254 Crustacea: Copepoda, Calanoida Richard P. Lim 1 and Lai Hoi Chaw 2 1 Department of Environmental Sciences, University of Technology Sydney, PO Box 123, Broadway, N.S.W., Australia (Email: Richard.Lim@uts.edu.au) 2 Sedaya College, 11 Jalan Manis, Taman Segar, Cheras 56100, Kuala Lumpur, Malaysia (Email: lai@sedaya.edu.my) INTRODUCTION The Calanoida is one of three orders of the subclass Copepoda living in fresh waters (Schram 1986); the other two being the Cyclopoida and Harpacticoida. Calanoids are distinguished from the cyclopoids and harpacticoids by the long antennules that often reach the caudal rami (Fig.1A). The antennules of the cyclopoids and harpacticoids generally do not reach the caudal rami. The thoracic section is also relatively larger than the abdominal section, and the articulating line occurs between the last thoracic segment and genital segment. Calanoids have a well-defined head that fuses posteriorly with one or two thoracic segments to form the cephalothorax; a thorax of six segments; and an abdomen or urosome of apparently two to five segments (a single segment may sometimes appear to be two segments) (Figs.1A, 2A). The paired appendages of the head consist of conspicuous antennules, small antennae, mandibles, maxillules, and maxillae. The paired thoracic appendages are maxillipeds on the first segment, well developed swimming legs on each of the succeeding thoracic segments, and a modified pair of legs on the last segment in the male (Fig. 2D). This last pair of legs is important for identification of many calanoids. The abdominal segments lack appendages and end in the bifid caudal rami (Figs.1B, 2B). The broader head and thoracic section is referred to as the metasome, and the abdominal section constitutes the urosome (Figs.1A, 2A). Calanoids are important consumers of phytoplankton and provide food for predatory invertebrates and fish, contributing to the energetics of aquatic ecosystems. GENERAL BIOLOGY Calanoids generally inhabit the open water (limnetic) regions of lakes, ponds, tin mine lakes, reservoirs and other standing water bodies, but some species do occur in vegetated standing water systems such as ricefields and swamps (Table 1). Tropodiaptomus vicinus is the only species that is found in ricefields (Table 1). A few large species live in flowing water.
Crustacea: Copepoda, Calanoida 255 In terms of similarities of assemblages of calanoids in various habitats, the greatest similarity is between those of tin mine lakes and fish ponds (Sorensen Similarity Index 67%) and 50% similarity between those of reservoirs and fish ponds (Lai and Fernando 1978). Ricefield and swamp assemblages are about 40% similar. There is no similarity in assemblages between fish ponds, reservoirs and tin mine lakes on the one hand, and ricefields and swamps on the other (Lai and Fernando 1978). Figure. 1. Calanoida Neodiaptomus handeli. A female; B female metasome 5 and urosome (dorsal view); C female 5th legs (posterior view).
256 Table 1. List of calanoids found in Peninsular Malaysia and Singapore. Species Habitat Neodiaptomus blachei (Brehm, 1951) Reservoirs N. botulifer Kiefer, 1974 Reservoirs, lakes, fish ponds, rivers N. handeli Kiefer, 1932 Pools, ponds N. malaindosinensis Lai and Fernando, 1978 Fish ponds N. meggitti Kiefer, 1932 Small stagnant water bodies N. mephistopheles Brehm, 1933 Reservoirs, rivers in coastal areas N. laii Kiefer, 1974 Reservoirs, tin mine lakes Pseudodiaptomus dauglishi Sewell, 1932 Reservoirs, rivers P. tollingerae Sewell, 1924 Reservoirs, rivers Tropodiaptomus hebereri Kiefer, 1930 Ponds T. ruttneri Brehm, 1923 Reservoirs T. vicinus Kiefer, 1930 Reservoirs, ricefields, rivers The long antennules are sensory and are also used for locomotion and feeding. The right antennule of the male is distinctly modified and geniculate (bent similarly to the knee) and is used for grasping the female during copulation (Fig. 2C). Most calanoids are herbivorous. Movements of the antennae and mouth-parts during swimming create vortices that bring food to the maxillae where they are filtered. Calanoids reproduce sexually. During copulation the female is clasped by the male who transfers sperm, contained in small packets (spermatophores), to the female genital segment. The sperm are stored in a special organ called the seminal receptacle. Fertilization occurs in the oviduct; the fertilized eggs are extruded externally and are carried in a single egg sac located ventrally on the abdominal region. On hatching the young undergo six naupliar instars followed by five copepodid instars before moulting into the adult form. REGIONAL TAXA Worldwide, calanoids are represented by seven families with the family Diaptomidae being the most diverse. This family is represented by 50 genera containing over 400 species (Dussart and Defaye 1983, 2001). In Peninsular Malaysia and Singapore it is the dominant family. Among the 20 genera found across the once connected land mass of Africa, India, Australia and probably the southern fringe of the Sunda Archipelago in the geological past, only two (Neodiaptomus and Tropodiaptomus) are widespread in Peninsular Malaysia and Singapore (Lai and Fernando 1978, 1979). A less common genus is the euryhaline Pseudodiaptomus (Lai and Fernando 1978). In contrast, the calanoids of Thailand are represented by Southeast Asian, Indian and East Asian taxa (Lai and Fernando 1981). These include the genera Neodiaptomus, Tropodiaptomus, Sinocalanus, Phyllodiaptomus, Heliodiaptomus,
