Mediterranean Marine Science Research Article
Indexed in WoS (Web of Science, ISI Thomson)
The journal is available on line at http://www.medit-mar-sc.net
First record of Paraprionospio coora Wilson, 1990 (Polychaeta: Spionidae)
from the Mediterranean Sea
H. YOKOYAMA1, E. DA LI2 and M. E. INAR2
1
National Research Institute of Aquaculture, Fisheries Research Agency, Minami-ise,
Mie 516-0193, Japan
2
Ege University, Faculty of Fisheries, Department of Hydrobiology, 35100 Bornova, Izmir, Turkey
Corresponding author:
[email protected]
Received: 28 October 2009; Accepted: 16 March 2010 Published on line: 21 April 2010
Abstract
The spionid polychaete Paraprionospio pinnata (Ehlers, 1901) has been widely reported from the
Mediterranean Sea. We examined some specimens belonging to the genus Paraprionospio that had
been collected from the Aegean Sea, the Sea of Marmara and the Spanish Mediterranean coast, and
identified them as Paraprionospio coora Wilson, 1990, which is new to the Mediterranean fauna. This
finding indicates that P. coora has a widespread geographical distribution in Australia, the Far East
and the Mediterranean, and suggests that the previous records of P. pinnata from the Mediterranean
are questionable.
Keywords: Paraprionospio coora; Taxonomy; Aegean Sea; Sea of Marmara; Turkey; Spain.
Introduction & HARTMAN, 1964; HARTMANN-
SCHRÖDER, 1965), resulting in it gaining
The spionid polychaete Paraprionospio recognition as a cosmopolitan species
pinnata (Ehlers, 1901) has been reported (LIGHT, 1978; MACIOLEK, 1985).
not only from the Mediterranean (BELLAN, FOSTER (1971) demonstrated that P. pin-
1964; DIAPOULIS & BOGDANOS, 1983; nata is a monotypic species which belongs
ERGEN, 1992; REDONDO & SAN to the genus Paraprionospio Caullery, 1914.
MART N, 1997; SIMBOURA & YOKOYAMA & TAMAI (1981), howev-
NICOLAIDOU, 2001; ERGEN et al., 2002, er, found that the Japanese specimens of
2006; INAR, 2005; DO AN et al., 2005) Paraprionospio pinnata comprised four dis-
but also from various temperate and trop- tinct forms of morphological variations based
ical waters in the world (e.g., FAUVEL, on a series of 11 characters including papil-
1932; WESENBERG-LUND, 1949; lae on posterior margins of the peristomi-
HARTMAN, 1960; DAY, 1961; IMAJIMA al wings, pigment patches on the peris-
Medit. Mar. Sci., 11/1, 2010, 133-141 133
tomium, accessory processes on the first lution. In the laboratory, the samples were
pair of branchiae, shapes of branchial lamel- sorted according to taxonomic groups un-
lae, filaments on the third chaetiger, a ven- der a stereomicroscope and preserved in
tral ridge on the eighth chaetiger, transverse 70% ethanol. Afterwards, specimens were
dorsal crests, a semi-transparent dorsal cu- identified and counted under stereo- and
ticle, interneuropodial pouches, lateral anal compound microscopes. The body length
cirri and the first appearance of nonlimbate and width of the 5th chaetiger (excluding
capillaries in neuropodia. They suggested parapodia) of the worms were measured
that the observed variations might be suffi- using an ocular micrometer. The specimens
cient to allow the forms to be distinguished examined were deposited at ESFM [Ege
at the specific level, but they did not deter- Universitesi Su Urünleri Müzesi (Museum
mine species names. Later, YOKOYAMA of Faculty of Fisheries, Ege University)].
(2007) published a revision of the genus A specimen which was collected from
Paraprionospio, in which 9 valid species the Spanish Mediterranean coast and de-
including 4 Japanese species that are P. coo- scribed as Paraprionospio pinnata in
ra Wilson, 1990, and 3 undescribed species REDONDO & SAN MART N (1997) was
(P. cordifolia Yokoyama, 2007, P. oceanen- also examined. The specimen was deposit-
sis Yokoyama, 2007 and P. patiens Yokoya- ed at MNCN (Museo Nacional de Ciencias
ma, 2007) were validated. ZHOU et al. (2008) Naturales).
also examined the Chinese specimens, which
were previously identified as P. pinnata, and Taxonomic Account
found that they belonged to the three species,
P. coora, P. inaequibranchia (Caullery, 1914) Paraprionospio coora Wilson, 1990
and an undescribed species (P. cristata Zhou, Paraprionospio sp. Form CI Yokoyama
Yokoyama & Li, 2008). The above-men- & Tamai, 1981: 311, Fig. 5.
tioned studies suggested a possibility of Paraprionospio coora Wilson, 1990: 266-
misidentification of the specimens, which 268, Figs 75-83; Yokoyama, 2007: 264, Fig.
were previously reported as P. pinnata. 8; Zhou et al., 2008: 309-311, Fig. 1.
