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˜ LLUPU ˜ LLUMA ¨ E AND HENN OJAVEER ¨U ¨ *, MART SIMM, ARNO PO MARIA PO ¨ EALUSE ESTONIAN MARINE INSTITUTE, UNIVERSITY OF TARTU, MA
10A 12618, TALLINN, ESTONIA
*CORRESPONDING AUTHOR:
[email protected] Received November 29, 2007; accepted in principle March 5, 2008; accepted for publication March 7, 2008; published online March 11, 2008 Corresponding editor: Roger Harris
Our new results confirm that the Ponto-Caspian cladoceran Evadne anonyx was first found in the Gulf of Finland in 1999. In the Gulf of Riga, the first specimens were detected in 2000. The observed distribution pattern, together with the recorded increase in the population density of the species of ca. 10 times during the years 2000 – 2006 indicate the recent successful establishment of E. anonyx in the low-salinity conditions (,5 psu) of the NE Baltic Sea. Evadne anonyx and the native E. nordmanni are present in mesozooplankton community from May to October. In the seasonal cycle, the maximum abundance of E. anonyx may occur later in the season than that of E. nordmanni. As the fecundity of the alien E. anonyx significantly exceeds that of the native E. nordmanni, we suggest that population abundance of E. anonyx will very likely increase in future and the species may colonize new areas in the recently invaded ecosystem.
I N T RO D U C T I O N Reviews of the marine cladocerans in the Baltic Sea traditionally consider five most abundant species: Podon intermedius, P. leuckarti, Pleopis polyphemoides, Evadne nordmanni and Bosmina obtusirostris maritima (Ackefors, 1969; Mo¨llmann et al., 2002). During the last decades, invasions of three additional cladoceran species, Cercopagis pengoi (Ostroumov, 1891), Cornigerius maeoticus (Pengo, 1879) and E. anonyx G.O. Sars 1897, all of Ponto-Caspian origin, have been recorded. The taxonomy, distribution, development and trophic relations of C. pengoi in the Baltic Sea have been relatively comprehensively studied (Gorokhova et al., 2004; Ojaveer et al., 2004; Simm and Ojaveer, 2006; Panov et al., 2007). However, regarding the other two alien cladocerans, there is only data available for the Gulf of Finland (Litvinsˇuk, 2005; Rodionova et al., 2005; Rodionova and Panov, 2006; Panov et al., 2007).
Evadne anonyx is a native species of the Caspian Sea (Rivier, 1966) and Aral lakes (though not currently present in the Aral due to increased salinity), and estuarine areas of the Black and Azov Seas (Mordukhai-Boltovskoi and Rivier, 1987; Rivier, 1998). In the Caspian Sea, the salinity tolerance of E. anonyx is from 9 to 13.5 psu and the species has been found over a temperature range 10 – 258C (Rivier, 1998). The species was first detected in the central Gulf of Finland in August 2004 (Litvinsˇuk, 2005). As E. anonyx is morphologically very similar to the native Evadne species in the Baltic Sea, E. nordmanni (Fig. 1), it was considered that the new species had potentially not been detected during routine monitoring studies. The re-analysis of the mesozooplankton samples from the eastern Gulf of Finland confirmed this assumption by showing that
doi:10.1093/plankt/fbn036, available online at www.plankt.oxfordjournals.org # The Author 2008. Published by Oxford University Press. All rights reserved. For permissions, please email:
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Successful establishment of the PontoCaspian alien cladoceran Evadne anonyx G.O. Sars 1897 in low-salinity environment in the Baltic Sea
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E. anonyx already occurred in this area since 2000 (Rodionova and Panov, 2006). In the eastern Gulf of Finland, E. anonyx was found to be present from late June to mid-September reaching maximum densities in July. During 2000 – 2004, the densities of E. anonyx increased from ,10 to over 100 ind. m23. The maximum abundance of E. anonyx was recorded in mid-July 2004, 157 ind. m23; however, over most of
the season, abundance did not exceed 100 ind. m23 (Rodionova and Panov, 2006).
METHOD To determine the possible occurrence of E. anonyx in the NE Baltic Sea, we re-analysed mesozooplankton
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Fig. 1. Photos of E. anonyx (A) and E. nordmanni (B) ( photos by A. Po˜lluma¨e).
