INCIDENCE AND NATURE OF TUMORS IN CAPTIVE WILD MAMMALS AND BIRDS' HERBERT L. RATCLIFFE

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1 INCIDENCE AND NATURE OF TUMORS IN CAPTIVE WILD MAMMALS AND BIRDS' HERBERT L. RATCLIFFE (From the Labmatory of Comparative Pathology of the Zoological Society of Philadelphia and the McManes Laborahy of Pathology of the University of Pennsylvania) The literature on disease in lower animals offers very little information as to possible variations in resistance or susceptibility of different animal groups to the development of neoplasms. Observations on captive wild mammals and birds have indicated, however, that all taxonomic groups may not be equally affected and that there may be distinct differences in organ and tissue susceptibility to tumor growth. A review () of the autopsy records of more than 5000 wild mammals and birds dying in the Philadelphia Zoological Gardens has shown that tumors occurred in about 2 per cent of all specimens. Mammals were much more frequently affected than were birds, although the latter were much more numerous in this series. The incidence of tumors also varied widely for different taxonomic groups (orders) of both mammals and birds. The neoplasms found in these animals involved a variety of tissues, but the gastrointestinal tract and related organs of mammals and the renaladrenalgonad tissues of birds, respectively, were more frequently the sites of tumor growth than other parts of the bodies. The skin of birds and the mucocutaneous junction of both birds and mammals were rarely affected by neoplasms. The present report is a second survey of all cases of tumors that have been found in wild birds and mammals dying in the Philadelphia Zoological Gardens from 90 to Those instances discussed in earlier publications (, 2) have been reexamined and included in the present discussion. The material available for study has almost doubled in volume since the first review was completed (92), and the present study has been undertaken to determine how well the earlier indications would be supported by more extended observations. Read before the American Association for Cancer Research, Philadelphia, April 932. * All birds and mammals dying in the Philadelphia Zoological Gardens receive poetmortem study, but this does not include brain and cord examination, except for special casea. 6

2 TUMORS IN CAPTIVE WILD MAMMALS AND BIRDS 7 Tumor diagnoses are based upon criteria employed in human pathology. The neoplasms of lower animals differ in no essential respect from those of man. Designations of malignancy offer the same possibilities of personal interpretation. Many of the individual cases have been discussed elsewhere (, 2, 3), so that morphology of tumors will not be treated here. Consideration has been limited to those cases in which parasitism and irritations imposed by conditions of captivity had no obvious r6e. Hence the following tumorlike formations have been omitted: adenomata of the thyroid of all animals, except in cases of definite malignancy with metastasis to other organs, papillomata of the esophagus of quail (Lophotryz) infested with Capillaria, sarcomatoid nodules of the ceca of pheasants infested with Heterakis, fibromata of the esophagus and stomach of animals infested with Spirocerca, and fibromata of the feet of birds. The last mentioned growths are thought to be the result of incorrect perches. In addition to these, 0 other cases for which records were incomplete are omitted also. Cases are grouped according to the zoological order and family. Tables have been prepared giving name, sex, individual and average exhibition periods, type, origin and behavior of tumors, numbers of animals in the order and in those families for which sufficient data have accumulated to allow discussion, and the average exhibition periods for order and family. Average exhibition periods for the various groups were obtained from exhibition periods of 50 males and 50 females taken at random from the records. When less than 50 of both sexes were represented, exhibition periods for all specimens were averaged. This has been necessary only for occasional families, since those orders with less than 200 representatives have not been discussed. Exhibition periods and averages of these are given, since they are the only measure of age common to all groups studied. The total specimens for the orders include not only totals for families in which tumors have been found, but all members of that order dying in the Philadelphia Zoological Gardens. The system of taxonomy used is, in general, that published by the Zoological Society of London (4) and recently adopted by the Zoological Society of Philadelphia. This has necessitated some rearrangement of all groups of animals so that cases described here may not entirely conform to previous publications (, 2, 3).

3 8 HERBERT L. RATCLIFFE MAMMALIA The autopsy records of 0,298 animals available for study at the present time include 3400 mammals, among which 96 tumors in 89 animals have been found. These cases were distributed among 9 of 4 orders, and,. with the exception of 3 of them, are listed individually in Tables I to V. TABLE I Primates (Name, sex, individual and average exhibition periods, and type, origin, and behavior of tumors for the affected animals; number of specimens examined and average exhibition periods for the order and affected families.) Exhibition Period (in months) CERCOPITHECIDAE Papio hamadryas d... Adenomnta, stomach Papio porcarius 8... Fibrosarcoma, ulna; metastasis to lungs, heart, gluteal muscles Papio cynocephalus 9... Adenocarcinoma, pancreas Fibroadenoma, uterus Macaw f uscut us d... Epidermoid carcinoma, cardia Adenoma, bileducts Macacus pileutus 0...Papilloma, cervix Cercopithecus sabaeus 0... Adenocarcinoma, pancreas; metastasis to liver 66 Average exhibition period of tumor bearers Specimens examined, family Average exhibition period for family CEBIDAE Cebwr faatuellus d... Adenoma, adrenal.... Specimens examined, family Average exhibition period for family..... LEMURID AE Lemur mongoz d... Adenoma, prostate Specimens examined, fnmily Average exhibition period for family Average exhibition period for tumor bearers in order Specimens examined, order Average exhibition period for order The order Primates, with the largest number of specimens among the Mammalia, had the lowest incidence of tumors in this class, and the shortest average exhibition period as well. Six of the 8 tumor bearers were members of the family Cercopithecidae, which also included more than half of the total for the order. The tumor incidence for this family, and the average exhibition period, were very low as compared to other families of mammals. The average exhibition period for the tumor bearers of the

