media, and poisons on the respiratory have the ways in which respiratory measure- rates of the various fractions and also on the ments are made. First, let us examine the per- ability of these fractions to form the high-energy centage distribution of the various methods. phosphate compounds found to be coupled to More than one-half of the investigations cited in their respiration. Section 2 have involved the use of the Warburg In figure 3 there appears the per cent of the manometric method (see fig. 5A), while 16 per total number of studies on invertebrate respira- cent have involved various forms of differential tion for which each type of procedure was used. manometer, including Fenn, Barcroft, and Thun- Selection of the whole organ (A), pieces of organ berg (fig. 5B). Another 11 per cent of these stud- (B), and homogenate (E) took place with approx- ies were concerned with the spectrophotometer imately equal frequency. A more revealing (fig. 5E), 5 per cent with chemical methods graph is that of figure 4. The diagonal line from (Winkler and micro -Winkler, fig. 5D), 4 per the lower left to the upper right corner of the cent with microvolumetric techniques (fig. 5C), TISSUE RESPIRATION IN INVERTEBRATES

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a> Section 2: PRESENTATION OF DATA: A TABLE OF RESPIRATORY RATES OF INVERTEBRATE TISSUES

18 TABLE OF RESPIRATORY RATES OF INVERTEBRATE TISSUES ANIMAL 20 TABLE OF RESPIRATORY RATES OF INVERTEBRATE TISSUES ANIMAL 22

28 TABLE OF RESPIRATORY RATES OF INVERTEBRATE TISSUES ANIMAL 30 TABLE OF RESPIRATORY RATES OF INVERTEBRATE TISSUES

ANIMAL 32

36 TABLE OF RESPIRATORY RATES OF INVERTEBRATE TISSUES

ANIMAL 38 TABLE OF RESPIRATORY RATES OF INVERTEBRATE TISSUES 39 ANIMAL 40

44 TABLE OF RESPIRATORY RATES OF INVERTEBRATE TISSUES

ANIMAL 46

48 TABLE OF RESPmATORY RATES OF INVERTEBRATE TISSUES

ANIMAL 50

52 TABLE OF RESPIRATORY RATES OF INVERTEBRATE TISSUES 53

ANIMAL 54 TABLE OF RESPIRATORY RATES OF INVERTEBRATE TISSUES 55 ANIMAL 56

58 OF RESPIRATORY RATES OF INVERTEBRATE TISSUES TABLE 59 ANIMAL 60

64 TABLE OF RESPIRATORY RATES OF INVERTEBRATE TISSUES ANIMAL 66

68 TABLE OF RESPIRATORY RATES OF INVERTEBRATE TISSUES ANIMAL 70

72 TABLE OF RESPIRATORY RATES OF INVERTEBRATE TISSUES 73 ANIMAL 74 Section 3: ANALYSIS OF DATA

EFFECTS OF CERTAIN INHIBITORS ON RESPIRATORY RATE

2, 4-DINITROPHENOL (DNP)

Effect: Respiration maximally stimulated by the concentration of DNP that produces maximal inhibition of ciliary activity; this effect noted in: MoUusca Pelecypoda Crassostrea virginica: Mantle; Maroney, Barber, and Wilbur, 1957 Mytiliis: Gill; Weller and Ronkin, 1952 Effect: Rise in respiratory rate; this effect noted in: Aschelminthes Nematoda Ascaris lumbricoides: Muscle; Chin and Bueding, 1954 Mollusca Pelecypoda Pinctada martensii: Gill; Kawai, 1957 Effect: Stability of rate of esterification of phosphate in suspension to which DNP has been added;

suggests that the phosphorylations result from anaerobic reactions; this effect noted in: Mollusca Gastropoda Helix pomatia: Midgut gland; Rees, 1953

CARBON MONOXIDE (CO)

Effect: Photoreversible inhibition of respiration, i.e., inhibition of respiration by CO in darkness but not in light; strongly suggests the involvement of cytochrome oxidase in the electron transport system; this effect noted in: Mollusca Pelecypoda Crassostrea gigas: Gill, mantle; Kawai, 1958 Cephalopoda Octopus macropus: Salivary gland; Ghiretti-Magaldi, Giuditta, and Ghiretti, 1958

CYANIDE

Effect: Inhibition of endogenous respiration; may indicate the involvement of cytochrome oxidase in the electron transport system; effect noted in: Porifera Demospongia Cinachyra cavernosa, Dysidea crawshayi, Geodia gibberosa, Ircinia fasciculata, Lissodendoryx

isodictyalis , Pseudaxinella rosacea, Spheciospongia sp., Tedania ignis, Terpios fugax, Tethya aurantia: Slices; Robbie, 1949

75 76 TISSUE RESPIRATION IN INVERTEBRATES

Coelenterata Hydrozoa Physalia phy salts: Tentacles; Robbie, 1949 Anthozoa Condylactis ,^iga7itea: Tentacles; Robbie, 1949 Gorgonia flabellum: Branches; Robbie, 1949 Plexaura flexuosa: Slices; Robbie, 1949 Mollusca Pelecypoda Crassostrea virginica: Mantle; Jodrey and Wilbur, 1955

Isognomon alata : Gill; Robbie, 1949 Mercenaria mercenaria: Gill, mantle, adductor muscle; Hopkins, 1949 Pinctada martensii: Gill; Kawai, 1957. Heart; Navez, Crawford, Benedict, and DuBois, 1941 Cephalopoda Loligo pealeii: Gill; also retina, lens and "cornea" of eye; Robbie, 1949 Arthropoda Crustacea Panulinis argus: Leg nerve, leg muscle, midgut gland; Robbie, 1949 Effect: Inhibition of endogenous respiration and complete or partial reversal of this inhibition by methylene blue; suggests the involvement of cytochrome oxidase; this effect noted in: Mollusca Pelecypoda Crassostrea gigas: Mantle, gill; Kawai, 1958 Cristaria plicata: Gill; Higashi and Kawai, 1959 Hyriopsis schlegelii: Gill; Higashi and Kawai, 1959 Arthropoda Crustacea Homarus americanus'- Leg nerves and nerve cord; Chang, 1931 Effect: Inhibition of endogenous respiration by cyanide but the inhibition not reversible by methylene blue; suggests that some terminal oxidase other than cytochrome oxidase may be involved in electron transport; this effect noted in: Mollusca Pelecypoda Crassostrea gigas: Gill; Okamura, 1959 Crassostrea virginica: Mantle; Jodrey and Wilbur, 1955

ANTIMYCIN A

Effect: Inhibition of respiration because the oxidation of succinate via the pathway involving the Slater factor is blocked; this effect noted in: Arthropoda Insecta Hyalophora cecropia: Wing epithelium of pupa and adult, Shappirio and Williams, 1957b Periplaneta americana: Coxal muscles of legs of adult; Harvey and Beck, 19 53

COMPARISON OF RESPIRATORY RATES OF VARIOUS TISSUES

The following studies are concerned with the comparative endogenous respiratory rates of various tissues of invertebrates; the results of no study are given here in their entirety. ANALYSIS OF DATA 77

Mollusca Gastropoda Helix pomatia: Cerebral ganglion > midgut gland > muscle of foot; Kerkut and Laverack, 1957 Pelecypoda Crassostrea gigas: Gill > heart > mantle; Kawai, 1959 Cristaria plicata: Gill > heart > mantle > adductor muscle; Higashi and Kawai, 1959 Gryphaea angulata: Gill > midgut gland > mantle > muscle; Chapheau, 1932 Hyriopsis schlegelii: Gill > heart > mantle > adductor muscle; Higashi and Kawai, 1959 Mercenaria mercenaria: Gill > mantle > muscle; Hopkins, 1946 Pinctada martensii: Gill > midgut gland > muscle of foot; Kawai, 1957 Cephalopoda Octopus vulgaris: Optic ganglion > branchial heart > gill > central heart > midgut gland > mantle muscle; Ghiretti-Magaldi, Giuditta, and Ghiretti, 1958 Arthropoda Merostomata Limulus Polyphemus: Forebrain > foregut > optic nerve (axon) > muscle > optic nerve (sheath); Shapiro, 1937 Crustacea Callinectes sapidus: Midgut gland > gill; Vernberg, 19 56 Clibinarius vittatus: Midgut gland > gill; Vernberg, 1956 Lobster (sci. name not given): Midgut gland > muscle; Kermack, Lees, and Wood, 19 54 Libinia dubia: Midgut gland > gill; Vernberg, 1956 Menippe mercenaria: Midgut gland > gill; Vernberg, 1956 Ocypode quadrata: Gill > midgut gland; Vernberg, 1956

Panopeus herbs tii: Midgut gland > gill; Vernberg, 1956 Sesarma cinereum: Gill > midgut gland; Vernberg, 1956 Uca minax: Midgut gland > gill in male; gill > midgut gland in female; Vernberg, 1956 Uca pugilator: Gill > midgut gland; Vernberg, 1956 Insecta Belostoma spp.: Flight muscle of adult > leg muscle; Perez-Gonzalez and Edwards, 1954 Hydrophilus ater: Flight muscle of adult > leg muscle; Perez-Gonzalez and Edwards, 1954 Periplaneta americana: Flight muscle of adult > leg muscle; Perez-Gonzalez and Edwards, 1954 Schistocerca infumata: Flight muscle of adult > leg muscle; Perez-Gonzalez and Edwards, 1954

SEX DIFFERENCES IN RESPIRATORY RATE

The following studies deal in part with the differences in respiratory rate between males and females; in some cases the differences are slight. Arthropoda Crustacea Callinectes sapidus: Midgut gland, gill; female > male; Vernberg, 1956 Libinia dubia: Midgut gland, gill; female > male; Vernberg, 1956 Menippe mercenaria: Midgut gland, gill; female > male; Vernberg, 1956 Ocypode quadrata: Midgut gland, gill; male > female; Vernberg, 1956 Panopeus herbstii: Midgut gland, male > female; gill, female > male; Vernberg, 1956 Pugettia producta: Midgut gland; male > female; Belding, Field, Weymouth, and Allen, 1942 Uca minax: Midgut gland, male > female; gill, female > male; Vernberg, 1956 Uca pugilator: Midgut gland, gill; male > female; Vernberg, 1956 Insecta Carpocapsa pomonella: Muscle, fat body of larva; female > male; Graham, 1946 Leucophaea maderae-. Thoracic muscle; rate of female approximately equal to rate of male; Samuels, 1956 Periplaneta americana: Leg muscle of adult; male > female; Barron and Tahmisian, 1948. Leg 78 TISSUE RESPIRATION IN INVERTEBRATES

muscle of adult; male > female; Allen and Richards, 1954. Flight and leg muscles of adult; male > female; Perez -Gonzalez and Edwards, 1954. Many tissues of adult; with exception of foregut, male > female; Sacktor and Thomas, 1955. Metathorax of adult; male > female; Kubista, 1956. Fat body of nymph; male > female; Young, 1958 Sarcoplmga bullata: Thoracic muscles of adult; female > male; Allen and Richards, 1954 Tenebrio molitor: Flight and leg muscles of adult; female > male; Allen and Richards, 1954

VARIATION IN RESPIRATORY RATE WITH AGE

Mollusca Pelecypoda Crassostrea virginica: Adductor muscle; decline in endogenous respiratory rate with age (from shell length of 5.0 cm. to one of 14.7 cm.); Hopkins, 1930 Gryphaea angulata: Mantle, gill, muscle, midgut gland; decline in endogenous respiratory rate with age (from 10-15 mos. to 6 yrs.); Chapheau, 1932 Mercenaria mercenaria: Posterior adductor muscle; decline in endogenous respiratory rate with age (from shell length of 6.5 cm. to one of 9 cm.); Hopkins, 1930. Adductor muscle, mantle, gill; decline in endogenous respiratory rate with age (from 2-6 yrs. to 7-20 yrs.), except respiratory rate of gill tissue of both size classes essentially the same during winter and spring; Hopkins, 1946

VARIATION IN RESPIRATORY RATE DURING CRUSTACEAN MOLT CYCLE

Arthropoda Crustacea Carcinus maenas: Muscle; cyanide-insensitive respiration (with added fructose) lowest just before ecdysis, then rising during ecdysis and in the post-ecdysial, soft-shelled stage, with maximum rate during intermolt; no oxygen uptake in the absence of fructose or glucose; Krishnan, 1954 Gecarcinus lateralis: Integumentary tissues; endogenous respiration just before ecdysis 1.6 times that during intermolt period; Skinner (MS.)

VARIATION IN RESPIRATORY RATE DURING INSECT LIFE CYCLE

Arthropoda Insecta Calliplwra erythrocepliala: Flight muscle; a-ketoglutaric oxidase activity relatively high during first seven days after adult emergence, lower during eighth to tenth day, then up again at 15 to 17 days; Lewis and Slater, 1954; Slater and Lewis, 1954 Hyalopiwra cecropia: Wing epithelium; fall in the activity of several enzymes within 24 hours of pupation, and then a marked rise in their activity during adult development; Shappirio and Williams, 1957b Periplaneta americana: Leg muscle; no marked difference in respiratory activity between 10- to 20-day adults and 95- to 185-day adults; Allen and Richards, 1954 Periplaneta americana: Leg and wing muscle, pigmented ("pink") or destined to be pigmented; respiratory activity low in nymphs, higher in 1- to 5-day adults, and still higher in 15- to 65- day adults; Brooks, 1957 Phormia regina: Muscle; cytochrome oxidase activity higher in 1-day adults than in 3- to 22-day adults; activity of certain other enzymes higher in older than in younger adults; Watanabe and Williams, 1951 ANALYSIS OF DATA 79

VARLATION IN RESPIRATORY RATE WITH SEASON

Mollusca Pelecypoda Mercenaria mercenaria: Gill, mantle, muscle; in general, endogenous respiratory rate highest in winter and early spring and lowest in August and September; Hopkins, 1946 Pinctada martensii: Gill; rise in endogenous respiratory rate from June to the middle of January; Kawai, 1957

VARIATION IN RESPIRATORY RATE WITH SALINITY

Mollusca Pelecypoda Mercenaria mercenaria: Gill, mantle, increase in endogenous respiratory rate with lowered salinity; adductor muscle, decrease in rate with lowered salinity; Hopkins, 1949 Arthropoda Crustacea Carcinus maenas: Gill; increase in endogenous respiratory rate with lowered salinity; Pieh, 1936

EFFECTS OF VARIOUS IONS ON RESPIRATORY RATE

Mollusca Gastropoda

Helix aspersa: Heart; rise in endogenous respiratory rate with increasing concentration of K"*"

ion, compared to the concentrations of Na+, Ca"'"'', and Mg "'""'"; Cardot, Faure, and Arvanitaki, 1950 Pelecypoda Mytilus galloprovincialis: Ventricle of heart; same as above; Cardot, Faure, and Arvanitaki, 1950 Cephalopoda Sepia officinalis: Nerve; same as above; Cardot, Faure, and Arvanitaki, 1950 Arthropoda Crustacea Libinia emarginata: Claw nerve; rise in endogenous respiratory rate with increasing concentra-

tion of K"*" ion to a maximum at 40 mM K^, then sharp drop in endogenous respiratory rate; Shanes and Hopkins, 1948

GRADIENT OF RESPIRATORY RATE ALONG LONG AXIS OF BODY

Annelida Clitellata Eisenia foetida: Viscera and body wall; U-shaped gradient in the endogenous respiratory rate and in succinoxidase activity along the long axis of the body; O'Brien, 1957 Octolasium cyaneum: Body wall; U-shaped gradient in succinoxidase activity; O'Brien, 1957 Arthropoda Insecta Periplaneta americana: Prothorax, mesothorax, metathorax, abdomen; decrease in endogenous respiratory rate from prothorax through metathorax, and then a rise in respiratory rate in abdomen; Kubista, 1956

GRADIENT OF RESPIRATORY RATE ALONG A NERVE Arthropoda Merostomata Limulus Polyphemus: Optic nerve; at 31° and 28° C, endogenous respiratory rate highest in 80 TISSUE RESPIRATION IN INVERTEBRATES

medial region of nerve, but at 16° C. rate highest in proximal region; endogenous respiratory rate at distal end lower than at proximal end; Guttman, 1935 Limulus Polyphemus: Optic nerve; at 24° C, endogenous respiratory rate highest in medial region of nerve; gradient much more pronounced for axon than for sheath; Shapiro, 1937

RESPmATORY RATE AFTER REMOVAL OF ENDOCRINE GLANDS Arthropoda Crustacea Carcinus maenas: Muscle; respiration (with added succinate) lower after eyestalk removal, higher again after addition of eyestalk extract; Scheer, Schwabe, and Scheer, 1952 Carcinus maenas: Muscle; cyanide-insensitive respiration (with added fructose) much lower than its pre-surgical level three days after eyestalk removal; remains low (but shows a gradual slight increase in level) up to 15 days after surgery; Krishnan, 1954 Homarus gammarus: Muscle; respiration (with added succinate) lower after eyestalk removal; Scheer, Schwabe, and Scheer, 1952

Palaemon squilla: Muscle; respiration (with added succinate) lower after eyestalk removal, in some cases higher again after addition of eyestalk extract; Scheer, Schwabe, and Scheer, 1952 Insecta Leucophaea maderae: Thoracic muscle; endogenous respiration of animals without corpora allata 1.2 times that of animals with corpora allata; Samuels, 1956

RESPIRATORY RATE FOLLOWING INJURY Arthropoda Insecta

Tachycines asynamorus: Muscles of hind femur; endogenous respiratory rate of cut muscles 1.4 times that of the intact muscles; Kubista, 1956 Section 4: DISCUSSION

In Section 2, data on tissue respiration in in- discuss the broader implications of certain stud- vertebrates are presented; in Section 3 some of ies presented here and suggest some conclusions these data plus others from the same investiga- regarding invertebrate tissue respiration that tions are analyzed. In the present section we may be drawn from them.

ENZYMES OF CITRIC ACID CYCLE

Respiratory activity of a tissue preparation, Without controls such as described above, or fraction thereof, when measured in the pres- one may not necessarily conclude that, because ence of added substrate, can be attributed solely a particular citric cycle substrate is metabol- to an enzyme acting on the added substrate only ized, only the enzyme acting specifically upon

if controls are included to indicate any incre- that substrate is being assayed. Other compo- ment of respiratory activity due to action of nents of the chain of enzymes may be concerned other enzymes on other substrates that may re- with the reaction, and the assay may be a meas- sult from oxidation of the original substrate. ure of their activity as well. For example, in order to determine the authentic Consequently in Section 2 we make no mention Q!-ketoglutaric dehydrogenase activity of insect of individual enzymes or enzyme systems. We in- sarcosomes, one should measure, as did Lewis dicate merely that a given assay measures endog- and Slater (1954), the respiratory rate of the enous respiration or, alternatively, respiration preparation first in the presence of Of-ketoglutar- in the presence of added substrate or substrates. ate and subsequently in the presence of a-keto- Although the data of Section 2 do not always glutarate plus malonate, the latter being a sub- justify a conclusion regarding the activity of any stance that inhibits succinic dehydrogenase. One particular enzyme of the citric acid cycle, never- may then attribute a difference in respiratory theless they clearly indicate that at least some rate to authentic a-ketoglutaric dehydrogenase enzymes of that cycle are present in the tissues activity (although one must still recognize the of invertebrates. possibility that, with malonate present, accumu- For other reviews dealing with this subject, lation of succinate may affect the rate at which see Krebs (1954), Gumbman, Brown, and Tappel a -ketoglutarate is oxidized). (1958), and Hammen and Osborne (1959).

