Eucyclops azorensis Defaye & Dussart, 1991

Hołyńska, Maria, Sługocki, Łukasz, Ghaouaci, Souad & Amarouayache, Mounia, 2021, Taxonomic status of Macaronesian Eucyclops agiloides azorensis (Arthropoda: Crustacea: Copepoda) revisited - morphology suggests a Palearctic origin, European Journal of Taxonomy 750, pp. 1-28 : 4-14

Eucyclops azorensis Defaye & Dussart, 1991

Figs 1−6 ; Tables 1−3 , 5

Eucyclops agiloides açorensis Defaye & Dussart, 1991: 121−126 , figs 2−14.

Eucyclops agiloides azorensis − Dussart & Defaye 2006: 38. — Alekseev 2019 (part): 499−501. Eucyclops leschermoutouae − Ghaouaci et al. 2017: 90. — Ghaouaci 2018: 64−67, figs 14−18.

Material examined

Paratypes

PORTUGAL • 2 ♀♀, 1 ♂; Azores, Flores Island, nº15245 , Ribeira Funda ; 20 Oct. 1971; Th. Monod leg.; MNHN Cp. 611 .

Other material

ALGERIA • 4 ♀♀, 2 ♂♂; Tébessa, Ain-Kemellal ; 35°22′09.8″ N, 7°34′51.3″ E; 903 m a.s.l.; 21 Apr. 2016; S. Ghaouaci leg.; salinity 4−7 ppt; surface area 1 ha; temporary pool; MIZ 1/2021/8 to 1/2021/13 • 3 ♀♀, 3 ♂♂ (mounted for SEM); same collection data as for preceding; MIZ .

PORTUGAL • 3 ♀♀, 1 ♂; Madeira Island, Ribeira de São João, Stn 1; 32°41′28.7″ N, 16°56′05.8″ W; water depth 0.5 m; 16 Sep. 2019; Ł. Sługocki leg.; water temp. 20.2°C; pH 7.4; conductivity 88.1 μS/cm; dissolved oxygen 9.46 mg /L; stream, rock pool without macrophytes; transparent water; MIZ 1/2021/1 to 1/2021/4 • 1 ♀; Madeira Island, ponds SE hills, Stn 3; 32°43′04.4″ N, 16°54′08.0″ W; water depth 3 m; 26. Sep. 2019; Ł. Sługocki leg.; water temp. 15°C; pH 7.2; conductivity 55 μS/cm; dissolved oxygen 5.34 mg /L; old seminatural reservoir with macrophytes and algae; fresh water supply; MIZ 1/2021/5 • 1 ♀; Madeira Island, Ribeiro de Frio, Stn 3; 32°44′19.6″ N, 16°54′13.6″ W; water depth 0.05 m; 23 Sep. 2019; Ł. Sługocki leg.; water temp. 15.1°C; pH 7.8; conductivity 130 μS/cm; dissolved oxygen 8.98 mg /L; stream, large rock pools with macrophytes and algae; MIZ 1/2021/6 • 1 ♀; Madeira Island, Ribeira de Machico, Stn 2; 32°44′09.3″ N, 16°47′57.9″ W; water depth 0.1 m; 16 Sep. 2019; Ł. Sługocki leg.; water temp. 19.5°C; pH 7.7; conductivity 193 μS/cm; dissolved oxygen 7.91 mg /L; stream, small rock pools with dominance of algae and emergent macrophytes; MIZ 1/2021/7 .

Comparative material

Eucyclops serrulatus

NETHERLANDS • 2 ♀♀; Friesland, 4 km E of Leeuwarden, Tytsjerk municipality, park; 53°12′ N, 5°54′ E; 19 Nov. 2008; M. Hołyńska & P. Koomen leg.; pond shore; MIZ 1/2021/14 to 1/2021/15 .

