Turk J Zool 31 (2007) 403-410 © TÜB‹TAK

A Preliminary Study on the Population Characteristics of the Lessepsian Species Pseudonereis anomala (Polychaeta: Nereididae) in ‹skenderun Bay (, Eastern Mediterranean)

Melih Ertan ÇINAR*, Cem ALTUN Ege University, Faculty of Fisheries, Department of Hydrobiology, 35100 Bornova, ‹zmir -

Received: 21.11.2006

Abstract: The present paper deals with the population structure and biology of Pseudonereis anomala collected from different shallow-water habitats of ‹skenderun Bay in September 2005. In all, 434 specimens of P. anomala were found in the area. The maximum density and biomass values of the species in the area were 2475 ind. m-2 (on Jania rubens) and 7.85 g m-2 (among the bivalve pharaonis), respectively. The relationships among the biometrical measurements of the P. anomala specimens were assessed using regression and correlation analyses. The growth of P. anomala seems to be allometric. Among the specimens examined, only one specimen had immature oocytes. Only plant remnants were found in the digestive tracts of the dissected specimens.

Key Words: Pseudonereis anomala, Nereididae, Polychaeta, Lessepsian, population structure, Levantine Sea, Turkey

Lessepsian Tür Pseudonereis anomala’n›n (Polychaeta: Nereididae) ‹skenderun Körfezi’ndeki (Levantin Denizi, Do¤u Akdeniz) Populasyon Özellikleri Üzerine Bir Ön Çal›flma

Özet: Bu çal›flma, Eylül 2005’de ‹skenderun Körfezi’nin çeflitli k›y›sal habitatlar›ndan toplanan Pseudonereis anomala’n›n populasyon yap›s›n› ve biyolojisini ele almaktad›r. Bölgede P.anomala’ya ait toplam 434 birey bulunmufltur. Bu türün bölgedeki azami yo¤unluk ve biyokütle de¤erleri s›ras›yla 2475 birey m-2 (istasyon K1, Jania rubens üzerinde) ve 7,85 g m-2 (istasyon K5, Brachidontes pharaonis üzerinde) olarak bulunmufltur. ‹skenderun Körfezi’ndeki P. anomala bireylerinin biyometrik ölçümleri aras›ndaki iliflkiler, regresyon ve korelasyon analizleri kullan›larak saptanm›flt›r. P. anomala’n›n büyümesi muhtemelen allometriktir. ‹ncelenen bireyler aras›nda, sadece bir bireyin olgun olmayan yumurtalar tafl›d›¤› bulunmufltur. Disekte edilen bireylerin sindirim kanallar›nda sadece bitki kal›nt›lar› bulunmufltur.

Anahtar Sözcükler: Pseudonereis anomala, Nereididae, Polychaeta, Lessepsian, populasyon yap›s›, Levantin Denizi, Türkiye

Introduction 2005). The main route of introduction of these species to Human-mediated species introduction is one of the the Mediterranean is by shipping and via the Suez Canal. major factors adversely affecting biological diversity Pseudonereis anomala Gravier, 1901, a Lessepsian (Elton, 1958). Although there is an increasing awareness species (i.e. a species that migrated from the Red Sea to of this problem at local and global levels, preventing the the through the Suez Canal), is known spread of and eradicating alien species is becoming to have been well-acclimated to environmental conditions difficult as global trade by shipping increases daily and of the eastern Mediterranean (Ben-Eliahu, 1975; Çinar many alien species have already achieved perpetuating and Ergen, 1995). It is a common species in hard-bottom populations in the Mediterranean. In all, 749 alien species communities in the Red Sea, and the Indian and Pacific are known from the Mediterranean Sea (Zenetos et al., oceans (Wu et al., 1985). In the Mediterranean Sea, this 2005) and 277 from the Turkish coasts (Çinar et al., species was first reported by Fauvel (1937) (off

* E-mail: [email protected]

403 A Preliminary Study on the Population Characteristics of the Lessepsian Species Pseudonereis anomala (Polychaeta: Nereididae) in ‹skenderun Bay (Levantine Sea, Eastern Mediterranean)

