Transcript

Organisms and food webs in rock pools:Responses to environmental stress and trophic

manipulation

Marie Arn6r

Department of Zoology, Stockholm UniversityS-106 91 Stockholm, Sweden

Stockholm 1997

Doctoral dissertation 1997

Marie Am&Department of ZoologyStockholm UniversityS-106 91 [email protected]

0 1997 Marie Am&ISBN 9 l-87272-53-9Printed by Jannes Snabbtryck AB, StockholmCover by Bibbi Mayrhofer

2

ERRATAOrganisms and food webs in rock pools:

Responses to environmental stress and trophic manipulationby

Marie Arnerpage line writtenSummary6 9 (1992) Physiological and life

history responses of Duphnia -magna to increasing salinity

6

1010111323

13 (submitted manuscript)

right 20 Koehn & Bayne 1988right 24 Koehn & Bayne 1988right 32 ..physiological index. (..left 21 (1996) has argued...left 22 Koehn R.K. &‘Bayne, B.L

(1988)

Paper III4 left 18 . ..The water was sieved..6 right 41 and nauplia to Cyclops

Paper IV12 left 21 . . . Daphnia generally had lower

biomass...

Paper V3 right 8 of salinity tolerance of the

DaphnM

should be

(1993) Effects of salinityon metabolism and lifehistory characteristics ofDaphnia magna(accepted for publication inFreshwater Biology)Koehn & Bayne 1989Koehn & Bayne 1989..physiological index (...(1996) have argued...Koehn R.K. & BayneB.L (1989)

The water (50 L tub-‘) was sievedand nauplia to total Cyclops

. . . Duphnia generally had higherbiomass.. .

of salinity tolerance of Daphnia

5 right 24 The ratios of nauplia to Cyclops The ratios of nauplia to totalCyclops

To my family

Abstract

Differential susceptibility of organisms and populations to environmental stress influ-ences the outcome of biological interactions and the structure of communities andecosystems. In this thesis, the effects of environmental stress on organism, populationand community levels were studied. ‘Die physiological responses to changes in salinityand exposure to pollutants were studied by comparing rock pool Gammurus duebeni andlittoral G. oceanicus with different tolerance to abiotic stress. Physiological and lifehistory responses of rock pool Duphnia magna to different salinities were examined. Ex-,perimental systems, originating from natural rock pools, were established to exploredirect and indirect impacts of cadmium and predator addition in freshwater plankton com-munities. Three different food web configurations were used: 1. phytoplankton andsmall-bodied zooplankton (Cyclops sp. and Chydorus sphaericus), 2. phytoplankton,small-bodied zooplankton and D. magna, and 3. phytoplankton, small-bodied zooplank-ton, D. magna and the invertebrate predator Notonectu sp. To evaluate the experimentalsystems, natural and experimental rock pools were compared.

Salinity stress negatively affected the physiological status of Gammurus and D.magna. G. duebeni, with higher tolerance to fluctuation in abiotic variables, was lessaffected by natural stress and pollutants than G. oceanicus. The physiological and lifehistory responses led to comparable conclusions in D. magna: i.e., salinity stressnegatively affected the physiological status of D. mugnu and hampered reproduction andgrowth. In the experimental food webs, cadmium inhibited phytoplankton productivityand decreased the biomass of cladocerans. Cadmium did not change the trophicinteractions between Duphniu and phytoplankton or between Duphniu and Notonectu.The regulation of lower trophic levels by Duphniu and Notonecta was important in theexperimental food webs. Notonectu produced a indirect positive (cascade) effect onphytoplankton and small-bodied zooplankton. It was possible to maintain experimentalphytoplankton-herbivore communities for several months. The experimental systemsresembled natural rock pools with permanent D. mugnu presence. Phytoplanktonbiomass was regulated by D. magna when the species was permanently present in bothnatural and experimental rock pools. Experimental rock pools may approximate otherfishless habitats and the spatial and temporal scales are most appropriate for studies ofplankton interactions.

4

Organisms and food webs in rock pools:Responses to environmental stress and trophic manipulation

Akademisk avhandling som for avlaggande av filosofie doktorsexamen vid StockholmsUniversitet offentligen forsvaras torsdagen den 29 maj 1997, kl. 10.00 ifiirelfsningssalen, Frescati Backe, Svante Arrhenius vag 21 A, Frescati

MarieavArnCr

Zoologiska InstitutionenStockholms UniversitetS-106 91 Stockholm

Stockholm 1997ISBN 9 l-87272-53-9

AbstractDifferential susceptibility of organisms and populations to environmental stress influ-ences the outcome of biological interactions and the structure of communities andecosystems. In this thesis, the effects of environmental stress on organism, populationand community levels were studied. The physiological responses to changes in salinityand exposure to pollutants were studied by comparing rock pool Gummurus duebeni andlittoral G. oceanicus with different tolerance to abiotic stress. Physiological and lifehistory responses of rock pool Duphniu magna to different salinities were examined, Ex-perimental systems, originating from natural rock pools, were established to exploredirect and indirect impacts of cadmium and predator addition in freshwater plankton com-munities. Three different food web configurations were used: 1. phytoplankton andsmall-bodied zooplankton (Cyclops sp. and Chydonrs sphuericus), 2. phytoplankton,small-bodied zooplankton and D. magna and 3. phytoplankton, small-bodied zooplank-ton, D. mugnu and the invertebrate predator Nofonectu sp. To evaluate the experimentalsystems, natural and experimental rock pools were compared.Salinity stress negatively affected the physiological status of Gummunrs and D. mugnu.G. duebeni, with higher tolerance to fluctuation in abiotic variables, was less affected bynatural stress and pollutants than G. oceunicus. The physiological and life history res-ponses led to comparable conclusions in D. magna: i.e., salinity stress negatively aflec-ted the physiological status of D. magna and hampered reproduction and growth. In theexperimental food webs, cadmium inhibited phytoplankton productivity and decreasedthe biomass of cladocerans. Cadmium did not change the trophic interactions betweenDuphniu and phytoplankton or between Duphniu and Notonectu. The regulation of lowertrophic levels .by Duphniu and Notonectu was important in the experimental food webs.Notonectu produced a indirect positive (cascade) effect on phytoplankton and small-bodied zooplankton. It was possible to maintain experimental phytoplankton-herbivorecommunities for several months. The experimental systems resembled natural rockpools with permanent D. magna presence. Phytoplankton biomass was regulated by D.mugnu when the species was permanently present in both natural and experimental rockpools. Experimental rock pools may approximate other fishless habitats and the spatialand temporal scales are most appropriate for studies of plankton interactions.

Table of contents

List of papers

Introduction

The rock pool ecosystem

Environmental stress- Background- Rock pool organisms and effects of salinity

changes and toxicants

Model systems and experimental rock pools- Background- The experimental rock pool systems: experienceand evaluation

Consumer and resource regulation- Experience from lake and experimental studies- Predation and competition in rock pool systems- Consumer regulation of lower trophic levels byNotonecta and Daphnia in experimental rock pools

- Effects of cadmium addition on trophic interactionsin rock pool food webs

Conclusions

References

Acknowledgements

1012

1313

151617

18

18

19

27

5

List of papers

The following papers are included in this thesis and will be referred to in the text bytheir Roman numerals. The published and accepted papers are reprinted with kindpermission of the publishers. .

I

II

III

IV

V

Tedengren M., Am& M. & Kautsky N. (1988) Ecophysiology and stressresponse of marine and brackish water Gammarus species (Crustacea,Amphipoda) to changes in salinity and exposure to cadmium and diesel-oil.Mar. Ecol. Prog. Ser. 47:107-l 16

ArnCr M. & Koivisto S. (1992) Physiological and life history responses ofDaphnia magna to increasing salinity. Hydrobiologia 259: 69-77

ArnCr M., Koivisto S., Norberg J. & Kautsky N. Trophic interactions in rockpool food webs: regulation of zooplankton and phytoplankton by JVutonectaand Daphnia. (submitted manuscript).

