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Corresponding author: Víctor M. Vidal-Martínez ( vvidal@cinvestav.mx ) Academic editor: Nic Smol
© 2019 David González-Solís, Lilia C. Soler-Jiménez, M. Leopoldina Aguirre-Macedo, John P. Mclaughlin, Jenny C. Shaw, Anna K. James, Ryan F. Hechinger, Armand M. Kuris, Kevin D. Lafferty, Víctor M. Vidal-Martínez.
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:
González-Solís D, Soler-Jiménez LC, Aguirre-Macedo ML, Mclaughlin JP, Shaw JC, James AK, Hechinger RF, Kuris AM, Lafferty KD, Vidal-Martínez VM (2019) Parasitic nematodes of marine fishes from Palmyra Atoll, East Indo-Pacific, including a new species of Spinitectus (Nematoda, Cystidicolidae). ZooKeys 892: 1-26. https://doi.org/10.3897/zookeys.892.38447
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Here, we present the results of a taxonomic survey of the nematodes parasitizing fishes from the lagoon flats of Palmyra Atoll, Eastern Indo-Pacific. We performed quantitative parasitological surveys of 653 individual fish from each of the 44 species using the intertidal sand flats that border the atoll’s lagoon. We provide morphological descriptions, prevalence, and mean intensities of the recovered seven species of adult nematode (Pulchrascaris chiloscyllii, Capillariidae gen. sp., Cucullanus bourdini, Cucullanus oceaniensis, Pseudascarophis sp., Spinitectus (Paraspinitectus) palmyraensis sp. nov., Philometra pellucida) and three larval stages (Pulchrascaris sp., Hysterothylacium sp., Cucullanus sp.). We recorded: Pulchrascaris chiloscyllii from Carcharhinus melanopterus; Capillariidae gen. sp. from Chaetodon lunula, Lutjanus fulvus, and Ellochelon vaigiensis; Cucullanus bourdini from Arothron hispidus; Cucullanus oceaniensis from Abudefduf sordidus; Pseudascarophis sp. from Chaetodon auriga, Chaetodon lunula, and Mulloidichthys flavolineatus; Spinitectus (Paraspinitectus) palmyraensis sp. nov. from Albula glossodonta; Philometra pellucida from Arothron hispidus; and three larval forms, Pulchrascaris sp. from Acanthurus triostegus, Acanthurus xanthopterus, Rhinecanthus aculeatus, Platybelone argalus, Carangoides ferdau, Carangoides orthogrammus, Caranx ignobilis, Caranx melampygus, Caranx papuensis, Chaetodon auriga, Chanos chanos, Amblygobius phalaena, Asterropteryx semipunctata, Valencienea sexguttata, Kyphosus cinerascens, Lutjanus fulvus, Lutjanus monostigma, Ellochelon vaigiensis, Mulloidichthys flavolineatus, Upeneus taeniopterus, Gymnothorax pictus, Abudefduf septemfasciatus, Abudefduf sordidus, and Stegastes nigricans; Hysterothylacium sp. type MD from Acanthurus triostegus, Carangoides ferdau, Chaetodon lunula, Chanos chanos, Kyphosus cinerascens, Abudefduf sordidus, and Arothron hispidus; and Cucullanus sp. from Caranx ignobilis. Spinitectus (Paraspinitectus) palmyraensis sp. nov. (Cystidicolidae) is described from the intestine of roundjaw bonefish Albula glossodonta. All the nematode species reported in this study represent new geographical records. We discuss how our survey findings compare to other areas of the Indo-Pacific, and the way the relatively numerical dominance of trophically transmitted larval stages likely reflect the intact food web of Palmyra Atoll, which includes a large biomass of large-bodied top predator sharks and ray-finned fishes.
Cucullanus, Hysterothylacium, Paraspinitectus, Philometra, Pseudascarophis, Pulchrascaris
Few studies have surveyed the parasites of all the fish species found in a habitat. In the Eastern Indo-Pacific, several studies have reported parasitic nematodes of marine fishes from Australia, French Polynesia, Okinawa (Japan), Palawan (Philippines) Indonesia, off New Caledonia,and the Hawaiian Islands (
Palmyra Atoll is one of the northern Line Islands located in the Eastern Indo-Pacific marine ecoregion (
This study is part of a larger project to understand the structure and function of the Palmyra Atoll’s food webs. This paper is a companion to three others examining different fish parasite taxa (
Individual fish were captured between 13 October and 10 November 2009, and 22 June and 28 July 2010, by seine, spear, and hook and line from the intertidal sand flats bordering the lagoon of Palmyra Atoll (05°53'00"N, 162°05'00"W). Immediately after capture, the fish were separated and anesthetised individually with 0.5 ml/L of 2-phenoxyethanol (Sigma, St. Louis, MO, USA) in plastic bags with lagoon water and transported to the laboratory facility of the Palmyra Atoll Research Consortium (PARC). Total length and weight (g) were recorded for each individual fish. Subsequently, cavities, musculature, and all internal organs were examined for metazoan parasites in a standardized way to permit a complete estimate of the nematodes intensity (
A total of 653 individual fish from 44 species were examined (Table
A total of 10 nematode taxa belonging to six families were found. Seven nematode species were adults and three were larvae (Table
Fish species examined from the lagoon flats of the Palmyra Atoll. N = number of fish examined; Max = maximum length reported for that fish species in FishBase (http://www.fishbase.se); range = total length range of the fish examined.
