Bothnian Sea, Gulf of Riga, metabolic rates, amphipods, Boreal Environment Research, sedimentation, affinis, northern Baltic Sea, Lehtonen Monographs, nutritional conditions, Baltic Sea, SR5, food conditions, Gulf of Finland, population, nutritional condition, Bothnian Bay, study, Finnish Environment Institute, benthic, Fisheries Research Institute, amphipod, Air Pollution Prevention Association, metabolic changes, food availability, food avail, Lehtonen K.K., Population dynamics, observed, Finnish Water Association, Kari K. Lehtonen Ecophysiology, Hannu Lehtonen, Finnish Meteorological Institute, metabolic measurements, Lehtonen, Finnish organisations, Finnish Institute of Marine Research, Kari K. Lehtonen, Finland Lehtonen, environment, University of Helsinki
BOREAL ENVIRONMENT RESEARCH
The Boreal Environment Research is a new journal published by seven Finnish organisations: the Finnish Environment Institute, the Finnish Game and Fisheries Research Institute, the Finnish Institute of Marine Re search, the Finnish Meteorological Institute, the Air Pollution Prevention Association, the Finnish Limno logical Society and the Finnish Water Association. The journal is published quarterly, and in addition, monographs can be published quarterly, and in addi tion, monographs can be published irregularly in a subsidiary series Monographs of the Boreal Environ ment Research. SCOPE OF THE JOURNAL Boreal Environment Research is an international interdisciplinary journal publishing original articles. reviews and short commentaries devoted to studies of various aspects of the boreal environment and its natu ral resources in particular on environmental problems, their assessment, understanding and management, as well as on the sustainable use of natural resources
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to environmental sci ences, linking pressures via sources of pollution to the occurring in the various media. Articles dealing with monitoring, experimental, theoretical and modelling studies as well as their combination are all welcome. EDITORS-IN-CHIEF Prof. Hannu L.ehtonen Department of Limnology P.O. Box 27 FIN-00014 University of Helsinki, Finland
EDITORIAL BOARD Dr. Sylvain Joffre, Finnish Meteorological Institute Dr. Juha Kbmari (Chairmain in 996), Finnish Environment Institute Dr. Harri Kuosa, Finnish Institute of Marine Research Dr. Kari Larjava, Technical Research Centre, Finland Prof. Hannu Lehtonen, University of Helsinki Dr. Gцran Nordlund, Finnish Meteorological Institute Dr. Martti Rask (Chairman in 1997), Finnish Game and Fisheries Research Institute Dr. Kari Ruohonen, Finnish Game and Fisheries Research Institute Dr. Pertti Seuna, Finnish Environment Institute EDITORIAL OFFICE Finnish Zoological and Botanical Publishing Board, P.O. Box 17 FIN-00014 Helsinki, Finland SUBMISSION OF MANUSCRIPTS Four copies of the manuscript are to be sent directly to the appropriate Editor-in-Chief. Manuscripts related to aquatic, marine and fisheries sciences to Prof. Han nu Lehtonen, and those related to atmospheric and ter restrial sciences to Dr. Sylvain Joffre. Indicate clearly to whom the correspondence should be sent, and in clude the telefax number and, when available, the e mail address. On a separate sheet, submit a list of four qualified and unbiased referees with complete names and addresses.
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MONOGRAPHS OF THE BOREAL ENVIRONMENT RESEARCH 7 Kari K. Lehtonen Ecophysiology of two benthic amphipod species from the northern Baltic Sea FINNISH INSTITUTE OF MARINE RESEARCH, FINLAND Helsinki 1997
ISSN 1239-1875 ISBN 952-11-0217-9 Hakapaino Oy, Helsinki 1997
Ecophysiology of two benthic amphipod species from the northern Baltic Sea Kari K. Lehtonen Academic dissertation To be presented, with the permission of the Faculty of Science of the University of Helsinki, for public criticism in the lecture room of the Division of Animal Physiology (Arkadiankatu 7) on January 16th, 1998, at 12 o'clock noon.
List of original publications
2.1 The spec is investigated: general biology
2.2 The species in relation to their environment
2.2.1 Nutritional conditions
2.2.2 Role in benthic mineralization processes
2.3 The study objectives
2.3.2 Biochemical composition
2.4 The study areas
2.4.1 Deep, open-sea area: Bothnian Sea
2.4.2 Eutrophied, coastal area: Gulf of Riga
2.4.3 Deep, open-sea area: post-bloom study
3 Material and methods
3.2 Measurement techniques
3.2.1 Determination of metabolic rates
3.2.2 Biochemical measurements
3.2.3 Population data
3.2.4 Bioenergetic calculations
3.2.5 Mineralization of carbon and nitrogen
3.2.6 Bothnian Sea: sedimentation
4 Compilation of main results
4.1.1 Effects of short-term starvation
4.1.2 Effects of temperature on ammonia excretion
4.1.3 Seasonal and spatial variations
184.108.40.206 Bothnian Sea
220.127.116.11 Other areas: post-bloom study
4.2 Body composition
4.2.1 Seasonal and spatial variations
18.104.22.168 Bothnian Sea
22.214.171.124 Other areas: post-bloom study
4.3 Observations at population level
4.3.1 Mineralization of carbon and nitrogen
4.3.2 Bothnian Sea: pelagic-benthic coupling
126.96.36.199 Seasonal and interannual variations in population dynamics
188.8.131.52 Carbon requirements of the amphipod population in relation to primary
production and sedimentation
5.1 Specific physiological characteristics of the species studied
5.1.2 Body composition
5.2 Effects of environmental nutritional conditions on the physiological condition of the
5.2.1 Primary production and sedimentation in thc Baltic Sea
5.2.2 Spatial variability in the condition of the amphipods in relation to environmental
5.2.3 Bothnian Sea: the time-lag
5.3 Utilization of organic matter by the amphipods: a system-wide view
5.3.1 Bothnian Sea: requirements in relation to inpot
5.3.2 Mineralization of carbon and nitrogen
5.4 Population dynamics: observations and hypotheses
5.4.1 Factors affecting the life-cycle
5.4.2 Interspecific interactions
5.4.3 Intraspecific interactions
Ecophysiology of two benthic amphipod species from the northern Baltic Sea
List of original publications
This thesis is based on the following papers, which are referred to by their respective Roman numerals:
Lehtonen K.K. 1994. Metabolic effects of short-term starvation on the benthic amphipod Pon
toporeia affinis Lindstrцm from the northern Baltic Sea. J. Exp. Mar. Biol. Ecol. 176: 269-283.
Lehtonen K.K. 1995. Geographical variability in the bioenergetic characteristics of Mo
noporeia/Pontoporeia spp. populations from the northern Baltic Sea, and their potential contribution
to benthic nitrogen mineralization. Mar. Biol. 123: 555-564.
Lehtonen K.K. 1996a. Ecophysiology of the benthic amphipod Monoporeia affinis in an open-sea
area of the northern Baltic Sea: seasonal variations in body composition, with bioenergetic consid
erations. Mar. Ecol. Prog. Ser. 143: 87-98.
Lehtonen K.K. I 996b. Ecophysiology of the benthic amphipod Monoporeia affinis in an open-sea
area of the northern Baltic Sea: seasonal variations in oxygen consumption and ammonia excretion.
Mar. Biol. 126: 645-654.
Lehtonen K.K. Physiological condition of the amphipods Monoporeia affinis (Lindstrom) and Pan
toporeia femorata Krшyer as an indicator of variations in benthic nutritional conditions in the Gulf
of Riga (Baltic Sea). Submitted manuscript.
Lehtonen K.K. & Andersin A.-B. Population dynamics, response to sedimentation and role in ben
thic metabolism of the amphipod Monoporeia affinis in an open-sea area of the northern Baltic Sea.
Papers I-IV are reproduced by the kind permissions of Elsevier Science, Springer Verlag
Monographs of the Boreal Environment Research No. 7
Ecophysiology of two benthic amphipod species from the northern Baltic Sea 9 Ecophysiology of two benthic amphipod species from the northern Baltic Sea Kari K. Lehtonen Finnish Institute of Marine Research, P.O. Box 33, FIN-00931 Helsinki, Finland Lehtonen, K.K. 1997. Ecophysiology of two benthic amphipod species from the northern Baltic Sea. Monographs of the Boreal Environment Research No. 7, 1997. Abstract Seasonal and spatial variations in the physiological condition of two benthic, deposit-feeding amphipods Monoporeia affinis LindstrOm and Pontoporeia femorata Krшycr from different ar eas of the northern Baltic Sea were investigated by examining their biochemical composition (mainly lipids) and metabolism (mainly ammonia excretion). In addition, by combining the metabolic and population data, the potential of the amphipod populations to mineralize carbon and nitrogen was estimated. The main part of the thesis consists of an extensive seasonal study on M. affinis at a deep, open-sea station in the Bothnian Sea (1991-1993). A seasonal study was also carried out in the Gulf of Riga (1994-1995) at two shallower stations characterized by different environmental conditions
. To acquire a broader view of spatial variations, in May-June 1993 a "snap-shot' study was carried out at 12 open-sea stations that covered the Bothnian Bay, Bothnian Sea and Gulf of Finland. Prior to all of these, an experimental study focusing on the effects of starva tion on the metabolism of M. affinis was made to form an understanding of the impact of nu tritional conditions. The results of these studies show distinct physiological and biochemical responses to changes in environmental conditions by the amphipods, with sedimentation of the spring bloom triggering most of the changes observed. The physiological parameters studied were ob served to vary significantly both seasonally and spatially, indicating variability in the bioener getic strategy of amphipods inhabiting environmentally dissimilar areas, nutrition being the most important regulatory factor. The results from the Bothnian Sea implied a tight pelagial benthos coupling, i.e. production and sedimentation of organic particulate matter
and utiliza tion by amphipods. Nutrition-related density-dependency is regarded as being the prime cause of the long-term oscillations in amphipod populations observed in earlier studies. The role of benthic amphipods in the mineralization of organic matter was shown to be marked especially in open-sea areas with low-to-moderate sedimentation rates and high amphipod densities. Key words: Baltic Sea, benthic amphipods, biochemical composition, bioenergetics, lipids, me tabolism, mineralization, Monoporeia affinis, Pontoporeiafrmorata, population dynamics, sea sonal variation.
