Monoporeia Affinis and Pon Toporeia Fern Ora Ta to Oxygen Deficiency

MARINE ECOLOGY PROGRESS SERIES Vol. 151: 135-141, 1997 Published May 22 Mar Ecol Prog Ser ~ ------1-.

Tolerance of the deposit-feeding Baltic amphipods Monoporeia affinis and Pon toporeia fern ora ta to oxygen deficiency

Birgitta Johansson*

Department of Zoology. Stockholm University, S-10691 Stockholm, Sweden

ABSTRACT: Tolerances of the 2 most common species of amphipods in the Baltic Sea to low oxygen concentrations were determ~nedover a range of ambient salinities in the Baltic. For both spec~esmore than half of the tested individuals had died by the end of 24 h of exposure to nearly anoxic water (0.2 mg O2 1.'). Despite its higher respiration rate and level of activity, Monoporeia affiniswas s~gnifi- cantly more tolerant than Pontoporeia femorata both to short (1 to 5 d) and long (24 d) per~odsof exposure to low oxygen levels. As long as the amphipods survived the tested salinity, there were only minor effects of salinity on their tolerance to oxygen deficiency. Among the common macrobenthic soft- bottom species in the study area, M. affinisand P. femorata seem to be the most sensitive to oxygen deficiency.

KEYWORDS: Oxygen def~ciency. Salinity . Arnphipods Monoporela affinis. Pontoporeia femorata - Baltic Sea

INTRODUCTION The present study is focused on the Baltic Sea proper, known for vast areas depleted of animals Today, benthic oxygen deficiency occurs as a short- through oxygen deficiency (Andersin et al. 1978). The or long-term phenomenon in many estuarine and shal- permanent halocline in the Baltic Sea prevents mixing low coastal areas. Density stratification of the water by of the water column, and as a result anoxia and hydro- a pycnocline, preventing oxygen exchange between gen sulphide occur commonly in the deep water surface and bottom water, is one important reason why (Andersin et al. 1978). The area affected varies oxygen deficiency occurs. Where present, eutrophica- depending on intrusions of oxygenated water from the tion aggravates the phenomenon by enhancing oxygen North Sea, which normally occur every 3 to 4 yr (Mat- consumption in the bottom water layer, often resulting thaus & FI-anck 1992). This oxygen deficiency is partly in oxygen levels low enough to negatively affect the a natural phenomenon. However, during the present benthic community (Officer et al. 1984, Rosenberg et al. century the oxygen deficiency has worsened and the 1990, de Jong et al. 1994, Turner & Rabalais 1994, re- areas affected have increased due to eutrophication. view in Diaz & Rosenberg 1995). In extreme cases, mass The input of nitrogen to the Baltic Sea has increased mortality (Steimle & Sinderman 1978, J~rgensen1980) about 4 times and that of phosphorus 8 times in this and emigration from affected areas have been reported century (Larsson et al. 1985). These nutrients have (Baden et al. 1990). But long before such dramatic stimulated pelagic primary production. Above the events occur, oxygen deficiency reduces benthic bio- halocline the macrobenthic biomass has increased mass (Gaston 1985, Friligos & Zenetos 1988), changes (Cederwall & Elmgren 1980) and below it the elevated species composition (Llanso 1992), and depresses sedimentation rate of organic material has increased growth (Weber & Kramer 1983. Nilsson & Skold 1996) oxygen consumption (review in Elmgren 1989). A and feeding rates (Widdows et al. 1989). decrease in number of species and macrofaunal biomass, or their total disappearance, has been reported as a result of oxygen deficiency (Cederwall & Elmgren

