Advances in Agricultural Science 05 (2017), 04: 01-12
Abundance and Biomass of the invasive copepod, Acartia tonsa Dana, 1849 around the fish cage culture in the southern Caspian Sea (Mazandaran-Kelarabad), Iran
A. Afraei Bandpei 1*, M. Rowshan Tabari 1, M. El-Sayed Abdel-Fatah 2, N. Khodaparast 1, H. Nasrolahzadeh 1
1Caspian Sea Ecology Research Center, Iranian Fisheries Science Research Institute, Agricultural Research, Education and Extension Organization (AREEO), Sari, Iran.2Oceanography Department, Faculty of Science, Alexandria University, Alexandria, Egypt.
The abundance and biomass of the invasive copepod, Acartia tonsa around the fish cage culture stations in the southern Caspian Sea were investigated in 2012. Sampling was conducted on a seasonally basis and at 3 stations. Station 1 at the site of the cage, station 2 at a distance of 500 meters in the west as the site of the cage control station and station 3 was chosen within 50 meters east of the location. The goal of this study was to examine the abundance and biomass of Acartia tonsa in the location of fish cages and comparison with the control station. A sample of 18083 specimens was collected. The abundance and biomass of different life stages of A. tonsa at different sites of fish cage culture were analysed. The results revealed that significant differences between abundance and biomass of A. tonsa in different life stages (p<0.05). The mean abundance and biomass were 142.38±14.83 individuals m-3 and 1.45±0.27 mg m-3, respectively. These stages of copepodite and nauplii represent 62.2% and 37.8% of total population, respectively. The minimum abundance and biomass frequency of A. tonsa was recorded in summer compared to other seasons. The results showed that abundance and biomass of nauplii were more than the copepodite; with an average of 108.8±15.6 individuals m-3 and 1.79±0.7 mg m-3 for copepodite and 213.8±189.8 individuals m-3 and 0.5±0.6 mg m-3 for nauplii. In conclusion, the abundance and biomass of calanoid copepod, A. tonsa at station 1 and station 3 were far more than the control station. These findings suggest that the accumulation of nutrients at cage sites increased available foods, leading to flourishing of A. tonsa.
Acartia tonsa is a Calanoid copepod species that can be found in a large portion of the world’s estuaries, brackish waters and areas of upwelling where food concentrations are high (Chen and Hare 2008). The wide distribution of A. tonsa may be a result of these copepods being transported as ballast in ships. Their tolerance to changes in salinity has likely contributed to their success as an invasive species in some regions (Svetlichny and Hubareva 2014). Acartia tonsa Dana is an eurythermic and euryhaline calanoid copepod species (Lance 1964) which occurs in a wide range of geographic areas, from temperate to subtropical waters. Within these regions, the distribution is restricted to habitats characterized by relatively high food levels, such as in estuaries and upwelling near-shore environments (Paffenhofer and Stearns 1988). A. tonsa is often the dominant component of the zooplankton assemblage in terms of abundance and biomass (Durbin and Durbin 1981; McManus and Foster 1998; Cervetto et al., 1999). It is an important grazer and omnivorous species, and a source of food for several marine and estuarine invertebrates and fish larvae (Marques et al., 2007). In Ria de Aveiro, A. tonsa represented an annual average density of 30% of the total mesozooplankton abundance (Morgado 1997). In the south European estuarine ecosystem, the species occurs throughout the year over a temperature range of 15–22 °C and salinities between 12 and 28 ppt (Leandro et al., 2010). In Europe, this species has grown extensively, and since the twentieth century onward, it has reached the Baltic Sea, Mediterranean Sea, Black Sea and Caspian Sea (Calliari et al., 2008).
Since 1982, A. tonsa has been recorded in the Caspian Sea and has grown enormously since 1983, and now it has the highest abundance of zooplankton in the southern Caspian Sea (Kurashova and Abdullaeva 1984). Before the invasion of A. tonsa, genus Calanipeda was predominant in the coastal waters of southern Caspian Sea (Roohi et al., 2010). The arrival of A. tonsa to the Caspian Sea had a positive effect on fish nutrition, but its blooming reduced the population of Calanipeda (Calanipedia aquae-dulcis) (Yelizarenko 1992). Hashemian et al., (2009) reported that 66 species of zooplankton were identified in Southern Caspian Sea, with 13 species of Protozoa, 22 species of Rotifera, 21 species of Cladocera, and Copepoda with 5 species, in which A. tonsa was dominant, representing 63% of total copepod. Rowshan Tabari et al., (2014) noted also that Calanoid copepods were the main population of zooplankton in the southern of the Caspian Sea, and A. tonsa comprised the highest frequency (65%) of abundance. According to the distribution, abundance and biomass of zooplankton community in Southeast Caspian Sea, A. tonsa was most abundant, representing 72% of total of zooplankton communities (Afraei Bandpei et al., 2016 b).
