Open Access

Early detection of potentially invasive invertebrate species in Mytilus galloprovincialis Lamarck, 1819 dominated communities in harbours

  • Cristina Preda1,
  • Daniyar Memedemin1,
  • Marius Skolka1Email author and
  • Dan Cogălniceanu1
Helgoland Marine Research201266:290

Received: 23 August 2011

Accepted: 7 January 2012

Published: 19 January 2012


Constanţa harbour is a major port on the western coast of the semi-enclosed Black Sea. Its brackish waters and low species richness make it vulnerable to invasions. The intensive maritime traffic through Constanţa harbour facilitates the arrival of alien species. We investigated the species composition of the mussel beds on vertical artificial concrete substrate inside the harbour. We selected this habitat for study because it is frequently affected by fluctuating levels of temperature, salinity and dissolved oxygen, and by accidental pollution episodes. The shallow communities inhabiting it are thus unstable and often restructured, prone to accept alien species. Monthly samples were collected from three locations from the upper layer of hard artificial substrata (maximum depth 2 m) during two consecutive years. Ten alien macro-invertebrate species were inventoried, representing 13.5% of the total number of species. Two of these alien species were sampled starting the end of summer 2010, following a period of high temperatures that triggered hypoxia, causing mass mortalities of benthic organisms. Based on the species accumulation curve, we estimated that we have detected all benthic alien species on artificial substrate from Constanţa harbour, but additional effort is required to detect all the native species. Our results suggest that monitoring of benthic communities at small depths in harbours is a simple and useful tool in early detection of potentially invasive alien species. The selected habitat is easily accessible, the method is low-cost, and the samples represent reliable indicators of alien species establishment.


Constanţa harbour Black Sea Invertebrates Alien species Recolonization Monitoring


Globalization and increasing trade lead to a higher rate of transfer of organisms around the world, some of which may have significant ecological or economical impact in the recipient area. Monitoring is a valuable tool that provides the opportunity to detect early potential crises such as biological invasions (Elzinga et al. 2001). Species accumulation theory offers information on the required sampling effort to detect the species from a studied area and is useful for testing various biodiversity sampling approaches (Gotelli and Colwell 2001). Species richness increases rapidly as more samples are collected due to the presence of common species, but this increase slows down as rare species are added (Bunge and Fitzpatrick 1993). Thus, the probability of detecting alien species including rare ones can be computed (Chao et al. 2009) and can be an effective measure of testing the efficiency of early detection systems.

As many other seas, the Black Sea is severely affected by anthropogenic changes (Leppäkoski and Mihnea 1996), biological invasions being one of the most important (Gomoiu et al. 2002; Paavola et al. 2005). The number of alien species inventoried in the Black Sea is continuously rising (e.g., Aleksandrov 2010; Alexandrov and Zaitsev 2000; Leppäkoski et al. 2002; Skolka and Gomoiu 2004). For example, Zaitsev and Öztürk (2001) reported 59 alien species in the Black Sea, but recent efforts of updating the status of European marine alien species increased the number to 184 including established, casual and cryptogenic species (Zenetos et al. 2009). We use the term ‘alien’ according to Richardson et al. (2000) to describe taxa present in an area outside their historical native range, following human-mediated introduction.

The benthic hard substrate has usually a complex structure and high species richness. The dominant species in the Black Sea is the mussel (Mytilus galloprovincialis Lamarck, 1819), which provides a secondary substrate for sessile species as well as appropriate conditions for many vagile species. Organisms living in the north-western part of the Black Sea are constantly subjected to environmental stressors (e.g., variable freshwater inflow from the Danube, fluctuating temperatures and oxygen levels) that cause mass mortality of shallow benthic communities followed by rapid recolonization.

In marine and brackish water environments, shipping is considered the main vector of alien species introductions (Reise et al. 1999). Constanţa harbour is the major Romanian transit hub providing connections between Central and Eastern Europe, Caucasus and Central Asia. Previous studies of the benthic communities on mobile substrate and planktonic associations inside Constanţa harbour showed that these are species poor, with a simplified structure composed of few resistant and/or opportunistic species (Petran 1984; Ţigănuş 1982).

Considering the great importance of shipping as a vector of alien species, monitoring programmes developed within the harbour are essential, since usually harbours have impoverished communities of organisms and are more prone to invasions (Galil 2000). We hypothesized that the benthic community on the harbours hard substrate would be unstable and has low species richness. The aim of our study was (1) to investigate the species composition of the shallow mussel beds inside the Constanţa harbour and the proportion of alien species and (2) to test the usefulness of the method in the early detection of newly established alien species.

Materials and methods

Study site

Located on the western coast of the Black Sea, Constanţa harbour (44°09′N 28°39′E) is situated at a distance of 157 km from the Danube (Sulina Branch) and 331 km from the Bosphorus Strait. Placed at the crossing of two Pan-European transport corridors, Constanţa harbour is among the first ten major European harbours. It has 140 functional berths and a handling capacity of over 100 million tons per year (Administration of Constanţa Port 2007). We selected three sampling sites from the entrance of Constanţa North harbour (Site 1) towards the inner part of the harbour (Site 2 and Site 3) (Fig. 1; Table 1). We used a Garmin 60CSx receiver to locate the sampling sites and Garmin MapSource version 6.15.6 for mapping.
Fig. 1

Location of sampling sites in Constanţa harbour

Table 1

Characteristics of the selected sampling sites

Sampling site


Depth (m)