0 Inter-Research 1997 Resale of full article not permitted Mar Ecol Prog Ser 151. 135-141, 1997

1990). When the oxygen concentration increases, Inc., USA). The accuracies of the oxygen meters were recolonization by macrofauna may follow (Leppakoski regularly checked, and adjustments made if necessary, 1969, Andersin et al. 1978, Gosselck & Georgi 1984, by comparing their readings with those obtained using Andersin et al. 1990, Andersin & Sandler 1991). the Winkler method. The oxygen concentration was The objective of this study was to measure the toler- decreased by increasing the flow of nitrogen gas, ance to oxygen deficiency of the 2 most abundant which was regulated by a magnetic valve controlled by macrobenthic animals in the Baltic Sea, the amphipods the oxygen meter. The flow of nltrogen gas was auto- ~Vonoporeiaaffinis (Lindstrom) and Pontoporeia fe- mat~callyswitched off once the desired oxygen con- morata Kroyer. Both live in soft sediments, M. affinis centration was reached. To obtaln very low oxygen mainly from 20 m depth and downwards and P. concentrations, the water surface was covered with femorata below 30 m depth (Segerstrsle 1950, Jarve- Plexiglas or floating plastic. This resulted in a stable kiilg 1973) Most individuals are found in the upper 5 cm and homogeneous oxygen concentration. Air was con- of the sediment, but they burrow down to 13 cm, with P. tinuously bubbled through the control tank. femorata on average found deeper than M. affinis(Hill Each replicate consisted of a round plastic beaker & Elmgren 1987). Both species are deposit-feeders and (380 m1 volume) with a lid. Holes in the sides of the primarily ingest the upper sediment layer (Lopez & Elm- beakers, covered with fine netting (0.5 mm mesh size), gren 1989). P. femorata has a lower respiration rate and allowed all replicates to receive the same oxygen con- is less active than M. affinis (Cederwall 1979). These centration while keeping the amphipods apart. Each amphipod species are important as prey for fish (Aneer beaker contained sieved, 3 cm deep sediment. At the 1975) and larger invertebrates (Abrams et al. 1990, Hill end of the experiments, the amphipods were trans- & Elmgren 1992), and probably also as effective biotur- ferred to well-oxygenated water and the number of bators which influence the biogeochemical processes in survivors counted after 30 min. the sediment as described for Pontoporeia hoyi (Robbins Effect of artificial sea water. For ~Vonoporeiaaffinis 1982).It is thus important to improve our knowledge of and Pontoporeia femorata, survival rates in natural and their tolerance to the oxygen deficiency that affects artificial sea water were determined at salinities of large areas of the Baltic Sea bottom. 6.5% and 9% for 34 d. The same tests were also carried out on M. affiniswith an exposure time at salinity 6.5% of 62 d. The natural sea water was concentrated METHODS by evaporation to gOh,and the artdicial sea water was made up with special aquarium salt ('hw-Marinemix + General methods. Field collections and experiments Bio-elements', Wiegant GmbH, Germany). Intact plas- were carried out during summer. Sediment and animals tic beakers (380 ml) were used, filled with 3 cm of were collected with a benthic sled at 30 to 40 m in the sieved sediment. Five (34 d experiments) and 10 repli- Baltic Sea, close to the Asko Laboratory (80 km south of cates of each treatment (62 d experiments), with 6 Stockholm), where natural sea water was obtained. The amphipods (-1800 m-2) in each, were included. sediment was homogenised by sieving through a Tolerance to oxygen deficiency. In the first expen- 0.5 mm screen. The amphipods were of the l+ age ment, the oxygen concentration was gradually class, hatched in early spring of the previous year. All decreased in consecutive steps in order to determine experiments were run in a temperature-controlled approximately how sensitive the amphipods were. The room at 5°C. The light and dark periods were regulated experimental tanks (215 X 42 X 15 cm) were filled with with a timer, and a dim green light (simulating natural natural sea water. The oxygen concentration was conditions) was on between 07:OO and 19:OO h in the rapidly decreased (within 6 h) to the target level. Expo- first 2 experiments and between 05:OO and. 21:OO h in sure to each oxygen concentration lasted for 24 h, the third tolerance experiment. Unless otherwise noted, starting with 0.8 mg O2 1-' (6.5% oxygen saturation) the tank water had the same salinity as the water in followed by 0.7 (5.7%), 0.6 (4.9761, 0.4 (3.3%) and which the amphipods had been collected (6.5"A). 0.3 mg O2 1-' (2.4%). For each species. 25 beakers with The experiments were run in rectangular tanks, and 4 amphipods each (-1200 m-2), which is within their the water was recirculated with a pump (440 1h-'). The normal range of densities according to Ankar & Elm- oxygen electrode was placed at the inlet end, and gren (1976), were placed in the experimental tank. nitrogen gas was supplied at the outlet end, which was Five beakers per species were taken out each day and screened off from the animal containers. The oxygen the survival rates recorded. Five control beakers with 4 concentration was monitored with an oxygen meter amphipods each were examined at the end of the (AOWL2/KOB/421, Processtyrning AB, Sweden), and experiment for each species. the readings were stored on a data logger (Analog A second experiment was run in the same way, Connection Jr and QuickLog PC, Strawberry Tree except that Monoporeia affinis alone was tested at a Johansson: Tolerance of Baltic amphipods to oxygen deficiency 137

