Population dynamics of the main copepod species in the Gulf of Gdańsk (the southern Baltic Sea): abundance, biomass and production rates

Samples used in this study were collected monthly during a three-year period between March 2010 and December 2012, at six stations located in the western part of the Gulf of Gdansk (the southern Baltic Sea) (Fig. 1). Five of the sampling stations (S1, S2, S3, S4, J23) were located on a depth gradient transect (depth from 5 to 40 m) and one station (M2 - 10 m deep). Station M2 is located in the western part of the Gulf of Gdansk. It is a semi-enclosed area, isolated from the rest of the Gulf of Gdańsk by the presence of a shoal. Due to the hydrological dissimilarity of the region from the rest of the bay, we found it advisable to include this station in our study area. The Sopot profile and the M2 station are part of the monitoring stations’ network, which are used for zooplankton monitoring since the 1970s. This provides a complete picture of this part of the bay. The zooplankton material was collected with a WP2 zooplankton sampling net (100 pm mesh size). Sampling at specific stations was performed in 10 layers. All samples were collected during daytime (mainly between 10 am and 2 pm) so the diurnal vertical migrations were not taken into account. Qualitative and quantitative laboratory analyses were performed in accordance with the Manual for Marine Monitoring in the COMBINE Programme of Helcom (Annex C-7).

Figure 1

The vertical distribution of copepod development stages was determined by computing weighted mean depths (WMD) (Bollens, Frost 1989, Renz, Hirche 2004) for the three studied species:

where n_i is the abundance (individuals m^-3) at each depth layer with the midpoint d_i The calculations were made for four stages: nauplii (N), copepodites CI-CIII, copepodites CIV-CV and adults.

Biomass was calculated from the abundance using weight standards after Hernroth (1985), and the obtained values were integrated for the whole water column. Finally, seasonal biomass values were derived by averaging the corresponding months. Carbon was calculated as 5% of the wet weight according to Mullin (1969). This conversion rate is usually used for the Baltic copepods, although as illustrated by Tanskanen (1994), it may lead to the underestimation of the zooplankton biomass.

Production of the copepodite stages of the studied species was calculated using Edmondson and Winberg’ equation (Edmondson, Winberg 1971) with the assumption that there were nonlimiting food conditions:

where PC_i represents daily potential production of stage i (g wet weight); N_i is the abundance of the corresponding development stage i; D_i is the development time of stage i (day^-1), and ΔW_i is the difference in wet weight of stage i. D_i of the developmental stages were calculated using Belehrádek’s function (Belehrádek 1957):

where a and ɑ for copepodite stages are 1 288 and -10.5 for Acartia spp., 1 466 and -10.4 for T. longicornis, 3044 and -13.9 for Pseudocalanus sp., respectively, and b is 2.05 for all taxa according to McLaren (1978, 1989). T was the ambient temperature (°C) and was determined for each stage on the basis of its WMD.

The temperature fluctuated throughout the study period between 15 to 20°C in June -September (Fig. 2). For the other months, the temperature was about 10°C and below. The thermocline was observed in 2010 from July to October, and in 2012 between August and October. Salinity oscillated throughout the study period around 7, which is typical of the Gulf of Gdansk (Fig. 3).The lowest value of salinity (6.6) for the study period was recorded in the surface water layer at the turn of July and August 2010.

Figure 2

Figure 3

During the three-year study period, the average copepod abundance reached the highest value between July and August. In 2010, the maximum abundance was observed in July (25 101 ind. m^-3) (Fig. 4), while in August the value was slightly lower and reached 24 570 ind. m^-3. The highest three-year value of copepod abundance was recorded in August 2011, i.e. 26 448 ind. m^-3. A significant decline in copepod abundance in 2010-2012 was observed from September to December. In September, the values ranged from 17778 ind. m^-3 (2011) to 16323 ind. m^-3 (2012). The years 2011-2012 were characterized by a similar distribution of abundance from January to June. From January to April, the average abundance of copepods in the Gulf of Gdansk gradually decreased below 736 ind. m^-3. In May, the concentration of copepods increased rapidly and was similar in both years (~7000 ind. m^-3) (Fig. 4).

