Download Organisms and food webs in rock pools

Organisms and food webs in rock pools:
Responses to environmental stress and trophic
manipulation
Marie Arn6r
Department of Zoology, Stockholm University
S-106 91 Stockholm, Sweden
Stockholm 1997
Doctoral dissertation 1997
Marie Am&
Department of Zoology
Stockholm University
S-106 91 Stockholm
[email protected]
0 1997 Marie Am&
ISBN 9 l-87272-53-9
Printed by Jannes Snabbtryck AB, Stockholm
Cover by Bibbi Mayrhofer
2
ERRATA
Organisms and food webs in rock pools:
Responses to environmental stress and trophic manipulation
by
Marie Arner
page line written
Summary
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9
(1992) Physiological and life
history responses of Duphnia magna to increasing salinity
(submitted manuscript)
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13
10
10
11
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23
right 20 Koehn & Bayne 1988
right 24 Koehn & Bayne 1988
right 32 ..physiological index. (..
left 21 (1996) has argued...
left 22 Koehn R.K. &‘Bayne, B.L
(1988)
Paper III
4
left 18 . ..The water was sieved..
right 41 and nauplia to Cyclops
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Paper IV
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left 21
. . . Daphnia generally had lower
biomass...
Paper V
right 8 of salinity tolerance of the
3
DaphnM
right 24 The ratios of nauplia to Cyclops
5
should be
(1993) Effects of salinity
on metabolism and life
history characteristics of
Daphnia magna
(accepted for publication in
Freshwater Biology)
Koehn & Bayne 1989
Koehn & Bayne 1989
..physiological index (...
(1996) have argued...
Koehn R.K. & Bayne
B.L (1989)
The water (50 L tub-‘) was sieved
and nauplia to total Cyclops
. . . Duphnia generally had higher
biomass.. .
of salinity tolerance of Daphnia
The ratios of nauplia to total
Cyclops
To my family
Abstract
Differential susceptibility of organisms and populations to environmental stress influences the outcome of biological interactions and the structure of communities and
ecosystems. In this thesis, the effects of environmental stress on organism, population
and community levels were studied. ‘Die physiological responses to changes in salinity
and exposure to pollutants were studied by comparing rock pool Gammurus duebeni and
littoral G. oceanicus with different tolerance to abiotic stress. Physiological and life
history responses of rock pool Duphnia magna to different salinities were examined. Ex-,
perimental systems, originating from natural rock pools, were established to explore
direct and indirect impacts of cadmium and predator addition in freshwater plankton communities. Three different food web configurations were used: 1. phytoplankton and
small-bodied zooplankton (Cyclops sp. and Chydorus sphaericus), 2. phytoplankton,
small-bodied zooplankton and D. magna, and 3. phytoplankton, small-bodied zooplankton, D. magna and the invertebrate predator Notonectu sp. To evaluate the experimental
systems, 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 less
affected by natural stress and pollutants than G. oceanicus. The physiological and life
history responses led to comparable conclusions in D. magna: i.e., salinity stress
negatively affected the physiological status of D. mugnu and hampered reproduction and
growth. In the experimental food webs, cadmium inhibited phytoplankton productivity
and decreased the biomass of cladocerans. Cadmium did not change the trophic
interactions between Duphniu and phytoplankton or between Duphniu and Notonectu.
