11 June 1992 PROC. BIOL. SOC. WASH. 105(2), 1992, pp. 275-298 NAUPLII AND COPEPODIDS OF THE CYCLOPOID COPEPOD DIOITHONA OCULATA (FARRAN, 1913) (OITHONIDAE) FROM A MANGROVE CAY IN BELIZE Frank D. Ferrari and Julie W. Ambler Abstract.?Som\\e^, appendage segments and armament elements of 6 nau- pliar and 6 copepodid stages are described for Dioithona oculata (Farran, 1913) from Belize. Dioithona oculata were cultured on Isochrysis galbana from egg through naupliar stage 5 with some individuals growing as far as copepodid stage 3; copepodid stages were collected from daytime swarms. At 31?C, de- velopment time from 50% Nl to 50% N5 was 3.8 days. New information about morphological development is described for appendage segments and arma- ment elements. Modified setae are present only on copepodids and are found on exopods of the mandible and maxillule, the endopod of swimming leg 4, and on the caudal ramus. The naupliar antennule is 2-segmented and the number of setae on this appendage is reduced from nauplius 6 to copepodid I. Development of ramal segments for swimming legs follows the common pattern for copepods with identical patterns for legs 1 and 2. The pattern of addition of setae and spines is identical for swimming legs 2 and 3. A study of formation homology for swimming leg 3 suggests that new segments form proximally to the distal-most segment of each ramus; new armament elements usually appear first at the proximal edge of the distal-most segment and sub- sequently become incorporated onto the next newly formed segment at the next molt. Oithonid copepods are among the nu- merically dominant copepod species in many estuarine, coastal, and oceanic eco- systems (Marshall 1949, Marlowe & Miller 1975, Peterson et al. 1979, Lonsdale 1981, Turner & Dagg 1983, Ambler et al. 1985, Roman etal. 1985, Paffenhoferet al. 1987). Some developmental stages of oithonid spe- cies have been described for nine species belonging to Oithona and one species of Dioithona (Table 1). No descriptions are available for the remaining oithonid genera, Paroithona and Limnoithona. From our studies of swarms of D. oculata, we describe changes in the exoskeletal morphology for all naupliar and copepodid stages, present molting rates for naupliar stages, compare our findings to developmental information known for other cyclopoid copepods, and discuss homologies of several appendages and their armament. Dioithona oculata is a tropical cyclopoid copepod with a circumglobal distribution in neritic areas (Nishida 1985). During the day, D. oculata often forms swarms, composed of copepodid stages, in coral reef and man- grove habitats (Emery 1968, Hamner & Cariton 1979, Ueda et al. 1983, Ambler et al. 1991). Along mangrove shores of cays off Belize, swarms of D. oculata among mangrove roots disperse at sunset to open water 3-5 m away, adjacent to shore. Before dawn the copepodids move back under the mangroves to form swarms during the day (Ambler et al. 1991). Females produce egg sacs at night, and approximately 24 hours later, nauplii hatch to join the plankton in the water adjacent to the mangroves (Am- \ 276 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON Table 1.?Sources of information about develop- ment of cyclopod copepods. Table 1.?Continued. Oithonidae Dioithona rigida Oithona atlantica O. brevicornis O. davisae O. nana O. nana O. oligohalina O. ovalis O. similis O. hebesl Ascidicolidae Ascidicola rosea Enterocola fulgens E. ferlilis E. laliceps Enteropsis capilulatus Haplosaccus elongatus Haplostoma alhicatum Haplostomella distincta H. oceanica Zanclopus cephalodisci Cyclopidae Acanthacyctops viridus Allocyclops sihaticus Apocyclops dengizicus Bryocyclops caroti Cyclops sirenuus Diacyclops bicuspidatus Ectocyclops rubescens Eucyclops serrulatus Graeteriella unisetigera Halicyclops negleclus Macrocyclops albidus Mesocyclops edax Speocyclops racovitzai Cyclopinidae Cyclopina tongifera Lemaeidae Lamprogtena chinensis Lernaea cyprinacea Ramamohana Rao (1958) [as Oithona] Gibbons & Ogilvie (1933) [as O. spiniroslris] Goswami (1975) Uchima(1979)[asa brevicornis] Haq(1965) [as Oilhoni- na] Murphy (1923) Fonseca & Almeida Pra- do(1979) Fanta(1976) Gibbons & Ogilvie (1933) [as O. helgolandica] Goswami (1975) [O. hebes is neotropical] Illg& Dudley (1980) Canu(1892) Illg& Dudley (1980) Illg& Dudley (1980) Illg& Dudley (1980) Ooishi (1980) Ooishi(1980) Ooishi (1980) Ooishi (1980) Caiman (1908) Lucks (1927) [as Cyclops] Rocha & Bjomberg [in litt.] Valderhaug & Kewalra- mani (1979) Bjornberg(1984) Gumey(1932) Amores-Serrano (1978) [as Cyclops] Carvallio(1971) Auvray & Dussart (1966) Lescher-Moutoue (1973) Candeias(1966) Defaye(1984) Amores-Serrano (1978) Lescher-Moutoue (1966) Goswami (1977) Kuang(1962) Grabda(1963) Notodelphyidae Doroixys uncinata Doropygus seclusus Nolodelphys affinis Pachypygus gibber Canu(1892) Dudley (1966) Dudley (1966) Hipeau-Jacquotte (1978) Pygodelphys aquitonaris Dudley (1966) Scolecodes huntsmani Dudley (1966) bier et al. 1990). Nauplii remain in the plankton until they molt to the first cope- podid stage (CI); CI's migrate horizontally to swarms among mangrove roots. Two other oithonid species are present with D. oculata in the plankton at night. O.fonsecae is found in tropical Atlantic lagoonal waters (Ferrari & Bowman 1980), and O. nana has a tropical oceanic and nearshore distribu- tion (Nishida 1985). Methods Copepodid stages of Z). oculata were sort- ed from preserved swarm samples collected at Twin Cays, Belize (le^SO'N, SS'OS'W), in May 1985, June 1988, and July 1990. Nauplii were cultured from eggs hatched from dropped egg sacs of females isolated from swarm samples collected in February and May 1989. Nauplii were kept in several 500 ml (February) or 50 ml (May) beakers of ambient seawater which were suspended with a styrofoam float in a water-bath cool- er, and fed a chrysomonad, Isochrysis gal- bana. Temperatures varied from 20-25''C in February and 30-31?C in May. In Feb- ruary, 12-80 nauplii from several beakers were collected daily; during May, 30-70 nauplii were collected from a 50 ml beaker in 8-12 hr intervals. Specimens were fixed with 2.0% formaldehyde, preserved in 0.5% propylene phenoxytol/4.5% proplylene gly- col/95.0% water, cleared in steps through 50.0% lactic acid/50.0% water to 100% lac- tic acid, and stained by adding a solution of chlorazol black E dissolved in 70.0% eth- anol/30.0% water. VOLUME 105, NUMBER 2 277 Table 2. ?Development of Dioithona oculata nauplii reared in laboratory from May 18, 1989 experiment. Time from egg hatching to 50% of stage i (T50), instar duration (T), coefficient of determination (R2) for linear regression of angular transformed percent stage versus time. In parentheses is probability of rejecting Ho: Slope = 0, Slope, and Intercept, n = number of points in regression. Stage n Ts? (hours) T (hours) R' Slope Inlercepl Nl 4 24.00 10.93 0.959 (0.0206) 0.225 -4.62 N2 3 34.93 34.89 1.000 (0.0105) 0.125 -3.57 N3 8 69.82 25.00 0.901 (0.0003) 0.0274 -1.13 N4 8 94.82 21.22 0.744 (0.0059) 0.0250 -1.59 N5 8 116.04 " 0.767 (0.0043) 0.0167 -1.15 Depending upon their availability, up to 30 specimens of each stage were measured to determine body length; caudal rami were included in body length measurements of copepodids. From 3 to 10 specimens of each stage were dissected; the number depended upon the degree of difficulty in determining structural morphology or variability of an appendage. Results consist of brief descrip- tions of changes in each appendage for each developmental stage. The ventral view of nauplii or lateral view of copepodids are shown for each developmental stage, and the appropriate appendages are illustrated. Descriptions of appendage segments or their armament elements are not repeated if they have not changed from the previous stage. Dense setules on a seta or spine are indi- cated in illustrations only over a short sec- tion of a seta and are not repeated for similar elements. Developmental times for naupliar stages were determined from the experiment start- ed on May 18, 1989. The time when 50% of the nauplii had molted to a particular stage was determined from linear regression of the angular transformation (Sokal & Rohlf 1969) of percent stage as a function of time. Developmental times were calculated as a difference of times between two successive stages for 50% of the specimens to molt. The angular transformation for each stage, which is the arcsine of the square root of the percent molted to the next stage, was used to meet the assumption of constant variance. Time was calculated from time zero (May 18, 0400) when females produce egg sacs (see Ambler et al. 1990). Naupliar stages are abbreviated Nl to N6; copepodid stages CI to CVI; male = m, fe- male = f Appendages are A1 = antennule; A2 = antenna; Mn = mandible; Mxl = maxillule; Mx2 = maxilla; Mxp = maxil- liped; swimming legs = legs 1^; posterior to these are two simple appendages = legs 5 and 6; caudal ramus = CR. Appendage segments are named following Boxshall (1985) with exopods = Re; endopods = Ri; medial lobes of a segment = li. Armament elements of appendages are spines and setae which are distinguished by apparent degree of flexibility (Dudley 1966); medial, ter- minal and lateral elements are si, st and se. Homology of appendages, their segments and elements in different developmental stages