constant oxygen concentration of 0.3 mg O2 1-l (2.4 %) water types (artificial vs natural) or salinities (6.5%"vs in natural sea water for 3 d. 9%0). There was, however, a difference in survival In a third experiment, survival after 24 d at low oxy- between species, with Monoporeia affinis having a gen concentrations was measured for Monoporeia affi- higher survival rate (88 to 100 %) than Pontoporeia nis and Pontoporeia femorata. The oxygen concentra- femorata (64 to 96%), (ANOVA, F = 13.2, p < 0.001). tions studied (mean * SD) were 1 2 * 0.3 (10%), 2.0 * The 62 d survival rates for M. affinislikewise did not 0.1 (l7%),4.0 * 0.1 (33%), 6.0 2 0.1 (49%) and 11.7 rt differ significantly between natural (92%) and artifi- 0.2 mg O2 1-I (95%, continuously air bubbled). Ten cial (90%) sea water. beakers for each treatment, with 4 amphipods in each (-1200 m-2), were included. The experiment was con- ducted as described above, in tanks (250 X 40 X 20 cm) Tolerance to oxygen deficiency with artificial sea water. Effect of salinity on tolerance to oxygen deficiency. Pontoporeia femorata was significantly more sensi- Tolerance to a low oxygen concentration (0.2 mg O2 tive to a stepwise reduction in oxygen concentration 1-' = 1.6%) at slightly increased and decreased salini- (from 0.8 to 0.3 mg O2 1-l) than Monoporeia affinis ties was tested. Artificial sea water was used in tanks (2-factorial ANOVA, F= 33.3, p < 0.001). There was no with dimensions of 54 X 34 X 32 cm. The amphipods significant difference in survival between days, and no were acclimatised for 2 wk, without sediment, to salin- interaction between day and oxygen concentration ities of 4% 6.5% and 9%". For each species and salin- was found (Fig. 1).More than 70% of the initial num- ity, 18 beakers with 4 amphipods (-1200 m-2) in each ber of P. femorata were dead after 5 d, by which time were included in each experimental treatment. The the oxygen concentration had been reduced to 0.3 mg amphipods were exposed to the low oxygen concentra- O2 I-', whereas all M. affinis were still alive. All tion in the salinity of acclimation. The air-bubbled con- amphipods in the control groups (1 1.5 mg O2 1-I= 94 %) trol consisted of 6 beakers for each species, and salin- were still alive at the end of the experiment. Compari- ity and survival rate were determined at the end of the son between the experimental and control groups on experiment. Day 5 revealed a significant interaction between oxy- In a second test of tolerance to oxygen deficiency at gen concentration and species (ANOVA, F = 3.8, p < different sallnlties, the oxygen concentration was 0.01): P femorata in the low-oxygen treatment had a slightly higher, 0.6 mg O2 1-' (5Yo), and the salinities significantly lower survival rate compared with M. affi- tested were 5% 6.5"h and 9%. The artificial sea water nis in the low-oxygen treatment and both M. affinis and tanks used were the same as those described and P. femorata in the control (SNK). above. The amphipods were acclimatised for 2 wk to After 1, 2, 3, and 4 d of exposure to a constant con- the test salinities, without sediment. After the acclima- centration of 0.3 mg O2 1-' (2.4 % oxygen saturation) tion period, 20 beakers (for each species and salinity), mortality rates for Monoporeia affinis were 4, 20, 56 with 6 amphipods (-1800 m-2) each, were trans- ferred to the test tanks. The control consisted of ,w*------*------*------*------* 6 beakers for each species and salinity and had a constant supply of air. The control survival -. rate was determined only once, at the end of '5 80':...... , the experiment. 2 ..I. _..__...... _..... 1 ...... ,,, - Statistical methods. Results were statisti- '. ...,..__ cally evaluated using analysis of variance g m-- X (ANOVA). The multiple comparison test Stu- 8 - dent-Newman-Keuls (SNK) was used in cases g -,-M -- ,,,,,, where significant variation was found using the 7 40 --+--Pfmrata m +oxygen saturauon ANOVA, and the homogeneity of variance was 5 tested with Cochran's C-test (Winer et al. 1991). $ 2o .. -.2 .