Hence, we examined some specimens of Material examined: The Aegean Sea:
Paraprionospio collected from the Aegean ESFM-POL/08-22, 1 specimen, 21 May 2008,
Sea, the Sea of Marmara and the Spanish Gerence Bay, Station 1, 38Æ26'32''N,
Mediterranean coast to identify species. 26Æ29'07''E, 45 m, mud with shell fragments,
coll. E. Da li; ESFM-POL/07-37, 9 speci-
Material and Methods mens, 17 October 2007, Izmir Bay, Sta-
tion 3, 38Æ28'50''N, 26Æ46'27''E, 40 m, mud,
Specimens of Paraprionospio were col- coll. E. Da li; ESFM-POL/08-23, 8 speci-
lected at 21 stations in the Aegean Sea and mens, 4 May 2008, Gerence Bay, Station 4,
the Sea of Marmara between the years 1999 38Æ27'17''N, 26Æ27'14''E, 52 m, sandy mud,
and 2008 (Fig. 1). Samples were taken by coll. E. Da li; ESFM-POL/00-192, 1 spec-
an anchor dredge and a Van Veen Grab at imen, 29 July 2000, Izmir Bay, Station 5,
depths ranging from 17 to 135 m. All ben- 39Æ44'22''N, 26Æ01'59''E, 60 m, sandy mud,
thic samples were sieved through a 0.5 mm coll. E. Da li; ESFM-POL/99-19, 1 speci-
mesh and then the retained material was men, 27 May 1999, Izmir Bay, Station 6,
fixed with a 4% formaldehyde-sea water so- 36Æ35'25''N, 26Æ47'03''E, 22 m, mud, coll.
134 Medit. Mar. Sci., 11/1 2010, 133-141
Fig. 1: Map showing sampling stations of Paraprionospio coora.
M. E. inar; ESFM-POL/00-201, 2 speci- 39Æ15'00''N, 26Æ32'05''E, 53 m, sandy mud,
mens, 14 July 2000, Izmir Bay, Station 7, coll. E. Da li; ESFM-POL/00-208, 4 spec-
38Æ35'10''N, 26Æ45'35''E, 33 m, mud, coll. imens, 14 September 2000, Kusadasi Bay,
E. Da li; ESFM-POL/00-189, 1 specimen, Station 11, 37Æ55'18''N, 27Æ07'41''E, 78 m,
3 August 2000, Saroz Bay, Station 8, mud, coll. E. Da li; ESFM-POL/00-196,
40Æ27'40''N, 26Æ29'57''E, 135 m, mud, coll. 4 specimens, 14 July 2000, Izmir Bay, Sta-
E. Da li; ESFM-POL/00-191, 2 specimens, tion 12, 38Æ40'36''N, 26Æ41'50''E, 62 m, mud,
13 August 2000, Gokceada Island, Station coll. E. Da li; ESFM-POL/00-213, 1 spec-
9, 40Æ10'40''N, 25Æ40'50''E, 104 m, mud, imen, 19 September 2000, Gökova Bay, Sta-
coll. E. Da li; ESFM-POL/00-193, 1 spec- tion 13, 36Æ54'40''N, 28Æ09'57''E, 19 m,
imen, 28 July 2000, Aegean Sea, Station 10, sandy mud, coll. E. Da li; ESFM-POL/00-
Medit. Mar. Sci., 11/1, 2010, 133-141 135
187, 1 specimen, 4 August 2000, Saroz Bay, peristomium (Fig. 2a). Notopodial postchaetal
Station 14, 40Æ36'08''N, 26Æ33'53''E, 66 m, lamellae on chaetigers 1–3 long, foliaceous,
mud, coll. E. Da li; ESFM-POL/00-210, distally pointed (Fig. 2b-d); posterior to
3 specimens, 29 September 2000, south west- chaetiger 4, becoming rounded and reduc-
ern of Dilek Peninsula, Station 15, ing in size (Fig. 1e-h); posterior to chaetiger
37Æ38'50''N, 27Æ01'17''E, 35 m, mud, coll. 10, elevated increasingly, showing triangu-
E. Da li; ESFM-POL/00-211, 4 specimens, lar to lanceolate (Fig. 2i,j). Neuropodial
15 September 2000, east of Agathonisi Is- postchaetal lamellae of chaetiger 1–3 lance-
land, Station 16, 37Æ23'55''N, 27Æ06'52''E, olate (Fig. 2b-d); posterior to chaetiger 4,
71 m, mud, coll. E. Da li; ESFM-POL/00- lamellae becoming rounded and reducing
209, 1 specimen, 29 September 2000, Ku- to low postchaetal ridges by about chaetiger
sadasi Bay, Station 17, 37Æ48'00''N, 9 (Fig. 2e-h). Three pairs of branchiae on