Crustacea: Copepoda, Calanoida 257 Allodiaptomus and Arctodiaptomus. Of the 11 species of the genus Neodiaptomus (Reddy 1994), seven have been recorded in Peninsular Malaysia and Singapore (Lai and Fernando 1978, Reddy 1994) (Table 1). In contrast, only three species of Tropodiaptomus out of 21 species in the Asian-Australian region have been recorded in Peninsular Malaysia and Singapore (Kiefer 1982; Lai and Fernando 1978, 1979; Table 1). Among the neodiaptomids, Neodiaptomus handeli (= N. schmackeri) is most widespread inhabiting fish ponds, reservoirs and some tin mine lakes (Lai and Fernando 1978). This species has a wide geographic distribution occurring in India, Siberia, Manchuria and China (Rajendran 1971). Figure 2. Calanoida Neodiaptomus handeli. A male; B male metasome 6 and urosome (ventral view); C segments 10 15 of right antennule (Greifantenna); D male 5th legs (posterior view); E, F antepenultimate segments with smooth and toothed spinous processes of right antennule, respectively.
258 There is very little information on the occurrence of calanoids in Borneo. Spandl (1924) listed five species: Arctodiaptomus wierzejskii, Diaptomus lamellatus, Tropodiaptomus vicinus, Neodiaptomus blachei and N. schmackeri. A. wierzejskii and D. lamellatus as identified by Spandl (1924) are most likely misidentifications due to mislabeled samples (see Fernando et al. 1987). This is based on the fact that the acknowledged distribution of A. wierzejskii is Palaearctic from Great Britain through Europe to northern Africa and northern Asia (Dussart and Defaye 1983). D. lamellatus (= Mixodiaptomus kupelwieseri) has a southern European distribution (Dussart and Defaye 1983). Lai and Fernando (1978) discuss the distribution of calanoids in Peninsular Malaysia and Singapore. The majority of the species occur in northwest Peninsular Malaysia (i.e. Kedah, Perlis, Penang, and Perak). They include N. handeli, N. laii, N. blachei, N. botulifer, N. mephistopheles, Tropodiaptomus ruttneri, T. vicinus, P. (S.) dauglishi and P. (S.) tollingerae. Fewer species (4) are found south of Kuala Lumpur and in northeast Peninsular Malaysia (i.e. Kelantan, Terengganu and Pahang). This greater number of species in the northwestern region of Peninsular Malaysia has been attributed to its geographical proximity to Indochina, India and mainland Asia and the prevalence of lentic habitats like reservoirs and tin mine lakes (Lai and Fernando 1978). Lim and Fernando (1985) refer to the previous literature and list 11 of the 12 species known from Malaysia. KEYS TO CALANOID COPEPODA The keys below were developed from the publications of Lai and Fernando (1978, 1979) and Reddy (1994). Detailed descriptions of the various species, listed in Table 1, can be found in Kiefer (1982), Lai and Fernando (1978, 1979, 1981), and Reddy (1994). Identification of female diaptomids is not easy. It is best accomplished by examination of the last metasomal segment, the genital segment and the fifth leg (Fig. 1). Male diaptomids can be more easily identified by examination of the structure of the fifth leg and the right antennule (Greifantenna), especially the process on the antepennultimate segment (Fig. 2). Key to genera and species: females 1. Urosome with two to three segments; distal edge of each segment is not toothed (Fig. 3A J)... 2 - Urosome with four segments; distal edge of at least the 3rd segment is toothed (Fig. 3K,L)...... Pseudodiaptomus..11 2. Genital segment generally much broader at proximal portion with large conspicuous spines on its proximal portion (Fig. 3A G)... Neodiaptomus..3 - Genital segment generally not broader at proximal portion with small inconspicuous spines on its proximal portion (Fig. 3H J)... Tropodiaptomus..9
Crustacea: Copepoda, Calanoida 259 Figure 3. Female Calanoida metasome and urosome (dorsal view). A Neodiaptomus botulifer; B N. malaindosinensis; C N. laii; D N. meggitti; E N. handeli; F N. mephistopheles; G N. blachei; H Tropodiaptomus vicinus; I T. hebereri; J T. ruttneri; K Pseudodiaptomus dauglishi; L P. tollingerae.