POLAND • 1 ♀; Mazovian Voivodeship, Milanówek ; 52°07.45′ N, 20°39.9′ E; 21 Aug. 2016; M. Hołyńska leg.; shallow pond with dense vegetation; MIZ 1/2021/18 • 1 ♀; West Pomeranian Voivodeship, Korytnica River ; 53°08.7′ N, 15°52.5′ E; 2 Jun. 2016; M. Hołyńska leg.; river shore; MIZ 1/2021/19 .

SWEDEN • 2 ♀♀; Lund , Botanical Garden; 55°42′ N, 13°12′ E; 9 Nov. 2008; M. Hołyńska leg.; pond littoral; MIZ 1/2021/16 to 1/2021/17 .

UKRAINE • 2 ♀♀; Danube ; V.I. Monchenko Collection; IZAN .

Description

Female (character states are shared by all specimens examined, unless stated otherwise)

HABITUS. Medium-sized Eucyclops , total body length ca 1 mm ( Fig. 1A ) − comparison of morphometric characters among Azorean, Madeiran and Algerian populations shown in Table 1 . Prosomal and urosomal somites often adorned with shallow pits ( Fig. 1B, D ). Pediger 4 with fine hairs at posterolateral angle and small spinules on lateral margin ( Figs 2A , 3A ). Pediger 5 posterolaterally bearing long and robust hairs. Genital double-somite as long or slightly shorter than wide ( Table 1 ). Single large copulatory pore oval shaped, located ventrally in anterior fifth of somite. Seminal receptacle as common in genus (cf. Fig. 8B ), anterior and posterior parts short in length, posterior part wider than anterior. Anal operculum nearly straight, anal sinus with 1-1 longitudinal row of spinules. Posterior margin of anal somite with continuous row of spinules. Caudal rami 3.5−6.0 times as long as wide ( Defaye & Dussart 1991, see also Table 1 for interpopulation variation), no hairs on medial margin. ʻSerraʼ (longitudinal row of spinules) on lateral margin extending from insertion of anterolateral (II) caudal seta to anterior ⅓−⅕ of rami, more anterior spinules shifted to ventral surface and can be unnoticed in dorsal view ( Fig. 1C ). Spinules present at insertion of posterolateral (III) caudal seta. Single pore present on ventral surface near lateral margin, slightly posterior to midpoint of ramus. Seta III with fine setules medially and short spinules laterally. Dorsal (VII) caudal seta shorter, while terminal accessory (VI) seta longer than posterolateral caudal seta ( Table 1 ).

ANTENNULE. 12-segmented, extending slightly beyond cephalothorax. Setation formula as common in genus: 1(I−V): 8 s; 2(VI−VII): 4 s; 3(VIII): 2 s; 4(IX−XI): 6 s; 5(XII−XIII): 4 s; 6(XIV): 1 s + 1 sp; 7(XV−XVI): 2 s; 8(XVII−XX): 3 s; 9(XXI−XXIII): 2 s + 1 ae; 10(XXIV): 2 s; 11(XXV): 2 s + 1 ae; 12(XXVI−XXVIII): 7 s + 1 ae. Aesthetasc on segment 9 short ( Fig. 2B ), 11−15 μm in length, not reaching beyond distal margin of segment. Aesthetasc on penultimate segment 30−34 μm long, almost reaching insertion of medial seta of segment 12. Segments 10−12 with smooth/finely serrate hyaline membrane. First antennulary segment bearing long spinules on ventral surface, spinules absent on other segments. Pits sometimes present on dorsal surface of more proximal antennulary segments ( Fig. 1D ). Terminal segment 4.3−6.3 times as long as wide.