Host examined | Fish common name | N | Infected hosts | Max (cm) | Range (cm) |
---|---|---|---|---|---|
Acanthuridae | |||||
Acanthurus triostegus (Linnaeus, 1758) | Convict surgeonfish | 50 | 7 | 27 | 10–18 |
Acanthurus xanthopterus Valenciennes, 1835 | Yellowfin surgeonfish | 20 | 3 | 70 | 20–40 |
Albulidae | |||||
Albula glossodonta (Forsskål, 1775) | Roundjaw bonefish | 24 | 13 | 90 | 37–58 |
Apogonidae | |||||
Cheilodipterus quinquelineatus Cuvier, 1828 | Five-lined cardinalfish | 5 | 0 | 13 | 5–6 |
Balistidae | |||||
Pseudobalistes flavimarginatus (Rüppell, 1829) | Yellowmargin triggerfish | 4 | 0 | 60 | 17–53 |
Rhinecanthus aculeatus (Linnaeus, 1758) | White-banded triggerfish | 18 | 2 | 30 | 8–24 |
Belonidae | |||||
Platybelone argalus argalus (Lesueur, 1821) | Keeltail needlefish | 2 | 1 | 50 | 9–36 |
Carangidae | |||||
Carangoides ferdau (Forsskål, 1775) | Blue trevally | 5 | 4 | 75 | 33–38 |
Carangoides orthogrammus (Jordan & Gilbert, 1882) | Island trevally | 3 | 2 | 75 | 25–35 |
Caranx ignobilis (Forsskål, 1775) | Giant trevally | 4 | 4 | 170 | 56–79 |
Caranx melampygus Cuvier, 1833 | Bluefin trevally | 6 | 6 | 117 | 31–66 |
Caranx papuensis Alleyne & MacLeay, 1877 | Brassy trevally | 5 | 2 | 88 | 12–41 |
Carcharhinidae | |||||
Carcharhinus melanopterus (Quoy & Gaimard, 1824) | Blacktip reef shark | 5 | 4 | 200 | 46–219 |
Chaetodontidae | |||||
Chaetodon auriga Forsskål, 1775 | Threadfin butterflyfish | 13 | 5 | 23 | 12–19 |
Chaetodon lunula (Lacepède, 1802) | Raccoon butterflyfish | 14 | 11 | 20 | 11–16 |
Chanidae | |||||
Chanos chanos (Forsskål, 1775) | Milkfish | 5 | 2 | 180 | 31–57 |
Gobiidae | |||||
Amblygobius phalaena (Valenciennes, 1837) | Whitebarred goby | 18 | 6 | 15 | 1.3–7 |
Asterropteryx semipunctata Rüppell, 1830 | Starry goby | 12 | 1 | 6 | 2–4 |
Gnatholepis anjerensis (Bleeker, 1851) | Eye-bar goby | 2 | 0 | 8 | 2–3 |
Istigobius decoratus (Herre, 1927) | Decorated goby | 5 | 0 | 13 | 7–11 |
Istigobius ornatus (Rüppell, 1830) | Ornate goby | 26 | 0 | 11 | 3–6 |
Istigobius rigilius (Herre, 1953) | Rigilius goby | 1 | 0 | 11 | 4 |
Oplopomus oplopomus (Valenciennes, 1837) | Spinecheek goby | 26 | 0 | 10 | 2–7 |
Psilogobius prolatus Watson & Lachner, 1985 | Longjaw shrimpgoby | 11 | 0 | 6 | 2–4 |
Valenciennea sexguttata (Valenciennes, 1837) | Sixspot goby | 14 | 1 | 14 | 2–9 |
Hemiramphidae | |||||
Hemiramphus depauperatus Lay & Bennett, 1839 | Tropical half-beak fish | 20 | 0 | 40 | 20–34 |
Kyphosidae | |||||
Kyphosus cinerascens (Forsskål, 1775) | Blue sea chub | 2 | 2 | 50 | 35–38 |
Lutjanidae | |||||
Lutjanus fulvus (Forster, 1801) | Blacktail snapper | 26 | 13 | 40 | 7–26 |
Lutjanus monostigma (Cuvier, 1828) | One spot snapper | 6 | 3 | 60 | 17–37 |
Mugilidae | |||||
Crenimugil crenilabis (Forsskål, 1775) | Fringelip mullet | 42 | 0 | 60 | 8–45 |
Ellochelon vaigiensis (Quoy & Gaimard, 1825) | Squaretail mullet | 54 | 7 | 63 | 3–32 |
Osteomugil engeli (Bleeker, 1858) | Kanda | 63 | 0 | 30 | 1–20 |
Mullidae | |||||
Mulloidichthys flavolineatus (Lacepède, 1801) | Yellowstripe goatfish | 52 | 6 | 43 | 8–37 |
Upeneus taeniopterus Cuvier, 1829 | Finstripe goatfish | 5 | 3 | 33 | 1–30 |
Muraenidae | |||||
Gymnothorax pictus (Ahl, 1789) | Paintspotted moray | 7 | 1 | 140 | 41–70 |
Ophichthidae | |||||
Myrichthys colubrinus (Boddaert, 1781) | Harlequin snake eel | 3 | 0 | 97 | 33–65 |
Pinguipedidae | |||||
Parapercis lata Randall & McCosker, 2002 | Y-barred sandperch | 13 | 0 | 21 | 2–3 |
Pomacentridae | |||||
Abudefduf septemfasciatus (Cuvier, 1830) | Banded sergeant | 12 | 1 | 23 | 14–20 |
Abudefduf sordidus (Forsskål, 1775) | Blackspot sergeant | 18 | 4 | 24 | 14–19 |
Chrysiptera glauca (Cuvier, 1830) | Grey demoiselle | 3 | 0 | 12 | 8–10 |
Stegastes nigricans (Lacepède, 1802) | Dusky farmerfish | 10 | 1 | 14 | 8–10 |
Serranidae | |||||
Epinephelus merra Bloch, 1793 | Honeycomb grouper | 2 | 0 | 32 | 13–24 |
Sphyraenidae | |||||
Sphyraena barracuda (Edwards, 1771) | Great barracuda | 2 | 0 | 200 | 65–76 |
Tetraodontidae | |||||
Arothron hispidus (Linnaeus, 1758) | White–spotted puffer | 15 | 7 | 50 | 17–49 |
Parasitic nematodes of fishes from the lagoon flats of Palmyra Atoll and their infection parameters; N = number of fish examined. *Larval forms.
