Research Article |
Corresponding author: Edgar F. Mendoza-Franco ( efmendoz@uacam.mx ) Academic editor: David Gibson
© 2018 Edgar F. Mendoza-Franco, Mariela del Carmen Rosado Tun, Allan de Jesús Duarte Anchevida, Rodolfo E. del Rio Rodríguez.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Mendoza-Franco EF, Rosado TMC, Duarte AAD, Rodríguez RER (2018) Morphological and molecular (28S rRNA) data of monogeneans (Platyhelminthes) infecting the gill lamellae of marine fishes in the Campeche Bank, southwest Gulf of Mexico. ZooKeys 783: 125-161. https://doi.org/10.3897/zookeys.783.26218
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During the examination of 913 fish specimens belonging to four families in the Campeche Bank (Gulf of Mexico), 23 gill ectoparasitic monogenean species were found, which belong to three families: Dactylogyridae, Microcotylidae and Diclidophoridae. The species Euryhaliotrema amydrum, E. carbuncularium, E. dunlapae, E. fajeravilae, E. fastigatum, E. longibaculum, E. paracanthi, E. tubocirrus, Haliotrematoides cornigerum, H. gracilihamus, H. heteracantha, H. longihamus, H. magnigastrohamus, H. striatohamus, Hamatopeduncularia bagre, Neotetraonchus bravohollisae, and N. felis (all Dactylogyridae) were found on the hosts Lutjanus synagris, L. griseus, Ariopsis felis, Bagre marinus, Archosargus rhomboidalis, and Haemulon plumieri. Additionally, Microcotyle archosargi, Microcotyle sp., and Microcotyloides incisa (all Microcotylidae) were found on L. griseus and A. rhomboidalis; finally, Choricotyle sp. 1, Choricotyle sp. 2, and Choricotyle sp. 3 (all Diclidophoridae) were found on H. plumieri. The prevalence, abundance, mean intensity of infection, and supplementary taxonomic revisions for all monogeneans found are provided. Partial sequences of the 28S rRNA gene were also obtained for monogeneans of ariid, sparid, and haemulid host fishes to explore their systematic position within the Monogenea. New locality and host records for some previously described species of Euryhaliotrema, Hamatopeduncularia, Microcotyle, and Choricotyle from lutjanid, ariid, sparid, and haemulid hosts were reported. The present study adds evidence supporting the interoceanic occurrence of the same monogenean species (on lutjanids) on the west-east Atlantic and Pacific Oceans (= amphiamerican species). As previously suggested, there are at least, two possibilities to explain that parasite distribution: differentiation of morphological features in these monogeneans have resulted in only slight to insignificant morphological changes developing over the extended period of 3.2 mya (when the Isthmus of Panama was closing) and/or speciation is only evident at molecular level.
Ariidae , Choricotyle , Euryhaliotrema , Haemulidae , Haliotrematoides , Hamatopeduncularia , Lutjanidae , Microcotyle , Microcotyloides , Monogenea , Neotetraonchus , Sparidae
The Campeche Bank (southwest Gulf of Mexico) represents an important marine ecosystem characterized by a high biodiversity, which is threatened by important overfishing and energy (petroleum) extraction activities (
Biodiversity is widely considered to correlate with ecosystem health, the presence or abundance of parasites becomes part of that positive biodiversity. Otherwise, the fewer the parasites observed, the worse the environmental conditions and thus the biodiversity (see
Despite their ecological and environmental effects, there have been few studies aimed at collecting and examining fish samples for parasites; in consequence, many parasite species go undetected or are poorly studied. Low availability and poor quality of material for examination also adds to this problem. This lack of knowledge about biodiversity also prevents us for understanding the connectivity between the northern and southern Gulf fisheries.
As part of a research project on fish parasite biodiversity in the Campeche Bank, we had the opportunity to undertake a survey of ectoparasitic monogeneans infecting the gill lamellae of six marine fish species. Here, we provided: 1) supplementary information and illustrations of the sclerotised and/or soft structures of the monogenean species found; 2) information on the prevalence and intensity of infections at each site sampled; and 3) data on the biometrical variability of individual monogenean species collected on different hosts. In addition, partial sequences of the 28S rRNA gene (D1–D3) were amplified from monogeneans of ariid, sparid, and haemulid hosts to explore their systematic position within the Monogenea. The occurrence of the monogenean species found with respect to the west-east Atlantic and Pacific divide is briefly discussed.
We studied the most abundant fish species (
All other measurements were obtained from unflattened specimens stained with Gomori’s trichrome stain. Measurements are in micrometers and expressed as the mean followed by the range and number (n) of structures measured in parentheses; body length and greatest width includes and exclude the haptor, respectively. Illustrations were prepared with the aid of a drawing tube on a Leica DM 2500 microscope with differential interference contrast and phase contrast optics. The direction of the coil (clockwise vs. counterclockwise) of the copulatory organ was determined following
Prior to DNA analysis, parasites were fixed with 96% ethanol and individually identified based on the morphology of their haptors. The haptor of each specimen was removed using syringe needles (used for insulin injections) and mounted unstained in a mixture of LA and GAP. The body of the worm was transferred to a labeled Eppendorf tube containing 96 % ethanol and stored at room temperature until required for molecular evaluation. Processed haptors were then remounted in Canada balsam (see Mendoza-Franco et al. 2009) and studied using an immersion oil objective on a DM2500 Leica microscope. These haptors were kept as molecular vouchers (hologenophore, i.e., the voucher specimen from which the molecular sample was obtained; see
Two to ten bodies of excised specimens from the gills of ariid, sparid, and haemulid fishes collected at each of the three sampling sites were placed individually in a 0.2 µl Eppendorf tube for genomic DNA extraction. Genomic DNA of each individual was extracted using 20 µl Chelex (100 sodium) and 5 µl proteinase K (at 10mg µl-1) to lyse parasite tissues. Specimens were immediately incubated for 3 h and 15 minutes at 96 °C to denature the proteinase K. Volumes of 5 µl were taken from each lysed preparation to serve as template DNA samples in the PCR assays. A fragment of the 28S rRNA gene (D1–D3) was amplified using the polymerase chain reaction (PCR). The internal primers Halio-F (5´-ACCCGCTGAATTTAAGCAT-3´) and Halio-R (5´-TGGTCCGTGTTTCAAGAC-3´) were used for amplification (
28S (D1–D3) sequences obtained in the current study were aligned with that of other monogenean species available in GenBank using Muscle algorithm implemented in Mega 7 (
A total of 913 fish specimens across six species [Lutjanus synagris (Linnaeus, 1758), Lutjanus griseus (Linnaeus, 1758) (Lutjanidae); Ariopsis felis (Linnaeus, 1766); Bagre marinus (Mitchill, 1815) (Ariidae); Archosargus rhomboidalis (Linnaeus, 1758) (Sparidae); and Haemulon plumieri (Lacepède, 1801) (Haemulidae)] were collected at the three locations aforementioned (San Francisco: 308 individuals–33.7%; Champoton: 335–36.7% and Seyba: 270–29.6%). 803 of these specimens (88%) were infected with monogeneans. A total of 23 monogenean species from three families was found (see Table
Gill ectoparasitic monogeneans (Platyhelminthes) on marine fishes from the Campeche Bank (southwest Gulf of Mexico).