4 TUMORS IN CAPTIVE WILD MAMMALS AND BIRDS 9 TABLE I Carnivora (Name, sex, individual and average exhibition periods, and type, origin, and behavior of tumors for the affected animals; number of specimens and average exhibition periods for the order and affected families.) Exhibition Period (in months) FELID AE Felis leo 9...Adenocarcinoma, uterus; metastasis to lungs. 70 (( (( 0... Leiomyoma, uterus.... I( C?... Scirrhous carcinoma, jejunum; metastasis to mesentery Felia curacal 9...Osteochondroma, nose... 0 Felis nebulosa 3....Endothelioma, pleura Felis o m 0...Fibroadenoma, bileducts Fibroadenoma, uterus Lymphangioma, omentum Feliv pardus d...lymphangioma, mesentery Felis tip s 3....Squamouscell carcinoma, rectum Average exhibition period for tumor bearers Specimens examined, family Average exhibition period for family CANIDAE Vulpes corsac Adenoma lp. ancreas Vulpes v. pennsylvanicus 8... Adenoma, bileducts Uroyon cinereoargentem Adenoma, bileducts Canis procyonoides 3... Adenocarcinoma, thyroid; metastasis to liver, lungs Canis familiaris 3... Adenocarcinoma, skin; metastasis, lungs Cortical adenomata, adrenal Canis latrans d... Chondrosarcoma, thyroid; metastasis to liver (teratoblastoma?) Canis mezicanus d... Basalcell carcinoma, skin II I ( d.... Squamouscell carcinoma, skin; metastasis to liver, lungs I( 9... Hypernephroma, kidney; metastasis to lungs, brain ( (I 9... Adenocarcinoma, thyroid; metastasis to lung 90 Canis anthus 9... Medullary carcinoma, pancreas; metastasis to liver Lycaon pictics 9...Endothelioma, pleura.... Average exhibition period for ( I tumor bearers.... Specimens examined, family Average exhibition period for family (Table continued on page 20) order Primates was more than six times that for all animals of this group. In the family Cercopithecidae the average exhibition period for tumor bearers was about eight times that for all animals. These differences considerably exceed those of any other order or family of either mammals or birds. The order Carnivora was second in number of specimens among the mammals and was also second in frequency of neoplasms.

5 20 HERBERT L. RATCLIFFE TABLE I Carnivora (continued) VIVERRIDAE Vivma tangalunga 8... Adenocarcinoma, lungs.... Viverra zibetha 9... Adenocarcimona, urinary bladder; metastasis to liver, lymph nodes..... Paradoxurua hermaphroditus 3.. Adenocarcinoma, pancreas... Gene& genetta 8....Basalcell carcinoma, nose, with direct extension to the orbit and brain.... Average exhibition period for tumor bearers,... Specimen8 examined, f dly Average exhibition period for family..... PROCYONIDAE Exhibition Period (in months) Procyon lotor 9...Adenoma, pancreas ( 9... Adenocarcinoma, duodenum; metastasis to lymph nodes Procyon carnuorus 8... Adenocarcinoma, nose Bassar~cua aalr&!wr 9... Basdcell carcinoma, nose; metastasis to liver 64 Nasw nuaw 9...Squamouecell carcinoma, nose; metastasis to brain Average exhibition period for tumor bearers... Specimens examined, family Average exhibition period for family URBIDAIU Urswr americanua 9...Medullary carcinoma, mammary gland; metastasis to lung I d...basalcell carcinoma, tongue Urm martimua 9... Adenocercinoma, adrenals; metastasis to lymph nodes, diaphragm, lungs Urm horribilis 8...Hypernephroma, kidney; metastasis to lungs, liver, retroperitoneum Average exhibition period for tumor bearers Specimens examined, family Average exhibition period for family Average exhibition period for tumor bearers in order Specimens examined, order Average exhibition period for order Thirtysix tumors were found in 33 animals belonging to this order. The average age for the tumor bearers was less than three times that for the order. Five families of this order were represented among the animals having tumors. These were: the Felidae, Canidae, Viverridae, Procyonidae, and Ursidae. Tumor incidence per family varied between 4.0 per cent for the Procyonidae with 25 autopsies, and 7.54 per cent in the Viverridae with 53 autopsies. Other families of the order Carnivora, except the Mustelidae, were represented by very few autopsies. The Mustelidae, however, had 25 representatives on record and an average exhibition