27Æ16'00''E, 31 m, mud, coll. E. Da li; chaetigers 1–3. First branchiae longest ex-
ESFM-POL/00-194, 2 specimens, 14 July tending posteriorly to about chaetiger 10
2000, Izmir Bay, Station 18, 38Æ40'36''N, (Fig. 2a), second branchiae extending pos-
26Æ37'05''E, 73 m, mud, coll. E. Da li; teriorly to about chaetiger 9, third pair short-
ESFM-POL/00-207, 3 specimens, 30 Septem- est extending to about chaetiger 6. In basal
ber 2000, Kusadasi Bay, Station 19, region of first branchial shaft, 2–5 conic
37Æ59'00''N, 27Æ11'15''E, 32 m, mud, coll. processes placed along anterior face. All
E. Da li; ESFM-POL/00-200, 1 specimen, branchiae bearing lamellar plates; in prox-
14 July 2000, Izmir Bay, Station 20, imal region of branchial shaft, lamella con-
38Æ35'10''N, 26Æ43'05''E, 61 m, mud, coll. sisting of single triangular plate; succeeding
E. Da li; ESFM-POL/00-622, 1 specimen, lamellae consisting of two plates; in middle
19 January 2000, Izmir Bay, Station 22, and distal regions, two plates united com-
38Æ39'19''N, 26Æ37'04''E, 69 m, mud, coll. pletely, showing flabellate-shape. A small
E. Da li; Sea of Marmara: ESFM-POL/08- protuberance usually present on dorsum
24, 1 specimen, 9 August 2008, Erdak Bay, near base of third branchiae (Fig. 2d), in-
Station 2, 40Æ18'42''N, 27Æ46'18''E, 17 m, stead of the slender filament in some of the
sandy mud, coll. E. Da li; Spanish Mediter- other Paraprionospio species. Anterior chaetae
ranean coast: MNCN 16.01/2646, 1 speci- all limbate capillaries bearing granules (Fig.
men, Station between Cape San Antonio 3a). Posterior to about chaetiger 16, no-
and Valencia Harbour, coll. CIS (Centro topodial limbate capillaries replaced by slen-
de Investigaciones Submarinas). der, nonlimbate capillaries. Neuropodial
Description: Largest complete speci- hooded hooks with 2–3 pairs of apical teeth
men, 42 mm long, 1.3 mm wide with 95 above main fang and striate secondary in-
chaetigers. Prostomium fusiform with round ternal hood from chaetiger 9 (Fig. 3b,c), ac-
or bluntly pointed anterior end (Fig. 2a), ex- companied by alternating nonlimbate slen-
tending posteriorly as a faintly raised ridge der capillaries (Fig. 3d) and one to two gran-
to first chaetiger. Two pairs of black, small ulated sabre chaetae (Fig. 3e). Notopodial
eyes in trapezoidal arrangement. Brown pig- hooded hooks with 3 pairs of apical teeth
ment patch usually present on lateral side above main fang and striate secondary in-
of peristomium (Fig. 2a). Faint groove just ternal hood appearing from about chaetiger
posterior to pigmented area on peristomi- 33 (Fig. 3f). No ventral bilobed flap on
um. Small papilla on posterior margin of chaetiger 8. No interneuropodial pouches
136 Medit. Mar. Sci., 11/1 2010, 133-141
Fig. 2: Paraprionospio coora collected from the Aegean Sea (a, ESFM-POL/99-19; b-k, ESFM-POL/08-
23). a, Anterior end in dorso-lateral view; b, 1st parapodium, in anterior view; c, 2nd parapodium, in
anterior view; d, 3rd parapodium, 3rd branchia and a protuberance near the base of the 3rd branchia,
in anterior view; e, 4th parapodium, in anterior view; f, 5th parapodium, in anterior view; g, 8th
parapodium, in anterior view; h, 9th parapodium, in anterior view; i, 15th parapodium, in anterior
view; j, 48th parapodium, in anterior view; k, posterior end, in ventral view.
