TRYPANOXYURIS (TRYPANOXYURIS) MINUTUS ASSOCIATED WITH THE DEATH OF A WILD SOUTHERN BROWN HOWLER MONKEY, ALOUATTA GUARIBA CLAMITANS, IN RIO GRANDE DO SUL, BRAZIL^*

TRYPANOXYURIS (TRYPANOXYURIS) MINUTUS ASSOCIADO COM A MORTE DE BUGIORUIVO ALOUATTA GUARIBA CLAMITANS, NO RIO GRANDE DO SUL, BRASIL

ABSTRACT

This paper reports the death of a wild, subadult male of a southern brown howler monkey (bugio-ruivo), Alouatta guariba clamitans. The animal was found dead by the owner of a 60 ha. farm (Fazenda São Maximiano), located along the interstate road BR-116, km 308, Guaíba, State of Rio Grande do Sul, southern Brazil, 30º10'46,74"S, 51º23'30,78"W, in August 2000. The paper also describes the specimens of Trypanoxyuris (Trypanoxyuris) minutus found in the cecum. All organs were examined for helminths but were negative, except the cecum, which was full of macerated leaf litter and nematodes. The cecum wall was hyperemic, very thin, and distended, possibly by the large volume of material present. All the cecum contents were suspended in 5 liters of 0.85% saline physiological solution, from which a sample of 10% was taken and thoroughly examined. Six thousand one hundred and eighty-seven nematodes were counted in the sample (males + females). A total of 61,870 helminths were estimated in the entire cecal infrapopulation.

KEY WORDS:
Trypanoxyuris (T.) minutus, Nematoda; Oxyuridae; Alouatta guariba clamitans; southern brown howler monkey; primates.

RESUMO

O presente trabalho relata o caso de morte de um espécime subadulto, macho, de bugio-ruivo, Alouatta guariba clamitans, encontrado morto pelo proprietário de uma fazenda (Fazenda São Maximiano), localizada no km 308 da BR-116, em Guaíba, RS, Brasil, (30º10'46,74"S, 51º23'30,78"W), em agosto de 2000. Descreve-se os espécimes de Trypanoxyuris (Trypanoxyuris) minutus encontrados no ceco. Todos os órgãos foram examinados para detectar-se helmintos, sendo negativos, exceto o ceco que estava repleto de matéria vegetal macerada e de nematóides. A parede do ceco estava hiperêmica e muito fina por estar distendida, possivelmente, pelo volume de material presente. Todo material do ceco foi suspenso em 5 litros de solução salina fisiológica 0,85%, de onde foi retirada uma amostra de 10% que foi completamente examinada. Foram contados 6.187 nematóides (machos + fêmeas) na alíquota e estimados 61.870 helmintos presentes no ceco.

PALAVRAS-CHAVE:
Trypanoxyuris (T.) minutus, Nematoda; Oxyuridae; Alouatta guariba clamitans; bugio-ruivo; primatas.

The parasitism of wild howler monkeys (Alouatta spp.) has been recently reviewed by STUART et al. (1998). These authors listed Trypanoxyuris (T.) minutus (Schneider, 1866) infecting various howler monkey species: A. caraya in Argentina (POPE, 1966; COPPO et al., 1979); A. fusca [probably misidentified, as A. fusca = A. guariba, does not occur in Venezuela (HILL, 1962; HIRSCH et al., 1991; ROWE, 1996) in Venezuela (INGLIS & DIAZ-UNGRIA, 1959; DIAZ-UNGRIA, 1965); A. palliata in Costa Rica (STUART et al., 1988) and Panama (THATCHER & PORTER, 1968); A. seniculus in Colombia (HUGGHINS, 1969), Brazil (STILES et al., 1929; INGLIS & DIAZ-UNGRIA, 1959), and in Surinam (VAN THIEL, 1925). KUNTZ & MYERS (1972) published a tabulation of all parasites of South American primates. The host-parasite list and prevalence values given by STUART et al. (1998) included species of protists and metazoans from A. belzebul, A. caraya, A. fusca, A. palliata (combined with reports on A. villosa from Panama), A. pigra, A. seniculus and Alouatta sp. STUART et al. (1998) called attention to the fact that "parasites should not be surveyed simply as discrete passengers or invaders within an innocent primate, but as members of a functional ecosystem in which the monkey and the parasite are interrelated elements".