Parasite family/species | Host families and species | |||||
---|---|---|---|---|---|---|
Lutjanidae | Ariidae | Sparidae | Haemulidae | |||
Lutjanus synagris | Lutjanus griseus | Ariopsis felis | Bagre marinus | Archosargus rhomboidalis | Haemulon plumieri | |
Dactylogyridae | ||||||
Euryhaliotrema amydrum | – | – | – | – | +⁰ | – |
E. carbuncularium ‡ | – | – | – | – | +⁰ | – |
E. dunlapae | – | – | – | +⁰ | – | |
E. fajeravilae † | – | +⁰ | – | – | – | – |
E. fastigatum † | – | +/ | – | – | – | – |
E. longibaculum | +/ | +⁰ | – | – | – | – |
E. paracanthi † | – | +/ | – | – | – | – |
E. tubocirrus | +/ | +/ | – | – | – | – |
Haliotrematoides cornigerum | +/ | – | – | – | – | – |
Hal. gracilihamus | – | +/ | – | – | – | – |
Hal. heteracantha † | +/ | +/ | – | – | – | – |
Hal. longimanus | +/ | – | – | – | – | – |
Hal. magnigastrohamus | +/ | – | – | – | – | – |
Hal. striatohamus ‡ | – | – | – | – | – | +/ |
Hamatopeduncularia bagre ‡ | – | – | – | +/ | – | – |
Neotetraonchus bravohollisae | – | – | +/ | – | – | – |
N. felis ‡ | – | – | +/ | – | – | – |
Microcotylidae | ||||||
Microcotyle archosargi ‡ | – | – | – | – | +⁰ | – |
Microcotyle sp. | – | – | – | – | +/ | – |
Microcotyloides incisa † | – | +/ | – | – | – | – |
Diclidophoridae | ||||||
Choricotyle sp. 1‡ | – | – | – | – | – | +⁰ |
Choricotyle sp. 2 | – | – | – | – | – | +⁰ |
Choricotyle sp. 3 | – | – | – | – | – | +⁰ |
Euryhaliotrema
Kritsky & Boeger, 2002: 12, fig. 1;
Euryhaliotrema amydrum Kritsky & Bakenhaster, 2011: 64, figs 17–24.
Archosargus probatocephalus (Walbaum, 1792)
A. rhomboidalis (new host)
San Francisco: 18 fish (mean TL 26.9 cm; range 17–23.6) infected of 18 examined (100 %); abundance, 37; intensity of infection, 22–51 worms. Seyba Playa: 25 fish (TL 28.4; 19.2–30.5) infected of 25 examined (100 %); abundance, 37; intensity of infection, 29–47. Champoton: 45 fish (TL 28.2; 24.7–30.5) infected of 45 examined (100 %); abundance, 23; intensity of infection, 8–35.
(measurements based on six specimens). Body 336 (305–350; 6) long; greatest width 80 (70–90; 4). Pharynx 23 wide. MCO a counterclockwise coil of 1–2 rings, proximal ring 11 (10–12; 5) diameter. Haptor 77 (67–84; 4) wide. Ventral anchor 31 (28–36; 10) long; dorsal anchor 43 (40–45; 9) long. Ventral bar 35 (30–41; 7) long; dorsal bar 33 (32–34; 4) long.
This species was originally described on the sheepshead A. probatocephalus from the Indian River Lagoon in Florida (
Six reference specimens in the CNHE (10607).
Archosargus probatocephalus
A. rhomboidalis (new host)
(measurements based on three specimens). Ventral anchor 48 (46–49; 4) long; dorsal anchor 41 (48–54; 3) long. Haptor 60 wide. Ventral bar 32–34 long.
In A. rhomboidalis, a simultaneous infection with E. amydrum was found. Since all worms could not be identified, the data on infection rate relate to E. carbuncularium and E. amydrum. Euryhaliotrema carbuncularium was originally described on A. probatocephalus from the Indian River Lagoon near Malabar, Brevard County, Florida (
The present study also provided the first molecular data of E. carbuncularium; there are two sequences (676 and 856 bp, respectively) of individual specimens of this monogenean species included within the analyses that shows that this species forms a sister lineage to that containing Euryhaliotrema mehen (Soler-Jiménez, García-Gasca & Fajer-Ávila, 2012) Kritsky, 2012, which is known on Lutjanus guttatus (Steindachner, 1869) in the Eastern Pacific (see Figure
Molecular phylogeny of the Dactylogyridae estimated by methods of Bayesian inference (BI) and maximum likelihood (ML) using partial sequences of the 28S rRNA gene (D1–D3). Species newly sequenced for this study are in bold. Species belonging to Microcotylidae were used as outgroups. The species name is followed by the GenBank sequence ID. Posterior probabilities of the BI followed by ML are given above the branches.
