BACTERIOLOGICAL REVIEWS, Sept. 1965 Vol. 29, No 3Copyright @ 1965 American Society for Microbiology Printed in U.S A

Symposium on Microbial InsecticidesIV. Diseases of Invertebrates Other Than Insects,

EDWARD A. STEINHAUSDivision of Biological Sciences, University of California, Irvine, California

INTRODUCTION.................................................................. 388ECONOMIC IMPORTANCE........................ 388Protozoa..................................................................... 389Porifera........................ 389Coelenterata........................ 389Ctenophora........................ 389Platyhelminthes........................ 389Aschelminthes........................ 389Bryozoa and Echiuroidea........................ 390Echinodermata........................ 390Mollusca..................................................................... 390Annelida........................ 391Arthropoda................................................................... 391

DISEASES AND ABNORMALITIES ........................ 391SUGGESTIONS FOR PROGRESS........................ 393LITERATURE CITED........................ 395

INTRODUCTIONThe same factors which in recent years moti-

vated the acceleration of research in insectpathology-both basic and applied-will soon, Iam sure, be motivating an increase in research onthe diseases of all other major groups of inver-tebrates. I should simply like to highlight thisconviction and to call attention to some of thesteps that might be taken to increase our knowl-edge of, and enhance research in, invertebratemicrobiology and invertebrate pathology gener-ally. From an applied standpoint, these mattersmay be considered against a background of theeconomic importance of invertebrates.At the risk of enumerating well-known general-

izations, I should like to repeat a few basic factsand convictions which serve as a framework forthe comments to follow. First, it is importantto keep in mind that invertebrates constitute97%0 of the known animal species on earth (1),and, although of this number of species some-where between 70 and 80%c are insects, thisstill leaves a tremendous variety and body oflife to consider from any aspect. Second, exceptfor isolated examples, we know virtually nothing

1 A contribution to the symposium "MicrobialInsecticides," presented at the Annual Meeting ofthe American Society for Microbiology, Washing-ton, D.C., 7 May 1964, under the sponsorship of theDivision of Agricultural and Industrial 1\icro-biology, with Harlow H. Hall as convener and Con-sultant Editor.

of the nature, extent, and importance of disease-both infectious and noninfectious-in noninsectinvertebrates. If the same intensity of researcheffort that in recent years has been brought tobear on the diseases of insects can be directedtoward the diseases of other invertebrates, it iscertain that the results will be abundant andrewarding. Third, comparative pathologists arecoming to the realization that considerable lightcould be shed on the phylogenetic evolution ofdisease as a biological process by including intheir consideration the study of disease in allgroups of invertebrates. The fruits of such studiesand the contributions to our knowledge of patho-gens and of the diseases they cause in man andother vertebrates, as well as in plants, are ob-vious. And fourth, because of the economic im-portance of both beneficial and destructive in-vertebrates, the economic importance of the useof disease agents in control of invertebrates andthe suppression of diseases in beneficial inverte-brates parallel the situation we have in insects.

ECONOMIC IMPORTANCE

In considering possible applications, such asthe microbial control of pests and the suppressionof disease in beneficial forms, it is appropriatethat we indicate, at least in a cursory manner,the economic importance of invertebrates otherthan insects. The economic importance of insectsis so well known and obvious that it is pointlessto discuss it here. Perhaps the same cannot be

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said with regard to that of most other inverte-brates. Unfortunately, space limitations makeit necessary to avoid, in this discussion, anequally important emphasis that could be giventhe potentialities of invertebrates as experi-mental animals, and their importance in the''economy of nature."The simplest way, it seems to me, in which to

present a thumbnail sketch of the economicimportance of invertebrates other than insectsis to comment briefly in this regard upon theprincipal phyla concerned, rather than to citemasses of statistics and numerical data; a ratherpedantic approach, to be sure, but under the cir-cumstances the most saving in time and in dis-traction from the main points I wish to make.Let us begin with the lowest forms and proceedphylogenetically in accordance with a com-monly accepted textbook arrangement of thephyla concerned, such as that used by Storerand Usinger (9), whose book, along with others(e.g., 2, 3, 4, 10), was also used to obtain someof the following statements concerning the im-portance of invertebrates.