6 TUMORS IN CAPTIVE WILD MAMMALS AND BIRDS 2 TABLE I Perissodactyla and Artiodactyla (Ungulata) (Name, sex, individual and average exhibition periods, and type, origin, and behavior of tumors for the affected animals; number of specimens and average exhibition period for the order and affected families.) PERISSODACTYLA EQUIDAE Exhibition Period (in month) Equus b. burchelli 0...Fibrosarcoma, cecum; metastasis to lung Specimens examined, family Specimens examined, order Average exhibition period for order ARTIODACTYLA BOVIDAE Biaun bison 0... Adenocarcinoma, bileducts Bos bubalis 0...Adenoma, pituitary Cupra hircus 8... Lymphosarcoma, mediastinum; metastasis to kidney, liver, lymph nodes Connochaetea gnou 0...Squamouscell carcinoma, rumen Garella iaabella ci... Osteoma, jaw Boselaphua tragocamelw 0...,Fibroma, uterus Average exhibition period for tumor bearers Specimens examined, family Average exhibition period for family., SUIDAE Swr acrofa 0... Adenocarcinoma, uterus ( 0... Adenocarcinoma, uterus; metaataais to liver, intestines, peritoneum Specimens examined, family CAMELID AE Camelua bactrianus d...cavernous hemangioma, liver, Lama pacoa d...medullary carcinoma, gallbladder; metastasis to intestines Specimens examined, family CERVIDAE Odocoileus virginianus 9... Fibroadenoma, bileducts... Specimens examined, family Average exhibition period for family..... Average exhibition period for tumor bearers in order Specimens examined, order Average exhibition period for order period of 3.7 months. These animals are similar in size and habits to the Procyonidae and Viverridae and live equally well in captivity. The absence of tumors among them is, therefore, noteworthy. The order Perissodactyla included only 39 animals in the present series. Heretofore it had been grouped with the Artiodactyla as the order Ungulata

7 22 HERBERT L. RATCLIFFE TABLE IV Rodentia (Name, sex, individual and average exhibition periods, and type, origin, and behavior of tumors for the affected animals; number of specimens and average exhibition periods for the order.) MURIDAE Peromyscus leucopus Fibrosarcoma, leg muscles; metastasis to Exhibition Period (in months) pelvis ( 9... Adenocarcinoma, mammary gland I I 9... Adenocarcinoma, mammary gland; metastasis to abdominal wall and pelvis Mus wagneri rotans 0... Adenocarcinoma, mammary gland li?... Adenocarcinoma, pylorus... 9,I 0... Adenocarcinoma, pylorus... ( I I 9... Adenocarcinoma, pylorus Fibroadenoma, mammary gland Tateru robusta 3...Fibrosarcoma, subcutis (I d... Squamouscell carcinoma, stomach; metastasis to liver I SCIURIDAE 9....Squamouscell carcinoma, skin.... Marmota monax 0...Adenoma, liver Sciurus carolinensis pennsylvanim 9...Hypernephroma, kidney Sciurua niger d... Adenocarcinoma, kidney I.. d... Adenoma, kidney Citellwr grammurus beecheyi... Osteoma, sternum... 8 HETEROMYIDAE Psrodipus richardsoni 8. I... Fibrosarcoma, urinary bladder Lymphosarcoma, generalized.... MYOCABTORID AE Myocaster coypus d... Adenocarcinoma, lung Fibroma, subcutis l( Adenocarcinoma, uterus.... DABYPROCTIDAE Dasyprocta marae 9... Squarnouscell carcinoma, larynx, CUNICULIDAE Cuniculus paca d... Lymphosarcoma, cecum; metastasis to mesenteric glands HYSTRICIDAE Hydrix longicauda 9... Scirrhous carcinoma, mammary gland; metastasis to lungs, liver, spleen, kidney JACULIDAE Jaculus jaculus?...angiolipoma, thorax ERETHIZONTID AE.Chorionepithelioma, uterus.... Erethizon dorsatum 0... Average exhibition period for tumor bearers in order.... Specimens examined, order Average exhibition period for order

