ACTA BIOLÓGICA COLOMBIANA
http://www.revistas.unal.edu.co/index.php/actabiol
ARTÍCULO DE INVESTIGACIÓN/RESEARCH ARTICLE
COMPLEMENTARY DESCRIPTION AND RECORD OF Neocyclops
ferrarii (Cyclopidae: Halicyclopinae) FROM NORTHERN
COLOMBIA
Descripción complementaria y registro de Neocyclops ferrarii
(Cyclopidae: Halicyclopinae) en el norte de Colombia
Juan Manuel FUENTES-REINÉS1, Eduardo SUÁREZ-MORALES2.
1
Grupo de investigación en Biodiversidad y Ecología Aplicada, Facultad de Ciencias Básicas, Universidad del Magdalena. Carrera 32
n.º 22–08. Santa Marta, Colombia.
2
El Colegio de la Frontera Sur. A.P. 424, 77014 Chetumal, Quintana Roo, México.
For correspondence. juanmanuelfuentesreines@yahoo.com
Received: 28th April 2016, Returned for revision: 27th September 2016, Accepted: 9th October 2016.
Associate Editor: Santiago Gaviria Melo.
Citation/Citar este artículo como: Fuentes-Reinés JM, Suárez-Morales E. Complementary description and record of Neocyclops ferrarii (Cyclopidae:
Halicyclopinae) from northern Colombia. Acta biol. Colomb. 2017;22(1):59-65. DOI: http://dx.doi.org/10.15446/abc.v22n1.57197
ABSTRACT
The interstitial cyclopoid copepod Neocyclops ferrarii Rocha, 1995 was found in samples obtained from littoral areas of Rodadero Bay,
northern Colombia. The specimens from Colombia share the diagnostic features of N. ferrarii presented in the original description.
However, the Colombian specimens show some degree of variation with respect to the type material in: 1) the number of teeth in the
labrum; 2) the length of outer exopodal spine on female leg 5; 3) the relative length of the mandibular palp setae; 4) length/width
ratio of caudal rami; 5) the length ratio of caudal setae VI/III; 6) the length ratio of caudal setae VII/VI; 7) the male body size; 8) the male
caudal rami length/width ratio; 9) This is the second record of this species after its original description from Belizean waters. In the
Caribbean region N. ferrarii most closely resembles N. vicinus Herbst, both of them bear an antennary exopod, a 12-segmented female
antennule, P3ENP3 armature formula 3,III, but can be separated from the latter by difference in the length/width ratio of the female
caudal ramus, the length ratio of caudal setae VI/III, the length ratio of caudal setae VII/VI, the male body size, the number of segment
of P4ENP, the armature details of mandibular palp and the number of segments of male P5. This is the second species of Neocyclops
recorded from Colombia and represents a distributional range expansion of N. ferrarii in the Caribbean Basin.
Keywords: coastal copepods, Caribbean Sea, distribution, zooplankton.
RESUMEN
El copépodo ciclopoide intersticial Neocyclops ferrarii Rocha, 1995 fue encontrado en muestras litorales obtenidas de la bahía
Rodadero, al norte de Colombia. Los especímenes de Colombia comparten las características diagnósticas de N. ferrarii de la
descripción original. Sin embargo, los especímenes colombianos muestran cierta variación con respecto al material tipo en: 1) el
número de dientes en el labro; 2) la longitud de la espina exopodal externa de la pata 5 de la hembra; 3) la longitud relativa de las
setas del palpo mandibular; 4) la relación largo/ancho de la rama caudal; 5) la longitud proporcional de las setas caudales VI / III;
6) la longitud proporcional de las setas caudales VII / VI; 7) la talla del macho; 8) la relación largo/ancho de la rama caudal del
macho. Este es el segundo registro de esta especie después de su descripción original en aguas de Belice. En la región Caribe N. ferrarii
se asemeja más estrechamente a N. vicinus Herbst, ambos poseen exópodo antenal, anténulas con 12 segmentos en la hembra, la
fórmula P3ENP3 de 3, III, pero diieren en la proporción de la rama caudal en la hembra, la longitud de las setas caudales VI / III y
VII / VI, el tamaño del macho, el número de segmento de P4ENP, en detalles del armamento del palpo mandibular y en el número
de segmentos de la P5 del macho. Esta es la segunda especie de Neocyclops registrada en Colombia y representa una expansión de la
distribución conocida de N. ferrarii en la Cuenca del Caribe.
Palabras clave: copépodos costeros, mar Caribe, distribución, zooplancton.
