Aquatic Ecology 38: 441456, 2004. 2004 Kluwer Academic Publishers. Printed in the Netherlands.

441

Seasonal variations in the physiological condition of the benthic amphipods Monoporeia affinis and Pontoporeia femorata in the Gulf of Riga (Baltic Sea)
Kari K. Lehtonen
Finnish Institute of Marine Research (FIMR) P.O. Box 33, FIN-00931, Helsinki, Finland; (phone: +358-9-613 941; fax: +358-9-613 944 94; e-mail: lehtonen@mr.)
Received 5 August 2002; accepted in revised form 4 February 2004

Key words: Ammonia excretion, Baltic Sea, Benthic amphipods, Gulf of Riga, Lipids, Seasonal variation

Abstract Seasonal variations in the physiological condition of two benthic deposit-feeding amphipods were studied in two environmentally differing areas in the Gulf of Riga Baltic Sea with the purpose of estimating their role in benthic mineralisation. At the shallower 26 m nearshore station, Monoporeia affnis exhibited low ammonia excretion rate VNH 4 throughout the year. After intensive accumulation of lipids in spring, the lipid reserves of the individuals became rapidly depleted during autumn. Gravid females in winter-early spring showed exceedingly low lipid and triacylglycerol TAG levels compared to studies carried out in open-sea areas. Pontoporeia femorata studied at the deeper 43 m offshore station exhibited a higher VNH 4 at all times with no signicant seasonal variation. Lipid and TAG accumulated continuously until November, reaching higher levels than recorded previously for this species. Experiments showed that the temperature coefficient Q10 determined for VNH 4 is likely to depend on the recent feeding history of the amphipods. Mineralisation of nitrogen and carbon by the 2 yr1. amphipod populations at the study sites was estimated to be 1.7-3.0 g C and 11.3-13.5 mmol NH 4 m Conclusively, both biotic and abiotic factors affect the condition of the amphipods, while the species also have genuine differences in their metabolic characteristics. clusively a subsurface deposit feeder Byrn et al. 2002. Physiological characteristics of these species have been shown to reect benthic nutritional conditions Lehtonen 1994, 1995, 1996, a,b; variability in lipid level and lipid class composition indicated different bioenergetic strategies in amphipod populations inhabiting hydrographically different environments, while an elevated ammonia excretion rate VNH 4 is usually caused by recent feeding on highquality food. The Gulf of Riga is a semi-enclosed bay mean depth 26 m of the Baltic Sea, with water exchange with the Baltic Proper through relatively narrow straits Figure 1. The gulf is greatly inuenced by riverine input from a large drainage area, with the

Introduction The amphipods Monoporeia affnis Lindstrmformerly named Pontoporeia affnis; see Bouseld 1989 and Pontoporeia femorata Kryer are usually highly dominant members of the soft-bottom macrozoobenthic communities of the northern Baltic Sea e.g., Segerstrle 1937; Elmgren 1978; Andersin et al. 1978, 1984; Lehtonen and Andersin 1998. As deposit-feeders they are exceedingly dependent on the nutritional characteristics of the upper sediment layer, which, in turn, is governed by the quantity and quality of sedimenting particulate matter. Furthermore, M. affnis has been shown to feed mostly on the sediment surface, while P. femorata is almost ex-

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Figure 1. Maps of the Baltic Sea A and the Gulf of Riga B. Main study stations: GR1 and GR5, supplementary study stations for VNH 4 studies: SR5, JML, GF1 and GF2.

river Daugava as the major source of nutrients and particulate matter. A gradual eutrophication of the gulf during the past decades has been observed Ojaveer 1995, characterised by relatively high levels of nutrients Yurkovskis et al. 1993; Kuts and Hkansson 1995 and primary production Andruaitis et al. 1992. An elevation in benthic biomass, mostly due to an increase in the abundance of molluscs, has also been recorded Lagzdins et al. 1987. In addition, a nonindigenous spionid polychaete, Marenzelleria viridis, invaded the soft bottoms in the 1990s with an exceptional efficiency Cederwall and Jermakovs 1999; Cederwall et al. 1999. Still, M. afnis and P. femorata remain as important members of the areas benthos as food for higher trophic levels, playing an important role in benthic mineralisation and physical reworking of the sediment surface layer. Large spatial and interannual variability in amphipod population densities are well-documented features, and these phenomena have mainly been attributed to variability in food resources, but also to competition in overgrown populations e.g., Andersin et al. 1978; Uitto and Sarvala 1991; Lehtonen and Andersin 1998. Lipids play an integral role in the bioenergetics of M. affnis and P. femorata and determine their reproductive output and, hence, the population dynamics of the species. Since environmental factors have a profound effect on animal populations,

one of the main aims of the present study was to examine ecophysiological characteristics of M. affnis inhabiting a relatively shallow marginal embayment that exhibits extensive seasonal variation in hydrographic conditions temperature, dissolved oxygen and comparing these with results from studies in open-sea areas where these factors remain relatively stable throughout the year Lehtonen 1995, 1996a, b. Since M. affnis and P. femorata occupy and feed in different sediment surface layers, more information on their metabolic features is needed for a better understanding of their consumption of deposited organic material and, generally, the feeding habits of the two species. Moreover, these investigations serve to estimate the role of the amphipod species in the benthic mineralisation processes in the Baltic Sea benthic environments. In this study, seasonal variation in the physiological condition of M. affnis and P. femorata from two different stations was investigated by measuring VNH 4 , lipid level and lipid class composition. Benthos samples for the description of community structure and population dynamics of the amphipods were also taken. Parallel sediment studies Carman et al. 1996 were utilised to describe the benthic habitats. The amphipod population data were combined with the VNH 4 measurements and previous studies on respiration rates Lehtonen 1996b and used in es-

443 timating the contribution of the amphipod populations to mineralisation of carbon and nitrogen at the study sites. NH+ 4 excretion measurements excretion measurements were carried out NH 4 aboard the vessels according to Lehtonen 1994, 1995. After a 24 h acclimatisation period 1-3 individuals were incubated in 23.9 ml asks in the dark at 4 C for 10-14 h, with 3-10 replicates and the excreted NH 4 was determined using the method of Solrzano 1969, as modied by Bayne et al. 1985. The individuals used in the experiments were stored at 80 C or in liquid nitrogen and freeze-dried. NH 4 1 1 excretion is given as mol NH d . 4 g dry wt The effects of temperature on VNH 4 were studied by additional experiments carried out in May 1995. Immediately after sampling the individuals were transferred to aquaria kept at 12 C, and the VNH 4 measurements were started after a 24 h acclimation period. Temperature coefficient Q10 for VNH 4 was determined using the equation log Q10 = log10 k2 k1 / t2 t1 where t1 and t2 are the experimental temperatures 4 and 12 C and k1 and k2 are the excretion rates at the respective temperatures. Unpublished data from similar experiments on Q10 of VNH 4 of the two amphipod species, performed at 4 deep 80 m open-sea stations in the Gulf of Finland and Bothnian Sea are also included here. Total lipid and lipid class analysis Freeze-dried amphipods were analysed for total lipid and lipid class composition using the micromethod of Gardner et al. 1985, with some modications Lehtonen 1995. Lipids are extracted from each individual in chloroform-methanol 2:1, followed by gravimetric determination of total lipid and lipid class analysis by TLC-FID using silica-layered Chromarods S-III and Iatroscan MK-5 analyser. Estimations of respiration and NH+ 4 release of the amphipod populations Amphipods from each sampling date were grouped into 0.5-mm length classes. Mean wet weights of the individuals representing each length class were obtained using the following length-weight power function equations FIMR, unpublished data, considered valid also for specimens from the Gulf of Riga:

