Calanoides natalis Brady, 1914

Bradford-Grieve, Janet M., Blanco-Bercial, Leocadio & Prusova, Irina, 2017, Calanoides natalis Brady, 1914 (Copepoda: Calanoida: Calanidae): identity and distribution in relation to coastal oceanography of the eastern Atlantic and western Indian Oceans, Journal of Natural History 51 (13 - 14), pp. 807-836 : 816-825

Calanoides natalis Brady, 1914

( Figures 1 (c, e); 5 – 11)

Calanoides natalis Brady, 1914, p. 4 , 5; pl. 1, figs, 6 – 11.

Calanoides carinatus: Vervoort, 1963, p. 81 – 82; De Decker, 1984, p. 329; Schnack, 1989, p. 142 – 146, figs 5, 6(3), 7(4), 8, 12; Ceballos et al., 2004, p. 739 – 750; Blanco-Bercial et al. 2006, p. 802.

Calanus carinatus: Brodsky, 1972 , in part, p. 64, 78 – 79, figs 77G, 100B

Calanoides c.f. carinatus: Prusova et al., 2011, p. 29 – 32, figs 5 – 8.

Type locality: Durban Bay, southwest Indian Ocean, South Africa.

Syntypes: Great Northern (Hancock) Museum, Newcastle-upon-Tyne, UK: NEWHM: 2.40 .08 (male); NEWHM: 40.09.

Material examined

Arabian Sea surface waters: 20.22° N, 58.75° E, 26 September, 2013: 10 males NIWA105465 ; 20.22° N, 58.75° E, 24 September 2013, 15 females NIWA105464 . Northeast Atlantic , Bay of Biscay 43.7° N, 6.15° W: NIWA105423 - NIWA105425 ; Benguela Current off Namibia: 26.67° S, 14.00° E, (1 nautical mile off Lüderitz), 19 January 2015: 24 females, 7 males NIWA115546 ; 23 females, 9 males NIWA115547 ; 21 females, 4 males; IMBR-Z3001 ; south of South Africa, 36.66° S, 21.54° E, 19 January 2007: 50 stage V copepodids NIWA115548 ; 28 females NIWA115549 .

Description

Female. Total length 2.53 mm (range 2.20 – 2.60 mm, mean 2.42 mm, n = 15). Prosome length 2.12 mm, urosome length 0.49 mm, prosome width in dorsal view 0.62 mm and prosome depth (dorsal to ventral) in lateral view 0.49 mm. Anterior margin of the head triangular in dorsal and lateral views, bluntly rounded in lateral view, more acutely rounded in dorsal view with anterolateral borders slightly convex ( Figure 5 (a, b)). Rostrum, extends into two long, posteriorly directed, filaments ( Figure 5 (h)). Urosome of four free somites, genital double-somite symmetrical in dorsal view, widest part at anterior one-quarter, bulges anteroventrally. The proximal width of small (30.6 µm long, 31.1 µm wide) anteroventral genital operculum (go) occupies about 21% (range 18.4 – 22.6%) of the widest width of the genital double-somite ( Figure 5 (e, f)). Pair of seminal receptacles (sr) in lateral view slant anteroventral to posterodorsal at 18° relative to posterior border of genital double somite. Caudal rami: seta I absent, setae II and III lateral, setae IV and V terminal, seta VI inner distal (seta V longest being longer than urosome including caudal rami), seta VII inserted immediately anterior to seta VI; setules decorate inner border ( Figure 5 (g)).