Acta biol. Colomb., 22(1):59-65, enero-abril 2017
DOI: http://dx.doi.org/10.15446/abc.v22n1.57197
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Fuentes-Reinés JM, Suárez-Morales E.
INTRODUCTION
The cyclopoid copepod genus Neocyclops Gurney, 1927 is
one of the most speciose in the subfamily Halicyclopinae;
currently, it is known to contain 25 species (Pesce, 2016;
Walter and Boxshall 2016). Members of this genus are marine
forms inhabiting epibenthic or interstitial environments (Lee
and Chang, 2015). The genus Neocyclops is cosmopolitan; it
has been recorded from coastal areas of the Indian, Atlantic,
and Paciic Oceans; about 60% of all known species are
recorded in the Indo-Paciic (Lee and Chang, 2015).
Petkovski (1986) split the genus into two subgenera according
to the number of exopodal segments of the male P5: the
subgenus Protoneocyclops, with four segments in the ifth leg
as in N. ferrarii, and Neocyclops s. str. with three segments; this
criterion has been questioned (Karanovic, 2008).
In the Americas, the countries with most records of
species of Neocyclops are Brazil, Bahamas, and Cuba (Herbst,
1955; Pleşa, 1973; Pesce, 1985). In Colombia, only one
species, N. stocki Pesce, 1985 from San Andres Island, has
been reported so far (Petkovski, 1986).
The copepod fauna from Colombia has received little
attention despite de diversity of fresh, marine and brackish
systems in both the Atlantic and Paciic coasts of the
country; more new species and records of Copepoda are
expected to be found in future studies. The aim of this paper
is to document the irst record of N. ferrarii in Colombia,
which expands the distributional range of this species in the
Caribbean Basin. In addition, we present a complementary
description of this species based on the Colombian
specimens and a comparative analysis with the other known
populations.
MATERIALS AND METHODS
Biological samples of littoral and limnetic habitats were
obtained from Rodadero Bay, Magdalena, northern
Colombia (11°14’10”N, 74°12’06”W) during ieldwork
carried out from August 2015 to March 2016, mainly in
the inshore areas covered by vegetation (mangrove) and a
small bank of oysters but also from the shallow limnetic
zones. Water salinity, pH, temperature was measured with
a multiparameter WTW 350i. Water samples were collected
manually using a 25-l bucket at both littoral and limnetic
habitats. Samples were iltered with a zooplankton net
(mesh size = 45 μm) and preserved in 70 % ethanol.
Copepods were sorted from all the samples and then
processed for taxonomical identiication including the
examination of the whole specimen and dissection of
selected appendages. Dissected appendages were mounted
in slides with glycerine and sealed with Canada balsam.
The specimens were measured in ventral position, from the
anterior end of the rostral area to the posterior margin of
the caudal ramus. Drawings were made with the aid of a
camera lucida mounted on an Olympus BX51 compound
microscope equipped with Nomarski DIC. The specimens
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Acta biol. Colomb., 22(1):59-65, enero-abril 2017
examined were deposited at the Museo de Colecciones Biológicas
de la Universidad del Atlántico, Barranquilla, Colombia
(UARC273M-UARC281M), where they are available for
consultation and/or further examination. Morphological
terminology follows Huys and Boxshall (1991). The
following abbreviations are used in the description: P1–P6=
irst to sixth swimming legs, EXP= exopod, ENP= endopod.
RESULTS
Taxonomy
Order Cyclopoida Burmeister, 1834
Family Cyclopidae Dana, 1846
Subfamily Halicyclopinae Kiefer, 1927
Genus Neocyclops Gurney, 1927
Neocyclops ferrarii Rocha, 1995
(Figures 1-3)
Description of female
The morphology of the female specimens from Magdalena,
Colombia agrees in general with previous descriptions and
illustrations provided by Rocha (1995). Body widest at
irst pediger, slightly tapering posteriorly (Fig. 1A). Body
length, excluding caudal setae, 756–826 μm (average =
780 μm; n = 7). Labrum trapezoidal, armed with ten blunt
teeth of different sizes, outermost being largest and thickest
(Fig. 3A). Urosome with four somites, genital double-somite
1.1 times as long as wide, with paired backwardly directed
spinous proximal processes visible in dorsal and ventral
views (Fig. 1A). Seminal receptacle as shown in Fig. 3B. Anal
operculum at middle of anal somite, not strongly convex,
with smooth posterior margins.