Material and methods Sampling Seasonal studies were performed at two stations: GR1 depth 26 m, close to the mouth of the river Daugava, and GR5 43 m in the southwest-central basin of the Gulf of Riga Figure 1. Selection of the stations was based on a benthic survey covering over 20 sites in the Latvian part of the gulf. They were regarded suitable because of clearly differing physical environments, adequate amphipod densities and for being within reasonable logistic distance from the shore for a year-round sampling scheme. Sampling was carried out with r/v Aranda of the Finnish Institute of Marine Research FIMR and the Latvian vessels Geofyzikis and Antonija in January, April, July, August, September and November 1994 and January, March and May 1995. At each station, 3-6 samples were taken with van Veen grabs biting areas: Latvian model 0.04 m2, Finnish model 0.1 m2 and passed through a small 1-mm sieve, using cooled 4-6 C seawater from the respective sites. The amphipods M. affnis at Station GR1 and P. femorata at Station GR5 were rapidly transferred to sand-bottom grain size 0.4 mm aquaria situated in the cold laboratory aboard Aranda or refrigerator aboard Latvian vessels adjusted to 4 C as used in the VNH 4 experiments. In most cases, only individuals from the reproducing generation both species are semelparous were studied. In addition, 5 van Veen samples were taken on each sampling occasion, passed through 1.0 and 0.5 mm sieves and stored in 5% formalin solution buffered with hexamin. After a minimum of 3 months in storage Dybern et al. 1976 the animals were identied to species level, enumerated and weighed wet wt. The body length of the individual amphipods was measured from the tip of the telson to the end of the rostrum to the nearest 0.5 mm. cf. Cederwall and Jermakovs 1999 and Cederwall et al. 1999. Near-bottom salinity and temperature were recorded each time with a CTD sonde, and dissolved oxygen concentration by Winkler titration.

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Figure 2. Seasonal variation in temperature A and dissolved oxygen B in the near-bottom water at the stations GR1 solid line and GR5 broken line during the study period. Winter values for oxygen are not available.

M . af finis: W mg wet wt = 0.016L mm3.05 P . femorata: W mg wet wt = 0.018L mm3.06 An empirical factor of 0.25 Lehtonen and Andersin, 1998 was applied to convert the wet weights to lyophilised dry weights. Mean dry weights from each length class obtained this way were tted into the model E aWb
1 where E excretion rate mol NH 4 d , W mean dry weight mg of the individuals from a given length class, b non-empirical exponent 0.75 Peters, 1983 and a mean intercept value, showing the level of NH 4 excretion i.e., a VNH4 , calculated for each sampling date. O2 consumption VO2 of both amphipod species was estimated using equations VO2 l O2 d1 14.29W mg dry wt0.770 October-April period, VO2 l O2 d1 18.32W mg dry wt0.774 MaySeptember period, and VO2 l O2 d1 13.93W mg dry wt1.030 gravid females, determined for M. affnis Lehtonen, 1996b. Detailed seasonal studies of this kind have not been performed on P. femorata. Application of M. affnis data to P. femorata probably overestimates the mineralisation potential for the letter species since P. femorata has been shown to have a lower metabolic rate than M. affnis Cederwall 1979. However, the magnitude of mineralisation of C by this species in the study area

is considered accurate using these equations. Empirical Q10 values of 1.7 and 2.0 for VO2 Lehtonen, in prep. were used for M. affnis and P. femorata, respectively. Since the amphipods use mostly lipids for metabolism a respiratory quotient RQ of 0.75 was chosen to convert VO2 to carbon C units. The VNH 4 of 1-mm length classes was calculated by tting the mean individual dry weights from each length class into the equation E aW0.75, where E 1 excretion rate mol NH 4 d , W lyophilised dry wt mg and a date-specic intercept Table 3. For the estimation of C mineralisation, the equations given above for VO2, determined for M. affnis Lehtonen, 1996b were used for both species. VNH 4 and VO2 were temperature-corrected using respective Q10 values of 3.8 and 1.7 for M. affnis, and 2.8 and 2.0 for P. femorata. Both excretion and respiration values were multiplied by the number of individuals in each respective length class, and the metabolism of the whole population was calculated by summing-up the values calculated for each length class. Daily respiration and NH 4 release are given as mg C or mol 2 1 NH m d . Annual total mineralisation as g C or 4 2 mmol NH m yr1 was calculated using linear in4 terpolation between the values measured at each sampling date.

Results Temperature and oxygen conditions In the summer, near-bottom temperatures up to 12 C GR1 and 9 C GR5 were recorded, while during winter-spring the temperature remained between 0.3-

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Table 1. Sediment characteristics at the sampling stations in June 1991. All data from Carman et al. 1996, except mean grain size Pallo et al. 1998. Station GR1 26 m Sediment description Mean grain size m 0-1 cm Loss on ignition % 0-1 cm 1-2 cm Water content % 0-1 cm 1-2 cm Organic C mol g dw1 0-1 cm 1-2 cm Organic N mol g dw1 0-1 cm 1-2 cm Sandy aleurite; light brown down to 2.0 cm 11.8 7.3 2.8 Station GR5 43 m Sandy-mud; light brown down to 4.5 cm 6.7 14.7 13.7

