Parasites (Isopoda: Epicaridea and Nematoda) from ghost and mud shrimp (Decapoda: Axiidea and Gebiidea) with descriptions of a new genus and a new species of bopyrid isopod and clarification of Pseudione Kossmann, 1881
Author
Boyko, Christopher B.
Author
Williams, Jason D.
Author
Shields, Jeffrey D.
text
Zootaxa
2017
2017-12-19
4365
3
251
301
journal article
31134
10.11646/zootaxa.4365.3.1
506d11e3-029a-482b-ad11-cff65e539fa9
1175-5326
1117980
C5AC71E8-2F60-448E-B50D-22B61AC11E6A
Heliconema
sp.
Fig. 11
Material examined.
United States
:
2 worms (7.4,
8.2 mm
),
ex
gill tissue of ovigerous female
Lepidophthalmus louisianensis
(13.0 mm CL), Grande Terre, Lousiana, coll. unknown,
25 May 1988
(
ULLZ
3531); 8 worms (3 extracted: 7.5, 9.7,
11.5 mm
; one specimen on SEM stub,
USNM
1459849
ex
ULLZ
10208),
ex
ventral thorax and base of third pereopods of female
L
.
louisianensis
(
8.8 mm
CL), inshore, Bay St. Louis,
Mississippi
, coll. unknown,
18 Jul 1990
(
ULLZ
10208); 1 worm (not extracted),
ex
gill tissue of female
L
.
louisianensis
(
8.9 mm
CL), outer beach, Bay St. Louis,
Mississippi
, coll. R. Griffis & D. L. Felder,
26
Jan 1991
(
ULLZ
10203).
Distribution.
Mississippi
and
Louisiana
,
U.S.
A
.
Host.
Lepidophthalmus louisianensis
(Schmitt, 1935)
.
Remarks.
Three specimens of
Lepidophthalmus louisianensis
(Schmitt, 1935)
were parasitized by juvenile non-encysted nematodes (
Fig. 11
). One of the parasitized hosts (ULLZ 3531) was an ovigerous female and contained two worms extending into the gills and thorax. The other two hosts were non-ovigerous females and contained one worm (ULLZ 10203) in the gill tissue and eight worms (ULLZ 10208) in the ventral thorax and bases of third legs. The extracted nematodes ranged in length from
7.4 to 11.5 mm
(8.9±1.7, n=5). Based on the morphology of the nematodes, particularly the structure of the mouth (
Fig. 11B, C
), they are members of
Physalopteridae
, most closely matching the genus
Heliconema
Travassos, 1919
. The oral aperture of each of our specimens has two pseudolabia; each pseudolabium has a pair of cephalic papillae, a large median conical tooth and ridged teeth (
Fig. 11B
) while the amphids are indistinct. These characters are similar to those of
H. brooksi
Crites & Overstreet, 1991
, which was described from the shrimp eel,
Ophichthus gomesii
(Castelnau, 1855)
, collected in
Mississippi
Sound, Gulf of
Mexico
.
Crites & Overstreet (1991)
also found a juvenile nematode in a shrimp,
Penaeus setiferus
(Linnaeus, 1767)
, and suggested that the juvenile specimen may also be
H. brooksi
but noted that additional research was required for verification. In addition to
H. brooksi
, an undescribed species of
Heliconema
from the sharptail eel,
Myrichthys acuminatus
(Gronow, 1854)
, also exists in the Gulf of
Mexico
(Moravec, pers. comm.).
Larvae of other
Heliconema
species are known from crustacean intermediate hosts. Those of
Heliconema anguillae
Yamaguti, 1935
, are known to occur in the brachyurans
Hemigrapsus
sp. and
Perisesarma bidens
(De Haan, 1835)
in
Japan
(
Katahira & Nagasawa 2015
) and it is possible that the “
Ascarophis
” third-stage larvae described by
Moravec
et al
. (2003)
from the brachyuran
Macrophthalmus
hirtipes
(Heller, 1865)
(=
Hemiplax hirtipes
(Jacquinot, in Hombron & Jacquinot, 1846))
in
New
Zealand
were also larvae of a species of
Heliconema
(Moravec, pers. comm.). Species of nematodes from other families also use callianassids as intermediate hosts and are trophically transmitted to elasmobranchs or bony fish as definitive hosts (
Poinar & Thomas, 1976
). For example, two unidentified species of
Ascarophis
van
Beneden, 1871
, were found in
Neotrypaea californiensis
(Dana, 1854)
from
California
(
Poinar & Thomas 1976
).
FIGURE 11.
Scanning electron micrographs of
Heliconema
sp.
ex
Lepidophthalmus louisianensis
(Schmitt, 1935)
(USNM 1459849
ex
ULLZ 10208). A, whole juvenile worm, lateral view; B, anterior end,
en face
view; C, anterior end, lateral view; D, posterior end, oblique view. P = cephalic papillae, to = median conical tooth, te = ridged teeth. Scale bars: A = 1 mm; B = 30 µm; C = 50 µm; D = 200 µm.
There are no reports on the specific diet of the shrimp eel,
O. gomesii
, but it is likely an opportunistic feeder, based on the stomach contents of congeners (
Casadevall
et al
. 1994
) and has been reported to feed “heavily on shrimps” (
Crites & Overstreet 1991
);
L. louisianensis
is therefore a potential prey item. Based on stomach content analyses, potential definitive hosts in the Gulf of Mexico for this species of
Heliconema
are bottom feeding fish predators of
L. louisianensis
, including croaker (
Menticirrhus
sp.,
Sciaenidae
) and unspecified catfish (
Felder & Rodrigues 1993
). Stingrays are also possible predators of
L. louisianensis
based on observations of their feeding habits (
Felder & Rodrigues 1993
).
Anguilliform fish host the highest diversity of
Heliconema
species but nematodes in this genus are also known from four other actinopterigian orders, as well as two orders of elasmobranchs (see
Akram 1996
;
Li
et al
. 2013
). Although two species of
Heliconema
have been reported from snakes,
Moravec
et al
., (2007)
summarized the persistent doubts as to the identity of the
type
hosts for
H
.
longissimum
(
Ortlepp, 1923
)
. The host of this nematode was originally identified as “snakes” (in quotation marks as originally given by
Ortlepp, 1923
) but this species has subsequently been reported several times from eel hosts. Interestingly, only one species of
Heliconema
was ever described from adult worms extracted from a host verified as a snake:
H
.
serpens
Fusco & Palmieri, 1980
, described from
Cerberus rynchops
(Schneider, 1799)
and found in only a single host individual (
Fusco & Palmieri 1980
). Because these snakes are well-known consumers of eels (
Gorman
et al
. 1981
) it is possible that the snake picked up the nematodes through parasitized prey and thus served as a postcyclic host (
sensu
Odening 1976
) for
H
.
serpens
; the snake was not a paratenic host because the worms were mature. If true, this would be analogous to the situation reported by
Goldberg
et al
. (2002)
who found mature lizard-parasitizing nematodes in the lumen of the digestive tract of snakes who preyed on parasitized lizards. Indeed,
Goldberg
et al
. (2002)
cautioned that any finding of adult nematodes in a snake must consider the possibility that the nematodes entered via the snake’s prey, their definitive host, and not because the snake ingested an intermediate host of the parasite.