RESULTS

Test of artificial sea water

Fig. 1 Pontoporeia femorata and Monoporeia affinis. Survlval rate Survival rates over 34 d for the 2 Species of [mean * SEM (standard error of mean)] after a stepwise decrease dur- amphipods did not differ significantly between ing 5 d from 0.8 to 0.3 mg O2 1-' 138 Mar Ecol Prog Ser 151: 135-141, 1997

oxygen treatment and 10.6 mg 0, I-' (86% oxygen saturation) in the control. More than 50% of both species had died after 24 h of exposure to nearly anoxic water at 0.2 mg O2 1-' (Fig. 3). NO significant differences were detected between species or salinities. When the control and oxygen-deprived groups were compared at salinities of 9OA and 6.5%, a 3-way interaction was found between oxygen concentration, species and salinity (F = 10.2, p < 0.01). All oxygen-deprived groups had a significantly lower survival rate than all control groups, and survival among the 1 2 4 6 12 control groups was (for reasons unknown) oxygen concentration rng 0, I-' lower for P. femorata at (SNK). In the next experiment, salinities of S%, Fig. 2. Pontoporeia femorata and Monoporeia affinis Survival rate (mean * 6.5%0 and 9% and an oxygen con- SEM) after 24 d of exposure to 1.2,2.0, 4.0, 6.0 and 11.7 mg O21-' centration of 0.6 mg O2 I-' (~O/V oxygen saturation) were used. The survival rate and 70% respectively. By contrast, all control (1 1.3 mg after acclimation was nearly the same for all salinities O2 I-' = 92% oxygen saturation) M. affiniswere still and both species (64 to 69% for Monoporeia affinis,56 alive at the end of the experiment, and their survival to 69 % for Pontoporeia femorata). The mean (+ SD) rates were significantly higher compared with the oxygen concentration in the experimental groups dif- group exposed to the low oxygen concentration at both fered only marginally between treatments and was not Day 3 and 4 (ANOVA, F= 10.8, p c 0.001, SNK). significantly differen.t; 5% = 0.64 rng O2 1.' (f0.04), 6.5% = 0.57 mg O2 1-' (kO 10), 9% = 0.58 mg O2 1-l (k0.03.). The statistical analysis (3-factorial ANOVA) Tolerance to long-term oxygen deficiency showed that P, femorata was s~gnificantlymore sensitive to oxygen deficiency than M. affinis(p < 0.001). For both species, survival rates at 1.2 mg 021-' (10% There was also a significant interaction between salin- oxygen saturation) were significantly lower compared ity and day (p c 0.05, Table 1, Fig. 4). M, affinissur- with those at the other concentrations after 24 d vived better than P femorata at all 3 oxygen levels and (ANOVA, F = 22, p < 0.001, SNK, Fig. 2). Monoporeia M. affinisexposed to a salinity of 9%asurvived better affinis was more tolerant than Pontoporeia femorata than M. affinisat 6.5% and 5%" in oxygen.-deprived (ANOVA, F = 127, p < 0.001). Lowest survival rate was found for P. femorata at 1.2 mg O2 I-', intermediate for M. affinisat 1.2 mg O2 1-' and P. femorata at 2, 4, 6 and 11.7 mg O2 1." and high- est survival for M. affinisat 2,4, 6, and 11.7 mg O2 1-' (SNK).