Koivisto S., ArnQ M. & Kautsky N. (1997) Does cadmium pollution changetrophic interactions in rockpool food webs? Accepted for publication inEnviron. Toxicol. Chem.

Am& M. & Koivisto S. Evaluation of the ecological relevance of a modelsystem: Seasonal development and patterns in natural and experimental rockpools (manuscript).

6

Introduction

Rock pools, water filled bed-rockdepressions, are patches of habitatdifferent from the surrounding shore aridare found on shores around the world.They are characterised by large spatial andtemporal variations and are considered asphysically harsh habitats (Ganning 197 1;Ranta 1982; Astles 1993; Metaxas &Scheibling 1993; Loder et al. 1996;Underwood & Skilleter 1996). Theseisolated habitats are commonly foundalong the Swedish and Finnish coastalareas of the Baltic Sea. Earlier studies ofrock pools in the Baltic Sea area haveemphasised species composition andabundance in relation to the physico-chemical characteristics (in particularsalinity) of the rock pools (Levander1900; Jarnefelt 1940; Lindberg 1944;Droop 1953; Ganning 1967; Bjorklund1972; Ranta 1979). Descriptive studies ofdifferent species and of physiologicaltolerance to normally fluctuating vari-ables and toxicants have been conductedby Forsman (195 l), Lagerspetz (1955,1958) (I, II) and the nutrient andmetabolic dynamics of rock pool eco-systems were studied by Ganning &Wulff (1969, 1970) and Ganning (1971).The systems have also been used formodelling approaches and studies ofpopulation dynamics (Wulff 1980;Pajunen 1990; Norberg & DeAngelis1997). Commonly studied are differentaspects of species coexistence andinterspecific competition (Vepsalainen1 9 7 8 ; Ranta 1979, 1982; Hanski &Ranta 1983; Bengtsson 1988) and theeffects of vertebrate and invertebratepredation have been studied in situ aswell as in laboratory experiments (Ranta

& Nuutinen 1985; Ranta et al. 1987;Ranta & Espo 1989; Pajunen & Salmi1991; III).

The objectives of this thesis can beseen in both a basic ecological and anecotoxicological context. Organisms andpopulations have different susceptibilityto environmental stress (natural andantropogenic), which influence the out-come of biological interactions and thestructure of communities and ecosystems.The effects of salinity changes andpollutants have been studied on orga-nism, population and community levels.Experimental systems, originating fromrock pools, were established to explorethe effects of trophic manipulations andthe addition of a toxicant in a freshwaterplanktonic community. In paper I, thephysiological responses to changes insalinity and exposure to cadmium anddiesel-oil were studied by comparing rockpool and littoral amphipods with differenttolerance to abiotic stress (Gammanzsduebeni Lilljeborg and G. oceanicusSegerstrlle, respectively). Physiologicaland life history responses of rock poolDuphnia magna Straus to different salini-ties were examined in paper II. Paper IIIcomprises studies of the regulation oflower trophic levels by D. mugnu and aninvertebrate predator, the backswimmerNotonecta sp. in the experimental rockpools. The direct and indirect impacts ofcadmium addition on trophic interactionswere also studied in the experimental foodwebs (IV). The last paper (V) presentsand compares the seasonal developmentin natural and experimental rock poolsand evaluates the relevance of theexperimental rock pool systems forecological studies.

7

The rock pool ecosystem

Scandinavian rock pools have beenclassified in different ways, for exampleaccording to salinity, distance from theshoreline, vegetation, area or durationalstability (permanent vs. ephemeral)(Levander 1900; Forsman 195 1; Ganning1971). The volume of rock pools rangesfrom a few litres to a few cubic meterswith weekly to monthly variationsdependent on season, volume, surface tovolume ra t io and the amount ofvegetation (Ganning & Wulff 1970;Ranta 1982; Bengtsson 1988). Rain,evaporation, sea spray and to lesser extentfreezing regulate the salinity of the rockpools. Annual salinity in medium sized(= lm3 ) freshwater and brackish waterpools normally fluctuates between 0 -4%0 S and 3 - 8 %O S, respectively(Ganning 1971; V). High concentrationsand large daily and seasonal fluctuationsof nutrients are common, reflecting thebiotic activities within pools as well asthe importance of nutrient additions byrain water run off (Ganning & Wulff1969; Wulff 1980; V). Rock pools aterarely anoxic, but large daily variations indissolved oxygen concentrations occur, asa consequence of primary production andrespiration in the pools. Normal dailyoxygen saturation levels in freshwater andbrackish water rock pools fhrctuatebetween 50 - 150% and 20 - 200 %,respectively (Ganning & Wulff 1970;personal observations). The primaryproduct iv i ty is usual ly high andautotrophic conditions generally prevailduring the summer season (Ganning &Wulff 1970).

The food webs of rock pools amsimple and the number of speciesgenerally increases with increasing poolsize (Ranta 1982). The small size of rock

8

pools means few microhabitats and alsolarge and rapid fluctuations in abioticvariables. The potential number ofspecies will thus be low. Salinity has asignificant influence on the distributionof planktonic algae, flagellates, daphnidsand rotifers in rock pools (J&rnefelt 1940;Droop 1953; Lagerspetz 1955; Bjorklund1972; Ranta 1982; V). However, manyof the inhabitants in rock pools tolerategreater fluctuations in salinity and otherabiotic variables than those normallyfound (see e.g Forsman 195 1; Ganning1967; 197 1). The habitat isolation makesdispersal more difficult and restrictscolonisation. Local extinctions of speciesin individual rock pools are common,whereas the species are present on aregional scale (within and among islands)(Hanski & Ranta 1983; Bengtsson 1988).The formation of dormant stages is acommon strategy in physically harsh andunpredictable environments (Hairston Jr.1987). This is common among zoo-plankton and many other groups of rockpool species (Ranta 1982). Water insects(imagines) and gammarids may escapewhen conditions deteriorate while otherspecies survive drought or freezing in thesediments. Other adaptations tounpredictable habitats are short lifecycles, rapid development to maturity andparthenogenetic reproduction. Living inephemeral or stressful habitats like rockpools may also offer advantages aspredators are relatively rare (Ganning1971; Sih 1987; Ranta & Espo 1989).

This thesis mainly deals with theecosystem of permanent freshwater rockpools (sensu Ganning 1971). The studiesof natural rock pools have been carriedout in the Askij area in the northernBaltic proper (Fig. 1). The distinctionsbetween different pools are not absoluteand permanent pools of intermediate

Fig. 1 The Baltic Sea and the study area (Asko).

freshwater - brackish water character havealso been studied (V). Typical freshwaterpools are situated high up on the shoreand have limnetic character. Most of theorganisms are planktonic whichfacilitates sampling (Wulff 1980).Primary producers are pelagic and benthicmicroalgae but also filamentous speciesoccur (Droop 1953; Ganning 1971;Hallfors 1984; Ranta et al. 1987, V).