Hosts | N | Infected hosts | Prevalence (%) | Mean intensity (±SD) | |
---|---|---|---|---|---|
Anisakidae | |||||
Pulchrascaris chiloscyllii | Carcharhinus melanopterus | 5 | 4 | 80 | 35 ± 26.5 |
Pulchrascaris sp.* | Acanthurus triostegus | 50 | 4 | 8 | 2.3 ± 1.9 |
Acanthurus xanthopterus | 20 | 3 | 15 | 1.3 ± 0.6 | |
Rhinecanthus aculeatus | 18 | 2 | 11.1 | 1 | |
Platybelone argalus | 2 | 1 | 50 | 10 | |
Carangoides ferdau | 5 | 2 | 40 | 42 ± 58 | |
Carangoides orthogrammus | 3 | 2 | 67 | 52.5 ± 72.8 | |
Caranx ignobilis | 4 | 4 | 100 | 71.3 ± 106.5 | |
Caranx melampygus | 6 | 6 | 100 | 53.7 ± 106.4 | |
Caranx papuensis | 5 | 2 | 40 | 8 ± 9.9 | |
Chaetodon auriga | 13 | 1 | 8 | 1 | |
Chanos chanos | 5 | 1 | 20 | 2 | |
Amblygobius phalaena | 18 | 6 | 33 | 7.2 ± 8.6 | |
Asterropteryx semipunctata | 12 | 1 | 8 | 3 | |
Valencienea sexguttata | 14 | 1 | 7 | 1 | |
Kyphosus cinerascens | 2 | 1 | 50 | 7 | |
Lutjanus fulvus | 26 | 12 | 46 | 5.2 ± 3.7 | |
Lutjanus monostigma | 6 | 3 | 50 | 4.7 ± 3.2 | |
Ellochelon vaigiensis | 54 | 4 | 7 | 1.5 ± 0.6 | |
Mulloidichthys flavolineatus | 52 | 5 | 10 | 1.4 ± 0.4 | |
Upeneus taeniopterus | 5 | 3 | 60 | 3.7 ± 1.5 | |
Gymnothorax pictus | 7 | 1 | 14 | 3 | |
Abudefduf septemfasciatus | 12 | 1 | 8 | 1 | |
Abudefduf sordidus | 18 | 1 | 6 | 1 | |
Stegastes nigricans | 10 | 1 | 10 | 1 | |
Hysterothylacium sp. type MD* | Acanthurus triostegus | 50 | 3 | 6 | 1.7 ± 0.6 |
Carangoides ferdau | 5 | 2 | 40 | 1.0 | |
Chaetodon lunula | 14 | 7 | 50 | 3.3 ± 1.6 | |
Chanos chanos | 5 | 1 | 20 | 6 | |
Kyphosus cinerascens | 2 | 1 | 50 | 2 | |
Abudefduf sordidus | 18 | 1 | 6 | 3 | |
Arothron hispidus | 15 | 3 | 20 | 7.0 ± 5.0 | |
Capillariidae | |||||
Capillariidae gen. sp. | Chaetodon lunula | 14 | 2 | 14 | 2.5 ± 0.7 |
Lutjanus fulvus | 26 | 1 | 4 | 1 | |
Ellochelon vaigiensis | 54 | 3 | 6 | 1.7 ± 0.6 | |
Cucullanidae | |||||
Cucullanus bourdini | Arothron hispidus | 15 | 7 | 47 | 6 ± 4.7 |
Cucullanus oceaniensis | Abudefduf sordidus | 18 | 2 | 11 | 1.5 ± 0.7 |
Cucullanus sp.* | Caranx ignobilis | 4 | 1 | 25 | 2 |
Cystidicolidae | |||||
Spinitectus (Paraspinitectus) palmyraensis sp. nov. | Albula glossodonta | 24 | 13 | 54 | 3.2 ± 4.0 |
Pseudascarophis sp. | Chaetodon auriga | 13 | 4 | 31 | 1 |
Chaetodon lunula | 14 | 2 | 14 | 3 ± 2.8 | |
Mulloidichthys flavolineatus | 52 | 1 | 2 | 1 | |
Philometridae | |||||
Philometra pellucida | Arothron hispidus | 15 | 6 | 40 | 20.8 ± 31.4 |
Male (1 mature specimen, measurements of one young specimen in parenthesis): elongate, relatively large nematodes, 68.01 (20.36) mm long, 767 (388) wide. Cuticular alae distinct. Lips small, greatly reduced, with tooth-like structures. Nerve ring located at first third of esophagus length, 503 (380); deirids posterior to level of nerve ring, 604, both from anterior body end. Excretory pore between base of subventral lips. Esophagus cylindrical, 2.96 (1.95) mm long, with large ventriculus at posterior end, 3.38 (2.12) mm long, and without ventricular appendage. Intestinal caecum anteriorly directed, somewhat larger than ventriculus, 3.57 (2.36) mm long. Spicules equal, similar, alate, 1.48 mm long; gubernaculum absent. Caudal papillae 51 pairs: 42 precloals pairs (some subventral and other sublateral), 4 adcloacal subventral pairs, 5 postcloacal (including phasmids). One single, ventral papilla on the anterior cloacal lip. Three cuticular plates immediately posterior to cloacal opening, with serrate edges. Tail conical, short, 298 (182) long.
