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. 2019 Mar 27;833:85–106. doi: 10.3897/zookeys.833.30835

Parasitic copepods (Crustacea, Hexanauplia) on fishes from the lagoon flats of Palmyra Atoll, Central Pacific

Lilia C Soler-Jiménez 1, F Neptalí Morales-Serna 2, Ma Leopoldina Aguirre-Macedo 1,3, John P McLaughlin 3, Alejandra G Jaramillo 3, Jenny C Shaw 3, Anna K James 3, Ryan F Hechinger 3,4, Armand M Kuris 3, Kevin D Lafferty 3,5, Victor M Vidal-Martínez 1,3,✉
PMCID: PMC6477860  PMID: 31048953

Abstract Abstract

We surveyed copepods parasitic on the fishes at Palmyra, a remote atoll in the Central Indo-Pacific faunal region. In total, we collected 849 individual fish, representing 44 species, from the intertidal lagoon flats at Palmyra and recovered 17 parasitic copepod species. The parasitic copepods were: Orbitacolaxwilliamsi on Mulloidichthysflavolineatus; Anuretesserratus on Acanthurusxanthopterus; Caligusconfusus on Carangoidesferdau, Carangoidesorthogrammus, Caranxignobilis, Caranxmelampygus, and Caranxpapuensis; Caliguskapuhili on Chaetodonauriga and Chaetodonlunula; Caliguslaticaudus on Rhinecanthusaculeatus, Pseudobalistesflavimarginatus, M.flavolineatus, Upeneustaeniopterus, Chrysipteraglauca, and Epinephalusmerra; Caligusmutabilis on Lutjanusfulvus and Lutjanusmonostigma; Caligusrandalli on C.ignobilis; Caligus sp. on L.fulvus; Caritusserratus on Chanoschanos; Lepeophtheiruslewisi on A.xanthopterus; Lepeophtheirusuluus on C.ignobilis; Dissonussimilis on Arothronhispidus; Nemesis sp. on Carcharhinusmelanopterus; Hatschekialongiabdominalis on A.hispidus; Hatschekiabicaudata on Chaetodonauriga and Chaetodonlunula; Kroyerialongicauda on C.melanopterus and Lernanthropus sp. on Kyphosuscinerascens. All copepod species reported here have been previously reported from the Indo-Pacific but represent new geographical records for Palmyra, demonstrating large-scale parasite dispersion strategies.

Keywords: Parasitic copepods, fish, geographical isolation, islands, Indo-Pacific, atoll

Introduction

Although there have been several surveys of copepods parasitic on Indo-Pacific fishes, including the Great Barrier Reef (Australia), New Caledonia, New Guinea, India, Taiwan and the Hawaiian Islands (Yamaguti 1963, Kabata 1966, Lewis 1968, Pillai 1968, 1985, Cressey and Boyle 1973, Cressey and Cressey 1979, Ho and Dojiri 1977, Deets and Dojiri 1990, Ogawa 1991, Ho and Lin 2004, Boxshall and Justine 2005, Tang and Kalman 2005, Palm and Bray 2014), the East Indo-Pacific has received little sampling effort. Lafferty et al. (2008) compared parasite communities, including parasitic copepods, at two coral atolls in the Line Islands chain of the central Pacific (Kiritimati Island and Palmyra Atoll). However, their analysis was limited to broad patterns of richness and abundance of morphospecies, conservatively grouped into broad taxonomic categories. Palm and Bray (2014) listed parasites from Hawaiian fishes, reporting 64 copepod species (13 families) from 298 identified fish species.

Palmyra Atoll is one of the northern Line Islands located in the Indo-Pacific (IP) marine ecoregion (Spalding et al. 2007), 1680 km SSW of Hawaii. It is presently a marine protected area and has not supported regular human settlement since World War II. Palmyra Atoll has a relatively long history with little to no exploitation (DeMartini et al. 2008, Sandin et al. 2008). All fishing has been prohibited at Palmyra since it became a US National Wildlife Refuge in 2000 (before that, its remoteness kept fishing pressure low).

As part of a larger project assembling food webs at Palmyra Atoll, we have been cataloging the parasites found in the system. This paper is a companion to two others examining different fish parasite taxa (Vidal-Martínez et al. 2012, 2017). We recovered a considerable number of parasitic copepods from 44 fish species. As such, our tabulation adds to the few published species descriptions or host records from the Central Indo-Pacific region (Cressey and Boyle 1973, 1979, Cressey 1977, Ho and Lin 2004, Palm and Bray 2014), with an emphasis on describing diversity of the copepod supracommunity (Bush et al. 1997) at this site. The goal of this study is two-fold. First, we list the copepod species recovered, and note, for each, taxonomic issues and report their prevalence, mean intensity and host species. Second, we then discuss this diversity survey with respect to previously published records for the region.

Material and methods

We collected fish by seine, spear, and hook and line from the intertidal sand flats bordering the lagoon of Palmyra Atoll between October 2009 and July 2012. To avoid loss or mixing of parasites among fishes, immediately after capture, we placed fish in individual plastic bags with lagoon water and transported them to the laboratory facility of the Palmyra Atoll Research Consortium (PARC). We examined only freshly killed fish (and the bag water). Observations were under a stereomicroscope. Skin and fins of each host were carefully examined. The gill arches were removed and examined under a stereomicroscope. The copepods obtained were counted, preliminarily identified, fixed in 95 % EtOH, labelled and stored in vials for later evaluation. Then, in the Laboratory of Aquatic Pathology of CINVESTAV-Mérida, specimens were mounted and cleared with lactophenol to identify species based on morphology using an Olympus BX-53 microscope (Olympus Corporation, Shinjuku, Tokyo, Japan). Prevalence and mean intensity concepts were applied following Bush et al. (1997). Synonyms for each host species and copepod species were obtained from FishBase (Froese and Pauly 2018) and World of Copepods (Walter and Boxshall 2018), respectively. Voucher specimens were deposited in the United States National Parasite Collection, Washington, DC (USNPC), and the Helminthological Collection of the Laboratory of Parasitology, at the Centre for Research and Advanced Studies, National Polytechnic Institute, Mérida, Yucatán, México (CHCM).

Results

Copepods of fishes from Palmyra lagoon flats

During this study, 849 individual fish from 44 species were collected. Fourteen of the 44 fish species examined were parasitized by at least one parasitic copepod species. Caranxignobilis (Forsskål) was host to three copepod species, the most of any fish. Acanthurusxanthopterus Valenciennes, Carcharhinusmelanopterus (Quoy & Gaimard), Chaetodonauriga Forsskål, Chaetodonlunula (Lacépède), Lutjanusfulvus (Forster), Mulloidichthysflavolineatus (Lacépède) and Arothronhispidus (Linnaeus) served as host for two copepod species. All other infected species hosted a single copepod species. Thirty fish species were found free of any copepod parasite (Table 1). Ten of the 17 copepod species recovered belong to the Caligidae family (Table 2).

Table 1.

