Biodiversity Data Journal : Taxonomy & Inventories
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Taxonomy & Inventories
First record of Caligus dussumieri Rangnekar, 1957 (Copepoda, Siphonostomatoida, Caligidae) from Malaysia, with notes on caligids found from Malaysia and on host-specificity of caligids on lutjanid fishes
expand article infoNorshida Ismail, Yusuke Nishida§, Susumu Ohtsuka§,|, Geoff Boxshall, James P. Bernot#,¤
‡ Faculty of Bioresources and Food Industry, Universiti Sultan Zainal Abidin, 22200, Besut, Terengganu, Malaysia
§ Graduate School of Integrated Sciences for Life, Hiroshima University, 1-4-4 Kagamiyama, Higashi-Hiroshima, 739-8528, Hiroshima, Japan
| Blue Innovation Division, Seto Inland Sea Carbon Neutral Research Center, 5-8-1 Minato-machi, Takehara, 725-0024, Hiroshima, Japan
¶ Department of Life Sciences, The Natural History Museum, Cromwell Road, London SW7 5BD, UK., London, United Kingdom
# Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, 20560, Washington DC, United States of America
¤ Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, 06269, Connecticut, United States of America
Open Access

Abstract

Background

In total, 14 species of Caligus have been reported from Malaysia. Amongst them, four species are reported from lutjanid fishes.

New information

Caligus dussumieri Rangnekar, 1957 is reported from Malabar snapper, Lutjanus malabaricus, purchased from a local wet market in Terengganu, Peninsular Malaysia. This is the first record of this species in Malaysia and it is only the second species assigned to the bonito-group of the genus Caligus to be reported from Malaysia. A key to species of the bonito-group is presented herein. The list of caligids infecting lutjanid fishes and the geographical distributions plus the known hosts of members of the bonito-group of Caligus are discussed.

Keywords

Caligidae, Lutjanidae, bonito-species group, sea lice, identification key, geographic distribution, host list

Introduction

Parasitic copepods of the genus Caligus Müller, 1785 (Siphonostomatoida, Caligidae) are well known as pests that cause serious economic losses in the marine aquaculture and fisheries industries globally (Ho and Lin 2004, Johnson et al. 2004, Nagasawa 2013, Arriagada et al. 2019, Hemmingsen et al. 2020). Heavy infestation by caligids, especially in fish kept in captivity, often results in secondary infection and disease outbreaks (Johnson et al. 2004). Therefore, the taxonomy, ecology and physiology of sea lice are particularly important and intensively studied.

To date, 269 valid species of Caligus have been described from a wide diversity of fish hosts (Walter and Boxshall 2023). Despite the exceptional diversity of aquatic organisms in Malaysia with approximately 1,955 fish species recorded in FishBase (Froese and Pauly 2023), only 27 identified species of parasitic copepods have been reported (Arthur and Shariff 2015, Ohtsuka et al. 2020a, Yahaya et al. 2022, Venmathi Maran et al. 2022). Amongst these, 16 species belong to the family Caligidae, namely: Caligus chiastos Lin and Ho, 2003, C. clemensi Parker and Margolis, 1964, C. eleutheronemi Shen, 1957, C. epidemicus Hewitt, 1971, C. epinepheli Yamaguti, 1936, C. hirsutus Bassett-Smith, 1898 (as Parapetalus hirsutus Basset-Smith, 1898), C. kanagurta Pillai, 1961, C. laticaudus Shiino, 1960, C. longipedis Basset-Smith, 1898, C. minimus Otto, 1821, C. malabaricus Pillai, 1961, C. punctatus Shiino, 1955, C. torpedinis Heller, 1865 (as C. rotundigenitalis Yu, 1933), C. stromatei Krøyer, 1863 (as C. multispinosus Shen, 1957), Hermilius longicornis Basset-Smith, 1898 and H. pyreventris Heller, 1865 (Leong 1984, Leong 1985, Venmathi Maran et al. 2009, Khoa et al. 2019, Yahaya et al. 2022).

Seven species groups have been established within the genus Caligus: the bonito-, confusus-, diaphanus-, macarovi-, productus-, pseudrorhombi- and undulatus-groups (Boxshall 2018, Ohtsuka and Boxshall 2019, Ohtsuka et al. 2020b). The bonito-group can be recognised on the basis of the following features: well-developed inner setae on the distal exopodal segment of leg 1 and the presence of a row of robust denticles along the outer margin of the second endopodal segment of leg 2.

The fish genus Lutjanus Bloch, 1790 (Lutjanidae) plays an important role in fisheries and aquaculture in Malaysia. The lutjanid catch contributed about 5.3% of the overall marine fish catch in 2021 (DOFM 2021). Bakar et al. (2018) identified 17 species of Lutjanus from Malaysia. Amongst them, Lutjanus malabaricus (Bloch and Schneider, 1801), commonly known as Malabar snapper, is one of the economically important species as they are recorded in 10 fish landing facilities across Malaysia: in Kedah, Penang, Perak, Selangor, Johor, Terengganu, Kelantan and Sabah (DOFM 2021). To date, only one species of parasitic copepod (C. malabaricus) has been described, associated with L. malabaricus from Malaysia (Leong 1984).

We have conducted taxonomic studies on metazoan parasites on commercially important fish obtained in the fish markets in Terengganu since 2019 (Ohtsuka et al. 2020b, Nitta et al. 2022) and, in this paper, we report a new locality record for Caligus dussumieri Rangnekar, 1957 from Malabar snapper, Lutjanus malabaricus. This species is re-described herein and we present notes on Caligus species parasitic on Lutjanus around the world and on the host-specificity of members of the bonito-group.