Monographs of the Boreal Environment Research No. 7
1 Background Throughout the history of Baltic Sea ecosystem re search, scientists have found themselves wandering too often in alleys of speculation over the physio logical characteristics of the studied organisms, seeking explanations for their findings at higher levels of biological organization. Although an abun dant number of basic ecological studies -- although often simply monitoring of the biomass and abun dance of organisms -- has been carried out in this area interest in examining the physiological charac teristics of organisms living in this exceptional envi ronment has been disappointingly low. Since physiological functions are the ones that really show us whether an organism is dead or alive, its level of activity, health, prospects of reproducing successfully, and potential gain of and effect on its environment, it is obviously of utmost importance to have basic physiological knowledge particularly of species that form the main components of the eco systems. Moreover, especially in connection with Environmental monitoring
, physiological and bio chemical parameters often come in handy as indica tors of the effects of changes in environmental conditions, provided they are interpreted in a sensi ble way. In the Baltic Sea, low species diversity is a char acteristic phenomenon, caused mainly by constantly low salinity (classically shown by Remane and Schlieper 1971). Due to this and other abiotic and biotic characteristics of the area, many researchers share a view of the Baltic Sea as a huge, unique pooi for scientific research. Certainly the physiological characteristics of organisms adapted to these condi tions tend to be rather special; this leads one to sus pect that knowledge on even closely-related species inhabiting true marine or limnic environments is not necessarily applicable to the organisms inhabiting the constantly brackish-water Baltic Sea. For practical reasons, the lack of physiological studies, especially with regard to the benthos, is most evident in the open-sea areas. However, inter esting phenomena that have not been explained by standard population analyses occur in these areas. Low diversity in the Baltic Sea simplifies food-web analysis and the study of many other biological in teractions. Under such conditions, knowledge of the physiology of a dominant species
in a study area can be very useful, especially in open-sea areas, because it can often be applied to large geographical area
s, not only to local communities
. In short, investigations of the ecological physiol ogy of certain, highly dominant species provides
valuable information about the functioning of the ecosystem in large geographical areas, as in the case of this study, the northern Baltic Sea. I was given an excellent opportunity to study the physiology of two amphipod species that dominate most open-sea soft bottoms of the northern Baltic Sea. I have tried not to waste this opportunity; the results and conclusions of my work are presented in this thesis. 2 Introduction 2.1 The species investigated: general biology The amphipods Monoporeia affinis (Lindstrdm) (formerly named Pontoporeia affinis; see Bousfield 1989) and Pontoporeia femorata Krшyer are domi nant members of the soft-bottom macrozoobenthic communities of the northern Baltic Sea (e.g. Seger strAle 1937, Ankar and Elmgren 1975, Elmgren 1978, Andersin et al. 1978, 1984). M. affinis is usually the dominant macrobenthic species, with densities reaching 10,000 md m 2 and more. Origi nally limnic, M. affinis survives in brackish water up to 7-8 % S. while the marine P. femorata is found in significant abundance only in >7% S. The two spe cies coexist in areas where the salinity is suitable to both. Because of their high abundance and specific biological characteristics, the amphipods form a most important link between the pelagic and benthic communities of the northern Baltic Sea, especially in open-sea areas. The amphipods feed mainly on organic detritus present in the surface layer of the sediment and on phytoplankton that reaches the bottom via sedimen tation. Both species are night-active, with M. affinis showing a higher swimming and metabolic activity than P. femorata (Cederwall 1979, Donner and Lindstrdm 1980). M. affinis also lives closer to the sediment surface (Hill and Elmgren 1987) and has a faster feeding rate than P. femorata (Lopez and Elmgren 1989). Both species are semelparous, usu ally reproducing in early spring. The life-cycle of M. affinis has been shown to vary markedly between locations and ranges from 1 to 4 years (e.g. Seger strAle 1937, Andersin et al. 1984, Leonardsson et al. 1988). The population densities and biomasses of both species show substantial spatial, seasonal and inter annual variations (e.g. Andersin et al. 1978, 1984, Sarvala 1986, Uitto and Sarvala 1991, Maximov 1997). Lake studies have revealed strong evidence of
Ecophysiology of two benthic amphipod species from the northern Baltic Sea 11
pelagic-benthic coupling, i.e. an interaction between the quantity and quality of algal blooms and the suc cess of benthic amphipod populations (Johnson and Wiederholm 1992, Fitzgerald and Gardner 1993); also, studies performed in shallow, coastal areas of the Baltic Sea show similar indications (Cederwall 1977, Elmgren 1978). Although comprehensive studies on the general biology of these amphipod species exist, their meta bolic and biochemical characteristics have received considerably less attention, with the exception of studies by Cederwall (1979) and Hill et al. (1992). Studies are available, however, on the metabolism of Diporcia spp. (formerly Pontoporcia hoyi [Bousfield 1989]), the North American
freshwater relative of M. affinis (Johnson and Brinkhurst 1971, Nalepa et al. 1983, Gardner et al. 1987, Gauvin et al. 1989). A typical feature for all the three amphipod species is their exceptionally high lipid content (e.g. Green 1971, Gardner et al. 1985a, b, Quigley et al. 1989, Hill et al. 1992). Since M. affinis and P. femorata are key components of the Baltic Sea benthos, fur ther knowledge of their physiology is essential to our understanding of their role in the ecosystem. 2.2 The species in relation to their environment 2.2.1 Nutritional conditions In open-sea areas, the nourishment of benthic de posit-feeders is largely dependent on autochthonous food sources. In contrast, in many coastal areas, the importance of allochthonous material may be sig nificant, but material that reaches the benthos in this way is usually of low quality (e.g. low nitrogen content
, refractory substances; e.g. Parsons et al. 1977) and not ideal food. As a result, the growth and overall bioenergetic strategy of benthic organisms in differerent sea areas are strongly influenced by geo graphically varying nutritional conditions. The nutritional quality
of the upper sediment layer is governed by both the quantity and quality of sedimentation input. In sub-boreal temperate waters, like the Baltic Sea, the major part of the annual sedimentation occurs during and slightly after the spring phytoplankton bloom, in open-sea areas within 5-6 weeks (e.g. Smetacek et al. 1978, Ku parinen et al. 1984, Leppдnen 1988). During the re mainder of the year the input is small (e.g. Jansson 1978, Andersson 1996). This pattern of sedimenta tion generates strong seasonal variability with re spect to the availability of good-quality nutrition for
benthic organisms, especially in areas where popu lations are dense and food resources become rapidly depleted. Furthermore, food availability is often strongly affected by inter- and intraspecific compe tition. Benthic organisms may confront periods compa rable to starvation due to the gradual depletion of food resources and deterioration of food quality. Capability to withstand nutritional stress is of crucial importance. Energy Storage
during food abundance and metabolic energy-saving adjustments triggered by food deficiency are mechanisms common to most organisms. Although immediate effects of poor nu trition are sometimes hard to recognize, the repro ductive potential of animals may become reduced and, eventually, the effects will be manifested at population level through a smaller amount of off spring and/or survival capacity of the young. 2.2.2 Role in benthic mineralization processes The fact that benthos plays an important role in the mineralization of organic particulate matter and in benthic nutrient dynamics has been acknowledged for a long time. As the dominant species of softbottoms in the northern Baltic Sea, M. affinis and P. femorata may have a significant influence on these processes, especially in areas of high population density
. Besides the direct mineralization of organic matter that results in the release of C2O and nutri ents, the strong bioturbation activities of benthic amphipods change the texture and chemical envi ronment of the top sediment layer, resulting in e.g. increased bacterial production (e.g. van de Bond et al. 1994). In this way amphipods may affect various benthic processes, e.g. the rates of nitrification and denitrification (e.g. PelegrI and Blackburn 1994, PelegrI et al. 1994). 2.3 The study objectives 2.3.1 Metabolism Oxygen uptake rate (I.;02) is a general measure of metabolic activity, while the ammonia excretion rate (lNH) implies protein catabolism; using their atomic equivalents, an index of physiological condi tion, the atomic O:N ratio can be obtained. At steady-state, the O:N ratio indicates the relative pro portion of protein used for energy production com pared to other main energy-yielding substrates, lipid and carbohydrate (e.g. Conover and Corner 1968,
Monographs of the Boreal Environment Research No. 7
review by Mayzaud and Conover 1988), and has been used for determining the physiological condi tion of various marine invertebrate groups, including amphipods (e.g. Pederson and Capuzzo 1984, Aarset and Aunaas 1990), mesozooplankton (e.g. Conover and Corner 1968, Mayzaud 1973, 1976) and bivalves (e.g. Bayne et al. 1985, Widdows 1978). In addition, metabolic rates can be used to estimate the potential of animal populations to mineralize organic matter. 2.3.2 Biochemical composition Gross biochemical composition (lipid, protein and carbohydrate), lipid class composition, and, more roughly, elemental composition (carbon and nitrogen) indicate the nutritional state, and the reproductive and survival potential of organisms. Spatially and seasonally differing environmental nutritional conditions are reflected in the body composition of animals, which must adjust their bioenergetic strategy to short- and long-term variations in food supply. Lipid accumulation is the most widespread long-term energy storage strategy in aquatic crustaceans. Lipid -- mainly triacylglycerols (TAG) -- has been shown to be the major energy storage component in M. affinis and P. femorata (Hill et al. 1992), and also in Diporeia spp. (e.g. Gardner et al. l985a,b, Gauvin et al. 1989, Quigley et al. 1989). Moreover, reproductive potential is largely dictated by lipid content since lipid is commonly used to the build-up of reproductive tissue and the formation of sexual products (e.g. review by Sargent and Henderson 1986, Gatten et al. 1980).
primary production and sedimentation, concentrated in the late spring - early summer period (VI). The metabolism (IV) and the gross biochemical and lipid class composition (Ill) of M. affinis were investigated to determine the effects of seasonal and interannual variations in food availability on their physiology and population dynamics. The contribution of the population to carbon and nitrogen mineralization in the benthic environment was esti mated by combining the metabolic measurements with population data (VI). Prior to these studies, an experiment was designed to study the effects of a short-term starvation period on the metabolism of M. affinis, in order to understand the responses of the amphipods to changes in food availability (I).
2.4 The study areas
2.4.1 Deep, open-sea area: Bothnian Sea The main part of this study was performed at a deep (125 m), open-sea station (Baltic Monitoring Programme Station SR5) in the Bothnian Sea (Gulf of Bothnia) (Fig. 1). The area is characterized by a seasonally constant near-bottom temperature range (2-5°C) and moderate rates of
Fig. 1. The study area: the northern Baltic Sea. Sea sonal studies were performed at stations SR5 (19911993), GR1 and GR5 (1994-1995); other stations were studied only in May-June 1993. · Monoporela affinis -dominated communities, 0 Pontoporeia femorata -dominated communities.