Fish species examined from the lagoon flats from 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
Acanthurustriostegus (Linnaeus, 1758) Convict surgeonfish 50 0 27 10–18
Acanthurusxanthopterus Valenciennes, 1835 Yellowfin surgeonfish 20 2 70 20–40
Albulidae
Albulaglossodonta (Forsskål, 1775) Roundjaw bonefish 24 0 90 37–58
Apogonidae
Cheilodipterusquinquelineatus Cuvier, 1828 Five-lined cardinalfish 5 0 13 5–6
Balistidae
Pseudobalistesflavimarginatus (Rüppell, 1829) Yellowmargin triggerfish 4 0 60 17–53
Rhinecanthusaculeatus (Linnaeus, 1758) Blackbar triggerfish 18 0 30 8–24
Belonidae
Platybeloneargalus (Lesueur, 1821) Keeltail needlefish 2 0 50 9–36
Carangidae
Carangoidesferdau (Forsskål, 1775) Blue trevally 5 0 75 33–38
Carangoidesorthogrammus (Jordan & Gilbert, 1882) Island trevally 3 0 75 25–35
Caranxignobilis (Forsskål, 1775) Giant trevally 4 3 170 56–79
Caranxmelampygus Cuvier, 1833 Bluefin trevally 6 2 117 31–66
Caranxpapuensis Alleyne & MacLeay, 1877 Brassy trevally 5 2 88 12–41
Carcharhinidae
Carcharhinusmelanopterus (Quoy & Gaimard, 1824) Blacktip reef shark 5 3 200 46–219
Chaetodontidae
Chaetodonauriga Forsskål, 1775 Threadfin butterflyfish 13 4 23 12–19
Chaetodonlunula (Lacepède, 1802) Raccoon butterflyfish 14 6 20 11–16
Chanidae
Chanoschanos (Forsskål, 1775) Milkfish 5 1 180 31–57
Gobiidae
Amblygobiusphalaena (Valenciennes, 1837) Whitebarred goby 18 0 15 1.3–7
Asterropteryxsemipunctata Rüppell, 1830 Starry goby 12 0 6 2–4
Gnatholepisanjerensis (Bleeker, 1851) Eye-bar goby 2 0 8 2–3
Istigobiusdecoratus (Herre, 1927) Decorated goby 5 0 13 7–11
Istigobiusornatus (Rüppell, 1830) Ornate goby 26 0 11 3–6
Istigobiusrigilius (Herre, 1953) Rigilius goby 1 0 11 4
Oplopomusoplopomus (Valenciennes, 1837) Spinecheek goby 26 0 10 2–7
Psilogobiusprolatus Watson & Lachner, 1985 Longjaw shrimpgoby 11 0 6 2–4
Valencienneasexguttata (Valenciennes, 1837) Sixspot goby 14 0 14 2–9
Hemiramphidae
Hemiramphusdepauperatus Lay & Bennett, 1839 Tropical half-beak fish 20 0 40 20–34
Kiphosidae
Kyphosuscinerascens (Forsskål, 1775) Blue sea chub 2 1 50 35–38
Lutjanidae
Lutjanusfulvus (Forster, 1801) Blacktail snapper 26 5 40 7–26
Lutjanusmonostigma (Cuvier, 1828) One spot snapper 6 1 60 17–37
Mugilidae
Crenimugilcrenilabis (Forsskål, 1775) Fringelip mullet 42 0 60 8–45
Lizavaigiensis (Quoy & Gaimard, 1825) Squaretail mullet 54 0 63 3–32
Valamugilengeli (Bleeker, 1858) Kanda 63 0 30 1–20
Mullidae
Mulloidichthysflavolineatus (Lacepède, 1801) Yellowstripe goatfish 52 8 43 8–37
Upeneustaeniopterus Cuvier, 1829 Finstripe goatfish 5 3 33 1–30
Muraenidae
Gymnothoraxpictus (Ahl, 1789) Paintspotted moray 7 0 140 41–70
Ophichthidae
Myrichthyscolubrinus (Boddaert, 1781) Harlequin snake eel 3 0 97 33–65
Pinguipedidae
Parapercislata Randall & McCosker, 2002 Y-Barred Sandperch 13 0 21 2–3
Pomacentridae
Abudefdufseptemfasciatus (Cuvier, 1830) Banded sergeant 12 0 23 14–20
Abudefdufsordidus (Forsskål, 1775) Blackspot sergeant 18 0 24 14–19
Chrysipteraglauca (Cuvier, 1830) Grey demoiselle 3 0 12 8–10
Stegastesnigricans (Lacepède, 1802) Dusky farmerfish 10 0 14 8–10
Serranidae
Epinephelusmerra Bloch, 1793 Honeycomb grouper 2 0 32 13–24
Sphyraenidae
Sphyraenabarracuda (Edwards, 1771) Great barracuda 2 0 200 65–76
Tetraodontidae
Arothronhispidus (Linnaeus, 1758) White-spotted puffer 15 9 50 17–49
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Table 2.

Parasitic copepods of fishes from the lagoon flats of Palmyra Atoll; N = number of fish examined. The authorities for parasites were included in the text.

Copepod species Hosts N Infected hosts Prevalence (%) Mean intensity (± SD)
Bomolochidae
Orbitacolax williamsi Mulloidichthys flavolineatus 52 1 1.9 1
Caligidae
Anuretes serratus Acanthurus xanthopterus 20 1 5 6
Caligus confusus Carangoides ferdau 5 2 40 2 ± 0.0
Carangoides orthogrammus 3 1 33.3 6
Caranx ignobilis 4 3 75 12.7 ± 12.2
Caranx melampygus 6 2 40 4 ± 0.0
Caranx papuensis 5 2 33.3 2 ± 0.0
Caligus kapuhili Chaetodon auriga 13 1 7.7 8
Chaetodon lunula 14 4 28.6 2.5 ± 1.7
Caligus laticaudus Rhinecanthus aculeatus 18 5.6 1
Pseudobalistes flavimarginatus 4 2 50 21 ± 26.9
Mulloidichthys flavolineatus 52 7 13.5 1.5 ± 0.5
Upeneus taeniopterus 5 3 60 2.7 ± 2.1
Chrysiptera glauca 3 1 3.33 2
Epinephalus merra 2 1 50 1
Caligus aff. mutabilis Lutjanus fulvus 26 4 15.4 1.75 ± 1.5
Lutjanus monostigma 6 1 16.6 2
Caligus randalli Caranx ignobilis 4 1 25 1
Caligus sp. Lutjanus fulvus 26 1 3.8 1
Caritus serratus Chanos chanos 5 1 20 4
Lepeophtheirus lewisi Acanthurus xanthopterus 20 1 5 1
Lepeophtheirus uluus Caranx ignobilis 4 1 25 4
Dissonidae
Dissonus similis Arothron hispidus 15 2 13.3 2 ± 0.0
Eudactylinidae
Nemesis sp. Carcharhinus melanopterus 5 2 40 2 ± 0.0
Hatschekiidae
Hatschekia longiabdominalis Arothron hispidus 15 8 53.3 100 ± 329.2
Hatschekia bicaudata Chaetodon auriga 13 3 23.1 7.3 ± 3.1
Chaetodon lunula 14 2 14.3 5 ± 1.4
Kroyeriidae
Kroyeria longicauda Carcharhinus melanopterus 5 2 40 16 ± 2.8
Lernanthropidae
Lernanthropus sp. Kyphosus cinerascens 2 1 50 2
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Order Cyclopoida Milne Edwards, 1840

Bomolochidae Claus, 1875

Orbitacolax Shen, 1957
Orbitacolax williamsi

Cressey & Cressey, 1989

Type host.

Scolopsistaenioptera (as S.dubiosus) (Cuvier) (Nemipteridae).

Other host and localities.

Scolopsistaenioptera (as S.dubiosus) from Okinawa, Japan (Cressey and Cressey 1989). Corisbatuensis (Bleeker) (Labridae) from Lizard Island, Australia (Muñoz and Cribb 2006). Thamnaconusdegeni (Regan) (Monacanthidae) from South Australia (Hayward et al. 2011).

Current host.

Mulloidichthysflavolineatus (Mullidae).

Site of infection.

Gills.

Prevalence and mean intensity.

1.9 and 1 (n = 52).

Specimens deposited.

CHCM No. 560 (voucher) (1 vial, 1 specimen ♀).

Remarks.

To date, the genus Orbitacolax includes 10 valid species, which form two clusters (Venmathi Maran et al. 2014), the hapalogenyos-group with four species (O.hapalogenyos, O.pteragogi, O.trichiuri, and O.unguifer) and analogus-group with six species (O.analogus, O.dactylopterusi, O.aculeatus, O.leptoscari, O.uniunquis, and O.williamsi). This second group is based on the second endopodal segment of leg 2 either no inner seta or having 1 inner seta. Particularly, O.williamsi lacks seta on the second endopodal segment of leg 2, as seen in our specimen and the original description provided by Cressey and Cressey (1989). However, Venmathi-Maran et al. (2014) pointed out that O.williamsi carries 1 inner seta in that segment, but this is likely inaccurate. Orbitacolaxwilliamsi has been found on western Pacific fishes from four families, suggesting that this parasite may have a low host specificity.

Order Siphonostomatoida Burmeister, 1835

Caligidae Burmeister, 1834

Anuretes Heller, 1865
Anuretes serratus

Shiino, 1954

Type host.

Prionurusscalprum (as Xesurusscalprum) Valenciennes (Acanthuridae).

Other host and localities.

Prionurusscalprum (as Xesurusscalprum) (Acanthuridae) from Seto, Wakayama Prefecture, Japan (Shiino 1954). Nasohexacanthus (Bleeker) (Acanthuridae) from Oahu, Hawaii (Lewis 1964a, Palm and Bray 2014); from Japan and India (Prabha and Pillai 1986). Prionurusmicrolepidotus Lacepède (Acanthuridae) from Australia (Boxshall 2018).

Current host.

Acanthurusxanthopterus (Acanthuridae).

Site of infection.

Gills.

Prevalence and mean intensity.

5 and 6 (n = 20).

Specimens deposited.

CHCM No. 561 (voucher) (1 vial, 1 specimen ♀).

Remarks.

The validity of the genus Anuretes is questionable given the considerable morphological overlap with the members of Lepeophtheirus (Dojiri and Ho 2013). Currently, Anuretes includes 21 valid species (Boxshall 2018, Walter and Boxshall 2018); of which A.serratus may be distinguished by stout spines on distal exopodal segment of leg 1, and a branched spine on first exopodal segment of leg 2 (Shiino 1954, Lewis 1964a), which were clearly observed in our specimens. In addition, A.serratus lacks sternal furca. According to Dojiri and Ho (2013), a sternal furca is rarely absent in species of Anuretes.

Caligus Müller, 1785
Caligus confusus

Pillai, 1961

Type host.

Caranxignobilis (as C.sansun) (Carangidae).

Other host and localities.