Chironomid larvae and ostracods oftenlive associated with benthic parts of thepools. Common zooplankton aredaphnids (D. magna, D. longispina, D.pulex), Chydorus sphaericus, cyclopoidcopepods and rotifers. D. magna generallydominates the zooplankton community infreshwater rock pools (Ranta & Espo1989; V). This species is widely spreadgeographically, but the large size (adult

9

females 5-6 mm) restricts the disitri-bution to smaller habitats (eutrophicponds, bog lakes, rock pools), devoid ofplanktivorous fish (Hebert 1978). D.magna is an efficient generalistic filter-feeder and may ingest food particlesranging from bacteria to microplankton(diameter of 0.2 to 150 l.trn) (Scavia andFahnenstiel 1988; Stockner and Porter1988; Lair 1991; Kerfoot and Kirk 1991).D. magna tolerates low oxygenconditions, high pH and wide ranges ofsalinity and temperature (Kobayashi dzGondi 1985; MacIsaac ef al. 1985; II).When conditions deteriorate, reproduc-tion changes from parthenogenetic tosexual and resistant ephippial eggs areproduced. D. magna is thus well adaptedfor the unpredictable and variable rockpool habitat. Migration between poolsoccurs most likely by passive transportof ephippia by water, wind or birds(Ranta 1979). The small size,parthenogenetic reproduction, highfecundity, short life span and easyhandling in the laboratory have promotedthe use of D. magna in aquatic toxicitytesting, although its ecological relevancehas been questioned (Koivisto 1995).Other consumers are represented by waterinsects (i.e. corixid species, divingbeetles) and the amphipod Gammarusduebeni (Ganning 1971; Pajunen 1977;Ranta 1982; Bengtsson 1988). Theamphipod G. duebeni is the only speciesoccupying all types of rock pools aroundthe Swedish coast, but is practicallynever found in the littoral zone (Forsman195 1; Ganning 197 1). Compared to otherBaltic Gammarus species, its physio-logical capacities are well developed tocope with fluctuations in salinity,temperature and dissolved gases(Bulnheim 1984). It is most abundant inbrackish-water and freshwater pools and is

omnivorous (Forsman 195 1; personalobservations). The species hibernates inthe bottom substratum and may migrateover the rock between pools (Forsman195 1; Ganning 1971). Vertebrate pre-dators are absent in most rock pools. Tobe omnivorous or to have severaldifferent types of prey, is advantageous inthe limited and unpredictable rock poolhabitat.

Environmental stress

BackgroundEnvironmental stress is here defined as anenvironmental change that results in areduction of net energy balance andproduction (i.e. growth and reproduction)(Koehn & Bayne 1988). If the net energybalance of the organism is reduced as aresponse to environmental stress (naturalor antropogenic), it can be assumed thatfitness is reduced (Koehn & Bayne 1988).The net energy balance decreases if theinputs are decreased by lower feeding ratesor assimilation efficiency and/or if theenergy losses are increased by higherrespiration and excretion rates.Differential susceptibility of organismsand populations to environmental stressinfluence the outcome of b io t icinteractions and the organisation ofcommunities and ecosystems (Dunson &Travis 1991). However, it is difficult topredict the outcome of environmentalstress on interspecific interactions,community structure and ecosystemfunction by extrapolating the results fromsingle-species and life history ex-periments (Kimball & Levin 1985;Leblanc 1985; Levin et al 1 9 8 9 ;Clements & Kiffney 1994). To resolvethis problem, different types of multi-species model systems have been

10

developed (see e.g. Taub & Cow 1980;Borgmann et al. 1988; Heimbach et al1992, IV).

The responses to salinity changes andexposure to cadmium and diesel-oil isfocused in this thesis. Organisms livingin rock pools (e.g Gammarus duebeni andDaphniu magna) are frequently confrontedwith rapid and large changes of severalabiotic variables and their physiologicalcapacities are well developed to cope withirregular fluctuations in salinity, tem-perature and dissolved gases (Bulnheim1972, 1979; 1984; Kobayashi & Gondi1 9 8 5 ; MacIsaac et al. 1985; I, II).Deviations from normal salinitiesinfluence the metabolic rates ininvertebrates. Adaptations to subnormalsalinities and life in freshwater involvedevelopment of more efficient mecha-nisms for water elimination and saltuptake, as well as reduced surface per-meability and increased capacities of saltretention (Kinne 1964). Euryhalinespecies, e.g. the genus Gammurus, haveusually higher oxygen consumption andhigher ammonium excretion rates insubnormal salinities (Kinne 1964;Spaargaren 1984; I). Reduced numbers ofhatched eggs have been found for G.u’uebeni in freshwater as compared tobrackish water (Kinne 1964). Reducedreproductive performance and mfinal size have also been reported infreshwater animals penetrating into asaline environment (e.g. D. magna)(Kinne 1964; Cowgill & Milazzo 1990,199 1). Sublethal concentration ofcadmium have been shown to reduce oxy-gen consumption in marine crustaceans(Thurberg et al. 1973). Increased proteinturn-over and associated increases inrespiration have been found for D. mugnuwhen exposed to chronic cadmium stress(Barber et al. 1990). It has been suggested

that species which tolerate a high degreeof natural abiotic stress are more tolerantto pollution stress as well (Fisher 1977;Leblanc 1985; paper I).

The 0:N ratio, that describes therelative proportions of oxygen consumedto nitrogen excreted, has been used todescribe the physiological status ofinvertebrates (Bayne ef al. 1985; Mayzauddz Conover 1988; Tedengren 1990; I, II).This index reflects the balance betweenfat, carbohydrate and protein substrates inthe metabolism (Mayzaud & Conover1988). There is empirical evidence that alowering in the 0:N ratio is an indicationof environmental stress (W&lows &Phelps 198 1; Carr & Linden 1984; Axiak& George 1987; Tedengren 1990). Thenitrogen part of the index is usuallyestimated by the excreted ammonium,which is the dominant released nitrogencomponent in crustaceans. 80 - 90 % ofthe total released nitrogen in bothGammarus and Daphnia magna iscomposed of ammonium (Sutcliff 1984;Mayzaud & Conover 1988; Urabe 1993).However, respiration and excretion ratesof soluble nitrogen may be affected byother factors, e.g. food abundance (star-vation), food quality and body size, whichadd uncertainty to the use of thephysiological index. (Conover & Comer1968; Lampert dz Bohrer 1984; EjsmontKarbin 1984; Mayzaud & Conover 1988;Urabe 1993). The correspondence of thephysiological index and life historycharacteristics of D. magna exposed todifferent salinities was studied in paper II.

Environmental stress also affects therelative abundance of organisms inaquatic ecosystems both directly andindirectly. Increased mortality or decreasedreproduction are examples of directnegative effects and the indirect effectsarise when species have different tolerance

11

to toxicants (Koivisto 1996). Forexample, if the predator is relatively moresusceptible to environmental stress, theprey species may experience a positiveindirect effect of reduced predationpressure. On the other hand, if the preyspecies are less tolerant, the predator isnegatively affected as the food supply isreduced. Cladocerans are among the mostsusceptible species to various conta-minants and a common indirect effect ofpollution is a decline in cladoceran abun-dance followed by increases in phyto-plankton and rotifer abundance (Hurlbertet al. 1972; Hodson et al. 1979;Hamilton et al. 1988; Borgmann et al.1989; Hanazato & Yasuno 1990; Webberet al. 1992; Havens 1994).

Rock pool organisms and eflects ofsalinity changes and toxicants

The effects of environmental stress on themetabolism of one rock pool species(Gammurus duebeni ) and one littoralspecies (G. oceanicus) were studied inpaper I. The two Gammarus species amcommon along the whole Swedish coast,and organisms from both marine (NorthSea) and brackish water (Baltic Sea) areaswere studied. Both species are adapted tovariable environmental conditions,characteristic of both rock pools and thelittoral zone. However, G. duebeni ismore tolerant to fluctuations in e.g.salinity, temperature and oxygen levelsthan other Baltic Gummurus species, andwas regatded as a relatively more broad-niched species (Bulnheim 1984). Therock pool species was expected to hemore tolerant to both natural and man-induced stress. The results from thelaboratory experiments supported thishypothesis, and respiration and the 0:Nratio were less affected by salinity,changes and/or additions of diesel-oil and

cadmium in the rock pool species. TheBaltic populations of G. duebeni and G.oceanicus were generally more sensitiveto salinity changes and treatments withdiesel oil and cadmium than North Seaconspecifics. The higher sensitivity topollutants of the Baltic populations maybe due to a number of factors such aschanges in the characteristics of toxicsubstances (metals) with salinity, thehigher relative ionic concentration of agiven amount of poisonous substance inthe low saline Baltic Sea water ascompared to the North Sea water, anddirect interactions of toxicants withmembrane permeability and osmoregu-latory mechanisms, which are alreadyunder strain at low salinities.

