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Memórias do Instituto Oswaldo Cruz
Fundação Oswaldo Cruz, Fiocruz
ISSN: 1678-8060 EISSN: 1678-8060
Vol. 97, Num. 7, 2002, pp. 959-963
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Mem Inst Oswaldo Cruz, Rio de
Janeiro, Vol. 97(7), October
2002, pp. 959-963
Parasitic Arthropods
of Some Wild Rodents from Juréia-Itatins Ecological Station, State of
São Paulo, Brazil
David Eduardo Paolinetti Bossi, Arício
Xavier Linhares/+, Helena de Godoy Bergallo*
Departamento de Parasitologia, Instituto
de Biologia, Universidade Estadual de Campinas, Caixa Postal 6109, 13083-970
Campinas, SP, Brasil *Departamento de Ecologia, Universidade Estadual do Rio
de Janeiro, Rio de Janeiro, RJ, Brasil
+Corresponding author. Fax: +55-19-3788.6282.
E-mail: aricio@unicamp.br
Received 20 March 2002
Accepted 9 July 2002
Work
supported by Fapesp, grant # 88/3649-4, Faep, grant # 519/88 and CNPq grant
# 301372/95-0.
Code Number: oc02218
A study of the associations between
three species of rodents in the Atlantic forest and their parasitic arthropods
was undertaken at the Juréia-Itatins Ecological Station, located in the
State of São Paulo, Southeastern Brazil, from March 1989 to February
1990. Individuals of three species, Oryzomys russatus, Proechimys iheringi
and Nectomys squamipes were captured and examined for ectoparasites.
Eleven species of parasitic arthropods were found, including four species of
insects and seven of Acari. Parasitism intensity, phenology, and rainfall were
positively correlated with the abundance of the ectoparasites and their hosts.
The most abundant host was O. russatus (Muridae: Sigmodontinae), and
the most common parasite on it was the laelapid mite Gigantolaelaps oudemansi.
The cuterebrid Metacuterebra apicalis caused myiasis in O. russatus.
A mutualistic association between the staphylinid beetle Amblyopinus sp.
and its host P. iheringi (Echimyidae) was observed. The few N. squamipes
captured had small numbers of ectoparasites.
Key words: rodent ectoparasites -
Acari - Diptera - Siphonaptera - Coleoptera - Atlantic rain forest - Brazil
Ectoparasitic arthropods that infest
mammals are either insects or acarines (Kettle 1985). Some ectoparasites such
as chewing and sucking lice are permanent, whereas most adult fleas and ticks
are temporary (Kim 1985). Some ectoparasites are biological vectors of pathogenic
organisms (viruses, bacteria, protozoans, and helminths) among their hosts (Kettle
1985).
Some studies that have examined ectoparasites
of small mammals in the Brazilian Atlantic forest (Fonseca 1939a, Guimarães
1945, Linardi 1977, Linardi et. al 1984, 1987, 1991, Guitton et al. 1986, Barros
& Baggio 1992, Bossi & Bergallo 1992, Barros et al. 1993, Carvalho et
al. 2001) have included species inventories, taxonomic descriptions, and records
of host-parasite associations. Others (Botelho et al. 1981, Barros-Battesti
et al. 1998) have evaluated the ectoparasites-host associations. The objectives
of the present study were to (1) describe the relationship between three Atlantic
forest rodent species and their ectoparasites; (2) assess the degree of host
ectoparasite specificity; and (3) examine the influence of rainfall on ectoparasite
abundance.
MATERIALS AND METHODS
The present study was undertaken
at the Juréia-Itatins Ecological Station (24o32'S; 47o15'W),
located in the municipalities of Peruíbe, Iguape, Miracatu and Itariri,
State of São Paulo, Southeastern Brazil. The climate is tropical humid,
with a mild, dry season from May to September. Annual rainfall is high (3,000
to 4,000 mm/yr) (Paixão 1984). During the present study, the wettest
month was January 1990 (546.3 mm), and the driest was August 1989 (49 mm). For
data analysis, the dry and cool period was considered to range from April to
September and the wet and warm period from October to March. The mean temperature
varies from 18.3°C to 25.6°C, with July being the coolest month and
February the warmest (Nascimento & Pereira 1988).
Field samples were obtained monthly
from February 1989 to March 1990. Small mammal trapping was conducted in an
irregular grid covering 5 ha, with 14 transects varying from 200 to 240 m, spaced
20-m apart. Wire-cage traps (120) baited with banana or manioc with peanut butter
were set on the forest floor for three consecutive nights (Bergallo 1994). Each
trap site was recorded and trapped animals were taken to a nearby station laboratory.
Handling of small mammals was similar to the procedure used by Gettinger (1992).