Alepesdjedaba (Forsskål) from Durban; Caranxcaballus (Günther) and Caranxcaninus (Günther) from Mexican Pacific and Ecuador; Caranxdjedaba (Forsskål) from Durban, South Africa and Sri Lanka; Caranxhippos (Linnaeus) from Galapagos Islands and Panama; Caranxignobilis from Taiwan, Indian and Australia; Caranxmelampygus Cuvier from Eniwetok Atoll and Taiwan; Caranxsexfasciatus Quoy & Gaimard from South Africa, Taiwan, Indonesia and Australia; Caranx sp. from Celebes and New Caledonia (all Carangidae); Coryphaenahippurus Linnaeus (Coryphaenidae) from Galapagos Islands and Panama; Decapterus sp. (Carangidae) from Tonkin Gulf, Vietnam; Elagatisbipinnulata (Quoy & Gaimard) (Carangidae) from Galapagos Islands, Panama, India and Taiwan; Elagatis sp. from Celebes; Epinephelustauvina (Forsskål) (Serranidae) from Kuwait; Rhabdosargusholubi (Steindachner) (Sparidae) from South Africa; Serioladumerili (Risso) (Carangidae) from Taiwan; Seriola sp. (Carangidae) from Colombia (Kabata 1968, Grobler et al. 2003, Ho and Lin 2004, Yuniar et al. 2007, Kazachenko et al. 2014, Morales-Serna et al. 2014, 2015, Boxshall 2018).

Current host.

Carangoidesferdau (Forsskål), Carangoidesorthogrammus (Jordan & Gilbert), Caranxignobilis, Caranxmelampygus and Caranxpapuensis Alleyne & MacLeay (all Carangidae).

Site of infection.

Gills.

Prevalence and mean intensity.

40 and 2 (n = 5) to Carangoidesferdau, 33.3 and 6 (n = 3) to Carangoidesorthogrammus, 75 and 12.7 ± 12.2 (n = 4) to Caranxignobilis; 33.3 and 2 (n = 6) to Caranxmelampygus; 40 and 4 (n = 5) to Caranxpapuensis.

Specimens deposited.

CHCM No. 562 (voucher) (1 vial, 1 specimen ♀) (from Caranxignobilis), CHCM No. 563 (voucher) (1 vial, 2 specimens ♂ ♀) (from Caranxpapuensis), USNM No. 1550598 (voucher) (1 vial, 1 specimen ♀) (from Caranxignobilis).

Remarks.

The genus Caligus contains approximately 250 species. According to Ho and Lin (2004), before the establishment of C.confusus, specimens of this species were confused with Caligusproductus (as Caligusalalongae) Dana, 1852 and Caligusconstrictus Heller, 1865. However, these authors pointed out nine characteristics known only for C.confusus. The morphology of our specimens (♂ and ♀) fits with the description of Ho and Lin (2004). Additionally, based on the examination of the present material and also that from previous surveys in the Eastern Pacific (Morales-Serna et al. 2014, 2015), we suggest that the shape of the first segment of the antenna and sternal furca may be useful in identifying C.confusus. Clearly, C.confusus has high affinity for carangid fish; nonetheless, this parasite can also be found on fish from different families. To date, it is distributed in tropical waters of the Eastern Pacific and Indo-Pacific, with no records for the Atlantic Ocean.

Caligus kapuhili

Lewis, 1967

Type host.

Chaetodonmiliaris Quoy & Gaimard (Chaetodontidae).

Other host and localities.

Chaetodonmiliaris Quoy & Gaimard, Chaetodonfremblii Bennett from Hawaii (Lewis 1967, Palm and Bray 2014). Chaetodonauripes Jordan & Snyder and Chaetodonvagabundus Linnaeus from Taiwan (all Chaetodontidae) (Ho and Lin 2007).

Current host.

Chaetodonauriga and Chaetodonlunula (Chaetodontidae).

Site of infection.

Gills.

Prevalence and mean intensity.

7.7 and 8 (n = 13) to Chaetodonauriga; 28.6 and 2.5 ± 1.7 (n = 14) to Chaetodonlunula.

Specimens deposited.

CHCM No. 564 (voucher) (1 vial, 1 specimen ♂) (from C.auriga). CHCM No. 565 (voucher) (1 vial, 1 specimen ♂) (from C.lunula). USNM No. 1550599 (voucher) (1 vial, 1 specimen ♂) (from C.lunula).

Remarks.

According to Lewis (1967) and Lin and Ho (2007), C.kapuhili is morphologically close to Caliguslaticaudus Shiino, 1960. However, the abdomen is 1-segmented in C.kapuhili and 2-segmented in C.laticaudus. We found specimens of C.laticaudus (see below), which facilitated our morphological analysis. Likewise, we identified C.kapuhili based on host preference, since this species has only been found on fish of the genus Chaetodon from the North-West Pacific.

Caligus laticaudus

Shiino, 1960

Type host.

Pagrusmajor (as Pagrosomusmajor) (Temminck & Schlegel) (Sparidae).

Other host and localities.

Pagrusmajor (as Pagrosomusmajor) (Sparidae) from Japan (Shiino 1960). Acanthurusolivaceus Bloch & Schneider (Acanthuridae) from Eniwetok Atoll; Dentextumifrons (Temminck & Schlegel) (Sparidae) from Korea; Lizahaematocheila (Temminck & Schlegel) (Mugilidae) from China; Caranxmelampygus (Carangidae), Lutjanusvitta (Quoy & Gaimard), Lutjanusrussellii (Bleeker) (Lutjanidae) and Parapristipomatrilineatum (Thunberg) (Haemulidae), Polydactylusplebeius (Broussonet) and Polydactylussextarius (Bloch & Schneider) (Polynemidae) from Taiwan; Parastomateusniger (Bloch) (Carangidae) from Malaysia; Filimanusheptadactyla (Cuvier) (Polynemidae) and Rhabdosargussarba (Forsskål) (Sparidae) from India (Ho and Lin 2004, Moon and Kim 2012). Gnathanodonspeciosus (Forsskål), Caranxsexfasciatus Quoy & Gaimard (Carangidae), Heniochusacuminatus (Linnaeus) (Chaetodontidae), Kyphosusbigibbus Lacepède (Kiphosidae), Pseudolabrusguentheri Bleeker (Labridae), Pagrusauratus (Forster) (Sparidae) from Australia (Boxshall 2018).

Current host.

Rhinecanthusaculeatus (Linnaeus), Pseudobalistesflavimarginatus (Rüppell) (Balistidae), Mulloidichthysflavolineatus, Upeneustaeniopterus Cuvier (Mullidae), Chrysipteraglauca (Cuvier) (Pomacentridae) and Epinephalusmerra Bloch (Serranidae).

Site of infection.

Gills..

Prevalence and mean intensity.

5.6 and 1 (n = 18) to Rhinecanthusaculeatus; 50 and 21 ± 26.9 (n = 4) to Pseudobalistesflavimarginatus; 13.5 and 1.5 ± 0.5 (n = 52) to Mulloidichthysflavolineatus; 60 and 2.7 ± 2.1 (n = 5) to Upeneustaeniopterus; 3.33 and 2 (n = 3) to Chrysipteraglauca; 50 and 1 (n = 2) to Epinephalusmerra.

Specimens deposited.

CHCM No. 566 (voucher) (1 vial, 2 specimens ♂ ♀) (from M.flavolineatus). USNM No. 1550600 (voucher) (1 vial, 1 specimen ♂) (from M.flavolineatus).

Remarks.

Ho and Lin (2004) indicated that the female of C.laticaudus may be identified by a combination of five characteristics (the corpus of the maxilliped with a large, conical protrusion in the myxal region; the terminal elements on last segment of exopod of leg 1 lack accessory processes; outermost element 1 of the four terminal elements of leg 1 exopod about one third of the length of other three elements which are subequal in length; formula of the 3-segmented exopod of leg 4 as I-0; I-0; III; and the terminal three spines on leg 4 subequal in length). Our results support the view that C.laticaudus infects fishes only from the Indo-West Pacific.

Caligus aff. mutabilis

Wilson, 1905

Type host.

Centropristisstriata (as Centropristesstriatus) (Linnaeus) (Serranidae).

Other host and localities.