Three reference specimens in the CNHE (10608).
Two slides, each containing a haptor of a specimen of E. carbuncularium used to amplify its DNA are deposited in the CNHE (10622).
Archosargus probatocephalus
A. rhomboidalis (new host)
(measurements based on seven specimens). Body 285 (200–360; 7) long; greatest width 63 (60–73; 3). MCO 17 (14–21; 7) long; proximal ring of the MCO 9 (8–10; 4) diameter. Haptor 54 (45–60; 4) wide. Ventral anchor 30 (29–31; 7) long; dorsal anchor 41 (37–47; 6) long. Hook pair 1, 14 (3) long.
A simultaneous infection with E. amydrum and E. carbuncularium occurred on A. rhomboidalis. Since all worms could not be identified, the data on infection rate relate to E. dunlapae, E. amydrum, and E. carbuncularium. Euryhaliotrema dunlapae was originally described on A. probatocephalus from the Indian River Lagoon near Malabar, Brevard County, Florida (
Seven reference specimens in the CNHE (10609).
Lutjanus argentiventris (Peters, 1869)
L. griseus (new host)
San Francisco: two fish (mean TL 28.1cm; range 21.6–39) infected of 65 examined (3 %); abundance, 0.1; intensity of infection, 1–2 worms. Champoton: 1 fish (TL 28.3; 25.2–37) infected of 37 examined (2.7 %), abundance, 0.05; intensity of infection, 2.
(measurements based on four specimens). Body 327 (200–380; 4) long; greatest width 76–80. Haptor 70 (65–75; 3) wide. MCO 19 (18–21; 4) long. Ventral anchor 39 (35–44; 8) long; dorsal anchor 55 (47–59; 8) long. Ventral bar 40 (33–54; 4) long; dorsal bar 37 (30–46; n = 4) long.
This species was described from L. argentiventris from the Perlas Archipielago, Panama by Kritsky and Mendoza-Franco (in
Four reference specimens in the CNHE (10614).
Haliotrema
fastigatum
Zhukov, 1976: 43, fig. 10;
Lutjanus apodus (Walbaum, 1792)
L. griseus
San Francisco: 63 fish (mean TL 28.1cm; range 21.6–39) infected of 65 examined (97 %); abundance, 12; intensity of infection, 10–18 worms. Seyba Playa: 40 fish (TL 28.5; 23–37) infected of 45 examined (88.8 %); abundance, 8; intensity of infection, 2–11. Champoton: 27 fish (TL 28.3; 25.2–37) infected of 37 examined (73 %); abundance, 4; intensity of infection, 4–11.
(measurements based on ten specimens). Body 356 (300–460; 9) long; greatest width 72 (54–95; 8). Haptor 70 (47–85; 8) wide. Pharynx 16 (13–18; 8) wide. MCO 32 (28–34; 7) long. Proximal ring of the MCO 18 (12–20; 8) diameter. Accessory piece 23 (21–24; 3) long. Ventral anchor 29 (27–30; 10) long; dorsal anchor 41 (38–45; 6) long. Ventral bar 36 (34–40; 7) long; dorsal bar 37 (35–46; 5) long. Hook 12 (11–12; 7) long.
Ten reference specimens in the CNHE (10621).
Haliotrema
longibaculum
Zhukov, 1976: 39, fig. 6;
Lutjanus mahogoni (Cuvier, 1828)
L. synagris and L. griseus (new host)
San Francisco: 68 fish (mean TL 28.2 cm; range 20–35.7) infected of 70 examined (97%); abundance, 12; intensity of infection, 8–19 worms. Seyba Playa: 77 fish (TL 28.4; 19.2–30.5) infected of 79 examined (97.5 %); abundance, 14; intensity of infection, 6–27. Champoton: 70 fish (TL 28.2; 24.7–30.5) infected of 75 examined (93.3%); abundance, 12; intensity of infection, 4–18.
(measurements based on ten specimens on L. synagris). Body 217 (190–270; 8) long; greatest width 62 (50–72; 4). Haptor 65 (55–80; 8) wide. Pharynx 19 (15– 24; 6) wide. MCO 21 (18–26; 6) long. Ventral anchor 25 (24–26; 9) long; dorsal anchor 37 (32–40; 11) long. Ventral bar 43 (33–49; 8) long; dorsal bar 32 (30–33; 5) long.
Euryhaliotrema longibaculum was originally described and depicted (as Haliotrema longibaculum) from L. synagris and L. mahogoni collected off Cuba (Area Havana) (
Ten reference specimens in the CNHE (10601).
Haliotrema
paracanthi
Zhukov, 1976: 42–43, fig. 9;
Lutjanus apodus
L. griseus
San Francisco: 6 fish (mean TL 28.1cm; range 21.6–39) infected of 65 examined (9 %); abundance, 0.09; intensity of infection, 1 worm. Seyba Playa: 2 fish (TL 28.5; 23–37) infected of 45 examined (4 %); abundance, 0.06; intensity of infection, 1–2; Champoton: 1 fish (TL 28.3; 25.2–37) infected of 37 examined (2.7 %); abundance, 0.02; intensity of infection, 1.
(measurements based on seven specimens). Body 348 (295–445; 6) long; greatest width 70 (70–92; 3). Haptor 71 (62–82; 4) wide. MCO 28 (25–34; 8) long. Proximal ring of the MCO 17 (13–20; 7) diameter. Ventral anchor 24 (23–25; n = 12) long; dorsal anchor 24 (24–25; n = 11) long. Ventral bar 31 (27–38; 7) long; dorsal bar 23 (23–24; 4) long. Hook 13 (12–14; 8) long.
This species was originally described as Haliotrema paracanthi by
Seven reference specimens in the CNHE (10613).