ProtozoaIt is unnecessary to elaborate on the economic

importance of members of the phylum Protozoa.These unicellular animals, ranging from obligateparasites to obligate mutualists, are so wellknown for the disease and harm they cause, aswell as the good they do, that it is meaninglessto comment on their economic importance, atleast as far as our present purposes are concerned.Whether one wishes to consider the protozoaamong the higher Protista, as most specialistsnow do, or as the lowest animals, they deserveconsideration because they are known to be sub-ject to infection by certain parasitic bacterialikeorganisms; they also harbor microorganisms inan apparent mutualistic relationship.

PoriferaCertain of the sponges, both "fished" and

farmed, have long served man for such commonusage as that of a bath and cleansing sponge tothat of serving as a source of iodine, fatty acidsof high molecular weight, cholinesterol, andother products. They are also sometimes enemiesof oysters, and a nuisance to fishermen in imped-ing trawling operations in certain areas of theworld such as in the Gulf of Mexico. A few spe-cies, such as the fire sponge in Florida, are irritat-ing to the skin. In 1938 the annual world pro-duction of sponges was 1.1 million kg; however,because of the presence of a fungus disease, aswell as through the advent of synthetic sponges,the production has fallen to about 0.4 million kg.

CoelenterataAmong the coelenterates, certain species of

jellyfish serve as food for man, others giveshelter to the young of commercially importantfishes, and others constitute part of the impor-tant plankton of the sea. On the negative sideshould be recorded the fact that some jellyfishin some parts of the world constitute a nuisanceto bathers. Hydras may constitute a pest inhatcheries where they kill significant numbers ofyoung fishes. At times these small fresh-waterhydrozoan polyps may infest fish nests in suchnumbers as to irritate the hands of fishermen,apparently by virtue of the nematocysts foundin these animals. Other hydroids are marine andcolonial, and include the stinging corals, stingingjellyfish, and stinging siphonophores, all ofwhich may injure swimmers. Sea anemones areused as food in some parts of the world. Truecoral is used for jewelry and decorative art, tosay nothing of the fact that they are reef buildersand today form natural harbors, provide waystations for air traffic, and constitute the basisof coral islands.

CtenophoraThe ctenophores are common marine plankton

organisms. They are known to devour greatnumbers of oyster larvae; they may also feedon larvae of certain mollusks and crustaceans,fish eggs, and small fish. Other than this, andthe role they play in the food chain of marinelife, they are of minor direct economic impor-tance to man.

PlatyhelminthesThe flatworms, which include the free-living

forms as well as flukes (external internal para-sites) and tapeworms (intestinal parasites ofvertebrates), are of great economic importance.This importance derives primarily from theharm they cause to man and to his domesticanimals through their parasitic habits. Of course,undomesticated animals, such as fish, rats, mice,wolves, and other vertebrates, also serve as hosts,both primary and intermediate. Sometimes, aswith certain fish tapeworms, invertebrates (e.g.,copepod crustaceans) are infested with somestages of the worms.

AschelminthesMlany authors include in this phylum the

classes Rotifera, Gastrotricha, Kinorhyncha,Nematoda, Nematomorpha, and Acantho-cephala. (The last-named is frequently consid-ered as a separate phylum.) Some of thesegroups are obviously of great economic impor-

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tance, as for instance the Nematoda. In fact,the economic importance of this class is difficultto overestimate. It includes those unsegmentedroundworms that cause serious diseases (hook-worm disease, trichinosis, filariasis, and others)in man. Other vertebrates, as well as inverte-brates, are also attacked by nematodes. Manyspecies pathogenic for insects are known, andsome slight progress has been made in usingnematodes to control insect pests. Many speciesof nematodes live in or about the roots of plants,and cause tremendous economic losses. Theannual crop losses caused by nematodes in Cali-fornia alone has been estimated at about 150million dollars per year. Less is known of theeconomic importance of the other classes of thephylum Aschelminthes, but we might mentionthat insects (as well as crustaceans, mollusks,diplopods, and other invertebrates, and certainvertebrates) are known to be attacked by spiny-headed worms (Acanthocephala) and by Nema-tomorpha. To be sure, from the economic stand-point, it should be remembered that not allspecies of insects attacked are harmful to man'sinterest; some species are distinctly beneficialand others fall in between. Certain members(e.g., Rotifera) of the phylum also are planktonanimals and are an important link in the foodchain in fresh waters, and especially serveas food for certain small worms and crustaceans.On the other hand, they have a purifying orcleansing effect on water by feeding on smallorganisms and bits of organic debris.

