PRIMATES, 8:75-82 (1967)

Parasites of the Kenya Baboon: Arthropods, Blood Protozoa and Helminths (Kenya, i966) ROBERT E. KUNTZ and BETTY ~UNE MYERS Department of Parasitology, Division of Microbiology and Infectious Diseases, Southwest Foundation for Research and Education San Antonio, Texas

Although there is an impressive list of parasites for baboons, a recent compilation (MYERS & KUNTZ, 1965) has stressed the great need for parasitological studies in the field where the baboons occur. A large proportion of records for baboons, as well as for other primates, is based upon an examination of hosts in which the parasite fauna has been greatly modified by varying periods in captivity. The desirability of survey type studies to provide more accurate host-parasite data on natural infections is obvious. The present report is one part of multidiscipline investigations conducted by the Division of Microbiology and Infectious Diseases of the Southwest Foundation for Research and Education (SFRE) in Kenya early in 1966. It is a continuation and expansion of parasitological studies on the Kenya baboon taken in different localities in 1964 (KALraR et al., 1965; KVNTZ & MYERS, 1966). Hosts were examined in three areas representing different ecological habitats. MATERIALS AND M E T H O D S On occasion, it was necessary to resort to shooting, but the majority of hosts was captured in baited live traps. Immediately after anesthetization with Sernylan (Parke-Davis, Detroit, Michigan), baboons were taken to the field laboratory. Ectoparasites were preserved in 70 per cent ethyl alchol. Thick and thin blood smears were prepared, the latter fixed in methyl alcohol, and all were stained with Giemsa. Standard technics were employed for parasite examination. After gross examination and collection of materials for associated microbiological disciplines, the viscera were removed from the carcass and placed in separate containers to minimize mixing of parasites. Organs were viewed macroscopically, prior to maceration and stripping to expose smaller parasites. Parasites were removed from This work was supported by Grant #5-R01-HE-03834-07 from the National Institutes of Health, U.S. Public Health Services.

76

R . E . KUNTZ & ]3. J. MYERS

macerated tissues after shaking in widemouth screw cap bottles and/or standing in several changes of clear well water. This technic increases parasite recovery since repeated washing facilitates removal of mucus, blood and other detritus which interfere with microscopical examination of materials. Parasites were transferred from sediments to clear water for final removal of debris. Helminths, after standing for 1/2 to several hours, were killed in hot water and then transferred immediately to formalin, acetic acid and alcohol (FAA) for fixation. After fixation, specimens were placed in screw cap vials with 70 per cent alehol plus 3 per cent glycerine, for return to San Antonio. Several blocks of tissue were removed from each lobe of lungs and fixed in 10 per cent formalin to allow for examination for lung mites. Each carcass was reexamined for the presence of filarial worms, sparganums, etc., which normally occur in somatic tissues. One gram of fecal material was removed from the lower bowel and preserved in merthiolate-iodine-formalin (MIF) solution (SAvP.RO& LAWLESS,1953), to permit a study of intestinal parasites and commensals. Cestodes were stained with Ehrlich's haematoxylin and nematodes were cleared in phenol to facilitate identification. In an attempt to provide accurate host, as well as parasite identification, study skins and associated skeletal materials were prepared for subsequent support in taxonomic evaluations of the Kenya baboon. Parasites and the SFRE collection of baboon study skins, with accompanying ecological data, have been deposited with the National Helminthological Collections (U. S. National Museum, Washington, D. C.) and the Division of Mammals of the same institution, respectively. If desired, more detailed host-parasite correlations may be made at a later date, after the current controversy of baboon taxonomy has been cleared. Subspeeifie or other designations indicating geographic variations of this primate must await final study of the Kenya and other collections. For present use, the Kenya baboon has been referred to as Papio doguera. Baboons were studied from three areas (Map 1): I. Kilifi (39 ° 8' E. 3 ° 7' S.) located near sea level in the coastal zone about 33 miles north of Mombasa, in an area classed as "coastal high grassbush" and "scattered tree grassland" (TRAV~ELL& LANGDALE-BROWN, 1962), with coastal sediments of red-yellow-sandy loams; II. Kimani (37 ° 5' E. 2 ° 8' S.) -located on the peneplain just east of the Masai-Amboseli game reserve in an area classed as "scattered tree grassland" and "desert-grass-bush," with variable soil types including mixed calcareous loams, greybrown silts and "black cotton" clays, at an altitude of approximately 4,000 ft. ; and III. Mau Narok (36 ° 0' E. 0.5 ° 0' S.), with 2 habitats worked 18 to 25 miles south of Nakuru in areas generally classed as "scattered trees and open grassland" interrupted by "highland grassland and highland forests" at 6,000 to 8,200 ft., characterized by a mixture of soil types, including calcareous sandy loams with some humic surface soil as welt as limestone outcroppings. For more detailed information on localities in which baboons were taken, reference should be made to KALTER et al. (ms).