usually was established by position and occasionally by morphology. For a few appendages, homology by formation was determined if the developing appendage or element of a succeeding stage was visible within the skeleton of the preceding stage. Results For experiments in February and May 1989, D. oculata was reared from Nl 278 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON Table 3. ?Length range (mm), number of somites or complexes [two or more fused somites] (S + C), ap- pendage buds and number of swimming legs (SI) on stages of Dioilhona oculaia. n = number of specimens. Suge n Range s + c Buds SI Nl 20 0.11-0.13 0 0 N2 18 0.12-0.14 0 0 N3 12 0.12-0.14 0 0 N4 10 0.15-0.16 mxl 0 N5 7 0.16-0.17 mxl 0 N6 20 0.19-0.21 mxl, legs 1,2 0 a 20 0.34-0.37 6 leg3 2 cn 20 0.39-0.42 7 leg4 3 CHI 30 0.43-0.49 8 legs 4 CIV 30 0.52-0.60 9 legs5,6 4 cv 30 0.59-0.67 10 leg6 4 CVIf 30 0.73-0.80 10 leg6 4 CVIm 30 0.64-0.70 11 leg6 4 through CIII on unialgal cultures of Iso- chrysis galbana. During February when temperatures varied between 20-25?C, CI were present 8-11 days after egg hatching. In May, sufficient nauplii were raised at nearly constant temperature (30-3 rC) to calculate development times for the first four naupliar stages (Table 2). N1 had the short- est development time (10.93 hr)and N2 the longest (34.89 hr). Durations of N3 and N4 were approximately one day. When the ex- periment was terminated 7.2 days after egg hatching, 56% of the animals had molted to at least N6, and 23% were copepodids. There are 6 naupliar and 6 copepodid stages of ?>. oculata. Body length and somite number are given in Table 3 and Figs. lA, E, 2A, D, 3A, E, 4A, 5A, 6A, 7A, 8A, E, and 9E. In Nl-5 all cephalic somites are fused into a single complex segment; in N6 this complex includes the first 3 thoracic somites. In CI-CVI all cephalic and the first thoracic somites are fused into a complex, and in addition in CVIf the seventh thoracic and first abdominal somites are fused lat- erally and ventrally into a genital complex. Posterior Armament and C^. ?N1-N2 (Fig. lA, E) 1 pair of setae. N3-N4 (Fig. 2A, D) 3 pairs of setae. N5-N6 (Fig. 3A, E) 5 pairs. CI CR (Fig. 4B) length 1.6 x width, I lateral, 1 dorsal, 4 terminal setae; medial- most terminal seta with thick base and re- curved medially. CII-CIII (Fig. 53) no setae recurved. CIV-CV (Fig. 7B) length 1.8 x width. CVIf (Fig. 8F) length 2.5 x width. CVIm (Fig. lOE) length 2.0 x width. Al.?[* = count includes a small, pointed seta; a = count includes an aesthetasc] Nl- N2 (Fig. IB) 2 segments with 3 and 4 setae. N3 (Fig. 2B) segment 2 with 7 setae. N4 (Fig. 2E) segment 2 with 12 setae. N5 (Fig. 3B) segment 1 with 4 setae, segment 2 with 14 setae. N6 (Fig. 3F) segment 2 with 16 setae. CI (Fig. 4C) 4 segments with 3, 3, 1 and 9 setae. CII (Fig. 5C) 7 segments with 3, 3, 2, 1, 1, 1 and 10 setae. CIII (Fig. 6B) 9 segments with 3, 3, 2, 3, 4, 1, 2, 2, and II setae. CIV (Fig. 7C) 11 segments with 2, 3, 6, 3*, 4, 4, 2a, 3, 2, 3 and 7a setae. CV (Fig. 8B) 11 segments with 7, 8, 3, 4*, 4, 4, 2a, 3, 2, 3, and 7a setae. CVIf (Fig. lOA) 11 segments with 2, 5, 10, 6*, 4, 4, 2a, 3, 2, 3, and 7a setae. CVIm (Fig. lOF) 15 segments with 2, 5, 4, 3, 2, 2, 1, 1, 1, 2, 2, 2, 3, 2, and 9aa setae plus 3 sensilla. ^2. ?Nl (Fig. IC) coxa 2 si; basis 2 si; Rel fused to basis; several indistinct seg- ments and 6 setae; Ri 1 4 setae. N2 (Fig. 1F) basis 3 si; Re 7 setae. N3 (Fig. 2C) coxa 3 si; Re 8 setae; Ril 5 setae. N4 (Fig. 2F) Re 10 setae; Ril 7 setae. N5 (Fig. 3C) Re 10 setae. N6 (Fig. 3G) Ril 8 setae. CI (Fig. 4D) coxa and basis fused 2 si; Rel wrinkled, 2 setae; Ri 10 setae. CII-CIII (Fig. 5D) Re 1 seta; Ril 5 setae; Ri2 6 setae. CIV-CVIf (Fig. 6G) Ri2 7 setae. CVIm (Fig. lOG) Ri all segments more elongate. M?. ? Nl (Fig. ID) coxa 1 si; basis 2 si; Rel 1 si; Re2 1 si; Re3 2 setae; Ril 2 si; Ri2 4 si. N2-N6 (Fig. IG) Re3 1 si; Re4 1 St; Ri 1 4 si. CI (Fig. 4E) coxa a gnathobase; basis 1 si; Re4 2 setae, lateral seta a brush; Ril fused with basis, 2 si; Ri2 4 setae. CII- CV (Fig. 5E) Ri2 5 setae. CVIf (Fig. 9A) Re4 1 si; Re5 1 seta a brush. CVIm (Fig. 9F) Ri 1 2 setae; Ri2 5 setae. A/xy.