8 TUMORS IN CAPTIVE WILD MAMMALS AND BIRDS 23 TABLE V Marsupialia (Name, sex, individual and average exhibition periods, and type, origin, and behavior of tumors for the affected animals; number of specimens and average exhibition periods for the order and affected families.) M ACROPODIDAE Mucropus rujus 3... Cl Exhibition Period (in months) Adenocarcinoma, stomach; metastasis to liver, spleen, kidney Adenocarcinoma, stomach; metastasis to lung, spleen..... G8 DIDELPHYIDAE LMelphys marsupidis 9... Adenocarcinoma, mammary glands... I( <( 8... Lymphosarcoma, generalized ( I ( 9... Squamouscell carcinoma, lungs Specimens examined, family Average exhibition period for family PER AMELIDAE Puruguliu lagotis 8... Adenocarcinoma, lung DABYURIDAE Dasyurus muculutus 3....Adenocarcinoma, small intestine; metastasis to liver, lungs, lymph nodes.... Dasyurus vioerrinus Medullary carcinoma, rectum.... Surcophilus ursinus?... Squamouscell carcinoma, perineum... Average exhibition period for tumor bearers in order.... Specimens examined, order Average exhibition period for order..... The order Artiodactyla was third among the mammals in numbers examined, and fourth in incidence of neoplasms. The family Bovidae, with approximately 40 per cent of the total specimens in this order, also includes 6 of the tumor bearers. Two other families, the Suidae and Camelidae, represented by small numbers of specimens, included 2 tumor bearers each, while the family Cervidae, which included 45 per cent of the total of the order, was represented by a single case among the tumor bearers. The Cervidae live and breed well in captivity although the average exhibition period has been considerably less than that for the order. However, in numbers examined and length of life in captivity the Cervidae may be compared to the Bovidae. The rarity of neoplasms among these animals is, therefore, noteworthy. The order Rodentia was fourth in magnitude among the mammals, but the incidence of neoplasms was higher than in any other order of either mammals or birds. The average exhibition period for this order exceeded that for the Primates

9 24 HERBERT L. RATCLIFFE The distribution of the tumor bearers among a relatively large number of families, none of which is well represented in total specimens, renders further discussion difficult. However, one family, the Muridae, should be mentioned. This family, with 0 tumor bearers among 67 animals, had the highest tumor incidence of any comparable group of either mammals or birds. The order Marsupialia was fifth in magnitude among the mammals and third in frequency of neoplasms. The average exhibition period for the order was considerably lowered because of the relatively short exhibition period of one family, the Didelphyidae. This family included more than half of the total for the order. In addition to the orders discussed, three others included one tumor bearer each : the Zenarthra with 50 autopsies, the Pinnipedia with 34 autopsies, and the Proboscidea with 4 autopsies. AVES The autopsy records of 0,298 animals included 6898 birds, among which 82 tumors in 8 animals have been found. These cases are distributed among 4 of 29 orders. Only 4 of these, however, will be considered in detail (see Tables VI to IX). The order Psittaciformes, with 42 tumor bearers among 75 specimens, had the highest incidence of neoplasms and the second largest number of representatives in the class Aves. All but 50 of the specimens in this order were members of the family Psittacidae, in which were included, also, the 42 tumorbearing animals. The average exhibition period for the tumor bearers was less than twice as great as that for the order. A single species, Melopsittacus undulatus, with 77 autopsies, was involved in 28 of the 42 cases, giving an incidence of tumors of 5.8 per cent. This frequency for a species is unparalleled among either birds or mammals. The order Galliformes was second among the Aves in tumor incidence. All of the tumor bearers in this order were members of a single family, the Phasianidae, which included all but 78 animals in the order. The average exhibition period for tumor bearers was less than twice as great as that for the order. The order Anseriformes, consisting of but a single family, the Anatidae, was third in tumor incidence. Sarcomatous growths predominated in this group, but with so small a series this is hardly of significance] especially since three epithelial tumors of renal origin could not be included because of incomplete records.