Haliotrema
tubocirrus
Zhukov, 1976: 40–41, fig. 7;
Lutjanus synagris
L. synagris and L. griseus
San Francisco: 69 fish (mean TL 28.2 cm; range 20–35.7) infected of 70 examined (98.6%); abundance, 14; intensity of infection, 8–20 worms. Seyba Playa: 77 fish (TL 28.4; 19.2–30.5) infected of 79 examined (97.5 %); abundance, 15; intensity of infection, 11–22. Champoton: 75 fish (TL 28.2; 24.7–30.5) infected of 75 examined (100 %); abundance, 17; intensity of infection, 5–27.
(measurements based on twelve specimens on L. synagris). Body 518 (402–640; 12) long; greatest width 81 (65–100; 8). Haptor 74 (53–100; 8) wide. Pharynx 28 (20–35; n = 6) wide. Male copulatory organ (MCO) 40 (35–43; n = 11) long. Accessory piece 29 (28–31; 5) long. Proximal ring of the MCO 24 (19–33; n = 8) diameter. Ventral anchor 26 (23–28; 16) long; dorsal anchor 26 (21–30; 13) long. Ventral bar 36 (32–42; 8) long; dorsal bar 28 (25–32; 8) long. Hook 13 (11–13; 12) long.
This species was originally described as Haliotrema tubocirrus from the gills of L. synagris, L. analis, L. apodus, Lutjanus cyanopterus (Cuvier, 1828) and Rhomboplites aurorubens (Cuvier, 1829) from the environs of Havana, Cuba (
The present specimens were identified as E. tubocirrus according to the redescription of this species made by
Twelve reference specimens in the CNHE (10604).
Haliotrema
cornigerum
Zhukov, 1976: 33–34, fig. 1;
Lutjanus synagris.
L. synagris.
San Francisco: 35 fish (mean TL 28.2 cm; range 20–35.7) infected of 70 examined (50 %); abundance, 3; intensity of infection, 1–7 worms. Seyba Playa: 24 fish (TL 28.4; 19.2–30.5) infected of 79 examined (30 %); abundance, 1; intensity of infection, 2–4. Champoton: 48 fish (TL 28.2; 24.7–30.5) infected of 75 examined (64 %); abundance, 14; intensity of infection, 1–21.
(measurements based on six specimens). Body 422 (320–545; 6) long; greatest width 65 (3). Haptor 60 (52–65; 5) wide. Pharynx 20 (18–23; 4) wide. MCO 56 (49–60; 6) long. Ventral anchor 40 (38–42; 6) long; dorsal anchor 53 (51–56; 10) long. Ventral bar 34 (33–34; 4) long; dorsal bar 30 (28–33; 5) long.
Identification of present specimens is based on diagnosis provided by
Six reference specimens in the CNHE (10603).
Haliotrema
cornigerum
Zhukov, 1976: 37–38, fig. 4;
Lutjanus apodus
L. griseus
San Francisco: 61 fish (mean TL 28.1cm; range 21.6–39) infected of 65 examined (94 %); abundance, 13; intensity of infection, 7–20 worms. Seyba Playa: 30 fish (TL 28.5; 23–37) infected of 45 examined (66.6 %); abundance, 8; intensity of infection, 3–8. Champoton: 35 fish (TL 28.3; 25.2–37) infected of 37 examined (94.6 %); abundance, 11; intensity of infection, 8–15.
(measurements based on ten specimens). Body 345 (270–400; 10) long; greatest width 75 (60–95; 5). Haptor 67 (60–75; 6) wide. Pharynx 13 wide. MCO 35 (31–40; 9) long. Ventral anchor 51 (46–54; 10) long, base 18 (17–19; 5) wide; dorsal anchor 65 (61–69; 20) long. Ventral bar 31 (30–34; 5) long; dorsal bar 30 (29–31; 5) long.
This species was originally described as Haliotrema gracilihamus on L. apodus from Campeche Bay (Area Havana) (
Ten reference specimens in the CNHE (10606).
Haliotrema
heteracantha
Zhukov, 1976: 36–37, fig. 3;
Lutjanus synagris
L. synagris and L. griseus
San Francisco: 40 fish (mean TL 28.2 cm; range 20–35.7) infected of 70 examined (57 %); abundance, 5; intensity of infection, 1–16 worms. Seyba Playa: 51 fish (TL28.4; 19.2–30.5) infected of 79 examined (64.5%); abundance, 17; intensity of infection, 2–13. Champoton: 35 fish (TL 28.2; 24.7–30.5) infected of 75 examined (46.6 %); abundance, 3; intensity of infection, 1–6.
(measurements based on six specimens on L. synagris). Body 418 (330–480; 8) long; greatest width 68. Haptor 80 wide. Pharynx 25 (20– 30; 2) wide. MCO 40 (30–45; 6) long. Ventral anchor 40 (38–42; 9) long; dorsal anchor 50 (47–52; 10) long. Hook 12 (3) long.
This species was originally described as Haliotrema heteracantha from L. synagris by
Both monogenean species are currently considered distinct based on the absence of a loop in the shaft of the MCO in H. heteracantha (present in Hal. guttati). However, examination of present specimens of H. heteracantha showed that morphology of the MCO is variable and a loop is present as well in the shaft of the MCO (see Figure
Six reference specimens in the CNHE (10602).
Haliotrema
longihamus
Zhukov, 1976: 35, fig. 2;
Lutjanus synagris
L. synagris
San Francisco: 15 fish (mean TL 28.2 cm; range 20–35.7) infected of 70 examined (21.4 %); abundance, 3; intensity of infection, 2–14 worms. Seyba Playa: 9 fish (TL 28.4; 19.2–30.5) infected of 79 examined (11.4 %); abundance, 1; intensity of infection, 2–6. Champoton: 2 fish (TL 28.2; 24.7–30.5) infected of 75 examined (2.6 %); abundance, 0.04; intensity of infection, 1–2.
(measurements based on ten specimens). Body 475 (390–560; 9) long; greatest width 84 (70–93; 5). Haptor 66 (58–72; 8) wide. Pharynx 25 (24– 30; 7) wide. MCO 48 (40–53; 11) long. Ventral anchor 75 (71–78; 17) long; dorsal anchor 77 (74–80; 17) long. Ventral bar 38 (37–40; 3) long; dorsal bar 39 (37–44; 4) long. Hook 12 (11–12; 10) long.
