Chapter XXXIII: Section XVIII: The Animal Parasites, Their Incidence and Significance (1)

FRED D. WEIDMAN, M. D.

It is quite to be expected that animal parasites would be found in the animals of zoological gardens, garnered as these beasts are from all parts of the world, tropical and otherwise. It inevitably follows that many of the forms should be strange and new, enticing one to the fascinating determination of their identity, life history and hygienic importance; and, developing from all this, one can easily imagine how limitless the opportunities are for scientific work in parasitology in a laboratory like ours.

As in other biological fields, the taxonomic range of parasites here is wide. It extends from the lowly protozoa to the insecta, and, dropping to the smaller subdivisions, includes not only most of the genera familiar to human parasitology but many known only among the lower animals. From the standpoint of the host, the biologic state of parasitism extends from the lowest protozoa to homo.

The above will suffice to indicate the wide range of parasitism in animals, but the extent of work actually done thus far in wild animal material is a different story. Collated, consistent studies, so far as I am aware, have been undertaken only at the London Garden, here at Philadelphia, and at Washington, D. C., by Dr. Charles W. Stiles and Albert Hassal. The data, collected by the last mentioned workers are incidental to the Index Catalogue of Veterinary and Medical Zoology, and embrace only the (index) phase indicated by the title, but it is so valuable, and withal so altruistic, that it must be credited. What other work there is is scattered where—not in literature—general biological, medical and veterinary. That at London has been conspicuous through the observations of Plimmer and of Beddard on filariæ and cestodes respectively, while the work of Nicoll must not fail of mention.

That the reader may the better appraise the sections of our own work which are to follow I wish at once to indicate their material basis. Ordinarily only the larger parasites are looked for at the autopsy table and there must be special indications to demand search for the finer ones. Those of microscopic size, or so minute as to be overlooked in the guise of seeds, vegetable fibres, etc., have not, both here and elsewhere, been routinely studied as have macroscopic ones.[107] From our autopsies there have accumulated records of nearly 900 parasites— some determined generically, others but as to order. The parasites have in greatest part been preserved and are available for further study; in the past, special groups have been culled out from time to time and examined. Where conditions have been pressing, as in certain epizoötics, investigations have amounted to more than observations and descriptions, and received detailed laboratory examinations with more or less animal experimentation as the occasion demanded.

The foregoing may suffice to apprise the reader that the subject of wild animal parasites has been but broached so that data are especially incomplete on life histories—a phase most important in relation to hygiene; but in spite of this and although the statistics are only approximate, as is the case in most parasitological work, these data have attained to sufficient proportions to justify at least a beginning in the matter of collating and generalization. At any rate the time has arrived to establish at least a nucleus for the accretion of data, which can be later subjected to confirmation or correction. We draw just a grain of comfort from the knowledge that the more fully worked field of human parasitology is also vulnerable to criticism of very much the same order.

THE VALUE OF PARASITOLOGICAL STUDIES IN ZOOLOGICAL GARDENS.

The foregoing chapters have made clear two fields of practical usefulness of any study in such gardens. These—hygiene in relation to the animals and comparison in relation to human beings—need therefore only to be mentioned at present since it is obvious that both benefit by our parasitological work. But there is yet a third—a scientific phase of parasitology which may be considered purely academic. It consists in morphological and other studies necessary for the identification of the parasite, the determination of its life history, etc. These last studies may still in a restricted sense include a modicum of the practical in so far as they have a bearing on the disease with which they are associated. But on the whole they are a source of danger for us since such things as studies on the finer structures of worms, taxonomic arrangements, descriptions of new species of commensals, etc., being alluring, are likely to lead one so far afield that eventually an attitude of stubborn resistance will have to be assumed in order to conserve that precious, volatile laboratory asset—time—for the more crying, practical problems ever reaching out to us.

However, in parasitological investigations as in other scientific work, immediate abstract information may at some time prove to be of greatest practical value. Thus for example if we can discover the exact facts concerning one phase of the life history of a certain parasite, it may be possible by hygienic measures, to break the cycle of development of the parasite at one point thereby preventing its completion. This information is perhaps obtained most readily in experimentation upon the rôle of lower animal forms in the pathogenesis of disease but where reliable evidence is lacking, help may be had by comparison with others in the same taxonomic group. Undoubtedly systematic classification will go far to help solve many of these riddles.

PATHOGENICITY OF ANIMAL PARASITES IN GENERAL.

The first question which arises in this connection concerns the actual ability of animal parasites to produce disease in wild animals. At once it will be seen that this must be a relative matter, for no one on one side would contend that every symbiont in an animal is harmful—parasites _sensu stricto_—nor on the other that none could possibly be, _i.e._, that all are always commensals. It is evident that the issue boils down to questions as to the extent to which they are harmful. Before attempting the answer let us consider the means by which the parasites may conceivably produce disease.

MODES OF DISEASE PRODUCTION (PATHOGENESIS).

The medical reader is familiar enough with the pathogenic powers of some animal parasites, but may be sufficiently interested to glance over specific wild animal instances illustrating them while they are being listed for those less familiar with this subject.

1. MECHANICAL OBSTRUCTION.

I refer here particularly to simple blockage of normal body passages as the result of bulk or mass. This occurs more commonly in the intestines than elsewhere on account of the greater frequency, greater numbers and larger size, in general, of parasites inhabiting this tract. Thus, we have recorded a liothrix (_Liothrix luteus_)[108] where the combination of a small host and consequently narrow gut and comparatively large parasite induced obstruction. Plimmer[109] records microfilaria clogging the brain capillaries. Shipley[110] mentions two specimens of _Ascaris lumbricoides_ obstructing the nares of a chimpanzee (_Pan niger_). Blockage may also be produced secondarily to the presence of the parasite, even in the absence of notable numbers of them, and quite apart from the element of verminous bulk. This occurs through inflammatory swellings which the worms excite. We saw many serious grades of this in our spiroptera epizoötic, the lumen of the proventricle being narrowed by swelling of the mucosa and more or less occluded by exudate and necrotic mucous membrane.

Yet another direction wherein a mechanical rationale pure and simple obtains is by the production of diverticula. Worms encysted in the gut wall may, by weight alone or by excitation of peristalsis, cause the wall to bulge outwards (or inwards even) like a pocket. Such a diverticulum has been noted in the gut of a Pale Cebus (_Cebus flavescens_)[111] parasitized by acanthocephalus, but in this case there were adhesions to the nearby stomach, and it is possible that in this individual case the diverticulum was a traction one, _i.e._, pulled out by the anchorage of adhesions externally.