Materials and methods

A single female specimen of Caligus dussumieri was found on the gills of L. malabaricus purchased from the fish landing facility of the Fisheries Development Authority of Malaysia (LKIM) Complex Pulau Kambing, located in Kuala Terengganu, Terengganu State, Malaysia on 19 October 2019. The fish host was purchased dead and brought back to be examined for parasites in the Aquatic Laboratory, Faculty of Bioresources and Food Industry, University Sultan Zainal Abidin Besut Campus. The body surface, head and gills of the host were examined for parasites. Parasite specimens were fixed in 70% ethanol until identification. The copepod specimen was immersed in lactophenol and examined using the Humes and Gooding (1964) slide method, on a differential interference microscope (BX-53, Olympus Co., Ltd.), equipped with a drawing tube. The body length was measured from the frontal margin of the cephalothorax to the posterior margin of the caudal ramus excluding the caudal setae. The specimen is deposited at the South China Sea Repository and Reference Center, Universiti Malaysia Terengganu, Malaysia (UMTCrus 1645). A second specimen of C. dussumieri from the Natural History Museum, London (Reg. No. NHMUK 2022.189–197), fixed in 70% ethanol and collected from L. johnii from the Ord River, Camden Sound, Western Australia on 11 September 2013, was also examined. It was cleared in lactophenol on a glass cavity slide and examined with light microscopy using a Leitz Diaplan microscope, equipped with differential interference contrast and with confocal laser scanning microscopy (CLSM) as detailed below. Terminology of adults and developmental stages follows Huys and Boxshall (1991), Ho and Lin (2004) and Piasecki et al. (2023).

Confocal Laser Scanning Microscopy

One female of Caligus dussumieri (NHMUK 2022.189–197) was examined using CLSM. The specimen was stained overnight in a saturated solution of Congo Red in 100% ethanol, then rinsed in distilled water until no Congo Red could be seen diffusing and prepared as a temporary mount in a 50% solution of glycerine and distilled water on a glass slide under a coverslip. The specimen was examined using a Leica TCS SP5, equipped with a Leica DM5000 B upright microscope and the Leica Application Suite Advanced Fluorescence software LAS AF 2.2.1. (Leica, Wetzlar, Germany). We used a 561 nm excitation wavelength from a DPSS 10 mW 561 nm laser set at 80% power and collected the emitted fluorescence in two channels: 570–630 nm artificially coloured green and 630–715 nm artificially coloured red. A series of image stacks were collected and the final images were obtained by maximum projection of the overlaid channels using the same Leica software. For the full-body dorsal and ventral images, multiple fields of view were combined using Adobe Photoshop v.25.1.

Taxon treatment

Caligus dussumieri Rangnekar, 1957

Nomenclature

Sinocaligus dussumieri (Rangnekar, 1957)

Pseudopetalus dussumieri (Rangnekar, 1957)

Caligus rivulatus (Pilla, Vankara and Chikkam, 2012)

Materials   Download as CSV 
  1. scientificName:
    Caligus dussumieri Rangnekar, 1957
    ; originalNameUsage:
    Caligus dussumieri Rangnekar, 1957
    ; taxonomicStatus:
    Accepted
    ; taxonID:
    349612 (urn:lsid:marinespecies.org:taxname:349612)
    ; parentNameUsage:
    Caligus Müller O.F., 1785
    ; kingdom:
    Animalia
    ; phylum:
    Arthropoda
    ; class:
    Copepoda
    ; order:
    Siphonostomatoida
    ; family:
    Caligidae
    ; genus:
    Caligus
    ; specificEpithet:
    dussumieri
    ; scientificNameAuthorship:
    Rangnekar, 1957
    ; higherGeography:
    South East Asia
    ; continent:
    Asia
    ; waterBody:
    South China Sea
    ; country:
    Malaysia
    ; stateProvince:
    Terengganu
    ; county:
    Kuala Terengganu
    ; verbatimLocality:
    LKIM Pulau Kambing
    ; verbatimCoordinates:
    5°19'N 103°7' 43.7"E
    ; verbatimLatitude:
    5.321971
    ; verbatimLongitude:
    103.1288
    ; samplingProtocol:
    Gill wash
    ; year:
    2019
    ; month:
    10
    ; day:
    19
    ; identificationID:
    urn:lsid:marinespecies.org:taxname:349612
    ; occurrenceID:
    A71C4FDE-7825-5C4B-9023-C44E1AC10847
  2. scientificName:
    Caligus dussumieri Rangnekar, 1957
    ; originalNameUsage:
    Caligus dussumieri Rangnekar, 1957
    ; taxonomicStatus:
    Accepted
    ; taxonID:
    349612 (urn:lsid:marinespecies.org:taxname:349612)
    ; parentNameUsage:
    Caligus Müller O.F., 1785
    ; kingdom:
    Animalia
    ; phylum:
    Arthropoda
    ; class:
    Copepoda
    ; order:
    Siphonostomatoida
    ; family:
    Caligidae
    ; genus:
    Caligus
    ; specificEpithet:
    dussumieri
    ; scientificNameAuthorship:
    Rangnekar, 1957
    ; higherGeography:
    Australia
    ; continent:
    Australia
    ; country:
    Australia
    ; county:
    Camden Sound
    ; locality:
    Western Australia
    ; verbatimCoordinates:
    16° 11.52’S 124° 32.52’E
    ; year:
    2013
    ; month:
    9
    ; day:
    11
    ; identificationID:
    urn:lsid:marinespecies.org:taxname:349612
    ; institutionCode:
    NHMUK
    ; collectionCode:
    Reg. Nos. 2022.189-197
    ; occurrenceID:
    ADE72616-49DB-57BB-89BA-3948143646FA

Description

Fig. 1

Figure 1.  