Effects of oxygen deficiency at different salinities

In the first experiment, Monoporeia affinisand Pontoporeia femorata were tested at salinities of 4% 6.5'A and

9%. At a salinity of 4%0, no results 24h d8h were obtained for P. femorata since it P fernorata did not survive acclimation. The mean Fig. 3. Monoporeia affinis and Pontoporeia femorata. Survival rate (mean oxygen concentration was 0.2 mg O2 SEM) after 24 and 48 h at salinities of 4O&. 6.5% and 9'Xm and oxygen concentra- 1-' 1.6% oxygen saturation) in the low- tions of 0.2 mg O2 1.' Control at 10.6 mg O2 I-' not shown. n.d.: no data obtained Johansson: Tolerance of Baltic arnph~podsto oxygen deficiency 139

Oday 1 periments M. affinis tolerated oxygen .day 2 deficiency better than P. femorata did. odsy 3 Since more active animals have a Qday U higher metabolic rate and greater en- mdsy 5 ergy requirements, they are normally more sensitive to decreases in oxygen concentration (review in Davis 1975). For example, a comparison of the 2 brittlestars Amphiura filiformis and Amphiura chiajei showed that A. chiajei, the species with t'he lower oxygen uptake, was more tolerant to oxygen deficiency (Rosenberg et al. 1991). 5% 65% 9 % 5 %D 65% 9 k M. affinis P. femorata Pontoporeia femorata has a lower respiration rate and is less active than Fig. 4. Monoporeia aff1nl.s and Pontoporeia femorata. Survival rates on Days 1 ~~~~~~~~i~ affinis (Cederwall 1979) 6.5% 9% O2 to 5 at salinities of 5%. and and an oxygen concentration of 0.6 mg and was therefore expected to be I-' Controls at 11.2 rng O2I-' not shown. 0 = no survival the more tolerant of the 2 species of amphipods. Another fact suggesting Table 1. Effects of the factors Species, Salinity and Day, and that P. femorata should be more tolerant of oxygen de- their interactions on the survival of Pontoporeia fernorata and ficiency is that, compared to M, affinis, it is found A/lonoporeia affjnis at 0.6 mg O2 1-l. ns: not significant deeper in the sediment, where oxygen concentrations tend to be lower (Hill & Elmgren 1987). However, it Effect F-value p-value turned out that M. affiniswas the more tolerant of the 2 species. M. affinisis a brackish-water species whereas Species 66.7 <0.001 Salinity 6.5 <0.01 P. femorata is a marine species (Segerstrale 1950, Dav 14.6 <0.001 1959), and brackish-water amphipods have been re- species X Salinity 1.9 ns ported to be more tolerant to oxygen deficiency than Species X Day 1.9 ns marine amphipods (Bulnheim 1979, Ritz 1980). The Salinity X Day 2.2 <0.05 salinity in the Asko area, where the amphipods were Species X Salinity X Day 0.6 ns collected, is about 6.5%0,close to the lower limit of survival for P. femorata. It was therefore of interest to determine whether salinity-related stress could explain treatments. Furthermore, the survival rate on Day 1 the lower tolerance to oxygen deficiency of P. was higher at a salinity of 9"A compared with survival fernorata, compared with A4. affinis. However, for as rates for each of the other 4 days and salinities. Sur- long as the amphipods survived the experimental vival rates in the high-oxygen treatment (56 to 690h salinity, there w7ere only minor effects of salinity on survival, 11.2 mg 0, 1-' = 91 % oxygen saturation) did their tolerance to oxygen deficiency. Other authors not differ significantly between species or salinities. have reported the tolerance of marine invertebrates to Furthermore, on Day 5, the control amphipods showed oxygen deficiency to be affected at decreased salinity, significantly higher survival than the amphipods with lower survival rates and earlier onset of impaired exposed to the low-oxygen treatment (ANOVA, F = physiological responses [Theede et al. 1969, Stickle et 125, p < 0.001). al. 1989, Kristoffersson & Kuosa 1990). Theede et al. (1969) suggested that euryhaline species are not affected by ].oweredsalinity as long as the critical sal.inity DISCUSSION limit is not reached. No significant effect of low salinity was detected in this study, even when P. femorata was In this study, Monoporeja affinis and Pontoporeia tested close to its lower tolerance limit of ~Yw. fenlorata tolerated low oxygen values in the same Generally, Pontoporeia femorata showed a lower range as those tolerated by other amphipods (Sprague survival rate than Monoporeia affinis in long-term 1963, Gamble 1970, Bulnheim 1979, Ritz 1980, Agnew experiments (natural vs artificial water and tolerance), & Taylor 1985, Agnew & Jones 1986, Nebeker et at even at higher oxygen concentrations, which is in 1992, Winn & Knott 1992, Maltby 1995). Mortality was agreement with previous laboratory observations below 50'4, for both M. affinisand P. femorata after 24 h (Johansson unpubl.). However, in short-term experi- exposure to nearly anoxic water (0.2 mg O2I-'). In 3 ex- ments, no difference in survival of control P. femorata 140 Mar Ecol Prog Ser 151. 135-141, 1997