71.7 41.2

87.0 84.0

2576 878

3950 3422

200 61

380 348

1.0 C at both stations Figure 2. Oxygen concentrations showed signicant seasonal variation 3 to 12 mg O2 l1 with a longer period of low-oxygen conditions at Station GR5 in late autumn Figure 2. Sediment characteristics and benthic community structure The study sites differed markedly in terms of sediment characteristics and benthic community structure. At Station GR1, the bottom consisted of muddy sand with a low organic content of the top sediment layer, while the bottom at Station GR5 was muddy and had a high organic content Table 1. The community data abundance and biomass are presented as annual means Figure 3. At Station GR1 the annual average of total abundance of macrozoobenthic organisms was an order of magnitude higher compared to Station GR5 5657 and 499 ind m2, respectively while the biomass was four times higher 156 and 38 g wet wt m2 Figure 3. The high density of the polychaete M. viridis at Station GR1 2374 ind m2 represents 33% of the total biomass. At Station GR5 this species plays a less signicant role 62 ind m2, 12% of total biomass. At Station GR1 a high abundance and biomass of the deposit/lter-feeding clam Macoma balthica 1429 ind m2, 55% of total biomass was observed. Here, also another benthic

amphipod, Corophium volutator was present 170 ind m2. The amphipod populations At Station GR1, M. affnis was the dominant amphipod species 1454 ind m2; 3.7% of total biomass, with complete absence of P. femorata. At Station GR5 P. femorata was 10 times higher in abundance compared to the co-existing M. affnis; however, both showed low densities 374 and 34 ind m2, respectively. Due to the difficulty in obtaining sufficient numbers of specimens at every sampling occasion, M. affnis was not studied at Station GR5. For size distributions, a 3-value moving average was used and the individuals were divided into year classes cohorts. The weight ranges obtained from monthly means of the amphipods studied were 2.13.4 mg M. affnis and 3.8-7.1 mg P. femorata lyophilised dry wt. Both species exhibited a 2-year lifecycle and offspring were released in late January P. femorata or March-April M. affnis. Lipid level and lipid content The lipid levels of M. affnis at Station GR1 showed a slight decline by 14 September 31.7% compared to 3 July 36.1% Figure 4. By 11 November, the

446 ence was found between the gravid females and the specimens collected on all other dates. Calculations based on changes in mean weights and lipid levels showed no net accumulation of lipid in M. affnis between 3 July and 11 November Table 3. Instead, net depletion of lipid intensied towards late autumn, and the gravid females showed a markedly high depletion rate by 5 January. Size-corrected values of the lipid content of the new reproducing generation born 1994 on 6 May 1995 were not different from previous years summer values. The lipid level of P. femorata at Station GR5 remained almost constant throughout the summerautumn 34.337.3% and was still relatively high on 11 November 30.2% Figure 4. Gravid females on the brink of spawning on 5 January showed a lipid level of 20.3%. Seasonal variability in the lipid content of a standard-size P. femorata 5.7 mg dry wt; obtained in a similar way as described for M. affnis was not marked until 10 November, while the lipid content of the gravid females 5 January was signicantly lower compared to others Table 2. Contrary to M. affnis at Station GR1, the lipid balance of P. femorata was positive i.e., net accumulation throughout the autumn, turning negative i.e., net depletion only between gravidity and offspring release Table 3.
Figure 3. Macrozoobenthic community structure at the study stations GR1 and GR5, presented as average abundance above and biomass below.

Lipid class composition In both species the seasonal patterns in triacylglycerol TAG levels followed closely those of total lipid levels. P. femorata at Station GR5 showed constantly higher TAG levels seasonal range: 63.080.8% compared to M. affnis at Station GR1 44.572.8% Figure 5. In P. femorata, the proportion of phospholipids PL varied between 10.7 and 21.6% and, in M. affnis, between 17.8 and 38.3%. The other measured lipid classes wax esters, free fatty acids, sterols/diacylglycerols and acetone-mobile polar lipids comprised altogether 6.115.4% and 7.520.0% in P. femorata and M. affnis, respectively. The dependence of the TAG content mg ind1 on the dry weight of the individuals as well as seasonal variability in the content of TAG were very similar to those of total lipid in both species Table 2. NH+ 4 excretion: seasonal variation A power failure in the ultrafreezer 80 C caused the destruction of the samples collected in January

lipid levels had declined to 20.9%, and, during maturation, ovigerous/gravid females continued to deplete lipid 5 January: 16.8%, exhibiting low lipid levels on 30 March 9.2%. After the spring bloom in early May 1995, the lipid level of the new reproducing generation born 1994 was high 37.1%. After pooling the seasonal data, the lipid content mg ind1 of M. affnis was found to be size-dependent Table 2. Thus, in addition to presenting the proportion of lipids of total dry weight Figure 4, seasonal variability in the lipid content was examined also by comparing the lipid contents of a standardsize individual, using the dry wt vs. lipid content regression equation given in Table 2 and the mean value of each monthly average weight of individuals representing the reproducing generation 2.7 mg dry wt; data from March and May 1995 not available. The lipid content of M. affnis was signicantly reduced by 11 November. The most signicant differ-

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Figure 4. Seasonal variation in lipid levels % dry wt of Monoporeia affnis and Pontoporeia femorata. Vertical bars indicate SE unless smaller than symbol.

and April 1994. However, estimations of the mean dry weights of the specimens used in excretion experiments were obtained from population samples and used for the calculation of VNH 4 , and, further, in the estimations of the mineralisation potential of the populations. The effect of body weight on VNH 4 of each species was studied by pooling the seasonal weight vs. excretion rate data, enabling a larger weight scale than possible with single-date measurements. Because of an attempt to establish a weight-rate relationship not affected by a recent input of goodquality food spring bloom sedimentation or physiological modications related to reproduction, the data were compiled selectively. Actual weights were not available on 19 April, and this data was omitted as well as the signicantly higher rates recorded on 6 May during high sedimentation of the spring bloom at Station GR1. For M. affnis, the dry weight vs. VNH 4 power regression proved to be non-signicant F1, 22 0.79, p 0.39. For P. femorata, the equa1 0.55 tion E mol NH F1, 40 4 d 0.054W mg 2 17.9, p 0.0001, r 0.31 was determined, giving evidence that the VNH 4 is clearly weight-dependent slope deviating signicantly from 1.0 but is affected also by other factors low r2. These factors include individual differences in recent feeding history or the amount of energy reserves which are likely to cause more inter-individual variability in VNH 4 than in oxygen consumption. While acknowledging these results, weight-correction of the excretion rates using

the common scaling exponent 0.75 Peters 1983 was considered in this case to be the most reliable method in examining the differences between the sampling dates and stations. ANOVA was performed on VNH 4 measurements made in April, July, August not at GR1, September, November 1994 and May 1995 for both stations separately. Results from January and March 1995 experiments were omitted from this analysis because of the small number of measurements due to difficulties in sampling. Gravid females were also discarded because of a distinctly higher VNH 4 which is unrelated to food conditions Lehtonen 1996b. The 4 males caught at Station GR5 on 11 November showed signicantly higher VNH 4 compared to others subadultstwo-sample t-test on weight-corrected rates: df 10, t 2.4, p 0.05. These were not included in the analyses because of a higher activity probably related to increased swimming activity and/or metabolic adjustments related to reproduction. Similar to lipid and TAG contents, the VNH 4 is given both as direct values per weight and as per standard individual weight for the whole study period. At Station GR1 the VNH 4 of M. affnis ranged be1 dry wt d1 durtween 13.0 and 28.9 mol NH 4 g ing the season, with the highest mean rate recorded on 6 May 1995 Figure 6, Table 4. ANOVA performed on weight-corrected rates calculated for a standard-size individual of 2.7 mg showed a significant difference in VNH 4 between the sampling dates F4, 32 7.0, p 0.0004; Tukeys test showed that

