Relationships of South American marsupials (Didelphimorphia, Microbiotheria and Paucituberculata) and hard ticks (Acari: Ixodidae) with distribution of four species of Ixodes
Author
Guglielmone, Alberto A.
Author
Nava, Santiago
Author
Díaz, Mónica
text
Zootaxa
2011
3086
1
30
journal article
46073
10.5281/zenodo.203193
22f6889c-9d62-47bf-af35-0efc62426aff
1175-5326
203193
Paucituberculata Ameghino
:
Caenolestidae Trouessar
(only family in the order)
1)
Ixodes jonesae
Kohls, Sonenshine and Clifford, 1969
is a South American species known from several specimens collected from
Sigmodontinae
and several larvae from Caenolastidae (Guglielmone
et al.
2003b).
Venezuela
, Táchira, South-West of
San Cristóbal
(
07º28´N
72º27´W
), L on
Caenolestes obscurus
(=
Caenolestes fuliginosus
(Tomes)) (Jones
et al
. 1972)
.
A total of 37 tick species were allegedly found on
Didelphimorphia
. Most tick species were occasionally found on these
types
of hosts, apart from some doubtful diagnoses such as those of
A. dissimile
on
Monodelphis
and
Didelphis
by Botelho
et al.
(2002), vague reports on marsupial infestation like that for
A. tigrinum
in
Paraguay
by Massi Pallarés and Benítez Usher (1982) or South American records of
A. pseudoconcolor
on
Philander
sp. in Guglielmone
et al.
(2003a).
Ticks found on
Didelphimorphia
are mostly
Ixodes
and to a lesser extent
Amblyomma
. Records from the Neotropical region with known tick stages found on South American marsupials total 239 for
Ixodes versus
46 for
Amblyomma
.
The difference in usage of
Didelphimorphia
as hosts for these genera is further enhanced because the total records for all species of
Amblyomma
for the whole Neotropical Region is 6947, while the corresponding number for all
Ixodes
is 1127. In other words, 21.2 % and 0.7 % of all records of
Ixodes
and
Amblyomma
, respectively, established in South
America
(exclusively or non-exclusively) are for infestation on
Didelphimorphia
and this difference is statistically significant (P <0.001, chi-square distribution).
Several species of
Amblyomma
were detected on
Didelphimorphia
, but with one exception, none of them appear to be strongly bound to these hosts. A total of 15 records correspond to the Neotropical and Nearctic
A. cajennense
; however, this represents a minimum of the approximately 1435 Neotropical records for this species. The same applies for the five records of
A. aureolatum
(a tick with an ample South American distribution) because total records for this species are 237. The only exception may apply to
A. fuscum
because there are six records of sub-adult ticks of this species on
D. aurita
(Barros-Battesti
et al
. 2005; Martins
et al.
2010; Sabatini
et al.
2010).
The situation is quite different for
Ixodes
.
A total of 12 species were determined on didelphimorph marsupials, but records of
I. affinis
,
I. aragaoi
,
I. boliviensis
,
I. fuscipes
,
I. lasallei
,
I. pararicinus
and
I. rubidus
do not seem to have ecological relevance, while the alleged record of
I. longiscutatus
is probably the result of an erroneous identification. Nevertheless,
Didelphimorphia
are important hosts for
I. amarali
,
I. loricatus
,
I. luciae
and
I. venezuelensis
.
Ixodes amarali
has been recorded on six occasions on
Didelphidae
belonging to
Didelphinae
; four of them were adult ticks collected (one record included larvae and nymphs of
I. amarali
) from
M. domestica
(Marmosini Hershkovitz)
, while the remaining records corresponded to adult ticks from
D. albiventris
and
D.
cf.
aurita
(
Didelphini
Gray). These few findings of
I. amarali
are considered of ecological relevance because they represent the majority of records for adult
I. amarali
.
All records of
I. amarali
, including those records different to
Didelphidae
, are from
Brazil
, more specifically from eastern
Brazil
(
Figure 1
).
The situation of
I. venezuelensis
is similar to that described for
I. amarali
because the records on didephimorphs are not abundant (14) but they are relevant for the total records for the species that is distributed in
Colombia
,
Costa Rica
,
Panama
and
Venezuela
(
Figure 1
). Nine records were from Marmosini as follows: two from
Marmosa
(all for subadult ticks), one for
Gracilinanus
(subadult ticks) and five for
Monodelphis
(two for subadult ticks, two for subadult and adult ticks and one for adult ticks), while the five records from
Didelphini
were for the genera
Philander
(four records of subadult ticks) and
Didelphis
(one record of adult ticks)
The records of
I. loricatus
and
I. luciae
on
Didelphimorphia
are numerous and they represent the majority of all records for both species. Hosts of the different tribes and species of
Didelphidae
for the different combination of parasitic stages of
I. loricatus
(including records form
Argentina
,
Brazil
,
Paraguay
and
Uruguay
) and
I. luciae
are shown in
Tables 1
and
2
, respectively.