Despite the ecological importance of A. tonsa and the role it plays in the food chain as a major primary consumer in the southern Caspian Sea, insufficient information is available on the abundance and biomass of its different life stages (Mazandaran- Kelarabad). Such information is important due to the current ecological changes that occur in the Caspian Sea as a result of the appearance of jellyfish (Mnemiopsis leidyi) in 1999 (Shiganova et al., 2004). The hypothesis is that there is a significant difference between the density and biomass of different stages of the life cycle of Acartia tonsa at different stations? Therefore, the goal of present study was undertaken to investigate the abundance and biomass of nauplii and copepodite of the copepod (A. tonsa) in the fish cage culture farming in the southwest Caspian Sea (Mazandaran-Kelarabad).
Materials and Methods
Seasonal sampling (in May, August, October and January) was carried out at three stations, namely station 1 (fish cage site), station 2 (500 m west of station 1) and station 3 (50 m east of station 1) in southern Caspian Sea (Mazandaran-Kelarabad) in 2012 (Figure 1). Table 1 showed the latitude and longitude situation of sampling area.
Zooplankton was sampled using a Juday net (opening diameter: 36 cm, mesh size: 100 μm) in a layer from the surface to 20 m depth. At every station, a vertical haul with a Juday net was carried out from bottom to surface using a handle pulley for heaving the net. Zooplankton samples were preserved in neutral 4% formaldehyde and analyzed in the laboratory as described by Wetzel and likens (1991).
Figure 1. Sampling stations in the southern Caspian Sea (Mazandaran-Kelarabad)
Table 1. Latitude and longitude of the sampling stations in the southern Caspian Sea (Mazandaran-Kelarabad)
Geographic latitude and longitude
Samples were divided into subsamples using a 1 ml Hensen-Stempel pipette and transferred to a Bogorov chamber for identification (Newell and Newell 1977). The lengths of individuals were measured and their weights calculated using their geometric form (Lawrence et al. 1987). At least 100 individuals were counted per sample and identified to species levels, and life-cycle stages were determined using an inverted microscope (Harris et al., 2000). Zooplankton taxonomic classification was performed based on Birstein. (1968), Kasimov (2000), James and Covich (2001).
All data was transmitted based on the rating, and then, by drawing the Q-Q form, as well as the Shapiro-Wilk test, and its normalization was confirmed (Siapatis et al., 2008). For statistical analysis, normalized data were tested using SPSS version 11.5. Pearson Correlation, parametric test (ANOVA) and Duncan test were performed on the normal and data transmitted. Pearson correlation tests were performed at a significant level of 1 and 5% (Bluman, 1998).
In the present study, 9965 individuals were counted in spring. The highest abundance (68.1%) and biomass (94.7%) were for copepodite, while nauplii showed the lowest abundance and biomass (31.9% and 5.3%, respectively. In general, males were more dominant than females. The percentage of male and female copepodite abundance in different stages of life cycles showed that the females of stages 5 and 6 were 9.5% and 13.5%, while males were 20.5% and 12%, respectively and the remnant were in the next stages (Figure 2).
Figure 2. Average Abundance and biomass of Acartia tonsa in different stations in spring. Note: I-VI is copepodite Stages (F=female, M=male)
Figure 3. Average Abundance and biomass of Acartia tonsa in different stations in summer. Note: I-VI is copepodite Stages (F=female, M=male)
In station 1, the highest abundance and biomass was at the 6th stage of male (VIM) with an average of 895.3±125.1 individuals m-3 and 24.2 ±2.4mg m-3, respectively. The lowest values were at station 3 with an average of 245.7±89.3individuals m-3 and 6.6±1.1mg m-3, respectively (Figure 2). The maximum and minimum abundance in different stages of nauplii was for nauplii II, with a mean of 813.9±200.1individuals m-3 (station 1) and 167.1±25.3individuals m-3 (station 3), respectively (Figure 2). A significant difference between abundance and biomass of A. tonsa at various life stages were found (ANOVA, P<0.05).