Medit. Mar. Sci., 11/1, 2010, 133-141 137
Fig. 3: Paraprionospio coora collected from the Aegean Sea (ESFM-POL/08-23). a, Notopodial lim-
bate capillary from chaetiger 4; b, neuropodial hooded hood from chaetiger 9, bearing 2 pairs of api-
cal teeth; c, neuropodial hooded hood from chaetiger 9, bearing 3 pairs of apical teeth; d, neuropo-
dial non-limbate capillary from chaetiger 9; e, sabre chaeta from chaetiger 39; f, notopodial hooded
hook from chaetiger 48.
from all specimens. Dorsum of chaetigers from Australia by WILSON (1990), but have
4–11 faintly biannulated. Dorsum of chaetigers 2–3 pairs of apical teeth in neuropodial hood-
12–17 transverse series of lighter colored ed hooks rather than only 2 pairs of apical
slightly raised ridges, 3 ridges per chaetiger. teeth. A variable number of apical teeth was
Membranous dorsal crests and semi-trans- noted within the Mediterranean specimens,
parent dorsal cuticle absent. Pygidium with suggesting that this is not a stable charac-
a long median anal cirrus and two short, lat- teristic to be used in distinguishing species.
eral cirri (Fig. 2k). Muscular gizzard pres- Interneuropodial pouches were found in
ent between chaetigers 6–8. most specimens collected from Australia
Distribution: Western Japan, more (WILSON, 1990) and in some specimens
southern than 37ÆN; Yellow Sea, East Chi- from Japan (YOKOYAMA, 2007) and Chi-
na Sea, New South Wales to Tasmania in na (ZHOU et al., 2008), whereas all Mediter-
Australia, Mediterranean. ranean specimens examined in this study
Remarks: The Mediterranean speci- lack this characteristic. However, it seems
mens of Paraprionospio coora closely agree this is not a stable characteristic which can
with the original description of the species be dependably used in distinguishing species,
138 Medit. Mar. Sci., 11/1 2010, 133-141
because the number of interneuropodial longest or the first and second branchiae
pouches varies from zero to about 30 even are approximately equal in length, the third
in a local population in Australia, China and pair is the shortest (branchiae are almost
Japan. The Mediterranean specimens have equal in size in P. pinnata); 3) P. coora has
a small protuberance on the dorsum near conic processes in the basal region of the
the base of third branchiae (Fig. 2d) instead first branchial shaft (no processes in P. pin-
of the slender filament in some of the oth- nata); 4) P. coora has a small protuberance
er Paraprionospio species (see Figs on the dorsum near the base of the third
1,10,11,13,14 in YOKOYAMA, 2007). branchiae (no protuberance in P. pinnata);
WILSON (1990), YOKOYAMA (2007) and 5) P. coora lacks a semi-transparent dor-
ZHOU et al. (2008) did not mention this sal cuticle (P. pinnata has a semi-transpar-
characteristic however, we found the same ent dorsal cuticle); and 6) Interparapodial
structure in the Japanese specimens of P. pouches are present in some specimens of
coora. Hence, we identified the Mediter- P. coora (absent in P. pinnata).
ranean specimens as P. coora. It is the first Paraprionospio coora has been reported
time this species has been recorded from the from distant regions (i.e. Australia, Japan
Mediterranean Sea; the present study has and China) before (WILSON, 1990; YO-
revealed the widespread geographical oc- KOYAMA, 2007; ZHOU et al., 2008). The
currence of P. coora from Australia, the Far occurrence of P. coora in the Mediterranean
East and the Mediterranean. Sea indicates that this species has a wider
The closely similar species Paraprionos- distributional pattern than we know now.
pio pinnata was first recorded from the west- Spionid polychaetes are known to invade dif-
ern Mediterranean by BELLAN (1964) and ferent zoogeographic regions as a result of
from the eastern Mediterranean by ERGEN their introduction via the ballast waters of
(1992). Later, this species was reported es- ships (BASTROP et al., 1997; INAR et al.,
pecially from the eastern Mediterranean 2005, 2006, 2008; DA LI & INAR, 2009)
(DIAPOULIS & BOGDANOS, 1983; or the introduction of molluscs into coastal
SIMBOURA & NICOLAIDOU, 2001; waters for further commercial cultivation
ERGEN et al., 2002, 2006; DO AN et al., (MORENO et al., 2006; RADASHEVSKY
2005; INAR, 2005) and the Red Sea et al., 2006). P. coora may be included in alien
(FAUVEL, 1933). The examination of the species however, at present their alien sta-
older benthic material, which was collected tus cannot be demonstrated based on scien-
in the Aegean Sea and identified as P. pin- tific data except for their extensive geo-
nata, in fact belongs to P. coora. This finding graphical distribution. The discovery of
suggests that the occurrence of P. pinnata this species in other parts of the world and
in the Mediterranean should be reexamined. genetic studies on its distant populations
Paraprionospio coora is closely related would shed more light on its alien status.
to P. pinnata in morphological and chaetal
appearances. However, P. coora easily Acknowledgements
distinguishes from P. pinnata in the follow-
ing characteristics 1) P. coora has a small We thank Guillermo San Martin for in-
papilla on posterior margin of the peris- forming us that his material was deposit-
tomium (no papilla in P. pinnata); 2) The ed in MNCN and to Javier Sa’ nchez Almaza’ n
first branchiae of P. coora are usually the for arranging the loan of the material.
Medit. Mar. Sci., 11/1, 2010, 133-141 139
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