Centropristisstriata (as Centropristesstriatus) (Serranidae) from North American waters (Wilson 1905). Acanthocybium sp., Euthynnus sp., Sarda sp., Scomberomorus sp., and Thunnus sp. (all Scombridae) from Colombia; Archosargusrhomboidalis (Linnaeus) (Sparidae), Chaetodipterusfaber (Broussonet) (Ephippidae), Mycteropercamicrolepis (Goode & Bean), Scomberomorusbrasiliensis Collette, Russo & Zavala-Camin, Scomberomorusmaculatus (Mitchill) (Scombridae) and Trachinotusgoodei Jordan & Evermann (Carangidae) from Brazil; Balistes sp. (Balistidae), Calamusbrachysomus (Lockington) (Sparidae), Centropomus sp. (Centropomidae), Chaetodipteruszonatus (Girard) (Ephippidae), Epinepheluslabriformis (Jenyns) (Serranidae), Hoplopagrusguentherii Gill (Lutjanidae), Katsuwonuspelamis (Linnaeus) (Scombridae), Kyphosuselegans (Peters) (Kyphosidae), Lutjanusguttatus (Steindachner), Lutjanusperu (Nichols & Murphy) (Lutjanidae), Menticirrhusundulatus (Girard) (Sciaenidae), Microlepidotusbrevipinnis (Steindachner) (Haemulidae), Mugilcephalus (Linnaeus) (Mugilidae), Paralabraxclathratus (Girard), Paralabraxmaculatofasciatus (Steindachner), Paralabraxnebulifer (Girard) (all Serranidae), Sardachiliensis (Cuvier), Scomberomorussierra Jordan & Starks (Scombridae) and Seleneorstedii Lütken (Carangidae) from Mexican Pacific; S.brasiliensis from Costa Rica; Scomberomoruscavalla (Cuvier) (Scombridae) from Surinam; S.maculatus from Florida; Scomberomorusjaponicus from Campeche (Gulf of Mexico); E.labriformis, Eucinostomusentomelas Zahuranec (Gerreidae), Haemulopsisaxillaris (Steindachner) (Haemulidae), Paralabraxcallaensis Starks (Serranidae), Chromiscyanea (Poey) and Chromismultilineata (Guichenot) (Pomacentridae) from Ecuador (Cressey and Cressey 1980, Luque and Tavares 2007, Gomes-Sanches et al. 2012, Morales-Serna et al. 2016).

Current hosts.

Lutjanusfulvus and Lutjanusmonostigma (Cuvier) (Lutjanidae).

Site of infection.

Gills..

Prevalence and mean intensity.

15.4 and 1.75 ± 1.5 (n = 26) to L.fulvus; 16.6 and 2 (n = 6) to L.monostigma.

Specimens deposited.

CHCM No. 567 (voucher) (1 vial, 1 specimen ♂) (from L.fulvus), CHCM No. 568 (voucher) (1 vial, 1 specimen ♂) (from L.monostigma). USNM No. 1550601 (voucher) (1 vial, 1 specimen ♂) (from L.monostigma).

Remarks.

Wilson (1905) observed that the genital complex of C.mutabilis varies according to the age of the individuals as well as the developmental stage of the eggs. Also, this author described C.mutabilis as having a short, 2-segmented abdomen. Later, Cressey and Cressey (1980) redescribed this species based on material collected from scombrid fish. These authors noted an incomplete 2-segmented abdomen and at least two other differences from the type specimens; however, such differences were not considered sufficient to propose a new species. Recently, Morales-Serna et al. (2014, 2015) reported C.mutabilis from different host species in the Eastern Pacific, but a molecular analysis revealed relatively high intraspecific genetic divergence among the C.mutabilis isolates. Our specimens share the morphological characteristics described by Cressey and Cressey (1980).

Caligus randalli

Lewis, 1964

Type host.

Acanthurustriostegus (Linnaeus) (Acanthuridae).

Other host and localities.

To our knowledge, C.randalli has not been recorded since its original description (Lewis 1964a). Acanthurustriostegus (Acanthuridae) from Hawaii (Lewis 1964a, Palm and Bray 2014).

Current host.

Caranxignobilis (Carangidae).

Site of infection.

Gills.

Prevalence and mean intensity.

25 and 1 (n = 4).

Specimens deposited.

CHCM No. 569 (voucher) (1 vial, 2 specimens ♂♀). USNM No. 1550602 (voucher) (1 vial, 1 specimen ♂).

Remarks.

Lewis (1964a) observed that Caligusrandalli is morphologically close to C.constrictus Heller, 1865. According to this author, one of the main differences between both species is the length of the urosome. The urosome of C.randalli is one and a half times the length of the urosome of C.constrictus. In the present study, we noted that C.randalli resembles Caligusaesopus Wilson, 1921. However, the urosome in C.aesopus is shorter than in C.randalli. Hayes et al. (2012) included C.aesopus and another nine species of Caligus (C.chorinemy Kroyer, 1863, C.tenax Heller, 1865, C.spinosurculus Pearse, 1951, C.germoi Pearse, 1951, C.rectus Pearse, 1952, C.confusus, C.cordyla Pillai, 1963, C.zylanica Hameed & Pillai, 1986 and C.equulae Ho & Lin, 2003) within a cluster of caligid species sharing the following characteristics in the female: bifid postantennal process; bifid posterior process on the maxillule; heavily ornamented apron of the third leg; an inner rosette of large spinules and prominent rib-like structure with a bifid apex, arising near the border with the intercoxal sclerite of leg 3: a massive and strongly incurved spine on the first exopodal segment of leg 3; and a 3-segmented exopod on leg 4 armed with I,I,III spines. Caligusrandalli also shares these characteristics, and after a detailed examination. We confirmed that the morphological characteristic of our specimens fit with the description Lewis (1964a) for C.randalli. This is also supported by records of C.randalli in the Central Pacific.

Caligus

sp.

Current host.

Lutjanusfulvus (Lutjanidae).

Site of infection.

Gills.

Prevalence and mean intensity.

3.8 and 1 (n = 26).

Specimens deposited.

CHCM No. 570 (voucher) (1 vial, 1 specimen ♂).

Remarks.

Caligus sp. is morphologically close to Caliguslaticaudus, mainly by the shape and armature of cephalothoracic appendages and legs. However, our specimen differs from C.laticaudus in the shape and size of the urosome. Unfortunately, the single specimen of Caligus sp. in our collection is not sufficient for a more detailed taxonomic study.

Caritus Cressey, 1967
Caritus serratus

Cressey, 1967

Type host:.

Chanoschanos (Forsskål) (Chanidae).

Other host and localities.

Chanoschanos (Chanidae) from Nosy Bé, Madagascar (Cressey 1967). Reported as Caritustolii from Tenualosatoli (as Hilsatoli) (Valenciennes) (Clupeidae) from Sassoon Docks, Bombay (Rangnekar 1984).

Current host.

Chanoschanos (Chanidae).

Site of infection.

Gills.

Prevalence and mean intensity.

20 and 4 (n = 5).

Specimens deposited.

CHCM No. 571 (voucher) (1 vial, 1 specimen ♀).

Remarks.

Currently, C.serratus is the unique valid species included in the genus Caritus. Morphological characteristics of our specimens agree well with the redescription provided by Dojiri and Ho (2013).

Lepeophtheirus von Nordmann, 1832
Lepeophtheirus lewisi

Hewitt, 1971

Type host.

Acanthurusolivaceus (Acanthuridae).

Other host and localities.

Acanthurusolivaceus (Acanthuridae) from Hawaii (Hewitt 1971). Nasohexacanthus (Bleeker), Acanthurustriostegus (Acanthuridae), Myripristis sp., Fistulariapetimba Lacepède (Fistulariidae) (Lewis 1964a, 1964b, Palm and Bray 2014).

Current host.

Acanthurusxanthopterus (Acanthuridae).

Site of infection.

Gills.

Prevalence and mean intensity.

5 and 1 (n = 20).

Specimens deposited.

CHCM No. 572 (voucher) (1 vial, 1 specimen ♂). USNM

No. 1550603 (voucher) (1 vial, 1 specimen ♂).

Remarks.

Lepeophtheiruslewisi was originally described as Dentigrypsbifurcatus by Lewis (1964a). However, Hewitt (1971) stated that there is not a useful character to separate Dentigryps Wilson, 1913 from Lepeophtheirus and, therefore, reassigned species of Dentigryps to Lepeophtheirus. As the name L.bifurcatus was preoccupied by L.bifurcatusWilson 1905, Hewitt (1971) renamed Lewis’ species as L.lewisi. The material of the present study corresponds to a male of L.lewisi. The identification of this species was difficult without female specimens; nonetheless, the morphology of our material fits the description provided by Lewis (1964a) for the male of L.lewisi. In addition, this copepod has been mainly found in acanthurid fish from the Central Pacific as in the present work.

Lepeophtheirus uluus

Lewis, 1964

Type host.

Caranxmelampygus (Carangidae).

Other host and localities.

Caranxmelampygus (Carangidae) from Oahu, Hawaii (Lewis 1964b, Palm and Bray 2014). Reported as Dentigrypsulua on Caranxignobilis from Heron Island, Australia (Ho and Dojiri 1977).

Current host.

Caranxignobilis (Carangidae).

Site of infection.

Gills.

Prevalence and mean intensity.

25 and 4 (n = 4).

Specimens deposited.

CHCM No. 573 (voucher) (1 vial, 2 specimens ♂♀).

Remarks.

Lepeophtheirusuluus was originally described as Dentigrypsulua by Lewis (1964b) and then transferred to Lepeophtheirus by Hewitt (1971). The morphology of our specimens corresponds to the original description.

Dissonidae Kurtz, 1924

Dissonus Wilson, 1906
Dissonus similis

Kabata, 1966

Type host.

Tetractenoshamiltoni (Richardson) (as Spheroideshamiltoni) (Tetraodontidae).

Other host and localities.

Tetractenoshamiltoni (as Spheroideshamiltoni) (Tetraodontidae) from Queensland, Australia (Kabata 1966). Arothronhispidus from Philippines; Arothronmeleagris (Anonymous) from Guam; Arothronnigropunctatus (Bloch & Schneider) from Australia, Philippines and New Guinea; and Arothronstellatus (Anonymous) (all Tetraodontidae) from New Guinea (Tang and Kalman 2005).