CYTOCHROME SYSTEM

There is convincing evidence for the presence (1949). Cyanide sensitivity is usually taken to of cj^ochrome oxidase as the terminal oxidase indicate that cytochrome oxidase and certain in tissues of certain mollusks and arthropods other enzymes may be involved in the terminal (see data of Section 2; see also Shappirio and electron transport system. Except under unusual Williams, 1957a, 1957b: Tappel, 1960; Pablo and conditions (see pp. 82-83) cyanide insensitivity Tappel, 1961; Sacktor, 1961). The possibility is generally considered evidence for the non- that cytochrome oxidase may be part of the involvement of these enzymes. With cyanide as terminal electron transfer system of other in- a respiratory poison, Robbie recorded marked vertebrates, including some sponges and coe- inhibition of endogenous respiration in all in- lenterates, is suggested by the work of Robbie vertebrate tissues so treated, with the exception

81 82 TISSUE RESPIRATION IN INVERTEBRATES

of the subumbrella of the jellyfish (Cassiopea nematodes have a unique terminal electron trans- frondosa) and the branchial tree of the sea cu- port system (Bueding and Charms, 1952) re- cumber (Isostichopus badionotus) . Concentrations mains open to question. of cyanide employed by Robbie ranged from Because the respiration of the diapausing X 10-2 10-^ 1 to 1 X M. The fact that even the Cecropia moth is unaffected by cyanide and lower concentrations of cyanide were inhibitory carbon monoxide, Schneiderman and Williams suggests that the cyanide may have been acting (1954a, 1954b) postulated that a terminal oxidase on cytochrome oxidase. other than cytochrome oxidase functions during It should be added here parenthetically that pupal diapause. Subsequently, by use of low tem- cyanide is a less specific inhibitor of cytochrome perature spectroscopy (see Keilin and Hartree, oxidase than is azide. Furthermore, although 1949), which intensifies the absorption bands of both C3^ochrome oxidase and tyrosinase are in- the cytochromes 10- to 20-fold, Shappirio and hibited by carbon monoxide, the inhibition of Williams (1957a) observed that cytochrome oxi- cytochrome oxidase is reversible by light, dase is still present in diapausing Cecropia whereas the inhibition of tyrosinase is not. pupae. During their study, in which they care- Possibly the inhibition of endogenous respira- fully traced the activity of the enzymes of the tion produced by cyanide in Robbie's study was terminal electron transport system in wing due to an inhibition of catalase, peroxidase, or epithelium during a portion of the life cycle, tyrosinase. Such a possibility, however, is slight, Shappirio and Williams (1957b) found that the for the concentration of these enzymes in animal activity of cytochrome oxidase falls to low (but tissues is too low for them to be playing a major still detectable) levels during diapause and then role in respiration. The lower concentrations of rises during adult development. They also found cyanide that Robbie found to be effective (e.g., (1957a) that the concentration of this and other X 10-5 1 M) also rule out the possibility that the respiratory enzymes drops markedly during inhibition depended upon a reaction of this poison pupal diapause and then rises again during adult with carbonyl groups in keto acids of the citric development. Significantly, however, whereas acid cycle. during diapause the concentration of cytochrome Laser (1944) has found that cyanide can cause c is less than 5 per cent of its pre-diapause level, an increase in respiratory activity. When he that of cytochrome oxidase remains relatively added 0.01 M cyanide to muscle homogenates of high (20% of its non-diapause level). Ascaris lumbricoides containing methylene blue, Recently Harvey and Williams (1958a, 1958b) Laser noted an increase in the rate of respira- and Kurland and Schneiderman (1959) reinvesti- tion greater than that shown by homogenates con- gated the question of the terminal oxidase in taining methylene blue but lacking high concen- diapausing pupae. Respiration of the whole ani- trations of cyanide. Apparently cyanide can mal throughout diapause is relatively insensitive combine with oxaloacetate to form a complex to inhibition by carbon monoxide, azide, and that, unlike oxaloacetate itself, is incapable of cyanide. Nonetheless, Harvey (1956), Kurland competitively inhibiting succinic dehydrogenase. and Schneiderman (1959), and Harvey and Williams Neither cytochrome oxidase nor cytochrome c (1961) showed that injury-stimulated and dini- is enzymatically detectable in muscle homogen- trophenol-stimulated uptake of oxygen by dia- ates of the nematodes Ascaris lumbricoides and pausing pupae is indeed sensitive to carbon Litomosoides carinii, although a low level of monoxide. Furthermore, in their independent cytochrome c and cytochrome oxidase activity is investigations, Kurland and Schneiderman (1959), apparent in muscle homogenates of the trematode studying total uptake of oxygen, and Harvey and Schistosoma mansoni (Bueding and Charms, Williams (1958b), studying the heart beat of un- 1952). However, a pigment with the same absorp- injured diapausing pupae, demonstrated that at tion maxima as reduced cytochrome c has been low oxygen tensions the diapausing pupa is carbon demonstrated spectroscopically in tissues of monoxide sensitive. The manometric studies Parascaris equorum and A. lumbricoides were measurements of the total gas uptake in the (Keilin, 1925) and in those of A. lumbricoides at presence of either oxygen or oxygen and carbon the temperature of liquid air (Keilin and Hartree, monoxide mixtures. That diapausing pupae may 1949). Thus the conclusion that these parasitic consume carbon monoxide as well as oxygen has DISCUSSION 83 recently been shown by Harvey (1961), who found pausing pupae compared to the low concentra- that carbon monoxide can stimulate oxygen up- tions of cytochrome c (Shappirio and Williams, take (see also Kurland and Schneiderman, 1959) 1957a, 1957b). Thus, although a large portion of and that 5 per cent of the total gas consumed may the oxidase may be inhibited by a respiratory be carbon monoxide. poison, enough oxidase remains unbound to per- On the basis of their findings, these several mit the transfer of electrons from cytochrome workers have concluded that during pupal dia- c to molecular oxygen. Clearly the apparent pause in Cecropia (and also in three closely insensitivity of diapausing pupal respiration to related species of saturniid moths) cytochrome the inhibitors of cytochrome oxidase is not an oxidase does serve as the terminal oxidase. actual insensitivity. Provided that respiration They account for the fact that respiration of is stimulated or, alternatively, provided that the diapausing pupae at reasonable oxygen tensions oxygen tension is lowered sufficiently for the and when unstimulated by dinitrophenol or by concentration of uninhibited cytochrome oxidase injury is apparently carbon monoxide-, azide- to become rate-limiting, a sensitivity to carbon and cyanide-insensitive by pointing to the excess monoxide, azide, and cyanide during pupal dia- of cytochrome oxidase in most tissues of diapause can be demonstrated.

COMPARISON OF RESPIRATORY RATES OF VARIOUS TISSUES \^ Let us leave the subject of respiratory en- gut gland has a higher endogeneous metabolic zymes and their inhibitors at this point and dis- rate than has the gill. However, in certain active cuss certain other aspects of invertebrate tissue terrestrial and intertidal species, the gill ex- respiration that have been investigated in the hibits a greater respiratory activity (Kermack, papers cited in this volume. Among the most in- Lees, and Wood, 1954; Vernberg, 1956). teresting work is that which concerns the com- A comment concerning the particulate frac- parative respiratory rates of different tissues. tions assayed by Ghiretti-Magaldi, Giuditta, and In three investigations (Shapiro, 1937, on Lim- Ghiretti (1957) is advisable. In order to facilitate ulus Polyphemus ] Kerkut and Lave rack, 1957, on homogenization, these investigators chose to Helix pomatia; Ghiretti-Magaldi, Giuditta, and freeze the tough muscles from the mantle and Ghiretti, 1958, on Octopus vulgaris) ganglionic tentacles of Octoptis vulgaris before fractionat- tissue proved to have the greatest endogenous ing them. In later work on Octopus (Ghiretti- respiratory activity. In general, ganglionic tis- Magaldi, Giuditta, and Ghiretti, 1958), they again sue respires most rapidly, foot or leg muscle used frozen muscle tissue for their preparations. most slowly, and various other tissues at inter- In still later studies on Aplysia, the sea hare mediate rates (Chapheau, 1932; Shapiro, 1937; (Ghiretti, Ghiretti-Magaldi, and Tosi, 1959), Hopkins, 1946; Kawai, 1957; Kerkut and Laverack, frozen buccal mass muscle, frozen midgut gland, 1957; Ghiretti-Magaldi, Giuditta, and Ghiretti, and frozen gizzard muscle were employed in the 1958; Higashi and Kawai, 1959; Kawai, 1959). preparation of slices and particles. Since freez- Among insects, flight muscles have consistently ing disrupts both cells and intracellular organ- higher endogenous respiratory rates than have elles of most tissues, the particulate material leg muscles (Perez-Gonzalez and Edwards, used in these investigations may well have been 1954). In most brachyuran crustaceans the mid- fragmented.

SEX DIFFERENCES IN RESPIRATORY RATE

The results of studies dealing in part with sex ceans, the respiratory rate of both midgut gland differences in respiratory rate present no clear and gill is higher in the female than in the male; picture. In some species of brachyuran crusta- in other species the reverse is true; in still .

84 TISSUE RESPIRATION IN INVERTEBRATES

other species the respiratory rate of the midgut ards, 1954; Perez-Gonzalez and Edwards; 1954; gland is higher in the male while that of the gill Sacktorand Thomas, 1955; Kubista, 1956; Young, is higher in the female (Vernberg, 1956; Belding, 1958). In several other species of insects, how- Field, Weymouth, and Allen, 1942). ever, tissues of the female have a higher respir- Among insects, the cockroach {Periplaneta atory rate than have those of the male (Graham, americana) exhibits a certain consistency as 1946; Allen and Richards, 1954), Furthermore, regards sex differences in the respiratory rate Samuels (1956) found that the endogenous respir- of its various tissues. With the exception of the ation of teased thoracic muscle is approximately foregut, all tissues in the male cockroach re- equal in both sexes of the Madeira cockroach spire at a higher rate than do those in the female {Leucophaea maderae) (Barron and Tahmisian, 1948; Allen and Rich-

VARIATION IN RESPIRATORY RATE WITH AGE

Studies on the variation in endogeneous respir- What effect aging may have on the respiratory atory rate with age have been carried out on three rate of arthropods is not easy to evaluate. The species of pelecypod mollusks, namely, the oys- level of respiratory metabolism in crustaceans ters Crassostrea virginica (Hopkins, 1930) and and insects depends so completely upon the stage Gryphaea angulata (Chapheau, 1932), and the qua- of an animal in the molt cycle or life cycle that hog Mercenaria mercenaria (Hopkins, 1930, 1946). its relation to the animal's chronological age is In each of these species the respiratory rate was often obscure. found generally to decline with advancing age.

VARIATION IN RESPIRATORY RATE DURING CRUSTACEAN MOLT CYCLE

Increase in size in arthropods is discontinuous during the intermolt period. In a second study. and periodic. It occurs only at the time of ecdy- Skinner (MS) traced changes in endogenous sis when the old exoskeleton is cast off, to ex- respiration shown by integumentary tissues of pose the new soft one underneath. Through uptake the land crab (Gecarcinus lateralis) . Oxygen up- of water, as in some crustaceans, or uptake of take is highest during the period just preceding air, as in some crustaceans and insects, the ecdysis, being 1.6 times that recorded during soft new exoskeleton is rapidly enlarged to the intermolt period. The apparent contradiction greater dimensions before it becomes hardened between these two sets of results can be ex- by tanning and, in the case of crustaceans, cal- plained as follows: metabolism of muscle can be cification. Growth (i.e., increase in the amount expected to be maximal during the non-growth, of body tissue), although a more extended proc- intermolt stage when the animal is active, while ess than is increase in size, nevertheless is the metabolism of integumentary tissues pre- timed to coincide with other preparations for sumably will be highest during the premolt ecdysis and with subsequent post-ecdysial period when these tissues are synthesizing the events. new exoskeleton. Two studies involving the respiration of crusta- To induce pre-ecdysial changes, ecdysis, and cean tissues during the molt cycle are cited in (if the animal survives) post-ecdysial altera- Section 2. In the first (Krishnan, 1954), the tions in a decapod crustacean, one need only cyanide-insensitive respiration (with added remove both eyestalks, for in these structures fructose) of muscle from the green crab (Car- are certain neurosecretory cells (X organ cells) cinus maenas) proved to be lowest during the that synthesize and release a neurohormone period just preceding ecdysis; the rate of respir- capable of inhibiting molting. Before its release, ation rose during the soft-shelled stage immedi- the molt-inhibiting hormone is stored within the ately following ecdysis and reached a maximum eyestalks in the sinus glands, which consist of DISCUSSION 85 swollen endings of neurosecretory cells that crab (Carcinus maenas), the lobster (Homarus synthesize the hormone. gammarus), and the shrimp (Palaemon squilla) Krishnan (1954) has studied the effects of eye- respire at a lower rate than do homogenates of stalk removal on the rate of tissue respiration. muscle from unoperated individuals, and that Three days after performing this operation on the rate increases after the addition of eyestalk Carcinus maenas, he found the respiratory rate extract to the homogenates. However, the data of muscle from animals without eyestalks to be submitted by these authors show that the effects decidedly lower than that of muscle from unoper- are rather small and quite variable. Further- ated crabs. Krishnan noted, nevertheless, that more, their data indicate that the addition of when all his data were plotted, the resulting eyestalk extracts to homogenates of muscle curves for the two groups of animals were simi- from Palaemon squilla in some cases increases lar. They differed mainly in that the curve for and in others decreases the respiratory rate. unoperated crabs was displaced to the right of As noted above, crustaceans and their excised the curve for operated crabs by a distance tissues respire at different rates according to representing six days. In other words, compara- stage in the molt cycle. Variability in results, ble decreases (and subsequent increases) in therefore, may be related to stage. Schwabe, respiratory rate of muscle occur in operated Scheer, and Scheer (1952) consider that synthe- and unoperated animals, although in the latter sis of the new exoskeleton begins during the late only after a lag of six days. Krishnan did not intermolt period, that is, in late stage C. This offer an explanation of these observations. The concept does not agree with that of Drach (1939), levels may be related to the stage of the animals according to whom the synthesis of a new exo- in their molt cycle. If the unoperated crabs were skeleton begins during the early premolt period, gradually approaching molt, the respiratory rate that is, in early stage D. If Drach's criteria, of their muscle would reflect this and would which are accepted by the majority of workers yield a curve resembling that of premolt crabs (see Renaud, 1949; Travis, 1955; Charniaux- without eyestalks. Because eyestalk removal Cotton, 1957; Skinner, 1958, [MS]; Passano, accelerates molt-preparatory processes, how- 1960), are valid, the variability in the results of ever, the two curves would remain separated in Scheer, Schwabe, and Scheer (1952) may be time. attributed to the fact that some of their animals

It may be noted that Bliss (1953), working were in the intermolt stage and some were in the with whole specimens of Gecarcinus lateralis, premolt stage. found the respiratory rate to be high immediately For several species of crustaceans, Kuntz after eyestalk removal and to remain high (1946) noted that low concentrations of sinus throughout the entire period preceding ecdysis. gland extract increased the rate of reduction of Thus a difference exists between the respira- methylene blue by midgut gland and that high tory rates of animals without eyestalks and of concentrations decreased the rate. A more com- their isolated tissues during the premolt period. plete report of this work has not appeared. As mentioned above, a molt-inhibiting hor- In a series of experiments on Carcinus more occurs in the eyestalks of crustaceans. In maenas (Skinner and Bliss, unpublished data), the preparation of an extract, the eyestalks are we found that homogenates of midgut gland con- homogenized, boiled, and centrifuged, and then taining extracts of one to five sinus glands re- the supernatant is removed for use. In this way, duced methylene blue at essentially equivalent an investigator obtains a protein-free extract, rates. On the other hand, homogenates that con- the chemical composition of which is in other tain leg muscle equal in wet weight to two sinus respects unknown. glands carry out this reduction one and one-half Several workers have attempted to demon- times faster. strate a direct effect of crustacean molt-inhibit- The variability of results in experiments of ing hormone on tissue respiration by the addi- this kind emphasizes the need for the use of tion of such eyestalk extracts to homogenates. (1) more highly purified hormonal preparations, Scheer, Schwabe, and Scheer (1952) have re- and (2) more definitive systems, such as those ported that, in general, homogenates of mus- containing isolated mitochondria or submito- cle from eyestalkless individuals of the green chondrial particles. 86 TISSUE RESPIRATION IN INVERTEBRATES

VARIATION IN RESPIRATORY RATE DURING INSECT LIFE CYCLE

Just as the respiratory metabolism of crus- Allen and Richards (1954) in the leg muscle taceans is correlated closely with the stage of of young (10- to 20-day) adults when compared the animal in the intermolt cycle, so the res- with older (95- to 185-day) adults. Lewis and piratory rate of an insect varies with the phase Slater (1954) and Slater and Lewis (1954) found of the insect in its life cycle (see also pp. 82-83). that the activity of the a-ketoglutaric oxidase Brooks (1957) reported the respiratory activity of system in the flight muscle from adults of the the cockroach (Periplaneta americana) to be low bluebottle fly (Calliphora erythrocepliala) was in pink muscles of the leg and wing from nymphs, relatively high right after adult emergence, higher in those of adults just after emergence, lower from the eighth to the tenth day, and high and still higher in those of older adults. On the again from the fifteenth to the seventeenth other hand, no clear difference was detected by day.

RESPIRATORY RATE FOLLOWING INJURY

Kubista (1956) reported that the endogenous tissues of a diapausing pupa, one must exercise respiratory rate shown by isolated muscle of caution, for injury alone can increase the meta- a cut femur in the stone cricket (Tachycines bolic rate both of the pupa (whole or subdivided) asynamorus) was 1.4 times that shown by muscle and of its isolated tissues (see Schneiderman and of an uncut femur. Williams, 1953; Harvey, 1956, 1961, MS a; When making respiratory measurements on Shappirio, 1960).

EFFECT OF ENVIRONMENT ON RESPIRATORY RATE

With regard to the magnitude of the respira- respiratory rate have revealed a general rise tory rate at various seasons, it appears that with increasing dilution, as in the gill and endogenous oxygen uptake is greater in certain mantle of the quahog Mercenaria mercenaria tissues of pelecypod mollusks found in the (Hopkins, 1949) and the gill of the green crab North Temperate Zone during the winter and Carcinus rnaenas (Pieh, 1936), or a fall, as in early spring than at other times during the year the adductor muscle of M. mercenaria (Hop- (Hopkins, 1946; Kawai, 1957). Two investiga- kins, 1949). tions concerned with the effects of salinity on

EFFECT OF VARIOUS IONS ON RESPIRATORY RATE

Increasing concentrations of the potassium Arvanitaki, 1950). With the claw nerve of the

(K"*") ion induce a rise in endogenous respira- spider crab (Libinia emarginata) there is a rise tion in the heart of Helix aspersa, the dented in endogenous respiratory rate with increasing garden snail, and Mytilus galloprovincialis , a concentrations of K"*" ion up to a maximum of mussel, as well as in the nerve of Sepia offici- 40 mM per liter, then as a sharp drop (Shanes nalis, the cuttlefish (Cardot, Faure, and and Hopkins, 1948).

GRADIENTS IN RESPIRATORY RATE

In the brandling or manure worm (Eisenia against distance from the head, a U-shaped foetida) the respiratory rate varies along the curve with maxima at head and tail results. A

length of the worm. If one plots respiratory rate similar U-shaped curve of succinoxidase activ- ,

DISCUSSION 87

ity occurs along the length of the blue worm, at 16° C). The axon of Limulus shows most of Octolasium cyaneum (O'Brien, 1957). Guttman the activity when compared with the sheath. (1935) and Shapiro (1937) recorded inverted, Lastly, Kubista (1956) found a decrease in the U-shaped curves in respiratory rate along the rate of oxygen uptake along the thorax of the

length of the optic nerve of Limulus polyphemus cockroach {Periplaneta americana) , with a rise the horseshoe crab, at 28° C. to 31° C. (but not again in the region of the abdomen.

Section 5: ABBREVIATIONS AND SYMBOLS

ABBREVIATIONS

For the most part, the abbreviations listed below are identical with those given in Webster's New International Dictionary, second edition, unabridged, 1958. ca., circa ml., milliliter, milliliters cm., centimeter, centimeters mo., month, months cm.^, square centimeter or centimeters moL, mole, moles da., day, days no., number equiv., equivalent O.D., optical density exp., experiment R.Q., respiratory quotient f.p., freezing point S, salinity g., gram, grams sci. name, scientific name hr., hour, hours s.g., specific gravity log, logarithm sp., species (singular) not indicated by author max., maximum spp., species (plural) not indicated by author mg., milligram, milligrams temp., temperature

\xg., microgram, micrograms wks., weeks

\x\., microliter, microliters wt., weight min., minute, minutes yrs., years

SYMBOLS

CHEMICAL SYMBOLS AND FORMULAS

ADP, adenosine diphosphate IC*", potassium ion ATP, adenosine triphosphate KCl, potassium chloride Ca"*"^, calcium ion KCN, potassium cyanide CaCl2, calcium chloride M, molar concentration; molarity; molar CO, carbon monoxide mM, millimol, millimols CyFe"^^, ferrocj^ochrome c (reduced cytochrome Mg"""^, magnesium ion c) MgCl2, magnesium chloride CyFe"^"'"'', ferricjd;ochrome c (oxidized cytochrome N, nitrogen (element) N2, nitrogen (gas)

DDT, dichlorodiphenyltrichloroethane Na"*", sodium ion DNP, 2, 4-dinitrophenol NaCl, sodium chloride DPN or DPN^, oxidized diphosphopyridine Na"'"/K^, ratio of sodium ions to potassium ions nucleotide O2, oxygen (gas) DPNH, reduced diphosphopyridine nucleotide P/O, ratio of phosphate formed to oxygen EDTA, ethylenediaminetetraacetic acid(versene) utilized; referred to as the P/O ratio HCN, hydrocyanic acid TPN, triphosphopyridine nucleotide H2O2, hydrogen peroxide TPNH, reduced triphosphopyridine nucleotide

89 90 TISSUE RESPIRATION IN INVERTEBRATES

MISCELLANEOUS SYMBOLS w5 cf, male 10-^ 1/100,000 or 0.00001

$ , female >, more than a., alpha <, less than

A, delta /, per M, micron %o, parts per thousand m/j, mlllimicro- (prefix) t, time (mg.N)"^ 1/mg.N V g, times the acceleration of gravity p, para ° C, degrees Centigrade Section 6: GLOSSARY

absorbancy: Sjoionymous with optical density; sion of hydrogen peroxide to water and mole- equal to -logio T. where T^transmittancy; cular oxygen. molar absorbancy index or extinction coeffi- citric acid cycle: Another name for tricarboxy- cient is the absorbancy of a 1-molar solution lic acid cycle or Krebs cycle; the primary through a 1-cm. light path. mechanism by which the aerobic oxidation of accessory glands: In insects and other inverte- metabolic intermediates to carbon dioxide and brates; secretory organs associated with re- water takes place. productive function. clitellate: Indicative of the fact that an annelid, adductor muscle: In bivalve mollusks, a muscle such as an earthworm or a leech, is sexually that closes the valves of the shell. mature and bears a clitellum. albuminous or albumen gland: In the higher clitellum: A glandular thickened region that gastropod mollusks; a part of the female re- secretes a capsule for eggs and may assist in

productive system, it secretes an albuminous attachment during copulation. material around the egg before the shell is collagenous: Pertaining to collagen, a protein added. The albuminous material serves as that is found in large amounts in connective food for the developing embryo. tissue. antimycin A: An antibiotic isolated from Strep- columella muscle: In gastropod mollusks; is tomyces spp.; inhibits the oxidation of suc- attached to the columella (central column) cinate at the level of the Slater factor. and serves to retract the body of the animal ascorbate: The salt of ascorbic acid; a reduc- into the shell. ing agent used to reduce cytochrome c. corpora allata: In insects; glands that secrete axoplasm: The cytoplasm of a nerve fiber. a hormone (juvenile hormone) capable of pre- Barcroft respirometer: A differential respirom- venting metamorphosis while permitting eter consisting of two flasks connected to a larval molting; also involved in the control manometer. In this closed system one flask of reproduction. serves as a thermobarometer; the other, as coxal muscles: In insects, crustaceans, and a tissue chamber. As the tissue consumes other arthropods; muscles of the coxa, which oxygen and produces carbon dioxide, which is is the first segment of a leg and which effects absorbed by alkali, both volume and pressure the articulation of the leg with the body. in the respiration chamber change. The differ- cytochrome c: A heme protein, the position of ence in pressure between the two flasks is which in the terminal electron transport chain

measured on the column of the manometer. is such that it may be reduced from the ferric brachyuran: Pertaining to the true crabs or (Fe+++) to the ferrous (Fe"*"*") form by cyto- Brachyura. chrome Cj, cj^ochrome b, flavoproteins, or branchial or respiratory tree: In sea cucumbers certain added reducing agents; also may be (Echinodermata), consists of two long, branch- oxidized by cj^ochrome oxidase or by certain ing tubes that arise from the cloaca and ter- added oxidizing agents.

minate blindly in the anterior portion of the cj^ochrome oxidase (cytochrome (23): A heme body cavity; functions in respiration and ex- protein that oxidizes cytochrome c and reduces cretion. molecular oxygen; its activity is inhibited by buccal mass: In mollusks, exclusive of bivalves; cyanide, azide, and carbon monoxide, the in- a more or less compact mass of muscles and hibition by carbon monoxide being light re- cartilage that supports and operates the radula. versible. catalase: An enzyme that catalyzes the conver- cytochrome system: A group of respiratory

91 . .