-N2-N3 (Figs. IE, 2A) 1 seta, N4 VOLUME 105, NUMBER 2 279 Fig. 1. Dioithona oculata. A-D nauplius I: A, ventral; B, antennule; C, antenna; D, mandible. E-G nauplius 2: E, ventral; F, antenna 2; G, mandible. Scales 1 (B-D, F, G) and 2 (A, E) equal 0.10 mm. 280 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON Fig. 2. Dioithona ocutata. A-C nauplius 3: A. ventral; B, antennule; C, antenna. D-H nauplius 4: D, ventral; E, antennule; F, antenna; G, maxillule; H, maxillulc variations (a = seta on 40% of May 1988 specimens and b = seta on one May 1988 specimen). Scales 1 (B, C, E-H) and 2 (A, D) equal 0.10 mm. VOLUME 105, NUMBER 2 281 1 Fig. 3. Dioithona oculata. A-D nauplius 5: A, ventral; B, antennule; C, antenna; D, maxillule. E-H nauplius 6: E, ventral; F, antennule; G, antenna; H, maxillule. Scales 1 (B-D, F-H) and 2 (A, E) equal 0.10 mm. 282 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON Fig. 4. Dioithona oculata. copepodid I: A, lateral; B, caudal ramus; C, antennule; D, antenna; E, mandible; F, mandibular gnathobase; G, maxillule; H, maxilla; I, maxilliped; J, leg I; K, leg 2; L, leg 3. Scales (B-L) and 2 (A) equal 0.10 mm. VOLUME 105, NUMBER 2 283 (Fig. 2G) a bilobed bud with basal segment; le 3 setae, li 4 setae [4 of 10 May specimens with an extra seta on basal segment; 1 other May specimen with li 5 setae]. N5 (Fig. 3D) basal segment 2 Si, le 4 setae; li 5 setae. N6 (Fig. 3H) basal segment 3 si. CI-CII (Fig. 4G) sympod lil 7 setae, li2 1 setae, li3 3 setae, li4 1 setae; Rel 4 setae, 2nd seta a brush; Ril 4 setae, CIII-CVI (Figs. 6H, 9C) sympod lil 9 setae. Mx2.-C\ (Fig. 4H) coxa lil 3 setae, li2 1 seta, li3 3 setae, li4 3 setae; basis with distal inner comer elongate as a curved claw, 2 si; Ril 4 si; Ri2 3 setae. CII-CV (Fig. 7H) Ri2 2 setae; Ri3 3 setae. CVIf (Fig. 11 A) Ri2 3 setae; Ri3 4 setae. CVIm (Fig. 1IC) Ri2 5 setae. Mx/J.?CI-CII (Fig. 41) praecoxa 3 si; coxa 1 si; basis 2 si; Ril 1 si; Ri2 4 setae. CIII (Fig. 6C) praecoxa 4 si; coxa 2 si; Ril 2 si. CIV-CVI (Fig. 9D, H) syncoxa 6 si; basis 2 si and inner row of hairs; Ri 1 3 setae. Leg /.-N6 (Fig. 3E) a bilobed bud le 3 setae, li 2 setae. CI (Fig. 4J) coxa naked; basis 1 se; Rel with 4 se, 3 si, 1 st; Ril 7 setae. CII (Fig. 5F) coxa 1 si; basis 1 si; Rel 1 se; Re2 3 se, 4 si, 1 st; Ril 1 si, Ri2 6 setae. CIII-CIV (Fig. 61) Rel 1 se, 1 si; Re2 3 se, 4 si, 1 st; Ri 1 1 si; Ri2 7 setae. CV- CVIf (Fig. lOB) Rel 1 se, 1 si; Re2 1 se, 1 si; Re3 3 se, 4 si, 1 st; Ril 1 si; Ri2 1 si; Ri3 6 setae. CVIm (Fig. 91) basis 1 si re- curved medially. Leg 2.-N6 (Fig. 3E) a bilobed bud Ic 3 setae, li 2 setae. CI (Fig. 4K) coxa naked; basis naked; Rel with 3 se, 3 si, 1 st; Ril 6 setae. CII (Fig. 5G) coxa 1 si; basis 1 se; Rel 1 se; Re2 2 se, 4 si, 1 st; Ril 1 si, Ri2 6 setae. CIII-CIV (Fig. 6J) Rel 1 se, 1 si; Re2 3 se, 5 si, 1 st; Ril 1 si; Ri2 7 setae. CV-CVI (Fig. IOC) Rel 1 se, 1 si; Rel 1 se, 1 si; Re3 3 se, 5 si, 1 st; Ril 1 si; Ri2 2 si; Ri3 6 setae. Leg 3. -CI (Fig. 4L) a bilobed bud le 3 setae, li 2 setae. CII (Fig. 5H) coxa naked; basis naked; Rel with 3 se, 3 si, 1 st; Ril 6 setae. CIII (Fig. 6D) coxa 1 si; basis 1 se; Rel 1 se; Re2 2 se, 4 si, 1 st; Ril 1 si, Ri2 6 setae. CIV (Fig. 7D) Rel 1 se, I si; Re2 3 se, 5 si, 1 st; Ril 1 si; Ri2 7 setae. CV- CVI (Fig. lOD) Rel 1 se, 1 si; Re2 1 se, 1 si; Re3 3 se, 5 si, 1 st; Ril 1 si; Ri2 2 si; Ri3 6 setae. Leg 4. -CII (Fig. 51) a bilobed bud le 3 setae, li 2 setae. CIII (Fig 6E) coxa naked; basis naked; Re 1 segment with 3 se, 3 si, 1 st, Ri 1 segment with 6 setae. CIV (Fig. 7E) coxa 1 si; basis 1 se; Rel 1 se, 1 si; Re2 3 se, 5 si, 1 st; Ril 1 si; Ri2 6 setae. CV (Fig. 7G) Rel 1 se, 1 si; Re2 1 se, 1 si; Re3 2 se, 5 si, 1 St. CVIf (Fig. 1 IB) Ri2 both and Ri3 proximal setae modified, slightly curved distally with hyaline flange along inner edge. CVIm (Fig. 11D) Ri2 both and Ri3 proxi- mal setae modified, straight with hyaline flange smaller than in female. Leg 5.?C\\\ (Fig. 6F) unilobed bud with 2 setae. CIV (Fig. 7F) bilobed bud with 3 setae. CV-CVI (Figs. 8D, H, 9J) basal lobe with 1 seta; 1 segment with 2 setae. Leg 6.-CIV-CVIm (Figs. 7F, 8D, 9K) unilobed bud with point and 1 seta. CVIf (Fig. 8H) unilobed bud with seta recurved dorsally. Discussion Our specimens of D. oculata differ from those (as Oithona oculata) of Nishida (1985) in the following: (1) Al of our females has two fewer segments; apparently our 3rd and 6th segments represent fused segments (Fig. IDA); (2) Mxp of the female has one fewer segment (Fig. 9D), i.e., praecoxa and coxa are fused, and medial spinules at base of segment 1 are absent; (3) modified setae on female and male Mn, Mx 1, leg 4, and male leg 1 are present (Figs. 9A, C, F, lOF, K). We believe that these modified setae are difficult to discern and may have been over- looked in earlier studies. Ferrari & Bowman (1980) described modified setae (previously noted for O. plumifera by Giesbrecht 1892, and for O. brevicornis and O. hebes by Wei- 284 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON Fig. 5. Dioilhona oculata, copepodid II: A. lateral; B, caudal ramus; C, antennule; D, antenna; E, mandible; F, leg 1; G, leg 2; H, leg 3; I, leg 4. Scales 1 (A) and 2 (B-I) equal 0.10 mm. lershaus 