The regulation of lower trophic levels by Duphniu and Notonecta 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-herbivore communities for several months. The experimental systems
resembled natural rock pools with permanent D. mugnu presence. Phytoplankton
biomass was regulated by D. magna when the species was permanently present in both
natural and experimental rock pools. Experimental rock pools may approximate other
fishless habitats and the spatial and temporal scales are most appropriate for studies of
plankton 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 Stockholms
Universitet offentligen forsvaras torsdagen den 29 maj 1997, kl. 10.00 i
fiirelfsningssalen, Frescati Backe, Svante Arrhenius vag 21 A, Frescati
MarieavArnCr
Zoologiska Institutionen
Stockholms Universitet
S-106 91 Stockholm
Stockholm 1997
ISBN 9 l-87272-53-9
Abstract
Differential susceptibility of organisms and populations to environmental stress influences the outcome of biological interactions and the structure of communities and
ecosystems. In this thesis, the effects of environmental stress on organism, population
and community levels were studied. The physiological responses to changes in salinity
and exposure to pollutants were studied by comparing rock pool Gummurus duebeni and
littoral G. oceanicus with different tolerance to abiotic stress. Physiological and life
history responses of rock pool Duphniu magna to different salinities were examined, Experimental systems, originating from natural rock pools, were established to explore
direct and indirect impacts of cadmium and predator addition in freshwater plankton communities. Three different food web configurations were used: 1. phytoplankton and
small-bodied zooplankton (Cyclops sp. and Chydonrs sphuericus), 2. phytoplankton,
small-bodied zooplankton and D. magna and 3. phytoplankton, small-bodied zooplankton, D. mugnu and the invertebrate predator Nofonectu sp. To evaluate the experimental
systems, 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 by
natural stress and pollutants than G. oceunicus. The physiological and life history responses led to comparable conclusions in D. magna: i.e., salinity stress negatively aflected the physiological status of D. magna and hampered reproduction and growth. In the
experimental food webs, cadmium inhibited phytoplankton productivity and decreased
the biomass of cladocerans. Cadmium did not change the trophic interactions between
Duphniu and phytoplankton or between Duphniu and Notonectu. The regulation of lower
trophic levels .by Duphniu and Notonectu was important in the experimental food webs.
Notonectu produced a indirect positive (cascade) effect on phytoplankton and smallbodied zooplankton. It was possible to maintain experimental phytoplankton-herbivore
communities for several months. The experimental systems resembled natural rock
pools with permanent D. magna presence. Phytoplankton biomass was regulated by D.
mugnu when the species was permanently present in both natural and experimental rock
pools. Experimental rock pools may approximate other fishless habitats and the spatial
and 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
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12
Model systems and experimental rock pools
- Background
- The experimental rock pool systems: experience
and evaluation
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Consumer and resource regulation
- Experience from lake and experimental studies
- Predation and competition in rock pool systems
- Consumer regulation of lower trophic levels by
Notonecta and Daphnia in experimental rock pools
- Effects of cadmium addition on trophic interactions
in rock pool food webs
15
16
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Conclusions
18
References
19
Acknowledgements
27
5
List of papers
The following papers are included in this thesis and will be referred to in the text by
their Roman numerals. The published and accepted papers are reprinted with kind
permission of the publishers.
.
I
Tedengren M., Am& M. & Kautsky N. (1988) Ecophysiology and stress
response 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
II
ArnCr M. & Koivisto S. (1992) Physiological and life history responses of
Daphnia magna to increasing salinity. Hydrobiologia 259: 69-77
III
ArnCr M., Koivisto S., Norberg J. & Kautsky N. Trophic interactions in rock
pool food webs: regulation of zooplankton and phytoplankton by JVutonecta
and Daphnia. (submitted manuscript).
IV
Koivisto S., ArnQ M. & Kautsky N. (1997) Does cadmium pollution change
trophic interactions in rockpool food webs? Accepted for publication in
Environ. Toxicol. Chem.
V
Am& M. & Koivisto S. Evaluation of the ecological relevance of a model
system: Seasonal development and patterns in natural and experimental rock
pools (manuscript).
6
& Nuutinen 1985; Ranta et al. 1 9 8 7 ;
Ranta & Espo 1989; Pajunen & Salmi
1991; III).
The objectives of this thesis can be
seen in both a basic ecological and an
ecotoxicological context. Organisms and
populations have different susceptibility
to environmental stress (natural and
antropogenic), which influence the outcome of biological interactions and the
structure of communities and ecosystems.
The effects of salinity changes and
pollutants have been studied on organism, population and community levels.