In summer, a total number of 825 specimens were counted. The highest and lowest abundance and biomass were for copepodite (67.2% and 89.5) and nauplii (32.8%, 10.5) stages. The abundance and biomass of A. tonsa at different life stages were significantly different (ANOVA, p<0.05). The percentage of male and female copepodite abundance in different stages of life cycles showed that the females of stages V and VI represented 9.2% and 7.3%, and the males were 12.4% and 9.6%, respectively (Figure 2). In station 1, the highest abundance and biomass was at the VIM stage of male with an average of 16.4±2.1 individuals m-3 and 0.44±0.1mg m-3, respectively, while the lowest values were recorded at VIF stage, at station3, with a mean of 7.9±1.1individuals m-3 and 0.24±0.1mg m-3, respectively (Figure 3). The maximum abundance in different stages of nauplii belonged to nauplii III with a mean of 113.1±24.21individuals m-3 (station 2) and minimum was nauplii II with a mean of 13.9±2.3individuals m-3 (station 1), respectively (Figure 3).
A total number of 4153 individuals were counted in fall. The results showed that a significant difference between abundance and biomass of A. tonsa in different life stages (P<0.05). The maximum and minimum percentage abundance and biomass of copepodite were 56.7% and 87.4% and of nauplii 43.3% and 12.6%, respectively. The percentage of females of stages V and VI was 8.8% and 10.6% and that of males was 8.6% and 9%, respectively (Figure 4). The nauplii III has the highest abundance in all stations with mean of 357.1±59.2individuals m–3. In general, females were more dominant than males. The highest abundance and biomass was at the VIF stage in station 1, with an average of 176.9±35.1 individuals m-3 and 5.5±0.1mg m-3, while the lowest values were recorded at VM in station 3, with a mean of 14.7±2.1individuals m-3 and 0.24±0.1mg m-3, respectively (Figure 4).
In winter season, 3141 samples were counted. The maximum and minimum abundance and biomass of copepodite was 49.5% and 88.3%. For nauplii, the values were 50.5% and 11.7%, respectively. Females of stages V and VI represented 13.3% and 11.7%, while males were 13.9% and 10.7%, respectively, and the remnant were in the next stages (Figure 4). In general, females were a bit more dominant than males. A significant difference in the abundance and biomass of A. tonsa in different stages was found (ANOVA, p<0.05). The highest abundance and biomass were at the VIM in station 1, with a mean of 68.8±14.6 individuals m-3 and 1.9±0.2 mg m-3. The lowest values were also recorded at VIM in station 3, with a mean of 24.6±3.6 individuals m-3 and 0.66±0.2 mg m-3, respectively. The nauplii I has the highest abundance in the different stations with a mean of 203.1±70.9 individuals m-3 (Figure 5).
Table 2 shows the abundance and biomass of A, tonsa in different months. The results revealed abundance and biomass were significantly affected by various month (p<0.05). The results indicated that the maximum abundance (301.96±40.55 individuals m–3) and biomass (3.54±0.92 mg m–3) were recorded in May, while the minimum values were in August (29.44±4.41 individuals m-3 and 0.26±0.04 mg m-3).
According to Pearson correlation analysis, there is a reverse correlation between abundance and biomass
Figure 4. Average Abundance and biomass of Acartia tonsa in different stations in fall. Note: I-VI is copepodite Stages (F=female, M=male)
Figure 5. Average Abundance and biomass of Acartia tonsa in different stations in winter. Note: I-VI is copepodite Stages (F=female, M=male)
Table 2. Average abundance and biomass of A. tonsa in different months in southern Caspian Sea. Values with different superscripts are significantly different at P<0.05.
Abundance (Individual m-3)
Biomass (mg m–3
Table 3. The relationship between abundance and biomass of A. tonsa and different variables based on correlation persons in the southern Caspian Sea (Mazandaran-Kelarabad). Note: **Correlation is significant at P< 0.01 * Correlation is significant at P< 0.05 (2-tailed).
Table 4. Abundance and biomass of Acartia tonsa in the Caspian Sea, as reported by different authors. Note: ind. is individual and mg is milligram.
