Research Article |
Corresponding author: Edgar F. Mendoza-Franco ( efmendoz@uacam.mx ) Academic editor: Kai Horst George
© 2022 Ana Luisa May-Tec, Carlos Baños-Ojeda, Edgar F. Mendoza-Franco.
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:
May-Tec AL, Baños-Ojeda C, Mendoza-Franco EF (2022) Parasitic crustaceans (Branchiura and Copepoda) parasitizing the gills of puffer fish species (Tetraodontidae) from the coast of Campeche, Gulf of Mexico. ZooKeys 1089: 73-93. https://doi.org/10.3897/zookeys.1089.79999
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New information on the marine parasitic crustaceans from the Campeche coast, Gulf of Mexico (GoM), can improve our baseline knowledge of the ecology of both the host and parasite by providing, for example, parameters of infection. Such knowledge is especially important for fish farming, so that appropriate quarantine measures can be established. Our aim was to morphologically identify the parasitic crustaceans infecting puffer fish of commercial importance in the coastal zone of Campeche, Mexico. We provide new information on four known species of parasitic crustaceans from 92 specimens representing five species of tetraodontid fish. The parasitic crustaceans Argulus sp. (Branchiura, Argulidae), Caligus haemulonis (Caligidae), Pseudochondracanthus diceraus (Chondracanthidae), and Taeniacanthus lagocephali (Taeniacanthidae) (all Copepoda) were found on Lagocephalus laevigatus, Sphoeroides nephelus, S. parvus, S. spengleri, and S. testudineus. This study revealed the occurrence of P. diceraus, which is of importance in aquaculture, on Sphoeroides annulatus in the Mexican Pacific. Additionally, our results and other documentary records provide the first evidence of the interoceanic occurrence of the same parasitic crustacean species in the south-southwest of Gulf of Mexico, the Atlantic Ocean, and the Pacific Ocean. Moreover, our study provides valuable information on the biodiversity of parasitic crustaceans present in the GoM on puffer fish which are of great commercial importance for human consumption, fisheries, and aquaculture.
Argulidae, aquaculture, biodiversity, Caligidae, Chondracanthidae, fisheries, interoceanic, Taeniacanthidae
Parasitic crustaceans are commonly known to cause serious lesions on farmed fish, causing destruction of gill tissue and favoring secondary infection, diseases, and massive mortality worldwide (
In Mexico, studies on parasitic crustaceans belonging to Branchiura and Copepoda are scarce considering the high diversity of host species inhabiting the vast aquatic ecosystems (
The diversity of fish on the Campeche coast includes species such as puffer fish (Tetraodontiformes, Tetraodontidae) which are considered an economically important resource in southern Mexico and have the potential for aquaculture (
Our aim was to identify morphologically the parasitic crustaceans infecting Lagocephalus laevigatus (Linnaeus, 1766), Sphoeroides nephelus (Goode & Bean, 1882), S. parvus (Shipp & Yerger, 1969), S. spengleri (Bloch, 1785), and S. testudineus (Linnaeus, 1758), all commercially important in the coastal zone of Campeche, Mexico. The geographic distribution of these copepods on puffer fish from the tropics is briefly discussed based on our findings and previous records.
Using gill nets, we collected 92 puffer fish (69 L. laevigatus, 17 S. spengleri, 2 S. testudineus, 2 S. parvus, and 2 S. nephelus) from Seybaplaya, Campeche, southern Gulf of Mexico (19°42.580'N, 90°44.155'W), between November 2020 and April 2021. Fish were kept on ice for a maximum of 8 h and transported to the Laboratory of Aquatic Parasitology of EPOMEX (Instituto de Ecología, Pesquerías y Oceanografía del Golfo de México), Universidad Autónoma de Campeche (
In total, 92 tetraodontid fish specimens were collected. The most abundant fish species was L. laevigatus, followed by S. spengleri, while S. testudineus, S. parvus, and S. nephelus were the least abundant species. Three parasitic crustacean species were found on L. laevigatus and a single species was found on the four Sphoeroides spp.