ANTENNA. Composed of coxobasis and three-segmented endopodite, and bearing 3, 1, 9 and 7 setae, respectively. Exopodite seta reaching distinctly beyond enp3, and bearing long setules proximally and short setules more distally ( Fig. 2C ). Coxobasis ( Figs 2C , 3B ) caudally ornamented with: hair-like spinules on proximolateral margin; longitudinal double rows near lateral margin, spinules in distal row sometimes distinctly smaller than those in proximal row; few small spinules near insertion of exopodal seta; transverse row at height of insertion of medial setae; oblique row below insertion of medial setae; and one or more groups of tiny spinules more proximally in medial half of segment. Spinules absent near distal margin. Frontal surface of antennal coxobasis ( Figs 2D , 3C ) with longitudinal row of spinules (6−15) along lateral margin and one or two oblique rows of long spinules and small spinules near proximal margin. Long hair-like spinules absent on distal and mediodistal margin.

MOUTHPARTS. Labrum (cf. Fig. 8G ). Distal margin with 9−12 teeth (some of those tiny), small spinules present on laterodistal lobes. Distal fringe hairs arranged in 1-1 group. Tiny spinules present on lateral margin at height of posterior end of epistoma in Madeiran and Algerian females − this character could not be verified in paratype specimens. Paragnaths with 4 (3+1) medial claws, as common in Cyclopidae . Mandible ( Fig. 2E ) with palp bearing two long and one short setae. Near palp transverse row of long spinules and smaller spinules arranged in oval pattern present on anterior surface of coxal gnathobase. Maxillule setation as common in Cyclopidae . Maxillulary palp ( Figs 1E , 2F ) naked, with one proximal and three apical setae, lateral lobe bearing three setae. Armature of maxilla (cf. Fig. 9 D−E) as common 1. = body length (μm); 2. = cephalothorax, length/ width; 3. = genital double-somite, length/ width; 4. = length of prosome/ length of urosome; 5. = length of caudal seta V/ length urosome; 6. = P5, length of medial spine/ length of segment; 7. = P5, length of apical seta /length of segment; 8. = P5, length of lateral seta / length of segment; 9. = caudal ramus, length/ width; 10. = length of caudal seta II/ length of caudal ramus; 11. = distance of insertion of caudal seta II, measured from posterior end of ramus/ length of caudal ramus; 12. = caudal setae, VII / III; 13. = caudal setae, VI /III; 14. = caudal setae, V/ III; 15. = caudal setae, IV/ III; 16. = length of caudal seta VI/ length of caudal ramus; 17. = length of caudal seta V /length of caudal ramus; 18. = length of caudal seta IV/ length of caudal ramus; 19. = length of caudal seta III/ length of caudal ramus; 20. = P4, length of coxopodite seta /height of medial expansion of basipodite; 21. = P4 enp3, length/width; 22. = P4 enp3, medial terminal spine /lateral terminal spine; 23. = P4 enp3, medial terminal spine/ segment length.

in Eucyclops , endopodite 2-segmented. Praecoxopodite and coxopodite separated on caudal surface and partially fused on frontal surface. Spinules distinctly large (cf. Fig. 9E , marked with arrow) or sometimes small near lateral margin of praecoxopodite on caudal surface. Armature of maxilliped (cf. Fig. 9 F−G) as common in Eucyclops , arthrodial membrane between terminal endopodal segment and its medialmost seta failed to form. Spinules on caudal surface of basipodite arranged in two transverse rows. Small flaplike structure present on frontal surface near lateral margin of syncoxopodite (cf. Fig. 9G , marked with arrow); tiny spinules on edge of flap observed in Madeiran and Algerian specimens. Frontal surface of syncoxopodite sometimes (some Madeiran and Algerian specimens) adorned with one or two rows of fine spinules, near flap-like structure.