The animals were placed in plastic bags with a cotton ball soaked with ethyl
ether until they became unconscious, after which they were marked using an ear-code
(Monteiro-Filho 1987), weighed, and sexed. Larger ectoparasites were removed
from the fur, ears and tail with fine combs, toothbrushes or tweezers and stored
in 70% alcohol. The hosts were subsequently released at the same trap site.
Ectoparasites that fell from the animals during anesthesia in the plastic bag
were also stored in 70% alcohol.
Analysis of variance was used to
test the effect of host species, parasite species and period of the year (dry
or wet) on parasite prevalence. Comparisons of parasite relative densities versus
host sex were done using Student's t-test. In addition to these analyses,
prevalence and mean intensity were determined for the most common species. Prevalence
is defined as the number of hosts infested with one or more individuals of a
particular parasite species or taxonomic group divided by the number of hosts
examined for that parasite. Mean intensity is the total number of parasites
of a particular species found in a sample divided by the number of hosts infested
with that parasite (Bush et al. 1997). Overall host and parasite abundances
by period of the year (dry or wet) were also analyzed using ANOVA. The analyses
were done using the SAS statistical program (SAS Institute 1987).
RESULTS
A total of 5,350 arthropods specimens
infesting 11 species was taken from 80 small rodents, 23 being the spiny rat
Proechimys iheringi Thomas, 51 the rice rat Oryzomys russatus
(Wagner) and 6 the water rat Nectomys squamipes (Brants). In addition
to the rodents, three species of marsupials: Didelphis aurita Wied-Neuwied,
Metachirus nudicaudatus (Desmarest), and Philander frenata (Linnaeus)
were captured, and the results will be presented elsewere.
Ectoparasites collected were Acari
Ixodidae: Ambly-omma cajennense (Fabricius), Haemaphysalis lepo-rispalustris
(Packard) and Ixodes sp.; Acari Lelapidae: Gigantolaelaps oudemansi
Fonseca, Androlaelaps (Haemolaelaps) sp., Gigantolaelaps
gilmorei Fonseca; Siphonaptera Rhopalopsyllidae: Polygenis (Polygenis)
roberti roberti (Rothschild);Siphonaptera Cteno-phthalmidae: Adoratopsylla
(Tritopsylla) intermedia intermedia (Wagner); Diptera Cuterebridae: Meta-cuterebra
apicalis (Guérin-Meneville); Coleoptera Staphylinidae: Amblyopinus
sp. Siphonaptera nomenclature is according to the one proposed by Linardi and
Guimarães (2000).
Seven arthropod species, totaling
5,148 individuals, were collected from 139 captures of O. russatus. This
represented 96.2% of the ectoparasites collected from all hosts. G. oudemansi
was the most frequent species (3,162 individuals), and was collected almost
exclusively on O. russatus. A.(Haemolaelaps) sp. (n = 550)
was collected exclusively on O. russatus. G. gilmorei (n = 717),
P. r. roberti (n = 155), M. apicalis, a subcutaneous parasite
(n = 25), and Ixodes sp. (n = 12), were also collected almost exclusively
on O. russatus, but with a frequency much lower than that recorded for
G. oudemansi (Table I). Other
ectoparasites collected on O. russatus included 12 nymphs and 505 larvae
of A. cajennense.
A total of 202 individuals, belonging
to 11 species of arthropods was captured from 75 captures of P. iheringi,
representing 3.8% of all arthropods collected on the hosts. The beetle Amblyopinus
sp. (n = 80), a mutualistic insect, was collected almost exclusively on this
rodent. Twelve Androlaelaps sp., and 3 H. leporispalustris were
collected exclusively on P. iheringi. Other ectoparasites collected on
this host included A. cajennense (larvae: n = 67);nymphs: ( n = 15),
G. oudemansi (n = 12), G. gilmorei (n = 4), Ixodes sp.
(n = 3), P. r. roberti (n = 5) and A. i. intermedia (n = 2) (Table
I).
Only 8 arthropods of 4 species (0.2%
of all specimens) were collected on N. squamipes, including G. oudemansi
(n = 4), A. cajennense larvae (n = 2), Amblyopinus sp. (n = 1)
and M. apicalis (n = 1).
There was no significant relationship
between parasite intensity and host sex for any host species. The mean parasite
intensities were, respectively, 1.90 and 1.77, on male and female O. russatus
(t498 = 1.27; P = 0.20), and 0.97 and 1.10 on male
and female P. iheringi (t572 = 1.17; P = 0.24).
The relationship between parasite
intensity and period of the year (dry or wet) was significant only for O.
russatus, with higher values in the wet (1.95) than in the dry (1.72) period
(t498 = 2.58; P < 0.01). Parasite intensity on P.
iheringi during the dry (1.11) and wet (0.96) months did not differ significantly
(t88 = 1.39; P = 0.16). N. squamipes was captured
with ectoparasites only during wet months.
