573 The parasitism of Schistosoma mansoni (Digenea–Trematoda) in a naturally infected population of water rats, Nectomys squamipes (Rodentia–Sigmodontinae) in Brazil
P.S.D’ANDREA"*, L.S.MAROJA",#, R.GENTILE$, R.CERQUEIRA$, " " A.MALDONADO J and L.REY " Departamento de Medicina Tropical, Instituto Oswaldo Cruz, Av. Brasil, 4365, 21045-900, Rio de Janeiro, RJ, Brazil # Seçag o de GeneT tica, Instituto Nacional de CaV ncer, Praça da Cruz Vermelha, 23, 20230-130 Rio de Janeiro, RJ, Brazil $ Departamento de Ecologia, Universidade Federal do Rio de Janeiro, Caixa Postal 68020, 21941-590, Rio de Janeiro, RJ, Brazil
(Received 1 September 1999; revised 12 November 1999; accepted 11 December 1999)
Schistosomiasis is a health problem in Brazil and the role of rodents in maintaining the schistosome life-cycle requires further clarification. The influence of Schistosoma mansoni on a population of Nectomys squamipes was studied by capture- recapture (1st phase, from June 1991 to November 1995) and removal (2nd phase, from April 1997 to March 1999) studies at Sumidouro, Rio de Janeiro, Brazil. During both phases coproscopic examinations were performed. At the 2nd phase the rodents were perfused and worms were counted. The population dynamics of parasites was studied. During the 1st phase, female reproductive parameters, longevity, recruitment and survivorship rates and migration patterns were studied in relation to schistosome prevalence. Water contamination (source of miracidia), abundance intermediate host and rodent migration were related to prevalence. The N. squamipes population was not obviously influenced by the infection, as shown by the high number of reproductive infected females, high longevity of infected individuals and the absence of a relationship between recruitment or survivorship rates and the intensity of schistosome infection. The data indicate that N. squamipes can increase transmission of S. mansoni in endemic areas and carry it to non-infected areas. Furthermore, this rodent can be used as an indicator of a transmission focus.
Key words: Schistosoma mansoni, Nectomys squamipes, Brazil, schistosomiasis, population dynamics.
body–tail length of 250 mm. They feed on aquatic insects, snails (that may be infected with S. mansoni), Schistosoma mansoni was introduced in Brazil during tadpoles and fruit (Ernest & Mares, 1986). Their the colonization in the XVI and XVII centuries reproduction occurs throughout the year but mostly (Despre! s et al. 1992; Tchuem Tchuente! et al. 1995). during rainy periods (Gentile et al. 1999). The The snail intermediate host (Biomphalaria) was mean permanence time observed in the field is already available with a large geographical dis- 75n4p144n5 days (D’Andrea et al. 1999) but in tribution, which facilitated the establishment and captivity N. squamipes can live up to 3 years (personal spread of this helminth. During the 1950’s it was observation). Under semi-natural conditions N. discovered that S. mansoni infected both human and squamipes can support the full development and wild mammals (Rey, 1993). Several species of the transmission of S. mansoni (Antunes et al. 1973; Sigmodontinae rodent, genus Nectomys, are the Kawazoe & Pinto, 1983). Other experimental studies primary candidates to become natural reservoirs of have also documented their high susceptibility to S. S. mansoni because of their semi-aquatic habits mansoni infection (Souza et al. 1992; Maldonado et (Ernest & Mares, 1986) which expose them to al. 1994) and their ability to eliminate viable eggs infection. They are distributed throughout a large (Rodrigues et al. 1992). High infection rates with S. area along watercourses including most endemic mansoni have also been reported in many natural areas of schistosomiasis (Ribeiro et al. 1998). When Nectomys populations (Rey, 1993). mature these rodents weigh 140–400 g and have a Understanding the role of rodents in transmission of S. mansoni is important for at least 2 reasons. Schistosome-transmitting rodents may significantly * Corresponding author: Departamento de Medicina complicate efforts to control schistosomiasis, and the Tropical, Instituto Oswaldo Cruz, Av. Brasil, 4365, 21045–900, Rio de Janeiro, RJ, Brazil. Tel and fax: j 011 use of rodents as hosts may alter some of the basic 55 21 280 3740. E-mail: dandrea!gene.dbbm.fiocruz.br properties of the worms, such as shedding patterns,