The distribution of biomass throughout the years 2010-2012 showed a similar trend as the abundance. The lowest values in both 2011 and 2012 were observed in April (6.64 mg C m^-3 -2011, 4.47 mg C m^-3 - 2012). The biomass of these crustaceans increased steadily in late summer and spring reaching the maximum values in August 2010 (145.30 mg C m^-3), 2011 (125.46 mg C m^-3) and 2012 (127.07 mg C m^-3). Through the rest of the year, the biomass values dropped to less than 80 mg C m^-3 in September and less than 30 mg C m^-3 in October and November (Fig. 5).

Figure 4

Figure 5

The biomass concentration of Acartia spp. was the highest among the studied taxa. The distribution of biomass values of Acartia spp. in 2011 and 2012 had a similar trend, with an increase between June and July and the maximum in September - 70.60 mg C m^-3 in 2011 and 63.57 mg C m^-3 in 2012 (Fig. 6). In 2010, the rapid growth observed between April and May was followed by a slight decrease in June. The maximum biomass in 2010 was noticed in August (96.85 mg C m^-3). During the cold months, the value of Acartia spp. biomass did not exceed 15 mg C m^-3 (Fig. 6).

Figure 6

The abundant occurrence of species from the genus Acaria during summer is typical of the Gulf of Gdańsk (Dzierzbicka-Głowacka et al. 2012) and the Baltic Proper (Holste 2010). According to Mudrak (2004), maximum abundance values of this copepod occur also in mid-summer. Abundance of this taxa was clearly correlated with water temperature (Table 1). Similar to the results obtained by Möllmann et al. (2000), who described the long-term trends in the biomass of the main mesozooplankton taxa in the central Baltic Sea, the fluctuations in the biomass of Acartia spp. and T. longicornis observed during our study were positively correlated with temperature. Due to its thermophilic nature, Acartia spp. tends to concentrate in the upper water layers since mid-spring was observed (Fig. 7). The optimum temperature for Acartia spp. ranges from 3 to 16°C, with the preferred temperatures above 10°C (Mudrak 2004). The lack of these copepods in the surface waters during summer might be caused by too high light intensity (Speekmann et al. 2000). Through the rest of the year, the population of Acartia spp. was dispersed in the whole water column.

Figure 7

The biomass of T. longicornis showed a similar distribution in particular months. In cold months of 2010-2012, the biomass values did not exceed 10 mg C m^-3 (Fig. 6). A significant growth of biomass was observed only in May (about 20 mg C m^-3). The upward trend continued until August where it reached its maximum. In 2010, the rapid growth of biomass began in May, like in the case of Acartia spp. June 2010 was the month when biomass reached minimum values (about 10 mg C m^-3), and this year’s maximum was recorded in July. T. longicornis had the second, smaller peak of biomass in autumn with the maximum in November. During this period, mean biomass values ranged from 14.36 mg C m^-3 in 2012 to 16.98 mg C m^-3 in 2011. This species had it highest concentrations in the summer when water temperature ranged from 15 mg C m^-3 to 18 mg C m^-3 (Fig. 6). Mudrak (2004) showed that T. longicornis occurs in the Gulf of Gdansk throughout the year, with the largest concentration in the summer months and autumn. The previous studies (Witek 1995) showed that June was the month with the maximum abundance, and July - the maximum biomass.

Between January and April, T. longicornis was present in the entire water column (Fig. 8). In May, the population moved to the upper water layers. In June, nauplii and stages CI and CII concentrated in the upper water masses, and stages CIII and CIV were found in the lower layers. Through the rest of the summer, this copepod preferred the lower water masses.

Figure 8

Pseudocalanus sp. had the lowest contribution to the copepod biomass in the Gulf of Gdansk during the study period. There was no clear pattern in the biomass of this species, as the highest values were recorded in different months. In August 2012, Pseudocalanus sp. biomass had the maximum value (4.60 mg C m^-3) (Fig. 6). In the remaining months of this year, the biomass did not exceed 1.5 mg C m^-3. In 2010, Pseudocalanus sp. had the lowest contribution to the biomass of Copepoda, as compared to the rest of the three-year period. The maximum of this year was recorded in March - only 2.24 mg C m^-3 and August - 2.21 mg C m^-3 (Fig. 6).