Bryozoa and EchiuroideaFreshwater species of these so-called "moss

animals" are capable of growing in water pipesto an extent that they may clog the pipe or ob-struct the flow of water. Because many speciesof Bryozoa have had a short geological historybut wide geographic distribution, their exo-skeletons are useful in correlating geologicalstrata. Thus, they are of economic importancein studying the cores brought up in drilling testwells for petroleum. Certain large species ofpeculiar worms (echiurids) serve as bait for codin Belgium and north Germany.

EchinodermataThe economic importance of echinoderms is

varied. Certain species of sea cucumbers are usedin large numbers by man as food (both dried andfresh); they are highly nutritious animals, con-sisting of 35 to 65% protein. Other species of seacucumbers are used as fertilizer, and still othersare useful because the poison (holothurin) theyproduce is effective in poisoning fish which are

then easily captured and used as food. Thispoison, in nonlethal doses, is known to reducerapidly and effectively sarcomas implanted inmice.

Asteroids, or starfish, are predators of oystersand clams. Indeed, these echinoderms areamong the greatest enemies of beds of oystersand clams, destroying annually millions ofdollars' worth of these valuable food animals.Starfish also feed on crustaceans, tube worms,and other invertebrates; on occasion, they de-vour small fish caught by the tube feet andpassed to the mouth.The gonads of echinoids, particularly sea

urchins, raw or roasted in the half-shell, areeaten by people of the Mediterranean region,South America, West Indies, and New Zealand,and formerly by American Indians. The Mar-seilles fish market alone handles over 100,000sea urchins a year. However, their importanceas food is far exceeded by the usefulness of seaurchins as materials for scientific research; theyare important experimental animals. An in-delible ink has been derived from certain speciesof sand dollar. On the harmful side it should bementioned that some echinoids (Strongylocen-trotus) damage steel pilings by their boringactivities. The common green sea urchin, also aStrongylocentrotus, is occasionally caught intrawls in large quantities, and the handling ofsuch large numbers is, because of a poison se-creted by the animal, irritating to the hands offishermen. Species of the genus Toxopneustessecrete such a potent poison that they aredreaded by fishermen; occasionally they arefatal for man.

MolluscaThere is no question but that, from an eco-

nomic standpoint, mollusks constitute one ofthe most important groups of invertebrates.Their value includes their use in serving ashuman food, the manufacture of buttons, andthe production of pearls. The study of theirshells (conchology) is a pleasant hobby as wellas a science. They also feed on cultivated plants,serve as intermediate hosts for parasitic worms,and damage wooden ships and wharves. Amongthose best known for their use as food are clams,oysters, abalone, snails, mussels, scallops, cockles.and squids and other cephalopods. The com-mercial value of these invertebrates as food(both "farmed" and "fished") is difficult toestimate, but it is obviously several hundredmillions of dollars a year. The combined value ofmollusks as fish bait, poultry food, jewelry,cutting tools, containers, souvenirs, and even

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as monev is truly great when considered on theworld scene. On the other hand, the existence ofsome of them is costly to man. Certain speciesof snails and slugs cause great agricultural lossesin certain parts of the world. The role played bycertain snails in harboring, for part of their lifecycles, flukes parasitic for man is highlighted bythe tremendous importance of schistosomiasisas a factor in the health of human beings in manyparts of the world. The loss in labor alone causedby this and similar diseases is incalculable.

Annelida

There exist more than 2,000 known species ofearthworms-the best-known annelids. Someof them are used as bait for fishing, and for thispurpose they are reared commercially in largenumbers. According to Storer and Usinger (9),ancient medical writers mention irrational usesof earthworms in human medicine, and some ofthese are still followed in parts of the Orient.In nature, practical value accrues from the largeturnover of soil by earthworms (especiallyLumbricus), which ingest the earth which passesthrough the digestive tract and is deposited onthe ground surface as small mounds of feces or"castings." An average earthworm produces itsweight in castings every 24 hr. The castings maybe a nuisance on lawns and golf greens. CharlesDarwin estimated that in favorable locationsearthworms may bring up 18 tons of soil peracre in a year. Westcott (11) mentioned that theirbeneficial action in soil goes much deeper thanany man-made spade, plow, or rototiller. Ap-proximately 10 tons of "perfect" soil is producedby a population of 50,000 specially bred earth-worms per acre. Although, according to West-cott, it is said that these annelids double thegrowing rate of young nursery trees and theharvesting rate of strawberries, Storer and Usin-ger stated that such claims are not true. In anycase, it is quite clear that worm cultivation ishelpful by turning over topsoil, allowing airand water to penetrate. Also, the depth of arabletopsoil in less fertile areas may be graduallyincreased by the worms. On rare occasions, theburrows may cause water seepage through irriga-tion ditches or enhance soil erosion on slopinglands. Another oligochaete (Tubifex) lives intubes on bottom muck; they probably aid inpurifying such waters. A polychaete (Eunice)casts off its posterior sexual segments, whichswarm at the surface of the sea. These are highlyprized as food by the natives of Samoa and Fiji.Earthworms serve as intermediate hosts for a