and M. affinis was found, except for P femorata at 9%0, Acknorvledgements. I thank Lars Byren, Britt Stamfors and in the first salinity experiment. Barbro Soderlund for field and laboratory assistance, and In addition to Monoporeia affinis and Pontoporeia Ragnar Elmgren for comments on the manuscript. The Stock- holm Centre for Marine Research provided access to boat and femorata, the below-thermocline macrobenthic com- field station facilities. Th~sstudy was supported by the munity in the study area (near the Asko laboratory) in- Swedish Natural Science Research Councll and the Swedish cludes the bivalve Macoma balthica, the isopod Saduria Environmental Protc.ction Agencl . entomon, the priapulid Halicryptus spinulosus and the polychaete Harmothoe sarsi. Of these species, H. spinu- LITERATURE CITED losus is the most tolerant to oxygen deficiency, being able to withstand anoxia for as long as 60 d (Oeschger Abrarns P, Hdl C, Elmgren R (1990) The functional response 1990).M. balthica is also very tolerant to anoxia, as indi- of the predatory polychaete, Harmothoe sarsi,to the am- cated by a 50%~mortality rate after 52 d (Dries & Theede ph~pod,Pontoporeia affinis. Oikos 59:261-269 Agnew DJ, Jones MB (1986) Metabolic adaptations of Garn- 1974),whereas S. entomon can only withstand anoxia for marus duebeni Liljeborg (Crustacea, Arnphipoda) to about 10 d (Hagerman & Szaniawska 1988, Kristoffers- hypoxia in a sewage treatment plant. Comp Biochem son & Kuosa 1990). Few data are available on the toler- Physiol A 84:475-478 ance of H sarsi to low oxygen levels. In a pilot study, Agnew DJ, Taylor AC (1985) The effect of oxygen tension on the physiology and distribution of Echinogammaruspirlofi small individuals (0.5 to 1 cm) survived oxygen concen- (Sexton & Spooner) and E. obtusatus (Dahl) (Crustacea: trations below 0.2 mg O2 1-Lfor 2 d, but all were dead Amphopoda). J Exp Mar Biol Ecol87:169-190 after 4 d (Johansson unpubl. data). H. sarsi is, however, Andersin AB. Cederwall H. Gosselck F. Jensen JN, Josefsson an early recolonizer in areas affected by low oxygen con- A, Lagzdins G, Rumohr H, Warzocha J (1990) Second peri- centrations and, based on field data, considered to tol- od~~assessment of the state of the marine environment of the Baltic Sea, 1984-1988; Background document. Baltic erate such conditions fairly well (Andersin et al. 1978). Sea Environ Proc 35B:Zll-275 Thus the result here for the 2 amphipod species indi- Andersin AB, Lassing J, Parkkonen L, Sandler H (1978) The cated that they are the least tolerant to oxygen deficiency decllne of macrofauna in the deeper parts of the Baltic of the macrobenthic species in the region of interest. proper and the Gulf of Finland. Kieler Meeresforsch, Son- derh 4:23-52 In the Gulf of Finland, no amphipods were found Andersin AB, Sandler H (1991) Macrobenthic fauna and oxy- after an extended period with low oxygen concentra- gen deficiency in the Gulf of Finland. Memo Soc Fauna tlons, whereas after an increase in oxygen concentra- Flora Fenn 67:3-10 tion, they recolonized the area (Andersin & Sandler Aneer G (1975) Composition