92 TISSUE RESPIRATION IN INVERTEBRATES

enzymes of primary importance in cellular membrane-bound cavities; some of the mem- respiration. The members of the chain are branes have small granules (ribonucleopro- thought to be aligned as follows: tein particles) attached to them, so that these membranes may appear rough-surfaced.

succinate ethylenediaminetetraacetlc acid (EDTA): Or

i versene; a complexing agent used to chelate DPNH-^flavoproteins-^cytochrome b—* cytochrome c—»cytochrome a-^cytochrome oxidase divalent metals and so effectively remove them from solution. hydroquinone (or) ascorbic acid (or) extinction coefficient: See absorbancy. /)-phenylenediamine. eyestalk extract: The supernatant obtained when dart sac: Found in one superfamily of land eyestalks of a decapod crustacean are homog- snails, the Helicacea; consists of a muscular enized, boiled, and centrifuged. caecum arising from the vagina and contains fat body: In insects, a tissue that fills the body a fine-pointed calcareous shaft. The shaft is cavity and contains large amounts of fat, pro- exchanged by the hermaphroditic partners tein, and glycogen. during courtship and serves as a releaser femur: The third (counting distad) and often the stimulus for courtship behavior. broadest segment of the leg of an insect. In dehydrogenases: Enzymes that are generally the metathoracic leg, the femur may be con- DPN- or TPN-linked and that catalyze the siderably enlarged to contain the muscles oxidation of certain metabolites. Neither used in jumping (as in a grasshopper or DPN nor TPN, however, is required by suc- cricket) cinic dehydrogenase, which transfers elec- Fenn respirometer: A type of differential trons to the cytochrome chain directly. respirometer; consists of two vessels con- dialysis: A method for the separation of large nected by a horizontal capillary tube contain- molecules from small by means of their un- ing an oil drop. As volume or pressure changes equal rates of diffusion through natural or within the respiration chamber, the oil drop sjmthetic membranes. moves. diapause: The condition of arrested growth, de- flavoproteins: A group of conjugated proteins velopment, or reproductive activity that occurs of primary importance in the electron trans- at a given stage in the life cycle of many arth- port system. ropods, notably certain hemimetabolous and fluorescence: The light emitted by a molecule holometabolous insects. as a result of absorption of radiation from an differential manometer: See Barer oft, Fenn, external source; persists only during irradia- and Thunberg respirometers. tion; is of longer wave length than is the in- digestive diverticula: See midgut gland. cident light. 2, 4-dinitrophenol (DNP): Dissociates or un- giant axon: A t3^e of nerve fiber of exception- couples ATP synthesis from aerobic respira- ally large diameter; found in lower verte- tion. brates and in certain invertebrates, including diphosphopyridine nucleotide (DPN): Or coen- annelids, crustaceans, insects, and cephalopod

zyme I; a hydrogen acceptor that is reduced mollusks; permits rapid conduction of nerve by a variety of substrates in the presence of impulses.

specific dehydrogenases; in turn, it reduces gizzard: In Aplysia and other Aplysiomorpha

a flavoprotein. (opisthobranchiate mollusks) , most of which ecdysls: In arthropods, the act of shedding or feed by cropping live seaweeds with paired casting the exoskeleton (shell). jaws and radula. The gizzard has two cham- electron transport system: See cytochrome bers, an anterior one for masticating and a system. posterior one with delicate teeth for straining. endogenous respiration: Respiration without hemimetabolous: Refers to an insect that under- added substrate. goes incomplete metamorphosis (egg — endoplasmic reticulum: An intracellular cj^o- nymph —»adult) plasmic system consisting of tubules and hepatopancreas: See midgut gland. vesicles that form a continuous network of holometabolous: Refers to an insect that under- >

GLOSSARY 93

goes complete metamorphosis (egg —» larva — oxidative phosphorylation: The process by pupa —»adult). which adenosine diphosphate (A DP) and inor- homogenate: Ideally, a cell-free suspension ob- ganic orthophosphate are converted to the tained by grinding tissues in such a way that high-energy compound adenosinetriphosphate cell structure is destroyed. (ATP); energy for this conversion is derived hydroqulnone: A reducing agent used to reduce from the transport of electrons through the cytochrome c. terminal electron transport system. Krebs cycle: See citric acid cycle. pallial: Refers to the mantle, especially of a larva: Immature, wingless, generally worm- moUusk. like form into which holometabolous insects particulate fraction: Any of several fractions hatch from the egg and in which they remain that are usually obtained from a tissue homog- until they change into pupae. enate by differential centrifugation. liver: See midgut gland. pedal retractor: In mollusks, a muscle that re- malonate: The salt of malonic acid; a dicarbox- tracts the foot. ylic acid that competitively inhibits the oxida- perienteric: Refers to the cavity that surrounds tion of succinic acid. the digestive tract. Malpighian tubules: Tubular organs opening /)-phenylenediamine: A reducing agent used to into the midgut or hindgut of insects; gener- reduce cytochrome c. ally believed to be excretory in function. P/0 ratio: Ratio of inorganic phosphate esteri- mantle: In mollusks, the fold of the body wall fied (to ATP) to the oxygen consumed during which, in shell-bearing forms, lines and the aerobic oxidation of a metabolite; denotes secretes the shell. the efficiency of utilization of energy made microsomes: An operational term referring to available by the transfer of electrons through the fraction obtained when homogenates freed the electron transport system. of large particulate matter are centrifuged polarograph: An instrument used in polarog- at high centrifugal forces; the fraction ob- raphy, which is concerned with oxidation- tained is composed essentially of fragments reduction reactions at an electrode. If poten- of ruptured endoplasmic reticulum (see defi- tials are measured while known currents are nition) and its attached particles. flowing through the cell, and these two param- midgut gland: Name preferred by many inver- eters are plotted against each other, a curve tebrate zoologists for the digestive gland of is obtained from which the character and con- mollusks and crustaceans; in mollusks, some- centration of a given material can be ascer- times called hepatopancreas, digestive diver- tained. ticula, or liver; in crustaceans, often called pupa: The intermediate, quiescent form as- hepatopancreas or liver. sumed by holometabolous insects following mitochondria: Intracellular particles (average the larval stage, or stages, and prior to the diameter, 1^) containing the enzymes and co- adult stage. enzymes that comprise the electron trans- quinol: See hydroqulnone. port system; involved in oxidative phosphory- radula: A chitinous, tooth-bearing ribbon used lation, and citric and fatty acid oxidations; by mollusks, exclusive of bivalves, for rasping can be collected in a relatively homogeneous food into minute particles. fraction by centrifugation (at 5000 x ^) of a respiratory quotient: Ratio of the volume of homogenate from which nuclei and cellular carbon dioxide produced to the volume of ox- debris have been removed by a low-speed ygen consumed during respiration. centrifugation. retractor muscle of foot: See pedal retractor. molt: A term frequently used, as in this volume, sarcosomes: Mitochondria of muscle. to indicate the growth processes undergone Slater factor: A component of the electron trans- by arthropods both before and after ecdysis, port chain operative between cytochrome b as well as during ecdysis. and cytochrome c; inhibited by antimycin A. nymph: Immature stage into which hemimetab- spectrophotometer: An instrument for the quan- olous insects hatch from the egg. titative measurement of the transmission of optical density: See absorbancy. light of a given wave length through a solution. 94 TISSUE RESPIRATION IN INVERTEBRATES

the transmission of the solvent being set at enzyme II; a hydrogen acceptor which is re- unity or at 100 per cent. duced by a variety of substrates in the pres- stellar nerve (see Connelly, 1952): In cepha- ence of specific dehydrogenases; in turn, it lopod mollusks; this term presumably re- reduces a flavoprotein. fers to the large nerve trunks that run from umbrella: The gelatinous bell-shaped or disk- the brain to each stellate ganglion; these shaped structure that comprises the greater nerve trunks are usually called the mantle or part of the body of a jellyfish. pallial nerves. volumeter: A closed-system, constant-pressure subumbrella: In jellyfishes; the concave or oral respirometer with two flasks connected by a surface of the umbrella (see definition). manometer and with an additional calibrated succinoxidase system: An enzyme system that arm permitting direct measurement of changes includes succinic dehydrogenase and part of in volume that result from respiration in one the electron transport system; catalyzes the flask; the second flask serves as a thermo- oxidation of succinate to fumarate and trans- barometer. fers the electrons so removed to oxygen via a Warburg respirometer: A single-flask, constant- portion of the terminal electron transport volume manometer in which the consumption system. of oxygen is measured as a function of a Thunberg respirometer: A type of differential change in pressure. respirometer. Winkler method: A chemical method for the tricarboxylic acid cycle: See citric acid cycle. determination of dissolved oxygen based on triphosphopyridine nucleotide (TPN): Or co- the oxidation of manganese. Section 7: GUIDE TO LITERATURE

Popular, semi-popular, and semi-technical references are indicated by an asterisk.

BIOCHEMISTRY: GENERAL REFERENCES Kleinholz (1957) Knowles and Carlisle (1956) Baldwin (1957) Passano (1960) Fruton and Simmonds (1958) Long, King, and Sperry (1961) CRUSTACEANS: GENERAL BIOLOGY (See also under Invertebrates) CELL FRACTIONS Balss (1940-1957) Allfrey (1959) Korschelt (1944) De Robertis, Nowinski, and Saez (1960) Duve (1957) CRUSTACEANS: HORMONES Green and Jarnefelt (1959)* (See also under Invertebrates) Hogeboom, Kuff, and Schneider (1957) Carlisle and Knowles (1959) Lehninger (1951) Kleinholz (1957) Novikoff (1957, 1959, 1961) Knowles and Carlisle (1956) Palade (1958) Koller (1960) Siekevitz (1957)* CRUSTACEANS: NEUROENDOCRINE SYSTEMS CELL STRUCTURE (See also under Invertebrates) (See also under Subcellular Morphology) Bliss (1956, 1959, 1960) De Robertis, Nowinski, and Saez (1960) Carlisle and Knowles (1959) Mercer (1961) Kleinholz (1957) Siekevitz (1957)* Knowles (1959) Wilson (1925) Knowles and Carlisle (1956) Zamecnik (1958)* Koller (1960) Passano (1960) CITRIC ACID CYCLE Scheer (1960) Baldwin (1957) Turner (1960) Colowick and Kaplan, vol. 1 (1955), vol. 3 (1957) Welsh (1955, 1961a) Cross, Taggart, Covo, and Green (1949) Green (1949, 1954, 1958*) 1951, 1957, CRUSTACEANS: PHYSIOLOGY Gumbman, Brown, and Tappel (1958) Hammen and Osborne (1959) Buddenbrock (1945-1954) Hogeboom, Kuff, and Schneider (1957) Waterman (1960-1961) Krebs (1954) Lehninger (1951, I960*) CYTOCHROMES Long, King, and Sperry (1961) Baldwin (1957) Chance and Williams (1956) CRUSTACEANS: CONTROL OF MOLTING Cooperstein and Lazarow (1951) Arvy, Gabe, and Scharrer (1956) De Robertis, Nowinski, and Saez (1960) Bliss (1956, 1959, 1960) Green (1958)* Carlisle and Knowles (1959) Green and Hatefi (1961)

95 96 TISSUE RESPIRATION IN INVERTEBRATES

Horecker and Stannard (1948) Lehninger (1951, 1961*) Keilin (1925) Long, King, and Sperry (1961) Keilin and Slater (1953) Schneider and Potter (1943) Lehninger (I960,* 1961*) Long, King, and Sperry (1961) INHIBITORS, METABOLIC LundegSrdh (1959) Morrison (1961) General Considerations Pablo and Tappel (1961) Sacktor (1961) Sizer (1957) Schneider and Potter (1943) Shappirio and Williams (1957a) Antimycin A Stannard and Horecker (1948) Potter and Reif (1952) Tappel (1960) Reif and Potter (1953) ELECTRON MICROSCOPY Azide Bargmann, Peters, and Wolpers (1960) Horecker and Stannard (1948) Bessis (I960)* Stannard and Horecker (1948) Clark (1961) Colowick and Kaplan, vol. 4 (1957) Carbon Monoxide De Robertis, Nowinski, and Saez (1960) Novikoff (1957) Lilienthal (1950) Palade (1956, 1958) Selby (1959) Cyanide Sjostrand (1957) Horecker and Stannard (1948) ELECTRON TRANSPORT SYSTEM Robbie (1948, 1949) Stannard and Horecker (1948) Chance and Williams (1956) Green (1954, 1957, 1958,* 1959) 2, 4-Dinitrophenol (DNP) Green and Hatefi (1961) Chance and Williams (1956) Green and Jarnefelt (1959)* Cross, Taggart, Covo, and Green (1949) Lehninger (I960,* 1961*) Green (1951) Long, King, and Sperry (1961) Loomis and Lipmann (1948) Potter and Re if (1952) Slater and Lewis (1954) ENZYMES: GENERAL CONSIDERATIONS INSECTS: CONTROL OF Baldwin (1957) GROWTH AND METAMORPHOSIS Boyer, Lardy, and Myrback (1959) De Robertis, Nowinski, and Saez (1960) Arvy, Gabe, and Scharrer (1956) Dixon and Webb (1958) Harvey (MS a) Duve (1957) Lees (1955) Frieden (1959)* Raabe (1959) Green (1949, 1957) Schneiderman and Gilbert (1959) Green and Jarnefelt (1959)* Turner (1960) Sumner and Myrback (1950-1952) Wigglesworth (1954, 1957, 1959*) Williams (1958)* ENZYMES, RESPIRATORY

Baldwin (1949,* 1957) INSECTS: GENERAL BIOLOGY Chance and Williams (1956) (See also under Invertebrates) Colowick and Kaplan, vol. 2 (1955) Cooperstein, Lazarow, and Kurfess (1950) Richards and Davies (1957) GUIDE TO LITERATURE 97

INSECTS: HORMONES Cadart (1957)* (See also under Invertebrates) Cambridge Natural History (see Harmer and Shipley, 1895-1909) Karlson (1956) Carter (1940) Raabe (1959) earthy (1958) Schneiderman and Gilbert (1959) Crowder (1931)* Wigglesworth (1954, 1957, 1959*) Galtsoff, Lutz, Welch, and Needham (1937)* Williams (1958)* Grasse (1948-1960) Harmer and Shipley (1895-1909)* INSECTS: NEUROENDOCRINE SYSTEMS Hyman (1940-1959) (See also under Invertebrates) Kiikenthal and Krumbach (1923-1938) Bargmann, Hanstrom, Scharrer, and Scharrer Lankester (1900-1909)* (1958) MacGinitie and MacGinitie (1949)* Koller (1960) Morton (1958)* Raabe (1959) Pennak (1953) Scharrer, B. (1959) Ricketts and Calvin (1952)* Scheer (1960) Sedgwick (1898-1909) Turner (1960) Smith, Petelka, Abbott, and Weesner (1954) Welsh (1955) Traite de Zoologie (see Grasse) Wigglesworth (1957) Ward and Whipple (1959) Wilson (1947,* 1951*) INSECTS: PHYSIOLOGY Yonge (1949)*

Roeder (1953) Wigglesworth (1951) INVERTEBRATES: HORMONES (See also under Crustaceans and Insects) INTERMEDIARY METABOLISM Arvy, Gabe, and Scharrer (1956) (See also under Enzymes: Kleinholz (19 57) General Considerations) Koller (1960) Baldwin (1957) Scharrer and Scharrer (1954a, 1954b) Dickens (1959) Krebs (1953) INVERTEBRATES: Prosser and Brown (1961) NEUROENDOCRINE SYSTEMS Sallach and McGilvery (1960) (See also under Crustaceans and Insects)

INVERTEBRATES: BOOKS WITH Bargmann, Hanstrom, Scharrer, and Scharrer ANNOTATED BIBLIOGRAPHIES (1958) Gabe (19 54) Borradaile, Potts, Eastham, and Saunders Koller (1960) (1958)* Naisse (1959) Brown (1950) Schneiderman and Gilbert (1959) Crowder (1931)* Stazione Zoologica di Napoli (1954) Roeder (1953) Welsh (1959, 1961b) Smith, Pitelka, Abbott, and Weesner (1954) INVERTEBRATES: PHYSIOLOGY INVERTEBRATES: GENERAL BIOLOGY Buddenbrock (1950-1961) Borradaile, Potts, Eastham, and Saunders Galtsoff (1961) (1958)* Nicol (1960) Bronn (1880-1961) Prosser and Brown (1961) Brown (1950) Scheer (1948) Buchsbaum and Milne (I960)* Scheer, Bullock, Kleinholz, and Martin (1957) 98 TISSUE RESPIRATION IN INVERTEBRATES

Van der Kloot (MS) Micro-Winkler Method

Barth (1942) METHODS Dam (1935) Fox and Wingfield (1938) Determination of Respiratory Rate: General Treatment Preparation of Tissues De Robertis, Nowinski, and Saez (1960) General Dixon (1951) Baldwin (1957) Umbreit, Burris, and Stauffer (1957)

Determination of Respiratory Rate: Differential Centrifugatiofi Special Techniques Allfrey (1959) Claude (1946a, 1946b) Barcroft Respirometer Duve (1957)

Dixon (1951) Hogeboom, Kuff, and Schneider (1957) Novikoff (1959) Umbreit, Burris, and Stauffer (1957) Schneider (1946) Fenn Respirometer Siekevitz (1957) Umbreit, Burris, and Stauffer (1957) Dixon (1951)

Density Gradient Centrifugation Polarograph Allfrey (1959) Barker and Miner (1961) Hogeboom, Kuff, and Schneider (1957) Umbreit, Burris, and Stauffer (1957) Homogenate Technique Spectrophotometer Allfrey (1959) Bayliss (1959) Umbreit, Burris, and Stauffer (1957) Chance (1954) Colowick and Kaplan, vol. 4 (1957) Isolation of Particulate Components Drabkin (1950) Allfrey Lundegardh (1959) (1959) Umbreit, Burris, and Umbreit, Burris, and Stauffer (1957) Stauffer (1957)

Thunberg Respirometer Slicing

Thunberg (1905) Deutsch (1936) Field (1948) Stadie and Riggs Volumetric Microrespirometer (Volumeter) (1944) Warburg (1931) So ho lander (1942) Scholander, Claff, Andrews, and Wallach (1952) Ultracentrifugation Wennesland (1951) Colowick and Kaplan, vol. 4 (1957) Warburg Respirometer

De Robertis, Nowinski, and Saez (1960) MICROSOMES Dixon (19 51) Allfrey and Mirsky (1961)* Umbreit, Burris, and Stauffer (1957) De Robertis, Nowinski, and Saez (1954) Warburg (1931) Hogeboom, Kuff, and Schneider (1957) Novikoff (1959) Winkler Method Pa lade (1956, 1958) Zamecnik (1958)* American Public Health Association (1955) GUroE TO LITERATURE 99