cestode of fowls and a lungworm of pigs. Thelatter parasite carries a virus that, in combina-

tion with a bacterium, causes swine influenza.Earthworms are also possible carriers of thegapeworm of fowls.

Another class of annelids, Hirudinea or leeches,have been used medically for "blood-letting,"and are sometimes used as fish bait. Leeches arepredatory, parasitic, or scavenging. The blood-sucking species attack various vertebrates, fromfish to man. In North Temperate regions theymay be a nuisance to persons wading or bathingin some waters, but they seldom cause seriousharm. The land leeches of southeastern Asia andneighboring islands are very abundant, and thesesometimes do cause severe injury to humanbeings.

ArthropodaOmitting the insects still leaves a great re-

mainder of arthropods that are of great economicimportance to man. Indeed, it would be futile toattempt any detailed review of the subject here.All major classes of the phylum are of economicimportance. They are highly esteemed as food(shrimp, crab, lobster, crayfish), to an amount ofover $100,000,000 annually in the United Statesalone. Some arthropods (scorpions, certainspiders) are directly poisonous and dangerous toman; others (phytophagous mites, sowbugs,millipedes) are pests of agricultural crops; others(ticks, mites, crayfish) are vectors or inter-mediate hosts of pathogens of man and otheranimals; others (certain copepods) directly para-sitize animals such as fish, prawns, and crabs;and still others (iospods) damage wharves andmarine buildings by their burrows. On the bene-ficial side, in addition to serving as food forhumans, some are important as predators onharmful insects, some are important constit-uents of sea plankton, some serve as food forfish and other sea animals that are important toman, some are useful as fish bait, and some areuseful as scavengers.

DISEASES AND ABNORMALITIESAlthough it has taken considerable time merely

to indicate, in the briefest and most cursorymanner, the economic importance of inverte-brates other than insects, much more could besaid on this subject. Moreover, I have ignoredthe potential economic importance of inverte-brates-especially that of the marine forms whichwill gain in importance as man learns to "farmthe seas." My reason for dwelling on the eco-nomic importance of the noninsect invertebrateswas to emphasize the worthwhileness of studyingtheir diseases, as we do those of insects. Thesedays it seems that unless we make this type of

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emphasis we have difficulty in securing adequatesupport budgets, in receiving the understandingof administrators and the public to both of whomwe must look for this support, and in obtainingthe interest of those who may be commerciallyinvolved. The justification of invertebrate pa-thology on other bases-such as what it teachesus of life and death, of the effect of disease onpopulations, of the use of invertebrates as ex-

perimental animals or as systems in the study ofpathological processes, of the nature of the path-ogens involved and of how learning of these wemight learn more about those that cause diseasesin man and other vertebrates-unfortunately,justification on these scientific rather thandirectly economic bases does not seem to gain usmuch even though it includes the highest ofmotivations.

In spite of the overall neglect of the study ofdisease in invertebrates, enough is known to as-sure us that every phylum, every taxon, indeedundoubtedly every species of invertebrate ani-mal is subject to disease-including infectiousdisease-if we but made the effort and knew howto discern the malady. I could have reviewedthose diseases that have been recorded as affect-ing members of each of the invertebrate phyla,but this would have been premature to estab-lishing the justification for such a review. More-over, space limitations require that a review ofthe diseases be postponed to a later time, eventhough such a review is sorely needed.