Experimental systems, originating from
rock pools, were established to explore
the effects of trophic manipulations and
the addition of a toxicant in a freshwater
planktonic community. In paper I, the
physiological responses to changes in
salinity and exposure to cadmium and
diesel-oil were studied by comparing rock
pool and littoral amphipods with different
tolerance to abiotic stress (Gammanzs
duebeni Lilljeborg and G. oceanicus
Segerstrlle, respectively). Physiological
and life history responses of rock pool
Duphnia magna Straus to different salinities were examined in paper II. Paper III
comprises studies of the regulation of
lower trophic levels by D. mugnu and an
invertebrate predator, the backswimmer
Notonecta sp. in the experimental rock
pools. The direct and indirect impacts of
cadmium addition on trophic interactions
were also studied in the experimental food
webs (IV). The last paper (V) presents
and compares the seasonal development
in natural and experimental rock pools
and evaluates the relevance of the
experimental rock pool systems for
ecological studies.
Introduction
Rock pools, water filled bed-rock
depressions, are patches of habitat
different from the surrounding shore arid
are found on shores around the world.
They are characterised by large spatial and
temporal variations and are considered as
physically harsh habitats (Ganning 197 1;
Ranta 1982; Astles 1993; Metaxas &
Scheibling 1993; Loder et al. 1996;
Underwood & Skilleter 1996). These
isolated habitats are commonly found
along the Swedish and Finnish coastal
areas of the Baltic Sea. Earlier studies of
rock pools in the Baltic Sea area have
emphasised species composition and
abundance in relation to the physicochemical characteristics (in particular
salinity) of the rock pools (Levander
1900; Jarnefelt 1940; Lindberg 1944;
Droop 1953; Ganning 1967; Bjorklund
1972; Ranta 1979). Descriptive studies of
different species and of physiological
tolerance to normally fluctuating variables and toxicants have been conducted
by Forsman (195 l), Lagerspetz (1955,
1958) (I, II) and the nutrient and
metabolic dynamics of rock pool ecosystems were studied by Ganning &
Wulff (1969, 1970) and Ganning (1971).
The systems have also been used for
modelling approaches and studies of
population dynamics (Wulff 1980;
P a j u n e n 1 9 9 0 ; Norberg & DeAngelis
1997). Commonly studied are different
aspects of species coexistence and
interspecific competition (Vepsalainen
1 9 7 8 ; Ranta 1979, 1982; Hanski &
Ranta 1983; Bengtsson 1988) and the
effects of vertebrate and invertebrate
predation have been studied in situ as
well as in laboratory experiments (Ranta
7
The rock pool ecosystem
pools means few microhabitats and also
large and rapid fluctuations in abiotic
variables. The potential number of
species will thus be low. Salinity has a
significant influence on the distribution
of planktonic algae, flagellates, daphnids
and rotifers in rock pools (J&rnefelt 1940;
Droop 1953; Lagerspetz 1955; Bjorklund
1972; Ranta 1982; V). However, many
of the inhabitants in rock pools tolerate
greater fluctuations in salinity and other
abiotic variables than those normally
found (see e.g Forsman 195 1; Ganning
1967; 197 1). The habitat isolation makes
dispersal more difficult and restricts
colonisation. Local extinctions of species
in individual rock pools are common,
whereas the species are present on a
regional scale (within and among islands)
(Hanski & Ranta 1983; Bengtsson 1988).
The formation of dormant stages is a
common strategy in physically harsh and
unpredictable environments (Hairston Jr.
1987). This is common among zooplankton and many other groups of rock
pool species (Ranta 1982). Water insects
(imagines) and gammarids may escape
when conditions deteriorate while other
species survive drought or freezing in the
sediments.
Other
adaptations to
unpredictable habitats are short life
cycles, rapid development to maturity and
parthenogenetic reproduction. Living in
ephemeral or stressful habitats like rock
pools may also offer advantages as
predators are relatively rare (Ganning
1971; Sih 1987; Ranta & Espo 1989).