FIG. 71.—ACANTHOCEPHALUS (THREE SPECIMENS) PROJECTING FROM THE INCISED
INTESTINES OF A PIGMY MARMOSET. COMPARE THE SIZE OF THE PARASITES,
WHICH MAY BE DISTINGUISHED BY THEIR ANNULATIONS, WITH THAT OF THE
INTESTINES.
]

FIG. 72.—BLOOD-RED NEMATODES PROTRUDING FROM FRONTAL SINUSES OF COMMON
OPOSSUM (DIDELPHYS VIRGINIANA). THE SKULLCAP HAS BEEN LIFTED OFF AND
THE POSTERIOR WALLS OF THE SINUSES BROKEN.
]

2. MECHANICAL IRRITATION.—In those instances where inflammation is the manifestation which reflects the simple mechanical effects of parasites it will be difficult indeed to prove, in the present state of our knowledge, that it is not rather the effect of associated toxic substances or excreta elaborated by the parasite. But instances of a purely mechanical irritation there must be, although one can scarcely put the finger upon them and say that this or that individual inflamed mucosa did not become so from a toxic cause. Omitting these then, the more certain, purer, more unequivocal examples will be those where physiological processes become exalted as the result of the parasitic irritation. An example in point is a case of volvulus in a Screech Owl (_Otus asio asio_).[112] Here it is probable that the parasites excited the gut to undue peristaltic action, and that during this process it became twisted. Worms in such passages as the nose and nasal sinuses (I have seen blood-red filariæ in the frontal sinuses of an opossum) undoubtedly produce nervous effects by their presence and movements. Those in the subcutaneous tissue (filariæ of wild cats) probably also do so. It is difficult to judge those cases where doubtfully sensitive parts are the ones affected. Probably the intestinal and intraperitoneal worms, and less certainly the generally-migrating ones analogous to _Filaria loa_, produce no nervous effects mechanically.

3. PRODUCTION OF HEMORRHAGES.—Hemorrhages large enough to kill suddenly are theoretically possible, since worms occasionally produce aneurysms which may rupture; we have seen such an accident in a Paradoxure (_Paradoxurus leucomystax_). But certainly it is the long continued, wasteful small hemorrhages that are important, inducing an anemia often of severe and fatal grade. The hookworms are the shining offenders here, yet we have seen very much the same effect from Acanthostoma in the intestine of monkeys. Œsophagostomum has also been incriminated at the London Garden in young Rhesus Macaques (_Macacus rhesus_)[113] where the young forms of the parasite did the damage as they burrowed into the wall of the gut.

4. OPENING UP AVENUES OF INFECTION.—This may be accomplished either by passage of parasites from one position normally containing bacteria to another which is susceptible to infection, or by devitalizing a tissue which is ordinarily resistant to infection; _i.e._, creating a _locus resistentiæ minoris_. The intestinal tract is the most common organ concerned, but the illustrations to follow will give variety. Thus, the mature examples of œsophagostoma in young rhesuses just referred to above burrowed into the gut wall and led to both local and general peritonitis. In one of our “spiroptera” parrots the worm had passed through the proventricular wall and a chronic fibrosis resulted around it. At the autopsy on a Rhesus Macaque Doctor Fox found a localized abscess adjacent to the gut wall, and in it a whipworm was imbedded. Passing from these examples of intestinal worms, I can mention the loss of a valuable Philippine Spotted Deer (_Cervus alfredi_) as the result of secondary infection of a cysticercus cyst of the lesser omentum which led to a nearby peritonitis. Lung infections are not uncommon. Murray[114] records that forty-four out of eighty-five young rhesus monkeys dying from pneumonia showed an acarian, and he ascribed the pulmonary irritation to certain crystals in the excreta of the mite. I have studied a case of bronchopneumonia in a prairie dog where great numbers of an arachnid were present. The reports of the London Zoological Society are replete with notes of round worm pneumonias of reptiles. These pulmonary cases must result from decreasing of tissue resistance by the presence of the worms, and are easy to understand, much more so than the intestinal infections when one recalls how sensitive lung tissue is to foreign bodies, and that there seems to be no indication that this tissue becomes accustomed to infestation such as may be argued for the gut. All these citations must convince us that parasites are most important predisposing agents to infection, and that this is one of the most sinister phases of animal parasitism.

5. DESTRUCTION OF TISSUE.—This heading does not refer to the comparatively trivial effects that accompany the more acute inflammations secondary to parasites, albeit certainly the absorption of their disintegrative tissue products has some effect on the economy; but our ideas of such are so vague as to justify their being disregarded here. What I refer to is the more massive destruction such as may occur in the blood, for instance, from the action of protozoa. There is also loss of mucosa in those chronic infestments of the stomach where we find excessive fibrous tissue overgrowth. The most striking example of tissue destruction we have seen was in the cirrhotic livers of prairie dogs affected by _Hepaticola hepatica_, where in extreme cases, the amount of functionating liver substance was reduced to a very small fraction of its normal bulk.[115]

6. TOXINS.—We have no direct evidence to offer that noxious products of parasites are concerned in producing disease in wild animals. The local effects of such toxins are not distinctive enough—individual enough to toxins or to the animal body—to separate them from the effects of such accompanying factors as bacterial inflammations; nor can we separate the general effects of these toxins from what might have been, for instance, the effects of an accompanying anemia of hemorrhagic or other origin. From a knowledge of what happens in human prototypes though, there is scant doubt that some one of the multitudinous species must be capable of producing toxins, but just which varieties are concerned cannot be listed by anyone. By analogy we can at most only suspect the hookworms and the dibothriocephalidæ. Under this same category of the toxins come the worm-products which are reputed to have a destructive effect upon the digestive enzymes in the gastrointestinal tract of the host, and which would thereby interfere with the proper assimilation of pabulum, resulting in malnutrition. For the same reasons as above indicated for the toxins one is unable to speak for or against these “anti-enzymes.”

