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Parasitic copepods (Crustacea, Hexanauplia) on fishes from the lagoon flats of Palmyra Atoll, Central Pacific
expand article infoLilia C. Soler-Jiménez, F. Neptalí Morales-Serna§, Ma. Leopoldina Aguirre-Macedo|, John P. Mclaughlin|, Alejandra G. Jaramillo|, Jenny C. Shaw|, Anna K. James|, Ryan F. Hechinger|, Armand M. Kuris|, Kevin D. Lafferty|, Victor M. Vidal-Martínez|
‡ Unidad Mérida, Merida, Mexico
§ Unidad Académica Mazatlán en Acuicultura y Manejo Ambiental, Mazatlan, Mexico
| University of California, Santa Barbara, United States of America
¶ University of California, San Diego, United States of America
Open Access

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: Orbitacolax williamsi on Mulloidichthys flavolineatus; Anuretes serratus on Acanthurus xanthopterus; Caligus confusus on Carangoides ferdau, Carangoides orthogrammus, Caranx ignobilis, Caranx melampygus, and Caranx papuensis; Caligus kapuhili on Chaetodon auriga and Chaetodon lunula; Caligus laticaudus on Rhinecanthus aculeatus, Pseudobalistes flavimarginatus, M. flavolineatus, Upeneus taeniopterus, Chrysiptera glauca, and Epinephalus merra; Caligus mutabilis on Lutjanus fulvus and Lutjanus monostigma; Caligus randalli on C. ignobilis; Caligus sp. on L. fulvus; Caritus serratus on Chanos chanos; Lepeophtheirus lewisi on A. xanthopterus; Lepeophtheirus uluus on C. ignobilis; Dissonus similis on Arothron hispidus; Nemesis sp. on Carcharhinus melanopterus; Hatschekia longiabdominalis on A. hispidus; Hatschekia bicaudata on Chaetodon auriga and Chaetodon lunula; Kroyeria longicauda on C. melanopterus and Lernanthropus sp. on Kyphosus cinerascens. 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. Caranx ignobilis (Forsskål) was host to three copepod species, the most of any fish. Acanthurus xanthopterus Valenciennes, Carcharhinus melanopterus (Quoy & Gaimard), Chaetodon auriga Forsskål, Chaetodon lunula (Lacépède), Lutjanus fulvus (Forster), Mulloidichthys flavolineatus (Lacépède) and Arothron hispidus (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
Acanthurus triostegus (Linnaeus, 1758) Convict surgeonfish 50 0 27 10–18
Acanthurus xanthopterus Valenciennes, 1835 Yellowfin surgeonfish 20 2 70 20–40
Albulidae
Albula glossodonta (Forsskål, 1775) Roundjaw bonefish 24 0 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) Blackbar triggerfish 18 0 30 8–24
Belonidae
Platybelone argalus (Lesueur, 1821) Keeltail needlefish 2 0 50 9–36
Carangidae
Carangoides ferdau (Forsskål, 1775) Blue trevally 5 0 75 33–38
Carangoides orthogrammus (Jordan & Gilbert, 1882) Island trevally 3 0 75 25–35
Caranx ignobilis (Forsskål, 1775) Giant trevally 4 3 170 56–79
Caranx melampygus Cuvier, 1833 Bluefin trevally 6 2 117 31–66
Caranx papuensis Alleyne & MacLeay, 1877 Brassy trevally 5 2 88 12–41
Carcharhinidae
Carcharhinus melanopterus (Quoy & Gaimard, 1824) Blacktip reef shark 5 3 200 46–219
Chaetodontidae
Chaetodon auriga Forsskål, 1775 Threadfin butterflyfish 13 4 23 12–19
Chaetodon lunula (Lacepède, 1802) Raccoon butterflyfish 14 6 20 11–16
Chanidae
Chanos chanos (Forsskål, 1775) Milkfish 5 1 180 31–57
Gobiidae
Amblygobius phalaena (Valenciennes, 1837) Whitebarred goby 18 0 15 1.3–7
Asterropteryx semipunctata Rüppell, 1830 Starry goby 12 0 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 0 14 2–9
Hemiramphidae
Hemiramphus depauperatus Lay & Bennett, 1839 Tropical half-beak fish 20 0 40 20–34
Kiphosidae
Kyphosus cinerascens (Forsskål, 1775) Blue sea chub 2 1 50 35–38
Lutjanidae
Lutjanus fulvus (Forster, 1801) Blacktail snapper 26 5 40 7–26
Lutjanus monostigma (Cuvier, 1828) One spot snapper 6 1 60 17–37
Mugilidae
Crenimugil crenilabis (Forsskål, 1775) Fringelip mullet 42 0 60 8–45
Liza vaigiensis (Quoy & Gaimard, 1825) Squaretail mullet 54 0 63 3–32
Valamugil engeli (Bleeker, 1858) Kanda 63 0 30 1–20
Mullidae
Mulloidichthys flavolineatus (Lacepède, 1801) Yellowstripe goatfish 52 8 43 8–37
Upeneus taeniopterus Cuvier, 1829 Finstripe goatfish 5 3 33 1–30
Muraenidae
Gymnothorax pictus (Ahl, 1789) Paintspotted moray 7 0 140 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 0 23 14–20
Abudefduf sordidus (Forsskål, 1775) Blackspot sergeant 18 0 24 14–19
Chrysiptera glauca (Cuvier, 1830) Grey demoiselle 3 0 12 8–10
Stegastes nigricans (Lacepède, 1802) Dusky farmerfish 10 0 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 9 50 17–49
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