Parasites of Kenya Baboon

77

$UDAN

-

/

UaANDA

",4

.', If'l; KENYA

HouNaro~ LAKE 'VICTORIA eNAIROBI

"Kim~ni

, .~x~\, f

? Map. 1.

Localities for study on parasites of Kenya baboons.

DISCUSSION Baboons are characterized, in part, by their extensive geographical distribution and by their adaptability to a wide variety of habitats. They range from the wooded grassland habitats of low lying coastal areas to the fairly open semi-arid, thornbush and savannah regions at middle altitudes (2,500 to 5,000 ft.) as well as to the higher, more heavily forested upland grass and mountainous areas above 9,000 ft. These primates are omnivorous, and have varying contact with man and other vertebrates dwelling in the same habitats. Even a moderately thorough evaluation of the parasitological problems associated with the widely scattered populations of Papio in the different ecological zones of Kenya would demand more field data and information than is currently available. Although the quantity of parasitological material in the present study is limited and does not warrant detailed correlation between hosts and the geographical areas from which obtained, certain trends or generalizations are indicated.

78

R.E. KUNTZ& B. J. Mx,ERs

Records in this report are based upon parasites obtained by external and internal examination of hosts in the field. For purposes of discussion, parasites are grouped by large, general categories and the numbers of hosts infected are indicated in Table 1. A R T H R O P O D S - Ticks: Amblyomma sp. were removed from baboons captured at Kilifi and Kimani. One male at the latter site was infested with both larvae and nymphs; Ixodes rasus NEUMANN, 1899, was recorded for 2 Papio taken at Mau Narok (1 5~ adult and nymphs); and Rhipicephalus puchellus (GERSTACKER, 1873) were attached to 3 baboons examined at Kimani. Lung mites: Lung mites and[or associated lesions were observed in the tissue samples from some hosts at all sites of collection, with the greatest rates of infection recorded for Mau Narok. Two species of lung mites, Pneumonyssus santos-diasi ZUMVT and TILL, 1954, and P. mossambicensis ZUMVT and TILL, 1954, have been recognized in our collections, but the taxonomic determinations have not been finalized. BLOOD P A R A S I T E S - Hepatocystis kochi (LAVERAN, 1899) GARNHAM, 1948, a haemosporidian common to the subhuman primates of Africa, was well represented in two of three populations sampled, but was absent in Papio taken at the higher Table 1. Arthropod, blood, and helminth parasites of Kenya baboon. Parasites ARTHROPODS Ticks Ambylomma sp. Ixodes rasus Rhipicephalus puchellus Lung mites Pneumonyssus santo-diasi Pneumonyssus mossarnbicensis BLOOD PARASITES Hepatocystis kochi HELMINTHS Cestodes Bertiella studeri Nematodes Abbreviata caucasica Oesophagostomum bifurcum Protospirura murlcola Streptopharagus pigmentatus Trichuris sp.