Caligus dussumieri Rangnekar, 1957, adult female.

A Habitus, dorsal view; B Antennule; C Antenna; D Mandible; E Maxilla; F Maxilliped; G Sternal furca.

Female. Body (Fig. 1A) 3.24 mm long, excluding setae on caudal ramus. Dorsal cephalothoracic shield subcircular, slightly longer than wide. 1.31 x 1.12 mm, excluding hyaline membrane along lateral margins. Shield tapering anteriorly; with large, conspicuous lunules. Fourth pediger wider than long, incompletely fused to genital complex. Genital complex about 1.96 times longer than wide with neck-like narrow part anteriorly and barrel-shaped posterior region. Leg 5 (Fig. 1A) represented by 1 plumose, outer protopodal seta and 2 plumose setae on exopodal papilla located on posterolateral margin of genital complex. Abdomen 1-segmented, about 2.8 times longer than wide. Caudal ramus (Fig. 2C) oval, 0.10 x 0.07 mm, expanded inwards distally; armed with 3 short and 3 long plumose setae and ornamented with row of setules along distomedial margin.

Figure 2.  

CLSM images of Caligus dussumieri Rangnekar, 1957.

A Exopod of leg 1, showing spinular ornamentation on plumose setae along posterior margin; B Rami of leg 2 showing ornamentation on outer margin of endopod and spatulate spine on first exopodal segment.

Australian female observed using CLSM (Fig. 3A, B) showing differential degree of staining over body surface. Dorsal cephalothoracic shield staining moderately and evenly, with heavier uptake of stain marking sutures anteriorly near origin of antennules, in area near eyes and along lateral edges of central thoracic zone of shield. Ventral curved rib marking boundary of cephalosome and incorporated first pediger strongly stained. Fourth pediger and fourth leg staining evenly. Genital complex and abdomen displaying marked differences in intensity of staining. Staining intense in small ovoid patch on dorsal surface of genital complex towards the posterior end, ventrally around the genital apertures and in the posterior part of the abdomen. Conversely, staining very light in other areas of genital complex and anterior part of abdomen.

Figure 3.  

CLSM images of Caligus dussumieri Rangnekar, 1957.

A dorsal view; B ventral view.

Antennule (Fig. 1B) 2-segmented; proximal segment carrying 27 plumose setae on anterodistal surface, 25 setose plus 2 naked (on dorsal side) setae; distal segment short with 1 subterminal seta on posterior margin and 11 setae plus 2 aesthetascs around apex. Antenna (Fig. 1C) 3-segmented; proximal segment smallest, with short blunt process on posteromedial corner; middle segment subrectangular, unarmed; distal segment forming long, curved claw armed with stout proximal seta and simple middle seta. Postantennal process (Fig. 1C) shorter than distal segment, tine curved inwards with blunt tip, ornamented with 2 multisensillate papillae on basal region and another multisensillate papillae present on sternum adjacent to base of process. Additional lobate process present between postantennal process and base of antenna. Mandible (Fig. 1D) stylet-like, with 4 sections, bearing 12 teeth on medial margin of distal blade. Maxillule (Fig. 1C) comprising large stout dentiform process and basal papilla with 3 setae (1 short, 1 medium and 1 long). Maxilla (Fig. 1E) 2-segmented; lacertus large and unarmed; slender distal segment (brachium) bearing rounded membranous subapical flabellum on anterior margin and terminating in 2 subequal claw-like elements (calamus and canna). Calamus longer than canna, ornamented with strips of serrated membrane arranged obliquely around surface; canna ornamented with strips of serrated membrane bilaterally. Maxilliped (Fig. 1F) 3-segmented; proximal segment (corpus) largest, unarmed, 2 unequal processes along myxal area, longer than next 2 segments combined (subchela); middle segment unarmed; distal claw longer than shaft, sharply pointed with long seta at base of claw. Sternal furca (Fig. 1G) subrectangular, box with tiny rounded outgrowth anteriorly, tines blunt and weakly divergent.