A majority of cladoceran species amexclusively freshwater animals, althougha few genera have colonised salineenvironments. Daphnia magna is com-monly found in brackish water rock poolsand salinity is known to affect thedistribution. In paper II we investigatedthe effects of salinity on metabolism andlife history characteristics of rock pool D.magna. The lowest 0:N ratio were foundat 8%0 S (as compared to freshwater and4%0 S), indicating that the most stressfulconditions prevailed at the highestsalinity. Based on the 0:N ratio, thephysiologically most favourable con-ditions were at 4%0 S. The life historycharacteristics showed that the mostsuitable salinity for growth andreproduction of D. magna was 4%0 S,whereas the lowest population growthrate was obtained at the highest salinity.The results showed that high salinityaffected the physiological status of D.magna negatively, hampering repro-duction and growth. The physiologicalindex and the life history variables led tocomparable conclusions, although the life

12

history characteristics appeared to bemore sensitive indicators of the mostfavourable treatment.

Model systems andexperimental rock pools ’

BackgroundThe opinions of what is the mostrelevant temporal and spatial scales andexperimental methods for studyingcommunity and ecosystem ecologydiverge (Lawton 1996, Drake et al. 1996,Carpenter 1996). The realism andrelevance of natural systems are indis-putable, but the sometimes over-whelming complexity complicates theunderstanding and interpretation ofpatterns and processes. Drake et al.(1996) has argued “that this inherentcomplexity of nature is what makes theuse of laboratory microcosms bothdesirable, valid and necessary”.Experimental systems (micro- andmesocosms) are models of natural eco-systems, including a selected part of thebiological processes and interactions thatoccur in the field. Model ecosystemsshould be isolated, self-maintaining, in-clude more than one trophic level andmaintain the same functions as the partof the ecosystem which it is supposed torepresent (Lalli 1990). The spatial scaleof model systems range from indoorlaboratory bottles to large outdoor en-closures of nature. Most work hasfocused on smaller organisms with shortgeneration time such as bacteria, soilorganisms, protists or plankton (Drake etal. 1996, Verhoef 1996). In a survey ofarticles treating species interactions, Iveset al. (1996) found that microcosmstudies generally were shorter than fieldstudies measured in real time, but

generally covered as many or moregenerations of the selected organisms.

There are obvious advantages withmodel systems. The input and output ofenergy, material and organisms can becontrolled and the small scale and simplestructure facilitates replication, repetitionand sampling. Some of these positivefeatures are at the same time valid groundfor criticising of model systems. It hase.g. been claimed that model systems aregenerally too simple in structure andassembled of species lacking sharedevolutionary history. Furthermore, thereare difficulties in extrapolating the resultsfrom studies of limited model ecosystemsto real world effects, due to e.g. the lackof seasonality or density-independentdisturbances. Despite this criticism, themis a general agreement that modelsystems may offer a bridge between thesimplicity of mathematical models orsmall scale experiments and the fullcomplexity of real systems (Lawton1996, Drake et al. 1996, Verhoef 1996).Carpenter (1996) suggested that the mainrole of microcosms are supportive to fieldstudies and that they can be used toeliminate hypothesised mechanisms,compare alternative mechanisms orestimate rates. The model ecosystems atesuitable for ecotoxicological studies asthe interactions between species, indirecteffects of toxicants and the impacts ofabiotic factors on toxicity of chemicalscan be studied without damaging theenvironment.

The experimental rock pool systems:experience and evaluation

Trophic interactions and the regulation ofphytoplankton and zooplankton werestudied in experimental freshwatersystems with three food web con-figurations: 1. phytoplankton and small-

13

bodied zooplankton, 2. phytoplankton,small-bodied zooplankton and Duphniumagna and 3. phytoplankton, small-bodied zooplankton, D. mugnu and thebackswimmer Notonecta sp. (III, IV).The small-bodied zooplankton mainlyconsisted of Cyclops sp. and Chydorussphaericus. Water and plankton orga-nisms originated from freshwater rockpools. The outdoor experimental systemswere established in 55 L plastic tubs withsand and small stones as bottomsubstrate. Water, phytoplankton, zoo-plankton and Notonecta were addedsuccessively to allow stabilisation of thesystems. Cadmium and Notonecta were&led six weeks after water addition andthe experiment was terminated eightweeks later because of high Notonectamortality. The experimental systems hadprobably too low productivity or weretoo small to support a third trophic levelduring long term experiments. Theexperiment used two cadmium levels:controls (no cadmium) and the nominalconcentration of 20 ppb; in all sixtreatments with five replicates each. Theexperiment was static, with no waterrenewal, but cadmium was replenishedwhen concentrations fell below thedesired concentration. About once a week,the experimental rock pools were sampledfor the estimation of phosphate andammonium concentrations, phytoplank-ton biomass, primary productivity, zoo-plankton species composition and bio-mass. Ammonium was analysed as it isgenerally the main inorganic nitrogencompound in rock pools (Wulff 1980).The results are presented in two parts;firstly the effects of Notonecta and D.magna on lower trophic levels andnutrient concentrations (III) and secondlythe combined effects of trophic

manipulations and cadmium addition(IV).

Rock pools were chosen as “mother-systems” as they are small and isolatedhabitats per se and include tolerantspecies suitable for handling inexperimental situations. An additionaladvantage for the ecotoxicological part ofthe manipulations was that D. magna is anatural component of the zooplanktoncommunity. The artificial rock poolshave been evaluated by comparingpatterns of seasonal development innatural and experimental rock pools (V).Experimental rock pools with phyto-plankton, small-bodied zooplankton andDaphnia magna studied in 1992 and 1993(III, IV) were used in the comparison.

The food webs of the experimentalrock pools included important parts of thebiological processes and interactions innatural freshwater rock pools.Phytoplankton - herbivore communitieswith naturally co-occurring species werepossible to maintain several months, i.e.exceeding more than one generation ofthe included species. The seasonaldevelopment resembled natural rock poolswith permanent Daphnia presence and thepattern of low phytoplankton biomass inassociation with Duphniu presence wasfound in both natural and experimentalrock pools and is well-known from lakestudies. Most variables, with theexception of phytoplankton biomass,were in the range found in natural pools,but tended to vary less. The lowerphytoplankton biomass and the lowerdegree of fluctuations of the variablesstudied were probably Partly aconsequence of the absence of rain waterrunoff, which restricted the immigrationof algal species and the input of nutrientsand water from the surroundings.Occasional water inflows also dilute the

14

population of herbivores (the number ofindividuals L-’ decreases), which partlymay decrease the grazing pressure onphytoplankton populations in naturalrock pools.

Consumer and resourceregulation

Experience from lake and experimentalstudies

Fish predation has strong impact on thecomposition and size structure ofzooplankton communities (Zaret 1980;Kerfoot & Sih 1987). Visually foragingplanktivorous fish prey selectively onlarge zooplankton species, often resultingin a zooplankton community dominatedby small species (Brooks & Dodson1965; Zaret 1980). In fishless lakes andponds, where invertebrate predators maybe important, large zooplankton speciesdominate. The large size of Daphniamagna makes it vulnerable to fishpredation and restricts its distribution tofishless habitats (Brooks & Dodson1965; Pont et al. 1991). Althoughinvertebrates generally are considered asless efficient predators than fish, theymay also cause substantial reductions ofzooplankton prey species. This has beenshown for backswimmers (Notonecta),phantom midge larvae (Chaoborus) andcalanoid and cyclopoid copepods(Murdoch et al. 1984; Williamson 1987;Brett 1992; Arnott & Vanni 1993;Gliwicz dz Stibor 1993). Many inverte-brate predators (e.g. Chaoborus, calanoidcopepods, corixids, water beetles) prefersmaller prey that are easier to handle andingest (Swift & Federenko 1975;Williamson & Butler 1986; Williamson1987; Black & Hairston 1988). Incontrast to most invertebrates and like

fish, young backswimmers prey selec-tively on the largest size classes ofzooplankton (Scott & Murdoch 1983;Murdoch et al. 1984; III). Notonecta doesnot ingest its prey, but kills it by poisoninjected through the piercing mouth-partsafter which it sucks out the prey juices(Scott & Murdoch 1983). Notonecta is aneffective predator on daphnids, andcapable to eliminate them under naturalconditions (Murdoch et al. 1984).