10 TABL~ VI Psittacijormes (Name, sex. individual and average exhibition periods. and type. origin. and behavior of tumors for the affected animals; number of specimens and average exhibition periods of order. family and one genus.) Exhibition Period (in months) P~ITFACIDAE Melopsitfucus undulatw, 0... Adenoma. kidney I d... Adenoma, kidney... I I I I I I 9... Adenoma. kidney Adenoma, kidney... d... Adenoma, kidney... d... Adenocarcinoma, kidney... d... Adenocarcinoma, kidney... d... Adenocarcinoma, kidney Adenocarcinoma, kidney... d... Adenocarcinoma, kidney Adenocarcinoma. kidney Adenocarcinoma. kidney Adenocarcinoma. oviduct Adenocarcinoma, ovary Adenocarcinoma, adrenal... d... Hypernephroma. adrenal carcinoma simplex. liver Carcinoma simplex. liver; metastasis to spleen d...fibrosarcoma. spleen; metastasis to liver.... d... Fibrosarcoma; spleen; metastasis to liver Fibrosarcoma, cloaca; metastasis to liver and spleen Fibrosarcoma. intestinal wall... d... Fibrosarcoma, intestinal wall; metastasis to liver...?...lipomata. body wall Lipomah. body wall Gliom a. brain: metastasis to liver... I d... Lymphosarcoma, generalized... d... Carcinomatoid embryoma. testis Average exhibition period for tumor bearers... Specimens examined. genus Average exhibition period for genus... Kakato& roseieapillu 9...Lipoma, abdominal wall Lipomata. abdominal wall Lipomata, abdominal wall... I?... Lipomata, abdominal wall... I 9...Lipomah. abdominal wall... Kakatoe galm ta 9... Adenocarcinoma. ovary...:... KakatoB moluccensis 6... Lymphosarcoma, generalized... Brotageris t i d... Fibrosarcoma, pectoral muscles... Aprosmictw, scapularis 9... Fibrosarcoma. ovary... Palaeornis cyanocephala?... Adenoma. kidney... Paluwrnis eupatrius 3... Carcinomatoid embryoma, testis... Conurwr holochlorua 9... Carcinomatoid embryoma. ovary... Ara militaris c?... Squamouscell carcinoma. esophagus... Leptolophua houandicwr?... Lipomata. body wall... Average exhibition period for tumor bearers in order... Specimens examined. order Average exhibition period for order

11 26 HERBERT L. RATCLIFFE TABLE VII Gallijormes (Name, sex, individual and average exhibition periods, and type, origin, and behavior of tumors for the affected animals; number of specimens examined and average exhibition periods for the order and affected family.) PHASIANIDAE Adenocarcinoma, lung.... Exhibition Period (in months) Genmeue nycthemerus 3... Chryaolophue pictue 0... Adenocarcinoma, kidney I I I 9... Adenocarcinoma, adrenal; metastasis to lung, liver, and heart It I d......adenoma, cloaca I I d......adenoma, kidney ( I I Adenoma, kidney Phaaianue versicolor 3...Fibrosarcoma, cecum II d... Lymphosarcoma, generalized Meleagris gallopavo 0... Adenocarcinoma, ovary; metastasis to kidney. 46 Average exhibition period for tumor bearers Specimens examined, family Average exhibition period for family Specimens examined, order Average exhibition period for order TABLE VIII Anserijormes (Name, sex, individual and average exhibition periods, and type, origin, and behavior of tumors for the affected animals; number of specimens examined and average exhibition periods for the order.) Exhibition Period (in months) ANATDAE Anser domestiezls 0... Fibrosarcoma, pectoral muscles; metastasis to kidney Anser fubalis 0....Myxosarcoma, pectoral muscles Chen h. hyperboreus 0...Fibroma, clavicle Anm phtyrhynchos Adenocarcinoma, ileum Plectropterus gamb&s Fibrosarcoma, humerus; metastasis to lung.. 35 Average exhibition period for tumor bearers Specimens examined, order Average exhibition period for order The order Passeriformes was by far the largest group included here, but tumor incidence was lower than for any comparable group of either birds or mammals. The average exhibition period of the tumor bearers was about twice that for the order. This order included a very large number of similar varieties, all of which were maintained under much the same conditions, and

12 TUMORS IN CAPTIVE WILD MAMMALS AND BIRDS I27 TABLE IX Passerif ormes (Name, sex, individual and average exhibition periods, and type, origin, and behavior of tumors for the affected animals; number of specimens and average exhibition period for the order.) FRINQILLID AE Exhibition Penod (in months) Siealia Jlaveola d... Adenocarcinoma, kidney Emberiza icteriea 8....Lipoma, scalp Paroaria cilcullala Myxosarcoma, knee Sm nus canarius 0... Lymphoid leucosis II il 0...Lymphoid leucosis PLOCEIDAE Taenwpygia caslanotia d... Adenocarcinoma, kidney; metastasis to lung. Queka quelea d...carcinomatoid embryoma, testis.... (I li d... Carcinomatoid embryoma, testis.... TIMALIIDAE Turdoides lerricolor 0....Adenoma, kidney Dryonastes berlhemgi 3... Fibrosarcoma, scalp Adenoma, kidney TANAQRID AE Thraupia palmarum d...lipoma, body wall ICTERIDAE Megaquisculw major 3... Adenocarcinoma, pancreas; metastasis to intestines... Wild TURDIDAE Planedieus m. migratorius 0... Hypernephroma, kidney; metastasis to intestines Turdw merula?... Hypernephroma, kidney; metastasis to liver. 42 Average captivity period for tumor bearers Specimens examined, order Average captivity period for order the tumor bearers were distributed among 5 families. The family Fringillidae, with 79 autopsies and an average exhibition period of 27.6 months, included 5 tumor bearers. The family Ploceidae, with 059 specimens and an average exhibition period of 36.9 months, included 3. The other 3 families had slightly more than 00 representatives each. The single case listed in the family Icteridae was included as evidence for tumors in birds under natural conditions. This bird, a fantailed grackle, was found dead in the garden. In addition to the cases tabulated, tumors were found in birds belonging to 0 other orders. The orders Accipitriformes and Strigiformes included 2 cases each. Eight other orders each had a single case. 46 8