Haliotrema longihamus Zhukov, 1976 was transferred to Haliotrematoides by Kritsky et al. (2009) based on the original figures of the anchor/bar complex and MCO of this species [see
Ten reference specimens in the CNHE (10599).
Haliotrema
magnigastrohamus
Zhukov, 1976: 38, fig. 5;
Lutjanus synagris
L. synagris
San Francisco: 65 fish (mean TL 28.2 cm; range 20–35.7) infected of 70 examined 92.8 %); abundance, 9; intensity of infection, 3–13 worms. Seyba Playa: 78 fish (TL 28.4; 19.2–30.5) infected of 79 examined (98.7 %); abundance, 17; intensity of infection, 8–28. Champoton: 69 fish (TL 28.2; 24.7–30.5) infected of 75 examined (92 %); abundance, 9; intensity of infection, 5–15.
(measurements based on ten specimens). Body 352 (295–382; 7) long; greatest width 66 (50–85; 7). Haptor 64 (52–78; 8) wide. Pharynx 15 (13–19; 3) wide. MCO 28 (25–35; 8) long. Ventral anchor 37 (36–39; 18) long; dorsal anchor 29 (29–31; 17) long. Ventral bar 42 (40–45; 9) long; dorsal bar 17–18 long. Hook 13 (12–13) long.
This species was originally described by
Measurements of the present finding fits well with the morphometric of H. magnigastrohamus provided by
Ten reference specimens in the CNHE (10600).
Haliotrema striatohamus Zhukov, 1981: 179, fig. 1; Mendoza-Franco et al. 2009: 1360–1362, figs 1–8 (redescribed and transferred to Haliotrematoides).
Haemulon aurolineatum Cuvier, 1830
H. plumieri
San Francisco: 80 fish (mean TL 28.8 cm; range 22–34) infected of 90 examined (88.8 %); abundance, 20; intensity of infection, 4–41 worms. Seyba Playa: 88 fish (TL 28.9; 21.5–31.3) infected of 90 examined (97.7%); abundance 136; intensity of infection, 30–417. Champoton: 90 fish (TL 28.8; 19.3–33.3) infected of 90 examined (100 %); abundance, 91; intensity of infection, 36–166.
(measurements based on twelve specimens). Body 378 (312–450; 12) long; greatest width 78 (62–95; 8). Haptor 68 (55–75; 11) wide. Pharynx 18 (17–20; 5) wide. Copulatory complex 44 (40–55; 9) long. MCO base 20 (20–22; 4) long. Ventral anchor 40 (35–43; 10) long; dorsal anchor 45 (39–47; 12) long. Ventral bar 35 (33–38; 7) long; dorsal bar 42 (40–48; 7) long. Testis 50 (45–55; 3) long, 33 (30–35; 3) wide.
Haliotrema striatohamus Zhukov, 1981 was redescribed and transferred to Haliotrematoides Kritsky, Yang & Sun, 2009 by Mendoza-Franco et al. (2009) as Hal. striatohamus based on specimens collected from the haemulids, H. aurolineatum, H. plumieri, and Haemulon sciurus (Shaw, 1803) from the southern coast of Quintana Roo, Mexico. This species is characterized in part, in having two accessory sclerites [4 (4–5; 6) long], at the tip of the superficial root of each the ventral anchor.
In the present study, partial molecular sequences (726–746 bp) of the 28S rRNA gene (D1–D3) of Hal. striatohamus are provided for the first time. These sequences shows that Hal. striatohamus collected from Campeche is a sister species of the clade containing Hal. guttati and Haliotrematoides spinatus Kritsky & Mendoza-Franco, 2009 (see Figure
Twelve reference specimens (CNHE 10612).
Two slides, each containing a haptor of a specimen of Hal. striatohamus used to amplify its DNA are deposited in the CNHE (10623).
Bagre marinus
B. marinus
San Francisco: 2 fish (mean TL 42.3 cm; range 38–45.3) infected of 4 examined (50 %); abundance, 1; intensity of infection, 2 worms. Seyba Playa: 2 fish (TL 28.3; 27–41.5) infected of 4 examined (50 %); abundance, 0.5; intensity of infection, 1. Champoton: 36 fish (TL 28.3; 30–45.2) infected of 43 examined (83. 7%); abundance, 3; intensity of infection, 2–6.
(measurements based on eleven specimens on B. marinus). Body 1,463 (1,200–1,850; 10) long; greatest width 217 (175–262; 11). Pharynx 87 (70–112; 5) wide. MCO a coiled tube with 1 counterclockwise ring 70 (58– 97; 10) long, ring 24 (21–30; n=5) diameter. Haptor 324 (262–395; 5) wide. Ventral anchor 61 (68–101; 10) long; base 20 (18–22; 3) wide. Dorsal anchor 247 (225–262; 15) long. Ventral bar 88 (68–101; 7) long. Dorsal bar 146 (125–180; 13) long. Germarium 162 (145–190; 3) long, 66 (62–70; 3) wide. Testis 390 long, 100 wide.
Hamatopeduncularia bagre was originally described on B. marinus from Alligator Harbor, Franklin County, Florida, USA (
A 768–770 bp fragment of the 28S rRNA gene (D1–D3) of H. bagre on B. marinus was obtained in the present study, which represents the first molecular data for this monogenean. There are three sequences of individual specimens of H. bagre included into the analyses that revealed that this species forms a sister lineage to that containing N. felis (see Figure
Eleven reference specimens from B. marinus in the CNHE (10615).
Three slides, each containing a haptor of a specimen of H. bagre used to amplify its DNA are deposited in the CNHE (10627).
Ariopsis felis
A. felis
(measurements based on seven specimens). Body 890 (762–1,025; 7) long; greatest width 158 (107–200; 7). Pharynx 67–80 wide. MCO 81 (70–90; 7) long. Haptor 128 (105–145) wide. Onchium 39 (32–43; 5) long. Ventral anchor 40 (37–42; n=8) long; dorsal anchor 42 (38–45; 9). Ventral bar 61 (56–65; 4) long; dorsal bar 44 (38–49; 4) long. Hook pair 7, 46 (40–52; 5).