260 3. Genital segment with conspicuously large posteriorly-directed outgrowth on right side (Fig. 3A,B)... 4 - Genital segment without outgrowth (Fig. 3C G)... 5 4. Outgrowth on right side of genital segment sausage shaped with terminal hyaline spine; left proximal region of same segment with broadly triangular bulge; left wing of 5th thoracic segment as long as right wing (Fig. 3A)... N. botulifer - Outgrowth on right side of genital segment conical shaped with large terminal spine; left proximal region of same segment without bulge; left wing of fifth thoracic segment longer than right wing (Fig. 3B)... N. malaindosinensis 5. Genital segment has large, irregular lobe on right distal corner; right spine on genital segment slender and twice as long as left spine (Fig. 3C)... N. laii - Genital segment without lobe on right distal corner; right and left spines on genital segment either equally short or left spine longer than right spine (Fig. 3D G)... 6 6. Genital segment short, plump or at least has strongly asymmetrical protrusions at its proximal portion (Fig. 3D,E); end claw of 5th leg with coarsely denticulate lateral margins (Fig. 4D,E)..... 7 - Genital segment elongate, slender and without strongly asymmetrical protrusions at its proximal portion (Fig. 3F,G); end claw of 5th leg with either finely spinulose or hairy lateral margins (Fig. 4A,B,C,F,G)... 8 7. Urosome with two segments; genital segment nearly symmetrical; shorter than the combined 2nd urosome segment and caudal rami; right proximal protrusion of the same segment inconspicuous and has only one spine; caudal setae normal (Fig. 3D)... N. meggitti - Urosome with three segments; genital segment strongly asymmetrical; longer than the combined remaining urosome segments and caudal rami; right proximal protrusion of the same segment very conspicuous and has two spines; caudal setae expanded proximally and bent (Fig. 3E)...... N. handelii 8. Left wing of 5th thoracic segment distinctly longer than right wing and postero-laterally directed; no spinules demarcating the fourth and 5th thoracic segments; left proximal protrusion on genital segment conspicuous (Fig. 3F)... N. mephistopheles - Left wing of 5th thoracic segment nearly as long as right wing and posteriorly directed; 4th and 5th thoracic segments demarcated by fine dorsal spinules (Fig. 3G)... N. blachei 9. Genital segment without bulge on right posterior corner (Fig. 3H)... T. vicinus - Genital segment with bulge on right posterior corner (Fig. 3I, J)... 10 10. Middle section of genital segment constricted; bulge on right posterior corner very prominent; knob on postero-dorsal edge of 5th thoracic segment (Fig.3I)... T. hebereri - Middle section of genital segment not constricted; bulge on right posterior corner not prominent; knob on postero-dorsal edge of 5th thoracic segment absent (Fig. 3J)...T. ruttneri 11. 3rd urosomal segment nearly twice the length of the preceding segment (Fig. 3K)...... P. dauglishi - 4th urosomal segment equals the length of the preceding segment (Fig. 3L)... P. tollingerae
Crustacea: Copepoda, Calanoida 261 Key to genera and species: males 1. Antepenultimate process usually serrated (Fig. 6B,F,G), if smooth (Fig. 6A,D,E) hyaline lobe present between the 5th leg (Fig. 5A,C,D,E). Thumb-like processes present on the ventral surface of right caudal ramus... Neodiaptomus...2 - Antepenultimate process, if present, is smooth (Fig. 6H,I,J). Hyaline lobe absent between the 5th leg (Fig. 5H,I,J). Thumb-like processes absent on the ventral surface of right caudal ramus... 8 2. Spine located about half-way between the proximal and distal ends of the 2nd exopod segment of the 5th leg (Fig. 5A,B,C,D).... 3 - Spine located either near the proximal or distal end of the 2nd exopod segment of the 5th leg but never as above (Fig. 5E,F,G)... 6 3. Antennules much longer than the length of the body. Without minute spine on 2nd exopod of the right 5th leg (Fig. 5A)... N. handeli - Antennules about the length of the body. A minute spine on 2nd exopod of the right 5th leg present or vestigial (Fig. 5.B,C,D)... 4 Figure 4. Female Calanoida right 5th leg. A Neodiaptomus botulifer; B N. malaindosinensis; C N. laii; D N. meggitti; E N. handeli; F N. mephistopheles; G N. blachei.