Actually, relatively little attention is beingpaid to the diseases of common invertebratesother than insects. With certain exceptions, re-ports are spotty and are usually quite cursoryand superficial in nature, especially in view ofwhat modern techniques and methodology couldreveal. This is really quite puzzling because therelative simplicity of invertebrates as model sys-tems for the study of disease should yield greatdividends. When one considers the great benefitsto mankind that have come from the study ofvirus diseases of bacteria; the study in depth oftobacco mosaic in plants, and the knowledge ofviruses gained from this study; the use of viral,bacterial, and fungal models in biochemistry andgenetics; the initiation of our knowledge ofphagocytosis by MIetchnikoff's discovery thatcertain wandering cells in the body cavity of awater flea, a crustacean of the genus Daphnia,were capable of engulfing and destroying thespores of an infecting yeast; or this same man'suse of starfish larvae in discovering the origin ofmacrophages from fixed mesenchyma; the his-torical importance of the study of the diseasesof the silkworm by such men as Bassi, Pasteur,

and others-when one considers such examples ofpathology involving lower forms of life, it is sur-prising there is any need for justifying a plea forthe intensification of comparative invertebratepathology. Yet, except for insect pathology,there appears to be little incentive for the studyof disease in invertebrates generally.

It has been pointed out that it took virtuallyall of the first 50 years of this century to convincethe general medical world that tumors in labora-tory mammals are enough like those in man tobe worth studying. The same may be said ofother types of disease. Why the delay in makingintensive studies all the way up and down thephylogenetic scale? We know so little of thephylogenetic evolution of disease processes-yetthere is so much to be gained from such studies.At least part, and perhaps the major part, of

the answer to this puzzling inertia lies, I believe.in the fact that it is difficult to see the practicalapplications of such knowledge. Unlike the ex-amples of 'Metchnikoff's discoveries just men-tioned, most of the work on the diseases of insectshas been motivated by pragmatic reasons. To besure, the amount of basic research being done ininsect pathology is encouragingly extensive, but,in most cases if one digs far enough he finds itsjustification in the possible utility that may befound of this knowledge, particularly as it relatesto agriculture. And this is fine! But seekingknowledge for the sake of knowledge should bejustification enough.

I feel obliged to remember that the greatamount of work (both basic and applied) on themaladies of the silkworm and the honey beewas to preserve and save these insects from theravages of disease, and also that much of thework being done in insect pathology today isaccomplished in the hope that insect pathogensmay be used as an aid in the safe control of insectpests. And, therefore, I should like to suggestthat the diseases of other invertebrates bestudied for the same reasons: to prevent diseasein beneficial animals and to use pathogens todestroy those animals harmful to man's in-terests. This would be in addition to the inde-terminable value such knowledge will have inbetter understanding disease processes in general,thereby enabling man to better understand themaladies that afflict him, his crops, and hislivestock.

So far, most consideration given to the diseasesof noninsect invertebrates has been given to thoseattacking beneficial or useful invertebrates. Thus,when, as has happened, disease wipes out oysterbeds, kills shrimp and prawns, decimates earth-worms, or destroys important laboratory cultures

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of hydras, we seek therapeutic or preventivemeasures as our forefathers did in the case of thediseases attacking the silkworm and the honeybee. This application of invertebrate pathologywill, of course, continue.

I must admit that as of this day I know of nosuccessful control (or even serious attempts atcontrol) of a harmful noninsect invertebrate bymeans of microorganisms. Many such inverte-brates are known to be killed off in large numbersin nature by what appear to be infectious agents-and thus control or suppression of numbers iseffected in nature. Furthermore, the problemsinvolved in using microbial pathogens in certainsituations, such as in the sea, are as difficult asany that are presented to the entomologist at-tempting to control insect pests on land. Butthere are invertebrates and situations that appearto be ripe for serious consideration from thestandpoint of microbial control. Consider, forexample, the possibilities that exist in the micro-bial control of those gastropods, such as snailsand slugs, that in some parts of the world causegreat agricultural and garden losses, and whichare only partially and imperfectly controlled bychemical pesticides. If, in addition to the judi-cious use of chemicals, we could make skillfuland careful use of pathogens, the required effortand investment are likely to be minor comparedto the resulting benefits. In addition, knowledgeof the disease of agriculturally important snailscould be extended to those snails of medicaland public health importance, with tremendousbenefits accruing to the health and welfare ofmankind. At any rate, with the gastropods wehave a potentially promising group with whichto begin our consideration of the microbial con-trol of noninsect invertebrates.

