New occurrences and host records for two species of parasitic isopods (Isopodaı Cymothoidaı Bopyridae) associated with caridean shrimps (Decapodaı Caridea) from Brazil
Author
Horch, Felipe Bezerra Ribeiro ı Amanda Porciuncula
Author
Williams, Jason D.
text
Journal of Natural History
2019
2020-01-14
53
39
2437
2447
journal article
24062
10.1080/00222933.2019.1704589
8f1615fb-8ba7-4fe9-9e10-013a9d175180
1464-5262
3666376
Probopyrus
cf.
pandalicola
(Packardı 1879)
Figures 2
ı 3
Abbreviated synonymy (see
Markham 1985
; the synonymy list below includes only taxonomic resources since
1985ı
see discussion for taxonomic notes and non-taxonomic references).
Bopyrus pandalicola
Packardı 1879: 308
–
310
ı fig. 262
[
type
locality: unspecifiedı east coast of the
United States
].
Probopyrus pandalicola –
Markham 1985: 26
–
35
ı 127
–
128 (Table 2; in part)ı 134ı figs. 7
–
8;
Verdi and Schuldt 1988: 22
–
24
;
Kensley and Schotte 1989: 112
ı 266 (lists; in part);
Jiménez and Vargas 1990: 457
–
462
ı figs. 1
–
11;
Román-Contreras 1993: 689
ı 690ı 694ı 695;
Brasil-Lima 1998: 209
;
Alvarez-León et al. 1999: 17
–
21
ı 19 (Table 1; in part)ı fig. 1;
Rocha and Bueno 2000: 134
ı 137ı 138;
Román-Contreras and Bourdon 2001: 918
ı 920 (Table 1)ı 922 (Table 2);
Román-Contreras 2004: 153
ı 154 (Table 1)ı 156ı 157 (Table 2)ı 161ı figs. 1ı 2; Román- Contreras and
Martinez-Mayén 2011:
1145
ı
1149ı
1150;
Pralon et al. 2018: 6
ı 7;
Saito et al. 2010: 173
(Table 1; in part)ı 179. not
Probopyrus pandalicola
:
Campos and de Campos 1989: 29
–
34
ı 33 (Table 1);
Alvarez- León 1993
: 307
–
308;
Alvarez-León et al. 1999: 17
–
21
ı 19 (Table 1; in part); Bunkley-
Williams and Williams 1998: 149
ı 150 (Table 1; in part).
Material examined
Brazil
: mature
female
(
4.4 mm
TL)ı Olivençaı Ilhéusı
Bahia
(
14°56
ʹ
28.4
”
Sı
39°00
ʹ
39.3
”
W
)ı 06/
V
/
2015ı
Coll. J.
T
.
Lisboaı infesting left branchial chamber of male
Palaemon northropi
(Rankinı 1898)
(
9.8 mm
CL) (
UFRGS 6630
); Mature male (
1.09 mm
TL)ı same data; mature female (
3.45 mm
TL) and mature male (
0.9 mm
TL)ı infesting right branchial chamber of male
P
.
northropi
(
4.5 mm
CL)ı same data; mature female (
2.6 mm
TL)ı infesting left branchial chamber of female
P
.
northropi
(3.0 mm CL)ı same data; mature female (
1.9 mm
TL)ı infesting left branchial chamber of female
P
.
northropi
(3.0 mm CL)ı same data; mature female (
1.5 mm
TL)ı infesting left branchial chamber of female
P
.
northropi
(
3.4 mm
CL)ı same data; mature female (
1.2 mm
TL)ı infesting left branchial chamber of female
P
.
northropi
(
3.5 mm
CL)ı same data; mature female (
2.7 mm
TL) and mature male (
0.9 mm
TL)ı infesting right branchial chamber of female
P
.
northropi
(
3.9 mm
CL)ı same data
.
Figure 2.
Probopyrus
cf.
pandalicola
(
Packard, 1879
)
, females (UFRGS 6630): (a), habitus dorsal view (4.4 mm TL); (b), habitus ventral view (4.4 mm TL); (c), antennule (left) and antenna (right) (3.45 mm TL); (d), barbula (2.6 mm TL); (e), maxilliped (2.6 mm TL); (f), maxilliped palp (2.6 mm TL); (g), maxilliped spur (2.6 mm TL); (h), oostegite 1, outer view (3.45 mm TL); (i), oostegite 1, inner view (3.45 mm TL); (j), right pereopod 1 (3.45 mm TL); (k), right pereopod 7 (3.45 mm TL). Scale bars: (a) and (b) = 1.0 mm; (c) = 0.1 mm; (d) = 0.37 mm; (e) = 0.2 mm; (f) and (g) = 0.1 mm; (h) and (i) = 0.25 mm; (j) and (k) = 0.1 mm.
Figure 3.
Probopyrus
cf.
pandalicola
(
Packard, 1879
)
, male (1.09 mm TL) (UFRGS 6630): (a), habitus ventral view; (b), habitus dorsal view; (c), antennule; (d), antenna; (e), left pereopod 1; (f), left pereopod 7. Scale bars: (a) and (b) = 0.25 mm; (c–f) = 0.05 mm.