448
Table 2. Monoporeia affnis and Pontoporeia femorata. Statistical analyses on the lipid and triacylglycerol TAG content of the individuals. Seasonal changes were studied using values calculated for a standard-size individual of each species. In the Tukeys multiple comparison test Table created for lipid and TAG in parentheses, statistical signicancies are indicated as *** p 0.001, ** p 0.01*, * p 0.05 and ns not signicant. a gravid females. ANOVA Monoporeia affnis GR1 Lipid mg 0.216 dry wt mg 0.455 - seasonal variation: ANOVA TAG mg 0.129 dry wt mg 1.211 - seasonal variation: ANOVA Pontoporeia femorata GR5 Lipid mg 0.332 dry wt mg 0.046 - seasonal variation: ANOVA TAG mg 0.282 dry wt mg 0.426 - seasonal variation: ANOVA Tukeys multiple comparison test Monoporeia affnis 2.7 mg dry wt Date 03 Jul 03 Jul 14 Sep 11 Nov 05 Jana 30 Mara 06 May ns ns *** *** *** *** *** *** ns ns F
df

p 24.1 62.0 6.1 15.0 0.0001 0.0001 0.02 0.0001

F1, F5, F1, F5,

36 24 30 23

F1, F6, F1, F6,

61 56 43 56

290.8 18.2 81.3 11.0

0.0001 0.0001 0.0001 0.0001

17 Aug

14 Sep

11 Nov

05 Jana

30 Mara

*** * *** ** *** *** ns ns

* ns *** ** *** **

ns ns *** **

*** ***

Pontoporeia femorata 5.7 mg dry wt Date 02 Jul 17 Aug 02 Jul 17 Aug 14 Sep 10 Nov 05 Jana 30 Mar 06 May ns ns ns ns *** ** *** *** ** ** ns ns

14 Sep

11 Nov

05 Jana

30 Mar

ns ns * ns *** *** ns ns ns ns

* ns *** *** ns ns ns ns

*** *** ns ns * ns

*** ** *** ***

ns ns

the rates measured on 6 May 1995 were higher than on all other dates 20 April and 2 July: p 0.001, 11 November: p 0.05, except on 14 September p 0.05. ANOVA without data from 6 May showed no difference between the rates F3, 26 2.24, p 0.11. At Station GR5, seasonal variation in the VNH 4 of P. femorata standardised for a 5.7 mg individual was not signicant ANOVA: F5, 42 1.4, 1 p 0.24, the range being 20.7-30.3 mol NH 4 g 1 dry wt d Figure 6, Table 4. NH+ 4 excretion: effect of temperature on rates The results indicate that the magnitude of the effect of temperature on VNH 4 is dependent on the initial level of excretion at 4 C Figure 7. The lowest

value for Q10 1.2 was recorded on 20 September 1995 at Station GF2 central Gulf of Finland for P. femorata, at a time when no signicant difference could be noted in VNH 4 measured either at 4 or 12 C t-test: t 1.36, df 17, p 0.19; at that time, VNH 4 at 4 C was as high as 64.6 mol g dry wt1 d1. The highest Q10 2.8 for P. femorata was recorded at Station GR5 on 6 May 1995, when the 1 1 d . For M. VNH 4 at 4 C was 32.7 mol g dry wt affnis, the highest coefficient 3.9 was calculated for individuals collected from Station JML western Gulf of Finland on 24 April 1996 4 C: 16.7 mol g dry wt1 d1 and lowest 2.2 at the same station on 13 August 1996 4 C: 26.6 mol g dry wt1 d1.

449

Figure 5. Seasonal variation in lipid class composition of Monoporeia affnis and Pontoporeia femorata as % of total lipids A and weight mg of each lipid class in a mean-size individual B. In B, data from March and May 1995 are missing because population samples needed for the calculation of mean weights were not collected. TAG triacylglycerols, PL phospholipids, Other wax esters free fatty acids sterols/diacylglycerols acetone-mobile polar lipids, G gravid females. Note different scales in B.

1 1 Figure 6. Variation in the VNH d for the reproducing generation of Monoporeia affnis and Pontoporeia femorata during 4 mol NH4 g the study period. Vertical bars indicate SE unless smaller than symbol. Results for April have been calculated using the mean weights of the studied generation obtained from population samples see text.

450
Table 3. Monoporeia affnis and Pontoporeia femorata. Net lipid accumulation or depletion rates g d1 in the reproducing generation, obtained by linear interpolation of changes in dry weight and lipid level % dry wt between sampling dates, and by calculating a mean daily rate for each period. G gravid females. M. affnis GR1 03 Jul 16 Auga 16 Auga 14 Sep 14 Sep 11 Nov 11 Nov 05 Jan G
a

Lipid g d1 0.1 0.4 0.8 2.5

P. femorata GR5 02 Jul 17 Aug 17 Aug 14 Sep 14 Sep 10 Nov 10 Nov 05 Jan G

Lipid g d1 6.3 7.0 4.1 14.1

Lipid level of M. affnis in 16 August used for calculation was estimated assuming a linear change between 3 July and 14 September

Table 4. Monoporeia affnis and Pontoporeia femorata. Seasonal values of the intercept a SD, determined for the equation E aWb E 1 mol NH 4 d , a intercept, W dry weight mg, b xed non-empirical exponent 0.75, describing the weight-specic NH4 ex cretion rate of the amphipods. n number of determinations. The intercept values were used in the calculations of total NH4 release by the amphipod populations. Date 1994 Jan 27 April 19 July 02/03 Aug 17 Sep 14 Nov 10/11 - Males 1995 Jan 05 - Gravid females May 06
a

n 6 9 7 9 3 3 8
b

GR1 Monoporeia affnis 0.0208 0.0223 0.0317 0.0289

n 7 6 9 8 6 3 3 4 3 10

GR5 Pontoporeia femorata 0.0392 0.0270c 0.0390 0.0172a 0.0511 0.0119 0.0470 0.0120 0.0452 0.0054 0.0487 0.0118 0.0611 0.0078 0.0903 0.0146 0.0792 0.0023 0.0450 0.0164

0.0051a 0.0081 0.0056b 0.0043

0.0297 0.0189c 0.0459 0.0080 0.0320 0.0105

Used for calculations in May 1994;

Used for calculations in August 1994; c Used for calculations in December 1993

Mineralisation of N and C by the amphipod populations At Station GR1, the release of NH 4 by the M. affnis population was estimated to range from 10.9 April 2 1 d Figure 8, while to 84.8 July mol NH 4 m 2 annual NH4 release was 13.5 mmol NH yr1. 4 m Daily respiration ranged between 3.9 January and 15.0 July mg C m2 d1, and annual C mineralisation was estimated at 3.0 g C m2 yr1. The release of NH 4 by the P. femorata population at Station GR5 ranged from 3.9 May to 67.4 mol 2 1 d AugustFigure 8, and annual NH NH 4 m 4 2 release was 11.3 mmol NH yr1. C mineralisa4 m tion was calculated to range between 0.7 May and 9.9 mg C m2 d1 August, annual total being 1.7 g C m2 yr1.