Vessel type

Number of monthly samples

Site 1

N 44.145701°

E 28.667786°


Oil trading berths



Site 2

N 44.160670°

E 28.658235°


Technical berths



Site 3

N 44.169762°

E 28.650945°


Cereals and general cargo

Bulk carriers



For a period of 25 months starting with December 2008, benthic communities were sampled monthly from hard substrate represented by vertical flat concrete structures. Samples were scraped from 0 to 2 m depths, weighing 1,500–2,000 g each. We chose the upper layer for this study because this area is dynamic, affected by extremely high (in summer) or low temperatures (in winter), occasional chemical pollution events (e.g., with hydrocarbons) and by oxygen deficiency. All these induce mass mortalities followed by recolonization. Each sample was stored in a plastic container, labelled and brought to the laboratory for washing and sieving (0.071 mm). Invertebrates were identified to the lowest taxonomic level possible using a Nikon SMZ645 stereomicroscope, based on the available field guides and monographs (e.g., Băcescu 1967; Cărăuşu et al. 1955; Grossu 1962; Marinov 1977; Morduhai-Boltovskoi 1968; Prenant and Bobin 1966). Nomenclature of species is in agreement with the World Register of Marine Species (Appeltans et al. 2011). Mussels M. galloprovincialis with shell lengths larger than 12 mm were measured individually with a digital calliper. Data on the physical and chemical properties of the seawater were provided by the National Institute for Marine Research and Development ‘Grigore Antipa’ in Constanţa.

Data analysis

Following identification, the species were classified in native and alien species, based on the available data in the literature regarding native ranges, historical and present distribution, pathways of introduction in the Black Sea. Nematodes and harpacticoides were not identified at species level and were not included in the following analyses. Polychaetes of the genus Polydora were considered a complex of sibling species and were referred to as ‘Polydora complex’. Seasons were established as periods of 3 months as follows: ‘winter’ (December–February), ‘spring’ (March–May), ‘summer’ (June–August) and ‘autumn’ (September–November).

The assumptions of normality were tested using Shapiro–Wilk test, and ANOVA was used to calculate the statistical significance of differences between samples. The relation between the monthly species richness and the average temperature was tested with Pearson’s product moment correlation coefficient. For tests and correlations, we rejected the null hypothesis if p ≤ 0.05. To estimate whether our inventory was complete, we computed species accumulation curves (SAC) using EstimateS 8.2 (Colwell 2009). Based on the presence–absence matrix, we computed five non-parametric incidence-based estimators of species richness using EstimateS 8.2 (Colwell 2009): ICE, Chao2, 1st and 2nd order jackknife estimators and the Bootstrap estimator.

The incidence-based coverage (ICE) estimator assumes that the detection probabilities vary among species (Eq. 1) (Chao and Shen 2009; Lee and Chao 1994). The Chao2 estimator (Eq. 2) uses the number of uniques (species detected in only one sample) and duplicates (species detected in only two samples) for the same purpose (Chao 1987).
$$ \begin{aligned} S_{\text{ice}} & = S_{\text{freq}} + \frac{{S_{{{ \inf }\,r}} }}{{C_{\text{ice}} }} + \frac{{Q_{1} }}{{C_{\text{ice}} }}\gamma_{\text{ice}}^{2} \quad {\text{where}} \\ \gamma_{\text{ice}}^{2} & = \max \left[ {\frac{{S_{\inf \,r} }}{{C_{\text{ice}} }}\frac{{m_{\inf \,r} }}{{\left( {m_{\inf \,r - 1} } \right)}}\frac{{\sum\nolimits_{j = 1}^{10} {j(j - 1)Q_{j} } }}{{\left( {N_{\inf \,r} } \right)^{2} }} - 1,0} \right] \\ \end{aligned} $$
$$ \hat{S}_{\text{Chao2}} = S_{\text{obs}} + \left( {\frac{m - 1}{m}} \right)\left( {\frac{{Q_{1} \left( {Q_{1} - 1} \right)}}{{2\left( {Q_{2} + 1} \right)}}} \right) $$
The frequency of uniques is used by 1st order jackknife estimator (Eq. 3), while the 2nd order jackknife (Eq. 4) uses the frequency of uniques and duplicates to estimate the number of undetected species (Burnham and Overton 1978). The Bootstrap (Eq. 5) is a reliable method related to the jackknife and has a wider applicability (Smith and van Belle 1984).
$$ S_{{{\text{jack}}1}} = S_{\text{obs}} + Q_{1} \left( {\frac{m - 1}{m}} \right) $$
$$ S_{{{\text{jack}}2}} = S_{\text{obs}} + \left[ {\frac{{Q_{1} (2m - 3)}}{m} - \frac{{Q_{2} (m - 2)^{2} }}{m(m - 1)}} \right] $$
$$ S_{\text{boot}} = S_{\text{obs}} + \sum\limits_{k = 1}^{{S_{\text{obs}} }} {\left( {1 - p_{k} } \right)^{m} } $$
The variables used are defined as follows: S estimated species richness, S obs observed species richness, Q j number of species that are observed in exactly j samples, m number of samples, C ice sample incidence coverage estimator, \( \gamma_{\text{ice}}^{2} \) estimated coefficient of variation of the Q i for infrequent species, p k proportion of samples that contain species k.

The sampling effort for the detection of the total number of species (or a determined percentage of the estimated species richness) was calculated using the non-parametric method proposed by Chao et al. (2009).