Leg 1 (Fig. 4A, Fig. 2A) with 2 segmented protopod bearing 1 inner and 1 outer small plumose seta plus bifid setule on outer margin. Intercoxal sclerite slender, with 2 papillae each bearing a setule present on sternum posterior to sclerite. Vestigial endopod reduced to tiny, pointed process located near base of exopod. Exopod 2-segmented, first segment with row of fine setules along inner margin and spiniform seta at outer distal corner; second segment with 3 large plumose setae ornamented along outer margin with stout spinules at base becoming finer towards tip and with short plumosities along inner margin; 4 terminal elements, spine 1 simple, spines 2 and 3 each with accessory process (Fig. 4a), seta 4 longest, stout and pinnate on only one side. Leg 2 (Fig. 4B, Fig. 2B) with intercoxal sclerite ornamented with marginal membrane along posterior margin; coxa with large plumose seta at posterior corner and minute setule on anterior surface; basis ornamented with marginal membrane on both inner and medial margins, bearing minute seta at outer distal corner plus setule near mid-point of inner margin. Endopod 3-segmented: first segment armed with inner plumose seta and ornamented with large denticles at outer distal corner; second segment with 2 inner distal setae plus row of robust denticles along outer margin; third segment with 6 plumose setae. Exopod 3-segmented: first segment with reflexed membrane dorsally and with pecten at base of long, stout, outer spine with spatulate tip extending obliquely across surface of second and third segments; second segment with relatively short outer spine, third segment armed with 1 small and 1 medium outer spine (latter ornamented with extensive marginal membrane), longer distal spine ornamented with membrane on outer side and plumosities on inner side, plus 5 plumose setae. Leg 3 (Fig. 5A) apron (protopod) bearing small, plumose outer seta and long, plumose inner seta and ornamented with membrane along outer and posterior margins, 4 patches of spinules plus 2 setule-bearing papillae on either side of innermost patch, plus 2 relatively long setules near posterior margin. Endopod 2-segmented, proximal segment small, armed with 1 long plumose seta; segment expanded to form velum fringed with setules along free margin; second segment armed with 6 plumose setae. Exopod 3-segmented, proximal segment small, with pecten-like membrane on inner margin of segment and with an expanded outer distal corner ornamented with strip of membrane located lateral to outer spine plus minute setule on outer margin, outer distal spine slightly curved, not reaching distal border of second segment (Fig. 5a); second segment with inner plumose seta and outer naked spine; third segment with 3 setiform spines increasing in size distally plus 4 inner setae. Leg 4 (Fig. 5B) plumose seta at outer distal corner of protopodal segment; exopod distinctly 2-segmented, first exopodal segment with long outer spine; second segment with 4 spines along oblique outer distal margin; each spine with pecten at base (Fig. 5b).

Figure 4.  

Caligus dussumieri Rangnekar, 1957 adult female.

A Leg 1, a Four terminal elements of Leg 1; B Leg 2.

Figure 5.  

Caligus dussumieri Rangnekar, 1957, adult female.

A Leg 3, a Proximal segment of leg 3 exopod; B Leg 4, b Distal elements of Leg 4 second segment.

Taxon discussion

The initial description of C. dussumieri was provided by Rangnekar (1957). It was later transferred by Pillai (1968) to his new genus Pseudopetalus Pillai, 1968, as Pseudopetalus dussumieri, but was subsequently transferred to Sinocaligus Shen 1957 as Sinocaligus dussumieri after Pseudopetalus was recognised as a junior synonym of Sinocaligus (Boxshall and Montu 1997, Dojiri and Ho 2013). In a recent comprehensive revision by Boxshall and Barton (2023), the complex taxonomic history of C. dussumieri was thoroughly examined. They proposed to recognise Sinocaligus as a junior subjective synonym of Caligus and returned S. dussumieri to its original combination as C. dussumieri. Boxshall and Barton (2023) also recognised Caligus rivulatus Pilla, Vankara and Chikkam, 2012, described from Lutjanus rivulatus Cuvier, 1828 in Indian waters, as a junior subjective synonym of C. dussumieri. The Malaysian specimen was identified as a mature pre-metamorphic female due to the presence of elongated and slender genital complex and abdomen, which corresponds closely with the developmental stage described in the previous studies by Pilla et al. (2012) and Boxshall and Barton (2023). This particular specimen measured 3.24 mm in total length, a measurement consistent with the total length range of C. dussumieri, referred to as C. rivulatus by Pilla et al. (2012), ranging from 2.36 to 3.12 mm. Similarly, it exhibited a comparable total length to the Australian specimens, which measured between 3.05 and 3.65 mm.

In comparison to the recent re-description of C. dussumieri from Australian waters as provided by Boxshall and Barton (2023), the C. dussumieri specimens from Malaysia displayed subtle differences including the presence of a neck-like constriction in the anterior part of the genital complex and the more barrel-shaped genital complex, features also observed in C. dussumieri from Indian waters (Rangnekar 1957, Pillai 1967, Pilla et al. 2012). As discussed below, we consider these differences can be explained by the pre-metamorphic stage of development of these sets of specimens.

Another minor difference was noted regarding the postantennal process. In the current study, C. dussumieri possessed trisensillate papillae, consistent with the description of Pillai (1985), while the Australian specimens exhibited bisensillate papillae. In addition, a rounded, lobate process was present between the postantennal process and the base of the antenna in the Malaysian female. The female from Malaysia lacked the patch of small setules at the base of the inner protopodal seta of leg 1, present in the other specimens. Furthermore, the tips of spines 2 and 3 on the distal exopodal segment of leg 1 were ornamented with a row of serrations, distinguishing them from previously described specimens from India and Australia.

A pecten-like structure at the outer distal corner of the first exopodal segment of leg 3 was observed in the present specimen, but this feature was not illustrated in previous studies. However, this structure's presence in the Australian material was subsequently confirmed through additional observations of Australian specimens in this study.

Identification keys

Key to species of the bonito-group of Caligus based on adult females

An identification key distinguishing between species in the bonito-group of Caligus based on characteristics of adult females is provided following Yamaguti (1954), Shen (1957), Yamaguti and Yamasu (1959), Rangnekar and Murti (1960), Pillai (1961), Cressey and Cressey (1980), Pillai (1985), Byrnes (1987), Cressey (1991), Izawa (1995), Lin and Ho (2001), Ho and Lin (2004), Suarez-Morales et al. (2008), Morales-Serna et al. (2014), Boxshall (2018), Kamanli (2020) and Boxshall and Barton (2023).

