Notas sobre Halicyclops (Copepoda, Cyclopoida, Cyclopidae) de Colombia y el Caribe occidental: un nuevo registro con una clave para las especies del Grupo "B" sensu Rocha (1991).
The cyclopoid copepod Halicyclops is a cosmopolitan genus represented by free-living planktonic forms (Chang 2012, Ueda and Nagai 2012); members of this genus dwell in a wide range of habitats, having been recorded from shallow coastal environments, including brackish coastal habitats and estuaries (Suarez-Morales and Fuentes-Reines 2014, Fuentes-Reines and Suarez-Morales 2015), salt marshes (Chang 2012), anchialine caves (Rocha et al. 2000), inland waters with increased salinity (Karanovic 2004), and fresh water (Rocha 1995a, Defaye & Dussart 1988, Fuentes-Reines et al. 2013, Luong 2016). A few species are known to live loosely associated with benthic invertebrates (Humes 1947).
According to Walter and Boxshall (2017) the genus currently contains 99 valid species and 13 subspecies, but the genus is in need of revision. In the Neotropical region 19 valid species have been recorded (Rocha 1995a, Rocha et al. 1998, Suarez-Morales and Fuentes-Reines 2014). Of these, only three species are hitherto known from Colombia: H. venezuelaensis Lindberg, 1954, H. exiguus Kiefer, 1934, and the recently described H. gaviriai Suarez-Morales and Fuentes-Reines 2014. The first species is known from Cienaga Grande de Santa Marta, Magdalena and Laguna Navio Quebrado (Fuentes-Reines et al. 2013, Fuentes-Reines and Suarez-Morales 2015) whereas the other two only from the Laguna Navio Quebrado, La Guajira, (Suarez-Morales and Fuentes-Reines 2014, Fuentes-Reines and Suarez-Morales 2015).
During a survey of the plankton community of the Cienaga Grande de Santa Marta, in the Colombian coast of the Caribbean, three species of the genus Halicyclops were collected: H. exiguus, H. venezuelaensis, and H. hurlberti Rocha, 1991. The aim of this paper is to provide additional morphologic data of these taxa and report the first occurrence of the latter species in the Caribbean. A key to the species of the genus (sensu Rocha, 1991) including H. hurlberti, is also provided.
Material and methods
Plankton samples were taken monthly from the Cienaga Grande de Santa Marta, Colombia (10[degrees]52'11.25"N; 74[degrees]19'31.64"W) from January to October 2017, mainly in the littoral areas with vegetation (mangrove) but also from open water. One thousand nine hundred forty-four (1944) liters of water were taken using a bucket of 25 L, filtered with a zooplankton net (45 [micro]m), and preserved in 70% ethanol.
Water salinity was measured with a WTW 3111 conductivity meter. Copepods were sorted from the original samples and then processed for taxonomical identification. Dissected specimens and appendages were mounted in glycerine and sealed with Canada balsam. Digital photographs were taken using a Kodak Easy Share C140 camera attached to a compound Olympus CX22 microscope. The specimens were measured in lateral position, from the anterior end of the rostral area to the posterior margin of the caudal ramus.
The specimens examined were deposited at the Museo de Colecciones Biologicas at the Universidad del Atlantico (UARC), Colombia. Morphological terminology follows Huys and Boxshall (1991). The following abbreviations are used in the descriptive section: P1--P6= first to sixth swimming legs, EXP= exopod, ENP= endopod, aps = apical seta, ins= Inner seta, Fig = Figure, UARC = Universidad del Atlantico Region
Caribe, [micro]m = micron
Order Cyclopoida Burmeister, 1834
Family Cyclopidae Dana, 1846
Subfamily Halicyclopinae Kiefer, 1927
Genus Halicyclops Norman, 1903
Halicyclops exiguus Kiefer, 1934
Material examined. Three adult females (UARC359-367M), Cienaga Grande de Santa Marta, Colombia, coll. J.M. Fuentes Reines.