The sca rc i ty o f small-bodiedzooplankton species in the presence oflarge-bodied species has been explainedby size-selective predation on small-bodied zooplankton species by inver-tebrate predators (Hall et al. 1970; Zaret1980; Vanni 1988; Arnott dz Vanni1993). Another possibility, the size-efficiency hypothesis, is that smallzooplankton are competitively suppressedby large-bodied (particularly daphnids)species that are more efficient filter-feeders (Brooks & Dodson 1965;Carpenter 1988; Arnott dz Vanni 1993).The competitive ability differs betweenlarge and small zooplankton and isinfluenced by e.g. the amount, qualityand frequency of food supply (Hall et al.1976; Gliwicz 8z Lampert 1990). Largedaphnids can ingest a larger size range offood particles than smaller cladocerans(Kerfoot 1987; Scavia and Fahnenstiel1988; Stockner and Porter 1988; Bern1990; Lair 199 1; Kerfoot and Kirk 1991).Consistently with the size-efficiencyhypothesis, large daphnids have beenshown to have lower food threshold andbe competitively superior to smallerDaphnia species at low and constant foodsupply under predator-free conditions(Gliwicz 1990). This is given by the factthat the assimilation rate increases morerapidly with increasing body size thanrespiration rate. The species with the

15

lowest food threshold may keep theresource level below the thresholdconcentration of other species sufficientlylong time to cause their exclusion. Thefood threshold is defined as the foodconcentration needed to assure thatassimilation equals respiration (Gliwicz1990). The competitive outcome can bereversed if filamentous algae are present,as larger cladoceran species are morenegatively affected by filaments (Gliwicz& Lampert 1990). The negative effectsarise due to reductions in ingestion ratesfor edible algae and increases inrespiration rates. The opposite view, thatfood threshold levels should be lower forsmall-bodied species and that small-bodied zooplankton should be com-petitively superior under low food levelsdue to higher foraging efficiency ofsmaller species on smaller particles, hasalso been shown (Dodson 1974; Neil11975; Tessier & Goulden 1987; Koivistoet al. 1992).

Fish manipulations in lakes have repeatedly demonstrated the existence oftrophic cascades. Commonly, increasedphytoplankton biomass follows theaddition or increase of planktivorous fish(see e.g. Carpenter 1988). Proposedmechanisms are reduced grazing rates,changes in the zooplankton communityto a dominance of smaller species withhigher nutrient regeneration rates perweight and recycling of nutrients by theplanktivore (Vanni & Findlay 1990).There are few experimental studies ofindirect effects of invertebrate predatorson phytoplankton (III). In a mesocosmstudy, Vanni and Findlay (1990) foundthat fish and the invertebrate predatorChaoborus caused similar reductions inzooplankton biomass. However, thephytoplankton biomass increased only inthe presence of fish. Their result

suggested that fish, but not Chaoborus,increased the availability of phosphorus,thereby promoting phytoplanktongrowth.

Numerous studies have shown that acombination of predation and resourcelimitation typically regulates freshwaterplankton populations and drives seasonalsuccessions (Threlkeld 1987; Hu &Tessier 1995; III). Data collected infreshwater ecosystems have generallyshown that resource regulation, withpositive relationships between prey (orresource availability) and consumerbiomass, is more important at the base ofthe food chain (McQueen et al. 1986).Predation or top down regulation, has itsmain support from experimental mani-pulations. It appears to be mostimportant at the top of food chains andhas been manifested as negative relation-ships between planktivore and zoo-plankton biomass and between large-bodied zooplankton (e.g. Daphnia) andphytoplankton biomass (McQueen et al.1986; Carpenter & Kitchell 1 9 9 2 ;Mazumder 1994; III).

Predation and competition in rock poolsystems

The effects of predation and zooplanktoncompetition have also been examined inrock pools. Invertebrate predatorsdominate in rock pools and fish isnormally absent. Introduction of fish innatural rock pools eliminated Daphniamagna, followed by an increase in thenumber of small-bodied species (Ranta etal. 1987). The number of phytoplanktoncells increased in two out of threemanipulations. In a study in experimentalrock pools, we found that three spined-stickleback (Gasterosteus aculeafus) eli-minated the D. magna population, fol-lowed by an increase in phytoplankton

16

biomass (At-n& & Koivisto personal ob-servations). In a laboratory study, Rantaand Espo (1989) found that rock poolcorixids and water beetles preyed on bothchironomid larvae and D. magna. Thewater insects preferred chironomids andonly small size classes of Daphnia wefecaptured. It has also been demonstratedthat corixids are able to decimatechironomids in natural rock pools(Pajunen & Salmi 1991), but it is lesslikely that the usually small water insectpopulations am able to regulate thedominating Daphnia populations in rockpools (Ranta & Espo 1989). Gammarusduebeni is omnivorous, capable to reduceD. magna populations under laboratoryconditions, and is also able to feed onmacroscopic green algae (Enteromotphasp.) (personal observations). Among theherbivorous species in freshwater rockpools, the cladocerans of the genusDaphnia and Chydorus sphaericus snregeneralistic filter feeders. In contrast tothe size-efficiency hypothesis, it has beenshown that growth and reproduction ofChydorus sphaericus at-e less affected bylow food levels than is D. magna(Koivisto et al. 1992). Within the genusDaphnia in rock pools, the smallestspecies (D. Zongispina) is competitivelysuperior to the largest species (D. magna)(Hanski & Ranta 1983). The trophicposition of the cyclopoid copepods isunclear. It has in the present studies beenassumed that Cyclops sp. change fromherbivory (nauplia) to carnivory (adults)during their ontogeny (Morgan 1980;Sprules 1988; Soto 1991; Adrian 1991).Cyclopoid copepodites may furthermoreenter the brood pouch of daphnids andprey on eggs (Gliwicz & Stibor 1993;Gliwicz & Lampert 1994).

Consumer regulation of lower trophiclevels by Notonecta and Daphnia in

experimental rock poolsThe regulation of phytoplankton andzooplankton by the backswimmerNotonecta and D. magna was studied inexperimental rock pools with two andthree trophic levels (III). The back-swimmer was added after an initial stabi-lisation period of six weeks, and theexperiment was terminated eight weekslater, due to high Notonecta mortality. Inthe two trophic level treatments, wepredicted lower phytoplankton biomass inthe presence of Daphnia, as compared tothe treatment with small-bodied zoo-plankton. We also expected Notonecta toreduce Daphnia, followed by an increasein phytoplankton biomass. The result ofthe manipulations showed that consumerregulation was a dominant force indetermining the biomass of phyto-plankton and Daphnia in a planktonicrock pool community. While Daphniareduced phytoplankton production andbiomass, small-bodied zooplankton(Cyclops and Chydorus) increased withincreasing phytoplankton biomass. Thissuggest that they were food limited and anegative correlation with Daphniabiomass hence indicates interspecificcompetition for limited resources. Thepresence of the invertebrate predatorNotonecta produced a top-down effectwhich was similar to that reported forplanktivorous fish, i. e. a reduction ofDaphnia followed by an increase ofsmall-bodied zooplankton species andphytoplankton biomass. Notonecta selec-tively preyed on Daphntit and the intensepredation reduced the Daphnia populationwhich was extinct within four weeks.The backswimmer seemed unable to useChydorus or Cyclops sis food resource andstarved to death after the extinction of the

Duphniu population. Ultimately, how-ever, resource availability determined thebiomass at each trophic level. The foodlimitation of zooplankton was indicatedby low egg ratios of Duphnia and apositive response of small-bodied zoo-plankton to increased phytoplankton bio-mass. The production of resource-limitedDuphnia could not support Notonectuwhich starved to death after the extinctionof Duphniu.