1 First abdominal somite grossly enlarged, wider than genital complex 2
Abdomen typically slender, rarely enlarged, but never wider than genital complex 4
2 Plumose setae on posterior margin of distal exopodal segment of leg 1 well developed (at least as long as distal spine 3) Caligus timorensis Izawa, 1995
Plumose setae on posterior margin of distal exopodal segment of leg 1 vestigial (shorter than distal margin spine 3) 3
3 Abdomen large, peach-shaped, only slightly longer than broad, with deep postero-median lobes Caligus caudatus Gnanamuthu, 1950
Abdomen elongate, tapering anteriorly and posteriorly, approximately 2.4 times longer than wide, lacking postero-median lobes Caligus formicoides Redkar, Rangnekar and Murti, 1949
4 Abdomen enlarged, about as wide as cephalothorax, but slightly narrower than genital complex; sternal furca absent Caligus grandiabdominalis Yamaguti, 1954
Abdomen distinctly narrower than cephalothorax and genital complex; sternal furca present 5
5 Genital complex with well-developed posterolateral lobes, extending to middle of abdomen; first exopodal segment of leg 4 with projecting triangular outer margin Caligus infestans Heller, 1865
Genital complex without posterolateral lobes or with lobes not reaching middle of abdomen; first exopodal segment of leg 4 with linear outer margin 6
6 Abdomen short, about as wide as long and less than half length of genital complex Caligus asymmetricus Kabata, 1965
Abdomen distinctly longer than wide (at least 1.5 times) and at least half length of genital complex 7
7 Leg 4 with conspicuous ornamentation of denticles on surface of first exopodal segment Caligus pauliani Nuñes-Ruivo & Fourmanoir, 1956
Leg 4 typically with single setule on margin of first exopodal segment, but lacking ornamentation of denticles on surface of segment 8
8 Leg 2 with outer spine on first exopodal segment very elongate with spatulate tip Caligus dussumieri Rangnekar, 1957
Leg 2 with outer spine on first exopodal segment typical, tapering towards tip 9
9 Abdomen at most about 2.5 times longer than wide 10
Abdomen at least 3 times longer than wide 16
10 Postantennal process reduced (lacking defined tine) Caligus phipsoni Basset-Smith 1898
Postantennal process with typical curved tine 11
11 Pair of triangular accessory processes present on body surface either side of sternal furca Caligus hoplognathi Yamaguti and Yamasu, 1959
Sternal furca lacking associated accessory processes on adjacent body surface 12
12 Genital complex as long as abdomen, with prominent posterolateral lobes Caligus bonito C. B. Wilson, 1905
Genital complex at least 1.3 times longer than abdomen, lacking distinct posterolateral lobes 13
13 Abdomen 2-segmented 14
Abdomen 1-segmented 15
14 First abdominal somite more than twice as long as small second (anal) somite Caligus malabaricus Pillai, 1961
Both abdominal somites about equal in width and length Caligus cossackii Bassett-Smith, 1898
15 Patches of fine spinules present posteriorly on ventral surface of abdomen Caligus mutabilis Wilson, 1905
Ventral surface of abdomen lacking patches of fine spinules posteriorly Caligus triabdominalis Byrnes, 1987
16 Abdomen longer than or about as long as genital complex, distinct indentation between longer and wider anterior part and small posterior region. Caligus quadratus Shiino, 1954
Genital complex at least 1.3 times longer than abdomen, no distinct indentation between posterior and anterior regions 17
17 Antenna with small, blunt posterior process on proximal segment 18
Antenna with small, pointed posterior process on proximal segment Caligus omissus Cressey and Cressey, 1980
18 Abdomen 1-segmented 19
Abdomen 2-segmented, second (anal) somite slightly longer than first abdominal somite Caligus tenuifurcatus Wilson, 1937
19 Total body length less than 3 mm; small chitinous process present between antenna and postantennal process Caligus chamelensis Morales-Serna, Pinacho-Pinacho, Gómez and Pérez-Ponce de León, 2014
Total body length more than 3 mm; lacking any chitinous process between antenna and postantennal process Caligus asperimanus Pearse, 1951

Discussion

In this present study, the genital complex and abdomen of the adult female examined using CLSM displayed differential intensity of staining. It is possible that this differential intensity of staining is an artefact, but we infer that the staining intensity indicates a difference in the properties of the cuticle. The stained specimen is an adult female immediately prior to the post-mating metamorphosis (see Boxshall and Barton (2023)) which involves marked lateral expansion and lengthening of the genital complex and the abdomen resulting in the development of the habitus shown for fully mature C. dussumieiri by Pillai (1985). The areas which undergo maximum expansion are the genital complex and anterior abdomen. The posteriormost part of the abdomen, corresponding to the anal somite, does not undergo expansion. It appears that the very lightly stained areas of cuticle correspond to the areas which undergo metamorphic expansion. The cuticle surrounding the genital apertures is heavily stained indicating that it is sufficiently rigid to enable the spermatophores to be deposited and attached securely during mating. It is probable that the area immediately around the genital apertures does not undergo any metamorphic transformation. Similarly, the patch of intensely stained cuticle on the dorsal surface at the rear end of the genital complex is located where the paired maxillipeds of the male might grasp the female during spermatophore transfer. This heavily-stained area might indicate another patch of more rigid cuticle that does not undergo change during the metamorphic expansion of the genital complex. Similar patterns of intensely stained patches were observed in the same regions on the dorsal and ventral surface of the genital complex in 14 other caligid species examined using CLSM and the same staining protocol (Bernot, unpublished), so this appears to be a general pattern and not just an artefact of staining in this specimen of Caligus dussumieri.