Ecophysiology of two benthic amphipod species from the northern Baltic Sea 13
2.4.2 Eutrophied, coastal area: Gulf of Riga A seasonal study to determine changes in the lipid content and NH of both M. affinis and P. femorata was carried out in the Gulf of Riga, a semienclosed subregion of the Baltic Sea (Fig. 1) (V). The gulf is heavily influenced by riverine input, the river Daugava being the main source of nutrients and particulate matter. A gradual eutrophication of the gulf during the past decades has been observed (reviewed in Ojaveer 1995), characterized by high levels of nutrients (Yurkovskis et al. 1993, KOuts and HAkansson 1995), primary production (Andruaitis et al. 1992, Tenson 1995) and changes in the zoobenthic community (Lagzdins et al. 1987). Both the nearshore (GR1: depth 28 m) and the offshore (GR5: 44 m) study stations exhibited seasonal fluctuations in near-bottom temperature (GRI: 0.3-12.0°C, GR5: 0.3-9.0°C) and oxygen conditions (GRI: 3.7-12.6 mg 02 l, GR5: 2.9-12.2 mg 02 l). Parallel population data by Yermakovs and Cederwall (in prep.) were used to estimate the contribution of the amphipod populations to benthic carbon and nitrogen mineralization. 2.4.3 Deep, open-sea areas: post-bloom study Soon after the sedimentation of the spring bloom, a "snap-shot" study was made to examine the lipid content and t>NH of 9 M. affinis and 3 P. femorata populations from different open-sea regions of the northern Baltic Sea, the Bothnian Bay, Bothnian Sea and Gulf of Finland (Fig. I) (II). The stations stud ied exhibited differing environmental characteristics, with depth ranging between 51 and 212 m, tempera ture between -0.1 and 4.2°C, and salinity between 3.4 and 8.0 %o (at the time of sampling). The three main subregions show marked differences in primary production (e.g. Lassig et al. 1978, reviews by Elm gren 1978, 1984) and probably also in sedimentation rates. The results obtained from the iNH meas urements were combined with population data to be able to estimate the contribution of the amphipod populations to benthic nitrogen mineralization at the time of sampling.
3 Material and methods 3.1 Sampling Sampling and measurements of metabolic rates were carried out aboard the nv "Aranda" of the Finnish Institute of Marine Research (FIMR), following, usually, the same procedure. van Veen grab samples were rinsed with cooled sea water and the am phipods were sieved gently upon a 0.5 mm mesh. The ampipods were transferred rapidly into the cold room, where they were kept in 15 1 aquaria contain ing aerated, filtered sea water and a 1.5 cm layer of fine, cleansed sand. The amphipods were kept in the dark at the experimental temperature (usually 4°C) for 1-3 days prior to metabolic measurements. The subsequent biochemical analyses were performed in FIMR laboratories. Sampling for the different stud ies was made as follows: -- I: Samples of M. affinis for the starvation experi ments were collected from the Bothnian Sea opensea station SR5 in March and June 1992. -- II: 12 stations in the Gulf of Finland, Bothnian Sea and Bothnian Bay were sampled for M. affinis and P.femorata during May-June 1993. -- III, IV, VI: seasonal samples of M. affinis were collected from the Bothnian Sea open-sea station SR5 on 17 occasions between January 1991-July 1993. -- V: seasonal samples of M. affinis (station GRI) and P. femorata (station GR5) were collected be tween April 1994-May 1995. For studying the ef fects of temperature on the tNH, additional sam ples of both species were taken at 3 open-sea stations in the Gulf of Finland and one in the Bothnian Sea (SR5) between May 1995-September 1996. In the Gulf of Riga, the Latvian vessels "Geofyzikis" and `Antonija" were also used for sampling. 3.2 Measurement techniques The techniques used are here described very briefly. detailed description
s of the methods are found in the papers indicated by Roman numerals.
Monographs of the Boreal Environment Research No. 7
3.2.1 Determination of metabolic rates After an acclimatization period of not less than 24 h, the amphipods were incubated for 12-24 h in 300-mi erleyenmayer flasks (2 CO , l?NH) (I, IV) or 25-mi liquid scintillation vials (\;NH) (I, II, V). Changes in oxygen and ammonia concentrations were deter mined using a modified Winkler method and the phenol-hypochiorite method of SolOrzano (1968), respectively. Weight-specific metabolic rates were calculated after the lyophilization and weighing of the experimental specimens. 3.2.2 Biochemical measurements The lyophilized individuals were homogenized and analyzed for total lipid using the method of Gardner et al. (1985a). Lipid classes were determined using TLC-FID (latroscan analyzer) (II, III, V). In the Bothnian Sea study, protein (Bradford 1976), and carbon and nitrogen (Heraeus CHN analyzer) were also determined (III). 3.2.3 Population data Population studies were carried out simultaneously with the determination of metabolic rates and bio chemical composition. The population sample
s (usually 5 Box Cores) were stored in 5% hexamin buffered formalin for 3 months prior to analysis. After counting, the body length and the wet and dry weights of the individuals were recorded (II, V. VI).
3.2.5 Mineralization of carbon and nitrogen Weight-specific excretion and respiration rates, de termined for individuals representing 1-mm length classes, were multiplied by the number of the indi viduals in each respective length class (II, V, VI). The metabolism of the whole population was calcu lated by summing-up the values of all length classes. Daily mineralization rates of the amphipod popula tion were obtained by linear interpolation between the metabolic rates measured at each sampling date; periodic (monthly, annual) values were obtained by summing daily values for the interval desired. 3.2.6 Bothnian Sea: sedimentation In the Bothnian Sea, sedimentation during 1991 and 1993 was measured by using an automated, funnelshaped multisample trap, moored at sampling station SR5 at the depth of 80 m (VI). The data obtained were used in the estimation of the proportion of de posited carbon and nitrogen assimilated by the local M. affinis population. The measured sedimentation rates, as well as parallel data on primary production at the study station in 1991 (Andersson et al. 1996), were interpolated linearly over the annual study pe riods, and periodical totals of production and sedi mentation (annual, monthly) were obtained from the daily rates. 4 Compilation of main results
3.24 Bioenergetic calculations In the Bothnian Sea study (III, IV), metabolic and biochemical parameters were converted to energy equivalents (Gnaiger 1983, Elliott and Davison 1975, Winberg 1971). Daily energy consump tion/accumulation rates were determined for a meansize individual from each annual cohort. Changes in these rates, due to growth and seasonal variability of the parameters in the equations describing metabolic rates (IV), were taken into account by applying lin ear interpolations of each parameter between each sampling date. Daily growth rates and the subse quent changes in the content of specific biochemical components (accumulation and depletion rates) were obtained in a similar way.
The results of the studies are presented here as a brief compilation only. An excessive use of numeri cal values has been avoided; for greater details, please consult the respective papers indicated by Roman numerals.
4.1.1 Effects of short-term starvation
During the course of the 8-d experiments M. affinis
showed a relatively small decrease in
pared to the reduction in CNH (I). Compared to the
June experiment, the amphipods in the March ex
periment showed low I)NH already at the start of
the experiment. In both of these experiments, the
Ecophysiology of two benthic amphipod species from the northern Baltic Sea 15
changes observed in metabolic rates resulted in ele vations in the O:N ratio, indicating a shift into more lipid-based metabolism as starvation progressed. Handling stress had a significant effect on the which was always highest immediately after sampling. In the Gulf of Finland population (LL4a; Fig. 1), the excretion rate measured directly after sampling was about twice higher than that recorded after keeping the amphipods for 4 h in the labora tory, and the rate remained stable after 24 h. How ever, following stabilization, the NH remained strikingly lower in amphipods collected from the Bothnian Sea station (SR5) compared to those col lected from the Gulf of Finland and Bothnian Bay (CVI). The estimated O:N ratios indicated lipiddominated energy metabolism in the Bothnian Sea population, while the catabolism of protein was more marked in the animals from the Gulf of Fin land; in the Bothnian Bay animals, the O:N ratios were intermediate. 4.1.2 Effects of temperature on ammonia excretion The magnitude of the effect of temperature elevation (from 4°C to 12°C) on the INH of the amphipods appeared to depend on the level of excretion at 4°C (V). For P. femorata the lowest temperature coeffi cient Q 10 (1.15) was recorded at station GF2 (Gulf of Finland) at a time of very high .)NH at 4°C, while the highest coefficient (2.80) was recorded at station GR5 (Gulf of Riga), the t)NH at 4°C being half that recorded at station GF2. For M. affinis, the highest coefficient (3.93) was found at station JML (Gulf of Finland) during low "ambient" t'NH, and the lowest (2.21) at the same station during a highexcretion period.
4.1.3 Seasonal and spatial variations
184.108.40.206 Bothnian Sea
For the early-summer period, in M. affinis an overall
increase in l.O2 of 22% was observed, but over
shadowed by dramatic increase in
higher than for the winter-spring period (Fig. 2)
(IV). During each of the three study years, the peak
of VNH occurred in the early summer, while inWINTER AND SPRING
the rate was extremely low. Due to
this high variability, combined seasonal (`NH vs.
dry weight data showed poor correlation. In general,
the gravid females showed a significantly higher
weight-specific NH compared to juveniles (non
mature individuals). The O:N ratios indicated that
M. affinis relied heavily on lipid for metabolic en
ergy production during most of the year, except in
early summer when the utilization of lipid and pro
tein was almost equal. Furthermore, the results indi
cate the existence of a time-lag between the
sedimentation of the phytoplankton bloom and the
metabolic response of the amphipods.
To examine the potentially biasing effect of sea
sonal changes in body composition on weight-spe
cific metabolic rates, biochemical data (III) were
employed to scale the /02 against the amount of
specific body constituents (protein, nitrogen, "non-
lipid dry weight"). In most cases, elevations in the
slope (b) of the allometric respiration (R) equations
(R=a . weightb) were observed, indicating a shift to
more size-independent metabolic rates (IV). Com
pared to the winter-spring period, however, the
higher level of t2 O observed during the May-Sep
tember period was evident irrespective of the weight
parameter used. The use of different weight parame
ters did not improve the poor
vs. weight cor
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limol N 1 Hindd 0.08
0 J F MA M J JASON D J FM
GAl GR5 SR5 (1991) SR5 (1992) SR5 (1993)
--U- -R- -0-
Fig. 2. Monoporela affinis and Pontoporeia femorata. Seasonal and spatial variations in ammonia excretion rate. The rates have been calculated for a 1 mg dry wt individual, using the metabolic scaling exponent 0.75. The data from the Bothnian Sea station 5R5 comprises measurements from 3 years (January 1991-July 1993). The Gulf of Riga stations (GR1 & GR5) were studied between January 1994 - May 1995; measurements performed in May 1995 have been incorporated to the curve between April and July 1994. G=gravid females, M=males. Adapted from papers (V and V.