Antennule ( Figures 5 (c), 6(a – f)). Twenty-four-segmented extending to about posterior border of second free urosomite, ancestral segments II – IV, X – XI, XXVII – XXVIII fused, length of segments in µm ( Table 3). Most setae are naked and of modified type (ms, Weatherby et al. 1994; Lenz et al. 1996), aesthetascs (a) or vestigial aesthetascs (va), which are found on quadrithek females; two ventral-most setae on ancestral segment I and one posterior seta on each of ancestral segments XXIV – XXVI plumose; long setae on segments XXV and XXVI pseudoannulate (pa, Weatherby et al. 1994). Fleminger (1985) notes that all females have trithek setal configuration (after Giesbrecht 1892 /3, p. 103, 138) on most antennule segments (one proximal seta, one distal seta and one distal aesthetasc). Males, on the other hand, have quadrithek setal configuration on ancestral segments III, V, VII, IX and XI (one proximal seta, one distal seta and two distal aesthetascs). Nevertheless, Fleminger (1985) also found that there was antennular dimorphism among females in a number of calanid genera: he called one form ‘ trithek ’, which is the normal female, and the other form ‘ quadrithek ’, which he hypothesized is a late-juvenile, potential male that has changed sex. Both trithek and quadrithek forms were found among the present female specimens. Setation of ancestral segments of quadrithek female ( Figure 6 (a)) as follows: I – 1 ms, 1a, 2 plumose setae; II-IV – 6 ms, 2a; V – 2 ms, 1a, 1va; VI – 2 ms, 1a; VII – 2 ms, 1a, 1va; VIII – 2 ms, 1a; IX – 2 ms, 1a, 1va; X-XI – 3 ms, 2a, 1va, 1 short wide curved seta (on segment X); XII – 1 ms, 1a; XIII – 2 ms, 1a; XIV – 2 ms, 1a; XV – 1 ms, 1a; XVI – 2 ms, 1a; XVII – 1 ms, 1a; XVIII – 2 ms, 1a; XIX – 1 ms, 1a; XX – 2 ms, 1a; XXI to XXIII – 1 ms, 1a; XXIV – 1 ms, 1a + 1pa (plumose); XXV – 1 ms, 1a + 1pa (plumose); XXVI – 1 ms + 1pa (plumose); XXVII – XXVIII – 6 ms, 1a.

Setation of ancestral segments of trithek female ( Figure 6 (e, f)) as follows: I – 1 ms, 1a, 2 plumose setae; II-IV – 6 ms, 2a; V – 2 ms, 1a; VI – 2 ms, 1a; VII – 2 ms, 1a; VIII – 2 ms, 1a; IX – 2 ms, 1a; X-XI – 3 ms, 2a, 1 short wide curved seta (on segment X); XII – 1 ms, 1a; XIII – 2 ms, 1a; XIV – 2 ms, 1a; XV – 1 ms, 1a; XVI – 2 ms, 1a; XVII – 1 ms, 1a; XVIII – 2 ms, 1a; XIX – 1 ms, 1a; XX – 2 ms, 1a; XXI and XXII – 1 ms, 1a; XXIII – 1 ms; XXIV – 1 ms, 1a + 1pa (plumose); XXV – 1 ms, 1a + 1pa (plumose); XXVI – 1 ms + 1pa (plumose); XXVII – XXVIII – 6 ms, 1a.

Antenna ( Figure 6 (g)) with separate coxa and basis; coxa with one long inner plumose seta, basis with two long inner setae each with rows of short setules. Exopod slightly longer than endopod; endopod two-segmented although line of fusion between segments 2 and 3 visible on posterior surface and marked by row of small spinules; segment 1 with two inner setae and distal outer patch of outer setules, terminal segment with 8 + 7 setae; exopod with segments I and II fused, segments III – IV fused – fusion line visible; ancestral segments I – VIII each with long plumose seta, terminal segment IX – X with 1 + 3 terminal setae.

Mandible ( Figure 7 (a)) coxal gnathobase damaged with opaline teeth missing, largest tooth ventral, separate from adjacent four teeth by wide gap; four small teeth follow and a longer dorsal tooth. Lash-like element broken off illustrated specimen. Basis with four inner setae; endopod two-segmented, segment 1 with large inner lobe, four distal inner setae and outer distal setules, segment 2 with 11 terminal setae, two of them shorter and row of outer setules; exopod five-segmented with 1,1,1,1,2 setae.

Maxillule ( Figure 7 (b)) praecoxal arthrite with full complement of 15 setae (four of them on posterior surface, one on anterior surface) and three or four large wide spines, and two to five small spines on posterior surface located midproximally; coxal endite with four terminal setae, epipodite with nine setae; basal endites 1 and 2 with four and four setae, respectively; exite with one seta; basis and endopod separate; endopod twosegmented with segments 1 and 2 fused – fusion line visible, with three, four, seven setae and five spinules on anterior surface; exopod with 11 setae.

Maxilla ( Figure 7 (c)) praecoxal endites 1 and 2 with 6 + 1 small and three setae, respectively; endites 2 and 3 on coxa with three and three setae, respectively, epipodite with one long plumose seta; endite 5 of basis longest with four setae, one of them heavier; endopod segment 1 with well-developed lobe bearing two short + one large setae, endopod segments 2 – 4 with two, two, three setae, respectively. Inner surfaces of endites 2 – 5 each with one seta that is shorter and more densely lined with long spinules than other setae; endopod segments 2 and 3 with inner setae shorter than outer setae.