Host relationships

Caligus dussumieri has been observed to infect two distinct host families, the Lutjanidae and Dussumieriidae. The adult males, copepodid (including chalimus) stages and mated, but not fully metamorphosed adult females were found on Lutjanus johnii from Australian waters (Boxshall and Barton 2023) and L. rivulatus from Indian waters (Pilla et al. 2012). Our new Malaysian female at the same stage of development is from L. malabaricus. Fully matured females with the typical expanded genital complex and abdomen have been found on the dussumieriids Dussumieria acuta Valenciennes, 1847 and D. elopsoides Bleeker, 1849 (as D. hasseltii Bleeker) both in Indian waters (Rangnekar 1957, Pillai 1968).

Lutjanids are a group of fish with high commercial value due to their desirable taste, ability to reproduce in captivity and tolerance to a range of salinity regimes which allow them to thrive in various marine environments including estuaries and mangroves as well as the open sea (Ibarra-Castro and Duncan 2007). In the family Lutjanidae, Lutjanus is the most species rich genus, currently accommodating 73 species (Froese and Pauly 2023). Twenty-eight species of caligid copepods have been recorded so far from Lutjanus species. Amongst these are five species belonging to the bonito-group within Caligus, namely: C. asperimanus, C. bonito, C. irritans, C. mutabilis and C. tenuifurcatus (Table 1).

Table 1.

Caligid copepods recorded from the genus Lutjanus Bloch,1790.

Lutjanus fish host

Caligus species

Geographic distribution

References

Lutjanus analis (Cuvier, 1828)

Caligus asperimanus Pearse, 1951

Carrie Bow Cay, Belize

Cressey (1991)

Caligus asperimanus Pearse, 1951

Bahamas

Cressey (1991)

Caligus asperimanus Pearse, 1951

off the coast of Rio de Janeiro, Brazil.

Oliveira et al. (2020)

Caligus robustus Bassett-Smith, 1898

Mexico

Cressey (1991)

Lutjanus apodus Walbaum, 1792

Caligus asperimanus Pearse, 1956

Carrie Bow Cay, Belize

Cressey (1991)

Caligus atromaculatus Wilson, 1913

Venezuela

Lagarde (1991)

Caligus tenax Heller, 1865

Venezuela

Lagarde (1991)

Caligus robustus Bassett-Smith, 1898

Belize

Cressey (1991)

Caligus xystercus Cressey, 1991

Belize

Cressey (1991)

Lutjanus argentimaculatus Forsskål, 1775

Caligus epidemicus Hewitt, 1972

Philipines

Ho et al. (2004)

Caligus lutjani Ho, Lin and Chang, 2007

Taiwan

Ho et al. (2007)

Caligus quadratus Shiino, 1954

Taiwan

Ho et al. (2007)

Lutjanus argentiventris Peters, 1869

Caligus asperimanus Pearse, 1961

Manabí Coast, Ecuador

Morales-Serna et al. (2016)

Caligus diaphanus Nordmann, 1833

Jaramijó, Ecuador

Morales-Serna et al. (2015)

Caligus latigenitalis Shiino, 1954

Bahía de Chamela, Mexican Pacific

Morales-Serna et al. (2014)

Caligus latigenitalis Shiino, 1955

Jaramijó, Ecuador

Morales-Serna et al. (2015)

Caligus serratus Shiino, 1965

Mexican Pacific

Morales-Serna et al. (2012), Morales-Serna et al. (2014)

Caligus schistonyx Wilson, 1905

Jaramijó, Ecuador

Morales-Serna et al. (2015)

Caligus tenuifurcatus Wilson, 1937

Mexican Pacific

Suarez-Morales et al. (2008), Morales-Serna et al. (2012), Morales-Serna et al. (2015)

Lutjanus bohar Forsskål, 1775

Caligus lutjani

Taiwan

Ho et al. (2007)

Lutjanus colorado Jordan and Gilbert, 1882

Caligus sclerotinosus Roubal, Armitage and Rohde, 1983

Bahía de Chamela,Mexican Pacific

Morales-Serna et al. (2014)

Lutjanus erythropterus Bloch, 1790

Caligus chiastos

Malaysia

Muhd-Faizul et al. (2012)

Caligus clemensi

Penang, Malaysia

Yahaya et al. (2022)

Caligus torpedinis (as C. rotundigenitalis)

Malaysia

Venmathi Maran et al. (2009)

Lutjanus fulviflamma Forsskål, 1775

Caligus chiastos

Taiwan

Ho and Lin (2004)

Caligus chiastos

Moreton Bay, Australia

Boxshall (2018)

Caligus epidemicus

Moreton Bay, Australia

Boxshall (2018)

Lutjanus fulvus Forster, 1801

Caligus mutabilis

Palmyra Atoll, Central Pacific

Soler-Jimenez et al. (2019)

Lutjanus griseus Linnaeus, 1758

Caligus atromaculatus Wilson, 1913

Florida

Cressey and Nutter (1987)