SUGGESTIONS FOR PROGRESSTo make some headway into the sea of ig-

norance to which I have been alluding, I shouldlike to suggest several preliminary broad stepsthat might be taken, recognizing that much moresophisticated and specific projects could be sug-gested.

Although the literature of insect pathologyhas been well reviewed and evaluated, this hasnot been done in the case of the diseases of mostof the other invertebrates. Recently, I made aquestionnaire survey of representative inverte-brate zoologists and pathologists and found fewwho were willing to attempt to review the litera-ture, or even to scan it, for mention of diseasesand abnormalities of noninsect invertebratesother than mollusks and nematodes. Yet some-how this first step toward finding out "where weare" must be taken.

Laboratories and departments of insect pa-thology should be encouraged to extend their re-search programs into the area of invertebratepathology generally. For those units associatedwith agriculture, this can be done initially byassociating the research with the need to knowmore about the diseases of such agriculturallyimportant invertebrates as mites, sowbugs,snails, slugs, earthworms, and nematodes. Thoseagriculturally oriented research institutionsfortunate enough to be able to conduct genuinelybasic research can be assured that, whateverinvertebrate and disease are the bases of study,the research involved will likely make contribu-tions of eventual practical importance. Even inagriculture there is justification for work on thediseases of marine invertebrates, unless onewishes to assume the position, which I find un-tenable, that agriculture ends at the seashore.Aside from the future needs to "farm the seas,"the present food resources of the oceans haveagricultural justification, although I am quiteaware that most of the responsibilities in thisarea are assumed by "marine resources" agencies,departments, and institutions. From the stand-point of pathology, however, there has been(with a few noteworthy exceptions) little en-couragement from such agencies, or from marinestations generally, to study "what goes wrong"with marine invertebrates, whether they con-stitute a food source or not. This point assumesadded significance when considering Walford'sestimate that 90% of the mass of animal life inthe sea consists of invertebrates (12).

Medically oriented laboratories and researchinstitutes should not only increase their use ofinvertebrates as experimental animals, but shouldalso investigate the diseases of invertebrates forknowledge concerning the nature and activitiesof pathogens, the morphological and functionalchanges which occur in lower animals sufferingdisease, the mechanisms of resistance such ani-mals have to microbial infections, and the valueof studying type diseases throughout the entirephylogenetic scale. The same rewards could ac-crue to veterinary medicine as to human medi-cine. The relative simplicity of the model systemsinvolved in disease in an invertebrate comparedto those in a vertebrate should afford investi-gators of disease of vertebrate animals ad-vantages and opportunities now being lost (5, 7).

Especially important is the necessity of de-partments of zoology, or of biology generally, toconsider pathology as one of the biologicalsciences; that "the abnormal, the diseased, andthe atypical are not the exclusive province of thephysician, medical researcher, veterinarian, or

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invertebrate pathologist" (8). Pathology shouldbe recognized and accepted as a legitimate partof biology curricula and research programs. Whatgoes wrong with life can be as important inunderstanding life processes and nature as whatgoes right (6, 8). From the biological standpoint,a microbial pathogen that attacks an invertebratecan be as interesting, as important, and asbasically significant as one that attacks a verte-brate. (If we had limited our study of pathogensto those that cause disease in animals, think whatgaps there now would be in our knowledge ofviruses and genetics without our possession of theinformation gained from the study of the plantand bacterial viruses!)We may also generalize with regard to micro-

organisms associated with invertebrates but notpathogenic for them. Whereas we have someknowledge of the microbiology of insects, we haveprecious little concerning the microbiology ofinvertebrates in general. Here is where thosemicrobiologists interested in the ecology ofmicroorganisms and in the relation of micro-organisms to other forms of life have a realchallenge and could have a "field day" of scienti-fic exploration. For example, fascinating non-pathogenic and mutualistic relationships arealready known to exist between bacteria andprotozoa, bacteria and nematodes-and thereare others-but what of the relationships be-tween microorganisms and sponges, shrimp,barnacles, coelenterates, ctenophores, echino-derms, and even such well-known forms asannelids and mollusks? The microbiology of theseinvertebrate animals is still largely tied in "bondsof ignorance."