Remarks. The specimens from Colombia share the diagnostic features from specimens of H. exiguus previously reported from the adjacent Guajira department in Colombia (Fuentes-Reines and Suarez-Morales 2015). Body robust, compact anteriorly (Fig. 1A). Body length, excluding caudal setae 490 [micro]m (n =3). This species can be easily separated from its congeners by a combination of the following characteristics that are present in our specimens: 1) last segment of antenna with five lateral setae (arrows in Fig. 1B), length/wide ratio about 3.0 (Fig. 1B), 2) fourth segment of female antennule less than twice as long as wide (Fig. 1C), 3) female P5 exopod elongate, inner spine (ins) and apical seta (aps) as long as or longer than the segment (Fig. 1D), 4) Inner basipodal spine of P1 (arrow in Fig. 1E) reaching at least midlength of third endopod of P1, 5) P4ENP3 with proximal inner seta (arrow in Fig. 1F) not reaching tip of inner apical spine.
In the specimens from Santa Marta examined the inner proximal seta of P4ENP3 does not reach beyond the apical inner seta (Fig. 1F), but in the specimens reported by Kiefer (1934, Abb. 3) from Haiti, Collado et al. (1984, fig. 7) from Costa Rica, and Fuentes-Reines and Suarez-Morales (2015, fig. 2e) from another Colombian locale, the inner proximal seta of P4ENP3 does reach beyond the apical element. This character appears to be variable in the species.
Distribution. Hitherto, this species has been recorded only from the Neotropical region; it has been reported in Haiti (Kiefer 1934) (but see Rocha et al. 1998), Costa Rica (Collado et al. 1984), French Guiana (Defaye and Dussart 1988), and Brazil (Rocha and Iliffe 1993). In Colombia this species has been reported in La Guajira department (Fuentes-Reines-Suarez-Morales 2015); the present record represents a modest range expansion in the country, which now includes the Magdalena Department. It is also the second record of the species in the Caribbean coast of Colombia.
Halicyclops venezuelaensis Lindberg, 1954
(Figs 2A-D, 3A, B)
Material examined. One adult female (UARC353-358M), Cienaga Grande de Santa Marta, Colombia, coll. J.M. Fuentes Reines.
Remarks. The specimen examined bears the diagnostic features of H. venezuelaensis as described by Lindberg (1954), Rocha (1995b) and Fuentes-Reines et al. (2013). Body robust (Fig. 2A); length excluding caudal setae: 616 pm. It can be easily recognized by a combination of characters including: 1) the long proximal seta on the first segment of maxilliped (arrow in Fig. 2B), 2) genital double-somite with lateral protuberances (Fig. 2C, arrowed), 3) ventral margins ofurosomites ornamented with large spines (arrows in Fig. 2D), 4) caudal ramus subquadrate, as long as wide (Fig. 2E), 5) inner basipodal spine of P1 (arrow in Fig. 2F) reaching beyond second endopodal segment, 6) P4ENP3 about 1.5 times as long as wide, inner apical spine (arrow in Fig. 3A) slightly longer than segment, 7) P5 EXP about 1.7 times as long wide, innermost spiniform seta (arrow in Fig. 3B) being the longest element of the exopod. The Colombian specimens bear subtle morphological discrepancies with the Belizean specimens reported by Rocha (1995b); in the Colombian populations (Fig. 2F, Fuentes-Reines et al., 2013, fig. 8D) the inner basipodal spine of P1 almost reaches the insertion point of inner seta of P1ENP3 whereas the same spine is shorter in the Belizean population, reaching the proximal margin of P1ENP2 (Rocha 1995b, fig. 29).
Distribution. This species appears to have a high tolerance to salinity variations, it has been recorded in brackish and freshwater habitats (Rocha 1995b, Fuentes-Reines et al. 2013, Fuentes-Reines and Suarez Morales 2015). It has been known to occur in the Venezuelan Caribbean coast, where it was originally described, but also in Belize, Mexico and Colombia (Lindberg 1954, Rocha 1995b, Suarez-Morales and Reid 2003).