220.127.116.11 Gulf of Riga At the nearshore station GRI, the `NH of M. of finis was slightly elevated in early May after the spring bloom, while at the offshore station GR5 sea sonal variation in the INH of P. femorata was not significant (Fig. 2) (V). Compared to M. affinis at station GRI, P. femorara at station GR5 had con stantly a significantly higher tNH. The gravid fe males of both species, as well as male P. femorata caught at station GR5 showed a significantly higher 1NH compared to juveniles. Dry weight vs. regressions proved to be non-significant for M. af finis, but data on P.femorata indicated that INH is weight-dependent although the correlation was not strong.
18.104.22.168 Other areas: post-bloom study Substantial variability in the excretion rates of the amphipods was observed to exist between the study regions. In theM. affinis populations of the Bothnian Sea the ` 1 NH was virtually identical at the 4 sta tions studied (II). In the eastern Gulf of Finland and the Bothnian Bay the tNH was almost twice that found in the Bothnian Sea. Regression analyses showed that the weight-specific INH of M. affiuzis was not dependent on spatial differences in dry weight, lipid level or neutral-to-polar lipid (NL:PL) ratio. At the Gulf of Finland stations LL6a and LL1 1, P. feniorata populations exhibited excretion rates close to those measured for M. affinis in the
Ecophysiology of two benthic amphipod species from the northern Baltic Sea 17
eastern Gulf of Finland and Bothnian Bay; however, the population at station LL9 showed a significantly lower rate. 4.2 Body composition 4.2.1 Seasonal and spatial variations 22.214.171.124 Bothnian Sea Seasonal changes in the biochemical composition of M. affinis at station SR5 (III) were closely coupled with the growth dynamics of the species at this loca tion (see below) (VI). During 1991-93, the lipid level (% dry wt) of the amphipods varied between 15-45% and showed both seasonal and interannual variation (Fig. 3). The lowest lipid levels always occurred in March-April, while rapid accumulation was recorded between late May and mid-June, with levels peaking in August-September. Accumulation rates of lipid were generally high in June-August, but the "net lipid balance" (accumulation minus de pletion) turned negative towards the late autumnwinter period. Gravid females had characteristically lower lipid levels (15-20%) compared to juveniles. Upid(%ofdrywt)
Triacylglycerols (TAG) were always the major lipid class (67-95% of total lipids), their levels corre lating significantly with the levels of total lipid and carbon. The phospholipid fraction comprised be tween 4-23% of the total lipid measured and each of the other lipid classes (free fatty acid
s, ster ols/diacylglycerols and acetone-mobile polar lipids [mostly pigments and glycolipids)) less than 7%. The NL:PL ratio was low in the spring and early summer, peaking between late summer and early autumn. The ratio was invariably higher in the 2+ year-olds compared to the I + year-olds, while, in general, the gravid females had a low NL:PL ratio. Protein comprised 17-29% of body dry weight, varying mainly according to season but also because of interannual variability in body size. Carbon (3356%) and nitrogen (5-9%) levels closely followed the seasonal patterns of the lipid and protein levels, respectively. The molar C:N ratio peaked in AugustSeptember; the ratio was lowest in April 1991, while in March-May 1992 and 1993 it was markedly higher, coinciding with higher lipid levels. As ex pected, the C:N ratio correlated significantly with the lipid:protein ratio. The gravid females showed a lower C:N ratio in comparison with the juveniles. Development of the energy content (J ind) in
0 J F MA M J JASON D J FM
GR1 GR5 SR5 (1991) SR5 (1992) SR5 (1993)
--U-- --- --0--
Fig. 3. Monoporela affinis and Pontoporeia femorata. Seasonal and spatial variations in lipid levels in individuals representing the reproducing generation in each study location. The data from the Bothnian Sea station SR5 comprises measurements from 3 years (January 1991-July 1993). The Gulf of Riga stations (GR1 & GR5) were studied between January 1994-May 1995; measurements performed in May 1995 have been incorporated to the curve between April and July 1994. G=gravid females. Adapted from papers Ill and V.
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mean-size individuals representing the different an nual cohorts showed similar seasonal patterns; interannual variations were due to the differences in the size of the individuals (VI). As might be expected when examining the observed, changes in lipid lev els, the energy value (J m 1 )g of the body matter showed seasonal and also interannual fluctuations, with the highest values in late summer (28.2 J mg') and lowest in spring (22.5 J mg). The energy value of the 1+ year-olds was invariably lower compared to the 2+ year-olds, until the latter entered the repro ductive phase. Bioenergetic calculations based on metabolic rates and changes in body composition showed that, during the winter-spring period, a sub stantial amount of metabolic energy is obtained by the combustion of body matter, mainly lipid. 126.96.36.199 Gulf of Riga In 1994, the maximum lipid level (36%) attained by M. affinis at the nearshore station GR1 in summer significantly reduced by November (21%) (Fig. 3) (V). Lipid balance calculations confirmed that the amphipods at station GRI did not accumulate lipid during that period. Ovigerous or gravid females continued to deplete lipid at a high rate, exhibiting extremely low lipid levels in March 1995 (9%). The population exhibited a 2-year life-cycle; after the spring bloom, the lipid level of the forthcoming re producing generation (cohort born in 1994) was al ready greatly elevated in early May 1995 (37%). In P. femorata at offshore station GR5, the de cline in the mean lipid level between July and No vember 1994 was considerably less (from 37 to 30%, Fig. 3). The lipid balance was positive throughout the autumn, only turning negative between gravity and the release of offspring. The forthcoming repro ducing generation (also having a 2-year life-cycle) showed moderate lipid levels in January and March 1995 (27%), but a sharp increase after the spring bloom in early May (37%).
The levels of TAG were constantly higher in P. femorata at station GR5 (seasonal range: 63-81%) compared to M. affinis at station GRI (44-73%), while the proportions of phospholipids were 11-22% and 18-38%, respectively. 188.8.131.52 Other areas: post-bloom study In M. affinis the lowest total lipid levels were re corded for both Bothnian Bay populations (mean 15%) (II). Individuals at the four Bothnian Sea sta tions showed higher levels (34%) than the three Gulf of Finland populations (24%). In the Gulf of Finland, P. femorata at station LL6a, despite being very large, had a lower lipid level (23%) than individuals from stations LL9 and ELI 1 (29%). The highest TAG levels were recorded in M. af finis at stations SR5 (Bothnian Sea) and F42 (Gulf of Finland) (mean 85%), while the amphipods at both Bothnian Bay stations had the lowest levels (54%). The NL:PL ratio was significantly dependent on the lipid level and dry weight of the individuals. In P. femorata the lipid class composition was similar at the three Gulf of Finland stations studied, with lower TAG levels (76%) compared to M. affmnis (except for M. affinis collected from the Bothnian Bay). 4.3 Observations at population level 4.3.1 Mineralization of carbon and nitrogen At the Bothnian Sea station SR5 the annual carbon mineralization potential of the amphipod population was 5-10 times higher than at the Gulf of Riga sta tions GRI and GR5 (Table I) (V, VI). With regard to nitrogen the release rates between the two subre gions were more similar, although the difference between 1991 and 1992 at station SR5 was about 2fold. In the post-bloom study, highly variable daily rates were recorded in the different study areas (II).
Ecophysiology of two berithic amphipod species from the northern Baltic Sea 19
Table 1. Monoporela affinis and Pontoporeia femorata. Mineralization potential of different amphipod popula tions. Rmjn and Rm = minimum and maximum daily mineralization rates during the year. Adapted from pa pers V and VI.