Caligus bonito

Isla de Margarita,Venezuela

Fuentes Zambrano et al. (2003)

Caligus bonito

Gulf of Mexico

Ho and Lin (2004)

Caligus irritans Heller, 1869

Venezuela

Lagarde (1991)

Caligus wilsoni Delamare Deboutteville

and Nunes Ruivo, 1958

Charlotte Harbor, Florida

Cressey (1991)

Lutjanus guttatus Steindachner, 1869

Caligus diaphanus Nordmann, 1834

Jaramijó, Ecuador

Morales-Serna et al. (2016)

Caligus mutabilis

Mexican Pacific

Morales-Serna et al. (2012), Morales-Serna et al. (2014)

Caligus sclerotinosus

Bahía de Chamela,Mexican Pacific

Morales-Serna et al. (2015)

Lutjanus jocu Bloch and Schneider, 1801

Caligus asperimanus

Carrie Bow Cay, Belize

Cressey (1991)

Caligus asperimanus

off the coast of Rio de Janeiro, Brazil.

Oliveira et al. (2020)

Lutjanus johnii Bloch, 1792

Caligus asperimanus

India Coast

Pilla et al. (2012)

Caligus auriilus Boxhall and Barton, 2023

Australia

Boxshall and Barton (2023)

Caligus chiastos

Malaysia

Venmathi Maran et al. (2009)

Caligus dussumieri

Australia

Boxshall and Barton (2023)

Lutjanus monostigma Cuvier, 1828

Caligus mutabilis

Palmyra Atoll, Central Pacific

Soler-Jimenez et al. (2019)

Lutjanus malabaricus

Caligus malabaricus

Malacca Strait, Malaysia

Leong (1984)

Caligus torpedinis (as C. rotundigenitalis)

India

Pillai (1967)

Lutjanus novemfasciatus Gill, 1862

Caligus bonito

Mexican Pacific

Ho and Lin (2004), Morales-Serna et al. (2012)

Lutjanus peru Nichols and Murphy, 1922

Caligus mutabilis

Mexican Pacific

Morales-Serna et al. (2012), Morales-Serna et al. (2015)

Lutjanus peru Nichols & Murphy, 1922

Caligus diaphanus

Bahía de Chamela,Mexican Pacific

Morales-Serna et al. (2014)

Caligus sclerotinosus

Bahía de Chamela,Mexican Pacific

Morales-Serna et al. (2014)

Lutjanus rivulatus Cuvier, 1828

Caligus nengai Rangnekar, Rangnekar & Murti, 1953

Taiwan

Ho and Lin (2004)

Caligus dussumieri

India

Pilla et al. (2012)

Lutjanus russellii Bleeker, 1849

Caligus quadratus

Taiwan

Ho and Lin (2004)

Caligus torpedinis (as C. rotundigenitalis)

Taiwan

Ho and Lin (2004)

Caligus pagrosomi Yamaguti, 1939

Taiwan

Ho and Lin (2004)

Caligus laticaudus

Taiwan

Ho and Lin (2004)

Lutjanus synagris Linnaeus, 1758

Caligus asperimanus

off the coast of Rio de Janeiro, Brazil.

Oliveira et al. (2020)

Caligus asperimanus

Carrie Bow Cay, Belize

Cressey (1991)

Caligus atromaculatus

Venezuela

Lagarde (1991)

Caligus praetextus Bere, 1936

Charlotte Harbor, Florida

Cressey (1991)

Caligus rufimaculatus Wilson, 1905

Florida and the Gulf of Mexico

Cressey (1991)

Caligus praetextus

Belize; Florida

Bere (1936), Cressey (1991)

Lutjanus vitta Quoy and Gaimard, 1824

Caligus laticaudus

Taiwan

Ho and Lin (2004)

Caligus torpedinis (as C. rotundigenitalis)

Taiwan

Ho and Lin (2004)

Lutjanus vivanus Cuvier, 1828

Caligus asperimanus

off the coast of Rio de Janeiro, Brazil.

Oliveira et al. (2020)

Lutjanus spp.

Caligus productus Dana, 1852

Mexican Pacific

Morales-Serna et al. (2012)

Species of Caligus, belonging to the bonito-group, are known from a variety of lutjanid hosts around the world. Caligus asperimanus and C. mutabilis exhibit a broad distribution and host range, having been reported from up to seven different lutjanid hosts in different regions, including Belize (Cressey 1991), the Bahamas, Brazil (Oliveira et al. 2020) and India (Pilla et al. 2012). While about three-quarters of reports of species of the bonito-group infecting lutjanids originated from North and South America, four species have been documented as infecting commercially exploited lutjanids from Asia, including L. johnii recorded from the coast of India (Pilla et al. 2012), L. malabaricus from the Malacca Strait and Terengganu Coast, Malaysia (Leong 1984), L. argentimaculatus from the Philippines (Ho et al. 2004) and L. russellii from Taiwan (Ho and Lin 2004).

In Malaysia, out of the 20 species of fish previously reported to serve as hosts for caligid copepods, three species of lutjanids are known to collectively host four species of Caligus: Lutjanus erythropterus hosts C. chiastos and C. torpedinis; L. johnii hosts C. chiastos; and L. malabaricus hosts C. malabaricus (Venmathi Maran et al. 2009).