Efsects of cadmium addition on trophicinteractions in rock pool food webs

The effects of cadmium addition werestudied parallel to the above describedtrophic manipulations (IV). We used acontrol (no cadmium added) and anominal cadmium concentration of 20ppb. Cadmium was added at the sametime as Notonectu. Cladocerans (Duphniuand Chydorus) were assumed to be themost susceptible species (Hurlbert et al.1972; Hodson et al. 1979; Hamilton eta l . 1 9 8 8 ; Borgmann e t a l . 1 9 8 9 ;Hanazato & Yasuno 1990; Webber et al.1992; Havens 1994), and an indirectpositive effect on phytoplankton,comparable to that of Notonectu additionwas expected. A significant cadmium xNotonectu interaction was also expected,i. e. a stronger reduction of Daphniawhen simultaneously exposed to bothmortality factors. Cadmium had anegative effect on all trophic levels, butthe results did not support thehypothesis. The added cadmium stronglyinhibited the phytoplankton production,which did not respond positively to

Duphniu biomass.Consequently, cadmium addition andpredation by Notonectu did not causesimilar effects in rock pool food webs.The backswimmer was a more efficient.predator on Duphniu than expected, and

eliminated the population within fourweeks. Daphnids subjected to Notonectupredation disappeared simultaneouslyfrom control and cadmium treatments,and the cadmium x Notonectu interactionwas insignificant.

Conclusions

Rock pool organisms are well adapted tolarge fluctuations in abiotic factors. Thisis exemplified in this thesis by a higherphysiological tolerance to salinitychanges in rock pool Gummarus duebenias compared to littoral G. oceunicus. Therock pool gammarid was less affected byadditions of diesel-oil and cadmium.Salinity is one of the variables thatrestricts the distribution of species inrock pools and high salinity negativelyaffected the physiological status of D.magna, leading to negative effects ongrowth and reproduction. The physio-logical index (0:N ratio) and life historyvariables led to comparable conclusions,supporting the relevance of thephysiological index. It has also beenshown that D. magna is more tolerant toe.g. copper than are other cladocerans(Koivisto et al. 1992), thus indicatingthat species tolerant to high degrees ofnatural abiotic stress are also moretolerant to pollution stress (Fisher 1977;Leblanc 1985).

The relevance of a particular ex-perimental system can be discussed ontwo levels: Firstly, does the modelsystem mimic the natural system it issupposed to represent? To evaluate ourexperimental units it can be concludedthat the seasonal development resemblednatural rock pools with permanentDuphniu magna presence. The patterns oflower phytoplankton biomass in asso-

18

ciation with Daphnia presence was foundin both natural and experimental rockpools and is well-known from lakestudies. Most variables, with theexception of phytoplankton biomass,were in the range found in natural poolsbut tended to be less variable. The lowerphytoplankton biomass and the lowerdegree of fluctuations were probablypartly an effect of the absence of waterinflow. However, this was an inevitableconsequence of the experimental set-up.Secondly, is the “original” systemecologically representative for otherecosystems, i.e. can we extrapolate fromthe particular to the general? Freshwaterrock pools differ in several ways fromlakes: The fluctuations in physico-chemical variables are larger in rockpools and probably influence the outcomeof biotic interactions and the organisationof communities to a higher degree than inlakes. The food webs are simple, andplanktivores are mainly represented bygeneralistic invertebrates unlikely toregulate the dominant daphnids. Thus, the“pelagic” part of rock pools are not simi-lar to that of most lakes. However, rockpools may fairly well approximate otherfishless habitats like ponds and bog lakesor a lake situation with low planktivorebiomass due to high piscivore abundance.As shown by this thesis, tolerance toabiotic variables may also implyincreased tolerance to pollutants and theuse of rock pool systems may thusunderestimate the impact of toxic com-pounds. On the other hand, if direct orindirect effects arise in this type ofsystems, they will probably also ariseelsewhere.

In my opinion, experimental eco-systems can be used to disclose potentialdirect and indirect impacts of e.g.addition/removal of species or environ-

mental stress. The results from theexperimental rock pools showed that thesize-selective invertebrate predatorNotonecta in low densities has thepotential to produce indirect positiveeffects on phytoplankton and smallzooplankton. This can be of importancein other fishless habitats. The addition ofcadmium negatively affected all trophiclevels, but the sens i t iv i ty differedbetween organisms (the studied clado-cerans were more affected than Cyclops).If a corresponding change, from clado-ceran to copepod dominance, occurs innatural freshwater systems, it will havemajor impact on phytoplankton biomassand the diet of planktivores. I suggestthat the experimental rock pools systemsam m o s t appropriate for studyinginteractions between phytoplankton andzooplankton or interactions withinzooplankton. Manipulations of levels andqualities of food supply as well as ofabiotic variables and toxicants could bepossible.

References

Adrian R. (1991) Filtering and feedingrates of cyclopoid copepods feeding onphytoplankton. Hydrobiologia, 210:217-223.

Arnott S.E. & Vanni M.J. (1993)Zooplankton assemblages in fishlessbog lakes: influence of biotic andabiotic factors. Ecology, 74: 2361-2380.

Astles K.L. (1993) Patterns of abundanceand distribution of species in intertidalrock pools. J. Mar. Biol. Ass., 73:555-569.

Axiak V. 8z George J.J. (1987)Bioenergetic responses of the marinebivalve Venus verrucosa on long-term

19

Clements W.H. & Kiffney P.M. (1994)Assessing contaminant effects athigher levels of biological orga-nisation. Freshwater Biology, 2 1:483-488.

Conover R.J. & Comer E.D.S. (1968)Respiration and nitrogen excretion bysome marine zooplankton in relationto their life cycles. J. Mar. Biol. Ass.48:49-75

Cowgill U.M. & Milazzo D.P. (1990)The sensitivity of two chulocerans towater quality variables: salinity andhardness. Arch. Hydrobiol. 120: 185-196

Cowgill U.M. & Milazzo D.P. (1991)Demographic effects of salinity, waterhardness and carbonate alkalinity onDaphnia magna and Ceriu&phrriadubia. Arch. Hydrobiol. 122:33-56.

Dodson S.I. (1974) Zooplanktoncompetition and predation: anexperimental test of size-efficiencyhypothesis. Ecology, 55: 605613.

Drake J. A., Huxel G.R. & Hewitt C.L.(1996) Microcosms as models forgenerating and testing communitytheory. Ecology, 77: 670-677.

Droop M.R. (1953) On the ecology offlagellates from some brackish andfreshwater rockpools of Finland. ActaBot. Fennicia, 5 1: l-52.

Dunson W.A. & Travis J. (1991) Therole of abiotic factors in communityorganization. Am. Nat., 138: 1067-1091.

Ejsmont-Karbin J. (1984) Phosphorousand nitrogen excretion by lakezooplankton (rotifers and crustaceans)in relationship to individual bodyweights of the animals, ambienttemperature and presence of food.Ekol. Pol., 32: 3-42.

Fisher N.S. (1977) On the differentialsensitivity of estuarine and open-

ocean diatoms to exotic chemicalstress. Am. Nat., 111: 871-895.

Forsman B. (1951) Studies on Gammarusduebeni Lillj., with notes on somerock pool organisms in Sweden.2001. Bidrag, Uppsala, Bd 29: 215-237.

Ganning B. (1967) Laboratory experi-ments in the ecological work onrockpool animals with special noteson the ostracod Heterocypris salinus.Helgolander wiss. Meeresunters., 15:27-40.

Ganning B. & Wulff F. (1969) Theeffects of bird droppings on chemicaland biological dynamics in brackishwater rock pools. Oikos, 20: 274-286.