Discussion Seasonal variations in lipid levels and lipid class composition In summer, lipid and TAG levels of M. affnis at Station GR1 were intermediate compared to other areas of the northern Baltic Sea Hill et al. 1992; Lehtonen 1995, 1996a but the decline towards winter was more striking. Offspring release occurred in March, and the gravid females were notably lipid-poor at that time 9.2%. The seasonal range in lipid levels was wide 22-37%; gravid females not included, resembling that recorded in the Bothnian Sea Lehtonen 1996a where a highly concentrated seasonal sedimentation pattern prevails, similar to most areas of the northern Baltic Sea Leppnen 1988; Heiskanen and Kononen, 1994; Lehtonen and Andersin 1998. In M. affnis, the dependence of lipid levels on resource

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Figure 7. Relationship between VNH 4 at 4 C and temperature coefficient Q10 for Monoporeia affnis and Pontoporeia femorata, as determined by VNH 4 at 4 and 12 C. Stations: GR1 and GR5 Gulf of Riga, SR5 Bothnian Sea, JML, GF1 and GF2 Gulf of Finland.

2 1 Figure 8. NH d , A and carbon mineralization mg C m2 d1, B by Monoporeia affnis and Pontoporeia femo4 release mol NH4 m rata populations at stations GR1 and GR5. The rates have been calculated separately for each 1-mm size class but are shown here as combined to 2-mm size classes.

452 input and competition during the previous season was examined by Lehtonen and Andersin 1998. The highest mean lipid level 2 July 1994: 37.3% in P. femorata at Station GR5 was higher than recorded by Paradis and Ackman 1976, Hill et al. 1992 and Lehtonen 1995. Excluding gravid females, the seasonal range in lipid levels was narrower than in M. affnis 27-37%. The lower lipid levels observed in P. femorata have been interpreted as an implication of a different bioenergetic strategy compared to M. affnis see Hill et al. 1992; Lehtonen 1995, corroborated by recordings of a lower swimming activity and VO2 Cederwall 1979 in this species. However, the present study shows that P. femorata is capable of attaining similar lipid and TAG levels often recorded for M. affnis. The positive lipid balance between 4.1 and 7.0 g lipid d1, Table 2 recorded for P. femorata at Station GR5 between 2 July and 11 November differs markedly from that of M. affnis at Station GR1, which had a zero-or-negative lipid balance throughout this period. For comparison, an open-sea population of M. affnis mostly showed a negative lipid balance in late autumn Lehtonen 1996a. The different lipid dynamics observed are likely related to differences in growth; in a coastal area the two species have been shown to have different growth patterns, with P. femorata continuing to grow in autumn while the growth of M. affnis ceases much earlier Uitto and Sarvala 1991. Also in an open-sea population of M. affnis a complete halt in growth in early autumn has been recorded Lehtonen and Andersin 1998. The reduced levels of lipid and TAG in gravid females seem characteristic for both species Hill et al. 1992; Lehtonen 1996a, and are associated with increased protein metabolism, which is reected in accelerated VO2 Lehtonen 1996a, b. In addition to functioning as stored energy for future metabolic needs lipids act as fuel for biosynthesis in the build-up of reproductive tissue and the formation of reproductive products e.g., Falk-Petersen et al. 1981; Clarke et al. 1985. The greatly diminished lipid stores found in M. affnis at Station GR1 in late autumn may reduce the ability of the gravid females to survive and take care of their brood until hatching. A low lipid content of the offspring may also directly reduce their viability Ouellet et al. 1992. Seasonal and spatial variations in VNH+ 4 The low VNH 4 levels recorded for M. affnis at Station GR1 are characteristically found in poor-nutrition situations e.g., in the open-sea areas of the northern Baltic Sea between late autumn and early spring, while the signicantly higher value observed in May 1995 is considered a metabolic response to the sedimentation of fresh organic matter Lehtonen 1996b. An even more marked elevation in the VNH 4 after the spring bloom was noted in a deep, open-sea M. affnis population from the Bothnian Sea Lehtonen 1996b. The higher and seasonally more stable excretion rate of P. femorata seems typical for this species Lehtonen 1995, and unpublished data and is probably related to different feeding patterns and growth dynamics Uitto and Sarvala 1991. Male P. femorata showed signicantly higher VNH 4 compared to subadults, which has also been observed in male M. afnis Lehtonen, unpublished data. This may be caused by a general increase in metabolic activity which is connected to enhanced swimming as the males, after maturation, seek actively for females Segerstrle 1937. A higher VNH 4 recorded here for gravid P. femorata seems typical for this life stage, and has also been observed in gravid M. affnis Lehtonen 1996b. In this case, high VNH 4 is not associated with food availability but caused by an increased use of body protein for metabolic energy production due to already depleted lipid reserves, and/or the increasing excretion of the developing embryos within the females marsupium. Potential effects of environmental conditions and intra/interspecic competition Because the two species were not studied in one and the same area, a direct assessment of the effects of environmental setting on the physiological condition of the amphipods cannot be made. However, previous studies on the ecological physiology of the species in other sea areas may be used to cast light on the underlying causes of the observed patterns in the condition of both amphipod species. In 1995, the peak of diatom sedimentation in the Gulf of Riga started to decline in the beginning of May, and from thereon the settling material had greater proportions of heterotrophic biomass and slowly-sinking phytodetrital material Lundsgaard et al. 1999; Olli and Heiskanen 1999; Reigstad et al. 1999. Due to the hydrodynamic conditions prevail-