The abundance of Pseudocalanus sp. is mostly dependent on salinity (Carter 1965), however, our research was conducted in a relatively shallow area with no clear halocline, which may be a reason for so low and chaotic distribution of this species. Unfortunately, due to the relatively low abundance there was no clear correlation between abundance and temperature (Table 1). From June, the highest abundance of Pseudocalanus sp. was observed in the bottom water layers (Fig. 9) due to the preference for colder water for the growth and development (Dzierzbicka-Głowacka 2004). Through the rest of the year, Pseudocalanus sp. was dispersed in the whole water column due to relatively low water temperature, not exceeding 10°C.

Figure 9

Figure 10 presents the weighted mean depths (WMD) of four established ranges of developmental stages (nauplii N, copepodites CI-CIII, copepodites CIV-CV and adults) of Acartia spp., T. longicornis and Pseudocalanus sp. at the deepest sampling station J23.

Figure 10

There are no clear patterns in the distribution of stages. The observed differences in the three-year mean WMD were >2 m between nauplii and adults of Acartia spp., >5 m between nauplii and adults of T. longicornis and 3 m between nauplii and copepodites CI-CIII of Pseudocalanus sp.

The differences in the mean annual WMD were: >3 m in 2010 and 2011 and >2 m in 2012 between nauplii and Acartia spp. adults; >6 m in 2010 and >4 m in 2011 and 2012 between nauplii and T. longicornis adults; >10 m in 2010 between copepodites CI-CIII and adults of Pseudocalanus sp.; >4 m in 2011 between copepodites CIV-CV and adults, and >8 m in 2012 between nauplii and copepodites CI-CIII of Pseudocalanus sp.

Acartia spp. individuals were primarily concentrated within the upper 17 m of the water column. After 3 years of the studies, it could be noticed that WMD of different developmental stages of Acartia spp. in the successive seasons did not change significantly, in contrast to T. longicornis. The maximum values of WMD for T. longicornis were observed in late summer. In September 2010 and 2011, WMD for adults of T. longicornis were 35 m and 28.5 m, respectively, and in August 2012 - 32.4 m. Pseudocalanus sp. individuals were not observed during summer and WMD in the remaining months was between 5 and 35 m for different developmental stages.

The results obtained in our studies are similar to those presented by Dzierzbicka-Głowacka et al. (2013) for the same area in 2006 and 2007. The authors observed all developmental stages of Acartia spp. remaining very close to each other, but the observed difference in the mean annual WMD was much lower. We have noticed that the stages of T. longicornis also seem to stay close to one another, but nauplii were found near the surface and adults preferred the deepest waters. The same conclusions were drawn by Dzierzbicka-Głowacka et al. (2013). As for Acartia spp., the difference in the mean annual WMD for T. longicornis was much lower in this study compared to that obtained by Dzierzbicka-Głowacka et al. In the case of Pseudocalanus sp., older stages (rather than younger ones) preferred greater depths. The differences in the mean annual WMD were the same as those obtained by Dzierzbicka-Głowacka et al. (2013) - approximately 30 m. Also, similarly to our study, Möllmann and Koster (2002) observed no significant relationship between the vertical distribution of different developmental stages and the depth for Acartia spp. and Temora longicornis. Renz and Hirche (2005) studied vertical distribution patterns as WMD for each stage of Pseudocalanus acuspes and concluded that it was stage specific. Similar results were obtained in our studies.

Over the three-year study period, a significant increase in the production of copepods was observed in the Gulf of Gdansk. The highest production rates were noted for Acartia spp., followed by T. longicornis, and the lowest amount was recorded for Pseudocalanus sp. Among those species, only Acartia spp. showed a clear correlation between temperature and production rates (Table 2). In the case of T. longicornis, there were probably other factors involved, like grazing having a stronger impact on the production rates, and in the case of Pseudocalanus sp., it was most likely the effect of data scarcity.