Order Arguloida Yamaguti, 1963
Family Argulidae Leach, 1819
Smooth puffer Lagocephalus laevigatus (Linnaeus) (Tetraodontidae) (TL: 27.5–47 cm).
Gills.
Prevalence: 9% (six fish infected of 69 examined); mean abundance: 0.14 ± 1.03; intensity range: 1–3 individuals.
Two voucher specimens deposited in the CNIN (171); collected on 30 November 2020.
These specimens are identified morphologically as Argulus sp., mainly by the shape and armature of cephalothoracic appendages, the presence of a modification of the first maxilla into a cup-like, stalked sucker, and legs (
Order Cyclopoida Burmeister, 1834
Family Chondracanthidae Milne Edwards, 1840
Sphoeroides maculatus (Bloch & Schneider, 1801) (type host) from California (
Southern puffer Sphoeroides nephelus (TL: 21.6–21.6 cm), least puffer S. parvus (TL: 19.5–23 cm), bandtail puffer S. spengleri (TL: 13.9–24.0 cm), and checkered puffer S. testudineus (TL: 17.2–26.0 cm).
Gills.
Sphoeroides nephelus: prevalence: 100% (two fish infected of two examined); mean abundance: 5 ± 1.4; intensity range: 4–6 copepods. S. parvus: 100% (two fish infected of two examined); 2 ± 1.4; 1–3 copepods. S. spengleri: 89% (16 fish infected of 18 examined); 5.72 ± 4.89; 1–19 copepods. S. testudineus: 100% (two fish infected of two examined); 4 ± 1.4; 3–5 copepods.
Ten voucher specimens (5 ♂, 5 ♀) from S. spengleri plus voucher and two specimens from S. nephelus, S. parvus, and S. testudineus deposited in the CNIN (172); collected on 27 April 2021.
(based on 10 females and 7 males). Adult female body 2.20–3.57 long. Head 0.75–0.87 long and 0.50–0.80 wide. Female genital complex elliptical, and entirely covered with small spines. Length of genital portion 1.34–2.35, and 0.56–1.0 wide. Length of egg strings 2.29–4.21 (Fig.
Pseudochondracanthus diceraus was originally described by
Irodes lagocephali Pillai, 1963: 124, fig. 7. Syn.
Taeniacanthus sabafugu Yamaguti & Yamasu, 1959: 102, pl. 4, figs 79, 89.
Lagocephalus laevigatus (type host) from Padre Island (Texas coast), Brazil, Alabama (Texas), Mississippi, and the Argentine Sea (
Smooth puffer Lagocephalus laevigatus (Linnaeus) (Tetraodontidae) (TL: 20.3–48.5 cm).
Gills.
Prevalence: 40% (28 fish infected of 69 examined); mean abundance: 1.10 ± 2.90; intensity range: 1–9 copepods.
Ten voucher specimens (10 ♀) deposited in the CNIN (173); collected on 30 November 2020.
(based on 10 females). Total body length (not including setae of caudal rami) 2.52–3.33; cephalothorax length 0.54–0.76 and width 0.76–1.01 (Fig.
Taeniacanthus lagocephali has been reported on Lagocephalus spp. from the Oriental region (Japan and Taiwan), the Ethiopian region (West Africa), the Nearctic region (GoM coast of Mississippi, Alabama, and Texas), and the Neotropical region (Brazil) (
Family Caligidae Burmeister, 1835
See Table
Smooth puffer Lagocephalus laevigatus (Linnaeus) (Tetraodontidae) (TL: 20.3–48.5 cm).
Gills.
Prevalence: 49% (34 fish infected of 69 examined); mean abundance: 3.63 ± 7.45; intensity range: 1–30 copepods.
Ten voucher specimens (5 ♀, 5 ♂) deposited in the CNIN (174); collected on19 January 2021.