In A. felis a simultaneous infection with N. felis was found. Since all worms could not be identified, the data on infection rate relate to N. bravohollisae and N. felis. Neotetraonchus bravohollisae was originally described on Galeichthys felis (Linnaeus) (now A. felis), from Dauphin Island, Alabama coast, Gulf of Mexico (
Seven reference specimens in the CNHE (10617).
Ancyrocephalus
felis
Hargis, 1955a: 186–187, figs 28–33;
Ariopsis felis
A. felis
San Francisco: 1 fish (mean TL 33.7 cm; range 25–37) infected of 11 examined (9 %); abundance, 0.09; intensity of infection, 1 worm. Seyba Playa: 14 fish (TL 32.3; 29–36.5) infected of 27 examined (52%); abundance, 2; intensity of infection, 2–4; Champoton: 8 fish (TL 34.2; 27.5–46) infected of 45 examined (17.8%); abundance, 1; intensity of infection, 1–3.
(measurements based on four specimens). Body 2,837 (2,550–3,250; 4) long; greatest width 432 (415–432; 3). MCO 332 (310–368; 4) long. Haptor 197 (155–237; 3) wide. Ventral anchor 41 (40–42; 7) long. Dorsal anchor 35 (35–36; 4) long. Ventral bar 38–48 long. Dorsal bar 35. Hook pair 7, 55 long.
This species was originally described as Ancyrocephalus felis on G. felis (now A. felis) from Alligator Harbor, Franklin County, Florida (
Present specimens are clearly conspecific with those of N. felis from A. felis as redescribed by these latter authors. All these specimens have an elongate tube of the MCO directed posteriorly and reaching level of anterior end of germarium. Currently, N. felis has been reported on A. felis from Dauphin Island, Alabama coast, Gulf of Mexico (Paperna, 1977); West Ship Island, northern Gulf of Mexico off Mississippi, USA; Gulf of Mexico off Telchac Puerto and Port of Celestun, Yucatan, Mexico (
Four reference specimens in the CNHE (10616). Another slide containing a haptor of a specimen of N. felis used to amplify its DNA is deposited in the CNHE (10801).
GenBank accession number MG586868.
Archosargus probatocephalus
A. rhomboidalis (new host)
San Francisco: 17 fish (mean TL 26.9 cm; range 17–23.6) infected of 18 examined (94.4 %); abundance, 4; intensity of infection, 2–6 worms. Seyba Playa: 23 fish (TL 28.4; 19.2–30.5) infected of 25 examined (92 %); abundance, 5; intensity of infection, 5–6. Champoton: 39 fish (TL 28.2; 24.7–30.5) infected of 45 examined (86.6 %); abundance, 4; intensity of infection, 3–9.
(measurements based on nine specimens) in Table
Measurements of Microcotyle archosargi and Microcotyle tampicensis (Monogenea) on fishes from the Gulf of Mexico.
Hosts [Archosargus (Sparidae) and Diapterus spp. (Gerreidae)/ Localities | ||||
---|---|---|---|---|
Measurements |
M. archosargi on A. probatocephalus from New York, USA ( |
M. archosargi on A. rhomboidalis from Campeche Bank (Present study) | M. archosargi on A. probatocephalus from Florida USA (Kritsky and Bakenhaster 2009) |
M. tampicensis† on D. olisthostomus from Tamaulipas (northern Mexico) ( |
Body length | 8,000 | 5,077 (3,775–6,000; n =6) | 4,360 (3,950–4,680; n =6) | 4,892 |
Greatest width | 800 | 550 (400–750; n = 8) | 413 (329–469; n = 8) | 589 |
Haptor length | – | 1,762 (1,050–2,600; n = 3) | – | 1,902 |
Number of clamps | 106 | 127 (121–135; n = 5) | 87 (82–90; n = 3) | 98 |
Anterior clamps (Length) | 40 | 44 (36–55; n = 7) | – | 45 |
Posterior clamps | – | 33 (28–40; n = 5) | – | 29 |
Anterior clamps (Wide) | 80 | 73 (59–95; n = 7) | – | 74 |
Posterior clamps | – | 45 (40–50; n = 6) | 53 (49–58; n = 7) | 41 |
Buccal organ length | 100 | 61 (50–70; n = 11) | 65 (59–71; n = 8) | 74 |
Wide | – | 48 (44–53; n = 7) | 90 (76–104; n = 8) | 70 |
Genital atrium length | 100 | 147 (105–180; n = 6) | – | 279 |
Genital atrium width | 80 (90–105)‡ | 146 (110–180; n = 7) | 149 (132–170; n = 6) | 150 |
Testes number | 20-35 | 16–26 | – | 13 |
Length | 90 | 68 (60–80; n = 6) | 63 (49–87; n = 12) (diameter) | 60 |
Egg length | 170 | 198 (182–212; n = 6) | – | 135 |
Specific placement of current specimens are in agreement with diagnosis provided by
These latter authors stated that M. archosargi has two bilateral zones of small spines lying slightly posterior to the armed genital atrium, which are close to the ventral surface of the worm, but somewhat deeper within the body than those of the genital atrium. We fully concur in these morphological observations based on examination of present specimens (see Figure
However, the five vouchers of M. tampicensis were flattened and/or distorted (i.e., one specimen with distorted genital atrium, two specimens with incomplete haptor and another specimen was fragmented in three parts) due to coverslip pressure, which may have altered the length of the genital atrium. Determination of possible synonymy, therefore, will depend on recollection of the specimens of M. tampicensis from D. olisthostomus in the Gulf of Mexico for comparison with M. archosargi. In other features, present specimens of M. archosargi from A. rhomboidalis metrically fit within range from those specimens found on A. probatocephalus (see Table
This study also provided the first molecular data for M. archosargi by adding a sequence (638 bp) of an individual specimen into the analyses. This sequence of M. archosargi on A. rhomboidalis from Campeche supports conspecificity of this monogenean with other microcotylids, i.e., Microcotyle sebastis Goto, 1894 reported on scorpaeniform hosts (Sebastodes maliger Jordan & Gilbert, 1880, Sebastodes caurinus Richardson, 1844 and Sebastes sp.) from the UK, Japan, and USA; Microcotyle erythrini van Beneden & Hesse, 1863 and Microcotyle arripis Sandars, 1945 reported on perciformes (Pagellus erythrini L.), and Arripis trutta (Forster, 1801) (
Molecular phylogeny of the Microcotylidae and Diclidophoridae estimated by methods of Bayesian inference (BI) and maximum likelihood (ML) using partial sequences of the 28S rRNA gene (D1–D3). Species newly sequenced for this study are in bold. Species belonging to Polystomatidae were used as outgroups. The species name is followed by the GenBank sequence ID. Posterior probabilities of the BI followed by ML are given above the branches.