We identified 74 species belonging to 15 taxonomic groups in the 70 samples collected from the harbour. Amphipod crustaceans and polychaets were the groups with the highest number of species (a list of species is provided in ‘Appendix’—Table 5). We also inventoried 10 alien species from seven higher taxa (Fig. 2). The investigated sites differed in species richness and composition, the highest number of species being registered at Site 1 (Table 2).
Fig. 2

Taxonomic groups and species (native and alien) identified in the samples from sampling sites

Table 2

Species richness and composition for the investigated sites

Sampling site

Site 1

Site 2

Site 3

No. of observed species




No. of higher taxa




Monthly average no. and standard deviation of species

24 ± 5.7

20 ± 5.1

21 ± 4.9

Month of highest observed species richness

January 2009

November 2009

December 2009

Month of lowest observed species richness

April 2009, June 2009, March 2010

July 2010

July 2010

Taxonomic groups with high number of species

Amphipoda (19%)

Polychaeta (19%)

Coelenterata (12%)

Decapoda (10%)

Polychaeta (21%)

Amphipoda (14%)

Coelenterata (12%)

Decapoda (10%)

Polychaeta (19%)

Amphipoda (18%)

Decapoda (11%)

Coelenterata (11%)

Regarding the seasonal dynamics, the highest number of species per sample was recorded in the cold season and the lowest species richness was registered in summer 2010 (Fig. 3). One-way ANOVA detected significant differences between seasons (F3,66 = 7.74, p < 0.001). Holm-Sidak multiple pairwise comparison indicated that the number of species detected in winter was significantly higher than in summer (t = 4.64, p < 0.001), spring (t = 3.47, p < 0.001) or autumn (t = 2.78, p = 0.007) (Fig. 3). A negative correlation was observed between the average temperature and species richness recorded monthly (r = −0.459, p = 0.021).
Fig. 3

Seasonal variation of species richness in the harbour

Of the ten alien macro-invertebrate species identified in the harbour, eight were present in all sites: Diadumene lineata (Verrill, 1869), Ficopomatus enigmaticus (Fauvel, 1923), Corambe obscura (Verrill, 1870), Rhithropanopeus harrisii (Gould, 1841), Balanus improvisus Darwin, 1854, Anadara sp., Mya arenaria Linnaeus, 1758 and Molgula manhattensis (De Kay, 1843). The hydrozoan Blackfordia virginica Mayer, 1910 was present at the harbour entrance (Site 1) only in December, while the barnacle Balanus amphitrite Darwin, 1854 was encountered inside the harbour only at Site 3 in December 2010.

Diadumene lineata was present both on natural and artificial hard substrata including mussels’ valves, sometimes in large numbers. In general, the abundance of D. lineata individuals exceeded that of native sea anemones like Actinia equina (Linnaeus, 1758) or Actinothoe clavata (Ilmoni, 1830). The presence of F. enigmaticus was limited to single individuals or groups of maximum 15 specimens living on mussels’ shells. C. obscura was present only during the cold season. R. harrisii was collected in most samples (89%) and had a higher relative abundance than the combined number of individuals of native brachyuran decapods. The barnacle B. improvisus was a dominant species in the harbour together with the native species of bivalves M. galloprovincialis and Mytilaster lineatus (Gmelin, 1791). Several juveniles of M. arenaria were observed in 10% of the samples collected. M. manhattensis was found mostly as single individuals inside the harbour at Sites 2 and 3 (in 12 samples) and less at the harbour entrance (in two samples). The majority (98%) of Anadara sp. individuals were sampled at Site 1 starting September 2010 (the rest of 2% was divided between S2 and S3) after a hot summer (27°C average air temperature between June and August 2010). The size distribution of the mussels sampled from the harbour varied seasonally (Fig. 4). During the autumn and winter of 2010, the percentage of mussels with shell lengths greater than 51 mm was lower compared to 2009. B. improvisus, R. harrisii and F. enigmaticus are the alien species easiest to detect in the harbour, with a probability of more than 80% as shown in Table 3. The proportion of alien species was similar for the three sites: 13.4% for Site 1, 13.8% for Site 2 and 15.8% for Site 3.
Fig. 4

Size distribution of mussels (M. galloprovincialis) sampled from Constanţa harbour: a spring, n = 3,213 in 2009, n = 2,345 in 2010; b summer, n = 4,626 in 2009, n = 1,411 in 2010; c autumn, n = 3,305 in 2009, n = 510 in 2010; and d winter, n = 2,956 in 2009–2010, n = 130 in 2010–2011

Table 3

Frequency of occurrence of benthic alien species within Constanta harbour monitoring network (%)


Site 1

n = 25

Site 2

n = 24

Site 3

n = 21


n = 70

Balanus improvisus





Rhithropanopeus harrisii





Ficopomatus enigmaticus





Corambe obscura





Diadumene lineata





Molgula manhattensis





Anadara sp.





Mya arenaria





Blackfordia virginica





Balanus amphitrite





The species accumulation curves have similar shapes for the three sampling sites but do not reach an asymptote (Fig. 5). The sampling effort required to detect 95% of the observed species richness is 51, while three samples are sufficient for the detection of 50% of the species (Fig. 6). Almost half of the species inventoried (~48%) were present in ten or less samples (out of 70) with 16% encountered in just one sample, suggesting a high species turnover. We then estimated the number of species using estimators of species richness (Table 4). The probability of a new alien species to be observed in the next sample is 0.0035, and the additional number of samples required to detect a new alien (S est) is 0. However, additional sampling effort is necessary for inventorying at least 90% of the total S est in the harbour (Table 4).
Fig. 5

Species accumulation curves (SAC) and 95% confidence interval (CI) for: a Site 1, b Site 2, c Site 3 (see Fig. 1) and d Constanţa harbour

Fig. 6

The estimated number of samples required to detect 50, 75 and 95% of the observed species richness (S obs) in the harbour

Table 4

Estimated species richness (mean, standard error and 95% confidence interval) based on non-parametric estimators of species richness computed using EstimateS 8.2 (Colwell 2009)