Alexandria, Egypt) and subsequently was found along the Material and Methods Israeli coast (Fauvel, 1955; Ben-Eliahu, 1975), the A cruise to the Turkish Levantine coast was Lebanese coast (Laubier, 1966), the Cypriot coast (Ben- undertaken in September 2005 to collect samples of Eliahu, 1972; Çinar, 2005), and the Turkish Levantine benthos from different depths and habitats. In this study coast (Ben-Eliahu, 1989; Ergen and Çinar, 1997). only samples taken from ‹skenderun Bay were evaluated. Recently, this species was found off the Turkish and Scuba diving and snorkeling were used at 8 shallow water Greek coasts of the Aegean and Ionian Seas (Çinar and stations (ca. 0-5 m; Figure 1). Specimens of Pseudonereis Ergen, 2005; Kambouroglou and Nicolaidou, 2006). anomala were only found on algae [Ulva sp., Jania rubens Clearly, this species has become an important invasive (Linnaeus) Lamouroux, Cystoseira sp., Padina pavonica component of shallow-water benthic communities of the (Linnaeus) Thivy] on rocks, and among Brachidontes eastern Mediterranean; however, no study has yet pharaonis (P. Fischer, 1870) at depths of 0-3 m. At all focused on its population characteristics in the Turkish stations samples were taken within a 20 × 20 cm region, although some data about its reproductive and quadrat. feeding behavior are given by Çinar and Ergen (2005). In the laboratory the samples were sorted under a This paper presents the population and bio-ecological stereomicroscope and specimens of Pseudonereis features of Pseudonereis anomala collected from anomala were separated from other taxa, identified, and different habitats in ‹skenderun Bay (Levantine coast of counted. The body length and width at chaetiger 10 Turkey) in September 2005. (excluding parapodia) of unbroken specimens (n = 93)

.

Figure 1. Map of the study area and sampling site locations.

404 M. E. ÇINAR, C. ALTUN

were determined with an ocular micrometer. The wet- The highest mean population density (550 ind. m-2) of weight of specimens was estimated using a balance Pseudonereis anomala was found on samples of the sensitive to 0.0001 g. All specimens measured were Lessepsian , Branchidontes pharaonis, whereas dissected to observe their gametes and gut contents. samples of the brown alga Padina pavonica contained only To characterize population structures of Pseudonereis a few individuals (Figure 3). The more structurally anomala in the area, regression and Pearson product- complex brown alga, Cystoseira sp., supported large moment correlation analyses were performed on the data individuals of P. anomala and the highest mean biomass set to assess the relationships among the biometrical score of the species was encountered in this habitat measurements taken. (Figure 3). The mean density and biomass values of Pseudonereis Results anomala on the mussel Brachidontes pharaonis varied according to station; 858 ind. m-2 and 3.83 g m-2 at In all, 434 specimens of Pseudonereis anomala were station K5, and 242 ind. m-2 and 1.83 g m-2 at station found at 8 stations located in and around ‹skenderun Bay. K1. The mean density of Pseudonereis anomala at stations A similar finding was noted with regard to the red varied from 779 ind. m-2 (station K1) to 8 ind. m-2 alga Jania rubens. The population and biomass values of (station K11), and the wet-weight biomass ranged from -2 -2 Pseudonereis anomala were higher on the alga samples 6 g m (station K7) to 0.04 g m (station K11 (Figure collected at station K1 and these values diminished at the 2). The maximum density and biomass values of P. anomala in ‹skenderun Bay were 2475 ind. m-2 (at station more northern stations (Figure 4). K1, on Jania rubens) and 7.85 g m-2 (at station K5, on The individual body length of Pseudonereis anomala in Brachidontes pharaonis), respectively. ‹skenderun Bay ranged from 0.2 to 27.3 mm (Figure 5); )

-2 1400 1200 1000 800 600 400 200

Mean population density (ind. m 0 K1 K5 K7 K7a K8a K9 K10 K11

) 7 -2 6 5 4 3 2 1

Mean biomass (wet weight g m 0 K1 K5 K7 K7a K8a K9 K10 K11 Stations

Figure 2. Mean density and biomass values of Pseudonereis anomala at stations in ‹skenderun Bay. Bar represents + standard error.

