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Acartia bifilosa (Copepoda: Calanoida): A clarification of the species and its

varieties inermis and intermedia

Article  in  Journal of Plankton Research · June 1998

DOI: 10.1093/plankt/20.6.1119 · Source: OAI

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Journal of Plankton Research Vol.20 no.6 pp.1119-1130, 1998

Acartia bifilosa (Copepoda: Calanoida): a clarification of the

species and its varieties inermis and intermedia
A.G.Hirst1 and E.Castro-Longoria
Department of Oceanography, University of Southampton, Southampton
Oceanography Centre, Empress Dock, Southampton SO14 3ZH, UK
Present address: George Deacon Division, Southampton Oceanography Centre,
Empress Dock, Southampton SO14 3ZH, UK

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Abstract. Adults of the calanoid copepod Acartia bifilosa and the varieties inermis and intermedia are
examined and described. This study brings to light discrepancies in the available keys to all these
forms. Individuals previously reported and also deposited in museum collections as A.bifilosa var.
inermis and var. intermedia are shown to be similar to A.bifilosa with respect to characteristics previ-
ously used for classification. Acartia bifilosa and its varieties were shown to possess setules on the
dorsal side of female and male urosomes, although there was great variation in the size and position
of these. The fifth legs (P5) of adult males and females were very similar in all individuals examined,
regardless of how they were previously classified, although the original descriptions are generally
inadequate or misleading. These results bring into doubt the arguments used by Rose (1929) to report
A.bifilosa var. inermis. A single unified species, A.bifilosa (Giesbrecht), is suggested here, with some
of the variation in its form being detailed. We believe errors may have occurred because of the angle
from which features were previously examined, and because some of the features could be missed
using light microscopy.

Introduction
The calanoid copepod Acartia bifilosa was first described by Giesbrecht (1881)
from samples collected at Kiel, Germany. Later, a more extensive description
with illustrations, based on specimens from the Gulf of Naples, Italy, was
completed by Giesbrecht (1892). Acartia bifilosa has since been reported from
the north and temperate Atlantic, North Sea, English Channel and Baltic
(Gurney, 1931; Rose, 1933; Bradford-Grieve, 1998), and the North Pacific, in the
Sea of Okhotsk (Brodskii, 1950), and Korean coastal waters (Yoo et al, 1991;
Shim and Choi, 1996). Although recorded from the open sea, it is characteris-
tically a brackish and estuarine species. Since the original species description, two
varietal forms of A.bifilosa have also been described in the literature. The species
and varieties are often the biomass- and abundance-dominant copepods in
reduced salinity waters not only around Europe (Brylinski, 1981; Collins and
Williams, 1982; Hirst, 1996), but also in the North Pacific (Shim and Choi, 1996).
Acartia bifilosa var. intermedia {Dias intermedius Poppe, 1887 = Acartia inter-
media) was described from the North Sea coast of Germany. Gumey (1931)
reported that 'A.intermedia is regarded by Van Breemen and Steuer as a synonym
of A.bifilosa. On the other hand, Timm (1896) states that it is distinguishable from
the typical form and that it is characteristic of the coastal region from the Ems to
the Elbe'. This variety has not featured in recent literature; we were, however,
able to obtain specimens described as var. intermedia, deposited in 1900, from the
Natural History Museum (London).
© Oxford University Press 1119
A.G-Hirst and E.Castro-Longoria

Acartia bifilosa var. inermis was described by Rose (1929) from the Loire
Estuary, France, and the Atlantic off Gibraltar. More recently, it has been
reported from the Bristol Channel, UK (Collins and Williams, 1982; Williams and
Collins, 1985), and the Forth Estuary, UK (Taylor, 1984), and possibly a number
of Irish estuaries (see Taylor, 1984).
Examinations of specimens from Southampton Water, UK, where A.bifilosa
has been previously recorded (Conover, 1957; Raymont and Carrie, 1964), have
revealed that individuals from this estuary bear similarities to the published
descriptions of A.bifilosa (Giesbrecht, 1881,1892), A.bifilosa var. inermis (Rose,
1929, 1933) and A.bifilosa var. intermedia (Poppe, 1887), but do not conform to
any of the descriptions singularly. Detailed examinations of material are reported
here to clarify the taxonomic position of A.bifilosa and its varieties.

