First record and redescription of Macandrewella cochinensis Gopalakrishnan, 1973 (Copepoda, Scolecitrichidae) from the Red Sea, with notes on swarm formation

Abstract During a study of the epipelagic zooplankton carried out near the fringing reef around Sharm El-Sheikh area, in the northern Red Sea, female and male specimens of the poorly known calanoid copepod Macandrewella cochinensis Gopalakrishnan, 1973 were collected. This is the first record of species occurrence in the Red Sea. Macandrewella cochinensis was previously known only from the offshore water of Cochin, south west of India. The Red Sea specimens are described in details herein to allow their comparison with the specimens from the type locality, because original description of M. cochinensis is incomplete and causes some taxonomic confusion. The most important characters that may have been overlooked in the original description are: shape of projections of the female distolateral prosomal borders, details of morphology of the asymmetrical female genital double-somite and presence of leg 5 in female.


Introduction
Members of the family Scolecitrichidae are distributed from pelagic to benthopelagic waters of the world oceans. The boundaries of the family Scolecitrichidae are not well defined as reported by Vyshkvartzeva (2001), Ohtsuka et al. (2003) and Boxshall and Halsey (2004). Boxshall and Halsey (2004) have considered this family to contain about 23-26 genera, however, less number of genera have been included in the family by Markhaseva and Ferrari (2005).
The genus Macandrewella Scott, 1909 belongs to the family Scolecitrichidae and has so far accommodated 12 nominal species (Razouls et al. 2013). The genus has hitherto been recorded exclusively from tropical and subtropical waters between 30°N and 20°S in the Indo-Pacific waters (Ohtsuka et al. 2002). Most members of the genus are hyperbenthic and have been collected from the near bottom samples on the continental shelves and slopes. Ohtsuka Nishida and Nakaguchi described in 2002 M. stygiana and M. omorii from the southern Japan from the near bottom at depth of 95-467 m. Farran (1936) collected three species (M. asymmetrica, M. mera and M. sewelli) from the Great Barrier Reef when a plankton net accidentally touched the bottom at a depth of 200 m. Macandrewella cochinensis described by Gopalakrishnan (1973) was found from 200 m to the surface, M. joanae was sampled by Scott (1909) from 1000 m to the surface. Other species were collected in vertical or surface plankton hauls where no exact depths of collection were specified (Ohtsuka et al. 2002). Ohtsuka et al. (2002) gave an excellent review and a key for all Macandrewella species recorded worldwide on the basis of shape of female genital double-somite, presence or absence of a female leg 5, the structure of the second and third exopodal segments of the male right leg 5 and the shape of the right endopod segment of the male leg 5.
Only one species M. chelipes Giesbrecht, 1896 has been recorded from the Red Sea (Giesbrecht 1896, Campaner 1989, El-Sherbiny 1997. During our plankton sampling in the Red Sea, another species of Macandrewella was first time found in swarms at surface waters. It is identified as M. cochinensis which up to now has only been recorded from the type locality off Cochin, south coast of India (10°10'N, 75°46'E). This paper describes Macandrewella cochinensis collected near a reef in a semi-enclosed small shallow bay in the northern Red Sea. Its habit of swarming in surface waters is also discussed.
Legs 1 to 4 biramous, with 3-segmented exopods; endopod 1-segmented in leg 1, 2-segmented in leg 2, 3-segmented in legs 3 and 4. Spines and setal formula are shown in Table 1. Leg 1 (Figs 5A-C) smallest, first exopodal segment with expanded medial margin bordered by naked lateral spinules (Fig. 5B), middle segment bearing lateral spine and medial seta, distal exopod segment with serrate spine and spiniform terminal seta; endopod bearing middle lateral knob with patch of fine setules terminally (Fig. 5C). Leg 2 (Fig. 5D) coxa and basis with pointed prominence on lateral margin; second exopodal segment with crescent-like row of spinules on posterior surface; third segment with middle patch of spinules posteriorly; first endopodal segment without any spinules; second endopodal segment bearing 6 acute spinules . Leg 3 (Fig. 5E) coxa with pointed prominence on lamellar lateral margin; basis with pointed process on medial distal corner; second exopodal segment with crescent-like row of spinules along distal margin, third segment with minute spinules distributed in curved row; second and third endopodal segments bearing 4 and 6 spinules, respectively. Leg 4 (Fig. 5F): second and third exopodal segments each bearing longitudinal row of stout spinules distributed as shown in Fig. 5F. Shape, number and distribution of spinules along second and third exopodal segment varies among individuals (Figs 5G,H).
Leg 5 (Fig. 5I) rudimentary, 2-segmented separated at base; each terminal segment cylindrical with medial papilla-like protrusion and constriction at one-third distal part (see also Fig. 3 F).
Mouth parts and legs 1-4 similar to those of female except fifth and sixth endopodal segment of maxilliped with longer setae (Fig. 5F) and third exopodal segment of leg 2 with different number and distribution of posterior surface setules (Fig. 5G).
Leg 5 (Figs 6H-K) elongated in general structure resembling that of the other species of the genus. Left leg (Fig. 6H) with coxa approximately as long as basis; basis with longitudinal keel-like structure along proximal half; exopod 2-segmented, second segment with lamellar plate covered with dense tuft of cilia and 2 elements terminally (Figs 6I, 7B); endopod one-segmented, shorter than exopod, bearing 2 medial triangular processes, one seta at tip and medially serrated margin (Fig. 6J). Right leg chelate (Fig. 6K); coxa with triangular expansion proximally; basis expanded laterally; first exopodal segment bearing 3 medial processes, one located proximally, middle irregular and distal somewhat triangular; second exopodal segment short, bearing internally directed process truncate curved at tip; third segment as long as previous segment, curved inward distally (Fig. 7B); endopod one-segmented, curved outward and recurved at tip, bearing round process distally and triangular process midway.