MITOCHONDRIA Green (1951, 1954, 1958*) Green and Hatefi (1961) Bessis (I960)* Green and Jarnefelt (1959)* Brachet (1957) Keilinand Slater (1953) Chance and Williams (1956) Krebs (1953, 1954) Colowick and Kaplan, vol. 4 (1957) Lehninger (1951, 1956, 1959, I960,* 1961*) Dalton and Felix (1957) Lehninger, Wadkins, Cooper, Devlin, and Dempsey (1958) Gamble (19 58) De Robertis, Nowinski, and Saez (1960) Long, King, and Sperry (1961) Green (1951, 1954, 1957, 1958,* 1959) Loomis and Lipmann (1948) Green and Hatefi (1961) Morrison (1961) Green and Jarnefelt (1959)* Sacktor (1961) Hogeboom, Kuff, and Schneider (1957) Siekevitz (1957)* Lehninger (1951, 1956, 1959, I960,* 1961*) Lehninger, Wadkins, Cooper, Devlin, and Gamble (1958) PHYSIOLOGY, GENERAL AND COMPARATIVE Novikoff (1957, 1959, 1961) Buddenbrock (19 50-1961) Palade (1956) Gorbman (1959) Rouiller (1960) Heilbrunn (1952) Sacktor (1961) - (sarcosomes) Martin (1961) Selby (1959) Prosser and Brown (1961) Siekevitz (1957)* Scheer (1948) Sjostrand (1957) Waterman (1961) Slater (1957) - (sarcosomes) Winterstein (1910-1925) Watanabe and Williams (1951, 1953) - (sarcosomes) RESPIRATORY DATA NEUROSECRETION, NEUROSECRETORY SYSTEMS, NEUROENDOCRINE SYSTEMS, Tissues AND NEUROHORMONES De Robertis, Nowinski, and Saez (1960) (See also under Crustaceans, Dittmer and Grebe (19 58) Insects, Invertebrates) Fruton and Simmonds (1953) Heilbrunn (1952) Arvy, Gabe, and Scharrer (19 56) Robbie (1949) Bargmann, Hanstrom, Scharrer, and Scharrer Wolvekamp and Waterman (1960) (1958) Bliss (1956) Knowles (1959) W^ole Animals

Roller (1960) Dittmer and Grebe (1958) Naisse (1959) Heilbrunn (19 52) Scharrer, B. (19 59) Prosser and Brown (1961) Scharrer, E. (19 59) Wolvekamp and Waterman (1960) Scharrer and Scharrer (19 54a, 1954b) Stazione Zoologica di Napoli (1954) SUBCELLULAR MORPHOLOGY Turner (1960) Welsh (1955, 1957, 1959, 1961a, 1961b) Bargmann, Peters, and Wolpers (1960) OXIDATIVE PHOSPHORYLATION Bessis (I960)* Brachet (19 57, 1961*) Chance and Williams (1956) Butler (1959)* Cross, Taggart, Covo, and Green (1949) Clark (1961) Dickens (1959) Colowick and Kaplan, vol. 4 (1957) 100 TISSUE RESPIRATION IN INVERTEBRATES

Dempsey (1958) Schmitt and Geschwind (1957) De Robertis, Nowinski, and Saez (1960) Selby (1959) Novikoff (1961) Sjostrand (1957) Palade (1956, 1958) Zamecnik (1958)* Section 8: BIBLIOGRAPHY

Allen, Willard R., and A. Glenn Richards (morphology), 10-11 (ecology), 12 (sys- 1954. Oxygen uptake of muscle homogenates tematics), 13 (geographical distribution), from three species of insects, in the pp. 1-669, 1285-1770, figs. 1-740, 1043- presence of added succinate, cyto- 1212. chrome c, and phosphate. Canadian Bargmann, W., B. HanstrOm, B. Scharrer, and Jour. Zool., vol. 32, pp. 1-8, figs. 1-5, E. Scharrer (eds.) tables 1, 2. 1958. Zweites Internationales Symposium Allfrey, Vincent aber Neurosekretion. Berlin, Gottingen, 1959. The isolation of subcellular compon- and Heidelberg, Springer-Verlag, pp. ents. In Brachet, Jean, and Alfred E. i-v, 1-126, 71 figs. Mirsky, The cell: biochemistry, physi- Bargmann, W., D. Peters, and C. Wolpers (eds.) ology, morphology. New York, Academic 1960. Fourth international conference on elec- Press, vol. 193-290, 1, pp. figs. 1-11, tron microscopy, Berlin, Sept. 10-17, table 1. 1958. Berlin, GcJttingen, and Heidel- Allfrey, Vincent, and Alfred E. Mirsky berg, Springer-Verlag, vol. 2, Biologi- 1960. How cells make molecules. Sci. Amer., cal-medical section, pp. i-xii, 1-639, vol. 205, pp. 74-82, illus. 650 figs. American Public Health Association Barker, G. C, and G. W. C. Miner 1955. Standard methods for the examination 1961. Polarography. Endeavour, vol. 20, pp. of water, sewage, and industrial wastes. 26-31, figs. 1-6. Tenth edition. New York, pp. 1-522, Barron, E. S. Guzman illus., tables. 1958. The regulatory mechanisms of cellular Arvy, L., M. Gabe, and B. Scharrer (eds.) respiration. Union Internatl. Sci. Biol., 1956. Colloque international sur I'endocrin- ser. B (Colloques), no. 27, Perspectives ologie des invertebr^s. Ann. Sci. Nat., in Marine Biology, pp. 211-232, figs. Zool. Biol. Animale, ser. 11, vol. 18, 1-16, tables 1-14. pp. 123-337, illus. Barron, E. S. Guzman, and Theodore N. Tahmi- Baldwin, Ernest sian 1938. On the respiratory metabolism of 1948. The metabolism of cockroach muscle Helix pomatia. Biochem. Jour., vol. 32, {Periplaneta americana) . Jour. Cellular pp. 1225-1237, fig. 1, tables 1-5. Comp. Physiol., vol. 32, pp. 57-76, figs. 1949. An introduction to comparative biochem- 1-4, tables 1-14. istry. Third edition. Cambridge, Uni- Barth, L. G. versity Press, pp. i-xiii, 1-164, figs. 1942. Regional differences in oxygen consump- 1-12, tables 1-9. tion of the amphibian gastrula. Physiol. 1957. Dynamic aspects of biochemistry. Zool., vol. 15, pp. 30-46, figs. 1-4, pi. Third edition. Cambridge, University 1, tables 1-11. Press, pp. i-xx, 1-526, figs. 1-39, Bayliss, L. E. tables 1-37. 1959. Principles of general physiology. Lon- Balss, Heinrich don, Longmans, Green and Co., Ltd., 1940-1957. Decapoda. In Bronn, H. G., Klas- vol. 1, The physico-chemical backgrounc sen und Ordnungen des Tierreichs. pp. 370-381. Leipzig, Akademische Verlagsgesell- Belding, Harwood S., John Field, II, Frank W. schaft, vol. div. 5, 1, book 7, nos. 1-5 Weymouth, and Shannon C. Allen

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1942. Studies on the metabolism of marine Brecht, K., G. Utz, and E. Lutz

invertebrate tissue. I. Respiration of the 1955. Uber die Atmung quergestreifter und midgut gland of the kelp crab (Pugettia glatter Muskeln von Kaltblutern in Ruhe, producta). Physiol. Zool., vol. 15, pp. Dehnung, Kontraktion und Kontraktur. 75-88, figs. 1-4, tables 1-6. Pfluger's Arch. Ges. Physiol., vol. 260, Bessis, Marcel pp. 524-537, figs. 1-8, table 1. 1960. The ultrastructure of cells. Basel, Sandoz Bronn, H. G. Monographs, pp. 1-112, figs. 1-81. 1880-1961. Klassen und Ordnungen des Tier- Bliss, Dorothy E. reichs. Leipzig, Akademische Ver- 1953. Endocrine control of metabolism in the lagsgesellschaft, vols. 1-6. land crab, Gecarcinus lateralis Brooks, Marion A. (Freminville). I. Differences in the 1957. Succinoxidase in the American cock- respiratory metabolism of sinusgland- roach. Ann. Ent. Soc. Amer., vol. 50, less and eyestalkless crabs. Biol. Bull., pp. 122-125, fig. 1. vol. 104, pp. 275-296, figs. 1-9, table 1. Brown, Frank A., Jr. (ed.) 1956. Neurosecretion and the control of 1950. Selected invertebrate types. New York, growth in a decapod crustacean. In John Wiley and Sons, Inc., London, Wingstrand, Karl Georg (ed.), Bertil Chapman and Hall, Ltd., pp. i-xx, 1-597, Hanstrom. Zoological papers in honour figs. 1-235.

of his sixty-fifth birthday, November Buchsbaum, Ralph, and Lorus J. Milne 20th, 1956. Lund, Zoological Institute, 1960. The lower animals: Living invertebrates pp. 56-75, figs. 1-7. of the world. In The world of nature 1959. Factors controlling regeneration of legs series. Garden City, New York, Double- and molting in land crabs. In Campbell, day and Co., Inc., pp. 1-303, illus. Frank L. (ed.), Physiology of insect de- Buddenbrock, W. von velopment. Developmental Biology Con- 1945-1954. Physiologic der Decapoden. In ference Series, 1956. Chicago, Univer- Bronn, H. G., Klassen und Ordnungen sity of Chicago Press, pp. 131-140, des Tierreichs. Leipzig, Akademische

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zoology," revised. Berkeley and Los [ MS.] The comparative endocrinology of the Angeles, University of California Press, invertebrates. Ann. Rev. Physiol., vol. pp. i-xiv, 1-446, figs. 1-138. 24. Stadie, William C, and Benjamin C. Riggs Vernberg, F. John 1944. Microtome for the preparation of tissue 1956. Study of the oxygen consumption of ex- slices for metabolic studies of surviving cised tissues of certain marine decapod tissues in vitro. Jour. Biol. Chem., vol. Crustacea in relation to habitat. Physiol. 154, pp. 687-690, figs. 1-3, tables 1, 2. Zool., vol. 29, pp. 227-234, fig. 1, tables Stannard, J. N., and B. L. Horecker 1-4. 1948. The in vitro inhibition of cytochrome Villee, Claude, Robert Lichtenstein, Neal oxidase by azide and cyanide. Jour. Biol. Nathanson, and Brita Rolander Chem., vol. 172, pp. 599-608, figs. 1-3, 1950. Studies of the carbohydrate metabolism table 1. of invertebrate tissues in vitro. Biol. Stazione Zoologica di Napoli Bull., vol. 99, p. 365. 1954. Convegno sulla neurosecrezione. Pubbl. Vincentiis, Mario de Staz. Zool. Napoli, vol. 24, suppl., pp. 1952. II ricambio della retina nei teleostei 1-98. (Scorpaena scrofa) e nei cefalopodi Sumner, James B., and Karl Myrback (eds.) (Octopus vulgaris). Contributo alio 1950-1952. The enzymes: chemistry and studio del metabolismo retinico. Pubbl. mechanism of action. New York, Aca- Staz. Zool. Napoli, vol. 23, pp. 215- demic Press, vol. 1, pt. 1 (1950), pp. 223, tables 1-3. i-xvii, 1-724; vol. 1, pt. 2 (1951), pp. Warburg, Otto (ed.) Translated i-x, 725-1361; vol. 2, pt. 1 (1951), pp. 1931. The metabolism of tumours. Smith, i-xi, 1-790; vol. 2, pt. 2 (1952), pp. i-xi, by F. Dickens. New York, R. R. 791-1440, illus., tables. Inc., pp. i-xxx, 1-327, illus., tables. Tappel, A. L. Ward, Henry Baldwin, and George Chandler 1960. Cj^ochromes of muscles of marine in- Whipple vertebrates. Jour. Cellular Comp. 1959. Fresh-water biology. Second edition 116 TISSUE RESPIRATION IN INVERTEBRATES

(Edmondson, W. T., ed.). New York, Eugene, University of Oregon Publica- John Wiley and Sons, Inc., London, tions, pp. 161-171. Chapman and Hall, Ltd., pp. i-xx, 1- 1959. Neuroendocrine substances. In Gorbman, 1248, lllus. Aubrey (ed.). Comparative endocrinology. Watanabe, Mary Ishimoto, and Carroll M. New York, John Wiley and Sons, Inc., Williams London, Chapman and Hall, Ltd., pp. 1951. Mitochondria in the flight muscles of 121-133, figs. 1, 2.

insects. I. Chemical composition and 1961a. Neurohumors and neurosecretion. In enzymatic content. Jour. Gen. Physiol., Waterman, Talbot H. (ed.). The physiol- vol. 34, pp. 675-689, figs. 1-5, tables ogy of Crustacea. New York, Academic 1-3. Press, vol. 2, pp. 281-311, figs. 1-3, 1953. Mitochondria in the flight muscles of table 1.

insects. II. Effects of the medium on 1961b. Neurohormones of Mollusca. Amer. the size, form, and organization of iso- Zool., vol. 1, pp. 267-272, figs. 1-3, lated sarcosomes. Ibid., vol. 37, pp. 71- tables 1, 2, 90, figs. 1-5, pi. 1, tables 1-4. Wennesland, Reidar Waterman, Talbot H. (ed.) 1951. A volumetric microrespirometer for 1960-1961. The physiology of Crustacea. New studies of tissue metabolism. Science, York, Academic Press, vol. 1 (1960), pp. vol. 114, pp. 100-103, figs. 1-3. i-xvii, 1-670; vol. 2 (1961), pp. i-xiv, Wernstedt, Christer 1-681, illus., tables. 1944. Metabolism of gill epithelium of a fresh- Waterman, Talbot H. water mussel. Nature, vol. 154, p. 463. 1961. Comparative physiology. In Waterman, Wigglesworth, V. B. Talbot H. (ed.). The physiology of 1951. The principles of insect physiology. Crustacea. New York, Academic Press, Fourth edition, revised. London, Methuen vol. 2, pp. 521-593, figs. 1-3. and Co., Ltd., pp. i-viii, 1-544, illus. Weichselbaum, T. E. 1954. The physiology of insect metamorphosis. 1946. An accurate and rapid method for the Cambridge Monogr. Exp. Biol., no. 1, determination of proteins in small pp. i-viii, 1-152, figs. 1-45, pis. 1-4. amounts of blood serum and plasma. 1957. The action of growth hormones in in- Tech. Bull. Amer. Jour. Clin. Pathol., sects. In The biological action of growth vol. 10, pp. 40-49, table 1. substances. Symposia Soc. Exp. Biol., Weinbach, Eugene C. no. 11, pp. 204-227, figs. 1-6, pis. 1-3. 1956. The influence of pentachlorophenol on 1959. Metamorphosis, polymorphism, differ- oxidative and glycolytic phosphorylation entiation. Sci. Amer., vol. 200, pp. 100- in snail tissue. Arch. Biochem. and 110, illus. Biophys., vol. 64, pp. 129-143, fig. 1, Williams, Carroll M. tables 1-4. 1958. The juvenile hormone. Sci. Amer., vol. Weller, Harry, and R. R. Ronkin 198, pp. 67-74, illus. 1952. Effects of 2, 4-dinitrophenol upon oxygen Wilson, Douglas P. consumption and ciliary activity in the 1947. They live in the sea. London, Collins, ctenidia of Mytilus. Proc. Soc. Exp. Biol. pp. 1-128, pis. 1-90. Med., vol. 81, pp. 65-66, table 1. 1951. Life of the shore and shallow sea. Sec- Welsh, John H. ond edition. London, Nicholson and Wat- 1955. Neurohormones. In Pincus, G., and K. son, pp. i-xvii, 1-213, figs. 1-10, pis. 1-44 V. Thimann (eds.). The hormones. New Wilson, Edmund B. York, Academic Press, vol. 3, pp. 97- 1925. The cell in development and heredity. 151, figs. 1-8, tables 1-4. New York, the Macmillan Co., pp. i- 1957. Neurohormones or transmitter agents. xxxvii, 1-1232, figs. 1-529. In Scheer, Bradley T. (ed.), Recent Winterstein, Hans (ed.) advances in invertebrate physiology. 1910-1925. Handbuch der vergleichenden BIBLIOGRAPHY 117

Physiologie. Jena, Verlag von Gustav Internatl. de Physiol., vol. 48, pp. Fischer, vol. 1, Physiologie der 370-372. Korpersafte Physiologie der Atmung, Wolvekamp, H. P., and Talbot H. Waterman Erste Halfte (1925), pp. i-xiii, 1-1456, 1960. Respiration. In Waterman, Talbot H. illus., tables; Zweite Halfte (1921), pp. (ed.), The physiology of Crustacea. New i-xii, 1-1052, illus.; vol. 2, Physiologie York, Academic Press, vol. 1, pp. 35- der Stoffwechsels, Erste Halfte (1911), 100, figs. 1-10, tables 1-14. pp. i-x, 1-1563, illus.; Zweite Halfte Yonge, C. M. (1924), pp. i-xi, 1-1152, illus., tables; 1949. The sea shore. London, Collins, pp. vol. 3, Physiologie der Energiewechsels, i-xvi, 1-311, figs. 1-88, pis. 1-40. Physiologie der Formwechsels, Erste Young, Roger G. Halfte, teil 1 (1914), pp. i-xiii, 1-1188, 1958. Aldolase and malic dehydrogenase in illus., tables, teil 2 (1914), pp. i-viii, the fat body of Periplaneta americana. 1-2041, illus.; Zweite Halfte (1910- Proc. 10th Internatl. Congr. Ent., vol. 1914), pp. i-xii, 1-1060, illus., tables; 2, pp. 369-370. vol. 4, Physiologie der Reizaufnahme, 1959. Oxidative metabolism of insect fat body. Reizleitung, und Reizbeantwortung Ann. Ent. Soc. Amer., vol. 52, pp. 567- (1913), pp. i-xii, 1-997, illus. 570, figs. 1-3, table 1. Winterstein, Hans, and Muhtar Basoglu Zamecik, Paul C. 1939. Sur le metabolisme de la corde ner- 1958. The microsome. Sci. Amer., vol. 198, veuse ventrale du ver de terre. Arch. pp. 118-124.

Section 9: INDEXES

Figures in boldface refer to Section 2: Presentation of Data: A Table of Respiratory Rates of Invertebrate Tissues. Figures in italics refer to Section 6: Glossary.