Parasitology (2000), 120, 573–582. Printed in the United Kingdom " 2000 Cambridge University Press P. S. D’Andrea and others 574 length of pre-patent period, or virulence. Studies on proximity to the sewage source of a small village. a natural population of N. squamipes in the mu- They had an open vegetation consisting of razor nicipality of Sumidouro, Rio de Janeiro State, Brazil grass, sparse shrubs and trees, with a secondary are reported. These studies characterize the para- forest at one of the edges of sites 3a and 3b. Site 4 was sitism of S. mansoni on this species and its influence along the same irrigation channel in an open flooded on host population size, longevity and female area with one major stream that received water and reproductive capacity. all the sewage from sites 3a and 3b. Site 4a was adjacent to site 4 but the trap line was established inside a forest fragment with a dense midstory and a high closed canopy. Site 5 was characterized by a continuous dense vegetation of Hedychium choron- arium (Zingiberaceae) in a flooded area, and had no Study area human habitation. Site 6 had only razor grass and The study was conducted in the Pamparra4 o and was located very close to human habitations but Porteira Verde adjacent valleys in Sumidouro, State above their sewage discharge (Fig. 1). of Rio de Janeiro, Brazil (22m 02h 46d S; 42m 41h 21d W). These valleys are part of a common hydric Field study system with many small permanent streams, ir- rigation channels and some flooded areas (Fig. 1). The study was divided in 2 phases. In the first phase, The landscape is composed of small rural properties June 1991 to November 1995, a mark-recapture with vegetable plantations, pasture lands and a few program was conducted to study the population small Atlantic Forest fragments. dynamics (Gentile et al. 1999) and the infection rates The region has a humid-mesotermic climate of the N. squamipes population at Pamparra4 o valley. (Nimer, 1979). Rainfall is seasonal and heaviest The size of the population was estimated using the between November and March (normal tempera- Minimum Number Known Alive estimator, MNKA tures between 23n2 and 25n4 mC, normal rainfall (Krebs, 1966), which considers as the population between 269n4 mm and 153n5 mm). The driest size, the number of animals captured and released at months generally extend from May to August a given session, plus those not captured at this (normal temperatures between 18n3 and 20n3 mC, session but captured before and after that. The normal rainfall between 24n7 mm and 44n2 mm). The survivorship and recruitment rates (Fig. 3) were mean temperature during the study period was estimated using the Jolly–Seber estimator (Jolly, 24n3p2n4 mC and the mean rainfall was 121n7p126n1 1965; Seber, 1965). Survivorship is the rate of (data obtained from National Institute of Meteor- animals that survived from one capture session to the ology of Rio de Janeiro). subsequent one, and recruitment is the rate of The study design was dictated by the semi-aquatic animals that were added to the population from one habits of the water rat, N. squamipes. All the capture capture session to the following one (in our case by lines were established along watercourses and birth or immigration). All captured rodents were flooded areas with 1 wire live trap set at intervals of weighed, sexed and individually marked by toe 13 metres. The capture sessions were carried out clipping. The reproductive condition of the females every other month for 5 nights. The capture sites was assessed by groping and visual observation of varied in their proximity to human habitations and, the dilatation of abdomen, and sexual maturity was therefore, in the level of water pollution from assumed as the minimum age and weight of males domestic sewage (a source of S. mansoni miracidia to with scrotal testes and females with open vagina the snail population). (D’Andrea et al. 1996). Water contamination of each capture site was Diagnosis of schistosome infection was based on evaluated considering data on the prevalence of coproscopic examinations (Katz, Chavez & Pelle- human population living nearby and the kind of grino, 1972). Surgical dischargeable hoods were domestic sewage (such as cesspool or direct discharge placed at the bottom of each trap acting as a faeces- into the watercourses). The abundance of N. collecting bag. Faecal samples were collected from squamipes, snails (Biomphalaria glabrata) and veg- every individual at each capture or recapture. The etable types were distinct among sites (Table 1). Site faecal samples from each individual were mixed 1 and its extension, 1a, were characterized by open (during the capture session) and later analysed using vegetation composed of sparse thickets, and by the 2 slides. The mean number of eggs per gram of absence of human habitations. Site 2 had an faeces was calculated following the modified Kato irrigation channel receiving water from the main method (Katz et al. 1972). stream of Pamparra4 o valley and from a non-polluted Schistosome prevalence in the N. squamipes popu- small effluent stream; it had sparse high trees, shrubs lation was calculated for each capture session except and razor grass. Sites 3, 3a and 3b were located along those where less than 5 animals were examined. the same irrigation channel but differed in their The numbers of infected and non-infected animals Schistosoma mansoni in Nectomys squamipes 575
Fig. 1. Map of the study area, Sumidouro city, Rio de Janeiro State, Brazil, showing adjacent valleys (Pamparra4 o and Porteira Verde) and capture sites (1–6).
