Reappraisal of Goezeella Fuhrmann, 1916 (Cestoda: Proteocephalidae), parasites of Neotropical catfishes (Siluriformes), with description of a new species from Pimelodella cristata (Heptapteridae)
Author
Philippe V. Alves
Author
Alain de Chambrier
Author
José L. Luque
Author
Tomáš Scholz
text
Revue suisse de Zoologie
2017
2017-09-30
124
2
335
350
journal article
31804
10.5281/zenodo.893547
106613a0-b98c-4607-a9e9-5b22b351ff81
0035-418
893547
Goezeella mariae
sp. nov.
Figs 1, 2, 5-9
,
22-30
Holotype:
CHIOC 38860a-f, a whole-mounted specimen (1 slide) and 5 slides of serial cross-sections, collected on 25.05.2013, host field no. BR AMP 46a. – MHNG-PLAT-97017 (2 slides of cross-sections).
Paratypes:
IPCAS C-759, a whole-mounted specimen (1 slide; hologenophore), host field no. BR AMP 106b. – CHIOC 38861, IPCAS C-759, MHNG-PLAT-86883, a whole-mounted specimen (one slide), 6 slides of serial cross-sections and 2 slides of sagittal sections of scolex, host field No. BR AMP 109a. – MHNG-PLAT-97016, a whole-mounted specimen (one slide; SEM voucher), host field no. BR AMP 111b; all specimens collected on 25.05.2013.
Type and only known locality:
Lowermost Amazon River near Macapá, State of Amapá, Brazil (00°01’N, 50°59’W).
Figs 16-19.
Goezeella siluri
Fuhrmann, 1916
ex
Pinirampus pirinampu
. (16) Pregravid proglottid, ventral view (MHNG-PLAT-21877). (17) Cross-section at ovary level (MHNG-PLAT-21879). (18) Terminal genitalia, dorsal view (MHNG-PLAT-21879). (19) Eggs drawn in distilled water (MHNG-PLAT-19858). Abbreviations: cc – chromophilic cells; ci – cirrus; cs – cirrus-sac; do – dorsal osmoregulatory canal; em – bilayered embryophore; ga – genital atrium; ln – longitudinal nerve cord; oe – outer envelope; on – oncosphere; oo – ovary outgrowths; te – testes; vi – vitelline follicle; vo – ventral osmoregulatory canal; vs – vaginal sphincter.
Figs 20-21.
Goezeella danbrooksi
de Chambrier, Rego & Mariaux, 2004
ex
Ageneiosus pardalis
(holotype, USNM 1370061). (20) Cross-section at middle part of proglottid. (21) ovary level. Abbreviations: do – dorsal osmoregulatory canal; lm – internal longitudinal musculature; ov – ovary; st – subtegumental muscle fibres; su – subtegumental cells; te – testes; tg – tegument; ut – uterus; vi – vitelline follicles; vo – ventral osmoregulatory canal.
Type and only known host:
Pimelodella cristata
(Müller & Troschel)
(
Siluriformes
:
Heptapteridae
).
Site of infection:
Anterior intestine.
Prevalence:
7 fish examined/4 fish infected (57%).
Representative DNA sequences:
A fragment 1491bp long of the
lsr
DNA (D1–D3 domains) (GenBank
MF370208
).
Etymology:
The species is dedicated to the first author’s mother, Maria Thereza Vieira Pinto Alves, for providing continuous support for his studies.
Description:
(based on 4 whole-mounted worms; 13 slides with serial cross-sections of mature proglottids and 2 slides with sagittal sections of 1 scolex; 1 scolex studied using SEM).
Proteocephalidae
. Testes, ovary, vitelline follicles and uterus cortical; small-sized worm. Total body length 14-38 mm (n = 3), maximum width up to 1.3 mm (n = 3). Strobila acraspedote, anapolytic, with longitudinal and transverse grooves, consisting of about 40-90 proglottids: 27-32 immature, 4-8 mature, 10-15 pregravid and 23-39 gravid. Immature and mature proglottids much wider than long (length: width ratio 0.17-0.35), pregravid proglottids markedly wider than long (length: width ratio 0.40-0.76) and gravid proglottids slightly wider than long to much longer than wide (length: width ratio 0.80-2.60).
