Research Article |
Corresponding author: Martha Angélica Gutiérrez-Aguirre ( marguta71@gmail.com ) Academic editor: Danielle Defaye
© 2016 Martha Angélica Gutiérrez-Aguirre, Adrián Cervantes-Martínez.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Gutiérrez-Aguirre MA, Cervantes-Martínez A (2016) Taxonomic evaluation of eleven species of Microcyclops Claus, 1893 (Copepoda, Cyclopoida) and description of Microcyclops inarmatus sp. n. from America. ZooKeys 603: 33-69. https://doi.org/10.3897/zookeys.603.7480
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Description and meristic analysis of eleven species of Microcyclops recorded in America were performed based on the examination of type specimens and fresh material. Microscopic analysis of oral appendages, such as the shape and armature of the distal coxal endite of the maxilla, the ornamentation on the caudal surface of the antenna, and the intercoxal sclerites and armament of the inner basis of all swimming appendages, were characteristics that allowed the differentiation between species. Among these species, our study confirmed the synonymy of M. diversus Kiefer, 1935 with M. ceibaensis (Marsh, 1919). The results of our observations showed that M. alius (Kiefer, 1935) is a junior synonym of M. dubitabilis Kiefer, 1934; the latter being confirmed as a valid species. Also, it is proposed that the records of M. rubellus (Lilljeborg, 1901) and M. varicans (Sars, 1863) in America should be revised as there are serious doubts about their distribution in America. The analysis suggested that M. anceps pauxensis Herbst, 1962 is distinct from M. anceps var. minor Dussart, 1984 and that both are likely different from M. anceps anceps (Richard, 1897). Finally a full morphological description of adult females of Microcyclops inarmatus sp. n. is presented.
Diversity, Mexico, morphology, species richness
In America, 16 species and subspecies of Microcyclops Claus, 1893 have been described and recorded: M. alius (Kiefer, 1935), M. anceps anceps (Richard, 1897), M. anceps pauxensis Herbst, 1962, M. anceps var. minor Dussart, 1984, M. ceibaensis (Marsh, 1919), M. dubitabilis Kiefer, 1934, M. echinatus Fiers, Ghenne & Suárez-Morales, 2000, M. elongatus (Lowndes, 1934), M. finitimus Dussart, 1984, M. furcatus (Daday, 1905), M. mediasetosus Dussart & Frutos, 1985, M. medius Dussart & Frutos, 1985, M. pumilis Pennak & Ward, 1985, M. rubellus (Lilljeborg, 1901), M. diversus Kiefer, 1935, and M. varicans (Sars, 1863).
In her publication of an identification key for South American cyclopoids,
Therefore, some questions on the taxonomic status of some species of Microcyclops in America remain unresolved. These taxonomic problems may be related to the lack of thorough and rigorous species descriptions.
In Mexico, some species with uncertain taxonomic status have been recorded, including M. ceibaensis, M. anceps, and M. dubitabilis (
The morphological analysis was performed following current standards for the taxonomic study of cyclopoid copepods (see
Material examined. The evaluation included analyses of holotypes, paratypes, and museum specimens deposited in different collections: the Collection of Zooplankton of
Terminology used for the armament of each appendage(s) follows
A1 Antennule
A2 Antenna
BspA2 Antennal basipodite
Bsp Basipodite
Enp1-Enpn First to “n” endopodal segment
Exp1-Expn First to “n” exopodal segment
P1, P2, P3, P4 First, second, third, and fourth swimming legs
P5 Free segment of fifth leg
Lateral, outermost terminal, outer median terminal, inner median terminal, innermost terminal, and dorsal caudal setae are coded as setae II, III, IV, V, VI, and VII, respectively.
The morphology of several species was examined using light microscopy: A1, A2, the mouthparts, the entire structure of all of the swimming legs, and other taxonomically relevant structures, such as the frontal or caudal ornamentation of BspA2, the ornamentation of the distal coxal endite of the maxilla, and the ornamentation of maxillular palp, were illustrated with the aid of a camera lucida.
Sources for the morphological data were the types, paratypes, and other museum specimens (Table 2, as Suppl. material
Below those morphological structures which are shared by all the species examined herein are described.
Antennule 11- or 12-segmented (Fig.
Antenna with coxa (without seta), Bsp (with 2 medial setae + one lateral seta representing Exp), and 3-segmented Enp (Fig.
Praecoxal arthrite and palp of maxillule naked; praecoxal arthrite with 3 chitinized distal claws, and one spinulose seta on caudal side. Inner margin with one biserially plumose seta plus six naked setae (Fig.