Daily rate mg C m 2
Annual total g C m 2
Daily rate j.tmoI NH m 2 R 111
Annual total mmol NH m 2
M. affinis SR5 1991* SR5 1992* SR5 1993** GRI l994*** P. femorata GR5 1994***
*Jan 15-Jan l4nextyear **Jan 15 1993 - Jul 28 1993 ***Dec 15 1993 - Jan 5 1995
4.3.2 Bothnian Sea: pelagic-benthic coupling 184.108.40.206 Seasonal and interannual variations in population dynamics During each study year the period of rapid growth commenced some weeks after the start of the spring bloom sedimentation and continued until autumn (VI). From late autumn to spring the growth of in dividuals ceased completely. Interannual differences between cohorts born in different years were ob served. The most marked differences in individual mean weight were observed in the gravid ca. 3-yearolds and 2+ year-olds collected in winter-spring of 1991 and the corresponding year-classes sampled in 1992 and 1993, which were twice the weight. The highest biomass values of the population occurred always in autumn and the lowest in spring. Further more, the abundance and biomass of the population showed a clear decreasing trend between 199 1-1993. 220.127.116.11 Carbon requirements of the amphipod population in relation to primary production and sedimentation At the Bothnian Sea station SR5 in 1991, the inten sive period of primary production occurred in AprilMay (Andersson et al. 1996), while sedimentation peaked slightly after; by early June about 90% of the annual carbon sedimentation had reached the bottom
(VI). A gradual reduction in the nutritional quality of the settling material was observed towards autumn. Of the annual primary production (105 g C m 2 ), an amount of carbon corresponding 17.5% was found sedimented in the 80 m trap. During the "active period" of sedimentation and amphipod growth (April 15-July 14), 20.5% sedimentation of the carbon produced occurred. In 1993, during the "active period", the organic material
deposited was ca. 50% less than in 1991. Using the data on primary production in 1991, the M. affinis population was calculated to have as similated 17.5% of the pelagially produced carbon. With specific regard to the "active period" (April 15July 14), a proportion of 10.2% was calculated. In both 1991 and 1993, during the "active period", about 50% of the sedimented carbon was calculated to have been assimilated by amphipods. The produc tion-to-respiration ratio (as carbon equivalents) dur ing this period was significantly higher in 1991 (1.23) compared to 1992 (0.46) and 1993 (0.58), indicating a significant allocation of food energy to growth in 1991. 5 Discussion Depending on area, season and even the year of sampling, the two amphipod species studied exhibit distinct variability in their metabolic rates and body composition. In the following sections these results
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are discussed in view of metabolic physiology, en ergy allocation, effect of environmental conditions and, ultimately, the population dynamics of the spe cies especially with respect to previous observations on the long-term oscillations in the populations M. affinis from the Bothnian Sea. Since the Bothnian Sea M. affinis population at station SR5 was studied more intensively than the others, with more information available on local environmental nutritional factors, the emphasis of the discussion is on the biology of this population. However, the studies performed in other areas, es pecially in the Gulf of Riga, provide excellent pos sibilities to compare amphipod populations inhabit ing areas characterized by different environmental conditions. 5.1 Specific physiological characteristics of the species studied 5.1.1 Metabolism The starvation experiments indicated that, after sampling stress has been overcome, food deprivation causes M. affinis to rapidly shift its metabolic bal ance towards lipid utilization, observed as marked elevations in the O:N ratio during starvation due to a decline in the Nl-I (I). Under low-nitrogen food conditions, a similar nitrogen-conserving metabolic strategy has been observed in the amphipod Callio Pius laeviusculus (Pederson and Capuzzo 1984). Nitrogen release rate appears to coupled with the nutritional state of the amphipods; this is a point of great interest in regard to the objectives of the whole study. Immediately after or some hours following col lection, M. affinis expressed a high tNH; a similar phenomenon is common in a number of inverte brates with different ecological niches and life strategies, including bivalves (Bayne and Scullard 1977), ctenophores (Kremer 1982), copepods (Le Borgne 1979), chaetognaths (Szyper 1981) and bur rowing amphipods (Hawkins and Keizer 1982). The high excretion rates observed are probably caused by increased metabolic demands during stress (e.g. Skjoldal and BAmstedt 1977). However, since the capturing procedure and maintenance conditions were identical throughout this research, stress cannot account for the disparity between the different study areas and seasons. In conclusion, the observed "station-and-season-specific" levels of 1NH (I, II, IV, V) must derive from (1) differences in the
amount of body energy reserves and/or (2) recent feeding history. In general, the excretion rates measured for M. affinis and P. femorata (I, II, IV, V) were lower than those measured for other benthic (e.g. Crangon sp.: Nelson et al. 1979, Regnault 1984, 1986, review in Regnault 1987) and pelagic (e.g. Conover and Cor ner 1968, Mayzaud 1973, 1976, Ikeda 1977) crusta ceans. The O:N ratio of M. affinis is strikingly high during most of the year compared to other benthic crustaceans (e.g. Pederson and Capuzzo 1984, Chapelle et al. 1994), indicating extensive use of substrates other than protein for energy production. The results imply, however, that P. fernorata has a higher excretion rate than M. affinis (II, V); further more, the excretion rate of P. feniorata seems to be less affected by changes in nutritional and tempera ture conditions (V). Despite these interspecific dif ferences, the catabolism of body protein seems to play a secondary role in the production of metabolic energy in both species, although seasonal variation in the LNH can be very marked (IV). It is interest ing to note that carnivorous feeding in aquatic crus taceans is usually associated with a high 1NH (Ikeda 1977, Blaika et at. 1982, Gaudy and Boucher 1983, Pederson and Capuzzo 1984). The low 1NH observed in M. affinis and P. femorata may signify that these amphipods are feeding mainly on material of plant origin. Controversy has surrounded the question of whether the t>NH of crustaceans depends on the availability of food (Conover and Corner 1968, Takahashi and Ikeda 1975, Ikeda 1977) or not (Gardner and Paffenhofcr 1982, Miller and Landry 1984). Some experimental studies have indicated that the excretion rate of benthic invertebrates is regulated predominantly by endogenous processes rather than by the quantity or quality of food (Hawkins and Keizer 1982, Gardner et al. 1983). In the present study cessation of feeding was not exam ined, but it is unlikely to be the cause of the reduced .)Nl-f observed in juvenile M. affinis during the autumn-winter period (IV). A more likely explana tion is in the quality or source of food, combined with increased utilization of reserve lipid for meta bolic needs. It is evident that differences in existing body energy reserves by themselves can invoke dif ferent physiological responses to varying feeding conditions, e.g. when lipid reserves fall below a certain threshold, protein catabolism will intensify. It has been claimed that sexually maturing Di poreia spp. stop feeding (Moore 1979, Quigley 1988, Quigley et al. 1989). Current bioenergctic studies do not, however, support this view with re
Ecophysiology of two benthic amphipod species from the northern Baltic Sea 21
gard to M. affinis, since their basic metabolic needs are not met by the combustion of body reserves alone (Ill). The elevated tNH recorded in gravid females of both species (IV, V) seems characteristic for this life-stage. Subsequently, the gravid M. af finis showed considerably lower O:N ratios com pared to juveniles in the same weight range or sea son (IV). It is apparent that the type of metabolic substrate utilized by the gravid females is deter mined by the amount of lipid reserves which reflect the long-term nutritional condition of the individu als. Compared to juveniles (V, observed also in male M. affinis [Lehtonen, unpublished data]) male P. frmorata showed a significantly higher t)NH. This is most likely a result of a general increase in activ ity, as males, following maturation, actively seek females (Segerstrвle 1937). Compared to the present studies, the somewhat higher iNH recorded in Lake Michigan for Di porcia spp. (Gardner et al. 1987, Gauvin et al. 1989) may, besides interspecific differences, be caused by osmoregulative adaptation, since crustaceans have been noted to increase excretion rates when trans ferred to lower salinity (Nalepa et al. 1983, Regnault 1984, Aarset and Aunaas 1990). However, in the salinity range of the present study stations (3.4-8.0 %o), the differing excretion rates observed cannot be explained by salinity (II, VI, V). It should be born in mind that, in the northern Baltic Sea, the marine P. femorata lives at the very limits of its salinity toler ance and its excretion rates may be affected by sa linity stress. At the deep Bothnian Sea station SR5, the tem perature remained practically at steady-state throughout the year (IV), and could not possibly be the cause of the observed metabolic changes in M. affinis. In the other deep areas studied, despite con siderable differences in depth, the ambient tempera tures were low at all stations at the time of sampling, with no logical correlation with the variable excre tion rates observed (II). Furthermore, at the Gulf of Riga station GR1, an increased t)NH in M. affinis was recorded in May, at a time of low temperature (2.9°C) (V). In conclusion, seasonal changes in tem perature do not provide an explanation for the ob served metabolic changes. In view of the above discussion on the potential abiotic factors, it is clear that the metabolic changes observed are a manifestation of increased feeding, activity and growth of the amphipods in response to the sedimentation pulse which reaches the bottom in late spring (IV, V). An elevation in O2 in response to food availability has been observed in crustaceans (e. g. Pederson and Capuzzo 1984, Torres et al.
1994) and is very likely caused by the so-called specific dynamic action (Kiшrboe et al. 1985). How ever, regarding the nitrogen excretion of M. affinis, seasonal variations in rates were less marked in the Gulf of Riga than in the Bothnian Sea (IV, V). Inter estingly, Gardner et al. (1987) did not register any effects of the sedimentation of the spring bloom on the t'NH of Diporeia spp. in Lake Michigan. These geographical dissimilarities between populations strongly suggest that it is environmental nutritional conditions that regulate the metabolic rates of these benthic amphipods; however, a straightforward in terpretation is bound to be invalid without a detailed examination of the prevailing nutritional conditions. Differences in the feeding history of the am phipods appears to regulate also the magnitude of the effect of elevated temperature on I.)NH (V). Furthermore, the effect of temperature on was, in general, more pronounced for M. affinis than for P. femorata, suggesting that the latter species is more capable of regulating its excretion rate as tem perature rises. The level of excretion by P. femorara at 4°C is usually higher than that of M. affinis (II, V). The advantages of this kind of metabolic strat egy with respect to adaptation are difficult to evalu ate without more detailed experimentation, but are probably linked to the earlier observations of behav ioural and physiological differences between the two species (e.g. Cederwall 1979, Lopez and Elmgren 1989). Assuming that Q 10 for t20 would remain close to 2.0, the practically temperature-independent iNH ( 1 =lQ .0 l5, V) recorded for P. femorata dur ing a high-excretion period would result in an ele vated O:N ratio following a temperature increase
, indicating a shift into a more lipid-based energy metabolism. ForM. affinis the Q 10 for iNH ranged between 2.2 and 3.9 (V), indicating that a tempera ture elevation increases the immediate use of protein for metabolic energy. Apparently, the two am phipods species have different capabilities for modifying their bioenergetic strategy, and, subse quently, differing modes of adaptation to varying temperature and nutritional conditions. To sum up the metabolic studies, the effects of nutritive factors on the metabolic rates and the qualitative utilization of body reserves arc evident. Since the tNH of the amphipods indicates the more-or-less recent feeding history of the individu als, it reflects the nutritional conditions prevailing in the benthic environment. Thus the recorded changes, especially in the NH , are useful indicators of both abundance and lack of good-quality food.