1969) on leg 4 of many Oithona females, including D. oculata, but failed to detect these setae on males of D. oculata. Oithonid species {O. nana, O. similis, O. brevicornis, O. hebes?, O. colcarva, and O. davisae) have been cultured on diets of chlo- rophyte flagellates, dinoflagellates, and chryptophyte flagellates (Haq 1965, Eaton VOLUME 105, NUMBER 2 285 Fig. 6. Dioithona ocu/ala, A-F copepodid III: A, lateral; B, antennule; C, maxilliped; D, leg 3; E, leg 4; F, leg 5. G-J copepodid IV: G, antenna; H, maxillulc; I, leg I; J, leg 2. Scales 1 (B-J) and 2 (A) equal 0.10 mm. 286 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON Fig. 7. Dioilhona oculata. A-F copepodid IV: A, lateral; B, caudal ramus, C, antennule; D, leg 3; E, leg 4; F, legs 5-6. G-H copepodid V: G, leg 4; H, maxilla. Scales 1 (B-H) and 2 (A) equal 0.10 mm. VOLUME 105, NUMBER 2 287 Fig. 8. Dioithona oculata, A-D copepodid V: A, lateral; B, antennule; C, leg 4; D, legs 5-6. E-H copepodid VI female: E, lateral; F, caudal ramus; G, leg 5 ventrolateral; H, legs 5-6. Scales 1 (B-D, F-H) and 2 (A, E) equal 0.10 mm. 288 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON Fig. 9. Dioithona oculala, A-D copepodid VI female: A, mandible; B, mandibular blade; C, maxillule; D, maxilliped. E-K copepodid VI male: E, lateral; F, mandible; G, mandibular blade; H, maxilliped; I, leg 1 basis; J, leg 5; K, leg 6. Scales 1 (A-D, F-K) and 2 (E) equal 0.10 mm. VOLUME 105, NUMBER 2 289 Fig. 10. Dioithona oculala, A-D copepodid VI female: A. antennule; B, leg 1; C, leg 2; D, leg 3. E-G copepodid VI male: E, caudal ramus; F, antennule; G, antenna. Scale 1 equals 0.10 mm. 290 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON Fig. 11. Dioithona oculata. A-B copepodid VI female: A, maxilla; B, leg 4. C-D copepodid VI male: C, maxilla; D, leg 4. Scale I equals 0.10 mm. VOLUME 105. NUMBER 2 291 1971 referenced in McLaren (1978), Go- swami 1975, Lonsdale 1981, Uchima 1979). Protozoans such as oligotrichines are in- gested by all stages of O. davisae (Uchima & Hirano 1986), and Murphy's (1923) kelp detritus for O. similis included protozoans. Diatoms are not as readily ingested by oi- thonids, but several species (O. similis, O. nana, and O. davisae) have been reported to ingest at least one species (Murphy 1923, Haq 1965, Uchima & Hirano 1986). Iso- chrysis galbana was sufficient for growth for most of the naupliar stages of D. oculata but growth of N5 and N6 may have been re- tarded. Growth of older nauplii and cope- podids probably depends on diets of larger protists such as the dinoflagellate Amphi- dinium klebsii. which was fed to adult fe- males for egg production (unpublished data). Females did not produce new egg sacs when offered other species such as newly hatched Anemia salina, the rotifer Asplancha sp., and Dunaliella salina. Older nauplii and co- pepodids may also need larger food species. The first feeding stages varies with co- pepod species, but it is usually the naupliar stage of longest duration (Landry 1983). For O. similis and O. davisae. Nl is the first feeding stage (Uchima & Hirano 1986). Or- ange droplets, probably yolk, were observed in the guts of Nl of Z). oculata; its first feed- ing stage is probably N2 because it is the naupliar stage of longest duration (Table 3). The development time for growth be- tween egg hatching and CI has been deter- mined for several oithonid species with varying precision. For most published stud- ies it is difficult to determine from methods if time from Nl to CI is the time to the first appearance of CI, or to the time of 50% CI which is used in the present study. Devel- opment time as a function of temperature (Fig. 12), however, shows a classical Beleh- radek function which has been observed for egg development rates (McLaren 1966). Goswami (1975) determined that O. hrev- icornis and O. hebesl developed from Nl to CI in 8-10 and 10-14 days, respectively, at 24-2 7?C. Several species of calanoid co- pepods raised at 15?C developed from hatching to CI in 6.5-9.8 days (Landry 1983), which was much faster than oithonid species (Fig. 12). Development time for D. oculata to 50% N5 was 3.83 days, and de- velopment to 50% CI probably is in the range of the other oithonid species. Since ambient temperatures near the Belizean mangroves are typically near 30?C, D. ocu- lata probably is adapted to growth at max- imal rates at these high temperatures. Dioithona oculata possesses a 2-seg- mented naupliar Al (Figs. IB, 2B, E, 3B, F), a brush-like seta on the exopod of both Mn and Mxl of all copepodids (Figs. 4E, F, 5E, 6H, 9A, C, F), and modified setae on the basis of the male leg 1 (Fig. 91). These structures have not