Table 1. Brief description of each studied site considering trapping effort (number of trap nights), water contamination, snail and rodent abundance (Mean values and standard deviation for Nectomys squamipes abundance.)
Nectomys Water Biomphalaria squamipes N. squamipes Trapping effort Trapping effort contamination by glabrata abundance abundance Site 1st phase 2nd phase human sewage abundance 1st phase 2nd phase
1 2325 900 Absent Absent 1n3p1n80n8p1n3 1a 775 — Absent Absent 0n5p0n9— 2 2325 900 Medium Rare 3n5p2n12n5p1n7 3 2325 — High High 1n6p2n1— 3a — 900 Very high High — 1n7p1n3 3b — 300 High High — 0n1p0n3 4 — 1200 High Medium — 0n6p1n2 4a 1550 — High Absent 1n4p1n5— 5 1550 600 Absent Absent 1n9p1n81n7p1n0 6 — 300 Absent Absent — 0n5p1n0 were estimated using the MNKA estimator. The of non-infected animals in the population. Since prevalence rate was based on the estimated number there is no known self-cure of schistosome infection, of infected animals divided by the estimated number all animals were considered infected at subsequent P. S. D’Andrea and others 576
0.6 25
0.5 20
0.4
15
0.3 Prevalence 10 0.2 Population size (MNA) and incidence 5 0.1
0.0 0
Jul 92 Jul 93 Jul 94 Jul 95 Jun 91Aug 91Oct 91Jan 92Mar 92May 92 Oct 92Dec 92Jan 93Mar 93May 93 Sep 93Nov 93Jan 94Mar 94May 94 Sep 94Nov 94Jan 95Mar 95May 95 Sep 95Nov 95 Population size Prevalence Incidence (MNA) Fig. 2. Population size, schistosome incidence and prevalence rate of the Nectomys squamipes population in the Pamparra4 o Valley, Sumidouro, Rio de Janeiro State, Brazil (1st phase of the study). Empty data when less than 5 individuals were captured. captures after their first positive examination. Then, for females). Adults are fully mature individuals, incidence was the number of individuals diagnosed weighing more than 190 g for males and more than as positive for the first time in a given capture session 215 g for females. (number of infected animals never captured before The relationship between the infection rates of plus the number of infected individuals found to be rodents and their population parameters was tested uninfected on previous capture sessions). using Spearman correlation. Time lags from 2 to 6 The second phase, from April 1997 to March 1999 months (1–3 capture sessions) were used in cor- was conducted at Pamparra4 o and Porteira Verde relation tests. These time lag periods were chosen valleys. The captured animals were removed and considering the biological cycles of S. mansoni and sacrificed in the laboratory. Schistosome prevalence its hosts, since the lower limit corresponds to the was based on both the coproscopic (Katz et al. 1972) time it takes for the infection detection and the upper and perfusion techniques (Smithers & Terry, 1965), limit corresponds to the maximum time to rodent the latter allowed determination of worm burden. population turn-over. The Mann–Whitney test was The presence of host embryos was also recorded and used to seek for differences between variables (Zar, the number of captured animals was used to calculate 1996). rodent abundance. The influence of S. mansoni parasitism on the Both phases (the mark-recapture and the removal water rat was considered only for the patent phase. phases) had the same capture effort per capture Thus, when comparing infected and non-infected session (400 trap nights), totalling 10800 trap nights individuals, the infected group included only rodents in the first phase (27 capture sessions) and 4800 trap eliminating eggs in their faeces. nights in the second phase (12 capture sessions). Classification of N. squamipes age was evaluated by weight (Gentile et al. 1999). Juveniles are non- reproductive individuals weighing less than 110 g for Characterization of S. mansoni infection in N. both sexes. Subadults are individuals in full re- squamipes productive condition with the lowest recorded weights or the heaviest individuals not yet mature In the first phase, the mean prevalence rate of S. (between 110 and 190 g for males and 110 and 215 g mansoni in N. squamipes was 26p14n2%, varying Schistosoma mansoni in Nectomys squamipes 577
1.2 25
1.0 20
0.8
15
0.6
10