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5.1.2 Body composition As stated earlier, a high lipid level is the striking biochemical feature in M. affinis, P. fernorata and Diporcia spp.. Over all the other body constituents measured here, the accumulation of lipid deserves most attention, since it clearly reflects the nutritional condition of the amphipods and plays a vital role in reproduction. The seasonal range in the lipid levels (17-45% including gravids) of the reproducing 2+ year-olds of the Bothnian Sea open-sea M. affinis population (III) was different from that recorded for the species at the Gulf of Riga nearshore station GRI (9-36%) (V). Also, both ranges were considerably wider than that reported by Hill et al. (1992) from a coastal popula Lion in the Askц area. The maximum levels equal levels measured in Lake Michigan for Diporeia spp. (Gardner et al. l985a,b, Gauvin et al. 1989). In con trast, in the Bothnian Bay, very low lipid levels (15%) were recorded in early June (II). Regarding lipid class composition, a similar kind of spatial variability was observed in the proportions of differ ent lipids (II, III, V). In the Bothnian Sea, TAG levels were always 70% of total lipids, but at the Gulf of Riga nearshore station GRI, TAG levels were 45-73%. In a coastal Asko area, Hill et al. (1992) recorded almost equal proportions of TAG and phospholipids in M. affinis in the spring. Evi dently, substantial spatial and seasonal variation in the lipid dynamics of the species exist; these differ ences are likely to be caused by varying nutritional conditions and have, most likely, a direct effect on the bioenergetic strategy and reproductive potential of the species. The high O:N ratio (>200) observed in M. affinis in winter-spring indicates an almost exclusive utili zation of lipids for energy production during the pe riod (I, III). Bioenergetic calculations (III) demon strated that, although growth had completely ceased (VI), M. affinis obtained energy from the environ ment also during the winter-spring period. In the open-sea area of the Bothnian Sea, high lipid (and especially TAG) level is serving as a means for sur viving long-lasting poor food conditions. The fe cundity of the individuals was observed to be lower than in coastal areas (VI; Cederwall 1977, Sarvala 1986); clearly, a trade-off between survival during unfavourable periods and high reproductive potential seems to be in effect in this strongly food-limited area (VI). The maximum lipid levels (37%) in P. femorata at the Gulf of Riga offshore station GR5 were sig nificantly higher than those recorded previously for this species (II; Paradis and Ackman 1976, Hill et al. 1992). Furthermore, excluding the gravid females,
the seasonal range in the lipid levels was rather nar row (27-37%). The lower lipid levels recorded for P. feniorata suggest that the species has a different bio energetic strategy by comparison to M. affinis (Hill et al. 1992, III). This is corroborated by observations on some other biological characteristics (e.g. Cederwall 1979, Lopez and Elmgren 1989). The Gulf of Riga study, however, shows that, under advanta geous food conditions, P. feniorata is capable of attaining high lipid and TAG levels, i.e. close to those recorded for M. affinis. The positive lipid bal ance recorded at station GR5 between July and No vember is even more distinct than that recorded for M. affinis at the Bothnian Sea, and dramatically dif ferent from the zero-or-negative lipid balance of M. affinis at station GRI (III, V). This shows that food availability plays a crucial role in determining the physiological condition of both species. The poten tially significant role of inter- and intraspecific com petition for food is discussed later. In most aquatic crustaceans the production of eggs is related to the lipid content of individuals (e.g. Clarke et al. 1985); in some cases, the relation between lipid mass and body size ("target size" of reproduction) is a triggering factor for the onset of the reproductive phase. In Bothnian Sea M. affinis, the lipid and TAG levels of the non-reproducing 1ч year-olds were always only slightly lower than that of the 2+ year-olds entering the reproductive phase (III). This implies that a high lipid level in M. affinis does not necessarily lead to the onset of reproduc tion, as the juveniles accumulate lipid merely for overwintering. A similar life-strategy has been dem onstrated for juveniles of the deep-water prawn Pan dalus borealis (Hopkins et al. 1993). It is possible that the main reason why the 1+ year-olds at the Bothnian Sea study station do not reproduce despite a high lipid level is because allocation of lipid for development of reproductive tissue and eggs would result in serious starvation before brood release, which normally occurs some 8 months after the ma jor -- and practically only -- period of sedimentation of good-quality food. In addition, a low lipid content may reduce the viability of offspring (Ouellet et al. 1992), and may be contributing to the observed in terannual variations in the recruitment success of the cohort (VI). In the Bothnian Sea (III), as well as in the Gulf of Riga (V), the lipid level of the reproducing gen eration of both M. affinis and P. femorara decreased in late autumn; especially at station GR1 the de crease was extensive in gravid M. affinis. Also Hill et al. (1992) noted a decrease in the lipid levels of males and females in October. Apparently, the sig nificantly reduced lipid and TAG levels in gravid females are characteristic for both species. Alloca
Ecophysiology of two benthic amphipod species from the northern Baltic Sea 23
tion of lipids and especially TAG to the elaboration of reproductive tissue has also been shown in krill (Falk-Petersen et al. 1981). Moreover, if feeding is reduced during and after maturation, the depletion of body lipid for maintenance metabolism is further accelerated. After fertilization the progressively in creasing metabolism of the developing embryos further reduces the total lipid and TAG contents of the "mother-brood -complex". Thus it is evident that the reduced lipid levels are causing the increased protein catabolism observed in gravid females (IV, V). In conclusion, the balance in the allocation of lipid between metabolism and reproduction is a key feature in the adjustment of the bioenergetic strategy of amphipods ·facing different environmental re gimes, and is intimately linked to the life-cycle of the species. 5.2 Effects of environmental nutritional conditions on the physiological condition of the amphipods In the section above, the seasonal and spatial vari ability in the metabolic and biochemical character istics of the amphipod species studied have been discussed, and it is apparent that differing environ mental conditions, especially those related to nutri tion, have a strong influence on the physiological condition of the animals. Pelagic processes, mainly primary production and sedimentation, have an es sential role, since they control the quantity and quality of food available in the benthic environment. In addition, other biotic (e.g. intra- and interspecific competition) and abiotic (e.g. temperature, re deposition of sedimented matter by near-bottom cur rents) factors can have a significant role. To gain insight into the role of primary produc tion and sedimentation in controlling the dynamics of benthic amphipod populations, it is necessary to examine the main features of these processes in the Baltic Sea. 5.2.1 Primary production and sedimentation in the Baltic Sea In the northern Baltic Sea, trophic conditions vary considerably between sea areas (e.g. Lassig et al. 1978, review by Elmgren 1984). The data on pri mary production and sedimentation at the Bothnian Sea station SR5 (Andersson et al. 1996, VI) are in accord with earlier research (e.g. Lassig et al. 1978, Kuparinen et al. 1984, Leppanen 1988, Andersson
and Rudehдll 1993, Heiskanen and Kononen 1994). Therefore, according to existing information about pelagic productivity, the subareas studied can be classified, roughly, as follows: Gulf of Finland and Gulf of Riga -- "eutrophic", Bothnian Sea -- "mesotrophic", and Bothnian Bay -- "oligotrophic". In acknowledging the typical relationship between primary production and sedimentation, it is evident that the benthos in the Gulf of Finland and the Gulf of Riga receives more organic particulate material during the growing season than the Bothnian Sea or the Bothnian Bay. In the Baltic Sea during the spring bloom, the downward flux of algae through the water column occurs within a few days, even in deeper areas (e.g. Smetacek et al. 1978, Smetacek 1985 and citations within). Since zooplankton grazers are generally of low abundance at the start of the spring bloom (e.g. Viitasalo 1994), large quantities of relatively un processed, high-quality material are likely to reach the benthos in relation to primary production. How ever, lateral transport processes (e.g. Graf et al. 1982, Leppanen 1988), resuspension and focusing of particulates in temporary or permanent sedimenta tion sinks may effect sedimentation patterns, thus creating serious problems in the reliability of gross deposition rates, especially in areas characterized by complex hydrodynamics. As a result, sedimentation can seldom be measured with sufficient reliability to create accurate carbon budgets for pelagic-benthic coupling. Although primary production during the spring bloom in the open-sea areas of the northern Baltic Sea does not show particularly striking interannual variation (reviews by Elmgren 1978, 1984, Lassig et al. 1978, Larsson and Hagstrom 1982, Andcrsson et al. 1996), local variation in sedimentation rates may well occur due to interannual differences in the suc cession and composition of the spring bloom phyto plankton assemblage. Diatoms are known to sink fast during the blooms (e.g. Smetacek 1985), while dinoflagellates mostly disintegrate in the water col umn (e.g. Heiskanen and Kononen 1994). Thus, in terannual variations in the respective proportions of dominating phytoplankton species may explain the changes in the quantity and quality of sedimented matter (VI), both of which are crucial to the benthos. Although still somewhat speculative, this is another potential factor corroborating the theory that changes in the dynamics of the pelagic component of the marine ecosystem have a direct effect on the ben thos.
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5.2.2 Spatial variability in the condition of the amphipods in relation to environmental nutritional conditions The present study shows that spatial variability in trophic characteristics between different subregions of the Baltic Sea is reflected as differences in the physiological condition and bioenergetic strategy of the amphipods. To proceed with the discussion, a hypothesis on the relationship between the nutri tional conditions prevailing in different Baltic Sea subregions and the ensuing physiological adaptations observed in the amphipods is presented. (1) Bothnian Sea. The observed high lipid levels imply that the amphipods in this sea region have adopted an energy storage strategy which ensures a maximum benefit from the short-but-intensive pe riod of spring phytoplankton sedimentation (II, 111, VI). A very low tNH (except in summer) indicates a low-quality diet and/or extensive utilization of lipid for energy production in order to save amino groups (II, IV). (2) Gulf of Riga (inshore vs. offshore areas). Primary production and nutrient levels in the Gulf of Riga are among the highest in the Baltic Sea, leading to a large deposition of organic particulate matter. In addition, although allochthonous riverine input in nearshore regions is high, the material is low in nu tritional quality. The nearshore station GRI con sisted of sandy mud with a low organic content, while the offshore station GR5 was characterized by organic-rich mud (Carman et al. 1996). It is con ceivable that resuspended fine particulate material is effectively transported from basin margins and re deposited at central-basin accumulation areas, espe cially after the breakdown of the thermocline in autumn. This material, together with the sedimenta tion of the potentially important late-summer phy toplankton bloom, offers a "new" food source for benthic organisms inhabiting the offshore areas. Consequently, the substantial lateral transport of material is likely to reduce food availability of ben thos in nearshore areas. Despite clear differences in the condition of nearshore and offshore amphipod populations -- which may be caused partly by inter specific differences -- the higher and more constant INH, despite a relatively high lipid level, indicate adaptation of the amphipods to more stable nutri tional conditions compared to the Bothnian Sea and Bothnian Bay. Implications of similar adaptations have been recorded also for the amphipods inhabit ing the eutrophic Gulf of Finland (II, Lehtonen un published data). (3) Bothnian Bay. The spring bloom peaks later than in the more southern areas, and is remarkably