Maxilliped ( Figure 7 (d)) directed ventrally so that setae on syncoxa and basis directed into animal ’ s midline; syncoxa with one, two, four, four setae; basis with three setae; endopod segment 1 partly separate bearing two setae; endopod segments 2 – 6 with the following setae – 4, 3, 2, 2 + 1, 3 + 1 –, respectively.

Legs 1 – 5 ( Figure 8 ) biramous, each ramus three-segmented with following setal formulae (Roman numerals indicate spines, Arabic numerals setae, outer border setation listed to the left in each group separated by ‘; ’):

Leg 1 (Coxa 0 – 1. Basis 0 – 1. Exopod I-1; I-1; II,1,4. Endopod 0 – 1; 0 – 2; 1,2,3);

Leg 2 (Coxa 0 – 1. Basis I-0. Exopod I-1; I-1; II,1,5. Endopod 0 – 1; 0 – 2; 2,2,4);

Leg 3 (Coxa 0 – 1. Basis I-0. Exopod I-1; I-1; II,1,5. Endopod 0 – 1; 0 – 2; 2,2,4);

Leg 4 (Coxa 0 – 1. Basis 1 – 0. Exopod I-1; I-1; II,1,5. Endopod 0 – 1; 0 – 2; 2,2,3);

Leg 5♀ (Coxa 0 – 0. Basis 1 – 0. Exopod I-0; I-1; II,1,4. Endopod 0 – 1; 0 – 1; 0,2,2).

Leg 1 distal posterolateral corner of endopod segment 1 with broadly triangular extension that cups segment 2 on the posterior surface, segments 2 and 3 outer distal corners usually pointed; proximoposterior surface of exopod segment 1 bearing small lobe. Leg 5 extends beyond posterior border of caudal rami, with outer distal corner of endopod segment 1 pointed; pore openings on anterior surface at base of outer border spines.

Male. Total length 2.41 mm, prosome 1.88 mm, prosome greatest width 0.50 mm, urosome length 0.50 mm. (Total length range 2.10 – 2.4 mm, mean 2.20 mm, n = 10.) Anterior margin of the head rounded in both dorsal and lateral views ( Figure 9 (a, b)). Rostrum extends into two long, ventroposteriorly directed, tapering filaments that extend as far as labrum ( Figure 9 (d)). Cephalic dorsal hump anterior border at about one-third the length of cephalosome. Urosome of five free somites, genital somite short, urosomite II as long as wide. Caudal rami extend laterally; seta I absent, setae II and III lateral, setae IV and V terminal (seta V longest), seta VI on inner border, seta VII inserted at inner distal corner.

Antennules ( Figure 9 (c), 10(a – d)) 22-segmented and extends as far as caudal rami when held straight posteriorly, symmetrical, with ancestral segments I – IV, V – VI, XXVII – XXVIII fused, IX – X partly fused on ventral surface, X – XI partly fused on posterodorsal surface. Aesthetascs larger than in female, doubled on segments III, V, VII, IX, XI. Most setae of modified (ms) type or aesthetascs (a); long setae on ancestral segments V, XXV, XXVI are of a ‘ pseudoannulate ’ type (pa) ( Weatherby et al. 1994). The distal-most, non-aesthetasc setae of segments X and XI foreshortened and clavate, respectively ( Figure 10 (d)). The proximal seta of ancestral segment III differs from other short mixed modality setae of most segments in that it is longer and with bluntly terminating tip. Setation of segments as follows: I – IV – 9 ms, 5a (proximal seta on ancestral segment III elongate and with bluntly round tip); V – VI – 3 ms, 1pa, 3a; VII – 2 ms, 2a; VIII – 2 ms, 1a; IX – XI – 6 ms, 5a; XII – 1 ms, 1a; XIII – 2 ms, 1a; XIV – 2 ms; 1a; XV to XX – 1 ms, 1a; XXI – 1a; XXII to XXIII – 1 ms, 1a; XXIV – 1 + 1 ms, 1a; XXV – 1pa+1 ms, 1a; XXVI – 1pa+1 ms; XXVII – 2 + 1 ms; XXVIII – 3 ms, 1a.