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Fig. 2. Location of sampling sites in the southern coast of the Gulf of Finland and in the NE Gulf of Riga.
R E S U LT S A N D D I S C U S S I O N
monitoring samples collected since 1997. These were collected at the southern coast of the Gulf of Finland— Narva Bay in the eastern and Tallinn Bay in the central part—and in the NE Gulf of Riga—Pa¨rnu Bay (Fig. 2). In the Tallinn and Narva bays, the samples were collected at six monitoring stations (depth range from 10 to 40 m) twice a month. In the Pa¨rnu Bay, sampling was performed on a weekly basis at three stations (depth range from 6 to 10 m, Fig. 2). Measurements of temperature and salinity were made using a CTD. Zooplankton sample collections and analysis for the abundance calculations fully followed the recommendations of HELCOM COMBINE (HELCOM COMBINE, 2006). Seasonal abundance dynamics of E. anonyx, together with comparisons with the native species E. nordmanni are based on 2006 data in the bays studied, whereas the fecundity analysis was performed on material collected from Pa¨rnu Bay in 2006. Body length of Evadne was measured from the top of the head to the end of the caudal outgrowths while the body height was determined from the top of the head to the end of brood pouch. In addition, fecundity of both parthenogenetic (number of embryos) and gamogenetic females (number of resting eggs) was determined. Depending on the species abundance, either all Evadne individuals or a random subsample of 100 specimens per sample was investigated. Altogether 475
Our results suggest that E. anonyx was first present in Tallinn Bay, in the central Gulf of Finland, already in 1999. In Narva and Pa¨rnu bays, the first individuals were found in 2000 (Table I). Such a pattern suggests that the invasion took place most likely by ship ballast water to different ports almost simultaneously. Although a 10-fold increase in population abundance was recorded in the eastern Gulf of Finland in the years 2000 – 2004 (Rodionova and Panov, 2006), the abundance of E. anonyx is relatively low, exceeding 100 ind. m23 only in a few cases. According to our data, the alien E. anonyx has shown approximately one order of magnitude increase in abundance in the NE Gulf of Riga until 2006 with maximum abundance exceeding 120 ind. m23. In the Gulf of Finland (Tallinn and Narva bays), the mean abundance is still below 100 ind. m23 (Fig. 3). Despite the recent increase, abundance of E. anonyx represents currently only about onetenth of that of the native E. nordmanni. The newcomer E. anonyx is constantly present in the Baltic mesozooplankton community from July, although one individual was found in late May. The native E. nordmanni appears in May. Evadne nordmanni basically disappears from the plankton in the beginning of August (at a water temperature of 198C and salinity of 5 psu) while only two individuals were found in late autumn. At the same time, however, the alien E. anonyx is present until October. In the NE Gulf of Riga, the
Table I: Records of E. anonyx in the Baltic Sea Record coordinates Location Gulf of Finland (Tallinn Bay) Gulf of Finland (Narva Bay) Gulf of Finland (Primorsk) NE Gulf of Riga
Latidude, N 59850’ 59838’ 60820’ 58813’
Longitude, E 24850’ 27827’ 28844’ 24818’
Record date 22 October 1999 3 August 2000 9 July 2000 12 June 2000
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Species abundance (volume studied) 3
Three individuals (1.5 m ) One individual (1 m3) Two individuals (1 m3) One individual (1 m3)
Data source Current study Current study Rodionova and Panov (2006) Current study
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E. anonyx and 1165 E. nordmanni individuals were measured. The differentiation between E. anonyx and E. nordmanni was made according to the two basic characteristics outlined by Rivier (1998): (i) formula of the setae—number of setae on the exopodites of thoracic limbs I– IV—for E. anonyx 2.2.2.1 and for E. nordmanni 2.2.1.1, and (ii) the shape of the cauda—for E. anonyx the cauda is formed of rounded tubercles and the cauda of E. nordmanni has two conical pointed outgrowths.