Nine reference specimens in the CNHE (10611). Another slide containing haptor of a specimen of M. archosargi used to amplify its DNA is deposited in the CNHE (10626).
GenBank accession number MG586867.
Archosargus rhomboidalis.
(measurements based on three specimens). Body 3,927 (3,235–4,950; 3) long. Maximum width 493 (310–670; 3) at germarium level. Two oral suckers 67 (55–80; 6) long by 44 (38–49; 6) width. Opisthaptor with eight narrow peduncles. Anterior clamps 34 (32–36; 3) long, 64 (58–72; 5) wide. Genital atrium 161 (155–175; 3) wide, with two bilateral zones of small spines lying posterior to the armed genital atrium and 2 posterolateral cavities. Number of testes 21–22, each subspherical 62 (50–70, 7) long, 67 (62–75; 6) wide. Eggs, 195 (187–200; 3) long, 55–105 wide, each with 2 polar filaments.
In this host species, A. rhomboidalis, a simultaneous infection with M. archosargi was found. Since all worms could not be identified, the data on infection rate relate to Microcotyle sp. and M. archosargi. The present specimens of Microcotyle sp. resembles those of M. archosargi and M. atriobursata [paratype (CNHE 0188) of Paramicrocotyle atriobursata] in the general morphology of the genital atrium, 1) two bilateral zones of small spines lying posterior to the armed genital atrium; 2) two posterolateral cavities; 3) genital atrium elliptical, occupying all postbifurcal area; in ventral view, the anterior margin of the atrium is gently curved; posteriorly, the atrium expands into a triangular shape to form an internal cavity surrounded by ventral lips with spines; anterior margin is projected as an operculum on the posterior margin (present in current specimens and M. atriobursata) (see figures 1 and 5 in Caballero y Caballero and Bravo-Hollis, 1972; Figure
Three reference specimens in the CNHE (10610).
Microcotyle
incisa
Linton, 1910: original description;
Lutjanus griseus
L. griseus
San Francisco: 13 fish (mean TL 28.1cm; range 21.6–39) infected of 65 examined (20 %); abundance, 1; intensity of infection, 1–4 worms. Seyba Playa: 24 fish (TL 28.5; 23–37) infected of 45 examined (53 %); abundance, 2; intensity of infection, 2–5; Champoton: 10 fish (TL 28.3; 25.2–37) infected of 37 examined (27 %); abundance, 1; intensity of infection, 2–6.
(measurements based on eleven specimens). Body 2,789 (1,100–4,300; 11) long; greatest width 452 (325–700; 9). Oral suckers, each 68 (63–78; 13) long, 41 (30–50; 11) long wide. Clamps, each with 52 (48–60; 8) long, 79 (68–90; 11) wide; posterior clamps 53 (46–55; 6) long, 38 (30–45; 10) wide. Prostatic bulb 79 (70–98; 6) long, 32 (25–35; 3) wide. Testes ovoid, post-ovarian, 21 to 23 in number. Eggs ellipsoidal, each with 223 (200–232; 8) long, 104 (90–123; 8) wide.
This species was originally assigned to Microcotyle based on specimens collected from L. griseus in Tortugas, Florida, and the Bermuda Islands, USA (
Eleven reference specimens in the CNHE (10605).
Haemulon plumieri (new host)
San Francisco: 53 fish (mean TL 28.8 cm; range 22–34) infected of 90 examined (58.9 %); abundance, 1; intensity of infection, 1–4 worms. Seyba Playa: 59 fish (TL 28.9; 21.5–31.3) infected of 90 examined (65.5%); abundance, 3; intensity of infection, 1–6. Champoton: 53 fish (TL 28.8; 19.3–33.3) infected of 90 examined (58.9%); abundance, 3; intensity of infection, 2–7.
Body, 2,260 (1,580–3050; 8) long. Maximum width 514 (400–635; 5) at germarium level. Two oral suckers 56 (45–60; 8) long by 40–44 width. Opisthaptor with eight narrow peduncles. Clamps 214 (150–362; 24) long, 191 (130–325; 20) wide, with 6–7 concentric arcs of small skeletal rods in dorsal fields of clamp and an apparent sucker on internal quadrant on clamp (see Ca and Sc in Figure
Choricotyle spp. from Haemulon plumieri from Campeche Bank, Mexico: Choricotyle sp. 1. (A), clamp (B), genital atrium (F), hook. Choricotyle sp. 2. (C), clamp (D), genital atrium (G), hook. Choricotyle sp. 3. (E), clamp. Scale bars: 100 µm and 20 µm for all figures, except E 50 µm and F, G 10 µm. Abbreviations: Ca = concentric arcs; Sc = sucker; Fi = filament; Mp = posterior portion of the medial sclerite; sh = shank.