lower in intensity; the "peak" is distributed more evenly over time or may be missing altogether (Lassig et al. 1978). In addition, high concentrations of allochthonous humic substances
of refractory na ture in the sediment are characteristic for this area (Gripenberg 1934). These factors are likely to cause the observed slow growth in the population (low production:biomass ratio) in the area (Andersin et al. 1984). Physiologically, poor nutritional conditions manifest as high tNH, in this case as a sign of an increased catabolism of body protein triggered by a low lipid level (I, II), but more information is needed on seasonal changes in the metabolism and biochemical composition of the amphipods from this specific area. 5.2.3 Bothnian Sea: the time-lag At the Bothnian Sea station SR5, a time lag between the sedimentation of the spring bloom and the physiological response (III, IV) and growth (VI) of the M. affinis population was observed. Previously, Uitto and Sarvala (1991) noted a time-lag between sedimentation and the growth of both M. affinis and P. feniorata in Tvarminne coastal area, attributing it mainly to progressive increase in temperature during the summer. However, a similar lag exists in the present study area, which is characterized by a con stant seasonal temperature regime. In the Baltic Sea, the physiological response of benthic macrofauna to sedimentation input has been studied only in shallow areas (Grafet al. 1982, 1983, Christensen and Kanneworff 1985; measured as bio chemical changes). In these studies, the response was shown to be immediate or delayed; interspecific differences in feeding behaviour, feeding niche and the principal source of nutrition are usually consid ered the main reasons for the varying speed of re sponse. Possibly, the fresh algal material must be partially processed by other benthic consumers (bacteria, meiofauna) before becoming optimally available to amphipods. Some microalgae show no signs of decomposition even after several weeks of exposure (Gunnison and Alexander 1975); further more, low temperature delays the decomposition process. From a physiological perspective, the long period of poor nutritive conditions during the winter may decrease the ability of the amphipods to assimi late food efficiently because of reduced levels of key digestive enzymes, as observed in the copepod Ca lanus hyperboreus (Head and Conover 1983). Thus, the observed time-lag is possibly a result of both temporarily impaired assimilation ability of the am-
Ecophysiology of two benthic amphipod species from the northern Baltic Sea 25
phipods and the suboptimal palatability of the fresh food. 5.3 Utilization of organic matter by the amphipods: a system-wide view 5.3.1 Bothnian Sea: requirements in relation to input Several studies at various locations have indicated that a large portion of the pelagial material produced is utilized by the benthos (e.g. Riley 1956, Ankar 1977, Elmgren .1978, Wassmann 1984, Bergstrom and Sarvala 1986). Apart from the macrozoobenthos, the meiofauna and bacteria have a very significant, and usually considered, predominant role in the utilization of deposited organic matter. In the Both nian Sea study area, the respiration of M. affinis comprises about 30% (seasonal average) of total benthic community respiration (Karjala et al. in preparation); combined with the allocation of carbon for growth (VI), it is apparent that a highly signifi cant portion of the sedimented organic matter at the location is consumed by amphipods. With regard to the utilization of the pelagially produced organic matter, taking into account the action of other consumers in both the pelagial and benthic food webs, annual carbon and nitrogen re quirements of the M. affinis population are high (VI). With regard to sedimentation, due to the diffi culties in measuring the actual amount of material deposited at the study site, the 50% assimilation rate by the amphipod population, calculated for the "active period" in 1991 and 1993, may be an over estimation. However, even if the actual deposition rates were, say, 2-3 times higher than those recorded here, the carbon (and nitrogen) demand of the am phipods would still underline that the population is strongly limited by food, considering the utilization of food by other components of the benthic system. 5.3.2 Mineralization of carbon and nitrogen The importance of benthic fauna in nitrogen miner alization processes, either by direct metabolism or by enhancing bacterial activity via bioturbation is well known. Gardner et al. (1987) estimated the ex cretion of an abundant Diporeia spp. population to be responsible for up to 42% of total benthic nitro gen release in Lake Michigan. Henriksen et al. (1983) showed that excretion by the amphipod
Corophium volutator could account for 80% of the net NH flux from the sediment and provide nitrify ing bacteria with a potentially significant source of NH. Moreover, bioturbation by C. volutator has been shown to enhance also benthic denitrification rates (PelegrI and Blackburn 1994, PelegrI et al. 1994). Since the excretion rate of amphipods is greatly determined by the availability of good-quality food (IV), the estimated NH release by the populations showed more variability than the rates of carbon mineralization, both seasonally and between the different sea areas (II, V, VI). The `post-bloom study', which provided information on `)NH close to their annual maxima, showed clearly that the highest daily NH release rate recorded at the Bothnian Sea M. affinis station US6b was due to the high population density (over 10,000 md r2 ) n (II). The moderately abundant P. feniorata population at the Gulf of Finland station LL6a had an almost equal rate of NH release, but this was attributed to the high weight-specific excretion rates and the large size of the amphipods (II). Another distinct case is the Bothnian Bay, where the small size of M. affinis resulted in a very low total release of NH despite a high weight-specific tNH and relatively abundant populations. These examples illustrate exquisitely that several factors -- abundance, size and metabolic activity of individuals -- are responsible for the ob served high variability in the rates of NH release by amphipod populations. By considering the scheme above, the observed differences in the annual mineralization rates of the amphipod populations of the Bothnian Sea and Gulf of Riga stations can be rationalized. In the Gulf of Riga the estimated annual total respiration rates (1.7 and 3.0 g C r2n yr') (V) recorded were considerably less than that recorded by Bergstrom and Sarvala (1986) for a coastal M. affinis population (11.9 g C r2n yr') in an area where summer temperatures up to 18°C were recorded; however, this was clearly due to higher abundance in the latter area. In the Bothnian Sea, despite a constantly low temperature, the annual respiration of the M. affinis population was even higher (14-17 g C m 2 yr') (VI). Consider ing the higher primary productivity of the Gulf of Riga discussed earlier, mineralization by the am phipods in the area probably plays only a minor role. Conversely, in the "mesotrophic" Bothnian Sea, metabolism by the abundant M. affinis populations is likely to be an exceedingly important component in benthic mineralization process.
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5.4 Population dynamics: observations and hypotheses 5.4.1 Factors affecting the life-cycle The longevity of the amphipods has been associated with depth and temperature (Segerstrбle 1937, Moore 1979, Leonardsson et al. 1988) and trophic conditions (Siegfried 1985). Reduced metabolic rates caused by constantly low temperatures are commonly considered to result in longer life-cycles. Metabolic rates may also be lower during adverse food conditions (IV). As discussed, the growth of M. affinis cannot be temperature-regulated in deep, open-sea areas (VI). Depth per se does not seem to be the decisive factor determining the condition of the amphipods, since high lipid levels were recorded both at deep and shallow stations (II, III, V). How ever, deep areas and depressions of the seabed often function as sedimentation sinks, creating favourable conditions for benthic life with regard to food avail ability. Considering these factors, in the shallower coastal areas where strong seasonal oscillations in temperature and more stable food conditions may have considerable effects on metabolism, the longterm bioenergetic strategy, life-cycle and population dynamics of the amphipods are likely to be different in comparison to deep, open-sea areas. 5.4.2 Interspecific interactions In addition to spatial differences in the direct input of food, the growth and condition of the amphipod populations may be strongly affected by interactions between species. In the Bothnian Sea and the other open-sea areas studied, amphipods are, overwhelm ingly, the dominant macrozoobenthic organisms (II, V, VI); thus, in these areas, interspecific competition for food (at macrozoobenthic level) as a factor regulating the condition of individuals and the population dynamics can be disregarded. This was not the case at the Gulf of Riga nearshore station GR 1, where other organisms (e.g. the polychaete Marenzdlleria viridis, C. volutator and the bivalve Macoma baithica; Yermakovs and Cerderwall in prep.) comprised by far the greatest part of the ben thic biomass and are certain to compete intensively for nourishment with M. affinis. Interspecific interactions include also the poten tial role of bacteria and meiofauna as a food source for the amphipods (e.g. Ankar 1977). Although not comparable with the algal sedimentation in terms of biomass, benthic bacteria are a more predictable and
stable food source (Johnson et al. 1989). However, bacteria have been shown to provide only 24-32% of the annual carbon requirements of a M. affinis population (Uitto and Sarvala 1991) and only 6% of the needs of the young-of-the-year (Goedkoop and Johnson 1994). Implications of predation on some meiofaunal taxa by M. affinis have been observed (Elmgren et al. 1986, `Olafsson and Elmgren 1991, Sundelin and Elmgren 1991). Active predation, however, can be questioned, but it is highly probable that the amphipods, at least when they have reached an adequate size, passively ingest meiofauna while processing the sediment. However, as discussed ear lier, the generally low 1NH does not support the idea of meiofauna being a significant food source for M. affinis. 5.4.3 Intraspecific interactions In food-limited areas, the growth of the population leads to faster depletion of the annual quality-food resources, resulting in reduced growth and less ac cumulation of energy reserves. Following a simple model, since the fecundity of amphipods is size-de pendent (VI, Cederwall 1977), reduced growth in the reproducing generation due to poor food availability results in a smaller number of offspring and, subse quently, a decline in population size
. However, a deeper examination reveals that the mechanisms regulating population size are far more perplexing. Variability in the recruitment success of the young-of-the-year has a potential role in the ob served long-term variations in population size (ca. 7year cycle, Andersin et al. 1978, 1984). Theoreti cally, even a minor increase in the proportion of off spring that survive the high-mortality "babyhood" period results in a distinctly more abundant cohort (e.g. Valiela 1984, review by Gosselin and Qian 1997). In spring 1991, the estimated number of off spring in the Bothnian Sea of M. affinis population was high, occurring during a period of very high population density (VI). Recruitment success was very significant (56%) despite the high density. Ex periments have indicated that high density together with the presence of older generations has a negative effect on the growth and survival of the young-ofthe-year M. affinis (Hill 1992). However, during a year of good food availability, competition between the young-of-the-year and the older cohorts is alle viated, and the prospect of the young passing the bottleneck of recruitment is increased. In 1992, the survival rate
was poor (12%), despite a somewhat reduced population size; this suggests that the input of food (not measured) had been smaller in 1992.