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maximum abundance of E. anonyx occurs later in the season (in August) than that of E. nordmanni (in June). However, in the Gulf of Finland, the abundance of both species reached a peak at the same time, in late June or early July (Fig. 3). Evadne anonyx occurs constantly in the plankton community when water temperature exceeds 158C and salinity 5 psu. Population maximum abundances were recorded when the water temperature was 198C and salinity 5.4 psu. In contrast, Rodionova and Panov (Rodionova and Panov, 2006) have found maximum abundances of E. anonyx in the eastern Gulf of Finland at somewhat lower temperatures of 17–188C. In the native environment (Caspian Sea), E. anonyx is present at maximum abundances when the water temperature is 16–208C and salinity 12–13 psu (Mordukhai-Boltovskoi and Rivier, 1987; Rivier, 1998). In contrast to our results where we have observed the disappearance of E. anonyx from zooplankton samples at water temperatures below 158C, Rodionova and Panov (Rodionova and Panov, 2006) reported finding the species even at temperatures below 128C.
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With respect to the salinity tolerance limits, it is important to mention that before invading the Baltic Sea, E. anonyx was not considered as a high risk species for low-salinity environments because it was thought that the species is unable to survive at salinities below 9 psu (Panov et al., 1999; Rivier, 1998). However, the results of our study confirm that the species was able to establish itself and is doing relatively well in the low salinity (around 5 psu) environment. For both Evadne species, parthenogenetic females dominated the population for most of the season. A decrease in their abundance in late September coincided with the increasing abundance of males and gamogenetic females. Males and gamogenetic females of the alien E. anonyx appeared in the zooplankton community during the population abundance peak, in the beginning of August with water temperature of 198C and salinity 5 psu. The maximum abundance of E. anonyx males and females with resting eggs was recorded in late September to early October, reaching up to 22% of the total population (Table II). Males and gamogenetic females of the native E. nordmanni appeared after the first peak of population abundance, in mid-June with water temperature of 188C and salinity 4 psu, and reached up to about 14% of the total population in the beginning of July (Table II). Gamogenetic females of E. nordmanni had only a single resting egg in the brood pouch (n ¼ 13). Evadne anonyx had 1.2 + 0.1 resting eggs on average (n ¼ 49). For both species, bisexual reproduction becomes most important when parthenogenetic fecundity reaches its minimum. With the onset of sexual reproduction, the population decreases significantly until complete disappearance from the plankton. The parthenogenetic fecundity of E. anonyx was significantly (P , 0.1, t-test) higher than that of E. nordmanni: 4.7 + 0.4 (n ¼ 121) and 4.0 + 0.2 (n ¼ 42), respectively. For both species, the parthenogenetic fecundity was found to be the highest when the species first appeared into the plankton, in July for E. anonyx and in May for E. nordmanni (Table III). From August to September, the fecundity of E. anonyx started to decrease with the lowest value in September. The fecundity of E. nordmanni reached its minimum in July and then increased again in August. Only a few parthenogenetic females of E. nordmanni were found in September. The parthenogenetic fecundity of E. anonyx correlated positively with water temperature (r 2 ¼ 0.83; P , 0.01), but there was no significant correlation with salinity. However, the parthenogenetic fecundity of E. nordmanni was negatively correlated with both, temperature (r 2 ¼ 0.54; P , 0.01) and salinity (r 2 ¼ 0.38; P , 0.05).
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Fig. 3. Abundance of E. anonyx (open circles, right scale) and E. nordmanni (black circles, left scale) (ind. m23) in the Gulf of Finland, Narva (A) and Tallinn Bay (B) and in the NE Gulf of Riga (C) in 2006.