Ganning B. 8z Wulff F. (1970)Measurements of community metabo-lism in some Baltic brackish waterrockpools by means of die1 oxygencurves. Oikos, 21: 292-298.

Ganning B. (1971) Studies on chemical,physical and biological conditions inSwedish rockpool ecosystems.Ophelia, 9: 51-105.

Ghwicz Z.M (1990) Food thresholds andbody size in cladocerans. Nature, 343:638640.

Gliwicz Z.M. & Lampert W. (1990)Food thresholds and body size inDaphnia species in the absence andpresence of blue-green filaments.Ecology, 7 1: 69 l-702.

Gliwicz Z.M. & Stibor H. (1993) Eggpredation by copepods in Daphniabrood cavities. Oecologia, 95: 295-298.

Gliwicz Z.M. & Lampert W. (1994)Clutch-size variability in Daphnia:Body-size related effects of egg-predation by cyclopoid copepods.Limnol. Oceanogr.; 39: 479-485.

21

Hairston Jr. N.G. (1987) Diapause as apredator-avoidance adaptation. In:Predation. Direct and indrect impactson aquatic communities. W. C.Kerfoot, & A. Sih, University Pessof New England, Hanover ‘andLondon, 28 1-299.

Hall D.J., Cooper W.E. & Werner E.E.(1970) An experimental approach tothe production dynamics and structureof freshwater animal communities.Limnol. Oceanogr., 15: 839-928.

Hall D.J., Threlkeld S.T., Burns C.W. &Crowley P.H. (1976) The size-efficiency hypothesis and the sizestructure of zooplankton com-munities. Ann. Rev. Ecol. Syst., 7:177-208.

Hamilton P.B., Jackson G.S., KaushikN.K., Solomon K.R. & StephensonG.L. (1988) The impact of twoapplications of atrazine on the plank-ton communities in situ enclosures.Aquat. Toxicol., 13: 123-140.

Hanazato T. & Yasuno M. (1990)Influence of time of application of aninsecticide on recovery patterns of azooplankton community in experi-mental ponds. Arch. Environ.Contam.‘Toxicol. 19: 77-83.

Hanski I. & Ranta E. (1983) Coexistencein a patchy environment: Threespecies of Daphnia in rock pools. J.Anim. Ecol., 52: 263-279.

Havens K.E. (1994) An experimentalcomparison of the effects of twochemical stressors on a freshwaterzooplankton assemblage. Environ.Pollut. 84:245-251.

HIllfors G. (1984) Filamentous rock-pool algae in t h e Tv&-minnearchipelago, S. east coast of Finland.Acta Bot. Fennica 126: l- 111.

Hebert P. D.N. (1978) The populationbiology of Daphnia (Crustacea,Daphnidae). Biol. Rev., 53: 387-426.

Heimbach F., Pflueger W. & Ratte H.-T.(1992) Use of small artificial pondsfor assessment of hazards to aquaticsystems. Environ. Toxicol. Chem.11:27-34

Hodson P.V., Borgmann U. & Shear, H.(1979) Toxicity of copper to aquaticbiota. In: Copper in the environment.part II: Health effects. J. 0. Nriagu,Joh Wiley & Sons, New York, 307-372.

Hu S.S. & Tessier A.J. (1995) Seasonalsuccession and the strength of intra-and interspecific competition in aDaphnia assemblage. Ecology, 76:2278-2294.

Hurlbert S.H., Mulla M.S. & WilsonH.R. (1972) Effects of anorganophosphorous insecticide on thephytoplankton, zooplankton, andinsect populations of fresh-waterponds. Ecol. Monogr., 42: 269-299.

Ives A.R., Foufopoulos J., Klopfer E.D.,Klug J.L. & Palmer T.M. (1996)Bottle or big-scale studies: How dowe do ecology? Ecology, 77: 681-685.

Jarnefelt H. (1940) Beobachtungen tiberdie Hydrologie einiger Scharetiimpel.Verh. Int. Ver. Theoret. Angew.Limn., 9: 79-101.

Kerfoot W.C. (1987) Cascading effectsand indirect pathways. In: Predation.Direct and indirect impacts on aquaticcommunities. Kerfoot W.C. & SihA., University Press of New England,Hanover, 57-70.

Kerfoot W.C. & Kirk K.L. (1991)Degree of taste discrimination amongsuspension-feeding cladocerans andcopepods: Implications for detrivory

22

and herbivory. Limnol. Gceanogr.,36: 1107-l 123.

Kerfoot W.C. & Sih A. (1987)Predation: Direct and Indirect Impactson Aquatic Communities. UniversityPress of New England, Hanover, NH:

Kimball K.D. & Levin S.A. (1985)Limitations of laboratory bioassays:the need for ecosystem level testing.Bioscience, 35: 165171.

Kinne 0. (1964) The effects oftemperature and salinity on marineand brackish water animals. II.Salinity and temperature salinitycombinations. Gceanogr. Mar. Biol.Ann. Rev. 2:281-339

Kobayashi M. & Gondi H. (1985)Horizontal moving of pale and redDaphniu magna in low oxygenconcentration. Physiol. Zool., 58:190- 196.

Koehn R.K. & Bayne, B.L. (1988)Towards a physiological and geneticalunderstanding of the energetics of thestress response. In: Evolution,ecology and environmental stress.Calow P., & Berry R.J., AcademicPress, London, 157- 171.

Koivisto S., Ketola M. & Walls M.(1992). Comparison of five cladoceranspecies in short- and long-term copperexposure. Hydobiologia 248: 125-136.

Koivisto S. (1995) Is Duphniu magnuecologically representative? Environ.Pollut., 90: 263-267.

Koivisto S. (1996) Toxicity testing froman ecological perspective: life historyand food web studies withCladocerans. Thesis. StockholmUniversity.

Lagerspetz K. (1955) Physiologicalstudies on the brackish water toleranceof some species of Daphnia. Arch.Sot. “Vanamo”, 9:Suppl.: 138-143.

Lagerspetz K. (1958) The brackish-watertolerance of some freshwaterCrustaceans. Verh. internat. Ver.Limnol., 13: 718-721.

Lair N. (199 1) Grazing and assimilationrates of natural populations ofplanktonic cladocerans in an eutrophiclake. Hydrobiologia, 2 15: 5 l-61.

Lalli CM. (1990) Enclosed experimentalmarine ecosystems: a review andrecommendations. Springer-Verlag,New York.

Lampert W. & Bohrer R. (1984) Effect offood availability on the respiratoryquotient of Daphnia magna. Comp.B&hem. Physiol. 78A:221-223.

Lawton J.H. (1996) The Ecotron facilityat Silwood Park: The value of “Bigbottle” experiments. Ecology, 77:665-669.

Leblanc G-A. (1985) Effects of copper oncompetitive interactions of twospecies of cladocera. Environ. Pollut.37: 13-25.

Levander K.M (1900) Zur Kenntnis &slebens in den stehenden Kleinge-wiissem auf der Sktieninseln. ActaSot. Fauna Flora 18: l-107.

Levin S.A., Harwell M.A., Kelly J.R. &Kimball K.D. (1989) Ecotoxicology:Problems and approaches. In: LevinS.A., Harwell M.A., Kelly J.R. &Kimball K.D. (Eds.) Ecotoxicology:Problems and approaches. Springer-Verlag, New York pp 3-7.

Lindberg (1944) Gkologisch-Geographische Untersuchungen zurInsecten Fauna der Felsenttimpeln ander Ktisten Finnlands. Acta zool.Fenn., 41: 1-178.

Loder III T.C., Ganning B. & Love, J.A.(1996) Ammonia nitrogen dynamicsin coastal rockpools affected by gullguano. J. Exp. Mar. Biol. Ecol., 196:113-129.

23

MacIsaac H . J . , Hebert P . D . N . &Schwartz S.S. (1985) Inter- andintraspecific variation in acute thermaltolerance of Duphniu. Physiol. Zool.,58: 350-355.