Caudal ramus (Fig. 3C) about 2.7–3.1 as long as wide,
with six setae, lateral seta II located slightly dorsally, outer
seta III short, spiniform and bipinnate, about 0.7 times as
long as ramus, a little longer than 1.3 length of inner seta VI.
Terminal seta IV about 3.5 as long as the ramus, seta V is the
longest. Dorsal seta VII slender, plumose, about 0.8 times
as long as inner seta VI, and slightly shorter (0.5 times) than
caudal ramus. Integumental pores pattern of caudal rami as
in igure 2C.
Antennules 12-segmented; armature as in type specimens
(Rocha, 1995) (Fig. 1B). Antenna (Fig. 1C) slender, distinctly
4-segmented, comprising basipod and 3-segmented
endopod. Surface of basipod smooth, about 3.2 times as
long as wide, with one long outer uniserially setulose seta
representing exopod, and two naked setae at inner distal
corner. First endopodal segment about 1.76 times as long as
wide, with one naked seta at halfway the inner margin. Second
endopodal segment longer than irst endopodal segment,
about 2.1 times as long as wide, with minute spinules along
outer margin (not illustrated); armed with one short medial,
two short subapical and two long apical setae along inner
margin. Third endopodal segment elongate, about 2.7 times
as long as wide, ornamented with one row of spinules along
Neocyclops ferrarii from Colombia
Figure 1. Neocyclops ferrarii from Rodadero Bay, northern Colombia. Adult female. A. Habitus. B. Antennule. C. Antenna. D. Mandibular palp.
E. Mandible. F. Maxillule. G. Maxilla. H. Maxilliped. Scale bars: A, C, G = 50 µm; B, D-F, H = 20 µm.
outer margin (not illustrated), bearing seven apical setae
including four geniculate and three slender setae.
Mandible (Figs. 1D-E), palp reduced to small segment
armed with three slender naked apical setae; longest seta
not reaching gnathobasal teeth, about ive times as long as
shortest one; the middle seta is twice as long as the shortest
(Fig. 1D). Coxal gnathobase well-developed; cutting edge
armed with inner group of three stout teeth and one spinous
element, middle group of six teeth and outer group of one
unipinnate spine and one outer unipinnate dorsal seta.
Maxillule (Fig. 1F), maxilla (Fig. 1G), and maxilliped
(Fig. 1H) as described by Rocha (1995).
P1-P4 EXP and ENP three-segmented, except for P4ENP
which is two segmented (Figs. 2A-D), armed as in Table 1.
Spine inserted at inner corner of P1 basis reaching the half
of second endopodal segment of P1 (Fig.2A). Intercoxal
sclerites of P1–P4 with distal margin smooth. Praecoxal
sclerites not expressed. Coxae unornamented, with transverse
internal chitinous ridges originating from medial (arrowed
in Figs 2A-D). P1-P4 EXP3 with setal formula 5,5,5,5 and
spine formula 3,4,4,3; each leg bearing two inner setae on
enp-2, and one inner seta on enp-1 and exp-1. P4ENP2-3
(Fig. 2D) fused; inner distal spine 1.36 times longer than
outer distal spine.
P5 (Fig. 3D) three-segmented; coxa unarmed, about 0.65
times as long as wide, basis about 1.7 times wider than long,
with outer plumose seta, exopod gradually broadening distally,
about between 2.0 (Belizean specimens) and 2.3 times longer
than wide, armed with outer pinnate spine slender apical
plumose seta lanked by two pinnate spines. Inner distal spine
1.1 times longer than outer spine, about 1.34 times as long as
lateral spine, 0.97 times as long as segment.
Acta biol. Colomb., 22(1):59-65, enero-abril 2017
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Fuentes-Reinés JM, Suárez-Morales E.
Figure 2. Neocyclops ferrarii from Rodadero Bay, northern Colombia Adult female. A. P1. B. P2. C.P3. D. P4. Scale bar: 50 µm.
Table 1. Armature formula swimming P1-P4. (Roman numeral indicating spines, Arabic numeral representing setae).
EXP
ENP
I-1; I-1;III,2,3
0-1; 0-2;I-I+1,3
P2
I-1;I-1; III,I+1,4
0-1; 0-2;I,II,,3
P3
I-1;I-1; III,I +1,4
0-1; 0-2; I,II,3
P4
I-1;I-1;II,I+1,4
0-1; I,II,4
P1
Male (allotype): Body 602–630 μm long (average 610±10
μm, n = 8). Urosome with six somites. Caudal rami shorter
than in female, 2.2 times longer than wide (Fig. 3I); one
specimen with relatively longer caudal ramus (2.6) (Fig.