This thesis mainly deals with the
ecosystem of permanent freshwater rock
pools (sensu Ganning 1971). The studies
of natural rock pools have been carried
out in the Askij area in the northern
Baltic proper (Fig. 1). The distinctions
between different pools are not absolute
and permanent pools of intermediate
Scandinavian rock pools have been
classified in different ways, for example
according to salinity, distance from the
shoreline, vegetation, area or durational
stability (permanent vs. ephemeral)
(Levander 1900; Forsman 195 1; Ganning
1971). The volume of rock pools ranges
from a few litres to a few cubic meters
with weekly to monthly variations
dependent on season, volume, surface to
volume ratio and the amount of
vegetation (Ganning & Wulff 1970;
Ranta 1982; Bengtsson 1988). Rain,
evaporation, sea spray and to lesser extent
freezing regulate the salinity of the rock
pools. Annual salinity in medium sized
(= lm3 ) freshwater and brackish water
pools normally fluctuates between 0 4%0 S and 3 - 8 %O S, respectively
(Ganning 1971; V). High concentrations
and large daily and seasonal fluctuations
of nutrients are common, reflecting the
biotic activities within pools as well as
the importance of nutrient additions by
rain water run off (Ganning & Wulff
1969; Wulff 1980; V). Rock pools ate
rarely anoxic, but large daily variations in
dissolved oxygen concentrations occur, as
a consequence of primary production and
respiration in the pools. Normal daily
oxygen saturation levels in freshwater and
brackish water rock pools fhrctuate
between 50 - 150% and 20 - 200 %,
respectively (Ganning & Wulff 1970;
personal observations). The primary
productivity is usually high and
autotrophic conditions generally prevail
during the summer season (Ganning &
Wulff 1970).
The food webs of rock pools am
simple and the number of species
generally increases with increasing pool
size (Ranta 1982). The small size of rock
8
Fig. 1 The Baltic Sea and the study area (Asko).
freshwater - brackish water character have
also been studied (V). Typical freshwater
pools are situated high up on the shore
and have limnetic character. Most of the
organisms are
which
planktonic
facilitates sampling (Wulff 1980).
Primary producers are pelagic and benthic
microalgae but also filamentous species
occur (Droop 1953; Ganning 1971;
Hallfors 1984; Ranta et al. 1987, V).
Chironomid larvae and ostracods often
live associated with benthic parts of the
pools.
Common
zooplankton are
daphnids (D. magna, D. longispina, D.
pulex), Chydorus sphaericus, cyclopoid
copepods and rotifers. D. magna generally
dominates the zooplankton community in
freshwater rock pools (Ranta & Espo
1989; V). This species is widely spread
geographically, but the large size (adult
9
omnivorous (Forsman 195 1; personal
observations). The species hibernates in
the bottom substratum and may migrate
over the rock between pools (Forsman
195 1; Ganning 1971). Vertebrate predators are absent in most rock pools. To
be omnivorous or to have several
different types of prey, is advantageous in
the limited and unpredictable rock pool
habitat.
females 5-6 mm) restricts the disitribution to smaller habitats (eutrophic
ponds, bog lakes, rock pools), devoid of
planktivorous fish (Hebert 1978). D.
magna is an efficient generalistic filterfeeder and may ingest food particles
ranging from bacteria to microplankton
(diameter of 0.2 to 150 l.trn) (Scavia and
Fahnenstiel 1988; Stockner and Porter
1988; Lair 1991; Kerfoot and Kirk 1991).
D. magna tolerates low oxygen
conditions, high pH and wide ranges of
salinity and temperature (Kobayashi dz
Gondi 1985; MacIsaac ef al. 1985; II).
When conditions deteriorate, reproduction changes from parthenogenetic to
sexual and resistant ephippial eggs are
produced. D. magna is thus well adapted
for the unpredictable and variable rock
pool habitat. Migration between pools
occurs most likely by passive transport
of ephippia by water, wind or birds
(Ranta
1979).
The
small
size,
reproduction,
high
parthenogenetic
fecundity, short life span and easy
handling in the laboratory have promoted
the use of D. magna in aquatic toxicity
testing, although its ecological relevance
has been questioned (Koivisto 1995).