405 A Preliminary Study on the Population Characteristics of the Lessepsian Species Pseudonereis anomala (Polychaeta: Nereididae) in ‹skenderun Bay (Levantine Sea, Eastern Mediterranean) )

-2 900 800 700 600 500 400 300 200 100

Mean population density (ind. m 0 Jania Cystoseira sp. Brachidontes Ulva sp. Padina rubens pharaonis pavonico )

-2 7 6 5 4 3 2 1 0 Mean biomass (wet weight g m Jania Cystoseira sp. Brachidontes Ulva sp. Padina rubens pharaonis pavonico Habitats

Figure 3. Mean density and biomass values of Pseudonereis anomala in habitats in ‹skenderun Bay. Bar represents + standard error. )

-2 2500

2000

1500

1000

500

Mean population density (ind. m 0 K1 K5 K10 K11 3.5 ) -2 3 2.5 2 1.5 1 0.5 0 Mean biomass (wet weight g m K1 K5 K10 K11 Stations

Figure 4. Mean density and biomass values of Pseudonereis anomala on the alga Jania rubens in ‹skenderun Bay. Bar represents + standard error. The under-water photograph of J. rubens was taken at station 10 by Alp Can.

406 M. E. ÇINAR, C. ALTUN

40 24 n = 93 20 30 16

20 12 8 10 Number of individuals

Number of individuals 4

0 0 51015202530 0 0.2 0.4 0.6 0.8 1 1.2 1.4 1.6 1.8 2 2.2 2.4 2.6 Body length (mm) Body width (mm) 80 70 60 50 40 30 20

Number of individuals 10 0 03551015202530 Body weight (mg)

Figure 5. The length, width, and weight frequency histograms of individuals of Pseudonereis anomala collected from ‹skenderun Bay in September 2005.

most commonly the length ranged between 5 and 10 mm 40 y = 0.0035x2.55 (n = 34). The body width varied between 0.2 and 2.46 35 R2 = 0.889, r = 0.89, P < 0.05 30 n = 93 mm, with individuals of 0.6-0.8 mm body width being 25 dominant (Figure 5). Although the individual biomass of 20 15 the species varied from 2 to 35 mg in the area, 75% of 10 the population had a biomass value between 2 and 5 mg, Body weight (mg) 5 0 showing the importance of juvenile individuals in the 010203051525 population (Figure 5). Body length (mm) 40 The length (mm)-weight (mg) relationship of 35 y = 2.51x2.95 30 R2 = 0.89, r = 0.91, P < 0.05 Pseudonereis anomala individuals is presented in Figure 25 n = 93 6. The regression formula for the relationship was W = 20 × 2.55 15 0.0035 L , indicating that the growth of P. anomala 10 is allometric, as the parameter b (2.55) was < 3. Body weight (mg) 5 However, the regression equation estimated between the 0 0 0.5 1 1.5 2 2.5 3 body width and weight suggests that growth could also Body width (mm) 40 be isometric as the parameter b (2.95) approaches 3. The 35 y = 0.0035e0.1275x relationship between the number of chaetigers and body 30 R2 = 0.8679, r = 0.72, P < 0.05 weight was exponential (Figure 6). The body weight 25 n = 93 20 remains somewhat constant in specimens with 16-43 15 chaetigers and suddenly increases in individuals having 10 Body weight (mg) more than 43. 5 0 The relationship between body length and the number 0 1020304050607080 Number of chaetigers of chaetigers of individuals of the species was logarithmic and the correlation score between these parameters was Figure 6. The length-weight, width-weight, and chaetiger numbers- significantly high (r = 0.92, P < 0.05) (Figure 7). A linear weight relationships of Pseudonereis anomala.