Order Cyclopoida Milne Edwards, 1840

Bomolochidae Claus, 1875

Orbitacolax Shen, 1957

Orbitacolax williamsi Cressey & Cressey, 1989

Type host

Scolopsis taenioptera (as S. dubiosus) (Cuvier) (Nemipteridae).

Other host and localities

Scolopsis taenioptera (as S. dubiosus) from Okinawa, Japan (Cressey and Cressey 1989). Coris batuensis (Bleeker) (Labridae) from Lizard Island, Australia (Muñoz and Cribb 2006). Thamnaconus degeni (Regan) (Monacanthidae) from South Australia (Hayward et al. 2011).

Current host

Mulloidichthys flavolineatus (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. Orbitacolax williamsi 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

Prionurus scalprum (as Xesurus scalprum) Valenciennes (Acanthuridae).

Other host and localities

Prionurus scalprum (as Xesurus scalprum) (Acanthuridae) from Seto, Wakayama Prefecture, Japan (Shiino 1954). Naso hexacanthus (Bleeker) (Acanthuridae) from Oahu, Hawaii (Lewis 1964a, Palm and Bray 2014); from Japan and India (Prabha and Pillai 1986). Prionurus microlepidotus Lacepède (Acanthuridae) from Australia (Boxshall 2018).

Current host

Acanthurus xanthopterus (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

Caranx ignobilis (as C. sansun) (Carangidae).

Other host and localities

Alepes djedaba (Forsskål) from Durban; Caranx caballus (Günther) and Caranx caninus (Günther) from Mexican Pacific and Ecuador; Caranx djedaba (Forsskål) from Durban, South Africa and Sri Lanka; Caranx hippos (Linnaeus) from Galapagos Islands and Panama; Caranx ignobilis from Taiwan, Indian and Australia; Caranx melampygus Cuvier from Eniwetok Atoll and Taiwan; Caranx sexfasciatus Quoy & Gaimard from South Africa, Taiwan, Indonesia and Australia; Caranx sp. from Celebes and New Caledonia (all Carangidae); Coryphaena hippurus Linnaeus (Coryphaenidae) from Galapagos Islands and Panama; Decapterus sp. (Carangidae) from Tonkin Gulf, Vietnam; Elagatis bipinnulata (Quoy & Gaimard) (Carangidae) from Galapagos Islands, Panama, India and Taiwan; Elagatis sp. from Celebes; Epinephelus tauvina (Forsskål) (Serranidae) from Kuwait; Rhabdosargus holubi (Steindachner) (Sparidae) from South Africa; Seriola dumerili (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

Carangoides ferdau (Forsskål), Carangoides orthogrammus (Jordan & Gilbert), Caranx ignobilis, Caranx melampygus and Caranx papuensis Alleyne & MacLeay (all Carangidae).

Site of infection

Gills.

Prevalence and mean intensity

40 and 2 (n = 5) to Carangoides ferdau, 33.3 and 6 (n = 3) to Carangoides orthogrammus, 75 and 12.7 ± 12.2 (n = 4) to Caranx ignobilis; 33.3 and 2 (n = 6) to Caranx melampygus; 40 and 4 (n = 5) to Caranx papuensis.

Specimens deposited

CHCM No. 562 (voucher) (1 vial, 1 specimen ♀) (from Caranx ignobilis), CHCM No. 563 (voucher) (1 vial, 2 specimens ♂ ♀) (from Caranx papuensis), USNM No. 1550598 (voucher) (1 vial, 1 specimen ♀) (from Caranx ignobilis).

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 Caligus productus (as Caligus alalongae) Dana, 1852 and Caligus constrictus 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

Chaetodon miliaris Quoy & Gaimard (Chaetodontidae).

Other host and localities

Chaetodon miliaris Quoy & Gaimard, Chaetodon fremblii Bennett from Hawaii (Lewis 1967, Palm and Bray 2014). Chaetodon auripes Jordan & Snyder and Chaetodon vagabundus Linnaeus from Taiwan (all Chaetodontidae) (Ho and Lin 2007).