Localities KILIFI

KIMANI

MAU NAROK

1/6 0/6 0/6

2/19 0/19 3/19

0/18 2/18 0/18

2/6 0/6

8/19 2/19

11/18 0/18

4/6

8/19

0/18

1/6

3/19

5/18

0/6 6/6 0/6 2/6 1/6

15/19 2/19 2/19 8/19 9/19

0/18 15/18 0/18 0/18 3/18

Parasites of Kenya Baboon

79

altitudes in the vicinity of Mau Narok. No microfilariae were detected in peripheral blood smears. H E L M I N T H S - Cestodes: The anoplocephalid tapeworm, Bertiella studeri (BLANCI-IARD,1891) STILES and HASSAL, 1902, a species reported from man as well as from new and old world monkeys, was represented in baboons sampled in all three localities. Nematodes: Abbreviata caucasica (yON LINSTOW, 1902) SCI-IULZ, 1927, a member of the physalopteridae, was removed from the intestinal tract of the majority of hosts examined at Kimani, but it was not found in baboons examined in the coastal habitats at Kilifi or the mountainous terrain of Man Narok. Oesophagostomum bifurcum (Cm~PLIN, 1849) RAILLI~T and HE~IRY, 1906, a strongylid nematode commonly recognized as the nodular worm and widely distributed in African primates, was recorded from all hosts taken at Kilifi and in the majority processed at Mau Narok. The rate of infection, however, was much lower in the Kimani baboons. Protospirura muricola GEDOELST, 1916, a spirurid ordinarily associated with rodents as hosts, was recovered from two Papio captured at Kimani. The genus Streptopharagus is commonly found in carnivores, rodents, and primates. In the present field study, Streptopharagus pigmentatus (YON Lr_NSTOW, 1879) RAILLIETand HENRY, 1918, occurred in baboons residing in the coastal area and in the open habitats at the middle altitudes of Kimani, but it was absent in animals processed at 6,000 to 8,200 ft. in the vicinity of Mau Narok. The whipworm, Trichuris, noted for its presence in primates, is listed for baboons in each of the three ecological habitats in which we worked. A specific designation for this parasite will not be available until a comparative study has been completed for members of the genus from different primates. No trematodes or acanthocephalans were recorded. NELSON (1965) has discussed in some detail host-parasite relationships, reservoir host situations and the biological requisites for infection of baboons. The probability for parasitism by helminths in these hosts runs high, as indicated in NELSON'S statement, "It is uncommon to find a baboon which is free of worms . . . . " Even though there is considerable information on the helminth parasites of Papio, most data have been collected incidental to overall or ancillary studies with little regard for ecological or geographic relationship. The present study is a preliminary step along the latter line. Although ticks do not occur in great abundance on baboons, several species have been reported for Papio in Africa (HooGSTRAAL& THEILER, 1959; THEILER, 1962; MYERS & KUNTZ, 1966). The importance, however, of the association of baboons, ticks and "Q" fever has been stressed by other investigators (KALTER,1965 ; NELSON,1965). With examination of hosts in the wild, establishment of new host records, e.g., Ixodes rasus and Rhipicephalus puchellus, as in the present report, is none too surprising since baboons are constantly on the move through the different ecological habitats in which these ectoparasites occur on other hosts. We failed to