(based on 10 females and 10 males). Adult female body caligiform, 2.70–3.30 long. Cephalothorax 1.50–1.80 long and 1.43–1.63 wide. Female genital complex longer than wide, lacking distinct posterolateral lobes (Fig.
Currently, the genus Caligus comprises more than 270 valid species worldwide (
Previous records of Caligus haemulonis on a wide variety of fish teleost (14 families) and one elasmobranch species having cosmopolitan distribution.
Host | Locality | Reference |
---|---|---|
Ariidae | ||
Ariopsis felis (Linnaeus, 1766) (as Hexanematichthys felis, Galeichthys felis and Arius felis) | Atlantic coast of USA |
|
Aspistor luniscutis (Valenciennes, 1840) (as Arius luniscutis, Notarius luniscutis) | Brazil |
|
Bagre marinus (Mitchill, 1815) (as Felichthys marinus and Bagre marina) | Atlantic coast of USA |
|
Carlarius heudelotii (Valenciennes, 1840) (as Arius heudelotii) | Africa, Mediterranean |
|
Genidens barbus (Lacepède, 1803) | Brazil |
|
Carangidae | ||
Campogramma glaycos (Lacepède, 1801) (as Lichia vadigo) | Mediterranean |
|
Caranx crysos (Mitchill, 1815) | Louisiana |
|
Caranx rhonchus Geoffroy Saint-Hilaire, 1817 (as Caranx angolensis) | Africa South |
|
Trachurus trachurus (Linnaeus, 1758) | Africa South |
|
Engraulidae | ||
Anchoa marinii Hildebrand, 1943 | Brazil |
|
Ephippidae | ||
Chaetodipterus faber (Broussonet, 1782) | Brazil, Florida |
|
Haemulidae | ||
Anisotremus virginicus (Linnaeus, 1758) | Belize |
|
Haemulon carbonarium Poey, 1860 | Belize |
|
Haemulon macrostomum Günther, 1859 | Belize |
|
Haemulon plumierii (Lacepède, 1801) | Belize |
|
Haemulon sciurus (Shaw, 1803) (type host) | Danish West Indies of Insular Caribbean |
|
Haemulon steindachneri (Jordan & Gilbert, 1882) | Brazil |
|
Orthopristis ruber (Cuvier, 1830) | Brazil, Florida |
|
Plectorhinchus mediterraneus (Guichenot, 1850) (as Diagramma mediterraneum) | Africa, Mediterranean |
|
Kyphosidae | ||
Girella tricuspidata (Quoy & Gaimard, 1824) | Australia |
|
Monacanthidae | ||
Aluterus schoepfii (Walbaum, 1792) (as Aleuterus schoepfi) | Florida |
|
Myliobatidae | ||
Aetobatus narinari (Euphrasen, 1790) (as Stoasodon narinari) | Tabasco to Campeche coast Gulf of Mexico |
|
Polynemidae | ||
Polydactylus quadrifilis (Cuvier, 1829) | Africa |
|
Pomatomidae | ||
Pomatomus saltatrix (Linnaeus, 1766) (as Temnodon saltator) | Mediterranean |
|
Rachycentridae | ||
Rachycentron canadum (Linnaeus, 1766) | USA |
|
Sciaenidae | ||
Argyrosomus regius (Asso, 1801) (as Sciaena aquila) | Mediterranean |
|
Bairdiella chrysoura (Lacepède, 1802) | Florida |
|
Menticirrhus americanus (Linnaeus, 1758) (as Menthicirrhus americanus) | Brazil, Florida |
|
Micropogonias furnieri (Desmarest, 1823) (as Micropogon furnieri) | Brazil |
|
Paralonchurus brasiliensis (Steindachner, 1875) | Brazil |
|
Pogonias cromis (Linnaeus, 1766) | Florida |
|
Pseudotolithus moorii (Günther, 1865) (as Corvina camaronensis) | Africa South |
|
Sciaena umbra Linnaeus, 1758 (as Corvina nigra) | Mediterranean |
|
Sciaenops ocellatus (Linnaeus, 1766) (as Sciaenops ocellata) | Louisiana |
|
Umbrina sp. | Africa South |
|
Serranidae | ||
Centropristis striata (Linnaeus, 1758) | Florida |
|
Sparidae | ||
Archosargus probatocephalus (Walbaum, 1792) | Florida |
|
Archosargus rhomboidalis (Linnaeus, 1758) | Brazil |
|
Dentex sp. | Africa, Mediterranean |
|
Dentex gibbosus (Rafinesque, 1810) (as D. filosus) | Africa South |
|
Pagrus sp. | Africa, Mediterranean |
|
Pagrus pagrus (Linnaeus, 1758) | Brazil |
|
Triglidae | ||
Prionotus punctatus (Bloch, 1793) | Brazil |
|
Trigla lyra Linnaeus, 1758 | Africa South |
|