Remarks
We have provisionally identified these specimens as
Probopyrus
cf.
pandalicola
which has been reported from
P. northropi
in Mexicoı Venezuelaı
and
Brazil
(
Markham 1985
). The new record from Ilhéusı Bahiaı
Brazil
is approximately
1200 km
south of previous collections of
P. pandalicola
from Vila Velhaı
Pernambuco
. The adult female specimens of
P
. cf.
pandalicola
analysed here (
Figure 2
) are characterised by a pyriform bodyı subtriangular cephalon with anterior margin slightly extending beyond pereionı subrectangular maxilliped with palp on anterior lobe bearing five setae and prominent spurı oostegite 1 internal ridge with five digitiform projectionsı dactyli of pereopods 1 and 7 deeply inset in propodiı and pleomeres separated laterally and pleotelson deeply bilobed. This combination of charactersı as well as those of the male (
Figure 3
)ı are closest morphologically to
P. pandalicola
(versus
P.
fl
oridensis
Richardsonı 1904) but without larval morphology or molecular data it is presently not possible to be more definitive in identification (see below). Howeverı the present female specimens differ from Markham
’
s (1985) material in having a broad frontal lamina (
Figure 2
(a)) (lacking frontal lamina in Markham
’
s specimens)ı antenna 2 with two articles (
Figure 2
(c)) (antenna 2 with three articles in Markham
’
s specimens) and maxilliped palp large and not inset in the distal margin of the anterior maxilliped article (
Figure 2
(eıf)) (maxilliped palp small and inset in the distal margin of the anterior maxilliped article in Markham
’
s specimens).
Probopyrus pandalicola
has a complex taxonomic history with multiple species being synonymised by
Markham (1985)
and purportedly recorded from over 15 species of freshwater and marine palaemonid shrimp (
Kensley and Schotte 1989
). Howeverı
Román-Contreras (1993)
concluded that three species synonymised by
Markham (1985)
are distinct from
P. pandalicola
:
P. bithynis
Richardsonı 1904
[Louisianaı
USA
infesting
Macrobrachium ohione
(Smithı 1874)
and
M. olfersii
(Wiegmannı 1836)
]ı
P.
fl
oridensis
[Floridaı
USA
infesting
Palaemon paludosus
(Gibbesı 1850)
]ı and
P. panamensis
Richardsonı 1912
[Paraisoı
Panama
infesting
M. acanthurus
(Wiegmannı 1836)
]. A fourth species
P. palaemoneticola
(Packardı 1881)
[Atlantic coastı
USA
from
Palaemon
Weberı 1795
] was later synonymised with
P. pandalicola
by
Román-Contreras and Martinez-Mayén (2011)
ı in agreement with Markham
’
s (1985) assessment. Adult female specimens of
P. bithynis
can be distinguished from
P. pandalicola
by horn-shaped anterolateral processes on the head and the presence of a largeı subtriangular high carina on the seventh pereopodı both of which are lacking in the material examined from
Brazil
. In additionı the epicaridium and cryptoniscus larvae of
P. bithynis
are distinct from
P.
fl
oridensis
and
P. pandalicola
(
Dale and Anderson 1982
)
. Unfortunatelyı adult specimens of
P.
fl
oridensis
and
P. pandalicola
are difficult to distinguish based on morphology (see Table
1 in
Román-Contreras and Bourdon 2001
); howeverı the larvae can be distinguished by morphometric analysis (
Dale and Anderson 1982
).
Jiménez and Vargas (1990)
were in error when stating
‘
it is impossible to separate the larvae of
P. pandalicola
and
P.
fl
oridensis’
; these authors presumably were only considering epicaridium larvae and did not take into consideration the morphometric data of
Dale and Anderson (1982)
that showed significant differences between both the epicaridium and cryptoniscus larval stages of
P.
fl
oridensis
and
P. pandalicola
(as well as differences in swimming speed and pigmentation of the cryptoniscus larvae). Thusı although almost morphologically indistinguishable as adultsı
P.
fl
oridensis
and
P. pandalicola
appear to represent reproductively isolated species and we accept the conclusion of others that they are valid species (
Román-Contreras 1993
;
Rocha and Bueno 2000
;
Saito et al. 2010
). Presently there are four species of
Probopyrus
recognised in
Brazil
:
P. bithynisı
P.
fl
oridensisı
P. palaemoni
Lemos de Castro and Brasil-Limaı 1974
[from
Palaemon pandaliformis
(Stimpsonı 1871)
]ı and
P. pandalicola
.
It is important to note that much work remains to be done in testing species boundaries in this group. Although
P. pandalicola
has been considered by some to be on both sides of the isthmus of
Panama
(
Kensley and Schotte 1989
;
Vargas-Ceballos et al. 2016
)ı the presence of the species in the eastern Pacific has been questioned (
Román-Contreras 2004
). These debates are amenable to testing with new collections and molecular data to determine if the species truly has such a wide geographic and host use pattern (known in some other bopyrids; see
Athelges
Gerstaeckerı
1862 in
McDermott et al. 2010
;
Argeia
Danaı
1853 in
An et al. 2015
) or represents an even more diverse cryptic species complex than currently recognised. Specimens of
P. pandalicola
collected from the Rhode Riverı Chesapeake Bayı MD have been sequenced for cytochrome oxidase subunit 1 (COI) and vouchered (USNM 1463140)ı thus can serve as a starting point for such work. Members of the genus
Probopyrus
are some of the best studied bopyrids in terms of morphology and development (e.g.
Dale and Anderson 1982
)ı ecology (e.g.
Beck
1979
ı
1980
; Chaplin- Ebanks and
Curran 2007
;
Conner and Bauer 2010
)ı and impacts on host physiology and/ or behaviour (reviewed in
Brinton and Curran 2015aı
2015b
). We urge researchers to appropriately preserve and voucher the parasites during future studies in order to allow for accurate identificationı particularly because some of the results on their interactions with hosts are potentially confounded by lack of taxonomic knowledge (
Conner and Bauer 2010
).