0.4 Population size (MNA) Survivorship and recruitment rates 5 0.2
0.0 0
Jul 92 Jul 93 Jul 94 Jul 95 Jun 91Aug 91Oct 91Jan 92Mar 92May 92 Oct 92Dec 92Jan 93Mar 93May 93 Sep 93Nov 93Jan 94Mar 94May 94 Sep 94Nov 94Jan 95Mar 95May 95 Sep 95Nov 95
Population size Survivorship Recruitment (MNA) Fig. 3. Population parameters of the Nectomys squamipes in the Pamparra4 o Valley, Sumidouro, Rio de Janeiro State, Brazil (1st phase of the study). Empty data when less than 5 individuals were captured. from zero to 57% among capture sessions. Preva- in 35 perfused N. squamipes. The sex ratio of worms lence rates higher than 20% were observed in 63% was 1n89 biased towards males (880 males, 464 of the cases. Incidence varied from zero to 30% (Fig. females – the parasites of 1 host were not sexed). 2). The number of eggs per gram of faeces ranged Fifty percent of the worm population was concen- from 12 to 300 eggs for infected individuals. In this trated in only 4n2% of the entire host population and study, 145 N. squamipes individuals were captured 90n0% was in 14n6% of the hosts. Considering only (87 males, 58 females), 119 of which were examined the infected individuals, 11n4% of the hosts harbour (72 males, 47 females), 29 of which were infected (16 half of the parasite population. The mean worm load males, 13 females). There were no differences in was 37n4p59n6 worms\infected host (1–309 worms) # prevalence between males and females (χ l 0n817, and the mean abundance was 17n61p41n6 worms\ ..1,..). captured host. The distribution of the Schistosoma In the second phase the mean prevalence rate was population, across the entire host population, had a 21n0p14n5, varying from zero to 42n9% among high coefficient of variation, 281n4% (mean l 14n7 capture sessions in which 5 or more individuals were and .. l 41n4) indicating a clumped worm dis- captured (Fig. 4). In this phase, 96 N. squamipes tribution which could be described by a negative were captured (66 males, 30 females), 38 of them binomial distribution (k l 0n315). Due to the dis- were infected (30 males, 8 females). The mean persed nature of the data, no statistical test to detect number of eggs per gram of faeces in infected significance could be performed. individuals was 132n2p119n5 (ranging from 12 to The total prevalence rates including all the 480). Despite the larger number of infected males individuals captured at any particular site, varied there was no significant difference in the prevalence among study sites (Table 2). Some sites could be # rate between sexes (χ l 2n18 ..) nor in the worm compared between phases due to the continuity of burden (z l 0n7 ..). The worm burden increased the study at the same place (site 1, 2, 3 and 3a and 5). with the weight of the animals, although the Although the prevalence rates varied among phases correlation was significant only for the most con- at the same study site, no statistically significant taminated area, site 3b (rs l 0n559, P l 0n05, α l 1). difference was detected. Prevalence rates at site 3 and Only 1 of 8 recently weaned animals from the 3a were very different between study phases (25% juvenile age class was already infected, and all worms and 61n9%) but, again, this was not statistically # were immature. A total of 1309 worms were collected significant (χ l 3n13; P ! 0n1). Only 1 infected P. S. D’Andrea and others 578
18 70
16 60
14
50 12
10 40
8 30 Prevalences (%)
Number of individuals 6 20
4
10 2
0 0 Apr 97 Jul 97 Sep 97 Nov 97 Jan 98 Mar 98 May 98 Jul 98 Sep 98 Nov 98 Jan 99 Mar 99 Number of Prevalence by Prevalence by captures Kato-Katz perfusion Fig. 4. Population size and prevalence rates of the Nectomys squamipes in the Pamparra4 o and Porteira Verde Valley, Sumidouro, Rio de Janeiro State, Brazil (2nd phase of the study). Empty data when less than 5 individuals were captured.
Table 2. Prevalence, eggs per gram of faeces and infection rates (abundance and intensity) of Schistosoma mansoni in Nectomys squamipes in each capture site, for both phases of the study (Mean values and standard deviation for eggs per gram of faeces considering the infected individuals, in parenthesis number of examined individuals.)