407 A Preliminary Study on the Population Characteristics of the Lessepsian Species Pseudonereis anomala (Polychaeta: Nereididae) in ‹skenderun Bay (Levantine Sea, Eastern Mediterranean) relationship was estimated between the body length and Pseudonereis anomala, could act as a potential food width (Figure 7). source for many large predators, including crabs and The body weight, width, length, and chaetiger fishes. However, Ben-Eliahu (1989) reported that number of Pseudonereis anomala samples collected from Perinereis cultrifera (Grube, 1840), a native nereidid the alga (Jania rubens) and mussel (Branchidontes species of the Mediterranean, was excluded from a pharaonis) did not differ significantly (t test, P < 0.05) shallow-water algal habitat along the Israeli coast, probably due to an inferior dispersal method; P. cultrifera Among the specimens examined, only one specimen appears to have direct, non-pelagic reproduction along had eggs in its coelomic cavity; egg mean diameter was the Levant coast and its dispersal is consequently more 67.9 µm ± 1.09 SE (n = 40) and minimum-maximum restricted than that of the migrant species (Pseudonereis values were 50 and 85 µm. No clues (enlarged eyes, anomala), which have the Heteronereis stage and are able modified parapodia, and swimming chaetae) of epitokal to swarm in the open sea. However, Rouabah and Scaps modifications were observed on the specimens. (2003) found a dense population of Perinereis cultrifera Dissection of the digestive tracts of Pseudonereis off the coast of Algeria reproducing exclusively by epitoky. anomala specimens collected in ‹skenderun Bay revealed Çinar and Ergen (2005) postulated that P. anomala has a that they largely consumed algae and detritus. Pieces of potential to compete with other native species for space algae, such as Padina pavonica, Cystoseira sp., and Jania and food. However, the functioning role of this species in rubens, were identified among the material gathered benthic communities along the Mediterranean coast and its from the digestive tracts of the specimens. In addition, impact on the native fauna is largely unknown. some filamentous algae and sand were also found. No Pseudonereis anomala was previously found in a residue of was identified in the digestive tracts of variety of shallow water benthic habitats (0-4 m), such as the dissected specimens. corals, rocks, algae, , and sand (Fishelson and Rullier, 1969; Wu et al., 1985; Ergen and Çinar, 1997; Discussion Çinar and Ergen, 2005). Ben-Eliahu (1991) regarded this species as an ecological generalist, a character suitable for In contrast to the alien serpulid species in the successful migrant species. Although P. anomala was Mediterranean, which have a negative economic impact, previously reported from undisturbed environmental as they foul artificial substrates, such as docks, ship hulls, conditions, Çinar and Ergen (2005) encountered it on the and sea-water intake pipes, alien nereidid species, such as mussel Mytilus galloprovincialis (Lamarck, 1819) in polluted harbors in the . The occurrence of 80 this species in polluted waters was also confirmed by 70 60 Kambouroglou and Nicolaidou (2006) off the coast of 50 . This shows that it has a wide ecological valance 40 y = 19.05Ln(x) + 6.65 that enables it to gradually extend its distributional range 30 R2 = 0.92, r = 0.92, P < 0.05 20 n = 93 from the eastern to the western Mediterranean. 10 Number of chaetigers 0 The population of Pseudonereis anomala in 010203051525 ‹skenderun Bay was mainly composed of juveniles, Body length (mm) 3 indicating that the reproduction period of the species y = 0.0847x + 0.1072 2.5 R2 = 0.91, r = 0.95, P < 0.05 took place in mid- or late summer. Only one specimen n = 93 2 carried immature oocytes (oocyte diameter: 50-85 µm), 1.5 without epitokal modifications. The diameter of mature 1 oocytes in specimens with epitokal modification may 0.5 Body width (mm) reach 195 µm (Çinar and Ergen, 2005). 0 010203051525 The maximum body length (27.3 mm) of Body length (mm) Pseudonereis anomala found in ‹skenderun Bay was Figure 7. The length-number of chaetigers and length-width smaller than that of populations found in the relationships of Pseudonereis anomala. (65 mm) (Fauvel, 1953; Day, 1967), Red Sea (45 mm)