Lastly, it must be acknowledged that one ofthe principal factors restraining the developmentof invertebrate pathology, invertebrate physi-ology, and invertebrate ecology is our generalignorance of and lack of attention to invertebrateanimals themselves. In a sense, directing atten-tion to the economic importance of some inverte-brates-as I did earlier in this paper-is a dis-service to the cause of learning about inverte-brates for the pure sake of knowing. Of coursethere are many exceptions, but in general mostof what zoologists know of invertebrates is basedon the study of economic forms, of forms easilymanipulated in the laboratory, and of theirtaxonomy. There has not been enough effort,enough support, enough motivation, indeed therehave not been enough invertebrate zoologists, toprovide us with truly comprehensive knowledgeof these animals without backbones. Especiallyis this true of the lower Metazoa. The tendency,in some quarters of biology, to consider taxonomyand morphology as dying, moribund, or irrele-

vant disciplines simply leaves unappreciated thefact that, although some groups of invertebrateshave been well studied in these respects, largegroups of invertebrates have not. MXIoreover, itfails to recognize that rapidly expanding dis-ciplines, such as genetics, are putting new lifeinto areas of biology which, to some, may appearto have stagnated. Not only does this situationapply to invertebrate zoology, but also we canpoint a similar accusing finger at microbiology,where so-called surveys of the microbiota areconsidered pass6 or pedestrian. There is noreason why we must close our eyes to the de-scription of new forms, to a study of their dis-tribution, and to their natural history, merelybecause many of us are engaged in biochemistryand biophysics as these relate to microorganismsand viruses. Surveys of the microbiota of in-vertebrate animals can be, and of course shouldbe, as sophisticated, as scholarly, as dynamic, asthorough, and as scientific as any other area ofmicrobiology. The classical fields are still fertile,and with their continued exploitation the molec-ular biologist will find-but probably not ap-preciate-that the taxonomist, the ecologist, and,yes, the naturalist, have provided him with newand exciting tools and life forms with which hecan continue his dynamic research. This, alone,is justification for the pursuit of invertebratemicrobiology or, as some may prefer to say it, thestudy of the microbiota of invertebrates. Onemay assume that such a pursuit would eitherinclude or lead to a consideration of those formspathogenic for invertebrates.As it relates to increasing our understanding of

disease in man and other mammals, I was im-pressed by the perception shown in a memoran-dum recently coming to my hands, written inJanuary 1963 by Clyde J. Dawe of the NationalCancer Institute, and referred to here with hispermission. In this document, Dr. Dawe de-plored the lack of study of comparative oncologyand especially the lack of study of neoplasia ininvertebrate animals. I believe strong parallelsand analogies exist between the points he makesand those that could be made relating to knowninfectious diseases of invertebrates. Among thespecific needs he saw in research in comparativeoncology were the following. (i) Collect cases ofnaturally occurring neoplasms, preneoplasticconditions, and borderline types of lesions thatmay be related to tumors, especially in inverte-brates, as there is the greatest dearth of knowl-edge about invertebrate neoplasms. We do notknow what cancers look like in most of the loweranimals. For example, in certain species of hydra,testes develop when the animals are held at lowtemperatures. When the temperature is raised,

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the testes atrophy, and peculiar somatic growthsappear in their stead. Are these structures analo-gous to teratomas? Is there significance in theJarallel between this phenomenon and the ob-servation that certain testicular neoplasms inman and some other mammals are more commonin undescended testes (subjected to relativelyhigher temperatures) than in the descendedtestes? (ii) Study systematically neoplasms of asmany organs as possible, each tumor beingtraced down the phylogenetic scale to the pointwhere the organ of origin had not yet developed.(iii) Develop tumor-induction systems in loweranimals so that neoplasms in these animals can bestudied in large numbers at will, as is presentlydone with mammals and birds in laboratories.For example, the carcinogenic effect of X rays,ultraviolet light, hormones, and chemical car-cinogens could be checked against selected in-vertebrates through the entire phylogeneticscale, in a manner similar to that used, to someextent, with fruitflies and cockroaches. (iv)Develop tissue-culture systems with cells, tis-sues, and organs of prototype animals in each ofthe phyla, and make comparative observationsof how homologous cell types behave in culture.For example, through the use of such culturesystems the relative tendencies of cells from thevarious phyla to undergo spontaneous trans-formation to neoplastic cells could be deter-mined. (v) Conduct biochemical studies toanswer such questions as, does ontogeny re-capitulate phylogeny so far as respiratory andmetabolic pathways are concerned? Do tumorsof animals of lower phyla show an increase overthe normal rate of anaerobic glycolysis of theorgan of origin, as claimed for mammalian neo-plasms? Does ontogeny recapitulate phylogenyin the sense that susceptibility to carcinogensfollows a parallel course in ontogeny and phy-logeny? (vi) Determine whether and how evolu-tionary processes have affected susceptibility tocarcinogens. Have susceptible genetic combina-tions been weeded out by selection? Can anyliving species be found in which the incidenceof neoplasia is so high that it can be used to ex-plain impending extinction of the species, oreven of a population? (vii) Study tumor trans-plantation on neoplasia in lower animals. Willtumor transplants cross species barriers morereadily in the lower phyla than in the higherones? (viii) Study the manner by which tumorsspread, comparing such spread in animals with-out circulatory systems with those having primi-tive circulatory systems and with those havingsophisticated or highly developed circulatorysystems. (ix) Study differentiation and function.Does a neoplasm in an animal with high re-