Halicyclops hurlberti Rocha, 1991
(Figures 3C-F, 4, 5)
Material examined. Two adult females (UARC335-343M), Cienaga Grande de Santa Marta, Colombia, coll. J.M. Fuentes Reines.
Remarks. The female specimens examined were assignable to H. hurlberti following the diagnostic characters presented by Rocha (1991) and Gomez and Rocha (2005). Habitus as in figure 3C, body relatively long, compact anteriorly, cephalosome with large rounded dorsal integumental window and length/ wide ratio = 1.1. Body length, excluding caudal setae = 588-602 pm (average = 595 [micro]m, n = 2). Labrum with 7-8 small medial teeth set between large lateral teeth (Fig. 3D). Urosome with four segments, genital double somite subquadrate, lacking lateral medial protrusions and with rounded integumental window on each side of posterior half (arrows in Fig. 3F), lateral margins not produced (Fig. 3E-F), caudal rami about 1.4 as long as wide (Fig. 4A), outer seta as long as ramus, dorsal seta (arrow in Fig. 4A) 1.5 times longer than ramus and three times longer than lateral seta, middle inner seta about 2 times as long as middle outer seta, the latter ornamented only with setules (arrow in Fig. 4B)
Antennules 6-segmented, fourth segment 1.6 times as long as wide (Fig. 4C). Antenna consisting of 4 segments (Fig. 4D), coxa reduced, unarmed, basis with two setae at inner corner; seta representing EXP present (arrow in Fig. 4D). ENP 2-segmented. Proximal endopodal segment with single seta on middle inner margin. Length/wide ratio of terminal endopodal segment ratio about 1.9 times as long as wide armed with 5 inner setae and 7 apical setae plus short spinule on proximal outer margin.
P1-P4 EXP and ENP 3-segmented (Figs 4E, F; 5A). Inner basipodal spine of P1 (arrow in Fig. 4E) reaching midlength of P1 ENP3. P2-P3 similar to each other in size and armature (Fig. 4F). P4 ENP3 about 1.6 times as long as wide; inner apical spine about 1.6 as long as segment and 1.7 times as long as outer apical spine. Proximal inner seta overpassing the inner apical spine (Fig. 5A). P5 unsegmented, EXP elongate, 1.4 times as long as wide, bearing 3 spines, all of them longer than segment, plus one flexible seta 1.2 times as long as segment (Fig. 5B). P6 represented by a small seta (arrow in Fig. 5C).
Halicyclops hurlberti belongs to the group of species "B" of Halicyclops with a 3443 spine formula but Rocha (1991) recognized a subgroup of species sharing the following characteristics: 1) caudal setae bearing only heteronomously distributed setules, 2) fourth segment of female antennule less than twice as long as wide, 3) inner spine of the second basipodite of P1 reaching at least midlength of P1ENP3. Halicyclops hurlberti is included in this group together with other 13 species: H. sinensis, Kiefer, 1928, H. canui Lindberg, 1941, H. pilifer Lindberg, 1949, H. blachei Lindberg, 1952, H. crassicornis Herbst, 1955, H. coulli Herbst, 1977, H. laminifer Herbst, 1982, H. glaber Rocha, 1983, H. pilosus Rocha, 1984, H. dussarti Rocha, 1995, H. ramirezi Menu-Marque and Sorarrain, 2007, H. continentalis Ueda and Nagai, 2009, and H. setiformisUeda and Nagai, 2012. Of these, seven are known from the Neotropical region.