Native species

Alien species

No. of observed species





90.3 ± 12.7


82.1 ± 14.9


10 ± 0.3



82.5 ± 0.01

72.2 ± 0.01

10.6 ± 0

1st order jackknife

85.8 ± 3.1

74.8 ± 3.0

11 ± 1

2nd order jackknife









Our monitoring system of benthic communities on hard artificial substrate at small depths proves useful in the early detection of potentially invasive alien species in harbours. On natural hard substrata the community of the stone mussels dominated by M. galloprovincialis has two components that are bathymetrically delimited and are characterized by specific assemblages of invertebrates (Băcescu et al. 1971). In the harbour area, these two components are combined and several species described as characteristic and abundant in natural areas are absent in the harbour. Instead, pollution resilient species are more common. The mussels M. galloprovincialis form a bed of 5–15-cm thickness providing interstitial space for other sessile organisms depending on their size. Overall, the mussels and the associated fauna in Constanţa harbour form a complex community, but the species richness is lower when compared with similar communities at the Romanian coast outside the harbour (Băcescu et al. 1971; Teacă et al. 2006a, b). The relationship between species richness and invasibility of a system is still widely debated (e.g., Borges et al. 2006; Herben et al. 2004; Kennedy et al. 2002; Levine and D’Antonio 1999). An efficient use of resources can contribute to the community’s resistance to the establishment of new alien species (Stachowicz et al. 1999). M. galloprovincialis, as the dominant species on the artificial substrate in the harbour, leaves little available space for the establishment of other sessile organisms.

At local scale, the invasibility of a given habitat is influenced by physical factors and the level of disturbance (Zaiko et al. 2007). At the Romanian coast of the Black Sea, the average salinity in 2010 was close to the minimum recorded during 1959–2010. The lowest salinity for the same year was observed in Constanţa area in July (10.09 PSU). Average sea water temperature was 13.6°C in 2009 and 14.1°C in 2010, close to the maximum value recorded between 1959 and 2010 at the Romanian coast. The highest value for Constanţa area in 2010 reached 29.8°C on 17th of August. The high surface water temperatures recorded during summer coupled to decaying organic matter produced by algal blooms and wastewater cause episodes of hypoxia that can affect even surface water. During the summers of 2009 and 2010, five hypoxia events were recorded in the water column. The lowest oxygen value (1.55 cm3/l) was registered in September 2010 at 20 m depth, in the southern part of the Romanian coast (Lazăr 2011). Inside Constanţa harbour at the end of July 2009, average values of salinity, temperature and dissolved oxygen at the surface were 12.1 PSU, 25°C and 14 mg/l, respectively. At the end of August 2010, average values of the parameters registered in the same locations inside the harbour were 13.8 PSU, 27.3°C and 9.4 mg/l (Lazăr 2011). High temperatures and low oxygen levels in summer led to changes in species composition and to significant differences between seasons.

These extreme events induce the mass mortality of shallow benthic communities and make the hard substrate available for recolonization by native and/or non-native species. The success of establishment of alien species is further facilitated in harbours by the constant flow of potential settlers. An optimal timing of arrival increases the chances of the alien species to become established. The occasional presence of alien species like Musculista senhousia (Benson in Cantor, 1842), Styela clava Herdman, 1881, Palaemon macrodactylus Rathbun, 1902, Hemigrapsus sanguineus (De Haan, 1835) and Dyspanopeus sayi (Smith, 1869) was recently recorded in other areas of the Romanian Black sea coast, including Constanţa South-Agigea and Midia Harbors, as well as Tomis and Eforie marinas (Micu and Micu 2004; Micu and Niţă 2009; Micu et al. 2010a, b). The percentage of alien species inventoried in the harbour was 13.5%, almost three times higher compared to other similar communities on natural and artificial hard substrata at the Romanian coast, outside the harbour. Cohen et al. (2005) conducted a rapid assessment survey for alien organisms in southern California and concluded that the number or proportion of alien/cryptogenic taxa is not significantly higher in harbour areas in comparison with non-harbour ones. However, we underline the importance of harbours as reservoirs for alien species, similar to other findings (e.g., Arenas et al. 2006; Ashton et al. 2006; Minchin 2007; Paavola et al. 2008).

The alien species identified in Constanţa harbour are euryhaline and tolerate wide ranges of salinity in their native areas. Most of them originate from the North Atlantic area while 30% are of Indo-Pacific origin or cosmopolite. With the exception of the nudibranch gastropod C. obscura, which is a preferential feeder on bryozoans and covered a previously empty niche, the other alien species observed are in the same trophic and functional groups as the native species (i.e., mainly suspension feeders). To understand their presence in Constanţa harbour, a brief description of these species is provided below.

The barnacle B. improvisus, one of the oldest documented introductions in the Black Sea, is a suspension feeder that facilitates the establishment success and development of the alga Enteromorpha intestinalis (L.) (Gomoiu and Skolka 1996; Kotta et al. 2006).

The anthozoan D. lineata originates in the north Pacific area. Its presence was mentioned from the Black Sea area since the 1960 under the name Aiptasiomorpha luciae (Verrill, 1898) (Băcescu et al. 1971). Due to its increased capacity to tolerate variable abiotic factors, D. lineata is a very widespread species.

Ficopomatus enigmaticus, a serpulid polychaete, was discovered in France and described by Fauvel (1922) who presumed it had arrived there on ships’ hulls. However, the origin of this species is still uncertain. In the Black Sea, F. enigmaticus was reported in the late 1920s (Annenkova 1929). F. enigmaticus tolerates a wide range of salinities (from 0 to ~55PSU) (Hill 1967), temperatures (0–35°C) and pH (4–9) (Bianchi 1981) and has the potential of building reef-like structures. The growth and spread of F. enigmaticus is dependent on environmental conditions, higher biomasses being reported in brackish waters (Schwindt et al. 2004). A F. enigmaticus-dominated community was reported from the Belona marina at the Romanian Black Sea coast (Micu and Micu 2004).