262 Figure 5. Male Calanoida fifth legs. A Neodiaptomus handeli; B N. mephistopheles; C N. botulifer; D N. malaindosinensis ; E N. meggitti; F N. blachei; G N. laii; H Tropodiaptomus hebereri; I T. ruttneri; J T. vicinus; K Pseudodiaptomus dauglishi; L P. tollingerae.
Crustacea: Copepoda, Calanoida 263 4. Exopod spine and minute exopod spine(s) of right 5th leg closely placed (Fig. 5B). Antepenultimate process distinctly serrated with 3 4 teeth (Fig. 6B)... N. mephistopheles - Exopod spine and minute exopod spine(s) of right 5th leg distantly apart (Fig. 5C). Antepenultimate process membranous (Fig. 6C, D)... 5 5. Right endopod of 5th leg tubular; 2nd exopod spine fairly long (Fig. 5C). Spines on segments 14, 15, and 16 of right antennule short or vestigial (Fig. 6C)... N. botulifer - Right endopod of 5th leg triangular; 2nd exopod spine short (Fig. 5D). Spines on segments 14, 15, and 16 of right antennule fairly long (Fig. 6 D)... N. malaindosinensis 6. Antepenultimate process smooth or membranous (Fig. 6E). End-claw of right 5th leg distinctly dilated near base (Fig. 5E)... N. meggitti - Antepenultimate process serrated (Fig. 6F,G). End-claw of right 5th leg not dilated near base (Fig. 5F,G)... 7 Figure 6. Male Calanoida antepenultimate segment of right antennule. A Neodiaptomus handeli; B N. mephistopheles; C N. botulifer; D N. malaindosinensis; E N. meggitti; F N. blachei; G N. laii; H Tropodiaptomus ruttneri; I T. vicinus; J T. hebereri; K Pseudodiaptomus dauglishi; L P. tollingerae.
264 7. Antepenultimate process with 2 3 teeth (Fig. 6F). Hyaline lobe between the 5th leg present. End-claw of 5th leg long (Fig. 5F)... N. blachei - Antepenultimate process with 4 8 teeth (Fig. 6G). Hyaline lobe between the 5th leg absent. End-claw of 5th leg short (Fig. 5G)... N. laii 8. Antepenultimate process present (Fig. 6H,I,J). Distal edge of urosomal segments not toothed (Fig. 7A,B)... Tropodiaptomus...9 - Antepenultimate process absent (Fig. 6K,L). Distal edge of one or more urosomal segments toothed (Fig. 7C,D)... Pseudodiaptomus...11 9. Spine on segment 12 of right antennule present. Circular saw of left 5th leg clearly divided into proximal coarse spinules and distal fine spinules (Fig. 5H)... T. hebereri - Spine on segment 12 of right antennule absent. Circular saw of left 5th leg with uniform fine spinules (Fig. 5I,J)... 10 10. Medial surface of terminal segment of exopodite of left 5th leg not bilobed and with fine uniform spinules (Fig. 5I)...T. ruttneri - Medial surface of terminal segment of exopodite of left 5th leg bilobed and with fine uniform spinules (Fig. 5J)... T. vicinus 11. Left and right limbs of 5th leg almost symmetrical (Fig. 5K)... P. dauglishi - Left and right limbs of 5th leg distinctly asymmetrical (Fig. 5L)... P. tollingerae Figure 7. Male Calanoida urosome (dorsal view). A Tropodiaptomus hebereri; B T. ruttneri; C Pseudodiaptomus dauglishi; D P. tollingerae.