Eggs per gram Prevalence Prevalence Eggs per gram of faeces 1st phase* 2nd phase* Prevalence Abundance Intensity Site of faeces 1st phase 2nd phase (%) (%) 2nd phase† 2nd phase 2nd phase
1 Zero Zero Zero Zero 10n00n22n0 1a Zero — Zero — — — — 291n5p116n6(13) 108p152n1(4) 26n014n335n73n18n9 337n2p13n7(5) — 25n0— — — — 3a — 143n4p122n5(13) — 61n985n750n759n6 3b — — ‡‡140 140 4— — — 0%60n01n94n3 4a 108n6p116n6(5) 27n5— — — — 5 114p79n3(4) 168p33n9(2) 6n910n021n12n817n3 6 — — — Zero Zero — —
* By Kato-Katz method. † By perfusion methodology. ‡ Only 1 (positive) individual captured. individual was captured at site 1, in the last capture observed that the coproscopic method gave 17 false session. This animal was an adult and probably came negatives when worm burdens of less than 6 couples from another area since there is low or no possibility were present, excluding 2 cases in which a single of local transmission due to the apparent absence of couple was detected. In general though there was snails and a human infection source. strong correlation between number of eggs per gram In comparison to the perfusion technique, we of faeces and worm load (rs l 0n636; P ! 0n001; .. Schistosoma mansoni in Nectomys squamipes 579
33) and also between S. mansoni females and eggs per lower, generally less than 10% (Duplantier, 1991) gram of faeces (rs l 0n659; P " 0n001; .. 31). except in 1 study where the rodent Pelomys sp. population had 46% of the individuals infected (Kawashima, 1978). The influence of parasitism over the rodent Novel host–parasite associations were often con- population sidered more harmful to the host but some ex- perimental evidence suggests the contrary (Ebert & There was no correlation between host population Herre, 1996). Considering that S. mansoni was size and its infection rate, nor between infection rate introduced in South America about 400 years ago and survivorship or recruitment rates. This was true (and much later in Sumidouro) the former hy- without time lags or with time lags of 2, 4 or 6 pothesis should be investigated since the high months. Infected rodents weighed more than non- infection rates found in Brazil could reflect the infected ones (mean 209n4p57n0g,n l 34 and mean recent host–parasite association between South 175n8p68n3g, n l 36 respectively; z l 2n03; P ! American rodents and S. mansoni. In both South 0n05). The permanence time of infected individuals America and Africa, the animal species with greatest (estimated longevity) was 125n6p136n6 days (ranging transmission potential are semi-aquatic as would be from 1 to 490, n l 64) and for non-infected was expected. It is believed that schistosomiasis infection 40n4p74n2 days (ranging from 1 to 355, n l 109), started in African rodents and that humans acquired presenting a statistically significant difference (z l it latter, as a lateral transference (Combes, 1990). 4n9; P ! 0n001). There was no significant difference The! ron & Pointier (1995) discussed the differences in infection rates between sexes. found between human and rodent strains of S. Nectomys squamipes females can maintain preg- mansoni in egg morphology, allozymes and behaviour nancy even though infected. In the first phase of the of cercariae, showing a new lateral transference that study all the infected females were pregnant (14 took place from humans to Caribbean rodents. individuals) as were half of the non-infected (21 In this study, 3 factors were related to the infection pregnant in 40 captured) females. This difference is level of N. squamipes: (1) contamination from human probably due to the higher permanence time of sewage in the rodent home ranges; (2) abundance of infected females. In the second phase, excluding site the snail vector populations in the site, and (3) 1 that had no infections, 24 females were at adult or migration of the rodents across capture sites. The subadult reproductive age and 7 were actually infection level of the rodents increased with the reproducing, 3 of which were infected with a low proximity of human residences, particularly in worm burden (3 and 8 worms). Across both phases site 3a that had the highest human prevalence the percentage of reproducing individuals was 37n5 rates (M. S. Soares, personal communication), the for the infected group and 25% for the non-infected strongest human influence with large sewage dis- group and the mean number of foetuses was charge, and the most abundant and stable snail 3n67p0n57 and 3n25p0n5, respectively. population. Intermediate levels of infection were The immigration patterns were ubiquitous as observed in sites, such as 5 and 2, that had no measured in the first phase excluding only the site 1 snails and that received intense immigration of where movements were restricted to a local scale N. squamipes from transmission areas. Little or no among sites 1 and 1a. There were no significant infection was found in the most isolated site, site 1, differences in mobility between infected and non- # where there was no observed immigration of rodents infected individuals (χ l 0n582 ..1,..). from other sites and which had no snail population or input of human sewage. The data corroborate the expected clumped dis- tribution for host–parasite association in helminths (Mitchell et al. 1990; The! ron et al. 1992). The In this study it was observed that the water rat N. spatial heterogeneity and low infection rate of the squamipes has very high susceptibility to infection snail population, B. glabrata (A. Giovanelli, personal with S. mansoni as shown by the