Caligus undulatus

Caligus undulatus: cosmopolitan pelagic caligid

Caligus undulatus was first described by Shen & Li (1959) from coastal plankton samples of Qingdao (Tsingtao) Harbour, eastern China. Subsequent pelagic records of this species came from India (Pillai 1966), Brazil (Montú 1982), Japan, Korea (Venmathi Maran & Ohtsuka 2008; Venmathi Maran unpubl. data) and Mexico (Suárez- Morales et al. 2012a). Generally, caligid females are larger than males, but in C. undulatus, males have a much larger body size than females; this unusual size sexual dimorphism remained unnoticed until the recent discovery of the species in Korean waters (Moon et al. unpubl. data).

The adult female of C. undulatus from Korea is larger (4.46 mm) (Moon et al. unpubl. data) than previously reported specimens (Shen & Li 1959; Venmathi Maran & Ohtsuka 2008; Venmathi Maran et al. 2012a). The Korean adult male (4.61 mm) (Moon et al. unpubl. data) is much larger than specimens from China (3.08 mm) (Shen & Li 1959), India (3.50 mm) (Pillai 1966), Japan (3.50 mm), Korea (3.52 mm) (Venmathi Maran & Ohtsuka 2008) and Mexico (2.82 mm) (Suárez-Morales et al. 2012a). Its wide size range (2.82- 4.61 mm) might reflect the geographical variability of the species. This peculiar feature of larger males has been reported in ca. 20 caligid species (Ho & Lin 2004a).

Until now, all reports of C. undulatus were based on specimens collected from plankton samples (Shen & Li 1959; Pillai 1966, 1985; Venmathi Maran & Ohtsuka 2008; Suárez-Morales et al. 2012a; Venmathi Maran et al. 2012a, b) (Table 2), but it has not yet been recorded from a fish host. Since it has been sighted in widely separated geographic areas, it is conceivable that its fish host is highly migratory (Ho & Lin 2004b; Venmathi Maran & Ohtsuka 2008). The recent finding of C. undulatus (Moon et al. unpubl. data) is the second record of this species in Korean waters. A detailed parasitological survey of the fish hosts in this country but also in other East Asian countries (China, Japan, Philippines, Taiwan) is required to help understanding the host-parasite dynamics of this widespread caligid. Since C. undulatus is a common zooplankter in coastal waters around the world it could potentially serve as a good model to elucidate the caligid life cycle, even though its host is as yet unknown.

C. longiramus Venmathi Maran, Ohtsuka & Jitchum, 2012 ♀ Japan Venmathi Maran et al. (2012b) C. ogawai Venmathi Maran, Ohtsuka & Shang, 2012 ♀, ♂ Japan Venmathi Maran et al. (2012c) C. quadrigenitalis Venmathi Maran, Ohtsuka & Shang, ♀ Japan Venmathi Maran et al. (2012c) 2012

The family Caligidae currently comprises ca. 450 valid species (Dojiri & Ho 2013), but information on the complete life cycle is only available for 18 species of Caligus (13 species) and Lepeophtheirus (five species) (Dojiri & Ho 2013; Venmathi Maran et al. 2013). The life cycle comprises eight stages, including two free-living naupliar stages, one infective copepodid followed by either four chalimus stages and the adult (in Caligus) or two chalimus stages, two preadult stages and the adult (in Lepeophtheirus) (Venmathi Maran et al. 2013).

Upon location of a suitable host the infective copepodid attaches itself by means of a frontal filament. This structure is considered an evolutionary novelty exhibited by many siphonostomatoids associated with vertebrate (Piasecki & MacKinnon 1993) and invertebrate hosts (Ohtsuka et al. 2007). Traditionally, it was assumed that the filament remained permanently attached to the host during the chalimus phase. However, we found free-living chalimus stages in plankton samples, especially in areas adjacent to aquaculture facilities, and identified the developmental stages based solely on the morphology of the frontal filament. The number of extension lobes on the frontal filament of caligids are consistent with other features of the chalimus stages and can be used as a character to distinguish between successive stages (Huys 2014). In the Caligidae, the formation and development of the frontal filament during molting follows two different patterns, the multi-node type (found in Caligus) or the singlenode type (in Lepeophtheirus) (Ohtsuka et al. 2009). Several works have reported the presence of developmental stages (chalimi) of Lepeophtheirus salmonis (Krøyer, 1837) in plankton samples adjacent to aquaculture facilities in Europe (Copley et al. 2005; Costello et al. 1998a, b; Penston et al. 2004; 2011). A study by Hull et al. (1998) revealed that L. salmonis can easily transfer from one host individual to another. Adults of Caligus sclerotinosus were collected in plankton samples off aquaculture facilities in Japan (Venmathi & Ohtsuka 2008) and Korea (unpubl. data) while copepodids of L. elegans Gusev, 1951 were collected around aquaculture facilities in Korea (unpubl. data). These data confirm that developmental stages of caligids are frequently found in the plankton but the discovery of adults in the water column is less easily explainable.

This pattern might also be applicable to the life cycle of some species of the cyclopoid families Ergasilidae (Ohtsuka et al. 2004) and Lernaeidae (Piasecki et al. 2004), both which utilize freshwater and brackish-water fish hosts. In contrast to caligiforms, the ergasilid life cycle involves six copepodid stages, the final one being the adult. All adult males die after mating in the water column, whereas only postmated adult females remain permanently or temporarily attached to the hosts. This strategy explains the presence of adult females in the plankton. These freeswimming ergasilid females were misidentified as members of the planktonic genus Limnoncaea Kokubo, 1914 before its rejection as a valid taxon (Ohtsuka et al. 2004) (similar to the pandarid genus Nogaus; cf. Boxshall & Halsey 2004). These temporarily planktonic females tend to carry fewer eggs per egg sac compared to congeners which remain permanently attached to the host.

Modifications of the body and appendages occur in adults of some ergasilids and lernaeids, but not in these presumably planktonic taxa (Ohtsuka et al. 2004; Piasecki et al. 2004). Thus, pelagic adults are likely to be common in the life cycle of caligiform copepods but the adaptive benefits of free-living adults detached from their hosts needs to be studied through laboratory experiments (Venmathi Maran & Ohtsuka 2008; Venmathi Maran et al. 2012a).