Fourth-stage larva (1 specimen): Length of body 11.56 mm long, 233 wide. Esophagus, ventriculus and intestinal caecum 1.25, 0.93, 1.08 mm, respectively. Nerve ring 275, deirids 355, both from the cephalic end. Tail 126 long.
Carcharhinus melanopterus (Quoy & Gaimard) (Carcharhinidae).
Intestine.
80 and 35 ± 26.5 (n = 5).
CHCM no. 619 (voucher) (1 vial, 1 specimen ♀).
These specimens are morphologically similar to P. chiloscyllii (reported as Terranova chiloscyllii), originally found in Chiloscyllium punctatum Müller & Henle and Mustelus antarcticus Günther (reported as Emissola antarctica) from the Central Queensland coast (
Third-stage larva (12 specimens): relatively long nematodes 6.99–12.42 mm long and 172–452 wide, whitish with lateral cuticular alae. Lips weakly developed and bearing a larval, ventral tooth, 5–12 long. Nerve ring encircling esophagus in its anterior third, 173–302 from anterior body end. Deirids slightly posterior to nerve ring, 225–273 from cephalic end. Excretory pore at base of subventral lip. Esophagus relatively long, 636–1,414 with elongated ventriculus at posterior end, 388–1,371 long. Intestinal caecum anteriorly directed and somewhat larger than ventriculus, 389–1,384 long. Tail conical, 99–179 long, without ornamentations. Some specimens with a single papilla at 1.65–5.78 mm from posterior end of body.
Acanthurus sordidus, A. triostegus, Acanthurus xanthopterus Valenciennes (Acanthuridae), Rhinecanthus aculeatus (Linnaeus) (Balistidae), Platybelone argalus argalus (Lesueur) (Belonidae), C. ferdau, Carangoides orthogrammus (Jordan & Gilbert), Caranx ignobilis (Forsskål), Caranx melampygus Cuvier, Caranx papuensis Alleyne & MacLeay (all Carangidae), Amblygobius phalaena (Valenciennes), Asterropteryx semipunctata Rüppell, Valenciennea sexguttata (Valenciennes) (all Gobiidae), M. flavolineatus, Upeneus taeniopterus Cuvier (Mullidae), Gymnothorax pictus (Ahl) (Muraenidae), L. fulvus, Lutjanus monostigma (Cuvier) (Lutjanidae), Abudefduf septemfasciatus (Cuvier), Stegastes nigricans (Lacepède) (Pomacentridae), C. auriga, C. chanos, K. cinerascens, E. vaigiensis.
Mesenteries.
5.6 and 1 (n = 18) to A. sordidus, 8 and 2.3 ± 1.9 (n = 50) to A. triostegus, 15 and 1.3 ± 0.6 (n = 20) to A. xanthopterus, 11.1 and 1 (n = 18) to R. aculeatus, 50 and 10 (n = 2) to P. argalus, 40 and 42 ± 58 (n = 5) to C. ferdau, 66.7 and 52.5 ± 72.8 (n = 2) to C. orthogrammus, 100 and 71.3 ± 106.5 (n = 4) to C. ignobilis, 100 and 53.7 ± 106.4 (n = 6) to C. melampygus, 40 and 8 ± 9.9 (n = 5) to C. papuensis, 33.3 and 7.2 ± 8.6 (n = 18) to A. phalaena, 8.3 and 3 (n = 12) to A. semipunctata, 7.1 and 1 (n = 14) to V. sexguttata, 9.6 and 1.4 ± 0.4 (n = 52) to M. flavolineatus, 60 and 3.7 ± 1.5 (n = 5) to U. taeniopterus, 14.3 and 3 (n = 7) to G. pictus, 46.2 and 5.2 ± 3.7 (n = 26) to L. fulvus, 50 and 4.7 ± 3.2 (n = 6) to L. monostigma, 8.3 and 1 (n = 12) to A. septemfasciatus, 10 and 1 (n = 10) to S. nigricans, 7.7 and 1 (n = 13) to C. auriga, 20 and 2 (n = 5) to C. chanos, 50 and 7 (n = 2) to K. cinerascens, 7.4 and 1.5 ± 0.6 (n = 54) to E. vaigiensis.