P1−P4. Setation as common in Eucyclops ( Table 2 ). P1 intercoxal sclerite ( Figs 1F , 4 A−B) frontally naked or with few short spinules. P2−P4 intercoxal sclerites with spinules arranged in 1-1 group on frontal surface; spinules hair-like in P2 and short in P3 and P4. Intercoxal sclerite caudally bearing single transverse row of short spinules in middle of segment in P1, and hairlike spinules in two or three transverse rows in P3−P4. Intercoxal sclerite caudally naked or bearing one or two transverse rows of spinules (or hairs) in P2. Free margin of P4 intercoxal sclerite naked ( Fig. 3D ) or sparsely pilose ( Fig. 4C ) in middle section. P1−P3 coxopodite setae homonomously setulose (long and fine setules in P1, short and spinule-like setules in P2−P3). P4 coxopodite seta heteronomously setulose. Proximal setules sometimes distinctly longer than those more distally; medial (inner) margin with continuous setulation, while on lateral (outer) margin setules proximally missing or discontinuous (‘gaps’), or sometimes continuous (Madeira, Ribeiro de Frio). Spinule pattern on caudal surface of P4 coxopodite ( Figs 3D , 4C ) as common in genus; number of spinules 8−14 in transverse row along distal margin, lateralmost spinule the longest one. Basipodite medially pilose in P1−P4 ( Figs 3D , 4A, C ), hairs long and fine in P1−P3, and shorter and thick in P4. Medial seta of P1 basipodite heteronomously setulose ( Fig. 4A ), bearing distinctly long setules on medial margin in proximal half, and shorter setules on lateral margin and more distal part of seta. With exception of P1 exp2, which is laterally pilose, all exopodal segments laterally naked (see P4 exopodite in Fig. 3 D−E). Spatulate modification (relatively short and flattened setae, with short setules) of setae on terminal exopodal and endopodal segments of P2−P4 sometimes occur (Madeira, Machico). Cuticle of inner, proximal margin of P4 enp2 ( Figs 3F , 4C , marked with arrow) thicker than in other parts of P4. None of setae of P4 enp3 reaching beyond tip of longer (medial) terminal spine.

P5 ( Fig. 1G ). One-segmented with three appendages. Medial spine strong and about twice as long as segment ( Table 1 ). Apical seta nearly as long or slightly longer (<1.5 ×) than medial spine, lateral seta slightly shorter but sometimes longer than medial spine. Small spinules present at insertion of medial spine.

Male ( Fig. 1H )

Only those features are mentioned, which differ from the corresponding character states in female. HABITUS. Total body length 0.69−0.95 mm (for morphometric data see Table 3 ). Pediger 4 and pediger 5 lacking posterolateral hairs. Length and width proportion of caudal rami 2.9−4.1. ʻSerraʼ absent on caudal rami ( Fig. 1I ), yet spinules present at insertion of anterolateral and posterolateral caudal setae.

ANTENNULE ( Figs 1J , 4D ). 16-segmented. Setation formula of antennule: 1(I−V): 8 s (incl. 2 modified brush setae) + 1 ae (distal); 2(VI−VII): 4 s (incl. 1 brush seta); 3(VIII): 2 s (incl. 1 brush seta); 4(IX): 2 s (incl. 1 brush seta) + 1 ae; 5(X): 2 s (incl. 1 brush seta); 6(XI); 2 s; 7(XII): 2 s; 8(XIII): 2 s; 9(XIV): 1 s + 1 sp + 1 ae; 10(XV) 2 s; 11(XVI) 2 s; 12(XVII) 2 s; 13(XVIII) 2 s + 1 ae; 14(XIX−XX): 2 s + 1 small cone + 1 plate; 15(XXI−XXIII): 1 s + 1 small cone + 2 plates + 1 ae; 16 (XXIV−XXV and XXVI−XXVIII): 4 s + 1 ae and 7 s + 1 ae. Aesthetascs on segment 1, 4, and 9 distinctly long: ~ 112 μm, 85 μm, and 61 μm, respectively (measured in Madeiran male).

ANTENNA. Antennal coxobasis ( Figs 1K , 4 E−F): spinule ornamentation reduced on caudal surface in medial half of segment ( Fig. 4E ).

MOUTHPARTS. Maxillar praecoxopodite, caudal surface: spinules absent near lateral margin.