Abundance (ind.m-3) (individuals m-3)
Hubareva et al., 2008
Hubareva et al., 2008
Northeast Caspian Sea
Krupa et al., 2015
Middle Caspian Sea
Krupa et al., 2015
Southern Caspian Sea
Rowshan Tabari et al., 2005
Southern Caspian Sea
Rowshan Tabari et al., 2009
Southern Caspian Sea
Rowshan Tabari et al., 2014
Southern Caspian Sea
with other variables (Table 3). These results showed that abundance and biomass were inversely correlated with months, stations and seasons, with a significant difference (p<0.01).
The present results showed that water salinity fluctuated between months, ranging from May to October (Figure 6). However, the two-way factorial analysis of variance indicated that the effects of Salinity and abundance of A. tonsa in different months were not significant (ANOVA, p>0.05).
Fish breeding in the cages on the southern shores of the Caspian Sea is native to Iran, and can play an important role in the development of aquaculture. However, if this practice is implemented without regard to environmental considerations, it can cause great damage to plankton communities in the Caspian Sea, since they are the first chain in the food pyramid (Afraei Bandpei et al., 2016 a). In recent decades, Southern Caspian Sea ecosystem has recently faced dramatic changes in nutrition network. The ecosystem of the Caspian Sea has changed from oligotrophic level”, based on the trophic index (TRIX) prior to the appearance of comb jelly (Mnemiopsis leidyi) to “meso-eutroph” after the arrival of the comb jelly (Nasrollahzadeh et al., 2016; Nasrolahzadeh 2008). These changes have led to a significant reduction in the biomass and abundance of zooplankton and change their species composition. As a result, the number of marine zooplankton coniferous species in the Caspian Sea has decreased in the late 20th century. For example, the removal of the dominant species, such as Eurytemora grimmi and E. minor from clumps and Acartia tonsa increased from 50% to over 85% of the zooplankton population (Roohi et al., 2010; Rowshan Tabari et al., 2014). Analysis of dynamics of Acartia tonsa in the Caspian Sea and other seas indicates a sharp reduction in abundance and biomass of A. tonsa in the southern Caspian Sea (Table 4). Under favorable environments, like estuaries, A. tonsa populations develop and bloom faster, and will be able to maintain itself, and often dominate the estuarine zooplankton community (Shiganova et al., 2004) as has been confirmed in the present study.
In most investigations of copepod population dynamics, a production estimate has been approached through studying populations’ life cycles, for example, cohort analysis (Landry 1975). For the sake of simplicity, however, naupliar stages (Heinle, 1966) and copepodid stages (Greze and Baldina 1964) have often been grouped as single units. Several authors have observed that naupliar larvae of marine copepods belonging to the same genus are remarkably similar, and sometimes identical. The present study showed that abundance of A. tonsa population was higher in spring than in other seasons. This might have been due to the approaching of the warm season, up-welling flood cycle, fish cage culture activities, phytoplankton flourishing and the availability of proper food for the A. tonsa as primary consumers. The highest abundance and biomass of A. tonsa in spring were recorded at station 1, presumably due to cage culture activity. The sixth stage of male life cycle (VIM) was more consistent at stations 1 and 3, which can be also due to the closeness of the two stations (the location of the cage) and the availability of food items. In summer, the abundance and biomass of different stages of A. tonsa life cycle in were highest at station 2, and stage 3 of nauplii and stage 6 of female life cycle were most abundant. This could have been related to stop fish breeding cage culture in summer.
There are many factors that affect copepod reproduction, such as egg production as a function of age, food availability, food quality, and water temperature. These factors have been extensively studied in copepods (Burris, 2014). In the present study, the abundance and biomass of A. tonsa in winter were modest at stations 1 and 3. The average density and biomass of the copepodite stage at station 1 and 3 were higher than at station 2, presumably due to fish breeding activity in the cages, increase in nutrient load, availability of food
Figure 6. Relationship between abundance of A. tonsa and salinity in the Kelarabad waters
and the male and female mating. Burris (2015) reported that a peak in the female sizes occurs in February and April in Long Island Sound of USA in which coincides with females mating season. Since the size of these copepods is dependent on food acquired as juveniles, the largest sizes should occur during times of high food (Burris, 2014), as confirmed by the results of the present study. A comparison between the amount of A. tonsa abundance in different seas showed they are less abundant in the southern Caspian Sea than in the Black Sea and Bospharus Strait (Tables 2 and 4). This has been attributed to the topographic and ecological conditions of the area, salinity, temperature, depth, time and place of sampling. According to Gubanov (2000), A. tonsa appeared and flourished in the Black Sea in early 1970s. They vigorously competed with the native species (Paracartia latisetosa), leading to severe threat and reduction in its abundance. This is because these two species occupy the same ecological niche, but the alien A. tonsa is apparently more resistant to pollution and eutrophication than P. latisetosa (Gubanov, 2000). These finds confirm the results of the present study.