Antenna, mandible, maxillule, maxilla and maxilliped sexually dimorphic with reduced setation. Antenna ( Figure 10 (e)) with separate coxa and basis; coxa with one short inner seta and inner tuft of setules, basis with two setae one of them vestigial. Exopod slightly longer than endopod; endopod two-segmented; segment 1 with two inner, short setae; terminal segment with 7 + 6 setae and patch of setules on outer border and; exopod with segments I – II fused, usually with two vestigial setae; segments III – V fused, with vestigial seta on each of segments II and IV and long plumose seta on segment V; segments VI to VIII each with long plumose seta; terminal segment IX – X with 1 + 3 terminal setae (one seta slight).

Mandible ( Figure 10 (f)) coxal gnathobase very reduced with teeth scarcely developed. Basis with one medium inner setae plus one vestigial seta and small process; endopod two-segmented, segment 1 with inner lobe and two distal inner setae, segment 2 with eight terminal setae; exopod five-segmented with 1,1,1,1,2 setae.

Maxillule ( Figure 10 (g)) praecoxal arthrite reduced with about six vestigial spines; coxal endite with two or three vestigial terminal setae, epipodite with seven long setae; basal endite 1 with three or four reduced setae, basal endite 2 with four reduced setae; exite without seta; basis and endopod separate; endopod three-segmented, with three, three, seven reduced setae; exopod with 10 + 1 vestigial setae.

Maxilla ( Figure 10 (h)) very reduced, about same size as syncoxa of maxilliped. Praecoxal endites 1 and 2 with one medium and two vestigial setae and two setae, respectively; endites 3 and 4 on coxa with two, two medium and one vestigial setae, respectively; epipodite without seta; endite 5 of basis with three medium setae; endopod segment 1 with short lobe bearing one medium seta; endopod with four setae.

Maxilliped ( Figure 10 (i)) reduced, syncoxa with variable setation: endites 1 – 3 with 0/1 seta, 0/1 small seta, 0/1/4 small setae, respectively, endite 4 with three reduced terminal spinules of variable size ( Figure 10 (i – k)); basis with three setae; endopod segment 1 separate bearing two setae; endopod segments 2 – 6 with 4, 3, 2, 2 + 1 enlarged plumose, 3 + 1 enlarged plumose setae, respectively; enlarged setae directed proximally towards base of limb.

Legs 1 – 4 as in female. Leg 5 ( Figure 9 (f, g)) with following setal formulae (Roman numerals indicate spines, Arabic numerals setae, outer border setation listed to the left in each group separate by ‘; ’):

Leg 5 ♂ left (Coxa 0 – 0. Basis 1 – 0. Exopod I-0; I-0; II,1,0. Endopod 0 – 0; 0 – 0; 0,I,0);

Leg 5 ♂ right (Coxa 0 – 0. Basis 1 – 0. Exopod I-0; I-1; II,1,0. Endopod 0 – 0; 0 – 0; 0,2,2).

Leg 5 ( Figure 9 (f, g)) asymmetrical, left leg 5 longest, extends beyond caudal rami when held straight posteriorly; coxa and basis longer than those of right leg; when fifth legs extended straight, border between exopod segments 2 and 3 distal to distal border of right leg exopod segment 2; exopod segment 2 length/width (C ’ /c ’) = 2.55; length of terminal spine of exopod segment 3 relative to length of its segment (A ’ /B ’) = 0.81; exopod segment 3 length/width (F/b ’) = 2.50; exopod segment 3 with five patches of fine setules on anterior surface. Right leg 5 endopod extends slightly short of distal border of exopod segment 2 – (C + D)/E = 1.11; length of exopod segment 3 relative to terminal spine (B/A) = 1.60.

Morphological variability

We note that among specimens from a single location there is a large degree of variability in the proportions of the male leg 5 ( Table 4). This variability extends to actual deformity, observed in one specimen from the Arabian Sea in which the left exopod segment 2 was short and swollen internally and exopod segment 3 was elongate. On the right, exopod segment 3 was shorter and broader than usual and had a very short terminal spine.

Comparisons made of the proportions of the male leg 5 of specimens from the Arabian Sea and off Namibia ( Table 4) gave contrasting results. There were no statistically significant differences between Arabian Sea and Namibian specimens ( Table 4) for the ratios A/F ‘, B/A, C + D/F, C ’ /c ‘, F/b ’ and b/c ‘ ( Figures 3 , 11 ). There appeared to be statistically significant differences in the ratios A ’ /B ‘ B/C, G/B ’ and G/H at α = 0.05. However, these differences are very subtle (10, 4, 9, 16%, respectively) and could be put down to the large number of tests increasing the probability of making a type I error. In applying a sequential Bonferroni test, only the difference in the G/H ratio was statistically significant.