Scolex 0.68-0.83 × 0.91-1.15 mm (n = 3), much wider than neck (proliferation zone), 0.83-1.20 × 0.75-0.81 mm, bearing 4 biloculate suckers, with loculi unequal in size; anterior loculus 158-161 (x = 160; n = 3) in diameter, posterior loculus 123-126 (x = 125; n = 3) in diameter; loculi separated by inconspicuous interlocular septum (
Figs 1, 2
,
22, 23
). Metascolex present, more wrinkled than neck (
Figs 1, 2
,
22
). Apex rounded, lacking apical organ, with few gland cells (
Figs 1, 2
,
22, 23
). Apex of scolex, lumen of suckers, surface between suckers and base of metascolex covered with acicular filitriches, less dense on lumen of suckers (
Figs 5-8
); neck covered with capilliform filitriches (
Fig. 9
).
Figs 22-27.
Goezeella mariae
sp. nov.
ex
Pimelodella cristata
. (22) Scolex, dorsoventral view (holotype, CHIOC 38860a). (23) Scolex, sagittal section (paratype, CHIOC 38861). (24) Pregravid proglottid, ventral view (paratype MHNG-PLAT-97016). (25) Gravid proglottid, dorsal view (holotype, CHIOC 38860a). (26) Terminal genitalia, dorsal view (holotype, CHIOC 38860a). (27) Eggs drawn in distilled water (paratype IPCAS C-759). Abbreviations: al – anterior sucker loculus; cc – chromophilic cells; ci – cirrus; cs – cirrus-sac; do – dorsal osmoregulatory canal; em – bilayered embryophore; ga – genital atrium; oe – outer envelope; on – oncosphere; pl – posterior sucker loculus; te – testes; vi – vitelline follicles; vo – ventral osmoregulatory canal; vs – vaginal sphincter.
Inner longitudinal musculature well-developed, formed by numerous, individual muscle fibres not forming compact bundles, more concentrated laterally (
Figs 28- 30
). Osmoregulatory canals situated at same level of lateral-most testes, median to vitelline follicles, markedly sinuous (
Figs 24-26
,
28-30
); ventral osmoregulatory canal wider than dorsal one (
Fig. 30
).
Testes numerous, spherical to oval, small, 34-46 in diameter, in 1 irregular layer, 103-167 (x = 134; n = 13) per mature proglottid (
Figs 24, 25
). Testes form 1 irregular field on dorsal side, less numerous alongside median line of proglottids (uterine stem), usually reaching laterally to osmoregulatory canals, dorsally overlapping cirrus-sac, vitelline follicles and sometimes ovary (
Figs 24-26
,
28- 30
). Testes present also in gravid proglottids.
Vas deferens coiled, with loops forming elongate field reaching to, but not crossing, median line of proglottid (
Figs 24-26
). Cirrus-sac elongated to pear-shaped, thinwalled (
Figs 24-26
,
28
), 130-213 × 59-85 (n = 13), its length representing 11-24% (x = 17; n = 13) of proglottid width. Sperm duct (internal vas deferens) sinuous (
Figs 24-26
,
28
). Cirrus muscular, reaching up to 64% (n = 13) of cirrus-sac length. Common genital atrium narrow, deep (
Figs 24-26
,
28
). Genital pores alternating irregularly, markedly pre-equatorial, situated at 7-17% (x = 11; n = 13) of proglottid length from anterior margin (
Figs 24-26
).
Fig. 28.
Goezeella mariae
sp. nov.
ex
Pimelodella cristata
. Cross-section at the cirrus-sac level (holotype, CHIOC 38860d). Abbreviations: cc – chromophilic cells; ci – cirrus; cs – cirrus-sac; ed – ejaculatory duct; va – vas deferens.
Ovary with wide isthmus in medulla and two follicular, grape-like lobes penetrating to dorsal cortex; numerous dorsal outgrowths present (
Figs 24, 25
,
30
). Length of ovary represents 21-31% (x = 26%; n = 13) of proglottid length, its width representing 57-77% (x = 66%; n = 13) of proglottid width (
Figs 24, 25
). Mehlis’ gland about 60- 138 in diameter, representing 8-11% of proglottid width (n = 13). Relative ovarian size, i.e., percentage of ovary surface to total surface of mature or pregravid proglottids (see de
Chambrier
et al
., 2012
), 10-15% (x = 12%; n = 13).