In the present study, the abundance and biomass of A, tonsa at the fish cages sites (station 1) were higher than at stations 2 and 3. Similar results were reported by Demir et al., (2001) that found the zooplankton density increased in the area of fish cages on the coast of Turkey due to increased amounts of ammonium, nitrate and phosphate. These results are in agreement with the previous studies which demonstrated that A. tonsa require high food concentration in the surrounding environment (Paffenhofer and Stearns, 1988). The expansion of this species in Southern Caspian Sea may therefore be a direct result of the drastic increase in eutrophication over the last few decades. It has been reported that salinity and temperature significantly affect the abundance of A. tonsa. In the present study, water salinity increased from May to August and decreased from October to January. In contrast, the abundance of A. tonsa declined from May to August, then increased in October. Denis and Nancy (1994) demonstrated that increased salinity and temperature significantly reduced the density and sinking velocity of A. tonsa and eggs spawned at a temperature of 30 °C and a salinity of 31%. These finds confirm the results of the present study. In conclusion, the abundance and biomass of calanoid copepod, A. tonsa at the establishment of fish breeding cages (station 1) and at distance of 50 meters (station 3) from the cage were far more than the control station (station 2) and there is a significant difference. Consequently, it is suggested that, in order to obtain more information on preservation of environmental integrity and ecosystem, a pilot ecological assessment (EIA) plan for fish breeding in cages in southern Caspian Sea is necessary.
The authors are grateful to Iranian Fishery Organization for funding a project No. 2-032-200000-02-8601. we are also grateful to Dr. Pourgholam for his assistance and cooperation in execution of this project. The efforts of the rest of the staff at the Caspian Sea Ecology Research Center are highly appreciated.
Afraei Bandpei MA, Nasrollahzadeh Saravi H, Roohi A, Parafkandeh F, Khodaparast N, Younesipour H, Nasrolahtabar A, Keihansani A (2016 a) Ecological Relationships between Biotic and Abiotic parameters within the establishment of Fish Farming Cage Culture in the southern Caspian Sea. Intl J Farm & Alli Sci. Vol., 5 (7): 491-502, ijfas.com/wp-content/uploads/2017/02/491-502.pdf .
Afraei Bandpei MA, Nasrollahzadeh Saravi H, Rahmati R, Khodaparast N, Keihansani A (2016 b) Examining the Effects of Fish Cage Culture on Phytoplankton and Zooplankton Communities in the Southern Coast of the Caspian Sea (Mazandaran Waters– Kelarabad). American Journal of Life Science Researches. 4(2): 104-117.
Birstein YA (1968) The North Caspian Benthos. Zool. Zurn, 18(3), (In Russian).
Bluman AG (1998) Elementary statistics: a step by step approach. USA: Tom Casson publisher, 3rd edition.
Burris ZPL (2014) Mating Dynamics of the Calanoid Copepods Acartia tonsa and Acartia hudsonica. PhD. Thesis. University of Connecticut, 621 pp.
Burris ZPL, Dam HG (2015) Female mating status affects mating and male mate-choice in the copepod genus Acartia. J. Plankton Res. 37(1): 183–196, https://doi.org/10.1093/plankt/fbu090
Calliari D, Andersen Borg MC, Thor P, Gorokhova E, Tiselius P (2008) Instantaneous salinity reductions affect the survival and feeding rates of the co-occurring copepods Acartia tonsa Dana and A. clausi Giesbrecht differently. Journal of Experimental Marine Biology and Ecology 362: 18-25.