SYSTEMATIC INDEX

Acheta domesticus (Linnaeus), Insecta, 55 bug, giant water. See Belostoma Annelida, 1, 2, 39-43, 79, 86, 87, 91, 92" Burgundy snail. See Helix pomatia Anodonta celensis, Pelecypoda, 21 Busy con, Gastropoda, 17 Anodonta cellensis (Schroter), 21 American cockroach. See Periplaneta americana Callinectes sapidus Rathbun, Crustacea, 45, 77 American lobster. See Homarus americanus Calliphora erythrocephala (Meigen), Insecta, 57, anemone, sea. See Condylactis gigantea 78, 86 Anthozoa, Coelenterata, 1, 2, 11, 76 Carcinides maenas, 45-47, 78-80, 84-86 Apis mellifera Linnaeus, Insecta, 55 Carcinus maenas (Linnaeus), Crustacea, 45-47, Aplysia, Gastropoda, 15-17, 83, 92 78-80, 84-86 Aplysia limacina de Blainville, 17 Carpocapsa pomonellaCLiimaeus), Insecta, 57, 77 Area ponderosa, 31 Cassiopea frondosa (Pallas), Scyphozoa, 11, 82 ark shell. See Noetia ponderosa Cecropia moth. See Hyalophora cecropia Arthropoda, 1, 2, 43-73, 76-81, 83-87, 91-93 cephalopod moUusks. See Cephalopoda, Mollusca ascarid, horse. See Parascaris equorum Cephalopoda, Mollusca, 1, 2, 33-39, 75-77, 79, ascarid, pig. See Asearis lumbrieoides 83, 86, 91-94 Asearis lumbrieoides Linnaeus, Nematoda, 11-13, Chaetopterus, Polychaeta, 39 75, 82 Cinachyra cavernosa (Lamarck), Demospongiae,

Asearis megaloeephala , 13, 82 9, 75 Aschelminthes, 1, 2, 11-13, 75, 82 clam. See Mactra Mercenaria mercenaria Astaeus , Crustacea, 45 clam, hard-shelled. See Atrina serrata Sowerby, Pelecypoda, 33 clam, soft-shelled. See Mya

Australian rock oyster. See Saxostrea Clibinarius vittatius , Crustacea, 47, 77 commercialis Clibinarius vittatus (Bosc), 47, 77 Axinella rosaeea, 9, 75 Clitellata, Annelida, 1, 2, 41-43, 79, 86, 87, 91, 92 cockroach, American. See Periplaneta americana bee, honey. See Apis mellifera cockroach, German. See Blattella germaniea beetle, water scavenger. See Hydrophilus ater cockroach, Madeira. See Leucophaea maderae Belostoma, Insecta, 55, 77 codling moth. See Carpocapsa pomonella bivalve moUusks. See Cephalopoda, MoUusca Coelenterata, 1, 2, 11, 76, 81, 82, 94 black blow fly. See Phormia regina conch. See Busycon Blattella germaniea Linnaeus, Insecta, 55 Condylactis gigantea Weinland, Anthozoa, 11, 76 blue crab. See Callinectes sapidus corals. See Gorgonia flabellum and Plexaura blue worm. See Oetolasium eyaneum flexuosa bluebottle fly. See Calliphora erythrocephala crab, blue. See Callinectes sapidus Bombyx mori (Linnaeus), Insecta, 55 crab, fiddler. See Uca minax and Uca pugilator brandling. See Eisenia foetida crab, ghost. See Ocypode quadrata

119 120 TISSUE RESPIRATION IN INVERTEBRATES

crab, green. See Carcinus maenas feather-duster worm. See Sabella pavonina crab, hermit. See Clibinarius vittatus fiddler crab. See Uca minax and Uca crab, horseshoe. See Limulus polyphemus pugilator crab, kelp. See Pugettia producta fleshfly. See Sarcophaga bullata crab, marsh. See Sesarma cinereum fly, black blow. See Phormia regina crab, mud. See Panopeus herbstii fly, bluebottle. See Calliphora erythrocephala crab, purple land. See Gecarcinus lateralis fly, flesh. See Sarcophaga bullata crab, red-jointed fiddler. See Uca minax fly, house. See Musca domestica crab, spider. See Libinia and Maja fresh-water mussel. See Anodonta cellensis, crab, stone. See Menippe mercenaria Cristaria plicata, and Hyriopsis schlegelii crab, striped shore. See Pachygraphsus eras sip es Galleria mellonella Crassostrea gigas (Thunberg), Pelecypoda, 21, (Linnaeus), Insecta, 57 75-77 garden snail, dented. See Helix aspersa gastropod mollusks. Crassostrea virginica (Gmelin), 23, 75, 76, 78, 84 See Gastropoda, Mollusca Gastropoda, crawfish. See Panulirus argus Mollusca, 1, 2, 15-21, 75, 77, 79, 83, crayfish. See Astacus 86, 91-93 cricket, greenhouse stone. See Tachycines Gecarcinus lateralis (Freminville), Crustacea, asynamorus 47, 78, 84, 85 Geodia cricket, house. See Acheta domesticus gibberosa Lamarck, Demospongiae, 9, 75 cricket, Japanese stone. See Tachycines German cockroach. See Blattella germanica asynamorus ghost crab. See Ocypode quadrata giant water bug. Cristaria plicata (Solander), Pelecypoda, 23, See Belostoma 76, 77 Gorgonia flabellum Linnaeus, Anthozoa, 11, 76 gorgonian, Crustacea, Arthropoda, 1-2, 45-53, 76-80, 83-86, purple. See Plexaura flexuosa 91-93, 95 grasshopper, differential. See Melanoplus cucumber, sea, 91. See also Isostichopus differentialis badionotus and Thyone grasshopper, red-legged. See Melanoplus cuttlefish. See Sepia officinalis fetnurrubrum Cydia pomonella, 57, 77 greater wax moth. See Galleria mellonella green crab. See Carcinus maenas greenhouse Demospongiae, Porifera, 1, 2, 9-11, 75 stone cricket. See Tachycines dented garden snail. See Helix aspersa asynamorus desert locust. See Schistocerca gregaria Gryllus domesticus, 55 Gryphaea Diestrammena japanica, 73, 80, 86 angulata Lamarck, Pelecypoda, 25, 77, 78, 84 differential grasshopper. See Melanoplus I differentialis Dreissena, Pelecypoda, 23 hard-shelled clam. See Mercenaria Dreissensia, 23 mercenaria hare, sea. See Aplysia Dysidea crawshayi de Laubenfels, Demospongiae, Helicacea, Gastropoda, 92 9, 75 Helix aspersa MUller, Gastropoda, 17, 79, 86 Helix hierosolyma, 19 earthworm, 43, 91. See Lumbricus terrestris Helix pisana MUller, 17 Echinodermata, 1, 2, 73, 82, 91 Helix pomatia Linnaeus, 17-19, 75, 77, 83 edible land snail, little. See Helix pisana Helix vermiculata Miiller, 19 edible land snail, white-lipped. See Helix hermit crab. See Clibinarius vittatus vermiculata Holothuroidea, Echinodermata, 1, 2, 73, 82 edible mussel. See Mytilus edulis Homarus americanus Milne- Edwards, Crustacea, Eisenia foetida (Savigny), Clitellata, 41, 79, 86 47-49, 76 Eledone, Cephalopoda, 33 Homarus gammarus (Linnaeus), 49, 80, 85 Homarus vulgaris, 49, 80, 85 fan, purple sea. See Gorgonia flabellum honey bee. See Apis mellifera INDEX 121

horseshoe crab. See Limulus polyphemus Lum.bricus terrestris Linnaeus, Clitellata, 43 house cricket. See Acheta domesticus Lymnaea stagnalis (Linnaeus), Gastropoda, 21 house fly. See Musca domestica Hyalophora cecropia (Linnaeus), Insecta, 5, Mactra, Pelecypoda, 27 57-63, 76, 78, 82, 83 Madeira cockroach. See Leucophaea m,aderae Hydrophilus ater Olivier, Insecta, 63, 77 Maja, Crustacea, 51 Hydrozoa, Coelenterata, 1, 2, 11, 76 manure worm. See Eisenia foetida Hyriopsis schlegelii (von Martens), Pelecypoda, marsh crab. See Sesarma cinereum 25, 76, 77 mealworm, yellow. See Tenebrio molitor Melanoplus differentialis (Thomas), Insecta, 65 Insecta, Arthropoda, 1, 2, 55-73, 76-81, 83, 84, Melanoplus femurrubrum, (De Geer), 65 86, 87, 91-93, 96, 97 Menippe m,ercenaria (Say), Crustacea, 51, 77 insects. See Insecta, Arthropoda Mercenaria m.ercenaria (Linnaeus), Pelecypoda, Ircinia fasciculata (Pallas), Demospongiae, 9, 75 27-29, 76-79, 84, 86 Isognomon alata (Gmelin), Pelecypoda, 25, 76 Merostomata, Arthropoda, 1, 2, 43-45, 77, 79,

Isostichopus badionotus (Selenka), Holothuroidea, 80, 83, 87 73, 82 Microciona prolifera (Ellis and Solander), Demospongiae, 9 Japanese stone cricket. See Tachycines migratory locust. See Locusta migratoria asynamorus MoUusca, 1, 2, 15-39, 75-79, 81, 83, 84, 86, jellyfish. See Cassiopea frondosa and 91-94 Pelagia noctiluca mollusks, bivalve. See Pelecypoda, Mollusca jellyfishes, 94. See also Scyphozoa, mollusks, cephalopod. See Cephalopoda, Coelenterata Mollusca Jerusalem land snail. See Levantina mollusks, gastropod. See Gastropoda, hierosolyma Mollusca kelp crab. See Pugettia producta moth, Cecropia. See Hyalophora cecropia moth, codling. See Carpocapsa pom.onella land crab, purple. See Gecarcinus lateralis moth, greater wax. See Galleria mellonella land snails. See Helix and Levantina moth, Polyphemus. See Telea polyphemus

Leander adspersus , 51, 80, 85 moth, saturniid, 83. See also Hyalophora cecropia leech, 43, 91 and Telea polyphemus Leucophaea maderae (Fabricius), Insecta, 63, mud crab. See Panopeus herbstii 77, 80, 84 mud dauber wasp. See Sceliphron cem.entarius Levantina hierosolyma (Boiss), Gastropoda, 19 Musca domestica Linnaeus, Insecta, 65 Libinia dubia Milne- Edwards, Crustacea, 49, 77 mussel. SeeMytilus and Driessena Libinia emarginata Leach, 49, 79, 86 mussel, edible. See Mytilus edulis Limulus polyphemus (Linnaeus), Merostomata, mussel, fresh-water. See Anodonta cellensis, 1, 43-45, 77, 79, 80, 83, 87 Cristaria plicata, and Hyriopsis schlegelii Lissodendoryx isodictyalis (Carter), Mya, Pelecypoda, 29 Demonspongiae, 9, 75 Mytilus, Pelecypoda, 29, 75 little edible land snail. See Helix pis ana Mytilus crassitesta Lischke, 29 Litomosoides carinii (Travassos), Nematoda, 82 Mytilus edulis Linnaeus, 29 lobster, 49, 77 Mytilus galloprovincialis Lamarck, 29, 79, 86 lobster, American. See Hotnarus americanus lobster, spiny. See Panulirus argus Nematoda, Aschelminthes, 1, 2, 11-13, 75, 82 locust, desert. See Schistocerca gregaria night crawler. See Lumbricus terrestris locust, migratory. See Locusta migratoria Noetia ponderosa (Say), Pelecypoda, 31 locust, South American. See Schistocerca infumata Octolasium cyaneum (Savigny), Clitellata, 43, 79, 87 Locusta migratoria (Linnaeus), Insecta, 63 octopus. See Eledone and Octopus Loligo pealeii Lesueur, Cephalopoda, 33-35, 76 Octopus, Cephalopoda, 37, 83 122 TISSUE RESPIRATION IN INVERTEBRATES

Octopus macropus Risso, 37, 75 Porifera, 1, 2, 9-11, 75, 81 Octopus vulgaris Lamarck, 37-39, 77, 83 Portuguese man-of-war. See Physalia physalis Ocypode albicans, Crustacea, 51, 77 Portuguese oyster. See Gryphaea angulata Ocypode quadrata (Fabricius), 51, 77 prawn. See Pandalus borealis- See also shrimp orange, sea. See Tethya aurantia Pseudaxinella rosacea (Verrill), Demospongiae, Ostrea circumpicta Pilsbry, Pelecypoda, 31 9, 75 Ostrea gigas, 21, 75-77 Pugettia producta (Randall), Crustacea, 53, 77 Ostrea virginica, 23, 75-76, 78, 84 purple gorgonian. See Plexaura flexuosa oyster. See Crassostrea gigas and Ostrea purple land crab. See Gecarcinus lateralis circumpicta purple sea fan. See Gorgonia flabellum oyster, Australian rock. See Saxostrea commercialis quahog. See Mercenaria mercenaria oyster, pearl. See Pinctada martensii oyster, Portuguese. See Gryphaea angulata red-jointed fiddler crab. See Uca minax oyster, tree. See Isognomon alata red-legged grasshopper. See Melanoplus oyster, Virginia. See Crassostrea virginica femurrubrum

Pachygrapsus crassipes Randall, Crustacea, 51 Sabella pavonina Savigny, Polychaeta, 39-41 Palaemon squilla (Linnaeus), Crustacea, 51, Sarcophaga bullata Parker, Insecta, 71, 78 80, 85 saturniid moth, 83. See also Hyalophora Pandalus borealis Kr0yer, Crustacea, 53 cecropia and Telea polyphemus Pandalus montagui Leach, 53 Saxostrea com.m. ere talis Iredale, Pelecypoda, 33 Panopeus herbstii Milne- Edwards, Crustacea, scallop. See Pecten 53, 77 Sceliphron cementarius (Drury), Insecta, 71 Panulirus argus (Latreille), Crustacea, 53, 76 Schistocerca gregaria (Forskal), Insecta, 71 Parascaris equorum Goeze, Nematoda, 13, 82 Schistocerca infumata Scudder, 73, 77 parchment worm. See Chaetopterus Schistosom.a mansoni Sambon, Trematoda, 82 peacock worm. See Sabella pavonina Scyphozoa, Coelenterata, 1, 2, 11, 82 pearl oyster. See Pinctada martensii sea anemone. See Condylactis gigantea Pecten, Pelecypoda, 31 sea cucumber, 91. See also Isostichopus Pecten irradians Lamarck, 31 badionotus and Thyone Pedalion alata, 25, 76 sea fan, purple. See Gorgonia flabellum Pelagia cyanella, Scyphozoa, 11 sea hare. See Aplysia Pelagia noctiluca (Forskal), 11 sea orange. See Tethya aurantia Pelecypoda, Mollusca, 1, 2, 21-33, 75-79, Sepia officinalis Linnaeus, Cephalopoda, 39, 84, 86, 91, 93 79, 86 pen shell. See Pinna muricata Sesarma cinerea, Crustacea, 53, 77 Periplaneta americaim (Linnaeus), Insecta, Sesarm.a cinereum (Bosc), 53, 77 65-71, 76-79, 84, 86, 87 shore crab, striped. See Pachygrapsus crassipes petit-gris. See Helix aspersa shrimp. See Palaemon squilla Phorm.ia regina (Meigen), Insecta, 71, 78 shrimp, pink. See Pandalus montagui. See also Physalia pelagica, Hydrozoa, 11, 76 prawn, Physalia physalis (Linnaeus), 11, 76 silkworm. See Bom,byx mori Pinctada martensii (Dunker), Pelecypoda, snail, Burgundy. See Helix pomatia 31, 75-77, 79 snail, dented garden. See Helix aspersa Pinna m.uricata Linnaeus, Pelecypoda, 33 snail, Jerusalem land. See Levantina

Platyhelminthes , 1, 82 hierosolytna

Platysamia cecropia, 5, 57-63, 76, 78, 82, 83 snail, little edible land. See Helix pis ana Plexaura flexuosa Kiikenthal, Anthozoa, 11, 76 snail, pond. See Lymnaea stagnalis Polychaeta, Annelida, 1,2, 39-41 snail, vineyard. See Helix pomatia Polyphemus moth. See Telea polyphemus snail, white-lipped edible land. See Helix pond snail. See Lym.aea stagnalis vermiculata ,

INDEX 123

snails. See Gastropoda, MoUusca Demospongiae, 11, 75 snails, land. See Helix and Levantina Tethya aurantia (Pallas), Demospongiae, 11, 75 soft-shelled clam. See Mya Thyone, Holothuroidea, 73 South American locust. See Schistocerca tree oyster. See Isognomon alata infumata Trematoda, Platyhelminthes, 82 Spheciospongia, Demospongiae, 9, 75 spider crab. See Libinia and Maja Uca minax (Le Conte), Crustacea, 53, 77 spiny lobster. See Panulirus argus Uca pugilator (Bosc), 53, 77 sponge, fire. See Tedania ignis sponge, red oyster. See Microciona prolifera Venus mercenaria, 27-29, 76-79, 84, 86 sponge, stinker. See Ircinia fasciculata vineyard snail. See Helix pom,atia sponges. See Porifera; also Cinachyra caver- Virginia oyster. See Crassostrea virginica nosa, Dysidea crawshayi, Geodia gibberosa, mud dauber. See Sceliphron cementarius Lissodendoryx isodictyalis , Pseudaxinella wasp, rosacea, Spheciospongia, Terpios fugax, and wax moth, greater. See Galleria mellonella Tethya aurantia water scavenger beetle. See Hydrophilus ater squid, 37. See also Loligo pealeii white-lipped edible land snail. See Helix Stichopus mobii, 73, 82 vermiculata stone crab. See Menippe mercenaria worm, blue. See Octolasium cyaneum stone cricket, greenhouse. See Tachycines worm, earth, 43, 91. See also Lumbricus asynamorus terrestris striped shore crab. See Pachygrapsus crassipes worm, feather-duster. See Sabella pavonina worm, manure. See Eisenia foetida Tachycines asynamorus Adelung, Insecta, worm, parchment. See Chaetopterus 73, 80, 86 worm, peacock. See Sabella pavonina Tedania ignis (Duchassaing and Michelotti)

Demospongiae, 9, 75 Xiphosura Polyphemus , 1, 43-45, 77, 79, 80, Telea Polyphemus Cramer, Insecta, 73 83, 87 Tenebrio molitor Linnaeus, Insecta, 73, 78 Terpios fugax (Duchassaing and Michelotti), yellow mealworm. See Tenebrio m.olitor

AUTHOR INDEX

Abbott, D. P., 97 Bartels, H., 43 Abood, L. G., 19 Barth, L. G., 98 Abraham, M., 19 Basoglu, M., 43 Allen, S. C, 53, 77, 84 Bayliss, L. E., 98 Allen, W. R., 67, 71-73, 78, 84, 86 Beck, S. D., 67, 76 Allfrey, V., 95, 98 Behrens, R., 43 American Public Health Association, 98 Belding, H. S., 53, 77, 84 Andrews, J. R., 35, 98 Benedict, D., 76 Arvanitaki, A., 17-19, 29, 39, 79, 86 Bessis, M., 96, 99 Arvy, L., 95-97, 99 Bliss, D. E., 85, 95, 99

Block, D. I., 69 Baldwin, E., 17-19, 95-98 Bodenstein, D., 67 Balss, H., 95 Borradaile, L. A., 97 Barber, A. A., 23, 75 Bowers, M. B., 35 Bargmann, W., 96-97, 99 Boyer, P. D., 96 Barker, G. C, 98 Brachet, J., 99 Barron, E. S. G., 37, 45, 65, 77, 84 Brecht, K., 21, 43 Barsa, M. C, 69 Bronn, H. G., 97 124 TISSUE RESPIRATION IN INVERTEBRATES

Brooks, M. A., 69, 78, 86 Drach, P., 85 Brown, A. W. A., 67 DuBois, A. B., 76 Brown, F. A., Jr., 97, 99 Durrani, M. Z., 13 Brown, W. D., 81, 95 Duve, C. de, 95, 96, 98

Buchsbaum, R. , 97 Buddenbrock, W. von, 95, 97, 99 Eastham, L. E. S., 97 Bueding, E., 13, 75, 82 Eckstein, B., 19 Bullock, T. H., 97 Edwards, G. A., 55, 63, 67, 73, 77, 78, 83, 84 Burris, R. H., 98 Ewer, R. F., 41 Butler, J. A. V., 99 Farmer, C. J., 67 Cadart, J., 97 Farr, A. L., 35, 47-49, 55-57, 71-73 Call, C. T., 69 Faure, S., 17-19, 29, 39, 79, 86 Calvin, J., 97 Felix, M. D., 99

Cardot, H., 17-19, 29, 39, 79, 86 Field, J., II, 3, 53, 77, 84, 98 Carlisle, D. B., 95 Folin, O., 67 Carter, G. S., 97 Foster, J. M., 35, 47 Carthy, J. D., 97 Fox, H. M., 39-41, 53, 98 Chance, B., 95, 96, 98, 99 Frieden, E., 96 Chang, T. H., 43, 47, 76 Fruton, J. S., 95, 99 Chapheau, M., 25, 77, 78, 83-84 Charms, B., 13, 82 Gabe, M., 95-97, 99 Charniaux-Cotton, H., 85 Galtsoff, P. S., 97 Cheldelin, V. H., 55 Gamble, J. L., Jr., 99 Chin, C.-H., 13, 75 Gardner, E. M., 42 Claff, C. L., 35, 98 Gerard, R. W., 43-45 Clark, G. L. 96, 99 Geschwind, N., 35, 100 Claude, A., 3, 98 Ghiretti, F., 15-17, 37-39, 75, 77, 83 Coelho, R. R., 35 Ghiretti-Magaldi, A., 15-17, 37-39, 75, 77, 83

Colowick, S. P., 95, 96, 98, 99 Gilbert, L. I., 96, 97 Connelly, C. M., 35, 94 Gilmour, D., 65 Conway, E. J., 71 Giuditta, A., 37-39, 75, 77, 83 Cooper, C, 99 Glaister, D., 29 Cooperstein, S. J., 35, 95, 96 Goodman, J. W., 35 Covo, G. A., 95, 96, 99 Gorbman, A., 99 Crawford, E. J., 35 Gordon, E. E., 9 Crawford, J. D., 76 Graham, K., 57, 77, 84 Cross, R. J., 95, 96, 99 Grasse, P. P., 97 Crowder, W., 97 Grebe, R. M., 99 Green, D. E., 95, 96, 99 Dalton, A. J., 99 Greenstein, J. P., 3 Dam, L. Van, 98 Gumbman, M., 81, 95 Dann, M., 43 Guttman, R., 43, 80, 87 Davies, R. G., 96 Dempsey, E. W., 99, 100 Hammen, C. S., 81, 95 De Robertis, E. D. P., 95, 96, 98-100 Handford, S. W., 27, 49

Deutsch, W., 1, 98 Hanstrom, B., 97, 99 Devlin, T. M., 99 Harmer, S. F., 97 Dickens, F., 97, 99 Hartline, H. K., 43-45

Dittmer, D. S., 99 Hartree, E. F., 5, 82 Dixon, M., 96, 98 Harvey, G. T., 67, 76 Drabkin, D. L., 98 Harvey, W. R., 57, 73, 82, 83, 86, 96 INDEX 125

Hatefi, Y., 95, 96, 99 Lees, A. D., 96 Heilbrunn, L. V., 99 Lees, H., 49, 77, 83 Higashi, S., 23-25, 76, 77, 83 Lehninger, A. L., 95, 96, 99 Hogeboom, G. H., 95, 98, 99 Lewis, S. E., 57, 78, 81, 86, 96 Hopkins, H. S., 23, 27, 31-33, 49, 76-79, 83, Lichtenstein, R., 17, 27-31, 39, 73 84, 86 Lilienthal, J. L., Jr., 96 Horecker, B. L., 96 Lindeman, V. F., 45 Horie, Y., 55 Lipmann, F., 96, 99 Hoskins, D. D., 55 Long, C, 95, 96, 99 Humphrey, G. F., 33 Loomis, W. F., 96, 99 Hyman, L. H., 97 Lowry, O. H., 35, 47-49, 55-57, 71-73 Ludwig, D., 69