Current host.

Arothronhispidus (Tetraodontidae).

Site of infection.

Gills.

Prevalence and mean intensity.

13.3 and 2 ± 0.5 (n = 15).

Specimens deposited.

CHCM No. 574 (voucher) (1 vial, 1 specimen ♀). USNM

No. 1550604 (voucher) (1 vial, 1 specimen ♀).

Remarks.

The family Dissonidae comprises only two genera, Innaprokofevnas Kazatchenko, 2001 with a single species (I.orientcolae Kazatchenko, 2001) and Dissonus with 12 species (D.excavatus Boxshall, Lin, Ho, Ohtsuka, Venmathi Maran & Justine, 2008; D.furcatus Kirtisinghe, 1950; D.glaber Kurtz, 1950; D.heronensis Kabata, 1966; D.hoi Tang & Kalman, 2005; D.inaequalis Boxshall, Lin, Ho, Ohtsuka, Venmathi Maran & Justine, 2008; D.kapuri (Ummerkutty, 1976); D.manteri Kabata, 1966; D.nudiventris Kabata, 1965; D.ruvetti Nuñes-Ruivo & Fourmanoir, 1956; D.similis; and D.spinifer Wilson, 1906).

According to Kabata (1966), D.similis is morphologically closer to D.furcatus. However, D.similis may be separated from D.furcatus and other congeners by the lack of a sternal furca or stylet and the presence of a genital spinulation extending over the anterior half to two thirds of ventral surface of genital complex (Tang and Kalman 2005, Boxshall et al. 2008). As indicated by Tang and Kalman (2005), D.similis is restricted to the tropical western Pacific and is highly host specific to tetraodontid fishes.

Eudactylinidae Wilson C.B., 1932

Nemesis

sp. Risso, 1826

Current host.

Carcharhinusmelanopterus (Carcharhinidae).

Site of infection.

Gills.

Prevalence and mean intensity.

40 and 2 ± 0.1 (n = 5).

Specimens deposited.

CHCM No. 575 (voucher) (1 vial, 1 specimen ♀).

Remarks.

Nemesis is one of 12 genera in the family Eudactylinidae and includes about nine species (Mangena et al. 2014). Nemesis species can be divided into two groups by the relative width of the cephalothorax, free thoracic segments and genital segments (Dippenaar et al. 2008). One group (consisting of most of the species) has a fourth free thoracic segment that is much narrower than the preceding three, whereas the other (consisting of N.lamna only) has all four segments of about the same width (Kabata 1979). The identification and comparison of Nemesis species belonging to the first group is difficult because of morphological variation among individuals and the inconsistencies in the literature (Hewitt 1969, Kabata 1979).

Hatschekiidae Kabata, 1979

Hatschekia Poche, 1902
Hatschekia longiabdominalis

Uyeno & Nagasawa, 2013

Type host.

Arothronhispidus (Tetraodontidae).

Other host and localities.

Arothronhispidus (Tetraodontidae) from Japan (Uyeno and Nagasawa 2013). To date, H.longiabdominalis has not been recorded from others host and locality.

Current host.

Arothronhispidus (Tetraodontidae).

Site of infection.

Gills.

Prevalence and mean intensity.

53.3 and 100 ± 329.2 (n = 15).

Specimens deposited.

CHCM No. 576 (voucher) (1 vial, 1 specimen ♀). USNM

No. 1550605 (voucher) (1 vial, 1 specimen ♀).

Remarks.

Of the nine genera included in the Hatschekiidae, the most speciose genus is Hatschekia, with approximately 140 valid species so far. According to Uyeno and Nagasawa (2013), H.longiabdominalis may be separated from other congeners by having a fusiform trunk with posterior lobes, the urosome markedly projecting beyond posterior lobes of the trunk, and unique intercoxal sclerites of legs 1 and 2, which strongly project from the middle of the anterior margin and bear four blunt processes on the posterior margin. We observed all of these characters in our specimens.

Hatschekia bicaudata

Kabata, 1991

Type host.

Chaetodonaureofasciatus Macleay (Chaetodontidae).

Other host and localities.

Chaetodonaureofasciatus (Chaetodontidae) from Australia (Kabata 1991). Chaetodonauripes Jordan & Snyder (Chaetodontidae) from Seto, Wakayama Prefecture, Japan (Izawa 2016).

Current host.

Chaetodonauriga and Chaetodonlunula (Chaetodontidae).

Site of infection.

Gills.

Prevalence and mean intensity.

23.1 and 7.3 ± 3.1 (n = 13) to Chaetodonauriga; 14.3 and 5 ± 1.4 (n = 14) to Chaetodonlunula.

Specimens deposited.

CHCM No. 577 (voucher) (1 vial, 1 specimen ♀) (from Chaetodonauriga). CHCM No. 578 (voucher) (1 vial, 1 specimen ♀) (from Chaetodonlunula). USNM No. 1550606 (voucher) (1 vial, 1 specimen ♀) (from Chaetodonlunula).

Remarks.

Our samples corresponded to a single mature female from each host, which were not dissected for morphological analysis. Nonetheless, these parasitic copepods resemble H.bicaudata in its habitus, antenna, maxilla, and armature of legs 1 and 2, as well as in its preferred hosts, which are butterfly fishes distributed in warm waters from Australia to Japan (see Izawa 2016).

Kroyeriidae Kabata, 1979

Kroyeria van Beneden, 1853
Kroyeria longicauda

Cressey, 1970

Type host.

Carcharhinuslimbatus (Müller & Henle) (Carcharhinidae).

Other host and localities.

Carcharhinuslimbatus (Carcharhinidae) from Florida. Carcharhinusbrevipinna (Müller & Henle) (Carcharhinidae) from Madagascar (Deets 1994).

Current host.

Carcharhinusmelanopterus (Carcharhinidae).

Site of infection.

Gills.

Prevalence and mean intensity.

40 and 16 ± 2.8 (n = 5).

Specimens deposited.

CHCM No. 579 (voucher) (1 vial, 1 specimen ♀). USNM No. 155607 (voucher) (1 vial, 1 specimen ♀).

Remarks.

The family Kroyeriidae comprises three genera, Kroeyerina Wilson, 1932 with nine species, Kroyeria with 15 species, and Prokroyeria Deets, 1987 with a single species (Walter and Boxshall 2018). Within Kroyeria, K.longicauda can be identified by the lateral tine on the deeply incised, bifid dorsal stylet, the lateral cuticular flange on the caudal rami, and the small number of unusually large endopodal denticulations of legs 1 to 4 that are unique to this species (Deets 1994).

Lernanthropidae Kabata, 1979

Lernanthropus de Blainville, 1822
Lernanthropus

sp.

Current host.

Kyphosuscinerascens (Forsskål) (Kyphosidae).

Site of infection.

Gills.

Prevalence and mean intensity.

50 and 2 (n = 2).

Specimens deposited.

CHCM No. 580 (voucher) (1 vial, 1 specimen ♀).

Remarks.

The genus Lernanthropus includes about 120 species and it is one of the commonest genera of parasitic copepods on marine fishes. In this study, a single female of Lernanthropus sp. was collected. We were unable to proceed with the species identification because of the lack of specimens for dissection, which is necessary to observe appendages of the cephalothorax as well as legs 1 and 2. Even with enough material, the identification of Lernanthropus sp. is quite difficult because many species have not been described with sufficient detail (Koyuncu et al. 2012).

Discussion

The present study is the first detailed survey of the diversity and ecological attributes of the parasitic copepods infecting fishes at Palmyra Atoll. All records we report here are new geographical records. Most copepods (10 of 17) belonged to the family Caligidae. Of these ten caligid species, six were in the genus Caligus and two in the genus Lepeophtheirus. These finding are in agreement with the fact that Caligus copepods are mostly found on warm water fishes, while Lepeophtheirus copepod diversity is low in the tropics (Ho and Lin 2004, Suárez-Morales and Gasca 2012, Morales-Serna et al. 2016). However, as far as we know, specific evolutionary or ecological mechanisms underlying this greater diversification Caligus species in the tropics are not well understood. On the other hand, in experiments carried out by Bravo et al. 2010, they suggest that species of Caligus are more active swimmers than species of Lepeophtheirus, which in turns increase transmission between hosts. Clearly, such swimming ability could be contributing to dispersal of Caligus and host switching. Several copepods species can parasitize multiple fish species (Dojiri and Ho 2013). This is the case of C.mutabilis found on Lutjanusmonostigma and L.fulvus in the present study however, this species has been reported in at least 13 families of marine fishes from the Atlantic and Pacific oceans (Morales-Serna et al. 2015).