13 28 HERBERT L. RATCLIFFE The data given in the preceding tables are summarized and compared with the survey of 92 in Table X. The increase in total specimens of both mammals and birds over the elevenyear period from 92 to 932 was accompanied by a proportional increase in the numbers of neoplasms discovered. There have been no pronounced variations of the incidence of tumors per order of mammals. Changes have occurred, but are TABLE X Summary of Tumor Incidence and Types of Tumors, Comparing Present Records with Those of 92 Order Primates }... Lemures Carnivora.... Perissodactyla... Artiodact yla } Rodentia..... Marsupialia... Others... ALL MAMMALS..... Psittaciformes... Galliformes... Anseriforrnes.... Passeriformes.... Accipitriformes... Strigiformes... Columbiformes... Others..... ALL BIRDS..... ALL ANIMALS Total , , ,505 5,365 Tumor 3ear era Incidence Total E. F rtioc , E. Epithelial origin. F. Fibrous Pissue in origin. * Three cases not included because of incomplete records., , ,898 0,298 runor bear. I Tumors Inci dence era E. F :tyl !I ! 8 3 i * slight, and have resulted in only one change of relative frequency, that between the orders Carnivora and Marsupialia. The situation is much the same among the 4 orders of birds. The order Galliformes, now second in frequency of tumors, is the only group to show a pronounced increase. The apparent decrease of tumor incidence for the order Anseriformes is explained by the fact that 3 cases could not be included. The orders Accipitriformes, Strigiformes, and Columbiformes have not shown in

14 TUMORS IN CAPTIVE WILD MAMMALS AND BIRDS 29 creases in tumors comparable to other avian groups, but the numbers in these 3 orders are too small to allow adequate discussion. There are at least two possible explanations for the fact that relative tumor incidence has remained unchanged in this series. () Susceptibility to tumor growth may be equal in all of the groups studied, but unequal adaptability to captive conditions may not allow equal opportunity for tumor development; or (2) the dif TABLE XI Comparison of Tumor Incidence for Families of Mammals in Terms ofthe Ratio of Average Exhibition Period to Estimated Longevity and in Terms ofthe Ratio of Average Exhibition Period of All Animals to Average Exhibition Period of Tumor Bearers in the Respective Families. Mammala PRIMATES... Cercopithecidae... Cebidae... CARNIVORA... Felidae... Canidae... Mustelidae.... Procyonidae... Viverridae... Ursidae... ARTIODACTYLA... Bovidae... Cervidae.... RODENTIA... Muridae... Sciuridae... Maturity Period w mo. yr. 3 mo. yr. MARBIJPIALIA... Macropodidae... 3 Didelphyidae... Mimated iongevity W8. loa Avera e Ca tivity herid All Tumor Animala Bearers YE YE Incidence ferences in tumor incidence found in this series may be expressions of natural resistance or susceptibility to neoplasia. A test of either possibility is dependent upon the following assumptions: () The average relative ages of different orders and families are equal when the animals enter the collection, and (2) the percentages of tumor bearers in any group will increase as the average age increases. Thus, if susceptibility to tumor development be equal in all groups, the incidence of tumors will be proportional to the ratio of the average exhibition periods to the

15 30 HERBERT L. RATCLIFFE natural longevity of the animal group. Exact knowledge as to longevity of various types of wild animals is scanty, but numerous attempts have been made to estitnate life span of animals generally (5, 6). For the present study, longevities of mammals have been estimated in terms of the time required for sexual maturity. This period, multiplied by 5, is taken as an estimate of the life span. These computations are seriously embarrassed by lack of exact information of the time required for sexual maturity in different TABLE XI Comparison of Tumor Incidence for Families of Birds in Terms of the Ratio of Average Exhibition Periods for All Animals to Average Exhibition Periods for Tumor Bearers in the Respective Families. PSITTACIFORMES Psittacidae... Melopsittacus... G ALLIFORMES Phasianidae... ANBERIFORMES Anatidae... PASSERIFORMES Fringillidae... Ploceidae... Average Captivity All Animals Tumor Bearers m. v Incidence families of mammals. The figures given are based upon known sexual maturity periods of related domesticated species and observations on wild animals that breed in captivity. At best the maturity periods and longevities given in Table XI are approximations. Limiting discussion to the families, it is seen that, in general, those for which the ratio of average captivity period to the estimated longevity is low have a relatively high incidence of neoplasms. For instance, the families Viverridae, Ursidae, and Canidae have more than 5 per cent of their numbers affected by neoplasms, and the ratio of average exhibition period to estimated longevity is under to 4. Conversely in those families for which this ratio is high the percentage of tumor bearers is low (Cercopithecidae, Macropodidae, and Didelphyidae). It is also seen, from this tabulation, that, in general, the percentage of tumor bearers per family has a similar relationship to the