Ito, T., 55 Lundegardh, H., 96, 98

Ishikawa, S. , 55 Lutz, E., 21 Lutz, F. E., 97 Jarnefelt, J., 95, 96, 99 Jodrey, L. H., 23, 76 Ma, T. S., 67, 71-73 Johnson, M. L., 43 McGilvery, R. W., 97 MacGinitie, G. E., 97 Kabat, E. A., 59-63 MacGinitie, N., 97 Kalckar, H. M., 15 Machado, A. L., 37 Kaplan, N. O., 95, 96, 98, 99 McShan, W. H., 63 Karlson, P., 97 Maroney, S. P., Jr., 23, 75 Kawai, K., 21-25, 29-31, 75-77, 79, 83, 86 Martin, A. W., 97, 99 Keilin, D., 5, 82, 96, 99 Mayer, M. M., 59-63 Kerkut, G. A., 19, 77, 83 Mercer, E. H., 95 Kerly, M., 29 Meyerhof, O., 15, 33, 37, 45, 51 Kermack. W. O., 49, 77, 83 Milne, L. J., 97 Keynes, R. D., 1 Miner, G. W. C., 98 Kilby, B. A., 71 Mirsky, A. E., 98 King, E. J., 95, 96, 99 Morrison, M., 96, 99 Kleinholz, L. H., 95, 97 Morrison, P. E., 67 Knowles, F. G. W., 95, 99 Morton, J. E., 97 Koller, G., 95, 97, 99 Moser, J. C., 69 Korschelt, E., 95 Myrback, K., 96 Kramer, S., 63, 71 Krebs, H. A., 3, 81, 95, 97, 99 Nachmansohn, D., 37 Krishnan, G., 47, 78, 80, 84, 85 Naisse, J., 97, 99 Krumbach, T., 97 Nathanson, N., 17, 27-31, 39, 73 Kubista, V., 69, 73, 78-80, 84, 86, 87 Navez, A. E., 76 Kuff, E. L., 95, 98, 99 Needham, J. G., 97 Kukenthal, W., 97 Nelson, W. L., 71 Kun, E., 19 Neville, E., 71 Kuntz, E., 85 Newburgh, R. W., 55 Kurfess. J. J., 96 Nicol, J. A. C., 97 Kurland, C. G., 82, 83 Nomura, S., 31 Novikoff, A. B., 95, 96, 98-100 Lankester, R., 97 Nowinski, W. W., 95, 96, 98-100 Lardy, H., 96 Laser, H., 11, 82 O'Brien, B. R. A., 41-43, 79, 87 Laverack, M. S., 19, 77, 83 Okamura, N., 21, 76 Lazarow, A., 35, 95, 96 Osborne, P. J., 81, 95 126 TISSUE RESPIRATION IN INVERTEBRATES

Pablo, I. S., 81, 96 Selby, C. C, 96, 99, 100 Palade, G. E., 95, 96, 98-100 Shanes, A. M., 49, 79, 86 Passano, L. M., 85, 95 Shapiro, H., 45, 77, 80, 83, 87 Pennak, R. W., 97 Shappirio, D. G., 5, 59-63, 76, 78, 79, 81-83, Perez -Gonzalez, M. D., 55, 63, 67, 73, 77, 78, 86, 96 83, 84 Shipley, A. E., 97 Peters, D., 96, 99 Siekevitz, P., 95, 98, 99 Pieh, S., 29, 45, 79, 86 Simmonds, S., 95, 99

Pitelka, F. A., 97 Sizer, 1. W., 96 Potter, V. R., 96 Sjostrand, F. S., 96, 99, 100 Potts, F. A., 97 Skinner, D. M., 47, 78, 84, 85 Prosser, C. L., 97, 99 Slater, E. C., 57, 78, 81, 86, 96, 99

Smith, R. I., 97 Raabe, M., 96, 97 Sperry, W. M., 95, 96, 99 Randall, R. J., 35, 47-49, 55-57, 71-73 Spiegel, M., 9 Rees, K. R., 19, 63, 75 Spiegelman, S. , 37

Reif, A. E., 96 Stadie, W. C., 1, 98

Renaud, L. , 85 Stannard, J. N., 65, 96 Richards, A. G., 67, 71-73, 78, 84, 86 Stauffer, J. F., 98 Richards, O. W., 96 Stazione Zoologica di Napoli, 97, 99 Ricketts, E. F., 97 Steinbach, H. B., 37 Riggs, B. C, 1, 98 Sumner, J. B., 96 Robbie, W. A., 3, 9-11, 25, 33, 53, 73, 75, 76, 81, 82, 96-99 Taggart, J. V., 95, 96, 99 Roberts, J. L., 51 Tahmisian, T. N., 65, 77, 84 Roberts, N. R., 35 Tappel, A. L., 81, 95, 96 Roeder, K. D., 97 Thomas, G. M., 69, 78, 84 Rolander, B., 17, 27-31, 39, 73 Thunberg, T., 23, 27, 31-33, 98 Ronkin, R. R., 75 Tosi, L., 15-17, 83 Rosebrough, N. J., 35, 47-49, 55-57, 71-73 Travis, D. F., 85 Rotta, A., 65 Turner, C. D., 95-97, 99 Rouiller, C, 99 Umbreit, W. W., 98 Sacktor, B., 65-69, 78, 81, 84, 96, 99 Utz, G., 21 Saez, F. A., 95, 96, 98-100 Sallach, H. J., 97 Van der Kloot, W., 98 Samuels, A., 63, 77, 80, 84 Vernberg, F. J., 45-53, 77, 83, 84 Sanborn, R. C, 57 Villee, C. A., 9, 17, 27-31, 39, 73 Saunders, J. T., 97 Vincentiis, M. de, 37 Scharrer, B., 95-97, 99 Scharrer, E., 97, 99 Wadkins, C. L., 99 Scheer, B. T., 45, 49-51, 80, 85, 95, 97, 99 Wallach, D. F., 35, 98

Scheer, M. A. R., 45, 49-51, 80, 85 Warburg, O., 1, 98 Schlegel, V., 63 Ward, H. B., 97

Schlieper, C, 29 Watanabe, M. I., 71, 78, 99 Schmitt, F. O., 35, 100 Waterman, T. H., 95, 99 Schneider, W. C, 3, 82, 95, 96, 98, 99 Webb, E. C, 96 Schneiderman, H. A., 82, 83, 86, 96, 97 Weesner, F. M., 97 Scholander, P. F., 35, 55, 63, 67, 73, 98 Weichselbaum, T. E., 55 Schulz, W., 15, 33, 37, 45, 51 Weinbach, E. C., 21 Schwabe, C. W., 45, 49-51, 80, 85 Welch, P. S., 97 Sedgwick, A., 97 Weller, H., 75 INDEX 127

Welsh, J. H., 95, 97, 99 Wingfield, C. A., 53, 98 Wennesland, R., 51, 98 Winterstein, H., 43, 99 Wernstedt, C, 23 Wolpers, C, 96, 99 Weymouth, F. W., 53, 77, 84 Wolvekamp, H. P., 99 Whipple, G. C, 97 Wood, J. D., 49, 77, 83 Wigglesworth, V. B., 96, 97 Wilbur, K. M., 23, 75, 76 Yonge, C. M., 97 Williams, C. M., 5, 57-63, 71. 76, 78, 81-83, Young, R. G., 55-57, 71-73, 78, 84 86, 96, 97, 99 Williams, G. R., 95, 96, 99 Wilson, D. P., 97 Zamecnik, P. C, 95, 98, 100 Wilson, E. B., 95 Zuazaga, G., 67, 71-73

SUBJECT INDEX abbreviations, 89 cyanide, 76; leg nerves, 47-49; ventral abdomen, of American cockroach, 69, 79, 87 nerve cord, 47 abdominal muscle, dorsal extensor. See dorsal anemone, sea. See sea anemone extensor abdominal muscle antimycin A, 61, 67, 76, 91; 96 absorbancy, 91 apparatus, biochemical and biophysical. See accessory glands, 91; of American cockroach, 67 continuous flow respirometer, fluorometric adductor muscle, 91; effect of age, 27, 78; effect measurement, polarograph, spectrophoto- of hydrogen cyanide, 29; effect of salinity, 29, meter 79, 86; effect of season, 21, 27; gray, 33; of apparatus, manometric. See manometer; also ark shell, 31; of Australian rock oyster, 33; Barcroft, differential, Fenn, Thunberg, and of fresh water mussel, 21-25, 77; of pearl Warburg manometers oyster, 31; of pen shell, 33; of quahog, 27-29,78, apparatus, volumetric. See differential volumeter, 79, 86; of Virginia oyster, 23, 78; red, 29; microvolumeter, Scholander-Wennesland white, 31-33 microrespirometer, volumeter, volumetric adult, developing, epithelium, 59-63, 78; of microrespirometer Cecropia moth, 59-63, 78; wing, 59-63, 78 ark shell, posterior adductor muscle, 31, 91 age, effect of. See under effect arthropods, effect of age, 84; effect of sex, air, 13, 21, 29-31, 39-41, 73 83, 84; effect of stage, 84; increase in size, albumen gland. See albuminous gland 84; molt cycle, 78, 84, 85, 93. See also albuminous gland, 91; of pond snail, 21; of vine- crabs, crustaceans, insects yard snail, 19 artificial sea water, 15, 29, 33, 45, 49-51 alcohol, 69 ascarid. horse. See horse ascarid American cockroach, abdomen, 69, 79, 87; ascarid, pig. See pig ascarid accessory gland, 67, 91; brain, 67-69; coxal ascorbate, 17, 57, 67, 71. 91 muscle, 67, 91; effect of age. 67-71, 78, 86; ascorbic acid, 33. 39, 63 effect of antimycin A, 67, 76, 91; effect of sex, Australian rock oyster, adductor muscle, 65-71, 77, 78, 84; effect of stage, 69-71, 78, 33, 91 86; fat body, 67-71, 78, 92; flight muscle, 67, axons, giant. See giant axons 78; gradient along body, 69, 79, 87; gut, 67-69. axoplasm, 91 78, 84; heart, 67; leg muscle, 65-71, 77, 78, 86; azide, 82, 83, 96 Malpighian tubules, 67-69, 93; muscle, 67-69, 78, 86; nerve cord, 67-69; nymph, 69-71, 78, 86, 93; respiratory quotient, 65, 93; testes, 67; Baldwin's phosphate solution, 17-19 thorax, 69, 78, 79, 87; wing muscle, 69-71, 78, Barcroft manometer (Barcroft respirometer), 86 3, 5, 6, 41-43, 47, 9L 98 American lobster, claw nerves, 47-49; effect of bee, honey. See honeybee 128 TISSUE RESPIRATION IN INVERTEBRATES

beetle, water scavenger. See water scavenger carbon monoxide, 21, 29-31, 37, 41-43, 75, beetle 82, 83, 96 Belar-phosphate buffer, 65 cardiac ganglion, of horseshoe crab, 43 Belar's solution, 63 catalase, 11-13, 82, 91 bicarbonate, 15, 33, 37, 51 Cecropia moth, developing adult, 59-63, biochemical and biophysical apparatus. See 78, 82; effect of antimycin A, 61, 76, 91; effect continuous flow respirometer, polarograph, of injury, 82, 83; effect of malonate, 57; effect spectrophotometer of stage, 59-63, 78, 82; epithelium, 59-63, 78, 82 biochemical and biophysical methods. See heart, 82; larva, 57, 93; midgut, 57; pupa, 5, biochemical and biophysical apparatus, 57-63, 78, 82, 83, 93; wing, 57-63, 78, 82 fluorometric measurement cell fractions. See fractions biochemistry, references, 95 cell structure, references, 95. See also sub- biology, general, references, in crustaceans, cellular morphology 95; in insects, 96; in invertebrates, 97 cell suspension, 3,4, 11-13. See also suspension black blow fly, cytochrome oxidase, 78, 91; centrifugation, density gradient, 98 effect of age, 71, 78; muscle, 71, 78 centrifugation, differential, 98 blow fly, black. See black blow fly centrifugation, ultra, 98 blue crab, claw nerve, 45; effect of sex, 45, cerebral ganglion, of vineyard snail, 19, 77. See 77; gill, 45, 77; leg nerve, 45; midgut also brain, forebrain, head ganglion, supraesoph- gland, 45, 77, 93 ageal ganglion blue worm, body wall, 43, 79; gradient along chemical methods, 5, 6. See also micro-Winkler, body, 43, 79, 86, 87; succinoxidase, 79, tetrazolium, and Winkler methods 86, 87, 94 chloride solution, isotonic. See isotonic chloride bluebottle fly, effect of age, 57, 78, 86; solution flight - muscle, 57, 78, 86; » ketoglutaric citrate, 15, 23, 49, 55, 65 oxidase, 78, 86 citric acid cycle, 81, 82, 91; references, 95 body wall. See body wall muscle clam, gill, 27; muscle, 27 body wall muscle, effect of gas phase, clam, soft-shelled. See soft-shelled clam 41-43; effect ; of suspending media, 13; claw nerve, effect of ionic concentration 49, 79, gradient along body, 41-43, 79; of blue 86; of American lobster, 47-49; of blue crab, worm, i 43, 79; of earthworm, 43; of 45; of horseshoe crab, 43; of spider crab, 49, feather-duster worm, 41; of horse 79, 86 ascarid, 13; of manure worm, 41, 79; clitellate, 91 of sabellid, 41; of vineyard snail, 19; clitellum, 41, 91 succinoxidase, 79, 94 cockroach, American. See American cockroach brachyuran, 91 cockroach, German. See German cockroach brackish water, 45 cockroach, Madeira. See Madeira cockroach brain, effect of sex, 69; of American codling moth, effect of sex, 57, 77; fat body, 57, cockroach, 67-69: of striped shore 77, 92; larva, 57, 77, 93; muscle, 57, 77; crab, 51. See also cerebral ganglion, respiratory quotient, 57, 93 forebrain, head ganglion, supraesophageal collagenous, 91 ganglion columella muscle, of vineyard snail, 19, 91 branchial gland, effect of gas phase, 39; of comparative respiratory rates, 76-78, 83 octopus, 39 concentration, effect of ionic. See under effect branchial tree, of sea cucumber, 73, 82, 91 conch, muscle, 17 brandling. See manure worm continuous flow respirometer, 35 buccal mass, 91 control of growth, references, 95, 96 buccal mass muscle, of sea hare, 15-17, 83; control of metamorphosis, references, 96 of vineyard snail, 19 control of molting, references, 95 bug, giant water. See giant water bug corpora allata, 91. See also effect of removal Burgundy snail. See vineyard snail coxal muscle, 91; effect of antimycin A, 67, 76; INDEX 129

effect of sex, 67; of American cockroach, 67; dehydrogenases, 92 of giant water bug, 55; of South American density gradient centrifugation, 98 locust, 73; of water scavenger bettle, 63 dented garden snail, effect of ionic concen- crab, blue. See blue crab tration, 39, 79, 86; heart, 17, 79, 86 crab, fiddler. See fiddler crab desert locust, fat body, 71, 92 crab, ghost. See ghost crab dialysis, 92 crab, green. See green crab diapause, 92; in Cecropia moth, 5, 57-63 crab, hermit. See hermit crab dichlorodiphenyltrichloroethane (DDT), 69 crab, horseshoe. See horseshoe crab differential centrifugation, 98 crab, kelp. See kelp crab differential locust, hind femur, 65, 92; crab, marsh. See marsh crab muscle, 65; respiratory quotient, 65, 93 crab, mud. See mud crab differential manometer, 3, 5, 6, 15, 33, 37, crab, purple land. See purple land crab 45, 51, 57, 92 crab, spider. See spider crab differential volumeter, 27-29, 43-45, 65 crab, stone. See stone crab digestive diverticula, 92. See midgut gland crab, striped shore. See striped shore crab 2, 4-dinitrophenol (DNP), 13, 23, 75, 82, crabs, comparative respiratory rates, 77, 83; 83, 92 effect of eyestalk removal, 45, 47, 80, 84, 85; diphosphopyridine nucleotide (DPN), 19, 92 effect of sex, 77, 83, 84; gill, 77, 83, 84; diphosphopyridine nucleotide, reduced midgut gland, 77, 83, 84, 93; molt cycle, (DPNH), 15-17, 59-61, 71 47, 78, 84, 85 distilled water, 13, 55 crayfish, nerve, 45 diverticula, digestive. See midgut gland cricket, greenhouse stone. See greenhouse DNP, 13, 23, 75, 82, 83, 89, 92 stone cricket dorsal extensor abdominal muscle, effect of cricket, house. See house cricket latitude, 53; effect of temperature, 53; cricket, Japanese stone. See greenhouse in prawn, 53; in pink shrimp, 53 stone cricket DPN, 19, 89, 92 crown. See tentacles DPNH, 15-17, 59-61, 71, 89 crustaceans, effect of eyestalk extract, 45, 51, 80, 92; effect of eyestalk removal, 45-51, earthworm, body wall, 43; clitellum, 91; 80, 85; effect of sinus gland extract, 84; effect of gas phase, 43; ventral nerve increase in size, 84; molt cycle, 47, 78, 84, cord, 43; respiratory quotient, 43, 93 85, 93; molt-mhibiting hormone, 85; ecdysis, 78, 84, 85, 92 references, 95 edible land snail, little. See little edible cucumber, sea. See sea cucumber land snail cuttlefish, effect of ionic concentration, 39, edible land snail, white-lipped. See white- 79, 86; effect of suspending medium, 39; lipped edible land snail nerve, 39, 79, 86 edible mussel, effect of suspending medium, cyanide, 55, 75, 76, 81-83, 96 29; effect of temperature, 29; gill, 29; cyanide, hydrogen. See hydrogen cyanide retractor muscle of foot, 29, 93 cyanide, potassium. See potassium cyanide EDTA, 55, 89, 92 cyanide-insensitive respiration, 47, 78, 80, 84 effect of age, 84; in American cockroach, cytochrome c, 15-23, 33-51, 55-73, 82, 83, 91 67, 71, 78, 86; in arthropods, 84; in cytochrome oxidase, 75, 78, 81-83, 91 black blow fly, 71, 78; in bluebottle fly, cytochrome system (electron transport system), 57, 78, 86; in pelecypod moUusks, 84; 5, 75, 81, 82, 91 in Portuguese oyster, 25, 78, 84; in cytochromes, references, 95, 96 quahog, 27, 78, 84; in Virginia oyster, 78, 84; on adductor muscle, 78, 91; on dart, sac, of vineyard snail, 19, 92 flight muscle, 57, 78, 86; on gill, 25-27, data, respiratory, 99 78; on leg muscle, 67-71, 78, 86; on DDT, 69 mantle, 25-27, 78, 93; on midgut 130 TISSUE RESPIRATION IN INVERTEBRATES