Vaginal canal slightly sinuous, surrounded by chromophilic cells, wider in terminal part (
pars copulatrix vaginae
); terminal vaginal sphincter present (
Figs 24-26
). Vagina anterior to cirrus-sac (n = 32). Vitelline follicles cortical, ventral, forming 2 long uninterrupted bands, occupying large triangular field, widened and confluent posteriorly at ovary level; lateral to lateral-most testes (
Figs 24-26
,
29
). Length of bands represents 73-91% (x = 83%) and 72-91% (x = 83%) of length of proglottid on poral and aporal side, respectively (n = 13) (
Figs 24, 25
). Uterus cortical, with development of type 2 (see de
Chambrier
et al
., 2004b
,
2015b
); uterine stem and diverticula (lateral uterine branches) in mature and pregravid proglottids lined with numerous chromophilic cells, extended much beyond branches (
Fig. 24
). Uterus with 14-25 lateral diverticula on each side (
Figs 24, 25
). Eggs oval, outer envelope 21-25 × 18-19, bilayered embryophore 19-20 × 13-15, oncosphere 9-10 × 11-12, embryonic hooks 5-6 long (
Fig. 27
).
Remarks:
Goezeella mariae
sp. nov.
differs from
G
.
siluri
and
G
.
danbrooksi
in having fewer testes (103- 167 vs. 183-310 and 282-366 in
G
.
danbrooksi
and
G
.
siluri
, respectively) and inconspicuous interlocular septum (not obvious in SEM images; see
Figs 1, 2
), rather than the septum conspicuous as in the two other species. The new taxon can be further distinguished from
G
.
siluri
by its smaller dimensions, such as the total body length (14-38 mm vs. 90-230 mm), scolex width (0.91-1.15 mm vs. 1.45-1.94 mm) and the length of the cirrus-sac (130-213 μm vs. 220-340 μm) as well as the appearance of the metascolex, which is more wrinkled in
G. mariae
sp. nov.
compared to that of
G
.
siluri
; compare
Figs 1, 2
with
Figs 3, 4
. Moreover,
G. mariae
sp. nov.
possesses a terminal, rather than markedly subterminal, vaginal sphincter as it is in
G
.
danbrooksi
.
The new species differs in its sequence of the partial
lsr
DNA gene (D1–D3 domains) from that of
G. siluri
from
P. pirinampu
in 14 nucleotides, i.e. genetic divergence 0.9%. A phylogenetic analysis (data not shown) revealed both taxa clustered in a clade comprising also both known species of
Gibsoniela
Rego, 1984
, i.e.
G
.
mandube
(
Woodland, 1935
)
and
G
.
meursaulti
de
Chambrier & Vaucher, 1999
, parasites of the auchenipterid catfish
Ageneiosus inermis
(Linnaeus, 1766)
in the Neotropical Region, but interrelations within this lineage remain unresolved. Close relationship of species of
Goezeella
with those of the genus
Gibsoniela
is not evident based on their morphology, because they differ in the position of the internal organs in relation to the inner longitudinal musculature (previously used to distinguish individual subfamilies – see
Rego, 1994
), but also by the morphology of the scolex (no metascolex in the latter genus) and their suckers (biloculate in
Goezeella
vs.
Figs 29-30.
Goezeella mariae
sp. nov.
ex
Pimelodella cristata
. (29) Cross-section at middle part of proglottid (holotype, CHIOC 38860d). (30) Cross-sections at ovary level
(
paratype MHNG-PLAT-86883). Abbreviations: do – dorsal osmoregulatory canal; lm – internal longitudinal musculature; ln – longitudinal nerve cord; ov – ovary; st – subtegumental muscle fibres; su – subtegumental cells; te – testes; tg – tegument; ut – uterus; vi – vitelline follicles; vo – ventral osmoregulatory canal.
triloculate in
Gibsoniela
) (
Rego, 1984
; de
Chambrier & Vaucher, 1999
).
To the best of our knowledge, this is the first parasite found in
Pimelodella cristata
. This heptapterid catfish was described from a tributary of the Branco River, Guyana (
Bockmann & Guazzelli, 2003
) and is distributed throughout the Amazon River basin, inhabiting the sand bottom of creeks and rivers (
Reis & Lima, 2009
).
Proteocephalus bagri
Holcman-Spector & Mañé-Garzón, 1988
and
P
.
rhamdiae
Holcman-Spector & Mañé-Garzón, 1988
, both from
Rhamdia sapo
(Valenciennes)
[syn. of
Rhamdia quelen
(Quoy & Gaimard)
] in Uruguay, are the only other proteocephalids known from heptapterids in South America (
Holcman-Spector & Mañé-Garzón, 1988
). In addition,
Proteocephalus brooksi
García-Prieto, Rodríguez & Pérez-Ponce de
León, 1996
was described from
Rhamdia guatemalensis
(Günther)
in Mexico by
García-Prieto
et al.
(1996)
.