Corambe obscura is a small nudibranch gastropod of North Atlantic origin that most probably arrived in the Black Sea around 1980 by shipping (Roginskaya and Grintsov 1997). Observations performed at the Romanian coast showed a preference of the mollusk for feeding and depositing eggs on Conopeum seurati (Canu, 1928) colonies rather than Cryptosula pallasiana (Moll, 1803) (Gomoiu and Skolka 1997). It tolerates a wide range of temperatures and salinities, but experimental studies showed that C. obscura has a reduced resistance in hypoxic conditions (Sagasti et al. 2001).

The crab R. harrisii is present in the Black Sea region since the 1930s, probably arrived by shipping from the Netherlands (Makarov 1939). The species is highly adaptable, living in waters of various salinities (preferable below 15PSU), temperatures and substrates (Băcescu 1967).

A few years after its arrival in the Black Sea in the 1960s, M. arenaria became the dominant species in the soft sediment associations at the Romanian littoral exceeding in some areas 1,500 g/m2 (Gomoiu 1981; Gomoiu and Porumb 1969). The bivalve was reported from soft benthic sediments in the harbour, but only as small individuals, the estimated biomass being about 1 g/m2 (Pecheanu et al. 2002).

Molgula manhattensis, a solitary ascidian, is commonly found in benthic communities in harbours. The species is resistant to polluted waters and tolerates various salinities and temperatures (Lambert and Lambert 1998).

The hydrozoan Blackfordia virginica was mentioned from the Black Sea since 1925 (Valkanov 1936). Even though Mills and Sommers (1995) consider the species native to the Black Sea, we consider it of North Atlantic origin similar to Zaitsev and Mamaev (1997) and Shiganova et al. (2005).

The striped barnacle, B. amphitrite, a widespread species found also in brackish waters, is a typical component of the fouling communities. The species is tolerant to pollution and other physical stress, being quite abundant in some harbours; for example, in Oostende B. amphitrite outcompetes B. improvisus (Kerckhof and Cattrijsse 2001).

Starting with September 2010, more than 900 specimens of Anadara sp. were sampled. It is possible to be A. transversa (Say, 1822) (syn. A. demiri Piani, 1981), a bivalve recorded for the first time in the Mediterranean basin in Izmir harbour in the 1970s (Demir 1977). Our identification was based on morphological traits but due to the fact that only immature individuals were sampled so far, further investigations are necessary. The presence of Anadara sp. in our samples corresponded with a sharp decrease in abundance of M. galloprovincialis adults (Fig. 4). Juveniles of M. galloprovincialis are more resistant to thermic shock, but temperatures of 30°C are lethal for the adults (Mirza and Crăciun 1989). The juveniles of Anadara sp. were interspersed between B. improvisus shells, M. lineatus and M. galloprovincials valves. By reducing the surface occupied by dominant native species, high temperatures and low levels of dissolved oxygen facilitate in some cases the establishment and spread of aliens.

The species accumulation curves for the sampling sites do not reach a plateau suggesting that more species will be inventoried with increasing sampling effort. We anticipate that the increase in the species richness from additional sampling will be mostly due to natives since the estimated number of alien species is close to the observed one.

The situation of alien species in the harbours of the Black Sea is poorly known. Investigations carried out in Odessa harbour (Ukraine) emphasized the need for baseline standardized surveys in the Black Sea harbours (Alexandrov et al. 2004). Increased attention is given to ballast water as vector for alien species, but fouling on ship’s hulls should not be neglected either. Information on species presence and abundance in harbours can improve predictions of invasion pathways and contribute to ranking of different vectors based on their importance. These aspects are equally important for the Black Sea basin, both as recipient and as donor region. Early detection of potentially invasive species is necessary for applying control/eradication measures and for testing the efficiency of such actions.


Given the fact that Constanţa harbour is a major transit hub, we investigated the structure of the benthic community on hard artificial substrate. The habitat selected for this study is dynamic and periodically subjected to extreme environmental conditions that destroy shallow benthic communities, leading to frequent recolonizations. Our results show that these communities are impoverished and unstable. As harbours are constant recipients of alien species, a good timing of arrival of these species increases the chances of establishment. Monitoring of benthic communities at small depths in harbours proved useful in the early detection of potentially invasive alien species. The selected habitat is easily accessible; the method is low-cost, and the samples represent reliable indicators of alien species establishment. We recommend it as a routine monitoring technique for harbours with a high transit.




The present study was funded by Consiliul Naţional al Cercetării Ştiinţifice din Învăţământul Superior (CNCSIS) PN II-IDEI 273/2007 and Centrul Naţional de Management de Programe (CNMP) PN II 32107/2008 grants. Access in the harbour enclosure was possible with the permission of Constanţa Port Administration. We thank Teodora Maria Onciu, Gabriela Mihaela Paraschiv, Tatiana Begun, Mihaela Mureşan, Florina Stănescu, Adrian Teacă, Gabriel Bănică, Marian Tudor and Răzvan Popescu-Mirceni for their help with sampling and species identification. We are grateful to Luminiţa Lazăr and Dan Vasiliu for the chemical and physical data supplied. We thank Erkki Leppäkoski, Laurenţiu Rozylowicz and the anonymous reviewers for their helpful suggestions that contributed to the improvement of the manuscript.