453 ing in the Gulf of Riga the sedimented matter is also effectively resuspended Floderus et al. 1999; Reigstad et al. 1999, and especially after the breakdown of the thermocline in autumn, the resuspended ne particulate material is to a great extent transported towards the central-basin accumulation area e.g., Station GR5. This substantial transport of material from the basin margins may offer a more long-lasting food source for benthic organisms at Station GR5 as compared to Station GR1. At the near-shore Station GR1 the organic content of the sediment surface layer 0-2 cm in depth was low Table 1; Carman et al. 1996. The inuence of the river Daugava, a constant provider of organic particulate matter of terrestrial origin e.g., vascular plant and macroalgae remains is high. However, this material is of considerably lower nutritional quality as compared to a marine food source such as sedimenting algae, which is readily assimilated by the benthos e.g., Parsons et al. 1977; Tenore et al. 1982. Despite their apparent good physiological condition the abundance of P. femorata at Station GR5 was not particularly high, while M. affnis at this location occurred in very low numbers Figure 3. The period of low oxygen concentrations observed in late autumn Figure 2 may have affected the distribution and abundance of the amphipod species especially at Station GR5. It is therefore concluded that, in the deep areas of the Gulf of Riga, a common mechanism may be at work in which pelagic eutrophication provides the benthos with increasing amounts of food. The subsequent deterioration of oxygen conditions lead to a reduced survival, reproduction and recruitment of amphiphod species. The benthic community at the study sites differs in terms of species biomass and abundance and is likely to be affected by intra- and interspecic competition for food. Compared to Station GR5, the 10-fold higher macrofaunal density at Station GR1 Figure 3 competing for the food resources is likely to have an effect on the physiological condition of species in this area. The high abundance of other macrobenthic deposit- and/or lter-feeders, especially M. balthica and C. volutator, and the overall higher diversity and biomass Figure 3 at Station GR1 keeps the competition pressure at a markedly higher level as compared to Station GR5. The meiofaunal communities at both stations belong to the most abundant recorded in the Baltic Sea, with densities of 900000 ind m2 Pallo et al. 1998. This important compartment of the benthos also utilises a signicant share of the annual input of quality food. Importantly, the abundance of harpacticoid copepods of 140000 ind m2 recorded at Station GR1 is among the highest observed anywhere in the world, while their number at Station GR5 is considerably smaller 35000 ind m2; Pallo et al. 1998. Besides competition, there exists evidence that meiofauna and even juvenile M. balthica are consumed by M. affnis lafsson and Elmgren 1991; Ejdung et al. 2000. No denite conclusion on the effect of competition can be drawn here due to the lack of studies in similar habitats with differing community structures and densities nor a proper assessment made of the quantity and quality of particulate matter received by the different areas in the Gulf of Riga. Effects of temperature on VNH+ 4 The effect of temperature on the VNH 4 was generally more pronounced for M. affnis than for P. femorata Figure 7. This may be caused either by interspecic differences or, as suggested by the apparent relation between the initial excretion rate at 4 C and Q10, by differences in environmental nutritional conditions. A slight increase in VO2 by 22% after the sedimentation of the spring bloom has been recorded for M. affnis Lehtonen 1996b, but, in that study, the acceleration of VNH 4 was ca. 7-fold compared to the pre-bloom situation. Since VO2 is mainly a measure of general metabolic activity, it is likely that the effect of temperature on VO2 is rather conservative with Q10 values close to 2.0, while VNH 4 is considerably more affected by nutrition. Similar phenomena have been recorded for zooplankters reviewed by Le Borgne 1986, showing different Q10 values for v and VNH 4 . The almost recorded for P. femtemperature-independent VNH 4 orata at Station GF2 during a high-excretion period Figure 7 would in this case result in O:N ratios indicative for a shift towards a more lipid-based energy metabolism following temperature increase, showing that these amphipods are capable of reducing VNH 4 in situations of a signicant loss of nitrogen. In M. affnis, the Q10 for VNH 4 ranged between 2.2 and 3.9, indicating that temperature elevation increases the immediate use of protein for metabolic energy if Q10 for VO2 would remain around 2.0. Thus, the initial levels of VNH 4 , indicating also a balance of metabolic substrates at the ambient temperature, seem to determine the type of response caused by elevations in temperature.

454 The temperature history of populations may play a role in adaptation. Compared to the amphipods at the deep stations in the Gulf of Bothnia SR5 and Gulf of Finland JML, GF1 and GF2 the populations in the Gulf of Riga are subject to a signicantly greater seasonal amplitude in temperature Figure 2. At the deep stations the seasonal temperature conditions were almost identical Station SR5, seasonal range 1991: 2.4-5.3 C, JML 1996: 3.7-4.4 C, GF2 1996: 3.7-4.2 C; FIMR, unpublished data. Therefore, nutritional factors seem to overshadow the effects of temperature on the VNH 4 of these amphipods. Apparently, M. affnis and P. femorata may have different capabilities of modifying their bioenergetic strategy and acclimatisation to varying temperature and feeding conditions. Mineralisation of C and N by the amphipod populations The C and N mineralisation potential of the amphipod populations studied is mostly dependent on their abundance and biomass, but is also inuenced by temperature. Partly due to the low temperature, mineralisation is very low during the winter-spring period Figure 8. In summer-autumn, the growth of the amphipods is intensive and together with a marked elevation in temperature, a signicant elevation in the metabolism of the population is observed. The estimated annual total respiration 1.7 and 3.0 g C m2 yr1 for P. femorata and M. affnis, respectively, is much less than recorded by Bergstrm and Sarvala 1986 for a coastal M. affnis population 11.9 g C m2 yr1, 31% of total benthic respiration. Temperature regime in that area, however, had a wider range with periods of 18 C and the density of the population was considerably higher compared to the present study. At a deep, open-sea station with a constantly low seasonal temperature range 2.45.3 C, Lehtonen and Andersin 1998 showed the annual respiration of the M. affnis population to be 14-17 g C m2 yr1. The estimated daily NH 4 release values 3.9 to 2 1 are average compared to m d 84.8 mol NH 4 other sites studied in the Baltic Sea up to 237 mol 2 1 d ; Lehtonen, 1995. Annual rates 11.3NH 4 m 2 yr1 are smaller than those re13.5 mmol NH 4 m corded by Lehtonen and Andersin 1998; 15-31 mmol 2 yr1 in an area where the abundance and NH 4 m biomass of the M. affnis population is considerably higher but the VNH 4 of the amphipods remains very low between autumn-spring Lehtonen 1996b. Between September 1991 and March 1992 in the Gulf of Riga, Aigars and Andruaitis 1993 recorded total benthic ammonium efflux rates ranging between 302 1 790 mol NH d mean ca. 300 mol NH 4 m 4 2 1 m d at a 27-m station close to Station GR1, and 2 1 between 30-660 mol NH d mean ca. 400 4 m 2 1 mol NH4 m d at a 37-m accumulation bottom well comparable to Station GR5. Calculating the potential share of amphipod excretion of these rates gives values ranging between 3-13% of total NH 4 efflux, with the exception of occasionally high values of ca. 30% at the times of very low total efflux rates 2 1 d as recorded in January-Feb30 mol NH 4 m ruary. Unfortunately, the late spring-early autumn period that presumably has the highest benthic activity was not studied by Aigars and Andruaitis 1993; assuming benthic efflux rates at least twice higher than the higher mean would yield values between 4-10% for the contribution of the amphipods to total NH 4 production. These values are in accordance with the results of Tuominen et al. 1999, who, in a laboratory experiment using manipulated sediment cores, found M. affnis to contribute 5-10% to the total NH 4 efflux. It is therefore concluded that excretion by the amphipods plays a small but stable role in the benthic nitrogen dynamics of the Gulf of Riga. Gardner et al. 1987 estimated the excretion of an abundant freshwater amphipod Diporeia hoyi population in Lake Michigan to comprise up to 42% of total benthic nitrogen release. Henriksen et al. 1983 showed that excretion by the amphipod C. volutator could account for 80% of the net NH 4 ux from the sediment, providing nitrifying bacteria a potentially signicant source of NH 4 . Bioturbation by C. volutator has been shown to enhance also benthic denitrication rates Pelegr and Blackburn 1994; Pelegr et al. 1994. Considering that M. affnis and P. femorata inuence benthic mineralisation processes directly by metabolising organic material and also indirectly by bioturbation, further investigations on their ecophysiology and behaviour would be advantageous in understanding benthic nutrient dynamics in soft-bottom areas of the Baltic Sea.