Other consumers are represented by water
insects (i.e. corixid species, diving
beetles) and the amphipod Gammarus
duebeni (Ganning 1971; Pajunen 1977;
Ranta 1982; Bengtsson 1988). The
amphipod G. duebeni is the only species
occupying all types of rock pools around
the Swedish coast, but is practically
never found in the littoral zone (Forsman
195 1; Ganning 197 1). Compared to other
Baltic Gammarus species, its physiological capacities are well developed to
cope with fluctuations in salinity,
dissolved
gases
and
temperature
(Bulnheim 1984). It is most abundant in
brackish-water and freshwater pools and is
Environmental stress
Background
Environmental stress is here defined as an
environmental change that results in a
reduction of net energy balance and
production (i.e. growth and reproduction)
(Koehn & Bayne 1988). If the net energy
balance of the organism is reduced as a
response to environmental stress (natural
or antropogenic), it can be assumed that
fitness is reduced (Koehn & Bayne 1988).
The net energy balance decreases if the
inputs are decreased by lower feeding rates
or assimilation efficiency and/or if the
energy losses are increased by higher
respiration and
excretion
rates.
Differential susceptibility of organisms
and populations to environmental stress
influence the outcome
of biotic
interactions and the organisation of
communities and ecosystems (Dunson &
Travis 1991). However, it is difficult to
predict the outcome of environmental
stress on interspecific interactions,
community structure and ecosystem
function by extrapolating the results from
single-species and life history experiments (Kimball & Levin 1985;
Leblanc 1985; Levin et al 1 9 8 9 ;
Clements & Kiffney 1994). To resolve
this problem, different types of multispecies model systems have been
10
developed (see e.g. Taub & Cow 1980;
Borgmann et al. 1988; Heimbach et al
1992, IV).
The responses to salinity changes and
exposure to cadmium and diesel-oil is
focused in this thesis. Organisms living
in rock pools (e.g Gammarus duebeni and
Daphniu magna) are frequently confronted
with rapid and large changes of several
abiotic variables and their physiological
capacities are well developed to cope with
irregular fluctuations in salinity, temperature and dissolved gases (Bulnheim
1972, 1979; 1984; Kobayashi & Gondi
1 9 8 5 ; MacIsaac et al. 1985; I, II).
Deviations from normal salinities
influence the metabolic rates in
invertebrates. Adaptations to subnormal
salinities and life in freshwater involve
development of more efficient mechanisms for water elimination and salt
uptake, as well as reduced surface permeability and increased capacities of salt
retention (Kinne 1964). Euryhaline
species, e.g. the genus Gammurus, have
usually higher oxygen consumption and
higher ammonium excretion rates in
subnormal salinities (Kinne 1964;
Spaargaren 1984; I). Reduced numbers of
hatched eggs have been found for G.
u’uebeni in freshwater as compared to
brackish water (Kinne 1964). Reduced
reproductive performance and m
final size have also been reported in
freshwater animals penetrating into a
saline environment (e.g. D. magna)
(Kinne 1964; Cowgill & Milazzo 1990,
Sublethal concentration of
199 1).
cadmium have been shown to reduce oxygen consumption in marine crustaceans
(Thurberg et al. 1973). Increased protein
turn-over and associated increases in
respiration have been found for D. mugnu
when exposed to chronic cadmium stress
(Barber et al. 1990). It has been suggested
that species which tolerate a high degree
of natural abiotic stress are more tolerant
to pollution stress as well (Fisher 1977;
Leblanc 1985; paper I).
The 0:N ratio, that describes the
relative proportions of oxygen consumed
to nitrogen excreted, has been used to
describe the physiological status of
invertebrates (Bayne ef al. 1985; Mayzaud
dz Conover 1988; Tedengren 1990; I, II).
This index reflects the balance between
fat, carbohydrate and protein substrates in
the metabolism (Mayzaud & Conover
1988). There is empirical evidence that a
lowering in the 0:N ratio is an indication
of environmental stress (W&lows &
Phelps 198 1; Carr & Linden 1984; Axiak
& George 1987; Tedengren 1990). The
nitrogen part of the index is usually
estimated by the excreted ammonium,
which is the dominant released nitrogen
component in crustaceans. 80 - 90 % of
the total released nitrogen in both
Gammarus and Daphnia magna is
composed of ammonium (Sutcliff 1984;
Mayzaud & Conover 1988; Urabe 1993).