3H); armature of rami as in female.
Antennule (Fig. 3E) 16-segmented; geniculate, armature
and segmentation as in N. vicinus (Lotufo and Rocha, 1993).
P5 (Fig. 3F) 4-segmented, with small intercoxal sclerite;
coxa unarmed, subquadrate; basis with outer plumose seta.
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First exopodal segment subrectangular, about 1.7 times as
long as wide, armed with an outer spine and single inner
seta, second exopodal segment as long as wide, bearing one
plumose apical seta plus two spines.
P6. Consisting of low plate armed with one inner spine
and two setae, outer seta about two times length of
middle seta (Fig 3G). Male identical to female in all other
respects.
Neocyclops ferrarii from Colombia
Figure 3. Neocyclops ferrarii from Rodadero Bay, northern Colombia Adult female. A. Labrum, ventral. B. Seminal receptacle, ventral. C. Caudal
rami. D. P5. E-F Adult male, D. Antennule. F. P5. G. P6. H. Caudal ramus, ventral view, most frequent size and proportion; I. same, individual with
longer ramus. Scale bars: A = 10 µm, B,C, H, I = 20 µm; D-G = 30 µm.
DISCUSSION
Following Pesce and Galassi (1993) and Rocha (1995), up
to eight valid species of Neocyclops have been recorded in the
Caribbean region: N. medius Herbst, 1955; N. vicinus Herbst,
1955; N. afinis Pleşa, 1961; N. improvisus Pleşa, 1973; N.
stocki Pesce, 1985, N. papuensis Fiers, 1986, N. geltrudeae
Pesce & Galassi, 1993; and N. ferrarii Rocha, 1995. Only
three, N. vicinus, N. medius, and N. ferrarii have been reported
in South America (Herbst, 1955, Lotufo and Rocha, 1993,
present data).
Neocyclops ferrarii is assigned to the subgenus Protoneocyclops
for its four-segmented male P4, this group contains nine
species (Lee and Chang, 2015); this characteristic is shared
with other two American congeners: N. papuensis and N.
geltrudeae.
Neocyclops ferrarii can be easily recognized from its
congeners by a unique combination of characters including:
1) large scar-like integumental ridges originating from
the medial margins of the coxa in all swimming legs; 2)
P4ENP2-3 fused; 3) mandibular palp with three elements,
4) dorsal caudal seta from 0.8-1.0 as long as ramus, 5) inner
seta on irst exopodal segment of male ifth leg plumose.
Rocha (1995) proposed the integumental pore pattern as
a useful character to distinguish closely related species of
Neocyclops. He compared the pore topography of N. ferrarii
with that of N. vicinus and N. medius (Rocha, 1995, ig. 20,
21). We were able to observe pores on the caudal rami
(arrowed in Fig. 3C); out of this group of species, and only
N, ferrarii has pores in this position.
The transverse chitinized scars occurred in all specimens
observed. Similar structures have been previously reported
for four species from Australia: N. australiensis (Karanovic,
2008, igure 54A, D), N. sharkbayensis (Karanovic, 2008,
igs. 58D, 59B), N. trajani (Karanovic, 2008, ig. 61C) and
Acta biol. Colomb., 22(1):59-65, enero-abril 2017
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Fuentes-Reinés JM, Suárez-Morales E.
N. hoonsooi (Lee and Chang, 2015, igs 4A-D) but in the irst
three species the scars are less pronounced.
Specimens from Colombia are identical in most aspects to
those reported from the type locality in Belize (Rocha, 1995),
however, these two population show subtle differences: 1)
labrum with ten teeth in specimens from Colombia (present
data, ig, 3A) vs. nine in populations from Belize (Rocha,
1995), 2) the outer exopodal spine on female leg ive is
relatively shorter in the Colombian specimens (0.7 times as
long as segment) than in the type population (0.9) (Rocha,
1995, ig. 17). 3) the relative length of the mandibular palp
setae differs in the two populations; the Belizean specimens
have two short setae that are subequally long, whereas the
Colombian specimens one of these setae is at least twice
as long as the other one; 4) length/width ratio of caudal
rami is about 2.7–-3.1 in the specimens from Rodadero
Bay (present data, Fig 3C ) whereas it is 2.4 in specimens
from Belize (Rocha, 1995; ig 10; Karanovic, 2008; Lee
and Chang, 2015); 5) the length ratio of caudal setae VI/
III differs in these species, it is clearly longer in specimens
from Belize (ratio 1.37) (Rocha 1995, ig. 10) whereas the
igure for our specimens from Colombia is 1.25; 6) the
length ratio of caudal setae VII/VI is smaller in specimens
from Colombia (ratio = 0.8) vs. 1.0 in type specimens
from Belize; 7) The male body size of this species has a
new range: the specimens from Colombia are larger (602630 μm) than those reported from Belize (520-580 μm)
(Rocha, 1995), 8) the male caudal rami length/width ratio
is another variable structure; it ranged between 2.2–2.6 in
the Colombian population vs. 2.2 in the Belizean specimens
(Rocha, 1995). Overall, we do not regard such differences
as evidence enough to suggest the erection of a new species
to accommodate our specimens from Colombia.