Acknowledgements This study was part of the interdisciplinary multinational Gulf of Riga Project, funded mainly by the Nordic Council of Ministers.

455 Hans Cederwall University of Stockholm and Vadims Jermakovs Institute of Aquatic Ecology, University of Latvia are thanked for delivering the benthos data. Special thanks are given to Ieva Upeniece Institute of Aquatic Ecology, University of Latvia for sampling and performing the excretion experiments aboard Latvian vessels. Other members of the Benthic Group of the Gulf of Riga Project, Bertil Widbom University of Stockholm, Juris Aigars and Parsla Pallo Institute of Aquatic Ecology, University of Latvia and Ann-Britt Andersin FIMR are also thanked for most enjoyable co-operation. Comments by Dr. K. Essink and two anonymous reviewers improved the nal version of the manuscript.
Symposium. Pergamon Press, New York, New York, USA, pp. 309316. Cederwall H. and Jermakovs V. 1999. Growth and production of three macrozoobenthic species in the Gulf of Riga, including comparisons with other areas. Hydrobiologia 393: 201210. Cederwall H., Jermakovs V. and Lagzdins G. 1999. Long-term changes in the soft-bottom macrofauna of the Gulf of Riga. ICES J. Mar. Sci. 56: 4148. Clarke A., Skadsheim A. and Holmes L.J. 1985. Lipid biochemistry and reproductive biology in two species of Gammaridae. Mar. Biol. 88: 247263. Dybern B.I., Ackefors H., Elmgren R. 1976. eds, Recommendations on methods for marine biological studies in the Baltic Sea. The Baltic Marine Biologists, Publication No. 1, 98 pp. Ejdung G., Byrn L., Elmgren R. 2000. Benthic predator-prey interactions: evidence that adult Monoporeia affnis Amphipoda eat postlarval Macoma balthica Bivalvia. J. Exp. Mar. Biol. Ecol. 253: 243251. Elmgren R. 1978. Structure and dynamics of Baltic benthos communities, with particular reference to the relationship between macro- and meiofauna. Kieler Meeresforsch Sonderh 4: 122. Falk-Petersen S., Gatten R.R., Sargent J.R. and Hopkins C.C.E. 1981. Ecological investigations on the zooplankton community in Balsfjorden, northern Norway: seasonal changes in the lipid class composition of Meganyctiphanes norvegica M. Sars, Thysanoessa raschii M. Sars, and T. inermis Kryer. J. Exp. Mar. Biol. Ecol. 54: 209224. Floderus S. Jhmlich S. Ekebom J. and Saarso M. 1999. Particle ux and properties affecting the fate of bacterial productivity in the benthic boundary layer at a mud-bottom site in South-Central Gulf of Riga. J. Marine Systems 23: 233250. Gardner W.S., Frez W.A., Cichocki E.A. and Parrish C.C. 1985. Micromethod for lipids in aquatic invertebrates. Limnol. Oceanogr. 30: 10991105. Gardner W.S., Nalepa T.F. and Malczyk J.M. 1987. Nitrogen mineralization and denitrication in Lake Michigan sediments. Can. J. Fish Aquat Sci. 32: 12261238. Heiskanen AS and Kononen K. 1994. Sedimentation of vernal and late summer phytoplankton communities in the coastal Baltic Sea. Arch. Hydrobiol. 131: 175198. Henriksen K., Rasmussen M.B. and Jensen A. 1983. Effect of bioturbation on microbial nitrogen transformations in the sediment and uxes of ammonium and nitrate to the overlying water. Ecol. Bull. 35: 193205. Hill C., Quigley M.A., Cavaletto J.F. and Gordon W. 1992. Seasonal changes in lipid content and composition in the benthic amphipods Monoporeia affnis and Pontoporeia femorata. Limnol Oceanogr 37: 12801289. Kuts T. and Hkansson B. eds 1995. Observations of water exchange, currents, sea levels and nutrients in the Gulf of Riga. SMHI Reports Oceanography No. 23, 109 pp. Lagzdins G., Saule A. and Pallo P. 1987. The change in benthic macrofauna as an indication of eutrophication in the southern part of the Gulf of Riga. In: Virbickas J., Racjunas L., Auktikalnene A., Astrauskas A. eds, Biological Resources of Waterbodies in the Basins of the Baltic Sea. Proceedings of the 22nd Scientic Conference on Investigations of Baltic Waterbodies, Vilnius. pp. 101-102. in Russian Le Borgne R. 1986. The release of soluble end products of metabolism.. In: Corner E.D.S., OHara S.C.M. eds, The Biological