16 TUMORS IN CAPTIVE WILD MAMMALS AND BIRDS 3 ratio of the average exhibition period for all animals in the family to the average exhibition period for tumor bearers. In either case the percentage of tumors in most families of mammals increases as the average age (exhibition period) increases. However, age alone does not explain the incidence of tumors in all mammalian families. The Mustelidae, Cervidae, and Cebidae compare well both in numbers autopsied and average length of life with other families of their respective orders, but these animals have developed very few neoplasms. Accordingly they are cited as possible examples of natural resistance to tumor development. Conversely the high incidence of tumors among the Muridae may be taken as indicating natural susceptibility to tumor growth. Since sexual maturity periods and longevities for wild birds are so imperfectly known, the differences in tumor incidence among the avian families have been compared only in terms of the ratio of average exhibition periods for all specimens in the family to the average exhibition period for tumor bearers (see Table XII). The ratio of average exhibition periods for the avian families to average exhibition period for tumor bearers of the families, in general, bears the same relation to tumor incidence as among the mammals. But, while there are wide differences in incidence of tumors per family of birds, the variations of the ratio of average exhibition period for the family to average exhibition period for tumor bearers in the family are not nearly so striking as with the mammals. However, it does not seem that age alone can explain the high percentage of tumor bearers in the genus Melopsittacus, the undulated grass parrakeets. The average exhibition period of these birds is no greater than that of the small song birds, Fringillidae, and other avian groups which have a very much lower percentage of tumors (see Table XII). Hence the undulated grass parrakeet, Melopsittacus undulatus, is cited as a possible example of naturally occurring susceptibility to tumor growth. The very low incidence of tumors in the Passerine family Ploceidae may, perhaps, be taken as a further example of natural resistance to tumor development. The ratio of average exhibition period for the family Ploceidae to average exhibition period for tumor bearers of the family is less than : 2, but tumor incidence is very low, 0.28 per cent. More than 000 birds belonging to this family were examined post mortem. Further analysis of the tumors occurring in this series of wild

17 32 HERBERT L. RATCLIFFE animals, in terms of the organs involved and tissues serving as foci of neoplastic change (Table XIII), shows that the digestive tract of mammals was the predominant site of tumor formation, and that epithelial newgrowths uccurred much more frequently than those of fibrous tissue. The genitourinary organs, the respiratory tract, and the skin and accessory structures also were often involved, and epithelium rather than fibrous tissues again predominated as the focus of tumor growth. TABLE XI Anatomic Distribution and Histogenesis of Tumors Integument Thyroid Adrenal Primates... Carnivora Perissodactyla.,,, Artiodactyla I Rodentia..... Marsupialia..... Othera... TOTAL ANIMALS Psittaciformes..... Galliformes... Anseriformes... Passeriformes... Others.... I E. F. 6 2 l4 2 E. F E. F. E. F TOTAL BIRDS l 4 E. Tumors of epithelial origin. F. Tumors of fibrous tissues. * Not included in total. The genitourinary organs of birds were the most important sites of tumor growth, and by far the greater number developed from epithelium. Tissues of the digestive tract and related structures also were frequently involved. These observations apply in a general way to all of the orders of mammals and birds, that is, the averages of organ system and tissue involvement for the classes apply very well to the distribution of tumors in the various orders. The notable exception was tumor formation in the integument of mammals, in which only 3

18 TUMORS IN CAPTIVE WILD MAMMALS AND BIRDS 33 orders were involved, and for one of these, the Rodentia, more tumors occurred in the surface structures than in any of the organ systems. The absence of neoplasms of the skin among horned animals, Artiodactyla, that are exhibited in large groups is noteworthy. It is of interest, also, that no skin tumors are recorded for birds. The one case of skin tumor found among birds could not be included because of incomplete records. DISCUSSION The data presented here are the results of observation on wild animals that have lived in an abnormal environment. Whether or not they are applicable to life under natural conditions may be questioned. However, the attempt has been made to eliminate cases in which abnormal stimuli, such as animal parasites and incorrect housing facilities, may have induced chronic tissue repair, The importance of unnatural diet and dietary deficiencies, and the lack of natural associations and activities, in the production of tumors should be considered, although these influences are by no means definite. It may well be that those mammalian and avian families cited as possible examples of immunity or susceptibility to tumor growth have been influenced by captivity and that their reactions under natural conditions would be entirely different. It is not intended, however, that these observations be regarded as conclusive in any way. They are merely to be taken as an index of variations of tumor growth in the various animal types available for study at this institution. Within these limits the records analyzed here seem to allow the following tentative generalizations : () Incidence of neoplasms for various orders and families of mammals and birds as found in the Philadelphia Zoological Gardens is apparently chiefly dependent upon two factors: average age of the group, and resistance or susceptibility to neoplasia. (2) Epithelial tissues of the organs of the digestive tract of mammals and the genitourinary apparatus of birds are more often subject to tumor growth than other parts of the bodies..(3) The class Aves is less affected by tumor growth than is the class Mammalia. There is little support for these assertions in the reports of postmortem observations on animals dying in the gardens of the Zoological Society of London (7). According to the publications of this Society, the incidence of tumors among mammals and birds dying in their gardens was less than half that for the Philadelphia