7. PRECLUSION OF NUTRITION.—This must be a very unimportant phase of the activity of intestinal parasites, when one compares the bulk of food which passes through the bowel and the average number of worms present; and the same holds good for some interstitial parasites like the adult filariæ. Even in amazingly heavy infestments of the intestines one will be constrained to dismiss this idea when he compares the bulk of parasites with that of the host, and recalls what the physiologist terms the “factor of safety” inherent in this tract as elsewhere. But in the case of blood parasites the matter may be different. Here we are concerned with the withdrawal of refined foodstuffs—those which have been worked over and over by subtle internal metabolic processes; and we are not so sure, especially on recalling the enormous numbers of parasites usual to blood infestments, that there is the capacity on the part of these internal processes to meet increased demands that we count upon for the intestinal functions. It is much more serious to be deprived of the finished product than of the crude because it means the undoing of “digestive” work all along the line, from gut to tissue cell. Furthermore, a blood infestment guarantees that the parasite has been feeding upon and depriving the animal of the precise foodstuffs the cells require, and not by any chance upon, even in part, intestinal substances that were wastes or residues. If we except the blood parasites, then, it seems safe to conclude on the whole that the amount of pabulum used by parasites is unimportant to the animal.

Having reviewed the manner in which parasites may conceivably be harmful, it is time to return to the question of the actual exercise of these powers.

The older appraisal of parasites in animals, namely that they were rather innocent of disease production, was suggested by and borrowed from the veterinarian, probably being engendered in him by their frequency in what appeared to be normal domestic specimens. Yet it is only proper to add that one of our former pathologists, and sometime professor of veterinary pathology, Dr. C. Y. White, is a medical man and is of much the same opinion. Older writers regarded worms even as “guardian angels” of children. Very recently Schwartz[116] reviews some work in this connection showing that, _in vitro_, some cestode extracts were inhibitory to certain bacteria (_B. anthracis_, _B. pyocyaneus_ and _B. dysenteriæ Shiga_). This relationship is so different from natural conditions as to need no further comment.

At the London Garden the view appears to be different. In the 1910 report they charge five deaths against perforation by worms of the stomach and intestines; in the 1911 report they record giant toads dead from lung infestment; in 1912 “eighteen cases of enteritis were due to worms”; and in 1917 they mention pneumonia in a toad and perforation of the stomach of a puma. These reports represented evidently the more striking, unequivocal examples of death from parasites which had outspoken anatomical expressions, and omitted those in which the more subtle agencies of parasitic pathogenesis were concerned. Their experience has apparently been much the same as ours.

The ideal approach to a decision in reference to the importance of parasites would appear to be a mathematical one, something as follows: First, to determine what species infest animals and how commonly, then to decide which ones are pathogenic and thirdly to estimate the severity of the disease induced; so that finally, by an analysis and comparison of the three results—a comparison and analysis judicial in the broadest sense—we might hope to come to an opinion. Let us consider the three avenues in order. At the first glance it must be evident that a list of all possible parasitic varieties does not exist and may never be compiled. The most that can be done is to tabulate the findings in scattered laboratories, data usually recorded in terms of the individual observer’s studies and often inadequate to give the compiler all the facts desired. The same remarks apply to the percentage incidence of parasitism. Not to prolong the academic discussion, suffice it to say that very much the same obstacles present in the second avenue—that of pathogenicity of the individual species. Our own data referring to this second heading will be presented later, but after the failure of the first avenue, the second and third lose greatly in value. At best, statistics can be only suggestive. Unless critically and suspiciously interpreted, and with a full appreciation of their limitations from a foreknowledge of the way in which they were compiled, they would only delude the reader and offend science, and so we abandon this line of reasoning.

At present the best results of the study of pathogenesis by animal parasites will probably be reached by a combination of methods, as follows:

1. Direct. How commonly do we see clinical symptoms and morbid anatomical changes that are incontrovertibly due to the parasite? We restrict ourselves here to a narrow group of infestments indeed, and think of such diseases as trichosomiasis in prairie dogs and spiroteriasis in parrots.

2. By comparison with analogous infestments of domestic animals and man— more thoroughly studied and therefore more accurately appraised, in general, as to pathogenicity; a comparison from the standpoint of disease production rather than natural habits of the parasite. Example, coccidiosis and hookworm disease in foxes and dogs.

3. By inference through deduction. This is the most unsatisfactory consideration of all, and should be well checked up and discounted. Here we would evaluate the known propensities of the parasite first, such as its size, motility, anatomic position in the host and the general pathological traits of the genus and family to which it belongs, etc., and then compare these verminous properties with those of the host—its size, temperament, physical stamina, etc. This third consideration must necessarily overlap with or be supplementary to the first two. For example, this consideration would have to be resorted to in many cases of ascaris infestment where anatomical changes are generally not demonstrable.

Acting on these three considerations, and after twelve years of observation on parasites here in the Garden, a fresh review of our records, and a recent review of the accessible relevant parasitological literature I have come to the conclusion that, considering wild animal collections the world over, there is no justification for an unqualified, definite answer to the question of pathogenic parasitism that will meet all conditions. We lack data on too many species that are not sufficiently represented in collections or indeed not represented at all. It is the liability to infestment of each order or family of beasts that will have to be determined, and, depending on the assortment each garden has on exhibition, will the importance of parasites to the garden as a whole vary.

Speaking for the Philadelphia Garden, I have come to the conclusion that on the whole parasitism does play an important part of our annual losses. The financial loss which could be charged against spiroptera alone is in the four figures, to say nothing of the difficulty of replacement of rare species. And while touching the financial phase let it be added that scientific work done now, it must be remembered, is not restricted to the present time or place, but is to be measured in dollars and cents with the yard stick applied to the future, and in other places than that where the initial work is done. Even if we cannot answer the question of the matter of importance the world over we can guarantee that it is sufficiently so in the Philadelphia and London Gardens to warrant a rigid supervision for parasitism; and since the other larger collections are probably made up of similar animals, albeit in different proportions, we surmise at least that it is likewise so with them.

IMPORTANCE OF PARASITES IN OTHER FIELDS.—In addition to their importance to exhibitions, animal parasites of wild animals are important first to man. The animal hosts may serve as porters of infestation, and interfere with attempts at eradication of the disease. The experience of the European with African sleeping sickness attests to this. Not to go farther than immediate examples I wish to note in this connection the occurrence in this Garden of scabies in an orang which was transmitted to a keeper, and of amebic dysentery in monkeys. Leiper[117] has called attention to a guinea-worm in a leopard.