CHCM no. 620 (voucher) (1 vial, 1 specimen ♀) (from A. triostegus), CHCM no. 621 (voucher) (1 vial, 2 specimens ♂ ♀) (from C. auriga), CHCM no. 622 (voucher) (1 vial, 1 specimen ♀) (from K. cinerascens), CHCM no. 623 (voucher) (1 vial, 1 specimen ♀) (from L. fulvus).
These larvae belong to the genus Pulchrascaris because of the position of the excretory pore between the subventral lips, absence of ventricular appendage, elongate esophagus, relatively large ventriculus, and intestinal caecum anteriorly directed and somewhat larger than ventriculus.
Third-stage larva (5 specimens): medium-sized nematodes, 3.00–8.64 mm long, 100–267 wide. Cuticular lateral alae extending along whole length of worm. Poorly developed lips, small, 18 long and 19 wide. Esophagus 270–680 long, with almost spherical ventriculus at distal part, 59–75 long and 57–87 wide. Ventricular appendage 481–595 long; intestinal caecum small, anteriorly directed, 67–274 long. Ratio for length of ventricular appendage and intestinal caecum 1: 2.10–7.73. Nerve ring at 116–279 from anterior end of body. Excretory pore slightly anterior to nerve ring, 137–198 from cephalic end. Deirids 395 from anterior end (observed in only 1 specimen). Tail conical, 121–227 long, with small spine-like mucron at tip.
Acanthurus triostegus, C. ferdau, C. lunula, C. chanos, K. cinerascens, A. sordidus, and A. hispidus.
Mesenteries and liver.
6 and 1.7 ± 0.6 (n = 50) to A. triostegus, 40 and 1.0 ± 0.0 (n = 5) to C. ferdau, 50 and 3.3 ± 1.6 (n = 14) to C. lunula, 20 and 6 (n = 5) to C. chanos and 50 and 2 (n = 2) to K. cinerascens, 5.6 and 3 (n = 18) to A. sordidus, 20 and 7.0 ± 5.0 (n = 15) to A. hispidus.
CHCM no. 624 (voucher) (1 vial, 1 specimen ♀) (from Chaetodon lunula), CHCM no. 625 (voucher) (1 vial, 2 specimens ♂ ♀) (from K. cinerascens).
Because of the presence of a small intestinal caecum, long ventricular appendage, rounded ventriculus and small mucron on the tail tip, these larvae are morphologically similar to those described by
Gravid female (1 damaged specimen, measurements of 1 young female in parentheses): long, thin and slender nematodes, 9.42 (8.80) mm long and 26 (37) wide. Muscular esophagus – (335). Stichosome formed by 4–6 (5) stichocytes. Eggs with polar plugs, thick-walled, 49–55 × 20–24 (–). Tail very short, 7 (6) long.
Chaetodon lunula, L. fulvus, and E. vaigiensis.
Stomach.
14.3 and 2.5 ± 0.7 (n = 14) to C. lunula, 3.8 and 1 (n = 26) to L. fulvus, 5.6 and 1.7 ± 0.6 (n = 54) to E. vaigiensis.
CHCM no. 626 (voucher) (1 vial, 1 specimen ♀) (from Chaetodon lunula), CHCM no. 627 (voucher) (1 vial, 2 specimens ♂ ♀) (from L. fulvus).
Specimens were damaged, but it was possible to observe the most important features to allocate them to the family Capillariidae, such as esophagus divided in muscular and glandular parts (stichosome), eggs with polar plugs, and the general shape of body. Since males are unknown, it is impossible to determine their generic or specific identity. This is the first capillariid nematode reported in C. ignobilis and the second for the family Carangidae in the southwestern Pacific Ocean, which was recorded in Carangoides oblongus (Cuvier) (Carangidae) off New Caledonia (
Male (5 specimens): medium-sized nematodes, 8.11–12.87 mm long, 223–413 wide. Esophagus 777–1,003 long and 126–240 wide at its posterior end. Anterior part of esophagus forming pseudocapsule (esophastome) 228–275 long and 129–185 wide. Nerve ring surrounding esophagus at its first third, 267–368 from anterior body end. Excretory pore beyond posterior end of esophagus, cervical papillae on distal end of esophagus or slightly posterior to it, 969–1,215 and 671–937, respectively, from cephalic end. Well-developed precloacal pseudosucker present, its distal part at 626–942 from posterior body end. Cloacal opening elevated. Eleven pairs of caudal papillae: 3 subventral, pedunculate precloacal pairs (first pair sometimes anterior to sucker and sometimes over anterior border), 4 adcloacal pairs (3 subventral, 1 lateral), 4 postcloacal pairs, including phasmids (1 subdorsal, 1 lateral, 2 subventral). One single papilla on anterior cloacal lip. Spicules similar, equal, alate, 982–1,543 with supporting structures along almost their whole length. Gubernaculum well-sclerotized, 116–140 long. Right and left postdeirids 3.94–6.37 and 1.92–3.27 mm, respectively, from posterior end of body. Tail conical 187–236 long, with pointed tip.