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Method
Six sets of samples variously described as A.bifilosa, A.bifilosa var. intermedia
and A.bifilosa var. inermis were examined here. Specimens of var. intermedia
deposited by D.Norman at the Natural History Museum (London) in 1900,
collected in the Jadebusens, on the North Sea coast of Germany, were available
to us. Specimens of var. inermis deposited by M.Rose at the Museum National
D'Histoire Naturelle (Paris), on 31 December 1937, were also made available.
The collection site of these specimens was not given, and although M.Rose
described this variety originally, we do not know whether the sample represented
the 'type' collection. Specimens assigned to A.bifilosa were available from
Southampton Water, UK, Storfjorden on the southern coast of Finland, Baltic
(samples courtesy of M.Koski, Finnish Institute of Marine Research, Finland),
and Breydon Water, UK (collected by R.Gurney, and deposited at the Natural
History Museum, London). Material identified as var. inermis from the Bristol
Channel, UK (Collins and Williams, 1982; Williams and Collins, 1985), was also
included in this study (samples courtesy of D.Conway, Plymouth Marine Labora-
tory, UK).
The original descriptions of A.bifilosa (Giesbrecht, 1881), and the varieties
intermedia (Poppe, 1885) and inermis (Rose, 1929), together with the later
descriptions of A.bifilosa (Giesbrecht, 1892; Rose, 1929; Gurney, 1931; Crisafi and
Crescenti, 1972), were compared to one another and to the specimens studied
here. A random selection of individuals was taken from each of the available sets
of material, adults were separated from juveniles and sexed. A compound light
microscope was used to observe male and female fifth pereiopods (P5s) and
urosomes, and a scanning electron microscope to examine and compare the
urosomes and P5s in greater detail. Emphasis was placed on the characteristics
previously used to separate the species and varieties.

Results
Morphological comparisons between the original descriptions and preserved
specimens are presented in a summarized form in Table I. According to Rose
1120
Table I. Comparisons of original descriptions oiA.bifilosa and varieties inermis and intermedia with those observed on specimens examined in this investigation
Acania bifilosa A.bifilosa var. intermedia A.bifilosa var. inermis A.bifilosa from
Southampton Water
Original descriptions Giesbrecht (1881,1892) Poppe (1885) Rose (1929)
Female urosome Genital and 2nd segment covered Urosome segments naked Urosome segments without
with rows of fine setules spines, drawn naked
Male urosome Without spines Urosome segments naked Sometimes setules on external
edge of segments 1 and 2
Female P5 Spine of PS slightly swollen at base, Spine of P5 bulbous at the base, Spine of P5 slightly swollen at
spine straight and toothed toothed on inner and outer edges the base and curved, toothed
on inner and outer edges on inner and outer edge
Male P5 Right Rel has two inner expansions, Right Rel with two inner expansions, Right Rel with two inner
and a small, heavy appendix on 3rd left segment ends with a spine expansions and last segment
left Re2+3 and a small appendix with two spines narrowed at base. Left Re2 with
at its end external spines grouped
Specimens examined Deposited by R.Gurney Deposited by D.Norman Deposited by M.Rose Collected in Southampton
Natural History Museum, London Natural History Museum, London Museum National D'Histoire Water, UK
(1950.9.20.170,171) (190O.3.29.321) Naturelle, Paris (Cp 1120)
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Female urosome Very few small setules present Some setules present (see Figure 2a) Setules present (see Figure la) Setules present
(see Figure 3a)
Male urosome Some setules present, but Some setules present (see Figure 2b) Setules present (see Figure lb) Setules present
variable and at times very
small (see Figure 3b-d)

Female P5 Spine bulbous at the base, As in all other specimens (see first As in all other specimens (see As in all other specimens (see
slightly curved, toothed on column description) first column description) first column description)
inner and outer edge
(see Figure 4a and b)
Right Rel has two inner expansions, As in all other specimens (see first As in all other specimens (see As in all other specimens (see
Male P5 and a heavy appendix on left column description) first column description) first column description)
Re2+3 with 2 spines, one at
either point (see Figure Sa and b)
A.CHiist and E.Castro-Longoria

(1929), female var. inermis have a naked urosome, whereas some males have
setules on the lateral margin of segments 1 and 2. The present study revealed
setules on the urosome segments of female and male A.bifilosa var. inermis speci-
mens deposited by M.Rose (see Figure la and b).
All females examined, regardless of their description as species or variety, were
found not to differ in any obvious way with regard to their P5. They all possess
very prominent bulges at the base of each of the P5 spines (see Figure 4a and b).
The bulge is more pronounced than described lor A.bifilosa by Giesbrecht (1881,
1892), Gurney (1931) and Crisafi and Crescenti (1972), and more similar to the
description by Rose (1929) for the variety inermis and by Poppe (1887) for the
variety intermedia. Figure 4a and b show the spine at different orientations, and
demonstrate the squareness of the proximal swelling of the P5 spine when viewed