Maxilliped with syncoxa bearing 2 or 3 spiniform setae, Bsp with two setae; and Enp two-segmented, first segment with 1 seta, second segment with 3 setae (Fig.
Armature formula of P1−P4 as in Table
Setation formula of the swimming legs in the Microcyclops species here examined (spine in Roman numerals, seta in Arabic numerals).
Coxa | Basis | Exp | Enp | |
---|---|---|---|---|
P1 | 0-1 | 1-I, or 1-0 | I-1; III-5 | 0-1; 1-I-4 |
P2 | 0-1 | 1-0 | I-1; IV-5 | 0-1; 1-I-5 |
P3 | 0-1 | 1-0 | I-1; IV-5 | 0-1; 1-I-5 |
P4 | 0-1 | 1-0 | I-0; III-5 | 0-1; 1-II-3 |
Microcyclops varicans Reid, 1992; Trans. Am. Microsc. Soc. 111(3), p: 249–250, figs 8d, 9c.
One adult female dissected on two slides: A1, A2 (slide 1,
10 adult females preserved in 90% ethanol with a drop of glycerine.
A pond in km 51 lado 1, Villahermosa-Frontera highway 18°23'16"N; 92°47'00"W.
the name of the species means un-armed in Latin; it refers to the absence of ornamentation on the intercoxal sclerites, the lack of spinules at base of caudal furcal setae, the reduced number of setae on second antennal endopod, and the reduced ornamentation on antennal basis.
One adult female collected 1.02.1935 from Laguna Rincon, Haiti (slide
One adult female collected 05.1986 from Shark river slough, Everglades National Park, Florida, USA (slide 2 of 7,
Adult female: Dorsal margin of prosomal somites smooth; body length 565 to 615 µm in paratypes. Antennule 12-segmented, not reaching the distal margin of the first prosomal segment (Fig.
Microcyclops inarmatus sp. n. Adult female, holotype (except A). A Habitus of one paratype specimen (
Adult male: unknown.
Antennule 12-segmented; antenna with 3-segmented Enp armed with 1, 6, and 7 setae respectively (Fig.
Microcyclops inarmatus sp. n. Adult female. A Antenna, caudal (
Basipodites of P1−P3 with long hair-like setules on the inner margins; one row of tiny spinules along the lateral margins of coxa; intercoxal sclerites naked (Fig.
Microcyclops inarmatus sp. n. Adult female. A P1, frontal (
Fifth pediger nude; P5 with one cylindrical free segment, 3.23 ± 0.4 times as long as wide, bearing one tiny medial spinule. Free segment 0.27 ± 0.01 times as long as distal seta (Figs
Microcyclops inarmatus sp. n. Adult female. A Anal somite and caudal rami, ventral (
Dorsal caudal seta (VII) 0.9 ± 0.1 times as long as caudal ramus, and innermost terminal caudal seta (VI) 1.4 ± 0.04 times as long as caudal rami (Fig.
Antennule 11, or 12-segmented (intra- and interpopulation variation); 3-segmented endopod of antenna bearing 1, 9, and 7 setae, respectively (Fig.
Microcyclops dubitabilis Kiefer, 1934. Adult female. A Antenna, frontal (
Dorsal margin of prosomal somites smooth (Fig.
Microcyclops dubitabilis Kiefer, 1934. Adult female. A First and second prosomal somite, dorsal (
Fifth pediger nude; P5 free segment cylindrical, 3.6 ± 0.8 times as long as wide, without inner spine. Free segment 0.4 ± 0.1 times the length of the distal seta (Figs
Seta VII 1.02 ± 0.3 times as long as caudal ramus, and seta VI 1.4 ± 0.2 times longer than caudal ramus. Relative lengths of terminal caudal seta from outermost caudal seta to innermost caudal seta are 1.0 : 4.9 : 7.1 : 1.6 (Fig.
Antennule 12-segmented (Fig.
Microcyclops ceibaensis (Marsh, 1919). Adult female. A Antennule, segments 2-12 (
Dorsal margin of prosomal somites slightly serrated (Fig.
Microcyclops ceibaensis (Marsh, 1919). Adult female. A Prosomal fringes, dorsal B P1, frontal (
P1 basis with long medial spine reaching distal third of Enp2P1. Spine ornamented with long setules near base and with short spinule-like setules more distally (Fig.
Fifth pediger nude (Fig.
Microcyclops ceibaensis (Marsh, 1919). Adult female. A Fifth pediger, dorsal (
Seta VII 0.7 ± 0.1 times as long as caudal ramus, seta VI 0.8 ± 0.1 times as long as caudal ramus. Relative lengths of terminal caudal seta from outermost caudal seta to innermost caudal seta: 1.0 : 5.7 : 9.5 : 1.8 (Fig.