LEGS. P4 intercoxal sclerite naked frontally and sparsely pilose on caudal surface ( Fig. 4G ). Cuticle of inner, proximal margin of P4 enp2 not thicker than in other parts of P4. Setae of P4 enp3 usually not reaching beyond tip of longer (medial) terminal spine – in male from Madeira, setae reached slightly beyond tip of corresponding spine. Leg 6 with three appendages: medial spine 36−48 μm long, not reaching posterior margin of succeeding urosomal somite (Azores, Madeira) or extending slightly beyond it ( Algeria); median seta 27−32 μm; and lateral seta 34−40 μm (length proportions in Table 3 ).

Geographic distribution ( Fig. 5 )

Azores (widely distributed in Santa Maria, Terceira, Pico, Faial and Flores islands − see Defaye & Dussart 1991), Madeira and North Africa ( Algeria, Tébessa and Souk-Ahras Provinces).

Habitats ( Fig. 6 )

Fresh and brackish, both temporary and permanent waterbodies: rock pools in creek (river) bed, ponds, reservoirs, rivers, creek marshes, livestock water troughs, and fishponds.

1. = body length (μm); 2. = cephalothorax, length/ width; 3. = genital double-somite, length/ width; 4. = length of prosome/ length of urosome; 5. = length of caudal seta V/ length urosome; 6. = P5, length of medial spine/ length of segment; 7. = P5, length of apical seta /length of segment; 8. = P5, length of lateral seta / length of segment; 9. = caudal ramus, length/ width; 10. = length of caudal seta II/ length of caudal ramus; 11. = distance of insertion of caudal seta II, measured from posterior end of ramus/ length of caudal ramus; 12. = caudal setae, VII / III; 13. = caudal setae, VI /III; 14. = caudal setae, V/ III; 15. = caudal setae, IV/ III; 16. = length of caudal seta VI/ length of caudal ramus; 17. = length of caudal seta V /length of caudal ramus; 18. = length of caudal seta IV/ length of caudal ramus; 19. = length of caudal seta III/ length of caudal ramus; 20. = P4, length of coxopodite seta /height of medial expansion of basipodite; 21. = P4 enp3, length/width; 22. = P4 enp3, medial terminal spine /lateral terminal spine; 23. = P4 enp3, medial terminal spine /segment length; 24. = P6, length of median seta/ length of medial spine; 25. = P6, length of lateral seta/ length of medial spine.

Figures

Fig. 1. Eucyclops azorensis Defaye & Dussart, 1991 (Algeria, Ain-Kemellal; MIZ), SEM micrographs. A−G. ♀. H−K. ♂. A. Habitus, lateroventral view. B. Last two urosomal somites, ventral view – note the integumental ornamentation of shallow pits. C. Caudal rami, ventral view. D. Rostrum area of the cephalothorax and first antennulary segments. E. Maxillulary palp. F. Leg 1, frontal view. G. Leg 5 and leg 6. H. Habitus, ventral view. I. Caudal rami, ventral view – note the lack of ʻSerraʼ on the lateral margin. J. Antennule, modified setae indicated by arrows on segments 4 and 5. K. Antennal coxobasis, frontal view. A–B, E show ♀-2; C–D, F show ♀-1; G shows ♀-3; H–I show ♂-2; J shows ♂-1; K shows ♂-3. Scale bars: A, H = 200 μm; B−G, I−K = 20 μm.

Fig. 2. Eucyclops azorensisDefaye & Dussart, 1991, ♀ (Azores, paratypes; MNHN Cp. 611). A. Pediger 4, lateral section, dorsal view. B. Antennulary segments 8−10, dorsal surface − note short aesthetasc on segment 9. C. Antennal coxobasis and first and second endopodal segments, caudal view – note the suture line between basipodite and coxopodite. D. Antennal coxobasis, frontal view. E. Mandible. F. Maxillule. A, C−F show ♀-1; B shows ♀-2. Scale bars: A−F = 50 μm.