Consistent with observations of the monogenean fauna of Palmyra Atoll fishes (Vidal-Martínez et al. 2017), parasitic copepod richness at Palmyra Atoll qualitatively appears low relative to other localities in the Indo-Pacific region. Most of the fish species we examined (30 of 44) were not parasitized by copepods, even with large sample sizes for some fish species (e.g. Acanthurustriostegus, n = 50). Several fishes that were unparasitized at Palmyra have copepod records at other sites. For example, Acanthurustriostegus, Gymnothoraxpictus, Epinephelusmerra and Sphyraenabarracuda have been reported as hosts of at least one species of parasitic copepod in other localities of the Indo-Pacific (Boxshall and Huys 2007, Palm and Bray 2014). Because ectoparasite species richness, host size and age are positively related (Rhode 1993, Muñoz and Cribb 2005), the lack of copepods in some host species could be due to our sampling of only young (Chanoschanos) or small individuals (Sphyraenabarracuda). Furthermore, the intertidal habitat sampled at Palmyra differs from the more often sampled fore-reef and reef flat habitats, making a direct comparison among studies difficult. More generally, Palmyra’s remoteness may contribute to its depauperate copepod parasite fauna. The Line Islands are far from the Austro-Malayan-Philippine region, the presumed center of origin of Indo-West Pacific (IWP) fishes and their parasites. Because we found fewer copepod species than described from Hawaii, which is still further from the presumed center of origin, we suggest that the remote location of the Line Islands and the particularly small size of Palmyra Atoll also contribute to the depauperate nature of the parasitic copepod fauna.

Supplementary Material

XML Treatment for Orbitacolax williamsi
zookeys.833.30835-treatment1.xml (15KB, xml)
XML Treatment for Anuretes serratus
zookeys.833.30835-treatment2.xml (12.7KB, xml)
XML Treatment for Caligus confusus
zookeys.833.30835-treatment3.xml (24.3KB, xml)
XML Treatment for Caligus kapuhili
zookeys.833.30835-treatment4.xml (12.1KB, xml)
XML Treatment for Caligus laticaudus
zookeys.833.30835-treatment5.xml (19.7KB, xml)
XML Treatment for Caligus aff. mutabilis
zookeys.833.30835-treatment6.xml (29.4KB, xml)
XML Treatment for Caligus randalli
zookeys.833.30835-treatment7.xml (13.9KB, xml)
XML Treatment for Caligus
zookeys.833.30835-treatment8.xml (4.7KB, xml)
XML Treatment for Caritus serratus
zookeys.833.30835-treatment9.xml (8.5KB, xml)
XML Treatment for Lepeophtheirus lewisi
zookeys.833.30835-treatment10.xml (13.6KB, xml)
XML Treatment for Lepeophtheirus uluus
zookeys.833.30835-treatment11.xml (10.2KB, xml)
XML Treatment for Dissonus similis
zookeys.833.30835-treatment12.xml (15.9KB, xml)
XML Treatment for Nemesis
zookeys.833.30835-treatment13.xml (9KB, xml)
XML Treatment for Hatschekia longiabdominalis
zookeys.833.30835-treatment14.xml (7.7KB, xml)
XML Treatment for Hatschekia bicaudata
zookeys.833.30835-treatment15.xml (9.7KB, xml)
XML Treatment for Kroyeria longicauda
zookeys.833.30835-treatment16.xml (7.7KB, xml)
XML Treatment for Lernanthropus
zookeys.833.30835-treatment17.xml (6.4KB, xml)

Acknowledgements

We acknowledge and thank the Palmyra Atoll National Wildlife Refuge, U.S. 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 U.S. 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 U.S. Government.

Citation

Soler-Jiménez LC, Morales-Serna FN, Aguirre-Macedo ML, McLaughlin JP, Jaramillo AG, Shaw JC, James AK, Hechinger RF, Kuris AM, Lafferty KD, Vidal-Martínez VM (2019) Parasitic copepods (Crustacea, Hexanauplia) on fishes from the lagoon flats of Palmyra Atoll, Central Pacific ZooKeys 833: 85–106. https://doi.org/10.3897/zookeys.833.30835