This description is a complement to the original description of
Two pores on lateral margin of second endopodal segment of P1, very long spinules present at insertion of apical spine of Enp2P1. Long medial spine of P1 basis with heteronomous setulation (Fig.
Fifth pediger with rows of spinules on ventro-lateral surfaces. Fifth leg with tiny spinule on inner margin (Fig.
The following description is complementary to the original description of
Microcyclops finitimus Dussart, 1984. Adult female (
Anal somite with continuous row of spinules along distal margin (ventrally and dorsally), but on ventral surface medial spinules are longer and stronger than lateral spinules (Fig.
Dorsal posterior margin of second prosomal somite with crenulated hyaline fringe (Fig.
Microcyclops anceps anceps (Richard, 1897). Adult female. A Second prosomal somite, dorsal (
Inner margin of basipodite with long and fine hairs in P1−P3 (Fig.
Strong spinules present (Figs
Microcyclops anceps anceps (Richard, 1897). Adult female. A Fifth pediger, genital double-somite (
Free segment of fifth leg 2.5 ± 0.2 times longer than wide, with relatively large spinule in distal position (Figs
Seta VII and VI 0.5 ± 0.1 and 0.8 ± 0.1times as long as caudal ramus, respectively. Relative lengths of terminal caudal seta from outermost to innermost, 1.0 : 4.9 : 7.1 : 1.3 (Fig.
Microcyclops anceps anceps showed the least variation in the qualitative and morphometric characters even though specimens were examined from a wide latitudinal range (Venezuela, Mexico, Guyana, Brazil, Guatemala, and Uruguay).
Microcyclops echinatus (from southeastern Mexico) and M. ceibaensis (from Honduras and southeastern Mexico) appeared morphologically similar. Similarities between these species are in: the length and width ratio of Enp2P4; the P4 sclerite with two rows of spines; the length ratio of the terminal caudal setae III and IV; the presence of spines at the insertion of setae II, and III; and the heteronomous ornamentation of the spine on the inner margin of Bsp P1. But the features that separate the specimens of these species were the insertion of the caudal seta II (69.5% in M. ceibaensis vs. 73.2% in M. echinatus); the length and width ratio of the caudal ramus is 3.6 in M. ceibaensiswhile 5.9 in M. echinatus; the presence of spines on the fifth pediger in M. echinatus vs. absence of these spines in M. ceibaensis; and the ornamentation of the inner basis of P4 with spine-like setae in M. ceibaensis vs. short setae plus hair-like setae in M. echinatus.
In 1935, Kiefer described two new species Cyclops (Microcyclops) diversus and Cyclops (Microcyclops) alius from Uruguay. The microscopic observations performed here, support the opinion of
The type specimens labelled as M. dubitabilis (from Trou Caiman, Haiti) and Microcyclops alius (from Barra Sta. Luzia, Uruguay) were morphologically similar to: 1) specimens identified as M. rubellus [including the specimen analysed by
Microcyclops dubitabilis clearly differs from M. varicans s. str. at least in the next features: the spines at the insertion of caudal seta III are present in M. dubitabilis, but absent in M. varicans; caudal ramus is 3.5-4 times as long as wide in M. varicans and shorter in M. dubitabilis. Medial spine of Enp2P4 is around 0.8 times as long as the segment in M. dubitabilis, whereas that in M. varicans is shorter (around 0.5); and the seta inserted at base of claw-like projection in the maxilla is armed only with strong teeth at its base in M. varicans, but this armament is more complex in M. dubitabilis. Therefore M. dubitabilis is not a synonym of M. varicans.
Microcyclops rubellus and M. varicans have been recorded in several regions of the world and were thought to be likely cosmopolitan (
The specimens from southeastern Mexico assigned to the new species M. inarmatus were morphologically similar to that from Laguna Rincon, Haiti identified as M. dubitabilis (
Microcyclops inarmatus sp. n. can be distinguished from M. varicans by the following characters (see also
The analysis that included specimens from a wide latitudinal range showed a highly conserved morphology primarily in the inner region of each swimming leg and oral appendages. Thus, we may speculate that some reports of M. varicans and M. rubellus recorded in the Americas are in fact M. inarmatus sp. n. and M. dubitabilis, respectively.