Crustacea: Copepoda, Calanoida 265 DESCRIPTION OF GENERIC CHARACTERS Genus Neodiaptomus Female: The antennules extend beyond the caudal setae. Fifth legs generally asymmetrical, the right leg stouter than the left; coxal spines large; end claws generally with denticulate margins; third exopodite segment reduced or absent, represented by two unequal spines; apex of endopodite obliquely cut on inner margin, pointed and lack setae. Male: The right antennule bears a prominent spine each on segments 10, 11, 13 15; antepenultimate segment with long or sometimes short spinuous process. Right leg 5, coxa produced into triangular, pointed or bifid lobe (intercoxal plate) at distal inner corner; endopodite long, 1-segmented, dilated at base and pointed at apex; lateral spine generally inserted at the middle of outer margin of second exopodite segment. Second exopodite of left leg 5 short, with a small thumb-like process and a short seta apically. Right caudal ramus with tooth-like chitinous structure on inner ventro-lateral corner. Genus Tropodiaptomus Female: The last thoracic lobes are usually symmetrical with bilobed lateral wings and distinct spine on outer lobe. Urosome symmetrical; caudal setae short. The endopod of fifth leg non-segmented with two slender setae at the distal end and a tuft of spinules at the base of the setae. Male: The right antennule has a spine each on segments 10, 11, 13 and 15. The process on the antepenultimate segment is always smooth. The second basopod of the right fifth leg has an outgrowth along its medial margin. The second exopod segment of the same leg has a hyaline spine near the base of the exopod spine. The exopod of the left fifth leg is fused into a single flattened structure, its margin and denticulation vary from species to species. The endopods of both left and right fifth legs are generally minute. Genus Pseudodiaptomus Female: Last thoracic segment has one or two pairs of spines on its dorsal surface. Distal edge of one urosomal segment with tooth-like spines. The genital segment has spines or setae. The caudal rami are longer than broad and their medial margins have a row of dense setae. Endopods of fifth legs absent; the terminal exopod segment of fifth leg bears three distinct spines. Male: Lateral wings of last thoracic segment bear 1 or 2 spines. Distal edge of urosomal segments has tooth-like spines. The right limb of the fifth leg is equal or smaller than the left limb.
266 REFERENCES Dussart B. and Defaye D. (1983) Repertoire mondial des crustaces copepodes des eaux interieures 1. Calanoides. Centre National de la Recherche Scientifique, Centre Regional de Publication de Bordeaux. Pp 224. Dussart B.H. and Defaye D. (2001) Introduction to the Copepoda. Backhuys, Leiden. Pp 344. Fernando C.H., Paggi J.C. and Rajapaksa R. (1987) Daphnia in tropical lowlands. Memorie dell'instituto Italiano di Idrobiologia 45: 107 141. Kiefer F. (1982) Comparative studies on morphology, taxonomy and geographical distribution of the species of the genus Tropodiaptomus Kiefer from Asiatic inland waters. (in German) Hydrobiologia, 93: 223 253. Lai H.C. and Fernando C.H. (1978) The freshwater Calanoida (Crustacea: Copepoda) of Singapore and Peninsular Malaysia. Hydrobiologia 61: 113 127. Lai H.C. and Fernando C.H. (1979) The Malaysian Tropodiaptomus (Copepoda: Calanoida) and its distribution. Hydrobiologia 65: 75 81. Lai H.C. and Fernando C.H. (1980) Zoogeographical distribution of Southeast Asian freshwater Calanoida. Hydrobiologia 74: 53 66. Lai H.C. and Fernando C.H. (1981) The freshwater Calanoida (Crustacea: Copepoda) of Thailand, Hydrobiologia 76: 161 178. Lim R.P and Fernando C.H. (1985) A review of the Malaysian freshwater Copepoda with notes on new records and little known species. Hydrobiologia 128: 71 89. Reddy R.Y. (1994) Copepoda: Calanoida: Diaptomidae. Key to the genera Heliodiaptomus, Allodiaptomus, Neodiaptomus, Phyllodiaptomus, Eodiaptomus, Arctodiaptomus and Sinodiaptomus. SPB Academic Publishing bv. Pp 221. Rajendran M. (1971) Redescription of the freshwater calanoid Neodiaptomus schmackeri and comments on interrelationships and distribution pattern of the schmackeri group of species. Crustaceana 21: 92 100. Schram F.R. (1986) Copepoda In: Crustacea. Oxford University Press. Pp 448 472. Spandl H. (1924) Entomostraken von Borneo. Annalen des Naturhistorischen Museums in Wien 38: 89 95.