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from the side. Previous poor descriptions are probably the result of the viewing
orientation.
Females of the variety inermis have been described as having P5 spines which
were curved at their ends, while the spines on A.bifilosa were described as being
almost straight (Rose, 1933). Not all workers have described A.bifilosa as having
almost straight P5 spines; indeed, curvature of these spines is most obvious in the
drawings of Crisafi and Crescenti (1972), while the P5 spines are straightest in the
drawings of Giesbrecht (1892). There is, therefore, certainly some degree of
gradation across the descriptions of A.bifilosa. Some degree of curvature was
observed in all the individuals examined here, although there was some variabil-
ity. Gurney's (1931) drawings of A.bifilosa female P5 spines show small teeth-like
processes on the internal side, while the drawings of Giesbrecht (1881,1892) and
Crisafi and Crescenti (1972) show spines both internally and externally. The
drawings of var. inermis by Rose (1929) show these teeth on the internal and
external sides. All of the specimens examined in this work had both internal and
external teeth on female P5 spines (see Figure 4a and b).
Descriptions of the male P5s of A.bifilosa have differed between authors. Rose
(1933) describes the P5 of var. inermis as being the same general structure as that
in A.bifilosa, except that the last segment of the right P5 is constricted at the base,
and has a group of three points at the end of the left P5 (i.e. the external spines)
in the variety. The male P5s of A.bifilosa drawn by Giesbrecht (1892) show
the last segment of the right P5 as being much less constricted at its base, and the
right Rel as having two inner expansions, and a small, heavy appendix on the
distal joint of the left P5 (Re2). All male P5s examined by us showed the same
characteristics; a representative P5 is shown in Figure 5a and b. The last segment
of the right P5 on the male is not as constricted as shown in the drawings of Rose
(1929), but generally not as broad as that given in the description of Giesbrecht
(1892). Our own observations using light microscopy revealed that the full width
of the base is not always obvious under some conditions of illumination. The male
right P5 Rel has two inner expansions, the proximal having a spine (not visible
in Figure 5a). The Re2 has a pronounced inner expansion, and the Re3 ends with
a heavy spine, and several clumps of spines on the middle external borders (see
Figure 5a). The terminal segment of the left P5 (see Figure 5b) ends in a heavy
spine (HS) and a triangular appendage (T) which has a covering of fine setules,

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Fig. 1. Acariia bifilosa var. inermis (deposited by M.Rose), (a) Female urosome, lateral view with spermatophore; (b) male urosome, dorsal view.
NJ s.
 (b)

g.

I
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Fig. 2. Acartia bifilosa var. intermedia (deposited by S.A.Poppe). (a) Female nirosome, lateral view; (b) male urosome, lateral view.
 Clarification of A.bifilosa and its varieties

and two spines, one on either of the outer points (marked by small arrows in the
figure), while being connected near the inner point.

Discussion
Rose (1929) based his description of A.bifilosa var. inermis on the absence of fine
setules on the dorsal surface of the female urosome, and on the female P5 being
curved instead of straight. Although there is variability in the phenotype of the
individuals examined in this study, particularly with respect to the pattern of
setules on the urosome, the classifications used previously to separate the species
and varieties are unfounded. Some confusion may have occurred because of the

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initial description of A.bifilosa (Giesbrecht, 1892), with female P5 spines being
illustrated as almost straight with no bulbous base. With respect to the descrip-
tion and drawings of Rose (1929), the last segment on the male right P5 is
described as constricted at the base, and this feature was observed in specimens
that were examined in the present study. This characteristic appears to be depen-
dent upon the angle at which it is viewed, however, and this may have led to the
confusion.
Rose (1929) also appeared to miss that setules were present not only on male
urosomes, but also female urosomes (see Figure la and b). We observed much
variability in the positioning and length of setules on the urosomes of males and
females. Other species of Acartia also show variability in the distribution of
setules on the urosome. Shadrin and Popova (1994) demonstrated wide variation
in the patterns on populations of Acartia clausi within the Black Sea through time.
Comparisons of SEM photographs of Acartia tonsa from the Straits of Magellan,
South America (Mazzocchi et al, 1995), and from the Black Sea (Belmonte et ai,
1994), show large differences. Bradford (1976) emphasizes the importance of
ornamentation of the posterior metasome and urosome segments as character-
istics in separating species. Although she acknowledges that the number of spines
and setules (hairs) may vary, their presence or absence seems to be a constant
character. We suggest that A.bifilosa and its varieties be re-grouped as one form.
Much of the confusion over varietal status of populations within A.bifilosa may
have arisen because of the difficulty in observing some characters using light
microscopy, and particular care needs be exercised when describing the distri-
bution and presence/absence of setules on the urosome.

Acknowledgements
The authors wish to thank the Natural History Museum (London), the Museum
National D'Histoire Naturelle (Paris), together with D.Conway (Plymouth
Marine Laboratory) and M.Koski (Finnish Institute for Marine Sciences,
Finland), for making specimens available. We thank Martin Sheader and Mike
Thurston for commenting on earlier drafts of this manuscript. A.G.H. was funded
by a NERC studentship (GT/4/92/261/A). E.C.-L. was funded by the Consejo
National de Ciencia y Tecnologia (CONACyT) Mexico, and the ORS awards
scheme.
1125
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A.G.Hirst and E.Castro-Longoria

1126
 (<=)

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i
,_, Fig. 3. Acartia bifilosa (deposited by R.Gurney). (a) Female urosome, lateral view; (b) male urosome, dorsal view; (c) male urosome, dorsal view; (d) the speci-
i-* men shown in (c) at greater magnification, showing the presence of small setules.
—J
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FIf. 4. Acartia bifilosa (from Southampton Water, UK) female P5s. (a) Viewed from above; (b) viewed from the side.
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9
©

Fig. 5. Acariia bifilosa (from Southampton Water, UK) male P5s. (a) Right P5; (b) left P5. HS, heavy spine; T, triangular appendage, small arrows mark outer
spines on the triangular appendage.
 A.G-Hirsl and E.Castro-Longoria

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Received on September 27, 1997; accepted on January 21,1998

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