Microcyclops inarmatus sp. n. has some similarities also to M. dubitabilis, but the following features differentiate these two species: setal formula of the antennal endopod (1, 9, 7 in M. dubitabilis vs. 1, 6, 7 in inarmatus); the ornamentation on the caudal surface of the antennal basis is less complex in M. inarmatus than in M. dubitabilis; setae on maxillular palp are more armed in M. inarmatus than in M. dubitabilis; and the basal seta inserted at base of claw-like projection in the maxilla is more simple in M. inarmatus, whereas M. dubitabilis has two opposite rows of different spines.
The inner margin of the basis of the first swimming leg has a long spine with heteronomous ornamentation in M. inarmatus, in comparison to the short, homonomously setulated spine on this site in M. dubitabilis. In addition, the inner margin of the basis of the fourth swimming leg bears long hair-like setae and the fourth sclerite is almost as long as wide in M. inarmatus, whereas in M. dubitabilis, this inner margin bears short setae and the fourth sclerite is wider than long. The free segment of the fifth leg has a tiny spine on the medial margin in M. inarmatus (not described in
Other species of Microcyclops which has 12-segmented antenna, caudal rami with innermost terminal caudal setae longer than outermost terminal caudal setae, spines present only ventrally on the distal margin of the anal somite, caudal rami short (no more than 3 times as long as wide), one spine on inner basis of P1, and the intercoxal sclerite of P4 quadrangular and naked, are M. davidi (Chappuis, 1922) and M. richardi (Lindberg, 1942). Microcyclops inarmatus sp. n. differs from these species in the surface ornamentation of P4 basipodite: long hair-like setules vs. short spine-like setules in M. davidi (sensu
Additionally, in M. richardi the free segment of P5 has no spine on medial margin, and the medial spine of Enp2P4 is short (0.6 times the length of the segment) in comparison with the new species. Finally, the seta on the base of the claw-like projection of the maxillar basipodite, is armed with tiny spinules in M. inarmatus, whereas in M. davidi it bears strong teeth on its base.
Microcyclops anceps pauxensis and M. anceps var. minor, described from the Amazonian region and Venezuela respectively, are similar in the number of segments of A1 (12-segmented); the length ratio of Enp2P4 (2.35 vs. 2.46); the intercoxal sclerite of P4 with two rows of spines; the length ratio of the lateral and medial apical spines of Enp2P4 (0.64 vs. 0.51); the length ratio of the medial apical spine of En2P4 and the segment (0.7 in both species), the insertion of the caudal seta II (lateral) is at 68% of the caudal rami length in M. a. pauxensis, and 70% in M. a. minor, and the continuous row of spines along the ventral and dorsal margins of the anal somite.
However, according to
Therefore, these taxa may constitute different species. The evaluation of mouthparts and the ornamentation of the inner region of each swimming leg in the type material may facilitate species delimitation. Unfortunately, the type material of both “subspecies” was not available to us.
Based upon morphological and morphometric features, eleven species and two subspecies of Microcyclops recorded in America were recognized. The following set of characters distinguishes between species: the ornamentation of the caudal surface of the antennal basis; the ornamentation of the setae of the maxillular palp; the shape and armature of the distal coxal endite of maxilla; and the basal seta in front of the claw-like projection of the maxillar basis. Previously, similar structures have been useful for differentiating other Cyclopinae species, such as Mesocyclops (
Among the specimens examined, the organization of the spine pattern on the antennal basipodite is similar to that proposed by
The micro-structures of the swimming legs as diagnostic characters have been explored in Mesocyclops. In Mesocyclops, the coxal and basis armament of the first and fourth trunk limbs are important (
Important diagnostic morphometric features for Microcyclops were the relative position of the lateral seta on the caudal ramus; the relative length of the outermost terminal caudal seta (III) and the outer median terminal caudal seta (IV); the relative length of caudal seta III and the inner median terminal caudal seta (V); and the length: width ratio of caudal ramus. Traditionally, the length ratio of the second endopod and its apical spines of the fourth trunk limb have been used as features to separate species of Microcyclops; however, as in another genus such as Eucyclops or Mesocyclops, the surface micro-structures together with the integumental armature and the meristic characters of the caudal rami are more informative.
This study is the first attempt to clarify the taxonomy of the species of Microcyclops recorded in America using detailed morphological analysis.
The microscopic analysis of oral and thoracic appendages facilitated better delineation of Microcyclops species recorded in America. The characters that better distinguish between species are the ornamentation of antennal basipodite, the armature of the coxal endite and basipodite of the maxilla, the surface ornamentation of the inner basis of P1, the structure of intercoxal sclerites of the trunk limbs, the length: width ratio of caudal ramus, the length proportion of the caudal setae, and the relative position of the lateral seta on the caudal ramus.
The analysis performed here show that M. alius is a junior synonym of M. dubitabilis, and support the opinion about the synonymy of M. ceibaensis and M. diversus.