Authors’ Affiliations

Faculty of Natural and Agricultural Sciences, Ovidius University of Constanţa


  1. Administration of Constanţa Port (2007) Constanţa Port Handbook 07–08. Textimage, ConstanţaGoogle Scholar
  2. Aleksandrov BC (2010) Modern tendencies of the Black Sea Biological Pollution. Naukovi zaniski Ser Biol 3(44):3–5Google Scholar
  3. Alexandrov B, Zaitsev Y (2000) Chronicle of exotic species introduction into the Black Sea. In: The Black Sea ecological problems: collected papers/SCSEIO. SCSEIO, Odessa, pp 14–19Google Scholar
  4. Alexandrov B, Bashtannyy R, Clarke C, Hayes T, Hilliard R, Polglaze J, Rabotnyov V, Raaymakers S (2004) Ballast Water Risk Assessment, Port of Odessa, Ukraine, October 2003: Final Report. GloBallast Monograph Series No.10. IMO LondonGoogle Scholar
  5. Annenkova NP (1929) Polychaete from relic Paleostomi Lake (the Caucasus) and the rivers connected with it. Dokl AN SSSR 6:138–140 (in Russian)Google Scholar
  6. Appeltans W, Bouchet P, Boxshall GA, Fauchald K, Gordon DP, Hoeksema BW, Poore GCB, van Soest RWM, Stöhr S, Walter TC, Costello MJ (eds) (2011) World register of marine species. Accessed on 20 Apr 2011
  7. Arenas F, Bishop JDD, Carlton JT, Dyrynda PJ, Farnham WF, Gonzalez DJ, Jacobs MW, Lambert C, Lambert G, Nielsen SE, Pederson JA, Porter JS, Ward S, Wood CA (2006) Alien species and other notable records from a rapid assessment survey of marinas on the south coast of England. J Mar Biol Assoc UK 86(06):1329–1337. doi: View ArticleGoogle Scholar
  8. Ashton G, Boos K, Shucksmith R, Cook E (2006) Rapid assessment of the distribution of marine non-native species in marinas in Scotland. Aquat Invasions 1(4):209–213. doi: View ArticleGoogle Scholar
  9. Băcescu MC (1967) Fauna Republicii Socialiste România Crustacea Decapoda. Vol IV(9). Editura Academiei RSR, BucureştiGoogle Scholar
  10. Băcescu MC, Müller GI, Gomoiu MT (1971) Ecologie marină vol. IV Cercetări de ecologie bentală în Marea Neagră—Analiza cantitativă, calitativă şi comparată a faunei bentale pontice. Editura Academiei RSR, BucureştiGoogle Scholar
  11. Bianchi CN (1981) Policheti serpuloidei. In: Sacchi CF (ed) Guida per il riconoscimento delle specie animali delle acque lagunari e costiere italiane. Consiglio Nazionale delle Ricerche Genova AQ/1/96 5, pp 187Google Scholar
  12. Borges PAV, Lobo JM, de Azevedo EB, Gaspar CS, Melo C, Nunes LV (2006) Invasibility and species richness of island endemic arthropods: a general model of endemic vs. exotic species. J Biogeogr 33:169–187. doi: View ArticleGoogle Scholar
  13. Bunge J, Fitzpatrick M (1993) Estimating the number of species: a review. J Am Stat Assoc 88(421):364–373View ArticleGoogle Scholar
  14. Burnham KP, Overton WS (1978) Estimation of the size of a closed population when capture probabilities vary among animals. Biometrika 65:625–633View ArticleGoogle Scholar
  15. Cărăuşu S, Dobreanu E, Manolache C (1955) Fauna României Crustacea Amphipoda Vol IV(4). Editura Academiei, BucureştiGoogle Scholar
  16. Chao A (1987) Estimating the population size for capture-recapture data with unequal catchability. Biometrics 43:783–791PubMedView ArticleGoogle Scholar
  17. Chao A, Shen TJ (2009) Program SPADE (Species Prediction And Diversity Estimation). Program and user’s guide published at Accessed 18 Mar 2011
  18. Chao A, Colwell RK, Lin CW, Gotelli NJ (2009) Sufficient sampling for asymptotic minimum species richness estimators. Ecology 90(4):1125–1133PubMedView ArticleGoogle Scholar
  19. Cohen AN, Harris LH, Bingham BL, Carlton JT, Chapman JW, Lambert CC, Lambert G, Ljubenkov JC, Murray SN, Rao LC, Reardon K, Schwindt E (2005) Rapid assessment survey for exotic organisms in southern California bays and harbors, and abundance in port and non-port areas. Biol Invasions 7:995–1002. doi: View ArticleGoogle Scholar
  20. Colwell RK (2009) EstimateS: statistical estimation of species richness and shared species from samples. Version 8.2 user’s guide and application. Accessed 18 Mar 2011
  21. Demir M (1977) On the presence of Arca (Scapharca) amygdalum Philippi, 1847 (Mollusca: Bivalvia) in the harbour of Izmir, Turkey. Ist Univ Fen Fak Mec Ser B 42:197–202Google Scholar
  22. Elzinga CL, Salzer DW, Willoughby JW, Gibbs JP (2001) Monitoring plant and animal populations. Blackwell Science, New YorkGoogle Scholar
  23. Fauvel P (1922) Un nouveau serpulien d’eau saumatre Mercierella n.g. enigmatica n. sp. Bull Soc Zool France 47:424–430Google Scholar
  24. Galil BS (2000) A sea under siege—alien species in the Mediterranean. Biol Invasions 2:177–186View ArticleGoogle Scholar
  25. Gomoiu MT (1981) Distribution of Mya arenaria L. populations in the western part of the Black Sea. Cerc mar-Rech mar IRCM 14:145–158Google Scholar