Caligus haemulonis and 13 other parasitic copepods are included in the Caligus productus group; they are characterized by loss of two and reduction or loss of the third of the three plumose setae on the distal exopod segment of the first swimming leg (see
This study represents the first records of branchiuran and copepod parasites on tetraodontids of the Campeche coast. Previous records from this area mentioned the presence of 15 species of copepods parasitizing elasmobranchs; some have also been reported for other elasmobranch species worldwide (
Members of Argulus have a wide range of fish hosts and environments (freshwater and marine) around the world. In the GoM, 10 species have been reported, especially from the north-northwest coast of the USA (
The morphological characteristics of specimens Taenicanthus lagocephali in L. laevigatus collected here agree with the original description and redescription of specimens from North and South America (
With exception of L. laevigatus, all other species of Sphoeroides examined were parasitized with P. diceraus. This suggests that Sphoeroides spp. could be the preferred hosts of this parasite. Future examination of other hosts in the same area is necessary to confirm this assumption. This is the first record of P. diceraus parasitizing a puffer fish from the GoM. In previous studies on parasitofauna of puffer fishes from the southern of GoM (
Our findings suggest that the composition of ectoparasites on puffer fishes from the Campeche coast differs from that reported for the Yucatán Peninsula by
The occurrence of P. diceraus in the Pacific and along the Campeche coast is noteworthy. Pseudochondracanthus diceraus was originally described in commercially important fish Sphoeroides maculatus from the Atlantic and Pacific coast of the USA (Wilson, 1908); however, S. maculatus is a fish native to the North Atlantic. Its presence in the Pacific is remarkable and it is tempting to speculate that its presence there is the result of translocation of parasites associated with the natural distribution of their hosts or a consequence of anthropogenic activities (i.e., host introductions;
On the other hand, the broad geographic distribution of P. diceraus could be explained by a hypothesis suggested by
Therefore, the geographical distribution of both parasitic crustacean and the monogeneans could be attributed to the dispersal capabilities of their hosts (
We have revealed the occurrence of marine parasitic crustaceans of importance for fish aquaculture on the Campeche coast. We have deduced that the composition of ectoparasites on puffer fishes of the Campeche coast and Yucatán Peninsula differ and this difference is associated with differing environmental characteristics of each area, despite the geographical proximity. Our results represent only a small fraction of diversity of parasitic crustaceans present in the GoM, but they provide valuable new information on the geographical distribution and hosts in the region (i.e., the occurrence of an interoceanic copepod species), which is especially relevant aquaculture. To explore host specificity, the ecological and parasite-host interaction associated with their distribution, studies focusing on morphology and phylogenetics are essential.
This research was supported financially by a postdoctoral grant (216405) and a master student fellowship (scholarship number 1077567) from CONACyT, Mexico, to A.L.M.-T. and C.B.-O., respectively. We thank to Francisco Javier Gómez Criollo (EPOMEX) for help with identifying the fish, and Mariela del Carmen Rosado Tun (Aquatic Parasitology, EPOMEX) for assistance during the laboratory work. We would like to express our sincere thanks to the administrative and academic authorities of the Universidad Autónoma de Campeche (