been described for other cyclopoid copepods. A reduction (from 20 to 16) of setae on A1 from N6 to CI (Figs. 3F, 4C) has been reported only for O. similis and O. atlantica. Presence on male leg 4 of three endopodal setae modified with a hy- aline flange similar to female leg 4 is unique to D. oculata (Fig. 1 IB, D). Development of exopodal and endopodal segments of the swimming legs of D. oculata follows the common pattern described by Ferrari (1988, 1991) with the segmentation pattern of legs 1 and 2 identical, while legs 3-6 are similar but one copepodid stage each out of register. The addition of armament elements to each ramus is a more complex process. Six conditions of appendage de- velopment (Table 4) can be defined: (A) a leg bud, (B) a reorganized swimming leg with 1-segmented exopod and endopod, (C) an early 2-segmented exopod and endopod, (D) a later 2-segmented exopod and endopod, (E) a final 2-segmented exopod and endo- pod, (F) a 3-segmented exopod and endo- pod. Conditions A-F occur in legs 1-2, con- ditions A-D, and F occur in leg 3, and conditions A, B, D, and F occur in leg 4. Addition of armament elements on legs 1- 292 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON DEVELOPMENT FROM N1 TO Cl 30 CO >- < 20 LU 1 10 ? O. colcarva Cb n o. nana A O. davisae O O. similis ? ? O D. oculata n ' ?T '?'. 10 20 30 TEMPERATURE (C) 40 Fig. 12. Development time (days) as a function of temperature from egg hatching to CI for oithonid species. Only mean values are plotted. When means are not given, the middle value of the range is plotted. Literature values of development time given as mean and standard deviation {O. colcarva by Lonsdale 1981), mean and range (O. davisae by Uchima and Hirano 1986), range (O. davisae by Uchima 1979), range (O. nana by Haq 1965), and overall mean and range of means (O. similis by Eaton 1971 as referenced in McLaren 1978). Dioithona oculata development time from 50% Nl to 50% N5 from Table 3. Standard deviation or range from means was 1.2 at most, except for O. similis with a range of 2.0. 3 occurs pinor to conditions B, C, D, and F. Addition of elements for leg 4 occurs prior to conditions in B, D, and F. For swimming legs 2 and 3, identical numbers of elements arc present on the ex- opod and endopod segments for each leg condition (Table 4). For leg 1 there are more elements present early in development and fewer present later in development than for legs 2 and 3. We have assumed that the early 2-segmented condition (condition C) is skipped for leg 4 so that numbers of exo- podal elements are identical to legs 2 and 3 but the endopod of leg 4 has fewer elements later in development. Inferences about homologies of several appendages of Z). oculata can be drawn from the development of their segments by com- paring morphology, position, or formation. Homology by morphology suggests that the Rel of naupliar A2 is fused to the basis, and that the medial recurved seta of CR on CI may become the second from medial seta on CR ofCII-CVI. In D. oculata the elongate lateral exten- sion of the basis of A2 (e.g.. Fig. IC) is a fused exopodal segment, and not an exten- sion of the basis as has been described as a part of the basis for Haplosaccus elongatus, Doropygus seclusus. Notodelphys affinis, Py- godelphys aquilonaris, and Scolecodes huntsmani, because several inner setae are added to it in later naupliar stages (Fig. 3G). Armament additions such as this have not been reported for the basis of other copepod appendages. In most descriptions of cycio- VOLUME 105, NUMBER 2 293 Table 4.?Number of armament elements for Dioithona oculata of the exopod (Re) and endopod (Ri) of legs 1-4. Six leg conditions: (A) leg bud, (B) reorganized swimming leg with 1-segmented exopod and endopod, (C) early 2-segmented exopod and endopod, (D) later 2-segmented exopod and endopod, (E) final 2-segmented exopod and endopod, (F) 3-segmented exopod and endopod are listed on the left; the number of setae plus spines present on each ramus are given to the left of the slash and the stage of development is given to the right. C = copepodid; n = nauplius; nc = no change from previous stage in numt)er of elements; np = condition not present for that leg. Leg Re Leg Ri Leg condition 1 2 3 4 1 2 3 4 bud 3/n6 3/n6 3/CI 3/CII 2/n6 2/n6 2/CI 2/CII 1 + 1 8/CI 7/CI 7/CII 7/CIII 7/CI 6/CI 6/CII 6/CIII 2 + 2 (early) 9/CII 8/CII 8/CI II np 7/ClI 7/CII 7/CIII np 2 + 2 (late) 10/CIII U/CIII 11/CIV 11/CIV 8/CIII 8/CIII 8/CIV 7/CIV 2 + 2 (final) nc/CIV nc/CIV np np nc/CIV nc/CIV np np 3 + 3 12/CV 13/CV 13/CV 13/CV 8/CV 9/CV 9/CV 8/CV poid naupliar development, a similarly elongate Rel articulates with a simple, unextended