Parasites are important to certain wild animal industries. The ones that have come to my attention are the fur seal (_Otoes alaskanus_) industry of the Pribiloff Islands and fox-farming in Newfoundland. In both of these instances the hookworm was concerned and entailed losses of thousands of dollars. Lucas, who conducted a United States Government commission to the seal grounds and after whom Stiles named the parasite, has left very full notes of the former disease. I have identified the same infestment in a young California hair seal (_Zalophus californianus_) which was born and died in this Garden. This indicates that the parasite might perhaps be found farther down the Pacific coast than hitherto suspected.

To hunters parasitism of animals must be important, but to an unknown and undoubtedly unimagined extent. The grouse plague of Scotland[118] is an example to point. Who knows but that the disappearance of some of our game animals, particularly birds, was not due more to disease than to the ravages of man? There is at least food for thought here.

OCCURRENCE OF ANIMAL PARASITES IN THE WILD.—It would be unbelievable that parasitism did not exist in the wild. It seems proper, however, to record some evidence. Diesing’s _Systema Helminthum_ is replete with references to Natterer’s Brazilian expedition. Nicoll speaks of a German expedition to Spitzbergen in 1898, and a Swedish one to Egypt in 1901, in both of which large numbers of parasitic forms were collected. Nicoll[119] found _Trichosoma hepaticum_ in a hare shot in the wild, and liver-flukes[120] in a kestrel shot on the coast of Scotland. Leiper[121] found nine species of worms in hippopotami during an expedition to Uganda, and[122] states that thirty-seven species of helminths were collected on an Antarctic voyage by Surgeon Atkinson. In an investigation of Grouse disease in Scotland, Fantham found many different blood and intestinal parasites. Dr. Charles B. Penrose tells me that all of the white-tailed deer he shot in the valley of the Swan River, Montana, were infested with liver-flukes, so much so that the liver was literally riddled by the disease, and yet the deer were fat. The black-tail deer of the same valley were not thus parasitized and were not as fat. In our own Garden we have found many tapeworms in wild cats[123] which had been too recently captured for the worms to have developed in captivity. Such instances might be still further multiplied.

A more important consideration is the fate of the parasites thence introduced into our Garden. Do they disappear of themselves? Naturally we can never make sweeping predictions, for future events will depend upon the life history of the individual parasite concerned. But by and large, once introduced it is better to assume the attitude of pessimism, and resign oneself against spontaneous disappearance and, what is worse, realize that the parasitism is likely to become indigenous. We have several pieces of evidence, however, that the infestment may occasionally quite disappear. Thus, I have seen _Coccidium bigeminum_ spontaneously disappear from a Swift Fox (_Canis velox_) and _Spiroptera incerta_ from a Macaw as proven at autopsy. Nicoll[124] remarks that certain trematode infestations were heavier in newly arrived animals than in ones long resident in the Garden. This is conceivable on the basis of individual worms dying out, _i.e._, fulfilling their life spans without the host becoming reinfested with fresh parasites. Precise information on the subject is supplied by Ackert[125] who found that cestodes disappeared from chickens in six to eight months when the birds were confined, _i.e._, protected from reinfestment. Moreover, it is known that worms can escape during acute infections, the infectious state of the economy producing conditions obnoxious to the parasite. We hear of many instances of their expulsion in human feces and vomitus during malaria and the exanthemata of childhood and know of similar discharge from animals during the death agony. I cite these data largely because they explain the scarcity or absence of parasites at autopsy in animals which were known to have been clinically infested.

FREQUENCY OF PARASITISM IN WILD ANIMALS

There can be little doubt that wild animals are more frequently infested than man, and furthermore with a larger number of parasites. I have no statistical basis for these opinions—they rest on personal observations of human and animal autopsies, and reports of findings in the tropics and elsewhere. They have therefore but the value of an individual opinion. I should estimate rather cautiously that wild animals are infested at least two or three times as frequently as man and much more heavily.

The first step in the discussion of the incidence of parasites must be that respecting the (host) classes and smaller taxonomic divisions—of course as they have been studied in this Garden. Certain statistical limitations were experienced and can be summarized as follows:

Data are not available on a sufficiently large number of animals to justify conclusions as far down as genera and species, except for such commonly and generously exhibited forms as monkeys and parrots. I have therefore in tabulating and reviewing our records, distributed the animals only as far as families—not into genera and species. The table (24) to follow will be found not to contain every family because to do so would needlessly enlarge it. Accordingly I have followed the policy of only indicating those genera and species showing either frequent or important infestment. I shall refer to those groups later as “susceptible” groups. If no family is recorded in the table it means that we have had no important numbers of infestments in it. The “remarks” column shows the individual parasite that has been particularly frequent or otherwise important. If there are no remarks it means that the species of parasites found have been scattering.

RESULTS OF REVIEW AND TABULATIONS.

We now pass to an analysis and discussion of the findings brought out in the previously mentioned review of our records and in Table 24. Viewed broadly we find that there is a wide variation in the susceptibility of different families to infestment. Those that are susceptible may be located by consulting the table, and each will therefore not be separately culled out and subjected to needless repetition. A few points are however worthy of separate mention. While there is a familial or generic susceptibility within certain orders it is unwise to generalize too broadly. Thus for example the Corvidæ have a high percentage in incidence for tropidocerca, syngamus and periproventricular worms, many families of Ungulata harbor echinococcus, and Carnivora are prone to show ascarids. On the other hand, among the copious exceptions to this may be cited the irregular liability to infestment exhibited by the Galli. Four varieties of these birds are represented but there are missing such important kinds as curassows, guans, guinea fowl and peafowl.