However, respiration and excretion rates
of soluble nitrogen may be affected by
other factors, e.g. food abundance (starvation), food quality and body size, which
add uncertainty to the use of the
physiological index. (Conover & Comer
1968; Lampert dz Bohrer 1984; Ejsmont
Karbin 1984; Mayzaud & Conover 1988;
Urabe 1993). The correspondence of the
physiological index and life history
characteristics of D. magna exposed to
different salinities was studied in paper II.
Environmental stress also affects the
relative abundance of organisms in
aquatic ecosystems both directly and
indirectly. Increased mortality or decreased
reproduction are examples of direct
negative effects and the indirect effects
arise when species have different tolerance
11
to toxicants (Koivisto 1996). For
example, if the predator is relatively more
susceptible to environmental stress, the
prey species may experience a positive
indirect effect of reduced predation
pressure. On the other hand, if the prey
species are less tolerant, the predator is
negatively affected as the food supply is
reduced. Cladocerans are among the most
susceptible species to various contaminants and a common indirect effect of
pollution is a decline in cladoceran abundance followed by increases in phytoplankton and rotifer abundance (Hurlbert
et al. 1972; Hodson et al. 1979;
Hamilton et al. 1988; Borgmann et al.
1989; Hanazato & Yasuno 1990; Webber
et al. 1992; Havens 1994).
cadmium in the rock pool species. The
Baltic populations of G. duebeni and G.
oceanicus were generally more sensitive
to salinity changes and treatments with
diesel oil and cadmium than North Sea
conspecifics. The higher sensitivity to
pollutants of the Baltic populations may
be due to a number of factors such as
changes in the characteristics of toxic
substances (metals) with salinity, the
higher relative ionic concentration of a
given amount of poisonous substance in
the low saline Baltic Sea water as
compared to the North Sea water, and
direct interactions of toxicants with
membrane permeability and osmoregulatory mechanisms, which are already
under strain at low salinities.
A majority of cladoceran species am
exclusively freshwater animals, although
a few genera have colonised saline
environments. Daphnia magna is commonly found in brackish water rock pools
and salinity is known to affect the
distribution. In paper II we investigated
the effects of salinity on metabolism and
life history characteristics of rock pool D.
magna. The lowest 0:N ratio were found
at 8%0 S (as compared to freshwater and
4%0 S), indicating that the most stressful
conditions prevailed at the highest
salinity. Based on the 0:N ratio, the
physiologically most favourable conditions were at 4%0 S. The life history
characteristics showed that the most
suitable salinity for growth and
reproduction of D. magna was 4%0 S,
whereas the lowest population growth
rate was obtained at the highest salinity.
The results showed that high salinity
affected the physiological status of D.
magna negatively, hampering reproduction and growth. The physiological
index and the life history variables led to
comparable conclusions, although the life
Rock pool organisms and eflects of
salinity changes and toxicants
The effects of environmental stress on the
metabolism of one rock pool species
(Gammurus duebeni ) and one littoral
species (G. oceanicus) were studied in
paper I. The two Gammarus species am
common along the whole Swedish coast,
and organisms from both marine (North
Sea) and brackish water (Baltic Sea) areas
were studied. Both species are adapted to
environmental
variable
conditions,
characteristic of both rock pools and the
littoral zone. However, G. duebeni is
more tolerant to fluctuations in e.g.
salinity, temperature and oxygen levels
than other Baltic Gummurus species, and
was regatded as a relatively more broadniched species (Bulnheim 1984). The
rock pool species was expected to he
more tolerant to both natural and maninduced stress. The results from the
laboratory experiments supported this
hypothesis, and respiration and the 0:N
ratio were less affected by salinity,
changes and/or additions of diesel-oil and
12
generally covered as many or more
generations of the selected organisms.