Among the species of Neocyclops reported from the
Caribbean region and adjacent areas (see Pesce, 2016), N.
ferrarii closely resembles N. vicinus Herbst, 1955 from Brazil.
Both of them bear an antennary exopod, a 12-segmented
female antennule, and a 3, III P3ENP3 armature formula.
However, N. ferrarii can be separated from N. vicinus by several
characters. In N. ferrarii the length/width ratio of the female
caudal rami is 2.4 – 3.1(Rocha, 1995, ig 10, Present data,
ig 3C), vs. 2.5–2.9 in N. vicinus (Herbst, 1955, taf. 33a-b;
Lotufo and Rocha, 1993, ig 20). The length ratio of caudal
setae VI/III differs in these species, it is quite longer in N.
ferrarii (ratio: 1.25-1.37) (Rocha 1.995, ig 10, present data,
ig 3C) while in N. vicinus ranges from 0.9-1 (Herbst, 1955,
taf. 33a-b; Lotufo and Rocha, 1993, ig 20). The length
ratio of caudal setae VII/VI is smaller in N. ferrarii (ratio 0.81) vs. 1.4 in N. vicinus.
The number of segments of P4ENP is an important
difference between these two species; in N. ferrarii P4ENP
it is two-segmented (Rocha, 1995, ig 16, present data, ig
2D) vs. three-segmented in N. vicinus (Herbst, 1955, ig 33E).
In addition, the mandibular palp is armed with 3 setae in N.
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Acta biol. Colomb., 22(1):59-65, enero-abril 2017
ferrarii (Rocha, 1993, ig. 11, present data, ig. 3D) vs. two
setae in N. vicinus (Herbst, 1955; Lotufo and Rocha, 1993,
ig. 21). The male P5 of N. ferrarii is four-segmented (Rocha,
1995, ig 18, present data, ig 3F) vs. a three-segmented
condition in N. vicinus (Lotufo and Rocha, 1993, ig 16).
The information presented in this paper allows an increase
of the total number of free-living cyclopoid copepods
reported for Colombia (Fuentes-Reinés and SuárezMorales, 2015) to 48 species. Neocyclops stocki was the irst
species of the genus recorded from Colombia (see Gaviria
and Aranguren, 2007); the present record of N. ferrarii
represents the second from this country the second from
this country.
Distribution and ecology
Neocyclops ferrarii was originally described from a pond
adjacent to mangroves in Belize (Rocha, 1995); it was
recorded later in the northern sector of the Yucatan Peninsula
from the stomach contents of a coastal ish (Suárez-Morales
et al., 2002); the species was advanced by these authors as
a possible endemic of the Yucatan Peninsula, but its inding
in Colombia allows us to discard this idea; hence, N. ferrarii
is now deemed to be restricted to the western Caribbean.
In Colombia this species was found in the littoral zone of
the Rodadero Bay in an area covered by mangrove and at
a depth of 0.70 m where water temperature varies over
the seasons in the range of 30 – 32 ºC, salinity is 36.1 psu,
and pH 8.3. These environmental conditions are within the
ranges of salinity (19–39 psu) and temperature (30–35 °C)
reported by Rocha (1995) for the type locality.
CONCLUSIONS
The information presented in this paper documents in detail
the irst record of Neocyclops ferrarii in Colombia and reveals
a number of subtle morphological variations between the
Colombian specimens and the Belizean population. Its
presence in Colombia increases its known distributional
range in the western Caribbean. This species can be confused
with its congener N. vicinus in the Caribbean region but they
can be separated by some important characters including
the length/width ratio of the female caudal ramus, the number
of segments of P4ENP, the armature details of mandibular palp,
and the number of segments of the male P5.
CONFLICT OF INTEREST
The authors declare that they have no conlict of interest.
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