Caluromys
Allen
has been found infested only twice with
I. luciae
; the contribution of Metachirini Hershkovitz was also minimal with just one record for
I. luciae
, while representatives of Thylamyini Hershkovitz have been found infested four times with
I. luciae
.
TABLE 1.
Records of
Ixodes loricatus
and their parasitic stages found on
Didelphimorphia
of the family
Didelphidae
from
bona fide
records in Argentina, Brazil, Uruguay and Paraguay, L= larva, N= nymph, A= adult.
Hosts
Didelphidae
|
A |
AN |
AL ANL |
N |
L |
NL Total |
Didelphinae
Didelphini
|
Chironectes minimus
Didelphis albiventris
*
|
1 31 |
0 6 |
0 0 3 2 |
0 0 |
0 0 |
0 1 0 42 |
D. aurita
**
D. marsupialis
Didelphis
sp.***
Lutreolina crassicaudata
|
19 0 24 9 |
2 0 1 5 |
1 0 1 0 1 0 0 1 |
0 0 0 0 |
0 0 0 0 |
0 22 0 1 0 26 0 15 |
Philander frenatus
|
9 |
1 |
0 1 |
1 |
0 |
0 12 |
P. opossum
Philander
sp. Marmosini
|
1 1 |
0 0 |
0 0 0 0 |
0 0 |
0 0 |
0 1 0 1 |
Marmosa murina
Marmosa
sp.
|
0 4 |
0 0 |
0 0 0 0 |
1 2 |
0 0 |
0 1 0 6 |
Monodelphis americana
M. dimidiata
|
0 0 |
0 0 |
0 0 0 0 |
1 0 |
0 0 |
0 1 1 1 |
M. sorex
Total
|
0 99 |
0 15 |
0 0 6 4 |
0 5 |
0 0 |
1 1 2 131 |
* Includes two records classified as probably
D. albiventris
;
**Includes 17 records classified as probably
D. aurita
; ***
Includes three records classified as
D. albiventris
and/or
D. aurita
.
Therefore, most records were from species belonging to the tribes
Didelphini
and Marmosini. The great majority of
I. loricatus
and
I. luciae
adults were found on
Didelphini
, but the situation is different for subadult ticks.
Table 1
shows that 30 records of
I. loricatus
on
Didelphimorphia
involved larval and/or nymphal ticks, of which 24 (80 %) were determined on
Didelphini
.
Table 2
shows 27 records of subadult
I. luciae
on
Didelphimorphia
, 21 of which (78 %) were from Marmosini. It appears that species belonging to
Didelphini
are the most important hosts for all parasitic stages of
I. loricatus
, while
I. luciae
appears to depend on
Didelphini
for adult maintenance and Marmosini to feed subadult tick. However, this should be considered a general statement because records are few, no information was obtained about densities of hosts and ticks, and the probability of trapping bias which was not considered for the analysis.
Literature on
I. loricatus
infesting
Didelphimorphia
shows a wide distribution range that includes
Argentina
,
Uruguay
,
Paraguay
,
Brazil
,
Venezuela
,
Panama
, while the record form
Colombia
is first record for this species. This range is augmented considering the records in
Guatemala
on a “wild host” by Monroy Lefebre and Cejas González (1988) and on
A. geoffroyi
in
México
by Keirans (1982, 1985). The southernmost record of
I. loricatus
is from an unknown host in Tierra del Fuego (
Argentina
) (Neumann 1901).
However, the only record each of
I. loricatus
from
Panama
and
Colombia
are known now to be the result of misidentification. Moreover, all records of this species from
Venezuela
have to be considered cautiously because Vogelsang and Cordero (1940) do not specify tick stages found on hosts and provide no clue how the diagnoses was obtained, while Jones
et al
. (1972) treat as tentative their records on
Didelphidae
, bringing doubts about the presence of
I. loricatus
in the country. The same condition applies to the record on “wild hosts” for
Guatemala
and conversely for the Mexican record on a monkey. Finally the record from Tierra del Fuego is also unconvincing because
I. loricatus
has not been found again south of 35ºS where
Didelphimorphia
is absent (see discussion section for further details). In brief,
bona fide
records of
I. loricatus
encompass
Uruguay
,
Argentina
,
Paraguay
and
Brazil
, most of them in eastern South
America
. The southernmost confirmed record for this tick is in La Balandra (
34º56´S
57º42´W
), province of Buenos Aires,
Argentina
(Nava
et al.