basis. Other cyclopoid species in which this segment is described correctly as fused include Ascidicola rosea and Ler- naea cyprinacea. The long, thick, recurved, medial seta on the distal edge of the CR of CI (Fig. 4B) of D. oculata may be the homologue of the long, thick, second-from-medial seta of CII (Fig. 5B). A distinctively modified medial seta like that of ?). oculata also is known for CI of Haplosaccus elongatus, Haplostoma albicatum, and Lernaea cyprinacea. Like D. oculata, CII of the first two species has a small, simple medial seta, and a longer thicker, second-from-medial seta. In CII- VI of L. cyprinacea, a distinctively modified seta of similar morphology to the modified medial seta of CI is present at the second- from-medial position. The medial seta in CII-VI is small and simple. Given these morphological data, an hypothesis that the medial seta of CI is the homologue of the second-from-medial seta in CII-VI of D. oculata seems reasonable. The identity of the seta on CI that is homologous to the medial seta on CII remains unresolved, al- though Dahms (1990) has described the transposition of two setae in similar posi- tions during the development of an harpac- ticoid copepod. Homology by position suggests that the endopod of Mxp is 2-segmented in all co- pepodids of D. oculata, and that the man- dibular Ril is fused to the basis except in CVI male in which it is an articulating seg- ment. In determining homologies for the 5-seg- mented Mxp of CI-II (Fig. 41) of D. oculata, we compared the position of groups of me- dial setae to similarly positioned groups of Archimisophria discoveryi (Boxshall 1985: fig. 34). Boxshall reviewed various pro- posed segment homologies of copepod post- mandibular appendages and, basing his argument on the origin and insertion of muscles, he designated the proximal two segments of Mx2 and Mxp, each with two setiferous lobes, as the praecoxa and coxa. Based on positions of similar setal groups, we have interpreted segmental homologies for Mxp of D. oculata as a praecoxa, coxa, basis and a 2-segmented endopod. Al- though praecoxa and coxa are fused later in development (Fig. 9D), the endopod of Z). oculata remains 2-segmented throughout its development, an inference which supports Ho's (1986) description of the oithonid maxilliped. The mandible of the CVI male of Z). ocu- lata possesses two articulating endopodal segments, while the first of these segments is fused to the basis in all other nauplii and 294 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON copepodids (Figs. 2G, 4E). Homologies of mandibular segments are somewhat prob- lematical; Izawa (1987) has suggested that the naupliar mandible of all cyclopoids has a 2-segmented endopod and a basis without medial lobes. Applying this definition, Ril (Fig. 2G) of D. oculata is fused to the man- dibular basis, so that Ril with its two to four prominant spines forms a distal medial lobe of the basis. The articulating segment is Ri2. In CI the second mandibular seg- ment is comprised of the basis and fused Ril with only two of the four prominent naupliar spines remaining; the articulating segment is Ri2. This condition also is found in CII-V and CVI female (Fig. 9A). We be- lieve that an alternate hypothesis, i.e., that the naupliar inner lobe is a true lobe of the basis and not the fused Ri2, provides no unambiguous interpretation of the two free segments of CVI male. Ito (1989) hypothesized that the basis of copepod appendages originated by fusions of proximal segments of the cxopod and endopod. Our information about fusion of Rel of A2 and Ril of Mn of D. oculata supports that hypothesis. Homology by formation suggests that the outer seta on segment 1 of A2 on CII-CVI is the remnant of the naupliar exopod, and that the addition of segments and armament of leg 3 usually occurs proximally on the distal-most segment. We observed seven specimens of N6 with a small, wrinkled lobe bearing two setae which was visible within the long, fused Re 1 of the nauplius. We believe that the wrin- kled lobe is the exopod of CI. In a specimen of CI, we observed the proximal section of a single, outer seta on segment 1 of the an- tennal exopod of CII which had formed within the wrinkled-lobe exopod of CI. However, we could not determine in which one of the terminal distal setae of CI the distal section of this seta of CII seta was formed. This seta is the homologue of an exopodal seta and the seta is a remnant in copepodids of the naupliar exopod. Lucks (1927), Hulsemann & Fleminger (1975), and Hulsemann (1991b) have used formation homology during copepodid de- velopment, rather than positional or mor- phological homology, to determine