Current host

Chaetodon auriga and Chaetodon lunula (Chaetodontidae).

Site of infection

Gills.

Prevalence and mean intensity

7.7 and 8 (n = 13) to Chaetodon auriga; 28.6 and 2.5 ± 1.7 (n = 14) to Chaetodon lunula.

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 Caligus laticaudus 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

Pagrus major (as Pagrosomus major) (Temminck & Schlegel) (Sparidae).

Other host and localities

Pagrus major (as Pagrosomus major) (Sparidae) from Japan (Shiino 1960). Acanthurus olivaceus Bloch & Schneider (Acanthuridae) from Eniwetok Atoll; Dentex tumifrons (Temminck & Schlegel) (Sparidae) from Korea; Liza haematocheila (Temminck & Schlegel) (Mugilidae) from China; Caranx melampygus (Carangidae), Lutjanus vitta (Quoy & Gaimard), Lutjanus russellii (Bleeker) (Lutjanidae) and Parapristipoma trilineatum (Thunberg) (Haemulidae), Polydactylus plebeius (Broussonet) and Polydactylus sextarius (Bloch & Schneider) (Polynemidae) from Taiwan; Parastomateus niger (Bloch) (Carangidae) from Malaysia; Filimanus heptadactyla (Cuvier) (Polynemidae) and Rhabdosargus sarba (Forsskål) (Sparidae) from India (Ho and Lin 2004, Moon and Kim 2012). Gnathanodon speciosus (Forsskål), Caranx sexfasciatus Quoy & Gaimard (Carangidae), Heniochus acuminatus (Linnaeus) (Chaetodontidae), Kyphosus bigibbus Lacepède (Kiphosidae), Pseudolabrus guentheri Bleeker (Labridae), Pagrus auratus (Forster) (Sparidae) from Australia (Boxshall 2018).

Current host

Rhinecanthus aculeatus (Linnaeus), Pseudobalistes flavimarginatus (Rüppell) (Balistidae), Mulloidichthys flavolineatus, Upeneus taeniopterus Cuvier (Mullidae), Chrysiptera glauca (Cuvier) (Pomacentridae) and Epinephalus merra Bloch (Serranidae).

Site of infection

Gills..

Prevalence and mean intensity

5.6 and 1 (n = 18) to Rhinecanthus aculeatus; 50 and 21 ± 26.9 (n = 4) to Pseudobalistes flavimarginatus; 13.5 and 1.5 ± 0.5 (n = 52) to Mulloidichthys flavolineatus; 60 and 2.7 ± 2.1 (n = 5) to Upeneus taeniopterus; 3.33 and 2 (n = 3) to Chrysiptera glauca; 50 and 1 (n = 2) to Epinephalus merra.

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

Centropristis striata (as Centropristes striatus) (Linnaeus) (Serranidae).

Other host and localities

Centropristis striata (as Centropristes striatus) (Serranidae) from North American waters (Wilson 1905). Acanthocybium sp., Euthynnus sp., Sarda sp., Scomberomorus sp., and Thunnus sp. (all Scombridae) from Colombia; Archosargus rhomboidalis (Linnaeus) (Sparidae), Chaetodipterus faber (Broussonet) (Ephippidae), Mycteroperca microlepis (Goode & Bean), Scomberomorus brasiliensis Collette, Russo & Zavala-Camin, Scomberomorus maculatus (Mitchill) (Scombridae) and Trachinotus goodei Jordan & Evermann (Carangidae) from Brazil; Balistes sp. (Balistidae), Calamus brachysomus (Lockington) (Sparidae), Centropomus sp. (Centropomidae), Chaetodipterus zonatus (Girard) (Ephippidae), Epinephelus labriformis (Jenyns) (Serranidae), Hoplopagrus guentherii Gill (Lutjanidae), Katsuwonus pelamis (Linnaeus) (Scombridae), Kyphosus elegans (Peters) (Kyphosidae), Lutjanus guttatus (Steindachner), Lutjanus peru (Nichols & Murphy) (Lutjanidae), Menticirrhus undulatus (Girard) (Sciaenidae), Microlepidotus brevipinnis (Steindachner) (Haemulidae), Mugil cephalus (Linnaeus) (Mugilidae), Paralabrax clathratus (Girard), Paralabrax maculatofasciatus (Steindachner), Paralabrax nebulifer (Girard) (all Serranidae), Sarda chiliensis (Cuvier), Scomberomorus sierra Jordan & Starks (Scombridae) and Selene orstedii Lütken (Carangidae) from Mexican Pacific; S. brasiliensis from Costa Rica; Scomberomorus cavalla (Cuvier) (Scombridae) from Surinam; S. maculatus from Florida; Scomberomorus japonicus from Campeche (Gulf of Mexico); E. labriformis, Eucinostomus entomelas Zahuranec (Gerreidae), Haemulopsis axillaris (Steindachner) (Haemulidae), Paralabrax callaensis Starks (Serranidae), Chromis cyanea (Poey) and Chromis multilineata (Guichenot) (Pomacentridae) from Ecuador (Cressey and Cressey 1980, Luque and Tavares 2007, Gomes-Sanches et al. 2012, Morales-Serna et al. 2016).