Ecophysiology of two benthic amphipod species from the northern Baltic Sea 27
Finally, in 1993, the survival of the offspring in creased markedly (38%), although sedimentation was about 50% lower than in 1991; by this time, the abundance of the population had reduced to half of that recorded in 1991, with the result that competi tion pressure was greatly relieved. A complex relationship between the amount of food input, population density and the relative por tions of individuals representing different annual cohorts seems to exist. However, a tentative mecha nism for explaining the interannual variability and even long-term oscillations in the Bothnian Sea am phipod populations can be formulated. First, we assume that the variability in the amount of the annual input of food is small. Thus, during the phase of annually rising population den sity, the mean size of the individuals gradually de creases, since progressively less food is available per capita. Once the density of the population has ex ceeded the "Carrying Capacity
" of the environment, the recruitment success of the young-of-the-year decreases markedly, or may even collapse, due to intraspecific competition for food. A key point to be observed here is that, since this study population exhibits a 3-year life cycle, the consequences of re cnlitment failure are only manifested in a significant way after 3 years, when the poorly-recruited cohort reproduces. Meanwhile, the small contribution of this cohort to the population actually increases the survival prospects of the others, especially the two following annual cohorts. Second, it is suggested that the depth of the ebb in the curve describing the long-term fluctuations in the abundance and biomass of the population should be determined by food conditions. If the two cohorts that follow the cohort that failed encounter years characterized by abnormally low sedimentation (that affects negatively their recruitment, survival or re production), the collapse in the population will be severe, despite the fact that intraspecific competition is constantly alleviated by a lowered density. How ever, if the following years are "normal" regarding nutritional conditions, the next two cohorts will thrive and yield a successful offspring when their turn to reproduce is at hand; in this case, the ebb in the curve will be only moderate. Conclusively, the effects of irregularities occurring in annual sedimen tation rates on the amphipod population are depend ent on the density and structure of the population. Most of the observed variations in the biochemi cal characteristics of the amphipods coincide with the changes recorded in environmental and popula tion parameters. In the Bothnian Sea M. affinis col lected in winter and spring 1991 were significantly
smaller than at corresponding times in 1992 and 1993 (VI). However, the lipid level of the am phipods was high in late summer during all study years (Ill), regardless of the observed variations in the secondary productivity of the population (VI). And yet this is not surprising since the abundance and biomass of the population showed a decreasing trend during the study years, leaving more food available for a smaller population to exploit. Con nected with the exceptional biochemical character istics of amphipods, a lipid-related "buffering ca pacity" may be in use, i.e. the energy reserves at tained during the previous year help to withstand a year of low sedimentation input. In the Gulf of Riga, the low-density population of P. femorata at station GR5 sustained unusally high lipid levels until late autumn, while M. affinis, occurring at station GRI in a considerably higher density, facing also a strenu ous interspecific competition (see above) showed rapid depletion of lipid deposits during the autumn (V). These characteristics are evidently connected not only to differences in the amount of food arriv ing at the bottom, but its ultimate availability to in dividual amphipods. As a concluding remark regarding competitive interactions within and between species, the present studies show that both the role of density-dependent regulation and, especially in coastal regions, inter specific competition for available food resources can be important biological factors affecting the popula tion dynamics of the amphipods in the northern Bal tic Sea. However, these mechanisms are strictly coupled with an exogenic regulating factor that emerges as the primary variable: the quantity and quality of available food. 6 Conclusions In what way does this work contribute to our knowl edge of the two amphipod species and their relation to the environment? The general conclusions ac quired in this thesis are presented below. 1 Although M. affinis and P. femorara differ in their behavioural and physiological characteris tics, the present study emphasizes the importance of nutritional conditions in regulating the bio energetic strategy of both species. 2 Variability in metabolism, particularly in am monia excretion, reflects changes in the avail ability and abundance of good quality food. Poor nutritional conditions shift the metabolic balance
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of the amphipods progressively towards the utili zation of reserve lipid, which is observed as a decreased ammonia excretion rate. Since the ef fect on the oxygen consumption rate is consid erably smaller, the ammonia excretion rate can be succesfully used as an indicator of benthic nutritional conditions, providing that the am phipods are properly acclimatized (avoiding handling stress and also starvation conditions) and not extremely lipid-poor (intensified catabo lism of body protein resulting in increased am monia excretion).
and the survival potential of the offspring. How ever, since interannual variations in the rates of primary production and sedimentation within specific locations do not seem to be dramatic and are likely to be non-cyclic, intraspecific competi tion for available food has probably a key position in the explanation of the previously recorded long-term oscillations in the population size of amphipods in open-sea areas.
3 Due to the functional anomalies related to their life-stage, adult individuals (males and gravid females) exhibit significantly different bioener getic characteristics compared to juveniles. 4 The magnitude of the effect of temperature rise on the ammonia excretion rate of amphipods seems to be associated with these rates measured at "ambient" near-bottom temperature (4° C) and, thus, with their recent feeding history. Of the two species, P. femorata seems more capable of regulating its nitrogen release when the tempera ture elevates, which may denote a shift into a more lipid-dominated metabolism at higher tem peratures. 5 Environmental food conditions strictly control the lipid dynamics of both amphipod species. Under a highly-concentrated seasonal sedimen tation pattern, the bioenergetic strategy of the amphipods includes a rapid accumulation of lipid (mainly triacylglycerols) after the spring bloom. The lipid is utilized for metabolic fuel under poor nutritional conditions, or reproduction; thus, its levels directly regulate the survival and repro ductive capacity of the individuals. 6 When abundant, the amphipods have a signifi cant effect on benthic mineralization processes especially in areas where annual sedimentation of organic matter is low or moderate. Besides abundance and temperature, the mineralization rates (especially of nitrogen) are determined by the degree of input of organic nzarter to the ben thic system, which is itself reflected as changes in the metabolic rates of individuals. 7 The coupling between sedimentation input and growth and condition of the amphipod popula tions is close, especially in food-limited open-sea areas. Interannual variability in the quantity and quality of sedimenting matter may result in dif ferences in growth, lipid accumulation, fecundity
7 Acknowledgements This kind of work cannot be done single-handedly (although I stubbornly thought so!). Numerous peo ple have contributed to the process that led to the initiation and completion of this thesis, by lending a helping hand during the physical part or boosting my morale during the desperate periods. However, space (in this case) is limited: if I tried to recall everyone who has handed me a benthos sample or a muchneeded beer during these important years, I would remain in square one. Starting from the cradle of my studies, the Divi sion of Animal Physiology, University of Helsinki: in the dark, cigarette-smelling second-floor corridor wandered an unorthodox duo, Professor Roif Kristoffersson and "The Mussel Girl" Inke Sunila. Both were instrumental in my choosing to attempt the strange art of the physiology of marine benthic organisms. With Inke, I spent some unforgettable (and some completely forgotten) moments in nu merous Helsinki watering holes, looking for ideas and inspiration! Tvдrminne Zoological Station was my next des tination, although only for an unfortunately brief period. I worked under a number of financiators and, under the star-studded late-autumn sky of Tvдr minne-by-the-sea, I came to understand the needs and art of independency (mind you, I still intend to publish my Mytilus works some day!). Next step was the crucial one, with Professor Paavo Tulkki calling me to duty para patria to master the art of being a gentleman instead of even a naval officer. The Department of Biological Ocean ography, at the Finnish Institute of Marine Research, has become my "temporary" home since 1990. Ami Andersin (rumoured to have been born on the 1.0 mm sieve) taught me the secrets of benthic am phipods, and as a dear friend and colleague puts up reasonably well with my sometimes explosive tem per. Forgetting nobody: hats off to the rest of the
Ecophysiology of two benthic amphipod species from the northern Baltic Sea 29
marvellous, good-spirited people at the Biological Department! Cruises aboard nv "Aranda" became everyday stuff during this assignment. A total of eleven months at sea did certainly not go without incidents, many of them memorably hilarious. The crew of the vessel is appreciated for making me feel safe even in rough weather, and the kitchen personnel for stuffing us with Argentinian beef prior to heavy sampling. The "Boys" from the Technical Department of FIMR always lent a helping hand (occasionally ex tended with a scary wrench), launching a couple of affectionate five-letter words not to be printed here. Since marine biology is a science that is highly international by nature, during the years I have had the pleasure of meeting a great number of colleagues from different countries, and shared valuable con versations which have contributed greatly to my limited understanding of the secrets of the Big Blue. The Gulf of Riga project, financed by the Nordic Council of Ministers, saved my buttocks for many years (although I guess nobody really knew what I was up to in the whole project...). Anyway, Hasse Cederwall (University of Stockholm) somehow kept faith in me, providing me also with the occasional shot of Irish. Other people within the Benthos Group that kept me good company during this personally important project were Bertil Widbom (University of Stockholm), leva Upeniece, Parsla Pallo, Juris Ai gars, Vadims Yermakovs (Institute of Aquatic Ecol ogy, University of Latvia), Oskars Stiebrins (Latvian Hydrometeorogical Agency) and Birger Larsen (Danish Geological Survey
). Technical assistance in putting up this final ver sion was kindly provided by Mrs. Leena Parkkonen and Ms Leena Rome, not forgetting the spirited-asusual language check by Mr. Richard Thompson Coon (Gulf of Finland Environment Society). The existence of the (in)famous Zuliman Child (Slight Return) heavy blues outfit (consisting tradi tionally of biologists only) parallels exactly my time spent with the amphipods. I warmly thank all you guys for dragging me down from the clouds every now and then by cracking a devastating basist joke or two. Without the band, a private place in the funny farm would have been guaranteed ages ago. For the more private part of my life, I want to thank my long-time companion, my friend Anneli for love and putting up with me during this crucial time; our lovely (and wild!) daughter Eeva has al ways made me smile (although now I had to seek refugee to be able to complete this job!). I give my humblest thanks to my late father Keijo K. Lehtonen and my mother Seija: without
your guidance and attitude towards life I would probably have become an economist or even worse. Thanks for giving me this life. The Doobie Brothers are given credits for the song Takin' it to the streets" - that goes as a thanks to my brother Janne for sharing the football fanati cism with me. Eavidaй. Praia da Rocha, Portugal April 1997 8 References Aarset A.V. & Aunaas T. 1990. Effects of osmotic stress on oxygen consumption and ammonia ex cretion of the Arctic sympagic amphipod Cam marus wilkitzkii. Mar. Ecol. Prog. Ser. 58: 217224. Andersin A.-B., Lassig J., Parkkonen L. & Sandier H. 1978. Long-term fluctuations of the soft bot tom macrofauna in the deep areas of the Gulf of Bothnia 1954-1974, with special reference to Pontoporeia affinis Lindstrцm (Amphipoda). Finnish Mar. Res. 244: 137-144. Andersin A.-B., Lassig 3. & Sandier H. 1984. On the biology and production of Pontoporeia affinis Lindstr. in the Gulf of Bothnia. Limnologica 15: 395-401. Andersson A., Hajdu S., Haecky P., Kuparinen J. & Wikner 3. 1996. Succession and growth limitation of phytoplankton in the Gulf of Bothnia (Baltic Sea). Mar. Biol. 126: 791-801. Andersson A. & Rudehдll A. 1993. Proportion of plankton biomass in particulate organic carbon in the northern Baltic Sea. Mar. Ecol. Prog. Ser. 95: 133-139. Andruiaitis, G., AndruInitis A., Bitenieks Y., Priede S. & Lenshs, E. 1992. Organic carbon balance of the Gulf of Riga. Proc. 17th CBO Conference, Norrkoping 1990, Swedish Hydrologiгal and Me teorological Institute Report. Ankar S. 1977. The soft bottom ecosystem of the northern Baltic Proper with special reference to the macrofauna. Contr. Askц Lab. 19: 1-62. Ankar S. & Elmgren R. 1975. A survey of the ben thic macro- and meiofauna of the AskO-Landsort area. Merentutkimuslait. Julk.IHavsforskningsinst. Skr. 239: 257-264. Bayne B.L. & Scuilard C. 1977. Rates of nitrogen excretion by species of Mytilus (Bivalvia: Mol lusea). J. mar. biol. Ass. U. K. 57: 355-369.
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