There are obvious advantages with
model systems. The input and output of
energy, material and organisms can be
controlled and the small scale and simple
structure facilitates replication, repetition
and sampling. Some of these positive
features are at the same time valid ground
for criticising of model systems. It has
e.g. been claimed that model systems are
generally too simple in structure and
assembled of species lacking shared
evolutionary history. Furthermore, there
are difficulties in extrapolating the results
from studies of limited model ecosystems
to real world effects, due to e.g. the lack
of seasonality or density-independent
disturbances. Despite this criticism, them
is a general agreement that model
systems may offer a bridge between the
simplicity of mathematical models or
small scale experiments and the full
complexity of real systems (Lawton
1996, Drake et al. 1996, Verhoef 1996).
Carpenter (1996) suggested that the main
role of microcosms are supportive to field
studies and that they can be used to
eliminate hypothesised mechanisms,
compare alternative mechanisms or
estimate rates. The model ecosystems ate
suitable for ecotoxicological studies as
the interactions between species, indirect
effects of toxicants and the impacts of
abiotic factors on toxicity of chemicals
can be studied without damaging the
environment.
history characteristics appeared to be
more sensitive indicators of the most
favourable treatment.
Model systems and
experimental rock pools
’
Background
The opinions of what is the most
relevant temporal and spatial scales and
experimental methods for studying
community and ecosystem ecology
diverge (Lawton 1996, Drake et al. 1996,
Carpenter 1996). The realism and
relevance of natural systems are indisputable, but the sometimes overwhelming complexity complicates the
understanding and interpretation of
patterns and processes. Drake et al.
(1996) has argued “that this inherent
complexity of nature is what makes the
use of laboratory microcosms both
necessary”.
valid
and
desirable,
Experimental systems (micro- and
mesocosms) are models of natural ecosystems, including a selected part of the
biological processes and interactions that
occur in the field. Model ecosystems
should be isolated, self-maintaining, include more than one trophic level and
maintain the same functions as the part
of the ecosystem which it is supposed to
represent (Lalli 1990). The spatial scale
of model systems range from indoor
laboratory bottles to large outdoor enclosures of nature. Most work has
focused on smaller organisms with short
generation time such as bacteria, soil
organisms, protists or plankton (Drake et
al. 1996, Verhoef 1996). In a survey of
articles treating species interactions, Ives
et al. (1996) found that microcosm
studies generally were shorter than field
studies measured in real time, but
The experimental rock pool systems:
experience and evaluation
Trophic interactions and the regulation of
phytoplankton and zooplankton were
studied in experimental freshwater
systems with three food web configurations: 1. phytoplankton and small-
13
bodied zooplankton, 2. phytoplankton,
small-bodied zooplankton and Duphniu
magna and 3. phytoplankton, smallbodied zooplankton, D. mugnu and the
backswimmer Notonecta sp. (III, IV).
The small-bodied zooplankton mainly
consisted of Cyclops sp. and Chydorus
sphaericus. Water and plankton organisms originated from freshwater rock
pools. The outdoor experimental systems
were established in 55 L plastic tubs with
sand and small stones as bottom
substrate. Water, phytoplankton, zooplankton and Notonecta were added
successively to allow stabilisation of the
systems. Cadmium and Notonecta were
&led six weeks after water addition and
the experiment was terminated eight
weeks later because of high Notonecta
mortality. The experimental systems had
probably too low productivity or were
too small to support a third trophic level
during long term experiments. The
experiment used two cadmium levels:
controls (no cadmium) and the nominal
concentration of 20 ppb; in all six
treatments with five replicates each. The
experiment was static, with no water
renewal, but cadmium was replenished
when concentrations fell below the
desired concentration. About once a week,
the experimental rock pools were sampled
for the estimation of phosphate and
ammonium concentrations, phytoplankton biomass, primary productivity, zooplankton species composition and biomass. Ammonium was analysed as it is
generally the main inorganic nitrogen
compound in rock pools (Wulff 1980).