  26. Gomoiu MT, Porumb F (1969) Mya arenaria L.—bivalve recently penetrated into the Black Sea. Rev Roum Biol Sér Zool 14(3):199–202Google Scholar
  27. Gomoiu MT, Skolka M (1996) Changements récents dans la biodiversité de la mer Noire dus aux immigrants. GeoEcoMarina 1:34–48Google Scholar
  28. Gomoiu MT, Skolka M (1997) A new gastropod opisthobranch at the Romanian Black Sea coast. GeoEcoMarina 2:201–205Google Scholar
  29. Gomoiu MT, Alexandrov B, Shadrin N, Zaitsev Y (2002) The Black Sea—a recipient, donor and transit area for alien species. In: Leppäkoski E, Gollasch S, Olenin S (eds) Invasive aquatic species of Europe. Distribution, impacts and management. Kluwer, Dordrecht, pp 341–350Google Scholar
  30. Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4(4):379–391. doi: View ArticleGoogle Scholar
  31. Grossu AV (1962) Fauna României-Bivalvia Vol III(3). Editura Academiei, BucureştiGoogle Scholar
  32. Herben T, Mandák B, Bímová K, Münzbergová Z (2004) Invasibility and species richness of a community: a neutral model and a survey of published data. Ecology 85(12):3223–3233. doi: View ArticleGoogle Scholar
  33. Hill MB (1967) The Life Cycles and Salinity Tolerance of the Serpulids Mercierella enigmatica Fauvel and Hydroides uncinata (Philippi) at Lagos. Niger J Anim Ecol 36(2):303–321View ArticleGoogle Scholar
  34. Kennedy TA, Naeem S, Howe KM, Knops JMH, Tilman D, Reich P (2002) Biodiversity as a barrier to ecological invasion. Nature 417:636–638. doi: PubMedView ArticleGoogle Scholar
  35. Kerckhof F, Cattrijsse A (2001) Exotic Cirripedia (Balanomorpha) from Buoys off the Belgian Coast. Senckenbergiana marit 31(2):245–254View ArticleGoogle Scholar
  36. Kotta J, Kotta I, Simm M, Lankov A, Lauringson V, Põllumäe A, Ojaveer H (2006) Ecological consequences of biological invasions: three invertebrate case studies in the north-eastern Baltic Sea. Helgol Mar Res 60:106–112. doi: View ArticleGoogle Scholar
  37. Lambert CC, Lambert G (1998) Non-indigenous ascidians in southern California harbors and marinas. Mar Biol 130(4):675–688. doi: View ArticleGoogle Scholar
  38. Lazăr L (2011) Contributions to the knowledge and evaluation of the eutrophication phenomenon in the marine coastal waters of Romania. Unpubl. PhD Thesis, Ovidius University of Constanta (in Romanian)Google Scholar
  39. Lee SM, Chao A (1994) Estimating population size via sample coverage for closed capture-recapture models. Biometrics 50:88–97PubMedView ArticleGoogle Scholar
  40. Leppäkoski E, Mihnea PE (1996) Enclosed seas under man-induced change: a comparison between the Baltic and Black Seas. Ambio 25(6):380–389Google Scholar
  41. Leppäkoski E, Gollasch S, Olenin S (eds) (2002) Invasive aquatic species of Europe. Distribution, impacts and management. Kluwer, DordrechtGoogle Scholar
  42. Levine JM, D’Antonio CM (1999) Elton revisited: a review of evidence linking diversity and invasibility. Oikos 87:15–26View ArticleGoogle Scholar
  43. Makarov AK (1939) About some new elements in the fauna of the Black Sea estuaries in connection with shipping. DAN URSS 23(8):818–821 (in Russian)Google Scholar
  44. Marinov T (1977) Fauna Bulgarica 6—Polychaeta. In aedibus Academiae Scientiarium Bulgaricae, Sofia (in Bulgarian)Google Scholar
  45. Micu D, Micu S (2004) A new type of macrozoobenthic community from the rocky bottoms of the Black Sea. In: Öztürk B, Mokievsky VO, Topaloğlu B (eds) International workshop on the Black Sea Benthos, 18–23 April 2004. Istanbul, pp 75–87Google Scholar
  46. Micu D, Niţă V (2009) First record of the Asian prawn Palaemon macrodactylus Rathbun, 1902 (Caridea: Palaemonoidea: Palaemonidae) from the Black Sea. Aquat Invasions 4(4):597–604. doi: View ArticleGoogle Scholar
  47. Micu D, Niţă V, Todorova V (2010a) First record of the Japanese shore crab Hemigrapsus sanguineus (de Haan, 1835) (Brachyura: Grapsoidea: Varunidae) from the Black Sea. Aquat Invasions 5(1):S1–S4. doi: View ArticleGoogle Scholar
  48. Micu D, Niţă V, Todorova V (2010b) First record of Say’s mud crab Dyspanopeus sayi (Brachyura: Xanthoidea: Panopeidae) from the Black Sea. Mar Biodivers Rec 3:e36. doi: View ArticleGoogle Scholar
  49. Mills CE, Sommers F (1995) Invertebrate introductions in marine habitats: two species of hydromedusae (Cnidaria) native to the Black Sea, Maeotias inexspectata and Blackfordia virginica, invade San Francisco Bay. Mar Biol 122:279–288. doi: Google Scholar
  50. Minchin D (2007) Rapid coastal survey for targeted alien species associated with floating pontoons in Ireland. Aquat Invasions 2(1):63–70. doi: View ArticleGoogle Scholar
  51. Mirza M, Crăciun C (1989) Biochemical and cellular responses of Mytilus galloprovincialis Lmk. to temperature stress. Cerc mar-Rech mar IRCM 22:279–288Google Scholar