TABLE 24.
_Incidence of Parasites in Animal Groups._
══════════════════════╤═══════════════════════════════╤════════════════════
Animal │ MAMMALIA │ Remarks
──────────────────────┼───────────┬────────┬──────────┼────────────────────
„ │ Number of │ Number │Percentage│ „
│Autospecies│Infested│ │
──────────────────────┼───────────┼────────┼──────────┼────────────────────
Primates │ [126]538│ 51│ 9.4│
Cercopithecidæ │ │ │ │
Sooty Mangabey │ 34│ 4│ 11.8│
Cercocebus │ │ │ │
fuliginosus │ │ │ │
Rhesus Macaque │ 60│ 6│ 10.│
Macacus rhesus │ │ │ │
Callitrichidæ │ │ │ │
Marmosets │ 43│ 7│ 16.3│
Cebidæ │ │ │ │
Squirrel Monkeys │ 8│ 3│ 37.5│
Other Cebus │ 87│ 10│ 11.5│Eight had Filaria
Monkeys │ │ │ │ gracilis.
Lemures │ 86│ 6│ 7.│
Carnivora │ 498│ 84│ 16.9│
Felidæ │ │ │ │
American Wild Cat │ 28│ 11│ 40.│Stomach and
│ │ │ │ intestines, 22;
Felis ruffus │ │ │ │Bronchi, 4; Muscles,
│ │ │ │ 7.
Spotted Wild Cat │ 5│ 4│ 80.│
Felis ruffus │ │ │ │
texensis │ │ │ │
Canada Lynx │ 10│ 4│ 40.│Ascarids only.
Felis canadensis│ │ │ │
Lions │ 10│ 3│ 30.│Ascarids in stomach
│ │ │ │ and
Felis leo │ │ │ │intestines.
Ocelot │ 15│ 5│ 33.│Uncinaria.
Felis pardalis │ │ │ │
Canidæ │ │ │ │
Gray Fox │ 28│ 1│ 4.│Cestodes.
Canis cinereo │ │ │ │
argenteus │ │ │ │
Red Fox │ 17│ 2│ 12.│Uncinaria.
Canis vulpes │ │ │ │
pennsylvanicus│ │ │ │
Swift Fox │ 5│ 2│ 40.│Uncinaria.
Canis velox │ │ │ │
Gray Wolf │ 18│ 2│ 11.│Ascarids.
Canis mexicanus │ │ │ │
Mustelidæ │ │ │ │
American Badger │ 17│ 7│ 41.│Physaloptera.
Taxidea taxus │ │ │ │
Procyonidæ │ │ │ │
Raccoon │ 42│ 2│ 5.│
Procyon lotor │ │ │ │
Ursidæ │ │ │ │
Bears │ 37│ 6│ 16.│Ascarids.
Otariidæ │ │ │ │
Hair Seal │ 20│ 1│ 5.│Uncinaria.
Zalophus │ │ │ │
californianus │ │ │ │
Rodentia │ 198│ 32│ 16.│
Sciuridæ │ 44│ 4│ 9.│Scattered through
│ │ │ │ four
Castoridæ │ │ │ │different genera.
American Beaver │ 17│ 4│ 23.│In three cases
│ │ │ │ oxyuris
Castor │ │ │ │and flukes in cecum.
canadensis │ │ │ │
Hystricidæ │ │ │ │
Canada Porcupine │ 47│ 17│ 36.│Cestodes 8, filaria
│ │ │ │ 11, oxyuris 9,
Erythizon │ │ │ │in peritoneal cavity
dorsatus │ │ │ │ also intestine.
dorsatus │ │ │ │
Hyraces │ 7│ 2│ 28.│Cestodes in bile
│ │ │ │ ducts.
Cape Hyrax │ │ │ │
Procavia capensis │ │ │ │
Ungulata │ 365│ 44│ 12.│
Equidæ │ │ │ │
Zebras │ 7│ 7│ 100.│Nematodes,
│ │ │ │ intestine.
Cervidæ │ │ │ │
Axis Deer │ 6│ 1│ 17.│C. tenuicollis.
Cervus axis │ │ │ │
Barasingha Deer │ 8│ 0│ │
Cervus duvanceli│ │ │ │
Eld’s Deer │ 6│ 0│ │
Cervus eldi │ │ │ │
Fallow Deer │ 20│ 1│ 5.│Echinococcus cysts.
Cervus dama │ │ │ │
Hog Deer │ 21│ 0│ │
Cervus porcinus │ │ │ │
Japanese Sika Deer│ 14│ 0│ │
Cervus sika │ │ │ │
typicus │ │ │ │
Red Deer │ 14│ 0│ │
Cervus elaphus │ │ │ │
Elk │ 29│ 2│ 7.│Trichocephalus.
Cervus │ │ │ │
canadensis │ │ │ │
White tailed Deer │ 33│ 2│ 6.│Echinococcus in lung
│ │ │ │ (2).
Mazama │ │ │ │
virginiana │ │ │ │
Mule Deer │ 8│ 5│ 62.│Four Cyst.
│ │ │ │ tenuicollis.
Mazama hemionus │ │ │ │
Camelidæ │ │ │ │
Llama │ 14│ 2│ 14.│
Lama glama │ │ │ │
Camels │ 9│ 4│ 44.│Hydatid cysts.
Suidæ │ 19│ 2│ 10.│
Edentata │ 16│ 2│ 12.5│
Armadillos │ 10│ 2│ 20.│
Marsupialia │ 175│ 45│ 26.│
Didelphyidæ │ │ │ │
Common Opossum │ 84│ 40│ 48.│Physaloptera, 38;
│ │ │ │ oxyuris, 5;
│ │ │ │ cestodes, 5;
│ │ │ │ nematodes in
│ │ │ │ lungs, 3; cysts in
│ │ │ │ peritoneal areolar
│ │ │ │ tissue, 2;
│ │ │ │ trematodes in
│ │ │ │ ileum, 1.
Didelphys │ │ │ │
virginiana │ │ │ │
Macropodidæ │ │ │ │
Kangaroos and │ 70│ 0│ 0.│
wallabies │ │ │ │
──────────────────────┼───────────┴────────┴──────────┼────────────────────
│ AVES │
Passeres │ │ │ │
Corvidæ │ │ │ │
Common Crow │ 16│ 7│ 44. }│Tropidocerca and
│ │ │ │ occasional
│ │ │ │ intestinal
│ │ │ │ cestodes. Syngamus
│ │ │ │ in crows. Few
│ │ │ │ filaria.
Corvus │ │ │ }│
brachyrhynchos│ │ │ │
brachyrhynchos │ │ │ }│
Magpies │ 28│ 18│ 64. }│
Jays │ 41│ 22│ 55.│Periproventricular
│ │ │ │ filaria,
│ │ │ │ strongylus.
Pies, choughs, │ 35│ 12│ 33.│There is a striking
etc. │ │ │ │ consistency of
│ │ │ │ infestment in the
│ │ │ │ different members
│ │ │ │ of Corvidæ both as
│ │ │ │ regards degree of
│ │ │ │ infestment and
│ │ │ │ species of
│ │ │ │ parasite present.
Sturnidæ │ │ │ │
Starlings │ 63│ 19│ 30.│Periproventricular
│ │ │ │ filaria largely.
Turdidæ │ 25│ 8│ 33.│Periproventricular
│ │ │ │ filaria largely.
│ │ │ │Thrushes and Robins.
│ │ │ │ None in American
│ │ │ │ thrushes, one in a
│ │ │ │ robin.
│ │ │ │Finches. Not
│ │ │ │ examined closely
│ │ │ │ at autopsy, but
│ │ │ │ there is a
│ │ │ │ scattering of
│ │ │ │ periproventricular
│ │ │ │ filaria and
│ │ │ │ intestinal
│ │ │ │ cestodes through
│ │ │ │ most of the
│ │ │ │ species.
Canaries │ 24│ │ │Were free from
│ │ │ │ parasites.
Picariæ │ │ │ │
Picidæ │ │ │ │
Woodpeckers │ 4│ 2│ 50.│
Rhamphastidæ │ │ │ │
Toucans │ 30│ 9│ 30.│Spiroptera largely.
Striges │ 142│ 2│ 7.│Remarkably free of
│ │ │ │ parasites.
Psittaci │ [127]774│ 124│ 16.│
Loriidæ │ │ │ │
Lorys │ 24│ 5│ 20.│3 spiroptera, 1
│ │ │ │ hemoproteus, 1
│ │ │ │ intestinal worm.
Cacatuidæ │ │ │ │
Cockatoos │ 4│ 2│ 6.│2 spiroptera.
Crested Ground │ 45│ 4│ 9.│4 spiroptera.
Parrakeet │ │ │ │
Calopsitta novæ- │ │ │ │
hollandiæ │ │ │ │
Psittacidæ │ │ │ │
Old World (Totals)│ 453│ 65│ 14.3│
Undulated Grass │ 121│ 2│ 1.6│1 spiroptera, 1
Parrakeet │ │ │ │ coccidium.
Melopsittacus │ │ │ │
undulatus │ │ │ │
Pennant’s │ 21│ 6│ 29.│6 spiroptera.
Parrakeet │ │ │ │
Platycercus │ │ │ │
elegans │ │ │ │
Rosehill Parrakeet│ 48│ 21│ 44.│20 spiroptera, 1
│ │ │ │ cestode.
Platycercus │ │ │ │
eximius │ │ │ │
Other old world │ 86│ 12│ 14.│12 spiroptera.
parrakeets │ │ │ │
Old world parrots,│ │ │ │
lovebirds, │ 74│ 13│ 18.│13 spiroptera.
eclectus. │ │ │ │
New World (Totals) │ 321│ 69│ 21.5│
Macaws │ 26│ 9│ 34.│9 spiroptera.
Conures │ 62│ 16│ 26.│15 spiroptera, 1
│ │ │ │ hemoproteus, 1
│ │ │ │ blood larva.
Amazons │ 164│ 27│ 16.5│24 spiroptera, 3
│ │ │ │ nematodes.
Other new world │ 69│ 17│ 10.│7 spiroptera.
parrots │ │ │ │
Accipitres │ [127]201│ 13│ 6.7│
Falconidæ │ │ │ │
Buzzards │ 55│ 4│ 7.3│
Eagles │ 44│ 1│ 2.3│
Serpentaridæ │ │ │ │
Vultures │ 29│ 1│ 3.4│
Miscellaneous │ 73│ 7│ 9.6│4 were blood
│ │ │ │ protozoa.
Galli │ 299│ 42│ 14.│
Phasianidæ │ │ │ │
Pheasants │ 95│ 20│ 21.│Heterakis in ceca.
Partridges │ 14│ 3│ 21.│
Quail │ 70│ 10│ 14.│Heterakis.
Megapodidæ │ │ │ │
Wild Turkeys │ 39│ 7│ 18.│Intestinal cestodes.
│ │ │ │ Coccidia twice.
Columbæ │ [128]163│ 14│ 9.│Mostly intestinal
│ │ │ │ cestodes, but
│ │ │ │ several
│ │ │ │ spiroptera.
Fulicariæ │ [128]38│ 7│ 18.│
Alectorides │ [128]41│ 10│ 25.│
Gaviæ │ [128]21│ 3│ 14.│
Steganopodes │ [128]22│ 1│ 5.│
Herodiones │ [128]105│ 21│ 20.│
Anseres │ [128]319│ 28│ 8.8│
Swans │ 48│ 7│ 14.│No significant
│ │ │ │ groupings.
│ │ │ │ Parasites
│ │ │ │ scattering. Few
│ │ │ │ intestinal
│ │ │ │ cestodes.
Geese │ 83│ 13│ 15.6│
Ducks │ 188│ 8│ 4.│
Struthiones │ 36│ 1│ 2.8│
──────────────────────┴───────────┴────────┴──────────┴────────────────────