19 34 HERBERT L. RATCLIFFE collection. However, the relative frequency of tumors among birds and mammals was approximately the same as reported here, although tumors of fibrous tissues occurred more often, especially among birds. The yearly death rate of animals exhibited in the London gardens has been 5 to 0 per cent higher than that in the Philadelphia gardens (8), and in those reports (9) giving death rates for both mammals and birds, the latter have had the lower frequency. In general, the reverse has been true for the Philadelphia gardens, mammals usually having had a lower yearly death rate (8). Hence it is difficult to explain the consistently lower frequency of tumors among birds as compared to mammals, although the higher death rates for the London gardens may account for the higher frequency of fibroustissue tumors. Studies on neoplasms of domesticated animals also offer little in support of the assertions made here with regard to the occurrence of tumors in lower animals. The records compiled by Feldman (0) show that, for the horse, cow, and dog, tumors increase in frequency as age increases. Records of tumors in other domesticated species are scanty. It is extremely difficult to compare reports of neoplasms in domesticated animals with observations on related wild species. Animals used for food receive postmortem study, but this rarely is extended to microscopy of tumors, and, the animals being slaughtered at a relatively early age, the incidence of tumors means very little. Many of the reports of tumors in domesticated animals have been concerned with a single type of neoplasm, without consideration of the relative frequency of other forms. So far as can be determined from available information, however, epithelial tumors rather than those of fibrous tissues predominate in dogs and cattle, while the reverse is true for horses. The skin and accessory structures of the dog, the gastrointestinal organs of the cow, and the genitourinary organs of the horse appear to be the important sites of tumor development. The common fowl seems to be the only domesticated avian species that has been well studied, and here the organs of the genitourinary apparatus have been most frequently affected by tumors. However, in view of the incompleteness of available data, it may be said that there are no clearcut examples among domesticated animals of racial resistance or susceptibility to tumor development that are entirely comparable to the instances observed among captive wild animals in the Philadelphia Zoological Gardens.

20 TUMORS IN CAPTIVE WILD MAMMALS AND BIRDS 35 SUMMARY The incidence of neoplasms for the orders and families of birds and mammals dying in the Philadelphia Zoological Gardens has shown very little variation over a period of eleven years. The percentage of animals in most orders and families that are affected by tumor growth is proportional to the average exhibition period of the group. That is, as age increases, incidence of tumors increases. Certain families of both birds and mammals have, however, a much lower incidence than should be expected from the average age for the group. Other avian and mammalian groups have much higher percentages of tumor bearers than the average age seems to warrant. Mammals, generally, are more subject to new growths of the digestive organs and birds to new growths of genitourinary organs than to neoplasms affecting other parts of the bodies. The class Aves is, as a whole, less subject to tumor growth than the Mammalia. REFERENCES. Fox, H.: Disease in Captive Wild Mammals and Birds, J. B. Lippincott, Philadelphia, Fox, H.: Observations upon neoplasms in wild animals in the Philadelphia Zoological Gardens, J. Path. & Bact. 7: 27, Fox, H.: Reports of the Laboratory and Museum of Comparative Pathology of the Zoological Society of Philadelphia, List of Vertebrated Animals exhibited in the Gardens of the Zoological Society of London. Vol. I. Mammals, by s. s. Flower; Vol.. Birds, by G. C. LOW, London, The Zoological Society. 5. MITCHELL, P. C. : On longevity and relative viability in mammals and birds, with a note on the theory of longevity, Proc. Zool. SOC. London, 9, p Fox, H. : Some observations on comparative constitution in man and lower animals, Proc. Am. Phil. SOC. 68: 27, Reports on the deaths occurring in the Society s gardens during the year, Proc. Zool. SOC. London, Fox, H.: Report of the Laboratory and Museum of Comparative Pathology of the Zoological Society of Philadelphia, HAMMERTON, A. E.: Reports on the deaths occurring in the Society s gardens during the year: 928, 929, and 930, Proc. Zool. SOC. London, 929, p. 49; 930, p. 357; 93, p FELDMAN, W. H.: Neoplasms of Domesticated Animals, W. B. Saunders Co., Philadelphia, 932. (For Discussion see page 72)