Figures

Figure 1. Photomicrographs of whole female (a–d) specimens in lateral view with antennules removed, and male (e) of: (a) Calanoides brevicornis (= Calanoides macrocarinatus) from 250–500 m, 42.41° S, 174.03° E; (b) Calanoides carinatus from 0–10 m, 43.67° S, 64.97° W; (c) Calanoides natalis from surface waters, Arabian Sea, 20.22° N, 58.75° E; (d) Calanoides philippinensis lateral view, Aru Basin, about 6° S, 133.5° E; (e) C. natalis from the Arabian Sea 20.22° N, 58.75° E. The Calanoides carinatus photo was made available by Drs Georgina Cepeda and Marina Sabatini (Consejo Nacional de Investgaciones Cientificas y Tecnicas, Argentina). Scale bar represents 0.5 mm.

Figure 3. Calanoides male leg 5 indicating the measurements made, from which the ratios in Table 4 were calculated. (A) Length of distal spine on right exopod segment 3; (B) length of right exopod segment 3 measured along inner border; (b) width of right exopod segment 3 measured at its widest part; (C) length of right exopod segment 2 measured along inner border; (D) length of right exopod segment 1 measured along inner border; (E) total length of right endopod; (A’) length of terminal spine on left exopod segment 3; (B’) length of left exopod segment 3 measured along inner border; (b’) width of left exopod segment 3 measured at its widest part; (C’) length of left exopod segment 2 measured along inner border; (c’) width of left exopod segment 2 measured at its widest part; (F) length of left exopod segment 3 measured along outer border; (G) length of outer distal spine on left exopod segment 2; (H) distance between proximal border of left exopod 3 and base of lateroproximal spine of exopod segment 3.

Figure 5. Calanoides natalis female: (a) dorsal view; (b) lateral view; (c) antennule; (d) genital doublesomite, lateral view; (e) genital double somite, dorsal view; (f) genital operculum (go) and left seminal receptacle (sr); (g) caudal ramus ventral view; (h) anterior head, ventral view. Scale bars represent 1.0 mm on figures (a–c) and 0.1 mm on the rest.

Figure 6. Calanoides natalis female: (a) quadrithek antennule, ancestral segments I–XIX; (b) quadrithek antennule, ancestral segments XX–XXVIII; (c) quadrithek antennule, ancestral segments X–XI; (d) quadrithek antennule, ancestral segments XXVII–XXVIII; (e) trithek antennule segments I–XI; (f) trithek antennule, ancestral segment XXIII; (g) antenna. a – aesthetacs; pa – pseudoannulate seta; va – vestigial aesthetasc. Scale bars represent 0.1 mm.

Figure 7. Calanoides natalis female: (a) mandible; (b) maxillule; (c) maxilla; (d) maxilliped. Scale bar represents 0.1 mm.

Figure 8. Calanoides natalis female: (a) Leg 1 coxa, basis and endopod; (b) leg 1 exopod; (c) leg 2, anterior surface; (d) leg 3, posterior surface; (e) leg 4, posterior surface; (f) leg 5, anterior surface. Scale bar represents 0.1 mm.

Figure 9. Calanoides natalis male: (a) dorsal view; (b) lateral view – note specimen laterally compressed c.f. Figure 8; (c) antennule; (d) anterior head, lateral view; (e) left caudal ramus, dorsal view; (f) leg 5, posterior view; (g) left leg 5 exopod segment 3. Scale mark 1.0 mm on figures a–d, 0.1 mm on rest.

Figure 10. Calanoides natalis male: (a) antennule ancestral segments I–XVII; (b) antennule ancestral segments XVIII–XXVIII; (c) antennule ancestral segments XXVII–XXVIII, setal numbers refer to numbering system of Weatherby et al. (1994); (d) antennule ancestral segments X and XI;(e) antenna;(f) mandible;(g) maxillule; (h) maxilla; (i) maxilliped; (j, k) maxilliped syncoxae from Benguela Current. Scale bars 0.1 mm.

Figure 11. Variability in distal part of left leg 5 of Calanoides natalis: (a–d) from off Namibia; (e–i) from the Arabian Sea. Note specimen (g) has stout outer distal spine on segment 2 and many other specimens have this spine attenuated and apparently easily broken e.g. (d) and (i).