Nor do all members of a genus necessarily show the same susceptibility, and the heterakis infestment in the pheasants illustrates this matter very well. It was limited almost entirely to two species—Amherst’s and Golden, whereas several frequently exhibited species showed none. The following table brings this out in more detail:

TABLE 25. _Heterakis in Pheasants._ ════════════════════════════════════════════╤════════╤════════╤════════ Species │ Total │Infested│ Per │ │ │ cent. │ │ │infested ────────────────────────────────────────────┼────────┼────────┼──────── Golden Pheasant (Chrysolaphus amherstiæ) │ 18│ 12│ 67 Amherst’s Pheasant (Chrysolaphus pictus) │ 16│ 5│ 31 Silver Pheasant (Gennæus nycthemerus) │ 19│ 1│ 5 Reeves’ Pheasant (Phasianus reevesi) │ 16│ 1│ 6 Ringnecked Pheasant (Phasianus torquatus) │ 12│ 0│ 0 Swinhoe’s Pheasant (Gennæus swinhoii) │ 10│ 0│ 0 ────────────────────────────────────────────┴────────┴────────┴────────

Enzoötics and environment played no part in the above figures. We have had no real heterakis enzoötics, for in but two instances did three heterakis deaths occur in a year, and two deaths per year have occurred in but four instances in the past twenty years. During this time there have been sufficient animals on exhibition and subjected to autopsy to indicate definitely that the two species named—Amherst’s and Golden, must be considered as more susceptible than the other varieties. Nearly all of the heterakis in quail likewise occurred in one species—seven of the ten cases occurred in a total of twenty-three Scaled Quail—but in these birds the infestment appeared in enzoötic form and cannot be viewed as indicating a preference for a species.