Gravid females (5 specimens, measurements of 1 young female in parentheses): body length 13.72–15.90 (5.23) mm long and 472–500 (220) wide. Esophagus 999–1,087 (600) long, 227–263 (106) wide at its posterior end. Esophastome 250–311 (197) long, 169–201 (129) wide. Nerve ring, excretory pore and deirids 318–367 (250), 1,150–1,377 (902), 805–971 (614), respectively, from anterior end of body. Vulva postequatorial 7.97–9.35 (3.30) from anterior end of body, with somewhat elevated lips and posteriorly directed muscular vagina. Eggs oval, 53–71 × 34–46 (–) in size, non-larvated. Tail conical, 294–385 (204) long.
Arothron hispidus.
Intestine.
46.7 and 6 ± 4.7 (n = 15).
CHCM no. 628 (voucher) (1 vial, 1 specimen ♀).
The measurements of these nematodes are similar to those of C. bourdini, a species described from lutjanid fishes off New Caledonia (
Male (1 specimen): medium-sized nematodes, whitish. Body length 6.22 mm, 183 wide. Muscular esophagus 678 long and 112 wide at its posterior part. Anterior end of esophagus forming a pseudobuccal capsule (esophastome), 214 long and 153 wide. Nerve ring slightly posterior to esophastome, 275 from anterior end of body. Deirids anterior to posterior end of esophagus, excretory pore posterior to it, at 609 and 797, respectively, from cephalic end. Eleven pairs of caudal papillae (including phasmids): 3 subventral precloacal pairs, 4 adcloacal pairs (3 subventral, 1 lateral), 4 postcloacal pairs (3 subventral, 1 lateral). A single, ventral papilla on the anterior cloacal lip. Spicules equal, similar, alate, 374 long. Gubernaculum well sclerotized, 112 long. Ventral precloacal sucker well developed, posterior margin at 690 from posterior end of body. Postdeirids 1.71 mm from tail tip. Tail conical with pointed tip, 112 long.
Abudefduf sordidus.
Intestine.
11.1 and 1.5 ± 0.7 (n = 18).
CHCM no. 629 (voucher) (1 vial, 1 specimen ♀).
This single male is morphologically similar to C. bourdini and C. oceaniensis, two species described from lutjanids off New Caledonia and Anguilla marmorata Quoy & Gaimard (Anguillidae) in Polynesia and Melanesia (
Third-stage larva (2 specimens): small nematodes, 1.45–1.53 long, 50– 51 wide. Esophagus 333–352 long, 38–39 wide at its posterior part. Esophastome 60–65 long and 44–50 wide. Nerve ring 139–151, excretory pore 374–413 and deirids 262. Excretory pore posterior to distal end of esophagus, deirids on its posterior end of esophagus or slightly anterior to it. Tail elongate, 105–113 long, with pointed tip.
Caranx ignobilis
Intestine.
25 and 2 (n = 4).
CHCM no. 630 (voucher) (1 vial, 1 specimen ♀).
These were two very small and poorly developed cucullanid larvae and it was not possible to identify them to species. Perhaps, they represent new infections, or this fish acts as paratenic host. These are the first cucullanid nematodes reported from C. ignobilis and the family Carangidae in the Indo-Pacific Ocean.
Gravid female (1 specimen): large, whitish nematode, 18.20 mm long, 158 wide. Anterior end rounded with two large rounded pseudolabia. Vestibule relatively short, 159 long, with anterior prostom and posterior part forming a transverse ring on anterior end of esophagus. Muscular esophagus short, narrow, 258 long; glandular part broader, 5 times longer than muscular one, 1.52 mm long. Nerve ring encircling muscular esophagus at its first third, 206 from anterior body end. Deirids small, bifurcated, situated between second and third thirds of vestibule length, 109 from anterior end of body. Excretory pore posterior to level of nerve ring, 220 from cephalic end. Vagina muscular directed posteriorly. Vulva pre-equatorial, 8.74 mm from anterior end of body, with not elevated lips. Fully developed eggs, thick-walled, larvated, without filaments, 31–36 × 24–29. Tail elongate, 239 long, with rounded tip.
Chaetodon auriga, C. lunula, and M. flavolineatus.
Stomach.
30.8 and 1 (n = 13) to C. auriga, 14.3 and 3 ± 2.8 (n = 14) to C. lunula, 1.9 and 1 (n = 52) M. flavolineatus.
CHCM no. 631 (voucher) (1 vial, 1 specimen ♀) (from C. auriga), CHCM no. 632 (voucher) (1 vial, 2 specimens ♂ ♀) (from M. flavolineatus).
The presence of rounded pseudolabia, bifurcated deirids, and elongate tail with rounded tip, make this female similar to those of the genus Pseudoascarophis. Nematodes belonging to this genus were originally reported in K. cinerascens from off Japan and later found in Parupeneus chrysopleuron (Temminck & Schlegel) (Mullidae), Genypterus chilensis (Guichenot) (Ophidiidae), Kyphosus sectatrix (Linnaeus) (Kyphosidae) from China, Chile, Brazil, respectively (
General
: medium-sized nematodes with transverse rings of markedly long, posteriorly directed spines. First ring situated at level of base of prostom (Figs
Spinitectus (Paraspinitectus) palmyraensis sp. nov. A anterior extremity of male, lateral view B, C cephalic end, apical and lateral views, respectively D region of vulva, lateral view E spines from different parts of body F anterior end, showing incomplete rows of spines G region of mid-body, showing missing spines H tail of female, ventral view I small spicule, lateral view J posterior end of male, lateral view.