Density and abundance of swarm
The density of M. cochinensis (adult and copepodites) in the studied area was about 422 individuals m -3 . Adults constituted the major part of the swarm (72.5%), while copepodids consisted mainly of the fourth (CIV) and fifth (CV) stages, forming only 27.5%. Among adults, males show a slightly higher percentage in the population than females (38.1 and 34.4 % respectively). On the other hand, male copepodids (26.0%) outnumbered females (1.5%).

Discussion
Original description of Macandrewella cochinensis by Gopalakrishnan (1973) is not enough detailed and contain only brief data on Macandrewella key characters valuable in congeners identification (Ohtsuka et al. 2002), e.g. projections of the female posterior prosomal borders, type of genital double-somite asymmetry, and female leg 5 present, or absent. In general, morphological characters of Macandrewella specimens collected from the northern Red Sea correspond to M. cochinensis and they are currently attributed to this species. However, their taxonomic status is expected to be proved when additional specimens from the M. cochinensis type locality will be obtained.
Macandrewella cochinensis closely resembles M. stygiana Ohtsuka, Nishida & Nakaguchi 2002 in dorsolateral processes on the prosomal ends of the female serrated and in the left ventrolateral process of the prosomal border extending nearly posterior margin of the genital double-somite. However, M. cochinensis is readily distinguishable from M. stygiana in the following characteristics: 1) the second and third urosomites are nearly equal in length (second urosomite longer than third one in M. stygiana); 2) female caudal left seta V 1.5 times longer than right (more than 2 times longer in M. stygiana); 3) female leg 5 is cylindrical, composed of 2 segments with 1 medial process and a constriction on the distal third of the distal segment (more flattened in M. stygiana); 4) the lateral middle process of the right endopod of male leg 5 is larger (smaller); 5) the lack of a medial distal process of the second exopodal segment of male right leg 5 (present); 6) the distal exopodal segment of male right leg 5 is relatively narrower in M. cochinensis (broader in M. stygiana).
The female of M. cochinensis is also similar to that of M. joanae Scott 1909 collected from Halmahera Sea, Indonesian Archipelago, but can be distinguished by the presence of ventrolateral processes on the distal prosomal borders that reach nearly to the midlength of the genital double-somite; the genital operculum is wider than long; the left middle seta on the caudal ramus is nearly 1.5 times as long as the right one but shorter than in M. joanae; the terminal segment of the female leg 5 is more reduced than in M. joanae and has no terminal elements.
Swarm formation is known in coastal and deep-sea calanoid families such as Acartiidae, Calanidae, Centropagidae, Pontellidae, Pseudodiaptomidae, Ridgewayiidae, Spinocalanidae, Temoridae, and Tortanidae (e.g. Hamner and Carleton 1979, Fleminger 1983, Ueda et al. 1983, Mauchline 1998, Heidelberg et al. 2010. However these species except for the Spinocalanidae form multispecies assemblages (Fleminger 1983, Mauchline 1998, Ivanenko et al. 2007). This is the first record of the family Scolecitrichidae to form a monospecific aggregation. The adaptive meaning of copepods' swarming is interpreted as being possibly related to: (1) antipredation against visual predators; (2) reduction of dispersion by currents; (3) facilitating and enhancing mating opportunity; (4) keeping position to feed on coral mucus (Mauchline 1998); (5) positioning in the volcanic gases (Fleminger 1983, Ivanenko et al. 2007). In case of Macandrewella cochinensis, the dominance of adult and swarming position near the surface are peculiar, suggesting the likelihood of the above-mentioned first and third possibilities. Many studies showed that most members of the family Scolectrichidae are detritivores (e.g. Nishida et al. 1991, Nishida andOhtsuka 1997). Regarding Macandrewella, Ohtsuka et al. (2002) in their study concluded that this genus is omnivorous voraciously feeding mostly on small crustacean carcasses and/or sloughs as well as radiolarians and diatoms.