Psittaci are on the whole, not susceptible to worms. It is true that we suffered a serious outbreak of spiropteriasis a few years ago, but if we consider this a closed chapter we can accept the above generality as stated. Among 774 parrots autopsied we have encountered but one cestode and three intestinal round worms.

The deer, likewise, are singularly free from intestinal parasites. I gave the detailed records of these animals in Table 24 to emphasize the scarcity of parasites even when fairly numerous specimens had been available for examination.

Other interesting features in the table are the outstanding infestments of squirrel monkeys and marmosets among the monkeys, of gastric and intestinal worms in the wild cats, and intestinal worms in the zebras.

The foregoing has had to do with parasitism from the standpoint of the host. The next phase, that of the individual parasite itself, interests more the strict parasitologist than the general zoologist; however, both will see how it may have a very practical value.

TABLE 26.
_Distribution of Parasitic Cases According to Parasitic Groups._
═════════════════════════════════════╤════════════════╤════════════════
Nematodes │ 183[129]│
Spiroptera │ 145│
Filaridæ │ 138│
Ascaris │ 30│
Physaloptera │ 28│
Uncinaria │ 25│
Tropidocerca │ 23│
Heterakis │ 22│
Trichocephalus │ 11│
Syngamus │ 9│
Trichina │ 2│
Hepaticola │ 2│
Other Miscellaneous │ 4│
Total Nematodes │ │ 622
Cestodes │ 165[129]│
Echinococcus │ 9│
Cysticercus │ 7│
Tænia │ 4│
Miscellaneous │ 3│
Total Cestodes │ │ 188
Trematodes │ │ 22
Acanthocephalus │ │ 4
Protozoa │ │ 14
Arthropods │ │ 6
Unclassified │ │ 34
─────────────────────────────────────┼────────────────┼────────────────
Grand Total │ │ 890
─────────────────────────────────────┴────────────────┴────────────────

INCIDENCE ACCORDING TO PARASITIC GROUPS.

Inasmuch as it has been physically impossible to determine specifically and classify efficiently the accumulations of verminous material from our autopsies I will not be able to tabulate parasitic groups even as closely as I did in the “animal host” table. Nevertheless sufficient has been done to illuminate in part certain phases of parasitism and to prevent a summary dismissal of the subject. Reviewing our cross index I have distributed the data into the following Table 26, the parasites being listed in the order of their frequency. It may serve only as a panorama of the situation, inasmuch as determinative study of a group amounts to a research in itself, and the multiplicity of them precludes a consistent study of every one. The data are based upon “cases of parasitism.” That is, each and every worm species occurrence has been counted, regardless of whether it was the same species that has been concerned over and over again, or in different anatomical positions (of different individual hosts, of course) or whether it was in association with other parasites.

ANALYSIS OF TABLE 26.

There is a grand total of 890 cases of animal parasitism embraced in the above table, which is a sufficiently large number to give representative value to some phases of the analysis.

In the first place nematode worms occur about three times as frequently as all other forms of parasites. In gardens where spiroptera has not figured so largely the proportion might be reduced to about two to one. Cestodes rank a poor second, trematodes a worse third, and acanthocephali a very bad last. This order agrees with our figures of 1913[130] and with the small series of Nicoll.[131] The latter worker found that the order was not changed when pains were taken to include also such smaller worms as could only be obtained from the host by using sieves, etc. Cestodes were not likely to be overlooked, but very small trematodes and nematodes were easily passed over.

VISCERAL DISTRIBUTION.

As to the individual organs which are most commonly parasitized our records show that with Aves as well as Mammalia the intestines are the parts most commonly affected. The stomach ranks second for both—the proventricle rather than the gizzard of birds corresponding, parasitologically speaking, to the stomach of mammals. We have found but one parasitic species in the gizzard of birds, _i.e._, immature forms of _Spiroptera incerta_ lying under the chitinous lining of the gizzard and only discoverable after the lining has been peeled off. The peritoneum comes third (air sacs of birds) due to the presence of filaridæ, and the blood fourth for the same reason. It is to be emphasized that, in our data, identical organs of mammals and birds should be about equally liable to infestment with the possible exception of the lungs. But in view of the small number of cases available there is no justification for speculating about the reason for this last difference, albeit the radical difference in the anatomy of the two classes is very inviting.

Now that our spiroptera enzoötic has subsided, the order above given will be changed, and in view of like disturbing factors other gardens should not expect the same order to hold invariably for their collection, since their enzoötics will depend somewhat on the preponderance of animals of one or another family which are likely to compose their exhibits. A single such enzoötic may suffice to disarrange the whole fabric, and if two or three are taken into account the order of organ involvement can be quite disrupted. To attempt to construct statistically an “order of frequency involved” which would stand for every garden would only lead to interminable adjustments on the basis of animals exhibited and of parasitic enzoötics, so that I have finally been reduced to a combination of our Garden statistics and the bloodparasitic ones of the London Garden. Doing this I have arranged in Table 27 the frequency of organ involvement as follows and estimated the percentage of animals infested. These figures are computed upon a different basis from that of Table 24. They naturally cover all animals and not the “susceptible” ones as in Table 24.

FIG. 73.—HUGELY DISTENDED PROVENTRICLE OF PARROT DYING WITH
SPIROPTERIASIS. COMPARE ITS SIZE WITH THAT OF THE HEART WHICH IS
ABOVE AND TO THE LEFT, AND THAT OF THE GIZZARD BELOW AND TO THE
LEFT.
]

TABLE 27. ═══════════════════════════════════╤═══════════════════════════════════ Mammalia │ Aves ───────────────────────┬───────────┼───────────────────────┬─────────── │ per cent. │ │ per cent. Intestines │ 9.0│Blood │ 6.5 Stomach │ 3.7│Intestines │ 3.5 Peritoneum │ 2.3│Proventricle │ 1.7 Blood │ 1.5│Air sacs │ 1.3 Lungs │ 1.0│Liver │ 0.3 Muscles │ 1.0│Gizzard │ 0.3 Liver │ 0.5│Scattering │ 0.4 ───────────────────────┼───────────┼───────────────────────┼─────────── Total │ 20.0│Total │ 14.0 ───────────────────────┴───────────┴───────────────────────┴───────────

The effect of this is at first sight startling in that it places the blood parasites of birds so far in the fore, but it must be at once recalled that the inquiries upon the blood parasites were much more searching—microscopic, than in the case of the other organs. If similar methods were applied to the others their percentage of parasitism might be notably raised—particularly that of the intestines.