References

  1. Boxshall GA. (2018) The sea lice (Copepoda: Caligidae) of Moreton Bay (Queensland, Australia), with descriptions of thirteen new species. Zootaxa 4398: 1–172. 10.11646/zootaxa.4398.1.1 [DOI] [PubMed] [Google Scholar]
  2. Boxshall GA, Huys R. (2007) Copepoda of New Caledonia. In: Payri CE, Richer de Forges B. (Eds) Compendium of Marine Species of New Caledonia, Doc.Sci. Tech. II7, seconde édition, IRD Nouméa, 259–265.
  3. Boxshall GA, Justine J-L. (2005) A new genus of parasitic copepod (Siphonostomatoida: Caligidae) from a razorback scabbardfish, Assurgeranzac Alexander (Trichiuridae) off New Caledonia. Folia Parasitologica, 52: 349–358. 10.14411/fp.2005.048 [DOI] [PubMed] [Google Scholar]
  4. Boxshall GA, Lin CL, Ho JS, Ohtsuka S, Venmathi Maran BA, Justine JL. (2008) A revision of the family Dissonidae Kurtz, 1924 (Copepoda: Siphonostomatoida). Systematic Parasitology 70: 81–106. [DOI] [PubMed] [Google Scholar]
  5. Bravo S, Treasurer J, Sepulveda M. (2010) Effectiveness of hydrogen peroxide in the control of Caligusrogercresseyi in Chile and implications for sea louse management. Aquaculture 303: 22–27. 10.1016/j.aquaculture.2010.03.007 [DOI] [Google Scholar]
  6. Bush A, Lafferty K, Lotz J, Shostak A. (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of Parasitology 83: 575–583. 10.2307/3284227 [DOI] [PubMed] [Google Scholar]
  7. Cressey RF. (1967) Caritus a new genus of caligoid copepod, with a key to the genera of Caliginae. Proceedings of the United States National Museum 123(3623): 1–8. 10.5479/si.00963801.123-3623.1 [DOI] [Google Scholar]
  8. Cressey RF. (1970) Copepods parasites on sharks from the west coast of Florida. Smithsonian Contributions to Zoology 38: 1–30. 10.5479/si.00810282.38 [DOI] [Google Scholar]
  9. Cressey RF. (1977) Boylealongispican g., n. sp. and other parasitic copepods from pacific fishes. Transactions of the American Microscopical Society 96(4): 467–476. 10.2307/3225664 [DOI] [Google Scholar]
  10. Cressey RF, Boyle HB. (1973) Five New Bomolochid Copepods Parasitic on Indo-Pacific Clupeid Fishes. Smithsonian Contributions Zoology 161: 1–25. 10.5479/si.00810282.161 [DOI] [Google Scholar]
  11. Cressey RF, Boyle HB. (1979) The Parasitic Copepods of Indo-West Pacific Lizardfishes (Synodontidae). Smithsonian Contributions to Zoology 296: 1–71. 10.5479/si.00810282.296 [DOI] [Google Scholar]
  12. Cressey RF, Cressey HB. (1979) The Parasitic Copepods of Indo-West Pacific Lizardfishes (Synodontidae). Smithsonian Contributions Zoology 296: 1–71. 10.5479/si.00810282.296 [DOI] [Google Scholar]
  13. Cressey RF, Cressey HB. (1980) Parasitic copepods of mackerel – and tuna – like fishes (Scombridae) of the world. Smithsonian Contributions to Zoology 311: 1–86. 10.5479/si.00810282.311.i [DOI] [Google Scholar]
  14. Cressey R, Cressey HB. (1989) A new species of Orbitacolax (Copepoda: Bomolochidae) and redescriptions of additional two species. Canadian Journal of Zoology 67: 2902–2909. 10.1139/z89-411 [DOI] [Google Scholar]
  15. Deets GB. (1987) Phylogenetic analysis and revision of Kroeyerina Wilson, 1932 (Siphonostomatoida: Kroyeriidae), copepods parasitic on chondrichthyans, with descriptions of four new species and the erection of a new genus, Prokroyeria. Canadian Journal of Zoology 65(9): 2121–2148. 10.1139/z87-327 [DOI] [Google Scholar]
  16. Deets GB. (1994) Copepod-Chondrichthyan coevolution: a cladistics consideration. PhD Thesis, University of British Columbia, Vancouver, 448 pp. [Google Scholar]
  17. Deets GB, Dojiri M. (1990) Dissonuspastinum n. sp. (Siphonostomatoida: Dissonidae), a copepod parasitic on a horn shark from Japan. Beaufortia 41: 49–54. [Google Scholar]
  18. DeMartini EE, Friedlander AM, Sandin SA, Sala E. (2008) Differences in fish-assemblage structure between fished and unfished atolls in the northern Line Islands, central Pacific. Marine Ecology Progress Series 365: 199–215. 10.3354/meps07501 [DOI] [Google Scholar]
  19. Dojiri M, Ho JS. (2013) Systematics of the Caligidae copepods parasitic on marine fishes. Koninklijke Brill NV, Leiden. 10.1163/9789004204256 [DOI]
  20. Dippenaar S, van Tonder R, Wintner S, Zungu P. (2008) Spatial distribution of Nemesislamna Risso 1826 (Copepoda: Siphonostomatoida: Eudactylinidae) on the gills of white sharks Carcharodoncarcharias off KwaZulu-Natal, South Africa, African Journal of Marine Science 30(1): 143–148. 10.2989/AJMS.2008.30.1.14.464 [DOI]
  21. Froese R, Pauly D. (2018) Editors FishBase. http://www.fishbase.org [10/2018]
  22. Gomes-Sanches E, Kerber CE, Paschoal F, Luque JL. (2012) First record of Caligusmutabilis (Copepoda: Caligidae), in sea-farmed Mycteropercamicrolepis (Perciformes: Serranidae) in Brazil. Revista Brasileira de Parasitologia Veterinária 21: 330–333. 10.1590/S1984-29612012000300031 [DOI] [PubMed] [Google Scholar]
  23. Grobler NJ, Van As JG, Oliver PAS. (2003) Additional morphological information on two species of Caligus (Copepoda: Caligidae) parasitic on South Africa marine and estuarine fish. African Zoology 38: 139–143. 10.1080/15627020.2003.11657201 [DOI] [Google Scholar]
  24. Hayes P, Justine JL, Boxshall GA. (2012) The genus Caligus Müller, 1785 (Copepoda: Siphonostomatoida): two new species from reef associated fishes in New Caledonia, and some nomenclatural problems resolved. Zootaxa 3534: 21–39. [Google Scholar]
  25. Hayward CJ, Svane I, Lachimpadi SK, Itoh N, Bott NJ, Nowak BF. (2011) Sea lice infections of wild fishes near ranched southern bluefin tuna (Thunnusmaccoyii) in South Australia. Aquaculture 320: 178–182. 10.1016/j.aquaculture.2010.10.039 [DOI] [Google Scholar]
  26. Hewitt GC. (1969) Some New Zealand parasitic Copepoda of the family Eudactylinidae. Zoology Publications from Victoria University of Wellington 49: 1–31. [Google Scholar]
  27. Hewitt GC. (1971) Species of Lepeophtheirus (Copepoda, Caligidae) recorded from the ocean sunfish (Molamola) and their implications for the caligid genus Dentigryps. Journal of Fisheries Research Board of Canada 28: 323–334. 10.1139/f71-044 [DOI] [Google Scholar]
  28. Ho JS, Dojiri M. (1977) Parasitic copepods on the fishes of the Great Barrier Reef, Australia Part II. Caligoida: Dissonus, Lepeophtheirus and Dentigryps. Publications of the Seto Marine Biological Laboratory 24: 77–97. 10.5134/175956 [DOI] [Google Scholar]
  29. Ho JS, Lin CL. (2003) Three species of Caligus (Copepoda: Caligidae) parasitic on fishes of the northeast coast of Taiwan. Journal of the Fisheries Society of Taiwan 30(1): 55–70. [Google Scholar]
  30. Ho JS, Lin CL. (2004) Sea lice of Taiwan (Copepoda: Siphonostomatoida: Caligidae). The Sueichan Press, Keelung.
  31. Ho JS, Lin CL. (2007) Two new species of taeniacanthid copepods (Poecilostomatoida) parasitic on marine fishes of Taiwan. Systematic Parasitology 67(1): 73–80. 10.1007/s11230-006-9073-3 [DOI] [PubMed] [Google Scholar]
  32. Izawa K. (2016) Some new and known species of Hatschekia Poche, 1902 (Copepoda, Siphonostomatoida, Hatschekiidae) parasitic on the branchial lamellae of Japanese actinopterygian fishes belonging to perciformes, with revision of the known species of the genus. Crustaceana 89: 209–238. 10.1163/15685403-00003503 [DOI] [Google Scholar]
  33. Kabata Z. (1965) Parasitic Copepoda of fishes. Report B.A.N.Z. Antarctic Research Expedition 8(6): 1–16. [Google Scholar]
  34. Kabata Z. (1966) Copepoda parasitic on Australian fishes, V. Genus Dissonus (Dissonidae). Annals and Magazine of Natural History 13: 211–226. 10.1080/00222936608656047 [DOI] [Google Scholar]
  35. Kabata Z. (1968) Two species of Caligus from New Caledonia. Crustaceana 1: 1–10. [Google Scholar]
  36. Kabata Z. (1979) Parasitic Copepoda of British fishes. The Ray Society, London, 468 pp. [Google Scholar]
  37. Kabata Z. (1991) Copepoda parasitic on Australian fishes, XIII: family Hatschekiidae. Journal of Natural History 25: 91–121. 10.1080/00222939100770081 [DOI] [Google Scholar]
  38. Kazachenko VN, Kovaleva NN, Ha DN, Nguyen VH, Thanh NV. (2014) Redescription of three caligid species of the genus Caligus Müller, 1785 (Copepoda: Caligidae), parasites of marine fish Decapterus sp. (Perciformes: Carangidae) from Tonkin Gulf, Vietnam. Tap Chi Sinh Hoc 36: 1–11. [Google Scholar]
  39. Koyuncu CE, Castro-Romero R, Karaytug S. (2012) Lernanthropusindefinitus n. sp. (Copepoda, Siphonostomatoida, Lernanthropidae) parasitic on Argyrosomusregius (Asso, 1801) (Pisces, Sciaenidae). Crustaceana 85: 1409–1420. 10.1163/15685403-00003138 [DOI] [Google Scholar]
  40. Lafferty KD, Shaw JC, Kuris AM. (2008) Reef fishes have higher parasite richness at unfished Palmyra Atoll compared to fished Kiritimati Island. EcoHealth 5: 338–345. 10.1007/s10393-008-0196-7 [DOI] [PubMed] [Google Scholar]
  41. Lewis AG. (1964a) Caligoid copepods (Crustacea) of the Hawaiian Islands: Parasitic on fishes of the family Acanthuridae. Proceedings of the United States National Museum 11: 137–244. 10.5479/si.00963801.115-3482.137 [DOI] [Google Scholar]
  42. Lewis AG. (1964b) The caligid copepod genus Dentigryps (Crustacea: Caligoida). Proceedings of the United States National Museum 115: 347–380. 10.5479/si.00963801.115-3487.347 [DOI] [Google Scholar]
  43. Lewis AG. (1967) Copepod crustaceans parasitic on teleost fishes of the Hawaiian Islands. Proceedings of the United States National Museum 121: 1–204. 10.5479/si.00963801.121-3574.1 [DOI] [Google Scholar]
  44. Lewis AG. (1968) Copepod crustaceans parasitic on the fishes of Enewetok Atoll. Proceedings of the United States National Museum 125: 1–78. 10.5479/si.00963801.125-3656.1 [DOI] [Google Scholar]
  45. Lin CL, Ho JS. (2007) Six species of sea lice (Copepoda, Caligidae) new to Taiwan. Journal of the Fisheries Society of Taiwan 34: 41–67. [Google Scholar]
  46. Luque JL, Tavares LER. (2007) Checklist of Copepoda associated with fishes from Brazil. Zootaxa 1579: 1–39. 10.11646/zootaxa.1579.1.1 [DOI] [Google Scholar]
  47. Mangena T, Jordaan BP, Dippenaar SM. (2014) Phylogenetic relationships and genetic diversity of Nemesis Risso, 1826 species found on different elasmobranch host species off the KwaZulu-Natal coast, South Africa. African Journal of Marine Science 36(2): 163–173. 10.2989/1814232X.2014.912992 [DOI] [Google Scholar]
  48. Moon SY, Kim IH. (2012) Sea lice (Copepoda, Siphonostomatoida, Caligidae) new to Korea, including three new species. Journal of Species Research 1: 175–217. 10.12651/JSR.2012.1.2.175 [DOI] [Google Scholar]
  49. Morales-Serna FN, Caña-Bozada V, Mera-Loor G, Loor-Andrade P, Fajer-Ávila EJ, Ho JS. (2015) New records of sea lice (Copepoda: Caligidae) from marine fishes in Jaramijó, an area with potential for sea-cage aquaculture in Ecuador. Zootaxa 3920: 366–380. 10.11646/zootaxa.3920.2.8 [DOI] [PubMed] [Google Scholar]
  50. Morales-Serna FN, Medina-Guerrero RM, Fajer-Ávila EJ. (2016) Sea lice (Copepoda: Caligidae) parasitic on fishes reported from the Neotropical region. Neotropical Biodiversity 2(1): 141–150. 10.1080/23766808.2016.1236313 [DOI] [Google Scholar]
  51. Morales-Serna FN, Pinacho-Pinacho CD, Gómez S, Pérez-Ponce de León G. (2014) Diversity of sea lice (Copepoda: Caligidae) parasitic on marine fishes with commercial and aquaculture importance in Chamela Bay, Pacific coast of Mexico by using morphology and DNA barcoding, with description of a new species of Caligus. Parasitology International 63: 69–79. 10.1016/j.parint.2013.09.005 [DOI] [PubMed] [Google Scholar]
  52. Muñoz G, Cribb TH. (2005) Infracommunity structure of parasites of Hemigymnusmelapterus (pisces: labridae) from lizard island, australia: the importance of Habitat and parasite body size. Journal of Parasitology 91(1): 38–44. 10.1645/GE-3321 [DOI] [PubMed] [Google Scholar]
  53. Muñoz G, Cribb TH. (2006) Parasite communities and diet of Corisbatuensis (Pisces: Labridae) from Lizard Island, Great Barrier Reef. Memoirs of the Queensland Museum 52: 191–198. [Google Scholar]
  54. Ogawa K. (1991) Ectoparasites of sawfish, Pristismicrodon, caught in fresh waters of Australia and Papua New Guinea. University Museum, University of Tokyo, Nature and Culture 3: 91–101. [Google Scholar]
  55. Palm HW, Bray RA. (2014) Marine Fish Parasitology in Hawaii. Westarp and Partner Digitaldruck, Hohenwarsleben XII, Germany, 320 pp. [Google Scholar]
  56. Pillai NK. (1961) Copepods parasitic on South Indian Fishes. Part I, Caligidae. Bulletin of the Research Institute, University of Kerala (C) 8: 87–130. [Google Scholar]
  57. Pillai NK. (1963) Copepods parasitic on South Indian fishes: Family Caligidae. Journal of the Marine Biological Association of India 5(1): 68–96. [Google Scholar]
  58. Pillai NK. (1968) Additions to the copepod parasites of South Indian fishes. Parasitology 58: 9–36. 10.1017/S0031182000073388 [DOI] [PubMed] [Google Scholar]
  59. Pillai NK. (1985) Parasitic copepods of Marine fishes. The Fauna of India. Zoological Survey of India, Calcutta, 900.
  60. Prabha C, Pillai NK. (1986) Additions to the copepods parasitic on the marine fishes of India. 4. on twenty-six species of Caligidae. Records of the Zoological Survey of India 79: 1–139. [Google Scholar]
  61. Rangnekar MP. (1984) Parasitic copepods from marine fishes of Bombay. In: Vervoort W. (Ed.) Studies on Copepoda II. Proceedings of the First International Conference on Copepoda, Amsterdam, The Netherlands, 24–28 August 1981.Crustaceana 7: 344–351.
  62. Sandin SA, Smith JE, DeMartini EE, Dinsdale EA, Donner SD, Friedlander AM, Konotchick T, Malay M, Maragos JE, Obura D, Pantos O, Paulay G, Richie M, Rohwer F, Schroeder RE, Walsh S, Jackson JBC, Knowlton N, Sala E. (2008) Baselines and Degradation of Coral Reefs in the Northern Line Islands. PLoS One 3(2): 1548 10.1371/journal.pone.0001548 [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Shiino SM. (1954) Copepods parasitic on Japanese fishes 3. On two new species of the genus Anuretes. Report of Faculty of Fisheries 1: 260–272. [Google Scholar]
  64. Shiino SM. (1960) Copepods parasitic on the fishes collected on the coast of Province Shima, Japan. Reports of the Faculty of Fisheries, Prefectural University of Mie 3(3): 471–500. [Google Scholar]
  65. Spalding MD, Fox HE, Allen GR, Davidson N, Ferdaña ZA, Finlayson M, Halpern BS, Jorge MA, Lombana A, Lourie SA, Martin KD, McManus E, Molnar J, Recchia CA, Robertson J. (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. BioScience 57: 573–583. 10.1641/B570707 [DOI] [Google Scholar]
  66. Suárez-Morales E, Gasca RA. (2012) New Lepeophtheirus (Copepoda: Siphonostomatoida: Caligidae) from Isla del Coco National Park, Costa Rica, Eastern Tropical Pacific. Revista de Biología Tropical 60: 235–242. [Google Scholar]
  67. Tang D, Kalman JE. (2005) A new caligiform copepod (Siphonostomatoida: Dissonidae) parasitic on Seriolahippos from western Australian waters, with new records and morphological variation for Dissonusnudiventris and Dissonussimilis and an updated key to the species of Dissonus. Journal of Parasitology 91: 427–437. 10.1645/GE-3370 [DOI] [PubMed] [Google Scholar]
  68. Uyeno D, Nagasawa K. (2013) The genus Hatschekia (Copepoda: Hatschekiidae) from pufferfishes (Tetraodontiformes: Tetraodontidae) off the Ryukyu Islands, Japan, with descriptions of four new species and a redescription of H.pholas. Folia Parasitologica 60: 61–74. 10.14411/fp.2013.008 [DOI] [PubMed] [Google Scholar]
  69. Venmathi-Maran BA, Moon SY, Adday TK, Khamees NR, Myoung JG. (2014) A new species of parasitic copepod Nothobomolochus and redescription of Orbitacolaxhapalogenyos (Yamaguti & Yamasu, 1959) (Cyclopoida: Bomolochidae) off Iraq. Acta Parasitologica 59: 675–685. [DOI] [PubMed] [Google Scholar]
  70. Vidal-Martínez VM, Aguirre-Macedo ML, McLaughlin JP, Hechinger RF, Jaramillo AG, Shaw JC, James AK, Kuris AM, Lafferty KD. (2012) Digenean metacercariae of fishes from the lagoon flats of Palmyra Atoll, Eastern Indo-Pacific. Journal of Helminthology 5: 1–17. 10.1017/S0022149X11000526 [DOI] [PubMed] [Google Scholar]
  71. Vidal-Martínez VM, Soler-Jiménez LC, Aguirre-Macedo ML, McLaughlin J, Jaramillo AG, Shaw JC, James A, Hechinger RF, Kuris AM, Lafferty KD. (2017) Monogenea of fishes from the lagoon flats of Palmyra Atoll in the Central Pacific. ZooKeys 713: 1–23. 10.3897/zookeys.713.14732 [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Walter TC, Boxshall G. (2018) World of Copepods database. http://www.marinespecies.org/copepoda [2018-10-02]
  73. Wilson CB. (1905) North American parasitic copepods belonging to the family Caligidae, part I: the Caliginae. Proceedings of the United States National Museum 28: 479–672. 10.5479/si.00963801.28-1404.479 [DOI] [Google Scholar]
  74. Wilson C.B. (1906) Report on some parasitic Copepoda collected by Professor Herdman, at Ceylon, in 1902. In: Herdman WA (Ed.) Report to the Government of Ceylon on the Pearl Oyster Fisheries of the Gulf of Manaar 5(34). 189–210.
  75. Wilson CB. (1913) Crustacean parasites of West Indian fishes and land crabs, with descriptions of new genera and species. Proceedings of the United States National Museum 44(1950): 189–227. 10.5479/si.00963801.44-1950.189 [DOI] [Google Scholar]
  76. Wilson CB. (1921) Report on the parasitic Copepoda collected during the survey of the Juan Fernandez Islands, 1916–1917. Natural History of the Juan Fernandez & Easter Islands 3: 69–74. [Google Scholar]
  77. Wilson CB. (1932) The copepods of the Woods Hole region, Massachusetts. Bulletin of the United States National Museum 158: 1–635. 10.5479/si.03629236.158.i [DOI] [Google Scholar]
  78. Yamaguti S. (1963) Parasitic Copepoda and Branchiura of fishes. New York: Interscience Publishers, 1104 pp.
  79. Yuniar AT, Palm HW, Walter T. (2007) Crustacean fish parasites from Segara Anakan Lagoon, Java, Indonesia. Parasitology Research 100: 1193–1204. 10.1007/s00436-006-0391-9 [DOI] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