Placement of present specimens in Choricotyle is based on examination of original descriptions of other species allocated or currently assigned to the genus in
The finding of Choricotyle sp. 1 constitutes the second record (the first being that of Choricotyle leonilavazquezae Lamothe-Argumedo, Aranda-Cruz & Pérez-Ponce de León, 1998, that occurs on the Pacific coast of Mexico) of a species of Choricotyle in Mexico and the first record on H. plumieri. In the present study, three species of Choricotyle (i.e., Choricotyle sp. 1, Choricotyle sp. 2 and Choricotyle sp. 3) were identified on this latter host species (see below) based on morphological features of the genital atrium, clamps and hooks on terminal lappets (when present), if they actually represent different species since variability in these diclidophorids might exhibit intraspecific differences in the shape or size of these structures above mentioned (see
The present study also provided the first molecular data on species of Choricotyle in Mexico; both sequences of Choricotyle sp. 1 included into the present analyses revealed that this species forms a sister lineage to that containing C. anisotremi (see Figure
Nine reference specimens, CNHE (10618).
Other two slides, each containing a haptor of a specimen of Choricotyle sp. 1 used to amplify its DNA are deposited in the CNHE (10624 and 10625).
Haemulon plumieri (new host)
Body, 1,500–2,100 long. Opisthaptor with eight narrow peduncles. Clamps 208 (175–250; 6) long, 235 (200–287; 8) wide with 8–9 concentric arcs of small skeletal rods in dorsal fields of clamp. Terminal lappet at posterior extremity with one pair (at least) of hooks, each 33–35 long, base 8 wide, with short filament (see Figure
Choricotyle sp. 2 has the characteristics and features of Choricotyle (i.e. species having four pairs of clamps and genital spines ranging from seven to twelve and exceptionally, from 28 to 30 in Choricotyle rohdei Cohen, Cardenas, Fernandes & Kohn, 2011). Choricotyle sp. 2 appears closest morphologically to Choricotyle sp. 1 based on the presence of concentric arcs of small skeletal rods in dorsal fields of clamp and terminal lappet with one pair of hooks of relatively similar size (i.e., 33–35 long vs. 27–33 in Choricotyle sp. 1) and having a filament connecting shank and base (see Figure
Two reference specimens, CNHE (10619).
Haemulon plumieri (new host)
Body, 620 long, 200 width. Opisthaptor with eight narrow peduncles. Clamps 196 (157–225; 3) long, 184 (200–287; 4) wide. Buccal organ, each 36–38 long. Vas deferens, Ootype and Mehli´s gland, seminal receptacle, genito-intestinal canal, oviduct and total number of testes not observed.
Haemulon plumieri was revealed to be simultaneously infected with Choricotyle sp. 1, Choricotyle sp. 2 and Choricotyle sp. 3. Because all worms could not be identified, the data on infection rate in Choricotyle sp. 1 relate to other two species, Choricotyle sp. 2 and Choricotyle sp. 3. A single specimen of this latter species collected from H. plumieri was immature (less than one mm in total length). Reproductive organs were minimally or undeveloped to determine the specific assignment precluding resolution of the specimen as new or previously described. However, assignment of the current specimen to Choricotyle is based on the morphological similarity of its haptoral sclerites to those of species of Choricotyle described above on H. plumieri.
One reference specimen, CNHE (10620).
In this study, we identified 23 gill-infecting monogenean species, assigned to three families (Dactylogyridae, Microcotylidae and Diclidophoridae) and seven genera (Euryhaliotrema, Haliotrematoides, Hamatopeduncularia, Neotetraonchus, Microcotyle, Microcotyloides, and Choricotyle), on marine fishes belonging to four families (Lutjanidae, Ariidae, Sparidae, and Haemulidae) from the Campeche Bank (southwest Gulf of Mexico) (see Table
Most monogeneans found on lutjanids in the present study were originally described from the area Havana (Gulf of Mexico) by
In the Campeche Bank, E. fajeravilae on L. griseus is reported for the first time; this monogenean species along with E. fastigatum, E. paracanthi, Hal. gracilihamus, and M. incisa in the Gulf of Mexico have previously been described and/or reported from the Pacific (
Molecular data from the present study provides evidence supporting morphological speciation of other monogeneans occurring on both sides of Isthmus. For example, E. carbuncularium from A. rhomboidalis from Campeche (Gulf of Mexico) appears to be phylogenetically associated with E. mehen from L. guttatus in the Eastern Pacific. Similarly, Haliotrematoides striatohamus from Haemulon plumieri appears to be a sister species of the clade containing Haliotrematoides guttati and Haliotrematoides spinatus, both from L. guttatus in the Pacific waters of Panama (see Figure
In summary, the present study provided six novel sequences of the 28S rRNA gene that advance our understanding of the morphology and host-parasite associations of other monogenean groups. For example, M. archosargi from the sparid A. rhomboidalis from Campeche clustered with other microcotylids (M. sebastis, M. erythrini and M. arripis) described and/or reported on perciform (Sparidae) and scorpaeniform (Sebastidae) fishes (Figure
Similarly, in some instances, congeneric and phylogenetically related monogeneans infecting hosts of the same family appear to be phylogenetically closely related based on 28S rRNA gene. For example, Choricotyle sp. 1 from the haemulid H. plumieri appears to be related to C. anisotremi on another haemulid, A. scapularis from Chile. Finally, sequences of H. bagre on B. marinus (present study) (also present on B. bagre from Brazil) show that this monogenean is a sister species of N. felis on A. felis (see Figure
This work was supported by the Consejo Nacional de Ciencia y Tecnología (CONACyT) Mexico (EFMF Grant “Biodiversidad morfológica y molecular de ectoparásitos de peces de importancia comercial en las costas de Campeche, Mexico- CB-2014-01 no. 242984). We thank Delane C. Kritsky for helpful comments on an earlier version of this manuscript and Anadelia Cu Escamilla, Francisco Javier Gomez Criollo Instituto EPOMEX, Universidad Autónoma de Campeche UAC), Paloma Guadalupe Juarez Camargo, Juan Enrique Pereañez for help during field and laboratory work. Julia Ramos Miranda (EPOMEX) assisted with the identification of some fishes. Dominique Roche (The Australian National University) reviewed the English of the manuscript.