SPECIAL PARASITOLOGIC CONSIDERATIONS.

At this point the statistical considerations of parasitism will give way to descriptions of certain specific infestments that have given us more or less concern.

The occurrence of single parasitic varieties or of well known species in an isolated host may occasionally be of practical importance, but usually they amount to little more than an academic study, whereas the repeated discovery of single parasitic kinds, or infestment of similar hosts, especially when grouped, raises the matter to a very practical level demanding attention. Such findings being not infrequent in our experience, it has been possible to study our material in a manner designed to show the frequency of various parasites in a certain host, the susceptibility of certain animals to parasites in general and the infestment of dissimilar hosts by the same parasite. The more important of these now follow.

AVIAN SPIROPTERIASIS.

This disease concerned parrots particularly but toucans, pigeons, and such widely separated species of birds as the starling, quail, thicknee and barbet have been occasionally affected. To the naked eye the parasite resembles the human hookworm, but differs in location, being a resident of the proventricle where it produces a swelling of the mucosa which interferes with the passage of food. Up to a hundred worms may be present in the one bird, and immature forms are occasionally found under the chitinous lining of the gizzard. The parasite burrows into the mucous membranes, occasionally penetrates quite through the wall into the air sacs, and on one occasion induced an adenomatous hyperplasia of the mucous membrane, and an adjacent “peritonitis.” Mucus is sometimes present in the droppings. Death may occur either acutely, or with emaciation. Spiroptera incerta Smith[132] is the common parasitic species of parrots, but I have found at least one other as yet unidentified species in the toucan, and there are probably more. In the eight year period 1906–1913 from 25 to 50 per cent. of our dead parrots showed this parasite every year, the total loss being 113 birds for this period—a most important infestment.

FIG. 74.—HISTOLOGIC SECTION THROUGH PROVENTRICULAR WALL OF PARROT,
SHOWING SECTIONS OF SPIROPTERA IN THE LUMEN AND MUCOSA. THERE IS
SOME GLANDULAR HYPERPLASIA (ADENOMATOID) AND NECROSIS OF THE LUMINAL
PORTIONS OF THE MUCOSA.
]

FIG. 75.—INFLAMMATORY ROUND CELL INFILTRATION AROUND NERVE TRUNK IN
WALL OF PROVENTRICLE. PARROT DEAD WITH SPIROPTERIASIS.
]

We approached the problem by diagnosing and isolating the infested birds through a microscopic examination of droppings, finding that by boiling the droppings in 5 per cent. NaOH solution we clarified them and made examination easier and more certain without at the same time destroying the parasitic ova. The result of the examination of all our parrots was the isolation of 14 per cent. of the parrot population; and as these died off the diagnosis of infestment was found confirmed at autopsy in every case. The parrot house was thoroughly renovated and no newly arrived parrots were admitted until after quarantining and examining droppings for ova. The toucans and other species, being housed elsewhere, were not quarantined. Following this, we were gratified to experience no more spiroptera deaths in parrots for seven years. Then, in 1920 and 1921, a new outbreak occurred in four toucans and several other scattering species, including two parrots; but none of these came from the main parrot house and probably represented a fresh importation. We attempted to cure the isolated verminous birds by medication but were unsuccessful. Likewise attempts at determining the life cycle of the parasite brought us no farther than that the ova developed larvæ in moist sand in six days. Feeding of ova, freshly passed and larvated did not produce infestment in parrots or pigeons. On the whole we can quote our experience with spiroptera as a most satisfactory example of the value of hygiene and as a result which could never have been accomplished by medication.

HEPATICOLA (TRICHOSOMA) HEPATICA IN PRAIRIE DOGS.

Bancroft[133] and Hall[134] have given us details concerning this parasite and the disease it causes. It is threadlike, several inches long, and permeates the livers of the gray rat, white rat and wild hare.[135] We first saw it in the more or less cirrhotic livers of several prairie dogs; later we observed it in a beaver and the gray rats of the Garden. In the prairie dogs and beaver the liver resembled that of fatty cirrhosis and was so considered on naked eye examination at our first autopsy. We were only set right when we came to the histological examination. It was remarkable how well conditioned some of the prairie dogs were in in the face of very extensive liver destruction; but on the other hand some were emaciated and a few of the spontaneously diseased showed at autopsy an enormous ascites. The outstanding features at autopsy were the large size of the liver and its pallor and hardness; and fine yellow lines could sometimes be made out twisting over the surface.

The disease affects wild rats differently from prairie dogs. In both the spontaneous and experimental disease the infestment was insignificant, amounting to perhaps three or four foci the size of a split pea near the anterior margins of the liver. Diagnosis may be easily confirmed by crushing the yellow infested portions of the liver between glass slides and examining microscopically for ova.

We have seen such a small number of cases of this disease because so few prairie dogs reach the autopsy table, yet there must be some important mortal factor in our prairie dog enclosure, for the Superintendent states that the population there does not increase in spite of the frequent births and additions from dealers. The animals almost invariably die under ground and their bodies are not recovered.

In order to test out the origin of the infestment we trapped two of our exhibition specimens, and the liver of both was found infested on surgical examination whereas six newly purchased ones had normal livers. The latter were secured fresh from their native habitat in the West, and their livers were examined through long surgical incisions and found free of infestment. Later we fed the ova (embryophores) from rat livers to these prairie dogs and on destroying them found them infested. We were also successful in transmitting the disease in the opposite direction, _i.e._, from prairie dog liver to white rat. From all this we feel sure that the prairie dog disease in our Garden was transmitted from the rat and that here is another reason for rat extermination in a zoological garden.

FIG. 76.—OVA OF HEPATICOLA HEPATICA IN LIVER OF PRAIRIE DOG. THEY HAVE
BIPOLAR OPENINGS. THERE IS DESTRUCTION OF LIVER TISSUE AND A LITTLE
INFLAMMATORY REACTION OF CELLULAR CHARACTER, BUT NO IMPORTANT
FIBROSIS.
]

FIG. 77.—UNCINARIA SMITHI COILED IN INTRAHEPATIC BILE DUCTS OF
GIRAFFE. NOTE MARKED PERIDUCTAL FIBROSIS IN THE NEIGHBORHOOD OF THE
PARASITES.
]