It is true that parasites can provide clues about host feeding patterns, frequency of contact with intermediate hosts, host distribution patterns and competitive interactions (STUART & STRIER, 1995). STUART et al. (1998) have also mentioned that the taxonomic confusion over host and parasite nomenclature, as well as the references in many obscure journals of South and Central America can add to the problem of understanding primate parasitology. Authors, in some cases, reported prevalence data for some parasite species listed, but did not present any information on the intensity of infection of these species. STUART et al. (1990) have conducted a coprological survey of monkey parasites belonging to the genus Alouatta, in Central America. In 1993, STUART et al. conducted the most comprehensive coprological survey of parasites of these monkeys, in the states of the southeastern region of Brazil. Although finding T. minutus, these authors only reported qualitative data, never mentioning intensity of infection values for any of the helminth species recorded nor any cases of death, which could have been attributed to any particular species of helminth. This report registers the death of a wild southern brown howler monkey possibly associated with the T. minutus infection.

The subadult male specimen of a southern brown howler monkey (bugio-ruivo), Alouatta guariba clamitans (Cabrera, 1940), was found dead by the owner of a 60 ha. farm (Fazenda São Maximiano), located along the interstate road BR116, km 308, Guaíba, State of Rio Grande do Sul, southern Brazil, 30º10'46,74"S., 51º23'30,78"W., on August 20, 2000. The contents of the viscera were examined for helminths using sieves (154 µm). Helminths were collected, fixed and processed according to AMATO et al. (1991). The size of the infrapopulation was determined through an aliquot of 10% of the total volume of cecal contents to estimate the total number of worms present (UENO & GONÇALVES, 1970). Measurements obtained from specimens mounted in Amann´s lacto phenol (Humason, 1972) (made with a Leitz Dialux 20 EB microscope) are in micrometers unless otherwise indicated. The range is followed by the number (n) of specimens measured for a particular character when the number is different than 10 (males) and 11 (females); and by the mean and SD values given within parentheses. Cross sections of males and females and en face mountings of the anterior extremity were hand-cut using a razor blade. Photomicrographs were made using a Zeiss Axiolab photomicroscope, with phase contrast. Some voucher specimens mounted in Canada balsam, and a large number preserved in ethanol 70 ºGL were both deposited in the Coleção Helmintológica do Instituto Oswaldo Cruz (CHIOC), Rio de Janeiro, RJ, Brazil.

Trypanoxyuris (Trypanoxyuris) minutus (Schneider, 1866)

Figs. 1 - 10

Figs. 1-4
Phase contrast photomicrographs of a male Trypanoxyuris (T.) minutus. Fig. 1. Anterior region (Bar = 100 µm). Fig. 2. Ventricular region: e - end of esophagus; b - bulb; i - intestine (Bar = 100 µm); Fig. 3. Posterior region, lateral view: s - spicule (Bar = 100 µm). Fig. 4. Copulatory bursa, ventral view: curved arrow - proximal end of spicule; straight arrow - tail spike (Bar = 50 µm).

Figs. 5-10
Photomicrographs of a female Trypanoxyuris (T.) minutus. Fig. 5. Anterior region: curved arrow - anterior extremity of lateral alae. Fig. 6. Posterior region: straight arrow - anus; curved arrow - posterior extremity of lateral alae (Bar for figures 5 and 6 = 500 µm). Fig. 7. "En face" view of the anterior extremity: arrows - apertures of amphidial pores (Bar = 25 µm). Fig. 8. Terminal portion of ovijectors: v - vagina; curved arrow - vulva) (Bar = 200 µm). Fig. 9. Anterior region (Bar = 100 µm). Fig. 10. Posterior region, with eggs (Bar = 100 µm).

General: small nematodes. Females straight, much larger than males. Males with curved posterior third of body. Both sexes, with cephalic plate square; amphidial openings (arrows in Fig. 7) between dorsal and sub-ventral cephalic papillae. Dorsal lip, bi-lobed. Lateral alae double-crested in females and singlecrested in males.