Spinitectus (Paraspinitectus) palmyraensis sp. nov. scanning electron micrographs. A, B anterior end of gravid female, apical and subapical views, respectively C detail of mouth, apical view D anterior end body, lateral view (arrow indicates deirids) E region of excretory pore, ventral view (arrow indicates the excretory pore) F deirids. Abbreviations: b submedian papilla, l labium, p pseudolabium, s sublabium.
Male (4 specimens, measurements of holotype in parenthesis): length of body 3.90–5.50 (4.92) mm, maximum width 89–115 (103). First cuticular ring 31–33 (33) from anterior extremity, armed with 11–14 (12) spines, 10–14 (12) long. Larger spines 22–23 (22–23) are at the level of the glandular esophagus. Vestibule including prostom 188–213 (188) long; prostom 21–28 (28) long and 7–9 (8) wide. Muscular esophagus 251–278 (261) long; glandular esophagus 0.82–1.55 (0.93) mm long, 32–41 (33) wide; length ratio of both parts of esophagus 1:3.2–4.2 (3.5). Entire esophagus and vestibule represent 28–31 (29)% of whole body length. Nerve ring and excretory pore 212–223 (223) and 233–254 (254), respectively, from anterior extremity. Deirids 30–32 (32) from anterior end of body. Posterior end of body ventrally curved, provided with well-developed caudal alae reaching posteriorly to end of tail (Figs
Spinitectus (Paraspinitectus) palmyraensis sp. nov. scanning electron micrographs. A transition zone of spination, lateral view B larger spines with pore-like on bases C posterior end of male showing area rugosa, sublateral view D tail of male, ventral view E region of cloaca, ventral view (asterisks indicate precloacal papillae) F tail tip of male, ventral view G posterior end female, lateral view (arrow indicates phasmid) H detail of tail tip.
Gravid female (4 specimens; measurements of allotype in parentheses): body length 5.89–7.14 (6.26) mm, maximum width 129–143 (143). First cuticular ring 27–31 (27) from anterior extremity, 11–14 spines 12–15 (12) long. Larger spines 12–14 (12–14) at the level of the glandular esophagus. Vestibule including prostom 183–211 (183) long; prostom 23–28 (28) long and 7–9 (7) wide. Muscular esophagus 273–300 (289) long; glandular esophagus 0.908–1.165 (1.165) mm long, 38–46 (46) wide; length ratio of both parts of esophagus 1: 3.3–4.1 (4). Entire esophagus and vestibule with prostome represents 23–26 (26)% of whole body length. Nerve ring and excretory pore 206–231 (206) and 219–266 (206), respectively, from anterior extremity. Deirids 26–30 (26) from anterior end. Vulva with slightly elevated lips, postequatorial, situated at 4.24–4.82 (4.58) mm from anterior extremity, representing 67–73 (73)% of body length. Vagina muscular, directed posteriorly from vulva (Fig.
The specific name of this nematode relates to the collection locality (Palmyra Atoll).
Albula glossodonta (Forsskål) (Albulidae).
Intestine.
Palmyra Atoll, Eastern Indo-Pacific Ocean.
54.2 and 3.2 ± 4.0 (n = 24).
Holotype and paratype (in SEM stub) specimens in the Helminthological Collection of the Institute of Parasitology, Academy of Sciences of the Czech Republic, Ceske Budejovice (no. N-1073) and CHCM no. 633 (allotype) (1 vial, 1 specimen ♀).
According to
Due to the presence of markedly reduced pseudolabia in the oral opening and a body covered by spinose rings, the nematodes herein described were assigned to the subgenus Paraspinitectus, as diagnosed by
Interestingly even though the three species within Paraspinitectus occur in closely related hosts, morphological differences are evident among species of Spinitectus parasitizing albulid fishes around the world. Potentially, ecological differences of their hosts or habitats are substantial enough to select for this interspecific variability.
Morphological features as reduced pseudolabia, small triangular sublabia in the oral opening, trifurcated deirids (probably also present in Spinitectus (P.) sp.), and spinose rings with two different patterns of arrangement are common to the three known forms assigned to the subgenus. These characteristics support the validity of the subgenus Paraspinitectus and highlight the need for detailed SEM examination of cystidicolid specimens to determine the substantial intraspecific differences when comparing among species.
Within the Cystidicolidae there is a recently created genus, Ascarophisnema Moravec & Justine, 2010 with remarkable similarities with the new species. Similarities between the Ascarophisnema and Spinitectus include trifurcated deirids (only reported in these two genera), the structure of the oral opening, and the number and distribution of caudal papillae. Although the presence of spinose rings in Spinitectus clearly set it apart from Ascarophisnema. Probably, both genera are closely related but a phylogenetic analysis using molecular and morphological data is needed to clarify this situation.
This is the second nominal species reported within the subgenus Paraspinitectus and represents a new geographical record (southern Pacific region), since the previous report was a generically identified female from the same host species.