high prevalence communication) can explain this clumped distri- rates, high number of Schistosoma eggs per gram of bution. These factors restrict the transmission foci to faeces and the high worm burdens observed in this a few very small areas. Rodents living at highly population. In other endemic areas of Brazil, water contaminated sites (like site 3), probably have several rat infection rates varied but were often over 30% contacts with infected snails during their life-time. and sometimes more than 90% (Veiga-Borgeaud et Another factor that can contribute to this aggregated al. 1986, 1987; Picot, 1992; Rey, 1993). In the distribution may be heterogeneity in host resistance Caribbean islands, overall prevalence of 40% was to the infection acquisition. observed in Rattus rattus, with annual variations The positive correlation between rodent weight ranging from 28 to 61% (The! ron et al. 1992). In and worm burden in the most infected area, together African wild rodents, infection rates were much with the rarity and low worm burden of unisexual in- P. S. D’Andrea and others 580 fections, shows that multiple infections are probably infected N. squamipes. Furthermore, their life-span common at least in the very contaminated areas. was not affected since we observed that infected In areas with little or no contamination, the animals individuals were older, considering body weights, may get infected only occasionally, perhaps once and had longer permanence time in the study area (at in a life-time. If an infected animal is in a non- the mark-recapture period of study). Despite the fact transmission area, it is probably an immigrant that that older animals are more likely to be correctly carried the worms from another site and may not diagnosed as positive, because as the coproscopic acquire more worms during its life-time, unless the method is less sensitive to recent and low burden infection establishes itself in this area. infections the observed pattern still showed no It was found that 50% of the parasite population decreased fitness of infected individuals. Laboratory was concentrated in only 4n1% of the host population data on experimental infection and pathological (very similar to the 4% of The! ron et al. 1992) and studies corroborated this mild host–parasite inter- 11n4% of the infected rodents harbour half of the action, since S. mansoni infection in N. squamipes parasite population (9% of The! ron et al. 1992). This caused low pathogenicity in spite of the long highly infected host group possibly plays an im- persistence of the infection (Silva et al. 1992). portant role in increasing the transmission rates at a Understanding the infection dynamics of S. local area, because their life-span does not seem to be mansoni in N. squamipes hosts can help clarify the reduced and, furthermore, we observed that worm role of N. squamipes in schistosomiasis transmission. burden was correlated with egg production. But, the The presence of infected individuals in places far importance of the less infected group, which from areas contaminated with human faeces shows accounts for 88n6% of the infected hosts, cannot be that these rodents can carry S. mansoni to places disregarded since they are numerous and can have a previously lacking transmission, complicating the crucial role in occasionally carrying the infection to control of this disease. Our data on epidemiology of new areas. N. squamipes indicate that this rodent can increase The population parameters (size, recruitment and transmission in endemic areas. Furthermore, it can survivorship) in the N. squamipes population did not be used as a natural indicator of a transmission focus, seem to be affected by schistosome infection. The because, when the possibility of acquiring parasites population dynamics of this rodent was not in- exists, the rodent population will test positive to the fluenced by the infection during the entire study infection. N. squamipes can also be used to access despite the steadfastness of high prevalence rates. In parasitological parameters not available for the theory, the parasites might regulate their host human population (The! ron et al. 1992). abundance (Anderson & May, 1979), but this has been proved to occur only in captive Mus musculus The authors are most grateful to the PAPES-FIOCRUZ, populations (Barker, Singleton & Spratt, 1991). It is Conselho Nacional de Desenvolvimento Cientı!fico e difficult to state a final conclusion in the absence of Tecnolo! gico (CNPq), Fundaça# o de Amparo a Pesquisa do controlled experiments to detect the effects of the Rio de Janeiro (FAPERJ), Fundaça# o Universita! ria Jose! parasite over wild host populations. The use of Bonifa! cio (FUJB), Ministe! rio do Meio Ambiente\ PROBIO, Fundaça# o de Amparo a Pesquisa de Sa4 o Paulo intervention experiments would be useful in de- (FAPESP) for their financial support; to J. W. F. Costa for tecting population regulation by macroparasites. his help in the field; to J. S. Garcia and G. O. Vieira for Amano et al. (1990) demonstrated a decreased their technical assistance and to Dr E. S. Loker and ability of infected mice (CBA-J strain) to produce Dr J. R. Machado-Silva for their comments on the viable offspring due to death of the mother, abortions manuscript. We are also grateful to C. E. Grelle and to D. A. Moraes for the improvement to Fig. 1. and to a large extent, infanticide with less than 35% success for infected females versus 70% for the non- infected one. 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