Males (n = 10) (Figs. 1-4): body length 2.40-3.02 mm (2.72 ± 1.8). Maximum width 129-153 (136 ± 12). Nerve ring 177-226 (200 ± 12), from anterior apex. Esophagus length, including bulb, 677-838 (761 ± 59). Bulb length 80-89 (87 ± 3); bulb width 81-88 (81 ± 4). Excretory pore 266 (n = 1), from anterior apex. Three pairs of sessile, post-cloacal papillae present. Pair of laterally placed, massive, post-cloacal papillae at base of tail spike, supporting caudal alae. Spicule length 40-44 (45 ± 2). Tail spike 8-10 long (9.5; 1.3). Ratios: body length/ esophagus length 3.15-3.81 (3.58 ± 0.2); body length/ spicule length 55.4-66.5 (60.2 ± 3.5); esophagus length/ nerve ring, from anterior apex, 3.36-4.00 (3.81 ± 0.2); esophagus length/bulb length 7.64-9.60 (8.75 ± 0.6); bulb length/bulb width 0.91-1.10 (1.1 ± 0.1).

Females (n=11) (Figs. 5-10): body length 7.10-8.50 mm (7.70 mm ± 463). Maximum width at vulva, 380540 (460 ± 45). Nerve ring 2.82 mm (n = 1), from the anterior apex. Excretory pore 1.51 (n=1), from anterior apex. Lateral alae begin at 398-531 (n=5) (460 ± 53) from anterior apex and end at 194-238 (n=6) (211 ± 18) from the tip of tail. Vulva 4.46-4.86 mm (n=2) (4.76 mm; 20), from anterior apex. Esophagus length, including bulb, 1.62-1.80 mm (1.72 mm ± 56) from anterior apex. Bulb length 97-153 (141 ± 20); bulb width 129-161 (151 ± 20). Tail length, from posterior apex, 1.26-1.62 mm (n=8) (1.41 mm ± 115). Eggs spindle shaped, flattened on one side, 44-46 (n=9) (45 ±1) long; 22-26 (n=9) (24 ± 2) wide. Ratios: body length/esophagus length 4.18-4.82 (n=10) (4.52 ± 0.2); body length/tail length 0.27-0.37 (n=8) (0.33); body length/egg length 171184 (n=9) (176 ± 6.7); body length/egg width 299-385 (n=10) (329 ± 28); esophagus length/bulb length 9.418.1 (n=10) (9.38 ± 2.3); bulb length/bulb width 234338 (n=10) (234 ± 30).

Taxonomic Summary

Host: Alouatta guariba clamitans (Cabrera, 1940).

Other hosts: to be found in all species of Alouatta.

Locality: Fazenda São Maximiano, interstate road BR116, km 308, Guaíba, RS, southern Brazil, 30º10'46,74"S., 51º23'30,78"W.

Intensity of infection: 6,187 nematodes counted in the sample of 500mL; 61,870 nematodes estimated in the cecum.

Specimens deposited: CHIOC - 34,957a-f mounted slides; CHIOC - 34,811 - wet material (ethanol 70 ºGL).

Remarks

Trypanoxyuris (T.) minutus is a parasite constantly reported from several species of monkeys in the genus Alouatta, either determined through coprological examinations (not counting the number of worms present) (STUART et al., 1990; STUART et al., 1993), or in papers of taxonomic nature (INGLIS & DIAZ-UNGRIA, 1959; HUGOT, 1985a and b; HUGOT, 1998; HUGOT, 1999; HUGOT et al., 1994; HUGOT et al., 1996).

The hyperinfection reported is intriguing because howlers are arboreal and rarely descend to the ground, although they sometimes do that to cross canopy gaps, reaching water reservoirs, or migrating between forest fragments (see BICCA-MARQUES & CALEGAROMARQUES, 1995). The behavior of living up in trees does not explain such a level of re-infection to and production of an infrapopulation of the observed magnitude.

There are no reports of deaths of wild howlers that could be attributed to this species of nematode. Thus, we are presenting the first possible record of a wild howler death for which a hyperinfection by T. (T.) minutus was responsible, even considering that the animal was found dead by the farm owner.

Acknowledgements

To Dr Nelson Matzembacher, the farm owner who collected the dead howler and brought it to our attention; Dr Jaqueline B. de Oliveira, Universidade Federal Rural de Pernambuco, Recife, PE; Dr Dely Noronha, curator of the Coleção Helmintológica do Instituto Oswaldo Cruz, Rio de Janeiro, for accepting the voucher specimens for deposition in the helminth collection of her institution; and to Prof. Ronald D. Rocco, M.A., Battle Creek, MI, USA, for revising the English version of the manuscript.

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Publication Dates

• Publication in this collection
  20 Sept 2024
• Date of issue
  Oct-Dec 2002

History

• Received
  30 Apr 2002
• Accepted
  09 Dec 2002