of the food of the Baltic herring 1991). Gaston (1985) reported similar results, with (Clupea harengus L.), fourhorn sculpin (Myoxocephalus quadricornjs L.) and eel-pout (Zoarces civiparus L.) from amphipod numbers markedly reduced at oxygen con- deep soft bottom trawling in the Asko-Landsort area dur- centrations below 2 mg O2 1-l. Such reductions may ing two consecutive years (1970-1972). Merentutkirnus- have further ecological consequences since amphipods lait Julk 239:146-154 in the sediment are probably responsible for much of Ankar S, Elmgren R (1976) The benthic macro- and meio- fauna of the Asko-Landsort area (horthern Baltic Proper). the bioturbation of the sediment. The deposit-feeding A stratified random sampling survey. Contrib Asko Lab amphipod Pontoporeia hoyi was capable of creating a Univ Stockholm 11:l-115 homogenised upper sediment layer (Robbins 1982). Baden SP, Loo LO, Pihl L, Rosenberg R (1990) Effects of This means that processes taking place at or near the eutrophication on benthic communities including flsh: sediment-water interface will be disturbed if the Swedish west coast. Arnbio 19:113-122 Bulnheim HP (1979) Comparative stud~eson the physiological amphipods die or become immobilised. In a review by ecology of five euryhal~neGammarus species Oecologia Krantzberg (1985), bloturbation affected the nitrogen 44:80-86 dynamics in the sediment by increasing nitrification Cederwall H (1979) Diurnal oxygen consumption and act~vity and denitrification rates. Thus the inhibition of denitri- of two Pontoporeia (Amphipoda, Crustacean) species. In: Nayior E,tidrtnoll RG (eds) Cyclic phenomena in marine fication could reinforce the effects of nutrient enrich- plats and arl~mals.Pergamon Press, Oxford, p 309-316 ment by allowing increased rates of NH,' recycling, as Cederwall H, f lmgren R (1980) Biomass increase of benth~c suggested by Kemp et a1 (1990). macrofauna demonstrates eutrophication of the Baltic Sea. Due to their normally high abundance and impor- Ophel~aSuppl 1.287-304 tance as prey for fish and invertebrates, as well as their Cederwall H, Elmgren R (1990) Biolog~caleffects of eutrophl- cation in the Baltic Sea, particularly the coastal zone. important contribution to biogeochemical cycling Ambio 19:109-112 through their bioturbating activity, the 2 studied Davis JC (1975) Minimal d~ssolvedoxygen requirements of deposit-feeding species of amphipods are central com- aquatlc Life with emphasis on Canadlan specles. a review. ponents of the Baltic benthic assemblage (Elmgren et J Fish Res Bd Can 32:2295-2332 de Jong VN, Boynton W, D'Elia CF, Elmgren R, Welsh BL al. 1990). The present study shows them to be particu- (1994) Responses to developments in eutrophication, in four larly sensitive to oxygen deficiency, with Pontoporein different North Atlantlc estuarine systems. In. Dyer KR. femorata being most susceptible. 01th RJ (eds)Changes Influxes In estuaries. 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This article was submitted to the editor A4anuscr1pt first received Novembe~7, 1996 Revised verslon accepted March 18, 1997