408 M. E. ÇINAR, C. ALTUN

(Fishelson and Rullier, 1969), and the Aegean Sea (51 factors affecting species diversity and density (Fishelson mm) (Çinar and Ergen, 2005). However, the sampling and Haran, 1986/87; Çinar, 2003). period of the present study took place soon after the The body length-weight relationship of the reproduction of this species in ‹skenderun Bay (according Pseudonereis anomala specimens may be indicative of to the number of juveniles in samples) and the largest allometric growth; however, the b value (2.95) in the specimens might have died after reproducing. Therefore, the body size of the species in ‹skenderun Bay might be regression equation calculated between the body width larger than what we measured. Ben-Eliahu (1989) found and weight of specimens of the species suggests isometric that large Mediterranean individuals of P. anomala living growth. This finding suggests that the width of the on a Dendropoma habitat off the Israeli coast were larger anterior segments increases proportionally to increasing than the largest specimens of this species in a similar body weight, but the length of worms, increasing by habitat in the Red Sea. The difference in body sizes adding new segments to the posterior part, represents an between the populations was thought to be, most allometric relationship with body weight. A similar finding probably, due to the colder Mediterranean temperature, was also noted by Omena and Amaral (2001), who found the local stability of the Mediterranean Dendropoma reef, that the allometric coefficient obtained from the length of or a combination of these and other reasons (Ben-Eliahu, the prostomium to chaetiger 13 showed a close value 1989). from an isometric growth (2.91). They explained that the Data concerning the population density and biomass length of the anterior part of the worm increases of Pseudonereis anomala are scarce. The population isometrically as the anterior region lengthens in density of this species is reported to be 47 ind. m-2 on proportion to weight and that this part of the body is Dendropoma reefs along the Mediterranean coast of more important in the worm’s total weight than the Israel and 15 ind. m-2 in a similar habitat of the Red Sea posterior part. Allometric growth was also previously (Ben-Eliahu, 1989). Çinar and Ergen (1995) reported the determined in the nereidid Laeonereis acuta (Treadwell, maximum density and biomass scores of P. anomala in 1923; Omena and Amaral, 2001) and the tube worm ‹zmir Bay as 100 ind. m-2 and 4.08 g m-2. In ‹skenderun Diopatra neapolitana Delle Chiaje, 1841 (Dagli et al., Bay, the maximum density and biomass values of P. 2005). -2 anomala were 2475 ind. m (on Jania rubens at station The present study provides information about the -2 1, mostly juvenile) and 7.85 g m (on Brachidontes population characteristics of Pseudonereis anomala found pharonis at station 5). The highest mean density values of in ‹skenderun Bay in September 2005. Future studies to P. anomala were encountered on the mussel B. pharonis be undertaken on the population structure and biology of and the brown alga Cystoseira sp. in ‹skenderun Bay. this Lessepsian species throughout the year will shed These habitats seem to have more complex structures for more light on its life history and functional role in the species settlement than others (J. rubens, Ulva sp., and invaded ecosystem. Padina pavonica) sampled. Brachidontes pharonis forms dense populations on rocky substrates in the area and sediments trapped among shells and byssuses could Acknowledgments provide more micro-habitats for the species. The thallus We are obliged to our colleagues at the Department of of Cystoseira sp. is more branched and larger than the Hydrobiology, Ege University, for their help in collecting other alga sampled, and so it could accumulate more and sorting the benthic materials and to 2 anonymous sediment and thereby provide more food for species referees for critically reading the manuscript. This work populations. The thallus structure and availability of was financially supported by TÜB‹TAK (Project Number: nourishment on the host plant were reported to be major 104Y065, coordinated by M.E. Çınar).

409 A Preliminary Study on the Population Characteristics of the Lessepsian Species Pseudonereis anomala (Polychaeta: Nereididae) in ‹skenderun Bay (Levantine Sea, Eastern Mediterranean)

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