Gravid female (3 specimens, measurements of 3 subgravid females in parentheses): large, yellowish nematodes, 111.42–140.70 (37.84–48.64) mm long, 0.94–3.29 (0.336–0.649) mm wide, with smooth cuticle and both ends rounded. Esophagus with anterior bulbous inflation, 220–267 (147–181) long and 163–182 (130–162) wide, with spacious lumen. Esophagus 1.59–2.06 (1.41–1.50) mm long, with dorsal esophageal gland not well demarcated, extended anteriorly to level of nerve ring. Esophageal gland with cell nucleus located at mid-length, at 0.915–1.07 (–) mm from anterior extremity. Small ventriculus 80–111 (50–80) long and 79–142 (75–85) wide, opening into intestine through valve. Nerve ring encircling esophagus just posterior to its anterior bulb, 279–407 (239–246) from anterior body end. Deirids and excretory pore not visible. Intestine brownish, straight and almost reaching the posterior end of body, forming ligament 325–690 (547–594) long, attached to the body wall near the caudal end. Ovaries extending near both ends of body. Uterus filled with larval mass (in gravid females) and developing embryos and eggs (in subgravid females). Larvae from uterus 345–492 long, with elongated tail. Posterior end of body rounded.
Arothron hispidus.
Body cavity.
40 and 20.8 ± 31.4 (n = 15).
CHCM no. 634 (voucher) (1 vial, 1 specimen ♀).
Due to the presence of the anterior inflation of the esophagus, weakly demarcated esophageal gland, its occurrence in the body cavity of a congeneric fish host (A. hispidus) and close geographical region (Southeastern Pacific Ocean), these females were identified as P. pellucida. Gravid females showed similar morphometric features than those reported by
The present study is the first detailed survey of the diversity and ecological attributes of the parasitic nematodes infecting fishes at Palmyra Atoll. Consistent with observations of the monogenean and parasitic copepod fauna of Palmyra Atoll fishes (Vidal-Martinez et al. 2017;
At a broad geographical scale, the most likely hypothesis to account for the paucity of parasitic nematodes at Palmyra Atoll is its geographical remoteness. Indeed, Palmyra Atoll apparently would show a pattern similar to that suggested by the island biogreography theory, where the large distance from the presumed centre of origin of Indo-West Pacific fishes and their parasites (the Austro-Malayan-Philippine region) would result in a low number of both fish and nematode parasite species. Further support for this explanation is the low species richness of fishes of the Line Islands, including Palmyra Atoll (
In our samples from the lagoonal flats of Palmyra Atoll, of the 10 nematode species recovered, seven were in the adult stage and three were larvae (Table
The most likely explanation for the numerical dominance of the larval stages of nematodes is the lack of fishery activity at Palmyra Atoll and the substantial biomass of large, piscivorous sharks and ray-finned fishes (
The life cycle of the members of the Pulchrascaris genus is unknown but being an anisakid nematode, it should include small marine crustaceans as first intermediate hosts, fishes as second intermediate hosts and elasmobranch fishes as definitive hosts (
Hysterothylacium sp. larval stages were parasitizing seven fish species from the intertidal lagoon at Palmyra Atoll (Table
Pseudascarophis sp. was also an adult nematode infecting three fish species (Table
The life cycle of the unidentified nematodes of the family Capillaridae is also unknown. However, based on the extant literature on the life cycles of the members of this family, it is likely that they use oligochaetes as first intermediate hosts (
There were three species of the genus Cucullanus infecting fishes from the sand flats of Palmyra Atoll (Table
The life cycle of Philometra pellucida (Table
In conclusion, despite the relatively low species richness of parasitic nematodes in the lagoonal flats at Palmyra Atoll, which is due to its remotedness, there were very interesting patterns at the local level, especially those related with the numerical dominance of larval stages of nematodes. Apparently, the lack of fishing at the atoll since 2001 (https://www.fws.gov/refuge/palmyra_atoll/) and its selective removal of definitive hosts such as sharks and piscivorous bony fishes applied is the most likely explanation for the high number of larval nematodes using fishes as second intermediate hosts.
We thank to the staff of the Laboratory of Electron Microscopy, Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, České Budějovice for technical assistance and Blanka Škoriková from the same institution for help in preparing drawings and plates. This study was partially supported by the Czech Science Foundation (Project no. P505/12/G112). This work was supported by the National Council of Science and Technology of Mexico – Mexican Ministry of Energy – Hydrocarbon Trust, project (201441). This is a contribution of the Gulf of Mexico Research Consortium (CIGoM). We acknowledge and thank the Palmyra Atoll National Wildlife Refuge, US Fish and Wildlife Service, Department of the Interior, the Nature Conservancy, and the United States Geological Survey for their support. We deeply thank the Nature Conservancy staff and US Fish and Wildlife staff who were friendly and helpful. We are particularly indebted to Franklin Viola, Amanda Meyer, Brad Kintz, Aaron Kierzek, Jan Eber, Anthony Wilson, Lynette Williams, Kathy Wilson, and Clara Viva-Rodríguez. We also thank Gareth Williams and Ingrid Knapp for sharing their field knowledge. This work also benefitted from a grant from the Marisla Foundation and a US National Science Foundation Grant (DEB-0224565). Any use of trade, product, or firm names in this publication is for descriptive purposes only and does not imply endorsement by the US Government.