Cervetto G, Gaudy R, Pagano M (1999) Influence of salinity on the distribution of Acartia tonsa (Copepoda, Calanoida). JExp Mar Biol Ecol 239:33–45, https://doi.org/10.1016/S0022-0981(99)00023-4
Chen G, Hare MP (2008) Cryptic ecological diversification of a planktonic estuarine copepod, Acartia tonsa”. Molecular Ecology. 17 (6): 1451–1468, https://doi:10.1111/j.1365-294X.2007.03657.x.
Demir N, Kirkagac MU, Pulatsu S, Bekcan S (2001) Influence of trout cage on water quality, plankton and benthos in an Anatolian Dam Lake. The Israeli Journal of Aquaculture-Bamidgeh 53:115-127.
Denise DM, Nancy HM (1994) The effects of salinity and temperature on the density and sinking velocity of eggs of the calanoid copepod Acartia tonsa Dana. Journal of Experimental Marine Biology and Ecology. Volume 179, Issue 2, 29 June 1994, Pages 235-252, doi.org/10.1016/0022-0981(94)90117-1
Durbin AG, Durbin EG (1981) Standing stock and estimated production rates of phytoplankton and zooplankton in Narragansett Bay, Rhode Island. Estuaries 4:24–41
Gubanova A (2000) Occurrence of Acartia tonsa Dana in the Black Sea. Was it introduced from the Mediterranean? Mediterranean Marine Science 1(1): 105-109.
Greze VN, Baldina EP (1964) Population dynamics and annual production of Acartia clausi Gies. and Centropages kroyeri Gies. in the neritic zone of the Black Sea. Tr. Sevastop. Biol. Stn. 17:249-261. (Fish. Res. Bd. Can. Transl. Ser. 893).
Heinle, D.R., 1966. Production of a Calanoid copepod, Acartia tonsa,in the Patuxent River estuary. Chesap Sci 7:59–74.
Hubareva EL, Svetlichny A, Kideys A, Isinibilir M (2008) Fate of the Black Sea Acartiaclausi and Acartia tonsa (Copepoda) penetrating into the Marmara Sea through the Bosphorus. Estuarine, Coastal and Shelf Science, 76/1: 131-140, https://doi.org/10.1016/j.ecss.2007.06.009
James HT, Covich AP (2001) Ecology and Classification of North American Freshwater Invertebrates, Academic press, 2nd edition
Kasimov A (2000) Methods of Monitoring in Caspian Sea, QAPP-POLIQRAF, Azerbaijan,
Kurashova EK, Abdullayeva NM (1984) Acartia tonsa (Calanoida, Acartiidae) in the Caspian Sea. Zool. J. 63, 6 (in Russian). http://dx.doi.org/10.12988/asb.2015.5530
Krupa E, Barinova S, Alyimov A (2015) Redescription of Acartia (Acanthacartia) tonsa Dana, 1849 (Copepoda: Calanoida) from the Caspian Sea. Advanced Studies in Biology, Vol. 7, 9, 393 – 402. http://dx.doi.org/10.12988/asb.2015.5530
Leandro LF, Teegarden GJ, Roth PB, Wang ZH, Doucette GJ (2010) The copepod Calanus
finmarchicus: a potential vector for trophic transfer of the marine algal biotoxin, domoic acid. J. Exp. Mar. Biol. Ecol. 382, 88–95, https://doi.org/10.1016/j.jembe.2009.11.002
Lance J (1964) The salinity tolerances of some estuarine crustaceans. Biol. Bull. mar. biol. Lab., Woods Hole 127:108-118
Landry MR (1975) The relationship between temperature and the development of life stages of the marine copepod Acartia clausi Giesbr. Limnol Oceanogr 20:854–857, doi/10.4319/lo.1975.20.5.0854/abstract
Lawrence SG, Malley DF, Findlay WJ, MacIver MA, Delbaere IL (1987) Method for estimating dry-weight of freshwater planktonic crustaceans from measures of length and shape. Can. J. Fish. Aquat. Sci, 44(1): 264-274.
Marques SM, Pardal MA, Pereira MJ, Goncalves F, Marques JC, Azeiteiro UM (2007) Zooplankton distribution and dynamics in a temperate shallow estuary. Hydrobiologia, 587: 213–223, doi:10.1007/s10750-007-0682-x.