Current hosts

Lutjanus fulvus and Lutjanus monostigma (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

Acanthurus triostegus (Linnaeus) (Acanthuridae).

Other host and localities

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

Current host

Caranx ignobilis (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 Caligus randalli 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 Caligus aesopus 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. Caligus randalli 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

Lutjanus fulvus (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 Caligus laticaudus, 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:

Chanos chanos (Forsskål) (Chanidae).

Other host and localities

Chanos chanos (Chanidae) from Nosy Bé, Madagascar (Cressey 1967). Reported as Caritus tolii from Tenualosa toli (as Hilsa toli) (Valenciennes) (Clupeidae) from Sassoon Docks, Bombay (Rangnekar 1984).

Current host

Chanos chanos (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

Acanthurus olivaceus (Acanthuridae).

Other host and localities

Acanthurus olivaceus (Acanthuridae) from Hawaii (Hewitt 1971). Naso hexacanthus (Bleeker), Acanthurus triostegus (Acanthuridae), Myripristis sp., Fistularia petimba Lacepède (Fistulariidae) (Lewis 1964a, 1964b, Palm and Bray 2014).

Current host

Acanthurus xanthopterus (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

Lepeophtheirus lewisi was originally described as Dentigryps bifurcatus 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. bifurcatus Wilson 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

Caranx melampygus (Carangidae).

Other host and localities

Caranx melampygus (Carangidae) from Oahu, Hawaii (Lewis 1964b, Palm and Bray 2014). Reported as Dentigryps ulua on Caranx ignobilis from Heron Island, Australia (Ho and Dojiri 1977).

Current host

Caranx ignobilis (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

Lepeophtheirus uluus was originally described as Dentigryps ulua 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

Tetractenos hamiltoni (Richardson) (as Spheroides hamiltoni) (Tetraodontidae).

Other host and localities

Tetractenos hamiltoni (as Spheroides hamiltoni) (Tetraodontidae) from Queensland, Australia (Kabata 1966). Arothron hispidus from Philippines; Arothron meleagris (Anonymous) from Guam; Arothron nigropunctatus (Bloch & Schneider) from Australia, Philippines and New Guinea; and Arothron stellatus (Anonymous) (all Tetraodontidae) from New Guinea (Tang and Kalman 2005).

Current host

Arothron hispidus (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

Carcharhinus melanopterus (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

Arothron hispidus (Tetraodontidae).

Other host and localities

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

Current host

Arothron hispidus (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

Chaetodon aureofasciatus Macleay (Chaetodontidae).

Other host and localities

Chaetodon aureofasciatus (Chaetodontidae) from Australia (Kabata 1991). Chaetodon auripes Jordan & Snyder (Chaetodontidae) from Seto, Wakayama Prefecture, Japan (Izawa 2016).

Current host

Chaetodon auriga and Chaetodon lunula (Chaetodontidae).

Site of infection

Gills.

Prevalence and mean intensity

23.1 and 7.3 ± 3.1 (n = 13) to Chaetodon auriga; 14.3 and 5 ± 1.4 (n = 14) to Chaetodon lunula.

Specimens deposited

CHCM No. 577 (voucher) (1 vial, 1 specimen ♀) (from Chaetodon auriga). CHCM No. 578 (voucher) (1 vial, 1 specimen ♀) (from Chaetodon lunula). USNM No. 1550606 (voucher) (1 vial, 1 specimen ♀) (from Chaetodon lunula).

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

Carcharhinus limbatus (Müller & Henle) (Carcharhinidae).

Other host and localities

Carcharhinus limbatus (Carcharhinidae) from Florida. Carcharhinus brevipinna (Müller & Henle) (Carcharhinidae) from Madagascar (Deets 1994).

Current host

Carcharhinus melanopterus (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

Kyphosus cinerascens (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 Lutjanus monostigma 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. Acanthurus triostegus, n = 50). Several fishes that were unparasitized at Palmyra have copepod records at other sites. For example, Acanthurus triostegus, Gymnothorax pictus, Epinephelus merra and Sphyraena barracuda 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 (Chanos chanos) or small individuals (Sphyraena barracuda). 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.

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.

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