XML Treatment for Orbitacolax williamsi
zookeys.833.30835-treatment1.xml (15KB, xml)
XML Treatment for Anuretes serratus
zookeys.833.30835-treatment2.xml (12.7KB, xml)
XML Treatment for Caligus confusus
zookeys.833.30835-treatment3.xml (24.3KB, xml)
XML Treatment for Caligus kapuhili
zookeys.833.30835-treatment4.xml (12.1KB, xml)
XML Treatment for Caligus laticaudus
zookeys.833.30835-treatment5.xml (19.7KB, xml)
XML Treatment for Caligus aff. mutabilis
zookeys.833.30835-treatment6.xml (29.4KB, xml)
XML Treatment for Caligus randalli
zookeys.833.30835-treatment7.xml (13.9KB, xml)
XML Treatment for Caligus
zookeys.833.30835-treatment8.xml (4.7KB, xml)
XML Treatment for Caritus serratus
zookeys.833.30835-treatment9.xml (8.5KB, xml)
XML Treatment for Lepeophtheirus lewisi
zookeys.833.30835-treatment10.xml (13.6KB, xml)
XML Treatment for Lepeophtheirus uluus
zookeys.833.30835-treatment11.xml (10.2KB, xml)
XML Treatment for Dissonus similis
zookeys.833.30835-treatment12.xml (15.9KB, xml)
XML Treatment for Nemesis
zookeys.833.30835-treatment13.xml (9KB, xml)
XML Treatment for Hatschekia longiabdominalis
zookeys.833.30835-treatment14.xml (7.7KB, xml)
XML Treatment for Hatschekia bicaudata
zookeys.833.30835-treatment15.xml (9.7KB, xml)
XML Treatment for Kroyeria longicauda
zookeys.833.30835-treatment16.xml (7.7KB, xml)
XML Treatment for Lernanthropus
zookeys.833.30835-treatment17.xml (6.4KB, xml)

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