Mayzaud P., Conover R.J. (1988) 0:Natomic ratio as a tool to describezooplankton metabolism. Mar. Ecol.Prog. Ser., 45: 289-302.

Mazumder A. (1994) Patterns of algalbiomass in dominant odd- vs even-link lake ecosystems. Ecology, 75:1141-l 149.

McQueen D.J., Post J.R. & Mills E.L.(1986) Trophic relationships infreshwater pelagic ecosystems. Can.J. Fish. Aq., 43: 1571-1581.

Metaxas A. & Scheibling R.E. (1993)Community structure and organi-zation of tidepools. Mar. Ecol. Prog.Ser., 98: 187-198.

Morgan N.C. (1980) Secondaryproduction. In: The functioning offreshwater ecosystems. LeCren E.D.,& Low-McConnell R.H., CambridgeUniversity Press, Cambridge, 25 l-267.

Murdoch W.W., Scott M.A. & EbsworthP. (1984) Effects of the generalpredator Notonecta (Hemiptera) upona freshwater community. J. Anim.Ecol., 53: 791-808.

Neil1 W.E. (1975) Experimental studiesof microcrustacean competition,community composition andefficiency of resource utilization.Ecology, 56: 605-624.

Norberg J. & DeAngelis D.L. (1997)Temperature effects on stocks andstability of a phytoplankton-zooplankton model and the dependenceon light and nutrients. Ecol. Model.,95: 75-86.

Pajunen V.I. (1977) Population structurein rock pool corixids (Hemiptera,

Corixidae). Ann. Zool. Fennici, 14:26-47.

Pajunen V.I. (1990) The populationdynamics of rock-pool corixids livingon supplementary food (Hemiptera,Corixidae). Ann. Zoo]. Fennici, 27:337-350.

Pajunen V.I. & Salmi J. (1991) Theinfluence of corixids on the bottomfauna of rock-pools. Hydrobiologia,222: 77-84.

Pont D., Crivelli, A.J. & Guillot F.(199 1) The impact of three-spinedstickle-backs on the zooplankon of apreviously fish-free pond. FreshwaterBiology, 26: 149-163.

Ranta E. (1979) Niche of Duphniuspecies in rock pools. Arch.Hydrobiol., 87: 205-223.

Ranta E. (1982) Animal communities inrockpools. Ann. Zool. Fennici, 19:337-348.

Ranta E. & Nuutinen V. (1985) Foragingb y t h e s m o o t h n e w t (7’riturusvulgar-is) on zooplankton: functionalresponses and diet choice. J. Anim.Ecol., 54: 275-293.

Ranta E., Hallfors S., Nuutinen V.,Hallfors G. & Kivi K. (1987) A fieldmanipulation of trophic interactionsin rock-pool plankton. Oikos, 50:336-346.

Ranta E. & Espo, J. (1989) Predation bythe rock-pool insects Arctocorisacurinuta, Cullicorim productu ( H e t .Cor ix idae ) and Potamonectesgriseostriatus (Col. Dytiscidae). Ann.Zool. Fennici, 26: 53-60.

Scavia D. & Fahnenstiel G.L. (1988)From picoplankton to fish: Complexinteractions in the Great Lakes. In:Complex interactions in lakecommunities. Carpenter S.R. (Ed.),Springer-Verlag, New York, pp 85-97.

24

Scott M.A. & Murdoch W.W. (1983)Selective predation by thebackswimmer, &tone&z. Limn.Oceanogr., 28: 352-366.

Sih A. (1987) Predators and preylifestyles: An evolutionary andecological overview. In: Predation.Direct and indirect impacts on aquaticcommunities. Kerfoot W.C. & SihA., University Press of New England,Hanover and London, 203-224.

Soto D. & Hurlbert, S.H. (1991) Shortterm experiments on calanoid-cyclopoid-phytoplankton interactions.Hydrobiologia, 215: 83-l 10.

Spaargaren D.H. (1984) The ammoniumexcretion of shore crab, Car&usmaenus, in relation to environmentalosmotic conditions. Nether. J. SeaRes. 15273-283.

Sprules W.G. & Bowetman J.E. (1988)Omnivory and food chain length inzooplankton food webs. Ecology, 69:418-426.

Stockner, J.G. & Porter KG. (1988)Microbial food webs in freshwaterplanktonic ecosystems. In: Complexinteractions in lake communities.Carpenter S.R.(Ed.), Springer Verlag,New York, pp 69-83.

Sutcliff D.W. (1984) Quantitative aspectsof oxygen uptake by Gammarus(Crustacea, Amphipoda): a criticalreview. Freshwater Biology 14: 443-489.

Swift M.C. & Federenko A.Y. (1975)Some aspects of prey capture byChaoboms larvae. Limnol.Oceanogr., 20: 4 18-425.

Taub F.B. & C o w M . E . ( 1 9 8 0 )Synthesising aquatic microcosms. In:Giesy J.P. Jr. (Ed.) Microcosms inecological research. TechnicalInformation Center, U.S. Departmentof Energy, pp 69- 103.

Tedengren M. (1990). Ecophysiology andpollution sensitivity of Baltic Seainvertebrates. Thesis, StockholmUniversity.

Tessier A.J. & Goulden C.E. (1987)Cladoceran juvenile growth. Limnol.Oceanogr., 32: 680-686.

Threlkeld S.T. (1987) Experimentalevaluation of Trophic-Cascade andnutrient mediated effects ofplanktivorous fish on planktoncommunity structure. In: Predation:Direct and indirect impacts on aquaticcommunities. Kerfoot W.C. & SihA., University Press of New England,Hanover, 161-173.

Thurberg F.P., Dawson M.A: & CollierR.S. (1973) Effects of copper andcadmium on osmoregulation andoxygen consumption in two speciesof estuarine crabs. Mar. Biol. 23: 171-175.

Underwood A.J. & Skilleter G.A (1996)Effects of patch-size on the structureof assemblages in rock pools. J. Exp.Mar. Biol. Ecol., 197:63-90.

Urabe J. (1993) N and P cycling coupledwith grazers’activities: Food qualityand nutrient release by zooplankton.Ecology, 74: 2337-2350.

V a n n i M . J . (1988) Freshwaterzooplankton community structure:introduction of large invertebratepredators and large herbivores to asmall-species community. Can. J .Fish. Aquat. Sci., 45: 1758-1770.

Vanni M.J. & Findlay, D.L. (1990)Trophic cascades and phytoplanktoncommunity structure. Ecology, 71:921-937.

Vepsilainen K. (1978) Coexistence oftwo competing corixid species(Heteroptera) in an archipelago oftemporary rock pools. Oecologia, 37:177-182.

25

Verhoef H. A. (1996) The role of soilmicrocosms in the study of ecosystemprocesses. Ecology, 77: 685-690.

Webber E.C, Deutsch W.G., Bayne,D . R . & Seesock W . C ( 1 9 9 2 )Ecosystem-level testing of a syntheticpyrethroid insecticide in aquaticmesocosms. Environ. Tox. Chem.11:87-105

Widdows J. & Phelps D.K (1984)Measurement of physiologicalcondition of mussels transplanteda long a pollution gradient inNarragansett Bay. Mar. Environ. Res.4:181-194.

Williamson C.E. & Butler N.M. (1986)Predation on rotifers by thesuspension-feeding calanoid copepod

Diaptomus pallidusOceanogr., 3 1: 393-402.

Limnol.

Williamson S.E. (1987) Predator-preyinteractions between omnivorousdiaptomid copepods and rotifers: therole of prey morphology andbehaviour. Limnol. Oceanogr., 32:167-177.

Wulff F. (1980) Animal communitystructure and energy budgetcalculations o f Daphnia magna(Straus) population in relation to therock pool environment. Ecol. Model.,11: 179-225.

Zaret T.M. (1980) Predation andfreshwater communities. YaleUniversity Press, New Haven andLondon.

26


Top Related