segment or setal homologies of copepod appendages. We used this method to determine the fate of swimming leg armament elements. Our findings are illustrated in Fig. 13. We stud- ied three specimens of CI in which the re- organized leg 3 of CII was visible within the leg 3 bud of CI, and one specimen of CII in which the reorganized leg 4 of CIII was vis- ible within the leg 4 bud of CII. From these specimens we infer that the three setae on the outer lobe of these leg buds become the distal-most outer spine, the terminal spine and the distal-most inner seta of the exopod (Fig. 13B); two outer spines and two inner setae are newly added. Two setae on the inner lobe of the leg bud become the middle two of six setae on the endopod; one ter- minal seta, the outer seta, and two proximal inner seta are new. We studied one specimen of CII in which leg 3 of CIII was present within leg 3 of CII. The new segment of both exopod and en- dopod formed proximally to the distal ra- mal segment (Fig. 13C). On this new exo- podal segment is the older, proximal-most, outer spine, and on the new endopodal seg- ment is the older, proximal-most, inner seta. New setae of CIII not formed within a seta of CII are the inner seta of the coxa, outer seta of the basis, and the proximal-most, inner seta on each distal ramal segment. We examined two specimens of CIII in which leg 3 of CIV was visible within leg 3 of CIII. No new segments are added but the proximal-most, inner seta of the distal seg- ment of the endopod and proximal-most, inner seta and outer spine of the distal seg- ment of the exopod were not formed within an element of CIII. These elements are pre- sumed new (Fig. 13D). We studied one specimen of CIV in which leg 3 of CV was present within leg 3 of CIV. The new segment on each ramus formed VOLUME 105, NUMBER 2 295 1 1 Fig. 13. Dioithona oculata. development of leg 3: A, primary bud of copepodid I with 3 setae on outer lobe and 2 setae on inner lobe. B-E, reorganized legs of copepodids II-V respectively. Oldest segment cross-hatched, youngest segment clear, oldest intermediate segment horizontally-hatched, youngest intermediate segment ver- tically-hatched. Oldest setae from copepodid I (#rs) are long; all others are cropped and new setae are black. New setae added to copepodids II-V arc labeled #2-#5 respectively. proximal to the distal ramal segment. On this new exopodal segment are the older, proximal-most, outer spine and inner seta, and on this new endopodal segment are two older, proximal-most, inner setae of differ- ing ages (Fig. 13E). New setae of CV not formed within a seta of CIV are the small thin inner seta of Rel, the proximal-most inner seta on the distal endopodal segment, and the proximal-most inner seta and outer spine of the distal segment of the exopod. Thus, for D. oculata, new leg segments appear to divide proximally from the distal- most, and oldest, segment of each ramus. Beginning at this distal-most and oldest seg- ment, each more proximal, successive seg- ments are younger than distal neighbors. New armament elements usually are formed at the proximal edge of the distal-most ra- mal segment. Older elements may be found both proximally and distally to this proxi- mal edge. Changes in genetic regulation of element addition could produce the pattern reported by Von Vaupel Klein (1984) for Euchirella messinensis. In D. oculata a lin- ear, symmetrical sequence of youngest-to- oldest armament elements may develop if new segments are added, continuously, one molt out of register and later than the newly added armament elements. The addition of ramal segments described above agrees in general with the pattern de- scribed by Hulsemann (1991a) for Drepano- pusforcipatus. A brief discussion of the pat- tern of development for segments and armament elements of leg 3 of D. oculata appears in Ferrari (1991). 296 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON Acknowledgments T. E. Bowman and J. Reid of the Smith- sonian Institution, and S. Nishida of the University of Tokyo commented on early drafts of the manuscript. This research was supported by the Caribbean Coral Reef Eco- systems Program of the Smithsonian Insti- tution and by the EXXON Corporation. This is contribution #350 of the Caribbean Coral Reef Ecosystems Program. We thank Klaus Ruetzler for his continued interest in tiny animals. Literature Cited Ambler, J., Cloem, F., & A. Hulchinson. 1985. Sea- sonal cycles of zooplankton from San Francisco Bay.-Hydrobiologia 129:177-197. , F. Ferrari, & J. Fomshcll. 1990. Diel cycles of egg production in copepods carrying egg sacs.-EOS 71:77. , , & . 1991. 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