The relationship between the mean
numbers of arthropods and the period of the year was significantly different
for M. apicalis found on O. russatus (Table
I).
The mean intensity of parasitic arthropods
during the wet and dry months was significantly different only for M. apicalis
(Table II). This parasite showed
a higher intensity of parasitism during the wet period.
Comparisons of the mean intensities
among arthropod species were significant for the hosts O. russatus (F
= 57.39; P = 0.0001) and P. iheringi (F = 2.28; P
= 0.0181) (Table III). N. squamipes
had too few parasites for meaningful statistical analysis. No lice were collected.
DISCUSSION
The type of traps used in this work
did not prevent the ectoparasites from abandoning their hosts. This could have
occurred with specimens of Amblyopinus sp., which some species normally
remain on the host only at night (Ashe & Timm 1987). Using combs, toothbrushes
or tweezers to sample the hosts could account for the absence of lice in samples,
since these ectoparasites usually remain firmly attached to the host. In addition,
it was not possible to determine the exact area of the host body where most
of the ectoparasites were collected. Bots of M. apicalis were located
on the lateral thoracic region and neck (Bossi & Bergallo 1992), and the
beetles Amblyopinus sp., were attached to the base of the tail.
O. russatus was the most abundant
host and also had the highest prevalence of ectoparasites. G. oudemansi,
the most commonly collected ectoparasite, was recovered almost exclusively from
O. russatus. According to Gettinger (1987), species of Gigantolelaps
are restricted to the genus Oryzomys. Only one species of flea, P.
r. roberti, parasitized this host, and showed a strong association
with O. russatus,since 98.1% of the fleas were found on this host. According
to Linardi (1984), Oryzomys is the main host genus for P. r.
roberti. Larvae of M. apicalis were found on O. russatus.
Although this parasite is large compared to the host, apparently it did not
affect the survival of the parasitized rodents since previously infested hosts
were recaptured with scars caused by the larvae leaving the host to pupate.
Linardi et al. (1991) found A.
i. intermedia on the marsupial Lutreolina crassicaudata (Desmarest),
and Guitton et al. (1986) found P. r. roberti on two species of Nectomys,
two species of Oryzomys, two species of Oxymycterus, and on Rattus
norvegicus (Berkenhout), Rhipidomys mastacalis (Lund) and Proechimys
dimidiatus (Günther). Two acarine species, G. oudemansi and
H. leporispalustris, were collected on P. iheringi, but they also
occur on the marsupial M. nudicaudatus (Bossi 1996), which probably preys
on P. iheringi.
The presence of only one Amblyopinus
sp. was not surprising. Fonseca (1939b) collected A. gahani Fauvel
on N. squamipes at Teresópolis and one of the authors (HGB) captured
N. squamipes with Amblyopinus sp. in a region close to the study
area. One unidentified species of Amblyopinus has been recovered from
the marsupial P. frenata (Bossi 1996). Ashe and Timm (1987) suggest
that the interaction between Amblyopinus and their hosts is probably
mutualistic.
Few individuals of N. squamipes,
a semi-aquatic rat, were captured, possibly because few traps were placed close
to water. Ectoparasites were scarce on this rodent, contrasting with the findings
of Linardi et al.(1987) who reported parasitism by other mites and fleas on
this rodent.
The variation in rainfall between
the driest and wettest months was high, but even in the dry months, the rainfall
averaged approximately 100 mm/mo. The relationship between parasite intensity
and period of the year was significant only for M. apicalis on the host
O. russatus. The cuterebrid M. apicalis showed a higher incidence
in the wet months as reported by Bossi and Bergallo (1992) and Vieira (1993).
According to JR Botelho (Universidade
Federal de Minas Gerais, pers. commun.), Ixodes sp. found on the rodents,
could be either I. amarili Fonseca or I. loricatus
Neumann. The marsupials D. aurita, M. nudicaudatus and P. frenata
were collected during this work and were parasitized by I. loricatus.
This could also be the same tick species parasitizing the rodents.
The ectoparasites found on O.
russatus showed differences in their intensities and can be separated into
three groups, one formed by the mite G. oudemansi, and the other two
by the remaining ectoparasites. G. oudemansi differed from the other
parasites due to its high rates of prevalence on O. russatus.
ACKNOWLEDGMENTS
To the late Lindolpho R Guimarães
for help with identification of the fleas, Ângelo P Prado for identification
of the flies, Donald D Gettinger for identification of the laelapid mites, José
Ramiro Botelho and Stephen Bennett for identification of the ticks and A Langguth,
for identification of the hosts.
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