  52. Morduhai-Boltovskoi FM (ed) (1968) Opredeliteli Fauna Cernogo i Azovskovo Morei vol I. Nauk, Dumka Kiev (in Russian)Google Scholar
  53. Paavola M, Olenin S, Leppäkoski E (2005) Are invasive species most successful in habitats of low native species richness across European brackish water seas? Estuar Coast Shelf Sci 64:738–750. doi: View ArticleGoogle Scholar
  54. Paavola M, Laine AO, Helavuori M, Kraufvelin P (2008) Profiling four brackish-water harbours: zoobenthic composition and invasion status. Boreal Env Res 13(2):159–175Google Scholar
  55. Pecheanu I, Oros A, Piescu V, Stoica E, Dumitrache C, Coatu V (2002) Taux des substances nuisibles pour le milieu marin dans les zones de dépôt des sédiments dragués du port Constanta. Cerc mar-Rech mar INCDM 34:183–196Google Scholar
  56. Petran A (1984) Sur la communauté zooplanctonique d’un milieu portuaire—l’aire portuaire de Constanţa (Mer Noire). Cerc mar-Rech mar IRCM 17:119–130Google Scholar
  57. Prenant M, Bobin G (1966) Faune de France 68. Bryozoaires, Imprimerie Barnéoud SA Laval, ParisGoogle Scholar
  58. Reise K, Gollasch S, Wolff WJ (1999) Introduced marine species of the North Sea coasts. Helgoländer Meeresunters 52:219–234Google Scholar
  59. Richardson DM, Pyšek P, Rejmánek M, Barbour MG, Panetta FD, West CJ (2000) Naturalization and invasion of alien plants: concepts and definitions. Divers Distrib 6:93–107View ArticleGoogle Scholar
  60. Roginskaya IS, Grintsov VA (1997) Range expansion of an alien invader—the nudibranch mollusk Doridella obscura Verrill, 1870 (Opisthobranchia: Corambidae) in the Black Sea. Veliger 40(2):160–164Google Scholar
  61. Sagasti A, Schaffner LC, Duffy JE (2001) Effects of periodic hypoxia on mortality, feeding and predation in an estuarine epifaunal community. J Exp Mar Biol Ecol 258:257–283PubMedView ArticleGoogle Scholar
  62. Schwindt E, De Francesco CG, Iribarne O (2004) Individual and reef growth of the invasive reef-building polychaete Ficopomatus enigmaticus in a south-western Atlantic coastal lagoon. J Mar Biol Assoc UK 84(3):987–993. doi: View ArticleGoogle Scholar
  63. Shiganova TA, Musaeva EI, Pautova LA, Bulgakova YV (2005) The problem of invaders in the Caspian Sea in the context of the findings of new zoo- and phytoplankton species from the Black Sea. Biol Bull 32(1):65–74. doi: View ArticleGoogle Scholar
  64. Skolka M, Gomoiu MT (2004) Invasive species in the Black Sea—ecological impact of new species intrusion in aquatic ecosystems. Ovidius University Press, Constanţa (in Romanian)Google Scholar
  65. Smith EP, van Belle G (1984) Nonparametric estimation of species richness. Biometrics 40:119–129View ArticleGoogle Scholar
  66. Stachowicz JJ, Whitlatch RB, Osman RW (1999) Species diversity and invasion resistance in a marine ecosystem. Science 286:1577–1579PubMedView ArticleGoogle Scholar
  67. Teacă A, Begun T, Gomoiu MT (2006a) Recent data on benthic populations from hard bottom mussel community in the Romanian Black Sea coastal zone. GeoEcoMarina 12:43–51Google Scholar
  68. Teacă A, Begun T, Gomoiu MT, Paraschiv GM (2006b) The present state of the epibiontic populations to the biocenosis of stone mussels in the shallow water off the Romanian Black Sea coast. GeoEcoMarina 12:53–66Google Scholar
  69. Ţigănuş V (1982) Données préliminaires sur le zoobenthos du substrat meuble de la zone portuaire Constanţa. Cerc mar-Rech mar IRCM 15:107–114Google Scholar
  70. Valkanov A (1936) Belezhki varkhu naskhite brakichny vody (Notes on our brackish waters). God Sofia Univ 32:1–133 (in Bulgarian)Google Scholar
  71. Zaiko A, Olenin S, Daunys D, Nalepa T (2007) Vulnerability of benthic habitats to the aquatic invasive species. Biol Invasions 9:703–714. doi: View ArticleGoogle Scholar
  72. Zaitsev Y, Mamaev V (1997) Biological diversity in the Black Sea: a study of change and decline. United Nations Publications, Black Sea Environmental Series, vol 3, New YorkGoogle Scholar
  73. Zaitsev Y, Öztürk B (2001) The Black Sea. In: Zaitsev Y, Öztürk B (eds) Exotic species in the Aegean, Marmara, Black, Azov and Caspian Seas. Turkish Marine Research Foundation, Istanbul, pp 73–138Google Scholar
  74. Zenetos A, Streftaris N, Micu D, Todorova V, Gollasch S, Joseffson M, Zaiko A, Olenin S (2009) Harmonisation of European Alien species databases: A 2009 update of Marine Alien Species towards the forthcoming SEBI2010 Report. In: Antunes C, Dias E, Morais P, Sousa R (eds) World conference on biological invasions and ecosystem functioning Porto (Portugal) 27–30 October 2009. Book of Abstracts, Candeias Artes Gráficas, Braga, pp 142Google Scholar


© Springer-Verlag and AWI 2012