Among the group of species recognized by Rocha (1991), H. hurlberti is closest to H. coulli but they can be easily distinguished by: 1) the proximal inner seta of P4ENP3 overpasses the inner apical spine in H. coulli (Herbst, 1977, Abb. 6) whereas in H. hurlberti it is as long as the inner apical spine (Fig. 5D, Rocha, 1991, fig. 6; Gomez and Rocha, 2005, fig. 12A), 2) the distal and proximal inner setae of P4ENP3 are thicker than the apical spines in H. hurlberti (Fig. 5D, Rocha 1991, fig. 6, Gomez and Rocha 2005, fig. 12A) whereas in H. coulli they are equally thick (Herbst 1977, Abb. 6), 3) inner basipodal spine of P1 reaching at least midlength of the P1ENP3 in H. hurlberti (Fig. 4E, Rocha 1991, fig. 4, Gomez and Rocha 2005, fig. 11B), whereas in H. coulli it reaches the distal margin of P1ENP3 (Herbst 1977, Abb. 5).
The specimens from Colombia show some subtle differences Figure 4. Halicyclops hurlberti, adult female. A. Caudal ramus. B. Setae IV-V of caudal ramus. C. Antennule. D. Antenna. E. P1. F. P2
Figure 5. Halicyclops hurlberti, adult female. A. P4, B. P5. C. P6. D. P4ENP3.
with respect to the descriptions by Rocha (1991) and Gomez and Rocha (2005); thus allows an expansion of the morphological knowledge of this species: 1) the caudal rami length/width ratio is about 1.4 in the Colombian specimen while in the Mexican and USA is 1.1 and 1.25, respectively (Rocha 1991, fig. 2, Gomez and Rocha 2005, fig. 2A,C); 2) the two subdistal inner setae of P2-3ENP3 barely reach beyond the distal end of the apical spines in the Colombian specimens (Fig. 2F), whereas in the USA specimens, the inner setae goes well beyond the distal end of the apical spines (Rocha 1991, fig. 5). Overall, we consider that these differences are within the intraspecific range and reveal affinities between the Colombian and Mexican populations.
Among the species known from Colombia, H. hurlberti closely resembles H. gaviriai in the following characters: 1) they share the same spine formula of P1-P4EXP3; 2) Both of them lack strong processes on the genital double-somite 3) the proximal inner seta of P4ENP3 overpassing tip of inner apical spine, 4) the length/wide ratio of fourth segment of antennule is less than 3. They can be separated by: 1) the P1 inner basipodal spine reaches the distal margin of P1 ENP2 in H. gaviriai (Suarez-Morales and Fuentes-Reines fig. 2A) whereas in H. hurlberti this spine is longer, reaching midlength of P1 ENP3 (Fig. 4E, Rocha 1991 fig 4, Gomez and Rocha 2005, fig. 11B) 2) length/wide ratio which is 1.56 in H. gaviriae vs. 1.4 in H. hurlberti and relative length of the spines of P5EXP, 3) the number of large lateral teeth (1 vs. 2 in H. hurlberti?) of the labrum, 4) the thickness of distal inner spines and apical spines of P4ENP3.
Distribution. Hitherto, Halicyclops hurlberti has been reported only from the Tihuana Estuary in the state of California, in the USA Pacific (Rocha 1991) and from an estuarine system in the state of Sinaloa, in the Mexican Pacific (Gomez and Rocha 2005). Its finding in this area of Colombia represents a geographic range extension of this species from the Eastern Tropical Pacific to the Guajira province sensu Morrone (2014) in the western Caribbean.
Habitat. The northern Cienaga Grande de Santa Marta is a shallow swamp (depth 0.5-1.5m), with temperature during the sampling period 31.2[grados]C, pH = 8.9, salinity = 15PSU and dissolved oxygen =7.86mg/L.