McManus GB, Foster CA (1998) Seasonal and fine-scale spatial variations in egg production and tryacylglycerol content of the copepod Acartia tonsa in a river-dominated estuary and its coastal plume. J Plankton Res, 20(4):767–785, doi=10.1.1.620.9539&rep=rep
Morgado FMR (1997) Ecologia do zooplâncton da Ria de Aveiro.Caracterização espacio—temporal, transporte longitudinal e dinâmica tidal, nictemeral e lunar. PhD Thesis, University of Aveiro, Portugal.
Nasrolahzadeh H, Afraei Bandpei MA, Pourang N, Najafpour S, Farabi MV, Gholamipour S, Firozkandian S, Rezaei M, Makhlogh A, Solimanroudi A (2016) Determination of heavy metal and petroleum pollutant in fish cage culture establishment (before breeding) in the Southern Caspian Sea (Mazandaran waters-Kelarabad). Final report. Caspian Sea Ecology Research Center, 98 P. (In Persian).
Nasrollahzadeh, H (2008) Ecological modeling on nutrient distribution and phytoplankton diversity in the southern of the Caspian Sea. PhD thesis, 243 p. USM.
Newell GE, Newell RC (1977) Marine plankton: a practical guide. London: Hutchinson, 207 pp.
Paffenhofer, G.A and Stearns, D.E. (1988) Why is Acartia tonsa (Copepoda: Calonoida) restricted to nearshore environments? Mar Ecol Prog Ser 42: 33-38.
Roshan Tabari, M, Fatemi SM, Pourgholam R, Mousavi R, Nadoushan R (2014) Latest Diversity Trend and Seasonal Abundance of Population of Zooplankton (Holoplankton) Communities in the South Caspian Sea, Iran. Iranian Journal of Fisheries Sciences 13(2) 437-448
Roshan Tabari M, Farabi M, Ganjian A, Rezvani G, Dostadr M, Rahmati R, Eslami F, Sabkara J, Khodaparast N, Kanani, M (2009) Diversity, distribution, abundance and biomass of Zooplankton in the southern Caspian Sea, Final report. Iranian Fisheries Sciences Research Institute (IFSRI), 105 P. (In Persian).
Roshan Tabari M, Pourgholam R, Salmani A, Farabi M, Ganjian A, Tahami F, Rezvani, G, Dostadr M, Rahmati R, Roohi A, Eslami F, Sabkara J, Khodaparast N, Kanani M (2005) Survey on abundance and biomass of Zooplankton in the southern Caspian Sea, Final report. Iranian Fisheries Sciences Research Institute (IFSRI), 125 P. (In Persian).
Roohi A, Kideys A, Sajjadi A, Hashemian A, Pourgholam R, Fazli H, Ganjian Khenari A, Eker-Develi E (2010) Changes in biodiversity of phytoplankton, zooplankton, fishes and macrobenthos in the southern Caspian Sea after the invasion of the ctenophore Mnemiopsis leidyi.Biol Invasions, 12, 2343–2361, doi:10.1007/s10530-009-9648-4
Shiganova TA, Dumont HJ, Sokolsky AF, Kamakin AM, Tinenkova D Kurasheva EK (2004) Population dynamics of Mnemiopsis leidyi in the Caspian Sea, and effects on the Caspian ecosystem. In: Dumont H, Shiganova TA, Niermann U (eds) In Aquatic Invasions in the Black, Caspian, and Mediterranean Seas, vol 35. Kluwer, Dordrecht, pp 71–111.
Siapatis A, Giannoulaki M, Valavanis V, Palialexis A, Schismenou E, Machias A, Somarakis S (2008) Modelling potential habitat of the invasive ctenophore Mnemiopsis leidyi in Aegean Sea. Hydrobiologia 612: 281–295, http://dx.doi.org/10.1007/s10750-008-9497-7
Svetlichny L, Hubareva E (2014) “Salinity tolerance of alien copepods Acartia tonsa and Oithona davisae in the Black Sea”. Journal of Experimental Marine Biology and Ecology. 461: 201–208. doi:10.1016/j.jembe.
Yelizarenko, M.M. (1992). Feeding of kilka in the Middle Caspian during the summer season In: Biological resources of the Caspian Sea. Abstracts of the 1st International Conference, September, 1992. BIVTS Kaspryba, Astrakhan, pp. 111-113.
Wetzel RG, Likens GE (1991) Immunological analysis. New York USA: Springer-Verlag, 391pp.doi. 10.1007/978-1-4757-4098-1