Caligus dussumieri is assigned to the bonito-group because of the presence of three plumose setae on the distal exopodal segment of leg 1 and a row of stout denticles along the outer margin of the second endopodal segment of leg 2 (Boxshall and Barton 2023). It also shares two additional characteristics common to members of this species group: a 3-segmented leg 4 with four spines on the second exopodal segment and the presence of a small blunt posterior process on the proximal segment of the antenna. The bonito-group is currently composed of 20 species: C. asperimanus Pearse, 1951, C. asymmetricus Kabata, 1965, C. bonito Wilson C.B., 1905, C. caudatus Gnanamuthu, 1950, C. chamelensis Morales-Serna, Pinacho-Pinacho, Gómez and Pérez-Ponce de León, 2014, C. cossacki Bassett-Smith, 1898, C. dussumieri Rangnekar, 1957, C. formicoides Redkar, Rangnekar & Murti, 1949, C. grandiabdominalis Yamaguti, 1954, C. hoplognathi Yamaguti and Yamasu, 1959, C. infestans Heller, 1865, C. malabaricus Pillai, 1961, C. mutabilis Wilson, 1905, C. omissus Cressey and Cressey 1980, C. pauliani Nuñes-Ruivo & Fourmanoir, 1956, C. phipsoni Basset-Smith 1898, C. quadratus Shiino, 1954, C. tenuifurcatus Wilson, 1937, C. timorensis Izawa, 1995, and C. triabdominalis Byrnes, 1987 (Boxshall 2018, Ohtsuka and Boxshall 2019, Kamanli 2020). Caligus dussumieri along with C. caudatus, C. formicoides and C. timorensis were recently added to bonito-group after the species were transferred from Sinocaligus to Caligus (Boxshall and Barton 2023).

Caligids from the bonito-group have been recorded from another 30 families of fish, of which eight families (Carangidae, Coryphaenidae, Hemiramphidae, Istiophoridae, Nematistiidae, Pomatomidae, Scombridae and Sphyraenidae) are generally known as pelagic fish and 21 families are demersal fish from families Ariidae, Balistidae, Caesionidae, Centropomidae, Embiotocidae, Ephippidae, Gerreidae, Haemulidae, Kyphosidae, Mugilidae, Mullidae, Oplegnathidae, Polynemidae, Pomacentridae. Rhinobatidae, Sciaenidae, Serranidae, Siganidae and Sparidae. However, they appear to predominantly parasitise members of the family Scombridae. The fact that they primarily infect pelagic fish, but also use many minor demersal fish as hosts may indicate a possible history of evolutionary host-switching from pelagic to demersal fish.

An interesting example of host-switching during development is known in C. pauliani (previously reported as C. biseriodentatus), which infects different hosts at different life stages. The adult females are known from the frigate tuna Auxis thazard Lacepède, 1800, while premetamorphic adults and copepodid stages characterised mainly by smaller size, slender genital somites and not bearing eggs, are known from a variety of host species belonging to the genus Scomberomorus Lacepède, 1801. This form of host-switching appears to involve mated females only given that both pre-metamorphic adult females and males occur on the first host, which is where mating takes place, while only the mated females are known from the second host where the metamorphic developmental changes are completed. Cressey and Cressey (1980) speculated that host-switching might have resulted from predatory activities of the host because A. thazard is known as a common and important prey item for many larger fishes (Frimodt 1995).

The bonito-group has a broad distribution in low to middle latitudes across all oceans, with a denser concentration in the Indo-Pacific. The distribution of species infecting Lutjanidae is primarily concentrated in low latitudes due to the abundance of lutjanid fish in tropical and subtropical areas, as indicated in Fig. 6. In Malaysia, two caligids belonging to the bonito-group (C. dussumieri and C. malabaricus) have been documented in association with two lutjanid fish species (present study and Leong (1984)). Notably, the exploration of caligid copepod diversity in neighbouring Southeast Asian countries has been limited, reflecting a broader scarcity of research on Caligidae in the region. In addition to Malaysia records, a total of five caligids species from the bonito-group have been identified from Southeast Asian countries. These include C. bonito from E. affinis and C. formicoides from D. elopsoides from Vietnam (Truong et al. 2022,) C. grandiabdominalis from Caesio cuning Bloch, 1791 in Indonesia (Yamaguti 1954), C. pauliani recorded from Scomberomorus spp. from Thailand, the Philippines and Indonesia (Cressey and Cressey 1980); and C. quadratus on Siganidae and Mullidae in the Philippines and Indonesia (Ho et al. 2004, Yuniar et al. 2007). This underscores the need for further investigations to improve our understanding of caligid copepod diversity and distribution in Southeast Asian waters.

Figure 6.  

Geographical distribution of species belonging to the bonito-group within Caligus.

Acknowledgements

We would like to express our sincere thanks to Mr Nik Ahmad Firdaus Nik Wan (ESERI, UniSZA) for helping in ArcGIS software for generating the map for this manuscript, Dr Ahmad Syazni Kamarudin and Miss Siti Nur Nadhirah for helping in sampling and support for this study, to Dr Danny Tang and reviewers for comments to improve this manuscript. This study was supported by a collaborative grant SRGS/2021/SRGS-IC/04 from Universiti Sultan Zainal Abidin, Malaysia (awarded to NI) and grants-in-aid of the JSPS (KAKENHI, No. 19H03032, awarded to S.O.; bilateral partnership program, No. JPJSBP120209924 awarded to S.O.). This material is based in part upon work supported by the NSF Postdoctoral Research Fellowships in Biology Program under Grant No. 2010898 to J.P.B.

References

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