80

R.E. KtrnTZ & B. J. MYnas

find other ectoparasitic arthropods in this study, but the louse Pedicinus hamadryas MJ~BERG, 1910, has been removed from a number of Papio doguera shipped to San Antonio from Kenya (KUNTZ & MYERS, in press) and trombiculid mites have been found attached to baboons examined in the Ruana Plains area of the Serengeti National Park (MYERS & Kuntz, unpublished). Lung mites apparently occur in baboons from many geographic areas (STRONG et al., 1965; MYERS • KUNTZ, 1965) and the nature of the life cycle precludes association with any particular habitat. Only Hepatocystis kochi was detected in the peripheral blood in this study. However, a long list of blood parasites, including several species of Plasmodium, have been recorded previously (MYERS & KUNTZ, 1965). The parasite was found in 92 of 122 Papio examined at Darajani by STRONG et al. (1965), and we recorded it from three different localities at 5,500 ft. and lower, in our previous study (KTJNTZ & MYERS, 1966). GARNHAM et al. (1961) made similar observations relative to altitude and infection, and he failed to detect H. kochi in primates taken above 6,500 ft. Helminths, depending upon requisites for completion of their cycles, may be associated with one type of habitat, but not another. The large tapeworm Bertiella studeri is supposedly dependent upon oribatid mites for propagation of the cycle. However, the distribution for this parasite apparently is not jeopardized to any great extent by an obligatory intermediate host, since Bertiella-infected baboons occur in many areas representing a wide range of ecological habitats. There is a definite hostage relationship for this cestode. We have found the parasite to be much more common in young baboons, whether examined in the field immediately after capture, or after several weeks in captivity. Variable relationships are manifest for some of the nematodes which depend on different invertebrates for propagation. In the present study, Abbreviata was found in the semi-dry region at the middle altitudes of Kimani, but not in the coastal or mountainous habitats, and Streptopharagus was not found in baboons taken in the upper altitudes of Man Narok. Oesophagostomumand Trichuris, nematodes with direct life cycles, were found in hosts at the 3 localities sampled, and have proved to be common parasites in the other survey type studies (KUNTZ & MYERS, 1966 and in press). T h e infection of 2 baboons by Protospiruramuricola constitutes a new host record. An appearance of Protospirura in Papio in the Kimani area is not entirely unexpected since the area is well populated with rodents, game and other primates, some of which obviously serve as optimal hosts. More detailed studies in Kenya may show this nematode to commonly parasitize baboons in some areas. BAYLIS (1928) has listed 16 species of rodents as the hosts for Protospirura in Nigeria alone, and FOSTERand JOHNSON (1939) have reported a situation in which this parasite was responsible for deaths in colonies of new world monkeys. Possibly, closer scrutiny of mixed collections of the large, fleshy nematodes removed from primates and other African vertebrates will show it to be more common that presently recognized. It is an accepted fact that the parasite record for a host in a given area is an ex-

Parasites of Kenya Baboon

81

pression of successful parasitism dependent upon a multitude of biological potentials which characterize the area. Unfortunately, most survey type investigations have not been sufficiently extensive or detailed to demonstrate the interrelationships of the baboon and its parasites to other parasite bearing vertebrates, including man, in the same habitat. SUMMARY Ticks occurred on some baboons examined at all habitats (coastal plain; semiarid, grassland thorn shrub, peneplain at 4,000 4-ft. ; upland grass and forest mountainous area at 6,000 to 8,200 ft.) and Ixodes rasus and Rhipicephalus puchellus are reported for the first time from Papio doguera. Pneumonyssus santos-diasi was observed in the three geographic areas studied, but Pneumonyssus mossambicensis was found only at the middle altitude. Hepatocystic kochi, however, was not detected in baboons taken at higher altitudes. Bertiella studeri parasitized baboons in each habitat. Ecological or habitat relationships were indicated for some of the nematodes: Abbreviata caucasica was removed from most hosts on the semi-dry thorn shrub plain at the middle heights, but not from animals in localities studied below and above this habitat; Oesophagostomum bifurcum and Trichuris parasitized baboons in the three habitats, but Streptopharagus pigmentatus was not recorded in Papio taken at 6,000 to 8,200 ft. ; Protospirura muricola was found in two baboons from the semidry thorn shrub plain at middle heights and constitutes a new host record.