, 2004), while the northernmost record lies in the Reserva Ecológica de Gurjaú (
08º14´S
35º00´W
) in the State of Pernambuco,
Brazil
(Botelho
et al.
2004) (see the note above in
I. loricatus
for not considering Curralinho (
01º43´S
49º43´W
) as the northernmost record of this species).
Figure 2
shows the distribution of
I. loricatus
with indication of wrong and doubtful records.
TABLE 2.
Records of
Ixodes luciae
and their parasitic stages found on
Didelphimorphia
of the family
Didelphidae
from
bona fide
records in Argentina, Belize, Bolivia, Brazil, French Guiana, Guatemala, Panama, Peru, Surinam, Trinidad and Tobago, and Venezuela. L= larva, N= nymph, A= adult.
Hosts |
A |
AN |
AL |
ANL |
N |
L |
NL |
Total |
Didelphidae
Caluromyinae
Caluromys lanatus
|
1 |
0 |
0 |
0 |
0 |
0 |
0 |
1 |
C. philander
Didelphinae
Didelphini
|
0 |
0 |
0 |
0 |
0 |
1 |
0 |
1 |
Didelphis albiventris
D. marsupialis
Didelphis
sp.
|
1 26 4 |
0 0 0 |
0 0 0 |
1 0 0 |
0 0 0 |
0 0 0 |
0 0 0 |
2 26 4 |
Lutreolina crassicaudata
Philander andersoni
P. opossum
Marmosini
|
1 3 16 |
0 0 0 |
0 0 0 |
0 0 0 |
0 0 0 |
0 0 0 |
0 0 0 |
1 3 16 |
Marmosa constantiae
|
0 |
0 |
0 |
0 |
1 |
0 |
0 |
1 |
M. murina
|
0 |
0 |
0 |
0 |
0 |
1 |
0 |
1 |
M. demererae
M. robinsoni
|
0 0 |
0 1 |
0 0 |
0 0 |
2 1 |
0 1 |
0 2 |
2 5 |
Marmosa
sp.
Monodelphis brevicaudata
*
Monodelphis
sp. Metachirini
|
1 0 1 |
0 0 0 |
0 0 0 |
0 0 0 |
0 2 1 |
1 1 0 |
0 6 1 |
2 9 3 |
Metachirus nudicaudatus
Thylamyini
|
1 |
0 |
0 |
0 |
0 |
0 |
0 |
1 |
Marmosops impavidus
Thylamys cinderella
|
1 0 |
0 0 |
0 0 |
0 0 |
0 1 |
0 0 |
0 0 |
1 1 |
T. venustus
Thylamys
sp. Total
|
0 0 56 |
0 0 1 |
0 0 0 |
0 0 1 |
1 1 10 |
0 0 5 |
0 0 9 |
1 1 82 |
* All references to
Monodelphis brevicaudata
have to be considered cautiously because considerable controversy exists about it and related species.
The distribution of
I. luciae
is also wide, including
Argentina
(north-west),
Bolivia
,
Peru
,
Brazil
,
French Guiana
,
Surinam
,
Trinidad-Tobago
,
Venezuela
,
Panama
,
Guatemala
,
Belize
and
Mexico
for records on
Didelphimorphia
. This distribution is augmented if
Colombia
(Wells
et al.
1981),
Costa Rica
,
Ecuador
(Guglielmone
et al.
2003b),
Nicaragua
(Jones
et al
. 1972) and
Honduras
(Onofrio 2002), all from undetermined hosts and unknown tick stages, are included in its range. However, the alleged southernmost record of
I. luciae
in Buenos Aires province,
Argentina
, by Ivancovich and Luciani (1992) is in error (see the note above in
I. luciae
and the discussion section for details).
Figure 3
shows the distribution of
I. luciae
.
FIGURE 1
. Distribution of
Ixodes amarali
(¤) and
I. venezuelensis
(․).
The monotypic order Microbiotheridae is peculiar because
D. gliroides
is infested by
I. neuquenensis
in southwestern
Argentina
and southern
Chile
in coincidence with the range of the hosts. The records are not numerous but all of them were from this host. Therefore,
I. neuquenensis
is the only species exclusively found on a South American marsupial.
Finally,
Paucituberculata
does not appear to be important hosts for
Ixodidae
because there is just one record for
I. jonesae
for this
type
of host. Nevertheless, this may also be a consequence of inadequate tick searching.