gland, 25, 78, 93; on muscle, 25-27, 57, on midgut gland, 31, 75, 76; on muscle, 13, 67-71, 78, 86; on wing muscle, 69-71, 86 78, 29, 67, 75, 76, 82; on nerve, 76; on nerve effect of environment, 86 cord, 76; on salivary gland, 37, 75; on effect of eyestalk extract, in green crab, 45, subumbrella, 82; on tentacles, 76; on wing 80, 85; in shrimp, 51, 80, 85; on muscle, epithelium, 61, 76, 82 45, 51, 80 effect of removal of corpora allata, in effect of eyestalk removal, 84, 85; in green Madeira cockroach, 63, 80; on thoracic crab, 45-47, 80, 85; in lobster, 49, 80, 85; in muscle, 80 purple land crab, 85; in shrimp, 51, 80, 85; effect of salinity, in green crab, 45, 79, 86; on muscle, 45-49, 80, 85 in quahog, 27-29, 79, 86; on adductor effect of gas phase, in earthworm, 43; in muscle, 29, 79, 86; on gill, 27, 45, 79, 86; feather -duster worm, 41; in greenhouse on mantle, 29, 79, 86 stone cricket, 73; in mussel, 29; in effect of season, in fresh-water mussel, 21; octopus, 37-39; in oyster, 21; in pearl in pearl oyster, 31, 79; in pelecypod oyster, 31; on body wall, 41-43; on mollusks, 86; in quahog, 27, 78, 79; on branchial gland, 39; on femur, 73; on gill, adductor muscle, 21, 27, 78, 79; on gill, 21, 29-31, 39; on heart, 21, 39; on kidney, 27, 31, 79; on mantle, 27, 79 39; on mantle, 21, 31; on midgut gland, effect of sex, 83, 84; in American cockroach, ' 31, 39; on optic ganglion, 39; on salivary 65-71, 77, 78, 84; in blue crab, 45, 77; in gland, 37-39 codling moth, 57, 77; in fiddler crab, 53, effect of injury, m greenhouse stone cricket, 77; in fleshfly, 71, 78; in ghost crab, 51, 73, 80, 86; in pupa, 82, 83, 86; on femur, 77; in kelp crab, 53, 77; in larva, 57, 77; 73, 80, 86; on leg muscle, 73, 80, 86 in Madeira cockroach, 63, 77, 84; in effect of insulin, in red oyster sponge, 9 mealworm, 73, 78; in mud crab, 53, 77; effect of ionic concentration, in cuttlefish, in nymph, 71, 78; in red-jointed fiddler 39, 79, 86; in dented garden snail, 17, crab, 53, 77; in spider crab, 49, 77; in 79, 86; in mussel, 29, 79, 86; in spider stone crab, 51, 77; on brain, 69; on coxal crab, 49, 79, 86; on heart, 17, 29, 79, 86; muscle, 67, 77, 78; on fat body, 57, 69-71, on nerve, 39, 49, 79, 86 77, 78; on flight muscle, 67, 73, 77, 78; on effect of latitude, in pink shrimp, 53; on foregut, 69, 83; on gill, 45, 49, 77, 83, 84; dorsal extensor abdominal muscle, 53 on hindgut, 69; on leg muscle, 67, 71-73, effect of metabolic inhibitors, 81-83; in 77, 78; on Malpighian tubules, 69; on American cockroach, 67, 76; in American metathorax, 69, 78; on midgut, 69; on lobster, 76; in Cecropia moth, 57, 61, 76, midgut gland, 45, 49, 77, 83, 84; on 82, 83; in fresh-water mussel, 76; in muscle, 57, 65-73, 77, 78, 84; on nerve jellyfish, 82; in mussel, 29, 75; in cord, 69; on thoracic muscle, 71, 77, 78, nematodes, in 82; octopus, 37, 75; in 84; on wing muscle, 69-71 oyster, 21, 75, 76; in pearl oyster, 31, effect of stage, 84, 85; in American cock- 75, 76; in pig ascarid, 13, 75; in roach, 69-71, 86; in Cecropia moth, Portuguese man-of-war, 76; in purple 59-63, 78; in green crab, 47, 78, 84; in gorgonian, 76; in purple sea fan, in 76; purple land crab, 47, 78, 84; on quahog, 27-29, 76; in sea anemone, 75; epithelium, 59-63, 78; on integumentary in sea cucumber, 82; in sea hare, 15; tissue, 47, 78, 84; on leg muscle, 69, 71, in silkworm, 55; in spiny lobster, 76; 86; on metathorax, 69; on muscle, 47, in sponge, 75, 81; in squid, 76; in 69-71, 78, 84, 86; on wing, 59-63, 78; on tree oyster, 76; in trematode, 82; wing muscle, 69-71, 86 in vineyard snail, 75; in Virginia effect of surgery, in green crab, 45-47, oyster, 23, 75, 76; on adductor muscle, 80; in greenhouse stone cricket, 73, 80, 29, 76; on branchial tree, 82; on eye, 76; 86; in lobster, 49, 80; in Madeira on gill, 21, 27-31, 75, 76; on gizzard, 15; cockroach, 63, 80; in shrimp, 51, 80; on heart, 21, 76, 82; on mantle, 21-23, on leg, 73, 80, 86; on muscle, 45-49, 29-31, 75, 76; on midgut, 55-57; on 73, 80, 86 INDEX 131 effect of suspending medium, in cuttlefish, 39; in feather-duster worm, body wall, 41; tentacles, 39 dented garden snail, 17; in edible mussel, 29; female duct, of vineyard snail, 19 in green crab, 45; in horse ascarid, 13; in femur, 92; effect of injury, 73, 80, 86; effect of mussel, 29; in octopus, 33, 37; in silkworm, 55; surgery, 73, 80, 86; of greenhouse stone in spider crab, 49-51; on body wall muscle, 13; cricket, 73, 80, 86 on gill, 29, 45; on heart, 17, 29; on midgut, 55; Fenn manometer (Fenn respirometer), 3, 5, 6, on nerve, 33, 37-39, 49-51; on stellate ganglion, 45, 55-57, 73, 92, 98 33 fiddler crab, effect of sex, 53, 77; gill, 53, 77; effect of temperature, in Australian rock oyster, midgut gland, 53, 77, 93 33; in edible mussel, 29; in horseshoe crab, 43, fiddler crab, red-jointed. See red-jointed 79, 80; in pink shrimp, 53; in prawn, 53; in fiddler crab quahog, 27; on gill, 27; on muscle, 29, 53, 63; fin nerve, of squid, 35 on optic nerve, 43, 79, 80 fire sponge, 9; effect of cyanide, 75 electron microscopy, references, 96 flavoproteins, 92 electron transport system, 5, 75, 81, 82, 92; fleshfly, effect of sex, 71, 78; flight muscle, references, 96 71, 78; thoracic muscle, 71, 78 endogenous respiration, 9-57, 63-73, 76, 78-84, flight muscle, 83; effect of age, 57, 78, 86; 86, 92 effect of sex, 67, 71-73, 77, 78; of American endoplasmic reticulum, 92 cockroach, 67, 77, 78; of bluebottle fly, 57, environment, effect of, 86 78, 86; of fleshfly, 71; of giant water bug, 55, enzymes, references, 96 77; of honeybee, 55; of mealworm, 73, 78; of epithelium, effect of stage, 59-63, 78; of mud dauber wasp, 71; of South American Cecropia moth, 59-63, 78; of developing adult, locust, 73, 77; of water scavenger beetle, 63, 59-63; 78; of pearl oyster, 31; of pupa, 59-63, 77. See also thoracic muscle, wing muscle 78, 93; of wing, 59-63, 78 fluid, perienteric, 13, 93 esophagus, of vineyard snail, 19 fluorescence, 92 estivation, effect on midgut gland, 19; in fluorometric measurement, 35 Jerusalem land snail, 19 fly, black blow. See black blow fly ethanol, 11, 13 fly, bluebottle. See bluebottle fly ethylenediaminetetraacetic acid (EDTA; versene), fly, flesh. See fleshfly 55, 92 fly, house. See house fly extensor abdominal muscle, dorsal. See dorsal foot, 83; fore, 19; middle, 19; rear, 19; of extensor abdominal muscle pearl oyster, 31, 77; of vineyard snail, 19, extinction coefficient, 92 77 extract, 47, 80, 85, 92 forebrain, of horseshoe crab, 45, 77 extract, eyestalk, 80, 85, 92. See also under foregut, effect of sex, 69; of American effect cockroach, 67-69, 77; of horseshoe crab, extract, sinus gland, 85 45, 77 eye, of horseshoe crab, 45; of octopus, 37; of fraction, nuclear, 3, 4, 47 squid, 33 fraction, particulate, 3, 4, 13, 21, 65, 83, 93, 98 eyestalk extract, 80, 85, 92. See also under fraction, soluble, 65 effect fractions, 3; references 95 eyestalk removal, effect of. See under effect fragments of organ or tissue, 3, 4, 43 fresh-water mussel, adductor muscle, 23-25, fan, purple sea. See purple sea fan 77, 91; effect of cyanide, 76; effect of fat body, 92; effect of sex, 57, 69-71, 77, 78; season, 21; gill, 23-25, 77; heart, 23-25, 77; of American cockroach, 67-71, 78; of mantle, 23-25, 77, 93; posterior adductor codling moth, 57, 77; of desert locust, 71; muscle, 21, 91 of German cockroach, 55; of house cricket, fructose, 47, 78, 80 55; of larva, 57, 73, 77, 93; of mealworm, fumarate, 15, 49, 55, 65 73; of nymph, 55, 71, 78, 93; of wax moth, 57; respiratory quotient, 57, 93 ganglion, cardiac, 43; cerebral, 19, 45, 77; 132 TISSUE RESPIRATION IN INVERTEBRATES

head, 37; of horseshoe crab, 43-45, 83; of land snail, 19; of kelp crab, 53; of lobster, 49; octopus, 33, 37, 77, of 83; squid, 35-37; of of marsh crab, 53; of mud crab, 53; of striped shore crab, 51; of vineyard snail, octopus, 37-39; of pearl oyster, 31; of pond 19, 77, 83; optic, 37, 77; pedal, 19; stellate, snail, 21; of Portuguese oyster, 25; of red- 33-35. See also brain, forebrain jointed fiddler crab, 53; of sea hare, 17; of garden snail, dented. See dented garden snail spider crab, 49; of spiny lobster, 53; of gas phase. See air, carbon monoxide, nitrogen, stone crab, 51; of vineyard snail, 17-19; oxygen; also under effect salivary, 37-39 general biology, references, in crustaceans, 95; glossary, 91-94 in insects, 96; in invertebrates, 97 glucose, 9, 13, 17, 27, 31, 37-39, 65, 73 German cockroach, fat body, 55, 92; nymph, gonad, of pearl oyster, 31 55, 93 gorgonian, purple. See purple gorgonian ghost crab, effect of sex, 51, 77; gill, 51, 77; gradient of respiratory rate, along long axis of midgut gland, 51, 77, 93 body, 41-43, 69, 79, 86, 87; along nerve, giant axons, of squid, 92; 1, 35 43-45, 79, 80, 87; effect of temperature, 43, giant nerve fibers. See giant axons 79, 80, 87; in American cockroach, 69, 79, 87; giant water bug, coxal muscle, 55, 77, 91; in blue worm, 43, 79, 86, 87; in horseshoe flight muscle, 55, 77; leg muscle, 55, 77 crab, 43-45, 79, 80, 87; in manure worm, 41, gill, 83; effect of age, 25-27, 78; effect of 79, 86 cyanide, 76; effect of gas phase, 21, 29-31, grasshopper, red-legged. See red-legged 39; effect of salinity, 27, 45, 79, 86; effect grasshopper of season, 27, 31, 78, 79; effect of sex, 45, greater wax moth, fat body, 57, 92; larva, 57, 93 49, 51, 53, 77; effect of suspending medium, green crab, during molt cycle, 47, 78, 84, 85, 93; 29, 45; epithelium, 23; inhibition by carbon effect of eyestalk extract, 45, 80, 85, 92; monoxide, 29-31; inhibition by hydrogen effect of eyestalk removal, 45-47, 80, 85; effect cyanide, 27; light- reversible inhibition by of salinity, 45, 79, 86; effect of sinus gland carbon monoxide, 21; of blue crab, 45, 77; extract, 85; effect of suspending medium, 45; of clam, 27; of edible mussel, 29; of fiddler gill, 45, 79, 86; muscle, 45-47, 78, 80, 84, 85 crab, 53, 77; of fresh-water mussel, 23-25, greenhouse stone cricket, effect of injury, 73, 77; of ghost crab, 51, 77; of green crab, 45, 80, 86; effect of surgery, 73, 80, 86; femur, 79, 86; of hermit crab, 47, 77; of marsh 73, 80, 86, 92; leg muscle, 73, 80, 86 crab, 53, 77; of mud crab, 53, 77; of mussel, growth, 84; control of, references, 95, 96 23, 29; of octopus, 39, 77; of oyster, 21, 77; gut, of American cockroach, 67; of horseshoe of pearl oyster, 31, 77; of Portuguese crab, 45. See also foregut, midgut, hindgut, oyster, 25, 77, 78; of quahog, 25, 77-79, 86; intestine of red-jointed fiddler crab, 53, 77; of scallop, 31; of soft-shelled clam, 29; of hare, sea. See sea hare spider crab, 49, 77; of squid, 33; of stone HCN, 27-29, 89 crab, 51, 77; of tree oyster, 25; pallial head ganglion, of squid, 37 margin, 31 heart, effect of gas phase, 21, 39; effect of gizzard, 92; effect of potassium cyanide, 15; ionic concentration, 17, 29, 79, 86; effect of of sea hare, 15, 83 suspending media, 17, 29; light- reversible gland, accessory, 67, 91; after estivation, 19; inhibition by carbon monoxide, 21; of albuminous, 19-21, 91; branchial, 39; American cockroach, 67; of Cecropia pupa, 82; during estivation, 19; effect of age, 25; of dented garden snail, 17, 79, 86; of fresh- effect of cyanide, 76; effect of gas phase, water mussel, 23-25, 77; of horseshoe crab, 37-39; effect of sex, 45, 49-53; inhibition 45; of little edible land snail, 17; of mussel, by carbon monoxide, 31; light- reversible 29, 79, 86; of octopus, 39, 77; of oyster, 21, inhibition by carbon monoxide, 37; midgut, 31, 77; of squid, 37; of vineyard snail, 17; 17-19, 31, 37-39, 45-53; of American of white-lipped edible land snail, 19 cockroach, 67; of fiddler crab, 53; of ghost hemimetabolous, 92 crab, 51; of hermit crab, 47; of Jerusalem hepatopancreas, 92. See midgut gland INDEX 133 hermit crab, gill, 47, 77; midgut gland, 47, Japanese stone cricket. See greenhouse stone 77, 93 cricket hexoses, 65 jellyfish, tentacles, 11; umbrella, 11, 94 hibernation, effect on midgut gland, 19; in Jerusalem land snail, estivation, 19; midgut vineyard snail, 19 gland, 19, 93 hind femur, 92; in differential locust, 65; in red-legged locust, 65; muscle, 65 KCN, 15, 47, 59-61, 67-71, 89 hindgut, effect of sex, 69; of American kelp crab, effect of sex, 53, 77; midg-ut gland, cockroach, 67, 69 53, 77, 93 holometabolous, 92 a-ketoglutarate, 19, 49, 55-57, 65, 71-73, 81 homogenate, 3, 4, 11-13, 17-19, 23, 33-35, Qf-ketoglutaric dehydrogenase, 81 41-51, 55-73, 82, 85, 93, 98 a-ketoglutaric oxidase, effect of age, 78, 86; honeybee, flight muscle, 55 in bluebottle fly, 78, 86; in flight muscle, hormone, molt-inhibiting, 85 78, 86 hormones, references, in crustaceans, 95; kidney, effect of gas phase, 39; of octopus, 39; in insects, 97; in invertebrates, 97 of vineyard snail, 19 horse ascarid, body wall muscle, 13; Krebs cycle (citric acid cycle), 81, 82, 91, 93 effect of suspending medium, 13 horseshoe crab, 83; cardiac ganglion, 43; land crab, purple. See purple land crab claw nerve, 43; effect of temperature, 43, land snail, Jerusalem. See Jerusalem land 79, 80; eye, 45; forebrain, 45, 77; foregut, snail 45, 77; gradient along a nerve, 43-45, 79, land snail, little edible. See little edible 80, 87; heart, 45; muscle, 45, 77; optic land snail nerve, 43, 77, 79, 80, 87 land snail, white-lipped edible. See white- house cricket, fat body, 55, 92; nymph, 55, 93 lipped edible land snail house fly, muscle, 65 larva, 93; effect of sex, 57; fat body, 57, 73, hydrogen cyanide, 27-29 midgut, 55-57; muscle, 57; of Cecropia hydrogen peroxide, 11-13 moth, 57; of codling moth, 57; of mealworm, hydroquinone, 17, 93. See also quinol 73; of silkworm, 55; of wax moth, 57 latitude, effect of. See under effect inhibition, light- reversible (photoreversible), leech, smooth muscle, 43 21, 37 leg muscle, 83; effect of age, 67-71, 78, 86; inhibitors, metabolic, 3; references, 96. See effect of cyanide, 76; effect of injury, 73, also antimycin A, carbon monoxide, cyanide, 80, 86; effect of sex, 67-73, 77, 78; effect 2, 4-dinitrophenol, hydrogen cyanide, malonate, of stage, 69-71, 78, 86; effect of surgery, potassium cyanide; also under effect 73, 80, 86; of American cockroach, 65-71, injury, effect of. See under effect 77, .78, 86; of coxa, 55, 63, 67, 73, 77, 78; insects, comparative respiratory rates, 76, 77, of femur, 73, 80, 86; of giant water bug, 55, 83; effect of age, 78, 84, 86; effect of sex, 77; of green crab, 85; of greenhouse stone 76-78, 83, 84; effect of stage, 78, 84, 86; cricket, 73; of mealworm, 73, 78; of nymph, flight muscle, 77, 78, 83, 86; leg muscle, 77, 71, 78, 86; of South American locust, 73, 78, 83, 86; references, 96, 97 77; of spiny lobster, 53; of striped shore insulin, effect of. See under effect crab, 51; of water scavenger beetle, 63, integumentary tissue, during molt cycle, 47, 78, 77; respiratory quotient, 65, 93 84; of purple land crab, 47, 78, 84 leg nerve, effect of cyanide, 76; effect of intermediary metabolism, references, 97 suspending medium, 51; of American intermolt cycle. See molt cycle lobster, 47-49; of blue crab, 45; of spider intestine, of sea cucumber, 73. See also gut crab, 51; of spiny lobster, 53 invertebrates, references, 97, 98 life cycle, variation during. See effect of ionic concentration, effect of. See under effect stage iso Citrate, 23, 35, 55, 71 light- reversible inhibition by carbon monoxide, isotonic chloride solution, 17-19, 29, 39, 45, 55 21, 37 134 TISSUE RESPIRATION IN INVERTEBRATES

little edible land snail, heart, 17 solution, sucrose. Wilder and Smith saline; liver, 93. See midgut gland also under effect lobster, effect of eyestalk removal, 49, 80, 85; mesothorax, of American cockroach, 69, 79 midgut gland, 49, 77, 93; muscle, 49, 77, metabolic inhibitors, 3; references, 96. See also 80, 85 antimycin A, carbon monoxide, cyanide, lobster, American. See American lobster 2, 4-dinitrophenol, hydrogen cyanide, malonate, locust, desert. See desert locust potassium cyanide; also under effect locust, differential. See differential locust metabolism, intermediary, references, 97 locust, migratory. See migratory locust metamorphosis, control of, references, 96 locust. South American. See South American metathorax, effect of sex, 69, 78; effect of locust stage, 69; of American cockroach, 69, 78, 79; of nymph, 69, 93 Madeira cockroach, effect of removal of methods, biochemical and biophysical. See corpora allata, 63, 80; effect of sex, 63, continuous flow respirometer, fluorometric 77, 84; thoracic muscle, 63, 77, 80, 84 measurement, polarograph, spectrophotometer malate, 15, 19, 23, 35, 49, 55, 65, 71 methods, chemical, 5, 6. See also micro- Winkler, malonate, 15, 57, 67, 81, 93 tetrazolium, and Winkler methods Malpighian tubules, 93; effect of sex, 69; methods, manometric, references, 98. See of American cockroach, 67, 69 manometer manometer, 3, 5, 6, 17-19, 39, 55, 63. See methods, volumetric. See differential volumeter, also Barcroft, differential, Fenn, Thunberg, microvolumeter, Scholander-Wennesland and Warburg manometers microrespirometer, volumeter, volumetric manometric apparatus. See manometer microrespirometer manometric methods. See manometer methylene blue, 11-13, 82, 85 mantle, 93; central zone, 23, 29; edge, 23, 25; microrespirometer, 43. See also micro- effect of age, 25-27, 78; effect of cyanide, volumeter, Scholander-Wennesland 76; effect of 2, 4-dinitrophenol, 23; effect microrespirometer, Thunberg microres- of gas phase, 21, 39; effect of salinity, 29, pirometer, volumetric microrespirometer 86; effect of season, 27, 79; epithelium, 31 microsomes, 3, 4, 93; references, 98 inhibition by carbon monoxide, 31; inhibition micro-volumeter, 3, 5, 6, 35. See also by hydrogen cyanide, 29; light-reversible volumeter, volumetric microrespirometer inhibition by carbon monoxide, 21; lobe, 23, micro- Winkler method, 3, 5, 6, 21, 31, 39, 98 25; marginal zone, 23; muscle, 31, 39; midgut, effect of malonate, 57, 93; effect of of fresh-water mussel, 23-25, 77; of octopus, sex, 69; effect of suspending medium, 55; 39, 77, 83; of oyster, 21, 77; of Portuguese of American cockroach, 67-69; of Cecropia oyster, 25, 77, 78; of quahog, 27-29, 77-79, moth, 57; of larva, 55-57, 93; of silkworm, 86; of scallop, 31; of vineyard snail, 19; of 55; of vineyard snail, 19 Virginia oyster, 23; pallial zone, 23 midg-ut gland, 83, 85, 93; after estivation, 19; mantle nerve, effect of suspending medium, after hibernation, 19; during estivation, 19; 33, 37; giant nerve fibers, 35; of octopus, during hibernation, 19; effect of age, 25, 33, 37; of squid, 35 78; effect of cyanide, 76; effect of gas manure worm, body wall, 41, 79; gradient phase, 39; effect of sex, 45, 49-53, 77; along body, 41, 79, 86; succinoxidase, 79, 94; inhibition by carbon monoxide, 31; of blue viscera, 41, 79 crab, 45, 77; of fiddler crab, 53, 77; of marsh crab, gill, 53, 77; midgut gland, 53, ghost crab, 51, 77; of hermit crab, 47, 77; 77, 93 of Jerusalem land snail, 19; of kelp crab, mealworm, yellow. See yellow mealworm 53, 77; of lobster, 49, 77; of marsh crab, 53, medium, suspending, 3. See also artificial 77; of mud crab, 53, 77; of octopus, 37-39, sea water, Baldwin's phosphate solution, 77; of pearl oyster, 31, 77, 78; of Portuguese Belar-phosphate buffer, Belar's solution, oyster, 25, 77; of red-jointed fiddler crab, distilled water, isotonic chloride solution, 53, 77; of sea hare, 17, 83; of spider crab, physiological saline solution. Ringer's 49, 77; of spiny lobster, 53; of stone crab, INDEX 135