Fig. 3. Eucyclops azorensis Defaye & Dussart, 1991, ♀ (Algeria, Ain-Kemellal; MIZ). A. Pediger 4 dorsal surface − note hairs at posterolateral angle. B. Antennal coxobasis, caudal view (inner medial seta broken). C. Antennal coxobasis and first endopodal segment, frontal view. D. Leg 4, protopodite and first exopodal and endopodal segments, caudal view. E. Leg 4, second and third exopodal segments, caudal view, (tips of some terminal setae were broken, seta length was reconstructed based on setae on the other side). F. Leg 4, second and third endopodal segments, caudal view – note thickened cuticle in inner proximal margin of second endopodite (arrow). A shows MIZ 1/2021/11; B−F show MIZ 1/2021/10. Scale bars: A−F = 50 μm.

Fig. 4. Eucyclops azorensis Defaye & Dussart, 1991 (Azores, paratypes; MNHN Cp. 611). A−C. ♀. D−G. ♂. A. Leg 1, frontal view − medial seta of basipodite is figured separately. B. Leg 1 intercoxal sclerite, frontal view. C. Leg 4, protopodite and first and second endopodal segments, caudal view – note thickened cuticle in inner proximal margin of second endopodite (arrow). D. First antennulary segment with two modified brush setae (arrows) and one aesthetasc (shaded), ventral view. E. Antennal coxobasis, caudal view. F. Antennal coxobasis and first endopodal segment, frontal view. G. Leg 4, caudal view. A shows ♀-2; B−C show ♀-1; D−G show ♂-1. Scale bars: A−G = 50 μm.

Fig. 5. Geographic distribution of Eucyclops azorensis Defaye & Dussart, 1991. Filled black circles show occurrences verified by the authors, and open circles show records taken from literature (Defaye & Dussart 1991; Ghaouaci et al. 2017; Ghaouaci 2018).

Fig. 6. Habitat variation in Eucyclops azorensis Defaye & Dussart, 1991. A−D. Madeira, Portugal. E. Tébessa, Algeria. A. Ribeiro de Frio, flowing water. B. Seminatural freshwater pond. C. Ribeira de São João, nearly standing water. D. Ribeira de Machico, flowing water. E. Brackish pond at Ain Kemellal.

Fig. 8. Eucyclops agiloides (G.O. Sars,1909), ♀ (Lake Tanganyika, Kirando; NHM). A. Pediger 4, dorsal view. B. Pediger 5 and genital double-somite (leg 5 is not figured), ventral view. C. Leg 5. D. Anal somite and caudal rami, dorsal view. E. Antennal coxobasis and first endopodal segment, caudal view. F. Antennal coxobasis, frontal view. G. Labrum – ʻepiʼ shows epistoma, laterodistal lobe is indicated by arrow. H. Paragnaths, ventral view (3+1 medial claws inserted on opposite surface of both paragnaths are not figured). A, D−H show ♀-1; B−C show ♀-2. Scale bars: A−H = 50 μm.

Fig. 9. Eucyclops agiloides (G.O. Sars,1909), ♀ (Lake Tanganyika, Kirando; NHM). A. Mandible, anterior view.B−C. Variation of the spinule ornamentation of the maxillulary palp. B. ♀-1 (one apical seta is broken off). C. ♀-3. D. Maxillar basipodite and two-segmented endopodite, caudal view. E. Maxillar syncoxopodite, caudal view – note short transverse row of spinules near lateral margin (arrow). F. Maxilliped, basipodite and two-segmented endopodite, frontal view. G. Maxilliped, syncoxopodite and basipodite, frontal view – note the flap-like structure (arrow). H. Leg 1, protopodite and first exopodal and endopodal segments, frontal view (coxopodal seta is figured separately). I. Leg 1, second and third exopodal segments, frontal view. J. Leg 1, second and third endopodal segments, frontal view. A shows ♀-2; B, D–E, G−J show ♀-1; C, F show ♀-3. Scale bars: A−J = 50 μm.