Microcyclops inarmatus sp. n. can be distinguished from other known species of the genus by the unique combination of several characters such as: morphometric characters of the second endopodite of fourth trunk limb and caudal ramus, presence of 6 setae on the second endopodal segment of antenna, antennal basipodite with just one group of spinules on caudal surface, lack of ornaments on the intercoxal sclerites of all swimming appendages, absence of spinules at base of lateral caudal and outermost terminal caudal setae, and basipodites of first to fourth swimming legs with long hair-like setules on inner margin.
The key is mainly based on the analysis performed in the descriptive section of this manuscript. Original descriptions were consulted in those species in which no microscopic observations could be made [Microcyclops anceps pauxensis (
1 | Cylindrical free segment of P5 smooth, without inner spine (Fig. |
2 |
-– | Cylindrical free segment of P5 with inner spine (Figs |
5 |
2 | Base of the outermost caudal seta (III) with a row of spines (Fig. |
3 |
– | Base of the outermost caudal seta (III) without a row of spines | 4 |
3 | Length (L): width (W) ratio of caudal ramus is 4.35; lateral caudal seta inserted at 69% of the total caudal ramus length; inner basis of P4 naked | Microcyclops medius |
– |
L: W ratio of caudal ramus is 2.48 ± 0.2; lateral caudal seta inserted at 71 ± 5.7 % of the total caudal ramus length (Fig. |
M. dubitabilis |
4 | L: W ratio of caudal ramus is 5 ± 1; lateral caudal seta inserted at 80 % of the total caudal ramus length | M. furcatus |
– | L: W ratio of caudal ramus is 2.3 ± 0.6; lateral caudal seta inserted at 55 % of the total caudal ramus length | M. pumilis |
5 | Inner spine of the cylindrical free segment of P5 tiny, articulated, inserted medially, and does not reach the distal margin of the segment (Figs |
6 |
– | Inner spine of the cylindrical free segment of P5 strong, unarticulated; inserted terminally, projected beyond the distal margin of the segment (Figs |
11 |
6 | Length ratio of the innermost (VI): outermost (III) caudal setae is 3.0; L: W ratio of caudal ramus is 2.3; lateral caudal seta inserted at 57 % of the total caudal ramus length | M. mediasetosus |
– | Length ratio of the innermost (VI): outermost (III) caudal setae is 1.6 to 2.0; L: W ratio of caudal ramus is 2.7 to 6.0; lateral caudal seta inserted at 60 to 75 % of the total caudal ramus length | 7 |
7 | Inner basis of P1 with hair-like setae, medial spine absent (Fig. |
M. finitimus |
– | P1 basis with medial spine (Figs |
8 |
8 | Inner basis of P1 naked, medial spine reaching the proximal half of Enp2P1 and with homonomous ornamentation; L: W ratio of caudal ramus is 5 to 6, with a row of spines at the base of the lateral caudal seta (II) that extends dorsally; and no spines at the base of the outermost caudal seta (III) | M. elongatus |
– | Inner basis of P1 hairy, medial spine reaching the distal half of Enp2P1 and with heteronomous ornamentation (Figs |
9 |
9 | Anal somite with a row of spines on ventral margin; no spines at the bases of the caudal setae II and III (Figs |
M. inarmatus sp. n. |
– | Anal somite with a row of spines along both ventral and dorsal margins; with spines at the bases of the caudal setae II and III (Fig. |
10 |
10 | Fifth pediger with spines on ventral and lateral surfaces (Fig. |
M. echinatus |
– | Fifth pediger nude ventrally and laterally; caudal ramus is 3.6 ± 0.4 times longer than wide (Fig. |
M. ceibaensis |
11 | No spines on the base of the caudal setae II and III; inner basis of P4 naked, unarmed | M. anceps var. minor |
– | Spines on the base of caudal seta III, no spines on the base of the caudal seta II (Fig. |
12 |
12 |
W ratio of caudal ramus is 3.7 ± 0.3 (Fig. |
M. anceps anceps |
– | L: W ratio of caudal ramus is 2.4; inner basis of P1 naked; inner basis of P4 with short hair-like setae | M. anceps pauxensis |
Danielle Defaye and Paula Rodríguez Moreno-Martin Lefèvre, Muséum National d’Histoire Naturelle, Paris; Hubert Höfer and Hans Walter Mittmann, Staatliches Museum für Naturkunde, Karlsruhe; Chad Walter, Smithsonian InstitutionNational Museum of Natural History, kindly allowed us to review
Table 2
Data type: RTF file
Explanation note: Biological material examined.