References
Aigars J. and Andruaitis A. 1993. Nutrient transport through the water-sediment interface in the Gulf of Riga. Proc. Latvian. Acad. Sci. B 10: 7377. Andersin A.B. Lassig J. and Sandler H. 1984. On the biology and production of Pontoporeia affnis Lindstr. in the Gulf of Bothnia. Limnologica 15: 395401. Andersin A.B. Lassig J. Parkkonen L. and Sandler H. 1978. Longterm uctuations of the soft bottom macrofauna in the deep areas of the Gulf of Bothnia 1954-1974, with special reference to Pontoporeia affnis Lindstrm Amphipoda. Finnish Mar. Res. 244: 13744. Andruaitis G., Andruaitis A., Bitenieks Y., Priede S. and Lenshs E. 1992. Organic carbon balance of the Gulf of Riga.. In: Proceedings of the 17th CBO conference, Norrkping 1990. Swedish Hydrological and Meteorological Institute Report. Bayne B.L., Brown D.A., Burns K., Dixon D.R., Ivanovici A., Livingstone D.R., Lowe D.M., Moore M.N., Stebbing A.R.D. and Widdows J. 1985. The Effects of Stress and Pollution on Marine Animals. Chap. Physiological procedures. Praeger Publishers, New York, New York, USA, pp. 161-178. Bergstrm I. and Sarvala J. 1986. Seasonal course of soft-bottom community respiration in a northern Baltic archipelago. Ophelia Suppl. 4: 17-26. Bouseld E.L. 1989. Revised morphological relationships within the amphipod genera Pontoporeia and Gammaracanthus and the glacial relict signicance of their postglacial distributions. Can. J. Fish. Aquat. Sc. 46: 17141725. Byrn L., Ejdung G., Elmgren R. 2002. Comparing rate and depth of feeding in benthic deposit-feeders: a test on two amphipods, Monoporeia affnis Lindstrm and Pontoporeia femorata Kryer. J. Exp. Mar. Biol. Ecol. 281: 109121. Carman R., Aigars J. and Larsen B. 1996. Carbon and nutrient geochemistry of the surface sediments of the Gulf of Riga, Baltic. Sea. Mar. Geol. 134: 5776. Cederwall H. 1979. Diurnal oxygen consumption and activity of two Pontoporeia Amphipoda, Crustacea species. In: Naylor E. and Hartnoll R.G. eds, Cyclic Phenomena in Marine Plants and Animals. Proceedings of the 13th European Marine Biology

456
Chemistry of Marine Copepods. Oxford Science Publications, Clarendon Press, Oxford, UK, pp. 109164. Lehtonen K.K. 1994. Metabolic effects of short-term starvation on the benthic amphipod Pontoporeia affnis Lindstrm from the northern Baltic Sea. J. Exp. Mar. Biol. Ecol. 176: 269283. Lehtonen K.K. 1995. Geographical variability in the bioenergetic characteristics of Monoporeia/Pontoporeia spp. populations from the northern Baltic Sea, and their potential contribution to benthic nitrogen mineralization. Mar. Biol. 123: 555564. Lehtonen K.K. 1996a. Ecophysiology of the benthic amphipod Monoporeia affnis in an open-sea area of the northern Baltic Sea: seasonal variations in body composition, with bioenergetic considerations. Mar. Ecol. Prog. Ser. 143: 8798. Lehtonen K.K. 1996b. Ecophysiology of the benthic amphipod Monoporeia affnis in an open-sea area of the northern Baltic Sea: seasonal variations in oxygen consumption and ammonia excretion. Mar. Biol. 126: 645654. Lehtonen K.K. and Andersin A.B. 1998. Population dynamics, response to sedimentation and role in benthic metabolism of the amphipod Monoporeia affnis in an open-sea area of the northern Baltic Sea. Mar. Ecol. Prog. Ser. 168: 7185. Leppnen J.M. 1988. Cycling of organic matter during the vernal growth period in the open northern Baltic proper. VI. Sinking of particulate matter. Finnish Mar. Res. 255: 97118. Lundsgaard C., Olesen M., Reigstad M. and Olli K. 1999. Sources of settling material: aggregation and zooplankton mediated uxes in the Gulf of Riga. J. Marine Systems 23: 197210. Ojaveer E. ed. 1995. Ecosystem of the Gulf of Riga between 1920 and 1990. Estonian Academy of Sciences, Estonian Academy Publishers, Tallinn, 277 pp. lafsson E., Elmgren R. 1991. Effects of disturbance by benthic amphipod Monoporeia affnis on meiobenthic community structure: a laboratory approach. Mar. Ecol. Prog. Ser. 74: 99107. Olli K. and Heiskanen A.S. 1999. Seasonal stages of phytoplankton community structure and sinking loss in the Gulf of Riga. J. Marine Syst. 23: 165184. Ouellet P., Taggert C.T. and Frank K.T. 1992. Lipid condition and survival in shrimp Pandalus borealis larvae. Can. J. Fish. Aquat. Sci. 49: 368378. Pallo P., Widbom B. and lafsson E. 1998. A quantitative survey of the benthic meiofauna in the Gulf of Riga eastern Baltic Sea, with special reference to the structure of nematode assemblages. Ophelia 49: 117139. Paradis M. and Ackman R.G. 1976. Localization of a marine source of odd chain-length fatty acids. I. The amphipod Pontoporeia femorata Kryer. Lipids 11: 863870. Parsons T.R.K. Takahashi M. and Hargrave B.T. 1977. Biological Oceanographic Processes, 2nd ed. Pergamon Press, Oxford, UK. Pelegr S.P. and Blackburn T.H. 1994. Bioturbation effects of the amphipod Corophium volutator on microbial nitrogen transformations in marine sediments. Mar. Biol. 121: 253258. Pelegr S.P, Nielsen L.P. and Blackburn T.H. 1994. Denitrication in estuarine sediment stimulated by the irrigation activity of the amphipod Corophium volutator. Mar. Ecol. Prog. Ser. 105: 285 290. Peters R.H. 1983. The Ecological Implications of Body Size. Cambridge University Press, Cambridge, UK. Reigstad M., Heiskanen A.S. and Wassmann P. 1999. Seasonal and spatial variation of suspended and sedimented nutrients C, N, P in the pelagic system of the Gulf of Riga. J. Marine Syst. 23: 211232. Segerstrle S.G. 1937. Studien ber die Bodentierwelt in sdnnlndischen Kstengewssern III. Zur Morphologie und Biologie des Amphipoden Pontoporeia affnis, nebst einer Revision der Pontoporeia-Systematik. Soc. Scient. Fenn. Comment. Biol. 7: 1181. Solrzano L. 1969. Determination of ammonia in natural waters by the phenolhypochlorite method. Limnol. Oceanogr. 14: 799801. Tenore K.R., Cammen L., Findlay S.E.G. and Phillips N. 1982. Perspectives of research on detritus: do factors controlling the availability of detritus to macroconsumers depend on its source? J. Mar. Res. 40: 473480. Tuominen L., Mkel K., Lehtonen K.K., Haahti H., Hietanen S. and Kuparinen J. 1999. Nutrient uxes, pore water proles and denitrication in sediment inuenced by algal sedimentation and bioturbation by Monoporeia affnis. Estuarine Coastal Shelf Sci. 49: 8397. Uitto A. and Sarvala J. 1991. Seasonal growth of the benthic amphipods Pontoporeia affnis and P. femorata in a Baltic archipelago in relation to environmental factors. Mar. Biol. 111: 237 246. Yurkovskis A., Wulff F., Rahm L., Andruzaitis A. and RodriguezMedina M. 1993. A nutrient budget of the Gulf of Riga; Baltic Sea. Estuarine Coastal Shelf Sci. 37: 113127.