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Table II: Weekly abundance values of E. anonyx and E. nordmanni (number of ind. m23) and the structure of the Evadne community in the NE Gulf of Riga during May –October in 2006 Week 1 2 3 4 1 2 3 4 1 2 3 1 2 3
June
July
August
September
1 2 3 4 1
October
Fp
Fg
M
— — — 7 — — — — 7 10 1 16 114 23 4 — 38 3 36 44
— — — 100 — — — — 100 100 100 100 93.3 100 84 — 100 100 75.6 70.7
— — — 0 — — — — 0 0 0 0 6.4 0 100 — 0 0 11.6 22.6
— — — 0 — — — — 0 0 0 0 0.3 0 0 — 0 0 12.7 6.8
E. anonyx (%) Juv
Number of ind. m23
E. nordmanni (%) Fp
Fg
M
Juv
— — — 0 — — — — 0 0 0 0 0 0 0 — 0 0 0 0
13 112 184 899 1356 692 567 463 423 4 27 124 29 — 0 — — — 1 2
100 100 100 94.0 90.0 83.5 88.9 84.7 86.2 100 87.5 93.9 92.1 — — — — — 0 34.7
0 0 0 0 0 0 3.0 2.0 0 0 3.3 0 1.0 — — — — — 100.0 34.7
0 0 0 0 0 1.4 6.0 13.3 13.8 0 3.2 0 3.1 — — — — — 0 30.6
0 0 0 6.0 10.0 15.1 2.1 0 0 0 6.0 6.1 3.8 — — — — — 0 0
Fp, percentage of parthenogenetic; Fg, gamogenetic females; M, males; Juv, juveniles.
Table III: Monthly dynamics of morphological and fecundity (number of embryos and resting eggs) characteristics (mean + SE) of E. anonyx and E. nordmanni in the NE Gulf of Riga during May–October in 2006 Parthenogenetic females
Month E. anonyx May July August September October E. nordmanni May June July August September October
n
Gamogenetic females
L
H
Number of embryos
n
L
H
Number of resting eggs
1 18 252 94 42
0.43 1.04 + 0.04 0.87 + 0.01 0.85 + 0.01 0.75 + 0.02
0.31 0.57 + 0.02 0.53 + 0.01 0.50 + 0.01 0.44 + 0.01
— 7.80 + 0.66 5.08 + 0.35 2.58 + 0.38 —
— — 22 13 14
— — 0.82 + 0.04 0.92 + 0.03 0.81 + 0.04
— — 0.52 + 0.02 0.54 + 0.01 0.47 + 0.02
— — 1.32 + 0.10 1.15 + 0.10 1.21 + 0.11
296 419 163 159 — 1
0.78 + 0.01 0.66 + 0.01 0.63 + 0.01 0.71 + 0.01 — 0.83
0.40 + 0.00 0.41 + 0.00 0.39 + 0.00 0.40 + 0.00 — 0.42
7.00 + 0.31 2.53 + 0.24 1.52 + 0.16 3.83 + 0.31 —
— 6 4 1 1 —
— 0.82 + 0.05 0.73 + 0.03 0.84 0.88 —
— 0.46 + 0.02 0.43 + 0.02 0.46 0.52 —
— 1 1 1 1 —
L, length (mm); H, height (mm).
The relationship between the body height and the number of embryos of the alien E. anonyx correlated positively (r 2 ¼ 0.51; P , 0.01; Fig. 4.), and the relationship was significant also with body length (r 2 ¼ 0.41; P , 0.01). A positive correlation between the number of embryos per batch and the body height of parthenogenetic females has been observed in E. nordmanni (Onbe, 1978), which was also confirmed by our results (r 2 ¼ 0.61; P , 0.01). However, unlike E. anonyx, there was no
correlation with body length in the case of E. nordmanni (r 2 ¼ 0.01; Fig. 4). In conclusion, our results suggest that the recent newcomer cladoceran E. anonyx will most likely further increase in abundance and colonize new areas in the Baltic Sea. Higher reproductive potential of the species may result in a situation where its abundance exceeds that of the native E. nordmanni. Evadne anonyx may become an important food recource of several
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Month May
Number of ind. m23
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FUNDING This work was partially supported by the Estonian Science Foundation (grant no 6751) and by the EU FP6 NoE project EUR-OCEANS.