generative powers display ability to differentiatein multiple directions, or are all neoplasms insuch animals totally undifferentiated? (x) Studythe extent to which tumors in invertebrates maybe virus-induced or virus-related. We know ofBird's report associating the formation of atumor in the European spruce sawfly with theactivity of a nuclear polyhedrosis virus. Are weoverlooking similar cases in other insects and ininvertebrates of other phyla? (xi) Conductmorphological, histological, and cytologicalstudies at all phylogenetic levels. (xii) Coordinatestudies in cancer epidemiology with those incomparative oncology. Invertebrates, availablein almost unlimited numbers, could be surveyedannually in specified areas as a method of check-ing on increased incidences of neoplasia thatmight be caused by radioactive, chemical, ormicrobial contamination. For example, faunaexposed to effluents from industrial plants mightoffer clues to carcinogens in man.

Dr. Dawe finished his list of areas of compara-tive oncology needing increased research with thestatement, "Perhaps we have been so intent onfinding a quick solution to the problem of cancerin man, that we have neglected to consider thatpart of the answer or answers might lie whereman had his beginnings-down at the bottom ofthe phylogenetic tree." I should like to suggestthat we extrapolate Dawe's concern to manyother types of disease occurring in man andhigher animals. As we extend our studies towardthe bottom or lower branches of the phylogenetictree, we are likely to detect basic patterns, toreveal common denominators, and to gain amore composite picture of disease as it relates tolife in general. Pathology is a basic biologicalscience and should be approached as such; whenwe make this type of approach, we shall in alllikelihood find applications beyond our imag-inations.

LITERATURE CITED

1. BORRADAILE, L. A., AND F. A. POTTS. 1958.The invertebrates. Cambridge Univ. Press,New York.

2. AIAcGINITIE, G. E., AND N. AACGINITIE. 1949.Natural history of marine animals. McGraw-Hill Book Co., New York.

3. PENNAK, R. W. 1953. Fresh-water inverte-brates of the United States. Ronald PressCo., New York.

4. RICKETTS, E. F., J. CALVIN, AND J. W. HEDG-PETH. 1962. Between Pacific Tides. StanfordPress, Stanford, Calif.

5. STEINHAUS, E. A. 1961. A call to invertebratepathologist. J. Insect Pathol. 3:i-iii.

6. STEINHAUS, E. A. 1963. Insect pathology and

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biomedical research. J. Insect. Pathol.5:i-iv.

7. STEINHAUS, E. A. 1963. Introduction, p. 1-27.Chap. 1, vol. 1. Insect pathology, an ad-vanced treatise. Academic Press, Inc., NewYork.

8. STEINHAUS, E. A. 1964. Pathology, a biologicalscience. J. Insect Pathol. 6:i-v.

9. STORER, T. I., AND R. L. USINGER. 1957.General zoology. McGraw-Hill Book Co.,New York.

10. TIHESSLER, D. K., AND J. LEMON. 1951.

Marine products of commerce. Their acqui-sition, handling, biological aspects of thescience and technology of their preparation

and preservation, 2nd ed. Reinhold Publish-ing Corp., New York.

11. WESTCOTT, C. 1946. The gardener's bug book.1,000 insect pests and their control. TheAmerican Garden Guild, Inc., and Double-day & Co., Inc., Garden City, N.Y.

12. WALFORD, L. A. 1958. Living resources of thesea. Ronald Press Co., New York.

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