51, 77; of vineyard snail, 17-19, 77 of femur, 73, 80, 86, 92; of fleshfly, 71, 78; of migratory locust, muscle, 63 foot, 19, 31, 77; of fresh-water mussel, 21-25, mince, 3, 4, 37, 41-43 77; of giant water bug, 55, 77; of gizzard, 15, mitochondria, 3, 4, 19-21, 35, 47-49, 55-57, 92; of green crab, 45, 80, 84; of greenhouse 71-73, 85, 93; references, 99 stone cricket, 73, 80, 86; of heart, 17-25, mollusks, pelecypod. See pelecypod moUusks 29, 31, 77; of hind femur, 65, 92; oi honeybee, molt, 93 55; of horse ascarid, 13; of horseshoe crab, molt cycle, 84, 85; changes in integimnentary 45, 77; of house fly, 65; of leech, 43; of leg, tissue during, 47, 78, 84; muscle during, 47, 51-55, 63-69, 73, 77, 78, 86; of little edible 78, 84; in green crab, 47, 78, 84; in purple land snail, 17; of lobster, 49, 77, 80; of land crab, 47, 78, 84 Madeira cockroach, 63, 77, 80; of mantle, 31, molt-inhibiting hormone, 85 39, 77, 93; of manure worm, 41, 79; of molting, control of, references, 95, 96 mealworm, 73, 77; of migratory locust, 63; morphology, subcellular, references, 99, 100 of mud dauber wasp, 71; of mussel, 29; of moth, Cecropia. See Cecropia moth nematodes, 82; of nymph, 71, 78, 86, 93; of moth, codling. See codling moth octopus, 39, 77, 83; of oyster, 21, 31, 77; of moth, Polyphemus. See Polyphemus moth parchment worm, 39; of pearl oyster, 31, 77; moth, wax. See wax moth of pen shell, 33; of pig ascarid, 11-13; of moths, saturniid. See saturniid moths pink shrimp, 53; of Portuguese oyster, 25, mud crab, effect of sex, 53, 77; gill, 53, 77; 77, 78; of prawn, 53; of quahog, 27-29, 77-79, midgut gland, 53, 77, 93 86; of red-legged grasshopper, 65; of scallop, mud dauber wasp, flight muscle, 71 31; of sea cucumber, 73; of sea hare, 15-17; muscle, adductor, 21, 23-27, 31-33, 77-79, of shrimp, 51, 53, 80; of South American 86, 5i;coxal, 55, 63, 67, 73, 77, 78, 91; locust, 73, 77; of spiny lobster, 53; of squid, during molt cycle, 47, 78, 84; effect of age, 35; of striped shore crab, 51; of thorax, 63, 25-27, 57, 67-71, 78, 86; effect of antimycin 71, 77, 78, 80; of trematode, 82; of vineyard A, 67, 76, 91; effect of cyanide, 76; effect of snail, 17-19, 77; of Virginia oyster, 23, 78; 2, 4-dinitrophenol, 13, 75, 92; effect of eye- of water scavenger beetle, 63, 77; of white- stalk extract, 45, 51, 80, 85, 92; effect of lipped edible land snail, 19; of wing, 69-71, eyestalk removal, 45-51, 80, 85; effect of 86; pink, 69-71, 86; red, 27-31; respiratory gas phase, 21, 39, 41-43; effect of hydrogen quotient, 57, 65, 93; retractor of foot, 29, cyanide, 29; effect of injury, 73, 80, 86; 33, 93; smooth, 23-25, 43; striated, 23-25; effect of ionic concentration, 17, 29; effect of white, 17, 21-23, 27, 31-33, 69; yellow, 21 latitude, 53; effect of potassium cyanide, 15; mussel, effect of 2, 4-dinitrophenol, 75; effect effect of removal of corpora allata, 63, 91; of gas phase, 29; effect of ionic concentration, effect of salinity, 29, 79, 86; effect of 29, 79, 86; effect of suspending medium, 29; season, 21, 27, 79; effect of sex, 63-73, gill, 23, 29, 75; heart, 29, 79, 86; inhibition 77, 78; effect of stage, 69-71, 78, 86; effect by carbon monoxide, 29; respiratory quotient, of surgery, 45-47, 63, 73, 80, 85, 86; effect 23, 93 of suspending medium, 11-13, 17, 29; effect mussel, edible. See edible mussel of temperature, 53; flight, 55-57, 63, 67, mussel, fresh-water. See fresh-water mussel 71-73, 77, 78, 86; gray, 23, 31-33; light- reversible inhibition by carbon monoxide, 21; nematode, 82 of American cockroach, 65-69, 77, 78, 86; of nerve, effect of cyanide, 76; effect of ionic ark shell, 31; of Australian rock oyster, 33; concentration, 39, 79, 86; effect of sex, 69; of black blowfly, 71, 78; of blue worm, 43, effect of suspending medium, 33, 37, 39, 51; 79; of bluebottle fly, 57, 78, 86; of body wall, effect of temperature, 43, 79, 80; giant 13, 19, 41-43, 79; of buccal mass, 15-19, axons, 35, 92; of American cockroach, 91; of clam, 27; of codling moth, 57, 77; of 67-69; of American lobster, 47-49; of blue columella, 19, 91; of conch, 17; of dented crab, 45; of claw, 43-49, 79, 86; of crayfish, garden snail, 17; of differential locust, 65; 45; of cuttlefish, 39, 79, 86; of earthworm, 43; of earthworm, 43; of edible mussel, 29; of fin, 35; of horseshoe crab, 43-45, 79, 80, 87; 136 TISSUE RESPIRATION IN INVERTEBRATES

of leg, 45-53; of mantle, 33, 37, 93. of oyster, Australian rock. See Australian rock octopus, 33, 37, of sea hare, 15; of spider oyster crab, 49-51, 79, 86; of spiny lobster, 53; oyster, pearl. See pearl oyster of squid, 35; optic, 43-45, 79, 80, 87; oyster, Portuguese. See Portuguese oyster ventral nerve cord, 43, 47, 67, 69 oyster, tree. See tree oyster neuroendocrine systems, references, 99; in oyster, Virginia. See Virginia oyster crustaceans, 95; in insects, 97; in invertebrates, 97 pallial, 93 neurohormones, references, 99. See also pallial nerve. See mantle nerve hormones parchment worm, muscle, 39 neurosecretion, references, 99 particle preparation, 15-17, 83 neurosecretory systems, references, 99 particle suspension, 17, 39 night crawler. See earthworm particulate fraction, 3, 4, 13, 21, 65, 83, 93, 98 nitrogen, 21, 37, 43 parts of organ or tissue, 1, 3, 4, 29, 31 nitrogen determination, 21, 55, 59-63, 67, peacock worm. See feather- duster worm 71-73 pearl oyster, adductor muscle, 31, 91; effect nuclear fraction, 3, 47 4, of cyanide, 76; effect of 2, 4-dinitrophenol, 75; nymph, 93; effect of sex, 71; fat body, 55, effect of gas phase, 31; effect of season, 31, 71, 92; leg muscle, 71, 86; metathorax, 79; epithelium, 31; foot muscle, 31, 77; of 69; American cockroach, 69-71, 86; gill, 31, 77, 79; gonad, 31; inhibition by carbon of German cockroach, 55; of house monoxide, 31; midgut gland, 31, 77, 93 cricket, 55; wing muscle, 71, 86 pedal ganglion, of vineyard snail, 19 pedal retractor, 93; effect of temperature, 29; octopus, 83; branchial gland, 39; effect of of edible mussel, 29; of pen shell, 33 gas phase, 37-39; effect of suspending me- pelecypod moUusks, effect of age, 78, 84; dium, 33, 37; eye, 37; gill, 39, 77; heart, 39, effect of season, 86 77; kidney, 39; light- reversible inhibition pen shell, pedal retractor muscle, 33, 93; by carbon monoxide, 37; mantle, 39, 93; posterior adductor muscle, 33, 91 mantle muscle, 39, 77, 83; mantle nerve, perienteric, 93 33, 37; midgut gland, 37-39, 77, 93; perienteric fluid, of pig ascarid, 13 optic ganglion, 37-39, 77; salivary gland, peroxidase, 82 37-39; stellate ganglion, 33; tentacles, petit-gris. See dented garden snail 39, 83 phase, gas. See air, carbon monoxide, oxygen; optic ganglion, effect of gas phase, 39; also under effect of octopus, 37-39, 77 phenol, 9 optic nerve, effect of temperature, 43, 79, 80; ;?-phenylenediamine, 17, 39, 49, 55, 93 gradient along nerve, 79, 80, 87; of phosphate solution, Baldwin's. See Baldwin's horseshoe crab, 43-45, 77, 79, 80, 87 phosphate solution orange, sea. See sea orange phosphorylation, oxidative, 93; references, 99 optical density, 93 phosphorylation quotient. See P/O ratio organ, whole, 1, 3, 4, 15-25, 29-39, 43-53, photoreversible inhibition, 21, 37 57, 65, 69, 73 physiological saline solution, 13 oxaloacetate, 82 physiology, references, comparative, 99; oxidase, terminal, 81-83 general, 99; in crustaceans, 95; in insects, 97; oxidative phosphorylation, 93; references, 99 in invertebrates, 97 oxygen, 13, 21, 29-31, 37-39, 43-45, 73, pieces of organ or tissue, 1, 3, 4, 21-33, 43-45 82-84, 91 87, pig ascarid, effect of 2, 4-dinitrophenol, 13, 75; oxygen cathode, 35 muscle, 11-13; perienteric fluid, 13 oyster, effect of cyanide, 76; effect of gas pink shrimp, dorsal extensor abdominal muscle, phase, 21, 75; gill, 21, 77; heart, 21, 53; effect of latitude, 53; effect of temperature, 31, 77; light-reversible inhibition by carbon 53 monoxide, 21, 75; mantle, 21, 77, 93 P/O ratio, 13, 21, 49, 57, 63, 89, 93 INDEX 137

92; of larva, 57, 93; of muscle, 57, polarograph, 5, 6, 21, 43, 93, 98 body, 57, Polyphemus moth, pupa, 73, 93; wing, 73 65; of mussel, 23; of quahog, 27 comparative, 76-78, 83 pond snail, albuminous gland, 21, 91 respiratory rates, Portuguese man-of-war, effect of cyanide, 76; respiratory tree, 91 pedal retractor tentacles, 11 retractor muscle of foot, 93; See Portuguese oyster, effect of age, 25, 78, 84; Ringer's solution, 45 respiratory quotient gill, 25, 77, 78; mantle, 25, 77, 78, 93; midgut R.Q. See gland, 25, 77, 78, 93; muscle, 25, 77, 78 worm potassium cyanide (KCN), 15, 47, 59-61, sabellid worm. See feather-duster 67-71 sac, dart, of vineyard snail, 19 prawn, dorsal extensor abdominal muscle, 53; saline solution, physiological, 13 effect effect of temperature, 53. See also shrimp salinity, effect of. See under phase, 37-39, 75; preparation, particle, 15-17, 83 salivary gland, effect of gas carbon monoxide, protein determination, 35, 47-49, 55-57, light-reversible inhibition by 69-73 37, 75; of octopus, 37-39 prothorax, of American cockroach, 69, 79 sarcoplasm, 65 93. See also pupa, 93; effect of injury, 82, 83, 86; epithelium, sarcosomes, 57, 63, 71, 81, 59-63, 78, 82; heart, 82; of Cecropia moth, mitochondria moths, 83 5, 57-63, 78, 82, 83; of Polyphemus moth, 73; saturniid gill, 31; mantle wing, 57-63, 73, 78, 82 scallop, adductor muscle, 31, 91; purple gorgonian, 11; effect of cyanide, 76 muscle, 31, 93 micro-respirometer, 51 purple land crab, during molt cycle, 47, 78, 84; Scholander-Wennesland tentacles, 11 effect of eyestalk removal, 85; integumentary sea anemone, effect of cyanide, 76; tree, 73, 91; intestine, tissue, 47, 78, 84 sea cucumber, branchial purple sea fan, branches, 11; effect of cyanide, 76 73; muscle, 73 See purple sea fan pyruvate, 9, 13, 37, 65 sea fan, purple. sea hare, buccal mass muscle, 15-17, 83, 91; cyanide, gizzard, 15, quahog, adductor muscle, 27-29, 77-79, 86, 91; effect of potassium 15; gland, 17, 83, 93; muscle, effect of age, 27, 78, 84; effect of cyanide, 83, 92; midgut 27-29, 76; effect of salinity, 27-29, 79, 86; 15-17, 83; nerve, 15 of cyanide, 75 effect of season, 78, 79; effect of temperature, sea orange, 11; effect water, 27-29, 39, 49; artificial, 15, 29, 27; gill, 27, 77-79, 86; mantle, 27-29, 77-79, sea 21, 86, 93; respiratory quotient, 27, 93 33, 45, 49-51 under effect quinol, 39, 93. See also hydroquinone season, effect of. See sections, thin, 1, 3, 4, 27 effect radula, 93 sex, effect of. See under 27-31, 39, 73 rates, comparative respiratory, 76-78, 83 sheets, thin, 1, 3, 4, 17, shell ratio, P/0, 13, 21, 49, 57, 63, 89, 93 shell, pen. See pen shore crab red-jointed fiddler crab, effect of sex, 53, 77; shore crab, striped. See striped of eyestalk extract, 51, 80, 85, gill, 53, 77; midgut gland, 53, 77, 55 shrimp, effect red-legged grasshopper, hind femur, 65, 92; 92; effect of eyestalk removal, 51, 80, 85; prawn muscle, 65 muscle, 51, 80, 85. See also red oyster sponge, effect of insulin, 9 shrimp, pink. See pink shrimp medium, 55; references, 95-100 silkworm, effect of suspending respiration, cyanide-insensitive, 47, 78, 80, 84; larva, 55, 93; midgut, 55 respiration, endogenous, 9-57, 63-73, 76, 78-84, sinus gland extract, 85 effect of age 86, 92 size, effect of. See respiratory data, 99 Slater factor, 93 9-11, respiratory enzymes, references, 96 slices of organ or tissue, 1, 3, 4, 76, 83, 98 respiratory quotient, 93; of American 15-19, 27, 31, 37-45, 53, 73, 75, mussel, 23-25; cockroach, 65; of codling moth, 57; of differ- smooth muscle, of fresh-water ential locust, 65; of earthworm, 43; of fat of leech, 43 138 TISSUE RESPIRATION IN INVERTEBRATES

snail, during activity, 19; during hibernation, substrates. See under individual name of 19; heart, 17 substrate snail. Burgundy. See vineyard snail subumbrella, 82, 94 snail, dented garden. See dented garden snail succinate, 11-13, 19, 23, 33-35, 39-51, snail, Jerusalem. See Jerusalem land snail 55-59, 63-73, 80 snail, little edible land. See little edible land snail succinic acid, 41 snail, pond. See pond snail succinic dehydrogenase, 81, 82, 92 snail, vineyard. See vineyard snail succinoxidase, 79, 86, 87, 94 snail, white-lipped edible land. See white- sucrose, 55 lipped edible land snail supernatant, 3, 4, 13, 47 soft-shelled clam, gill, 29 surgery, effect of. See under effect soluble fraction, 65 suspending medium, 3. See also artificial solution, Baldwin's phosphate, 17-19; isotonic sea water, Baldwin's phosphate solution, chloride, 17-19, 29, 39, 45, 55; physiological Belar-phosphate buffer, Belar's solution, saline, 13 distilled water, isotonic chloride solution, South American locust, coxal muscle, 73, 77, physiological saline solution. Ringer's 91; flight muscle, 73, 77; leg muscle, 73, 77 solution, Wilder and Smith saline, sucrose; spectrophotometer, 3, 5, 6, 15-19, 23, 35, also under effect 47-49, 59-63, 67-71, 93, 98 suspension, 3, 4, 19, 63 spectroscopy, 5, 82 suspension, cell. See cell suspension spider crab, claw nerve, 49, 79, 86; effect of suspension, particle. See particle suspension ionic concentration, 49, 79, 86; effect of sex, symbols, 89, 90; chemical, 89 49, 77; effect of suspending medium, 51; systems, neuroendocrine, references, in gill, 49, 77; leg nerve, 51; midgut gland, 49, crustaceans, 95; in insects, 97; in inverte- 77, 93 brates, 97 spiny lobster, effect of cyanide, 76; leg

muscle, 53; leg nerve, 53; midgut gland, teased tissue, 3, 4, 51, 55, 63-67, 73, 84 53, 93 temperature, effect of. See under effect sponge, 9, 11, 81; effect of cyanide, 75. See tentacles, effect of cyanide, 76; of feather- also sea orange duster worm, 39; of jellyfish, 11; of octopus, sponge, fire. See fire sponge 39, 83; of Portuguese man-of-war, 11; of sponge, red oyster. See red oyster sponge sabellid, 39; of sea anemone, 11 sponge, stinker. See stinker sponge terminal oxidase, 81-83 squid, cerebral ganglion, 37; effect of testes, of American cockroach, 67 cyanide, 76; eye, 33; fin nerve, 35; giant tetrazolium method, 19

axons, 1, 35-37, 92; gill, 33; heart, 37; thin sections of organ or tissue, 1, 3, 4, 27 mantle nerve, 35; muscle, 35; stellate thin sheets of organ or tissue, 1, 3, 4, 17, ganglion, 35 27-31, 39, 73 stage, effect of. See under effect thoracic muscle, effect of removal of corpora stellar nerve, 94. See mantle nerve allata, 63, 80, 91; effect of sex, 63, 71, 77, stellate ganglion, effect of suspending 78; of fleshfly, 71, 78; of Madeira cockroach, medium, 33; of octopus, 33; of squid, 35 63, 77, 80 stinker sponge, 9; effect of cyanide, 75 thorax, effect of sex, 69; effect of stage, 69; stone crab, effect of sex, 51, 77; gill, 51, 77; gradient along body, 69, 79, 87; of American midgut gland, 51, 77, 93 cockroach, 69, 79, 87; of nymph, 69, 93 stone cricket, greenhouse. See greenhouse Thunberg manometer (Thunberg microrespiro-

stone cricket meter, Thunberg respirometer), 3, 5, 6, 23, stone cricket, Japanese. See greenhouse 27, 31-33, 49, 94, 98 stone cricket tissue, during molt cycle, 47; integumentary, striped shore crab, brain, 51; leg muscle, 51; 47; of purple land crab, 47 strips of organ or tissue, 3, 4, 21-23 TPN, 89, 94 subcellular morphology, references, 99, 100 tree, branchial. See branchial tree INDEX 139 tree oyster, effect of cyanide, 76; gill, 25 Warburg manometer, 3, 5, 6, 9-33, 37-57, trematode, 82 63-73, 94, 98 tricarboxylic acid cycle, 94. See citric acid wasp, mud dauber. See mud dauber wasp cycle water, artificial sea, 15, 29, 33, 45, 49-51 triphosphopyridine nucleotide (TPN), 94 water, brackish, 45 tyrosinase, 82 water, distilled, 13, 55 water, sea, 21, 27-29, 39, 49 water bug, giant. See giant water bug ultracentrifugation, 98 water scavenger beetle, coxal muscle, 63, 77, 91; umbrella of jellyfish, 11, 82, 94 flight muscle, 63, 77; leg muscle, 63, 77 urea, 15, 33, 37, 51 wax moth, greater. See greater wax moth white-lipped edible land snail, heart, 19 43-53. ventral nerve cord, effect of cyanide, 76; whole organ, 1, 3, 4, 15-25, 29-39, 57, effect of sex, 69; of American cockroach, 65, 69, 73 73 67-69; of American lobster, 47; of Wilder and Smith saline, 55, 63, 67, earthworm, 43 wing, effect of age, 69-71, 78; effect of antimycin versene (ethylenediaminetetraacetic acid; A, 61, 76, 91; effect of sex, 69-71; effect of 69-71, 78, 82; epithelium, 59-63, EDTA), 55, stage, 59-63, cockroach, vineyard snail, 83; albuminous gland, 19, 91; 78, 82; muscle, 69-71; of American 57-63, of develop- body wall, 19; buccal mass muscle, 19, 91; 69-71; of Cecropia moth, 78; of cerebral ganglion, 19, 77; columella muscle. ing adult, 59-63, 78, 82; of nymph, 71, 93; of pupa, 57-63, 73, 78, Id, 91; dart sac, 19, 92; effect of Polyphemus moth, 73; 2, 4-dinitrophenol, 75, 92; esophagus, 19; 82, 93 effect female duct, 19; foot, 19, 77; heart, 17; wing muscle, effect of age, 69-71, 78, 86; of hibernation, 19; kidney, 19; mantle, 19, 93; of sex, 69-71; effect of stage, 69-71, 78, 86; of nymph, midgut, 19, 77; midgut gland, 17-19, 93; American cockroach, 69-71, 78, 86; 69-71. pedal ganglion, 19 71, 78, 86, 93; pink, 69-71, 86; white, Virginia oyster, adductor muscle of, 23, 78, 91; See also flight muscle effect of age, 78, 84; effect of cyanide, 76; Winkler method, 3, 5, 6, 29, 94. 98 effect of dinitrophenol, 23, 75, 92; mantle, worm, blue. See blue worm 23, 75, 93 worm, earth. See earthworm viscera, gradient along body, 41, 79; of worm, feather-duster. See feather-duster manure worm, 41, 79; succinoxidase, 19,94 worm mealworm volumeter, 94, 98. See also differential worm, meal. See yellow volumeter, microvolumeter, Scholander- worm, parchment. See parchment worm Wennesland microrespirometer, volumetric worm, peacock. See feather-duster worm worm micro respirometer worm, sabellid. See feather-duster volumetric apparatus. See differential volu- worms, clitellate, 41, 43 meter, Scholander-Wennesland microrespir- fat body, ometer, volumeter, volumetric microres- yellow mealworm, effect of sex, 73, 78; pirometer 73, 92; flight muscle, 73, 78; larva, 73, 93; volumetric methods. See volumetric apparatus leg muscle, 73, 78 volumetric microrespirometer, 3, 5, 6, 51, 55, or tissue, 3, 4, 23-25, 45 63, 67, 73, 98 zones of organ

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