Ackefors, H. (1969) Ecological zooplankton investigations in the Baltic proper 1963–1965. Rept. Inst. Mar. Res. Lysekil. Fish. Board. Swed. Ser. Biol., 18, 1– 139. Gorokhova, E., Faherberg, T. and Hansson, S. (2004) Predation by herring (Clupea harengus) and sprat (Sprattus sprattus) on Cercopagis pengoi in a western Baltic Sea bay. ICES J. Mar. Sci., 61, 959–965. HELCOM COMBINE (2007) http://www.helcom.fi/groups/monas/ CombineManual/en_GB/Contents/. Cited 5 February 2007. Lehtiniemi, N. and Linde´n, E. (2006) Cercopagis pengoi and Mysis spp. alter their feeding rate and prey selection under predation risk of herring (Clupea harengus membras). Mar. Biol., 149, 845–854. Litvinsˇuk, L. F. (2005) Evadne anonyx Sars, 1897 (Cladocera, Polyphemoidea, Podonidae) – novyj predstavitel´ fauny Baltijskogo Morya. In Rivier, I. K., Shcherbina, G. K. H. and Krylov, A. V. (eds), Biologicheskie resursy presnyh vod: bespozvonochnye. Rybinskij dom pechati, Rybinsk. Fig. 4. Correlation between the number of embryos per batch and the body length (black circles) and total length (open circles) of parthenogenetic females of E. anonyx (A) and E. nordmanni (B).
zooplanktivorous fish in the region. In parallel, E. anonyx may also become, at the same time, prey of the alien predatory cladoceran C. pengoi which seems to prefer small-sized cladocerans (B. o. maritima) to all available other prey (Ojaveer et. al., 2004, Lehtiniemi and Linde´n, 2006). The fact that E. anonyx is performing well in the low-salinity environment in the NE Baltic Sea suggests that our knowledge on tolerance limits for even essential abiotic parameters of marine zooplankton is not sufficient for making predictions of potential new invaders. Finally, due to the continuously accumulating evidence of new invasions worldwide, the current study also points to the need for, and importance of, proper storage of all collected biological samples, to be able, if required, to track the spread and abundance of alien species over previous decades.
Mordukhai-Boltovskoi, F. D. and Rivier, I. K. (1987) Predatory Cladocerans Podonidae, Polyphemidae, Cercopagidae and Leptodoridae of the World Fauna. Nauka Publishing, Moskow. Mo¨llmann, C., Ko¨ster, F. W., Kornilovs, G. et al. (2002) Long-term trends in abundance of cladocerans in the Central Baltic Sea. Mar. Biol., 141, 343 –352. Ojaveer, H., Simm, M. and Lankov, A. (2004) Population dynamics and ecological impact of the non-indigenous Cercopagis pengoi in the Gulf of Riga (Baltic Sea). Hydrobiologia, 522, 261–269. Onbe, T. (1978) The life cycle of marine cladocerans. Bull. Plankton Soc. Japan, 25, 41–54. Panov, V. E., Krylov, P. I. and Telesh, I. V. (1999) The St. Petersburg harbour profile. In Gollasch, S. and Leppa¨koski, E. (eds), Initial Risk Assessment of Alien Species in Nordic Coastal Waters. Nord 8. Nordic Council of Ministers, Copenhagen, pp. Panov, V. E., Rodionova, N. V., Bolshagin, P. V. et al. (2007) Invasion biology of Ponto-Caspian onychopod cladocerans (Crustacea: Cladocera: Onychopoda). Hydrobiol., 590, 3– 14. Rivier, I. K. (1966) K taksonomij Evadne anonyx Sars. Tr. Inst. Biol. Vnutr. Vod., 12, 151–158. Rivier, I. K. (1998) The Predatory Cladocera (Onychopoda: Podonidae, Polyphemidae, Cercopagidae) and Leptodorida of the World. Backhuys Publishers Leiden, The Netherlands. Rodionova, N. V. and Panov, V. E. (2006) Establishment of the Ponto-Caspian predatory cladoceran Evadne anonyx in the eastern Gulf of Finland, Baltic Sea. Aquatic Invasions, 1, 7– 12.
AC K N OW L E D G E M E N T
Rodionova, N. V., Krylov, P. I. and Panov, V. E. (2005) Invasion of the Ponto-Caspian Predatory Cladoceran Cornigerius maeoticus maeoticus (Pengo, 1879) into the Baltic Sea. Oceanologia, 45, 66– 68.
The authors thank two anonymous referees whose comments substantially improved the quality of the manuscript.
Simm, M. and Ojaveer, H. (2006) Taxonomic status and reproduction dynamics of the non-indigenous Cercopagis in the Gulf of Riga (Baltic Sea). Hydrobiologia, 554, 147–154.
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