Key to the species of Halicyclops belonging to Group "B" sensu Rocha (1991)
1A. Spine formula 2-3-3-3 H. canui Lindberg, 1941 1B. Spine formula 3-4-3-2 2A 1C. Spine formula 3-4-3-3 3A 1D. Spine formula 3-4-4-3 4A 2A. L/W of the P4ENP3 is about 1-5-1.7, serration of urosomal dorsal frills is almost equally coarse on the second through fourth somites H. setiformis Ueda and Nagai, 2012 2B. L/W of the P4ENP3 is about 1.1, serration of urosomal dorsal frills is very fine on the second and third somites compared to the fourth somite H. blachei Lindberg, 1952 3A. Genital double-somite with round lateral processes, fourth urosomite with squarely produced hyaline frill along the posterodorsal margin H. laminifer Herbst 1982 3B. Genital double-somite with triangular lateral processes, fourth urosomite without squarely produced hyaline frill along the posterodorsal margin H. continentalis Ueda and Nagai, 2009 4A. Genital double somite without lateral process 5 4B. Genital double somite with lateral process 6 5A. Spine inserted at inner corner of leg 1 basis of P1ENP goes beyond of P1ENP3, proximal inner seta overpassing the inner apical spine, the proximal and distal setae and the apical spines are equal in thickness H. coulli Herbst 1977 5B. Spine inserted at inner corner of leg 1 basis of P1ENP reaching midlength of P1ENP3, proximal inner seta is as long as the inner apical spine, the proximal and distal inner setae of P4ENP3 are thicker than apical spines H. hurlberti 6A. Caudal ramus divergent H. pilifer Lindberg, 1949 6B. Caudal ramus no divergent 7 7A. P4ENP3 without inner setae H. glaber Rocha 1983 7B. P4ENP3 with inner setae 8 8A. P4ENP3 inner setae very short, not reaching the midlength of inner apical spine of P4EN3 9 8B. P4ENP3 inner setae at least reaching midlength or beyond inner apical spine of P4EP3 10 9A. Posterior margin of genital double somite with larger denticulate hyaline membrane H. ramirezi Menu Marque and Sorarrain, 2007 9B. Posterior margin of genital double somite without larger denticulate hyaline membrane H. crassicornis Herbst, 1955 10A. Spine inserted at inner corner of leg 1 basis of P1ENP goes beyond of P1ENP3 H. pilosus Rocha, 1984 10B. Spine inserted at inner corner of leg 1 basis of P1ENP reaching midlength of P1EN3 11 11A. Urosomites with coarsely serrate frills H. sinensis Kiefer, 1928 11B. Urosomites with fine serrate frills H. dussarti Rocha, 1995
We are indebted to Dr. Samuel Gomez (Universidad Nacional Autonoma de Mexico, Instituto de Ciencias del Mar y Limnologia, Mexico) for kindly providing useful taxonomic literature during the development of this work and for confirming the identification of Halicyclops hurlberti.
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Juan M. Fuentes-Reines (1) * and Eduardo Suarez-Morales (2)
(1) Universidad del Magdalena, Grupo de Investigacion en Biodiversidad y Ecologia Aplicada, A. A. 731 Santa Marta, Colombia.
(2) El Colegio de la Frontera Sur, Unidad Chetumal, A.P. 424, 77014 Chetumal, Quintana Roo, Mexico
* Corresponding author.
Email Juan M. Fuentes: firstname.lastname@example.org
Email Eduardo Suarez: email@example.com
Published online: 30/05/2018
Leyenda: Figure 1. Halicyclops exiguus, Female. A. Habitus, B. Antenna, C. Antennule, D. P5. E. P1. F. P4ENP3
Leyenda: Figure 2. Halicyclops venezuelaensis. Adult female. A. Habitus, B. Maxilliped. C-D. urosome, ventral view. E. Caudal rami. F. P1.
Leyenda: Figure 3. Halicyclops venezuelaensis. Adult female. A. P4ENP3. B. P5. C-F. H. hurlberti, adult female. C. Habitus. D. Labrum. E. Urosome. F. Genital double somite
Leyenda: Figure 4. Halicyclops hurlberti, adult female. A. Caudal ramus. B. Setae IV-V of caudal ramus. C. Antennule. D. Antenna. E. P1. F. P2
Leyenda: Figure 5. Halicyclops hurlberti, adult female. A. P4, B. P5. C. P6. D. P4ENP3.
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|Title Annotation:||TRABAJOS ORIGINALES|
|Author:||Fuentes-Reines, Juan M.; Suarez-Morales, Eduardo|
|Publication:||Revista peruana de biologia|
|Date:||May 1, 2018|
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