In the winter-spring periods of 2010-2012, the production rates for Acartia spp. and T. longicornis increased steadily and the observed values were similar for both taxa. In the spring of 2010, the production rate was approximately 4 mg C m^-2 d^-1, while in 2011 and 2012, this value was 2 mg C m^-2 d^-1 (Fig. 11). The production for Acartia spp. and T. longicornis reached a peak in the summer. The exception is 2010, when the maximum production for T. longicornis occurred in spring. The estimated value of production in the summer was significantly higher for Acartia spp. than for T. longicornis and ranged from 12 mg C m^-2 d^-1 (2010) to 18 mg C m^-2 d^-1 (2011), while the production rate for T. longicornis did not exceed 3 mg C m^-2 d^-1 in the summer period (Fig. 11).

Figure 11

The average daily production of Pseudocalanus sp. did not exceed 0.8 mg C m^-2 d^-1 over the three years. The results show the highest production in the summer of 2011 (0.77 mg C m^-2 d^-1). In 2010, the average daily production ranged from 0.02 mg C m^-2 d^-1 in winter and spring to 0.10 mg C m^-2 d^-1 in summer, while in 2012 the average daily production ranged from 0.02 mg C m^-2 d^-1 in spring to 0.17 mg C m^-2 d^-1 in summer (Fig. 11).

The estimation of copepod secondary production is one of the most important objectives in marine ecology, because it explains and predicts the amount of energy transferred within communities and ecosystems to higher trophic levels (Renz et al. 2012).

During the study period, Acartia spp. and T. longicornis were characterized by higher rates of production in comparison with Pseudocalanus sp. Taxa were recorded in all studies, but the maximum value of production was reported in the summer. This seems to correlate with natural population dynamics of those species in the Baltic Sea (Wiktor 1985), (Dippner et al. 2000; Renz, Hirche 2005; Schulz et al. 2012). Higher production rates of Acartia spp. and T. longicornis correspond also with the trend observed by Möllmann and Koster (2002) and Renz et al. (2007) in the central Baltic.

When comparing the results with the literature from 2006 and 2007, we notice a significant decrease in the average daily production of T. longicornis in the Gulf of Gdansk. The 2010-2012 results for Acartia spp. compared with the previous research conducted in the Gulf of Gdansk indicate a slight production growth in the winter, and a production decrease in spring. A significant change occurred for Pseudocalanus sp.: the previous studies showed the maximum value of production for this taxon in the winter, while the present results show the highest production in the summer.

In 2004, the research on the secondary production was conducted in the southern North Sea. The results showed the lowest values in October (0.04 mg C m^-2 d^-1) and February (0.07 mg C m^-2 d^-1), while the maximum was recorded in May and June (136 mg C m^-2 d^-1 and 124 mg C m^-2 d^-1, respectively). Such large differences in the value of production for Pseudocalanus sp. may be caused mainly by the life strategy and metabolic processes of the organisms. The Pseudocalanus sp. population of the North Sea is in fact about 3 times larger than in the Baltic Sea. The North Sea population also develops 3-5 times faster, which may cause the secondary production of this taxon to be 10 times higher (Renz, Hirche 2005; Renz et al. 2007).

Values of secondary mesozooplankton production in the Bornholm Basin described by Dahmen (1999) significantly exceed our results in the Gulf of Gdansk. Dahmen (1999) observed the highest values of secondary production for all species in July 1991, (CI-adult stages). The largest part in the secondary production of Copepoda was contributed by T. longicornis - about 200 mg C m^-2 d^-1, followed by Acartia spp. - about 170 mg C m^-2 d^-1 and Pseudocalanus minutus - about 80 mg C m^-2 d^-1. More than two times lower production were obtained in October 1988 (CI-adult stages) for Acartia spp. and Pseudocalanus minutus, while the secondary production for T. longicornis remained high at about 165 mg C m^-2 d^-1. Such a large discrepancy compared to our results was most likely caused by differences in the calculation method as well as specific characteristics of the study areas, mainly the sampling depth.

In 1977, Ciszewski and Witek published the results on the secondary production of two copepod species: Acartia bifilosa and Pseudocalanus elongatus in Gdansk Basin. In these studies, growth rates were determined from a lab culture. Additional secondary production values were calculated as annual production rates: 16.75 for Acartia bifilosa, and 12.42 for Pseudacalanus elongatus which makes them difficult to compare.