Acknowledgments The authors wish to express their indebtedness to: Dr. S. S. Kalter, Division of Microbiology and Infectious Diseases, Southwest Foundation for Research and Education, for general support in field studies; Dr. Henry W. Setzer, Division of Mammals, U. S. National Museum, Washington, D. C. for identification of hosts; Dr. Harry Hoogstraal, Naval Medical Research Unit No. 3, Cairo, Egypt, U.A.R., for identification of ticks; Dr. William B. Hull, Bureau of Medicine and Surgery, Navy Department, Washington, D. C. for identification of lung mites, and Mr. William Maples for assistance in procurement of baboons. REFERENCES BAYLIS,H.A., 1928. On a collection of nematodes from Nigerian mammals (chiefly rodents). Parasitology, 20(3): 280-304. FOSTER, A.O. & C.M. JOHNSON, 1939. A preliminary note on the identity, life cycle and pathogenicity of an important nematode parasite of captive monkeys. Am. J. Trop. Med. Hyg., 19(3) : 265-277. GARNHAM,P.C.C., R.B. HEISCH,& D.M. MINTER,1961. The vector of Hepatocystis (Plasmodium) kochi: The successful conclusion of observations in many parts of tropical

82

R.E. KUNTZ& B. J. MYERs

Africa. Trans. Roy. Soc. Trop. Med. ~ Hyg., 55(6): 535-537. HOOGSTRAAL, H. & G. TrtEILER, 1959. Ticks (Ixodoidea, Ixodidae) parasitizing lower primates in Africa, Zanzibar and Madagascar. J. Parasitol., 45(2): 217-222. KALTER,S.S., 1965. Virus studies on normal baboons. In: The Baboon in Medical Research, H. VAGTBORQ(ed.) Proceedings of the First International Symposium on the baboon and its use as an experimental animal University of Texas Press, Austin, pp. 407-420. - - , R.E. KtrNTz, Y. AL-DooRY, & A. KATZBERQ, 1966. Collection of biomedical study materials from baboons (Papio sp.) in Kenya: Preliminary report. Laboratory Animal Care, 16(2): 161-177. - - , B.J. MYERS, A.K. EUGSTER, A.R. RODRIGUEZ,M. BEHNKE, • G. V. KALTER (Unpublished data). The collection of biomedical specimens from baboons, Kenya, Africa, 1965. (Manuscript). KuIqTZ, R.E. & B.J. MYERs, 1966. Parasites of baboons (Papio doguera PUCHERAN,1856) captured in Kenya and Tanzania, East Africa. Primates, 7(1): 27-32. - & - - , in press. Microbiology parameters of the baboon (Papio). In: The Baboon in Medical Research Vol. II, H. VAGTBORG(ed.) Proceedings of the Second International Symposium on the baboon and its use as an experimental animal. University of Texas Press, Austin. MYERs, B.J. & R.E. Ku~qTZ, 1965. A checklist of parasites reported from the baboon. Primates, 6(2) : 137-194. - & (Unpublished data), NELSON, G.S., 1965. The parasitic helminths of baboons with particular reference to species transmissible to man. In: The Baboon in Medical Research, H. VAGTBORG(ed.) Proceedings of the First International Symposium on the baboon and its use as an experimental animal. University of Texas Press, Austin, pp. 441-470. SAPERO, J.J. & D.K. LAWLESS,1953. The M I F stain-preservation technic for the identification of intestinal protozoa. Am..[. Trop. Med. ~ Hyg., 2: 613-619. STRONG,J.P., J.H. MILLER,& H.C. McGILL (JR.), 1965. Naturally occurring parasitic lesions in baboons. In: The Baboon in Medical Research, H. VAGTBORG(ed.) Proceedings of the First International Symposium on the baboon and its use as an experimental animal. University of Texas Press, Austin, pp. 503-512. THEILER, G., 1962. The Ixodoidea parasites of vertebrates in Africa south of the Sahara (Ethiopian Region). Project S. 9958. Report to the Director of Veterinary Services. Onderspoort June, 1962. 260 pp. TRAPNELL, C . G . & I . LANGDALE-BRoWN,1962. Natural resources of East Africa. In: The Natural Vegetation of East Africa, E. RUSSELL(ed.) The English Press, Nairobi, Kenya, pp. 92-102. [Received Nov. 29, 1966]