The results are presented in two parts;
firstly the effects of Notonecta and D.
magna on lower trophic levels and
nutrient concentrations (III) and secondly
the combined effects of trophic
manipulations and cadmium addition
(IV).
Rock pools were chosen as “mothersystems” as they are small and isolated
habitats per se and include tolerant
species suitable for handling in
experimental situations. An additional
advantage for the ecotoxicological part of
the manipulations was that D. magna is a
natural component of the zooplankton
community. The artificial rock pools
have been evaluated by comparing
patterns of seasonal development in
natural and experimental rock pools (V).
Experimental rock pools with phytoplankton, small-bodied zooplankton and
Daphnia magna studied in 1992 and 1993
(III, IV) were used in the comparison.
The food webs of the experimental
rock pools included important parts of the
biological processes and interactions in
natural
freshwater
rock
pools.
Phytoplankton - herbivore communities
with naturally co-occurring species were
possible to maintain several months, i.e.
exceeding more than one generation of
the included species. The seasonal
development resembled natural rock pools
with permanent Daphnia presence and the
pattern of low phytoplankton biomass in
association with Duphniu presence was
found in both natural and experimental
rock pools and is well-known from lake
studies. Most variables, with the
exception of phytoplankton biomass,
were in the range found in natural pools,
but tended to vary less. The lower
phytoplankton biomass and the lower
degree of fluctuations of the variables
studied were probably
Partly
a
consequence of the absence of rain water
runoff, which restricted the immigration
of algal species and the input of nutrients
and water from the surroundings.
Occasional water inflows also dilute the
14
population of herbivores (the number of
individuals L-’ decreases), which partly
may decrease the grazing pressure on
phytoplankton populations in natural
rock pools.
fish, young backswimmers prey selectively on the largest size classes of
zooplankton (Scott & Murdoch 1983;
Murdoch et al. 1984; III). Notonecta does
not ingest its prey, but kills it by poison
injected through the piercing mouth-parts
after which it sucks out the prey juices
(Scott & Murdoch 1983). Notonecta is an
effective predator on daphnids, and
capable to eliminate them under natural
conditions (Murdoch et al. 1984).
The
scarcity of
small-bodied
zooplankton species in the presence of
large-bodied species has been explained
by size-selective predation on smallbodied zooplankton species by invertebrate predators (Hall et al. 1970; Zaret
1980; Vanni 1988; Arnott dz Vanni
1993). Another possibility, the sizeefficiency hypothesis, is that small
zooplankton are competitively suppressed
by large-bodied (particularly daphnids)
species that are more efficient filterfeeders (Brooks & Dodson 1965;
Carpenter 1988; Arnott dz Vanni 1993).
The competitive ability differs between
large and small zooplankton and is
influenced by e.g. the amount, quality
and frequency of food supply (Hall et al.
1976; Gliwicz 8z Lampert 1990). Large
daphnids can ingest a larger size range of
food particles than smaller cladocerans
(Kerfoot 1987; Scavia and Fahnenstiel
1988; Stockner and Porter 1988; Bern
1990; Lair 199 1; Kerfoot and Kirk 1991).
Consistently with the size-efficiency
hypothesis, large daphnids have been
shown to have lower food threshold and
be competitively superior to smaller
Daphnia species at low and constant food
supply under predator-free conditions
(Gliwicz 1990). This is given by the fact
that the assimilation rate increases more
rapidly with increasing body size than
respiration rate. The species with the
Consumer and resource
regulation
Experience from lake and experimental
studies
Fish predation has strong impact on the
composition and size structure of
zooplankton communities (Zaret 1980;
Kerfoot & Sih 1987). Visually foraging
planktivorous fish prey selectively on
large zooplankton species, often resulting
in a zooplankton community dominated
by small species (Brooks & Dodson
1965; Zaret 1980). In fishless lakes and
ponds, where invertebrate predators may
be important, large zooplankton species
dominate. The large size of Daphnia
magna makes it vulnerable to fish
predation and restricts its distribution to
fishless habitats (Brooks & D o d s o n
1965; Pont et al. 1991). Although
invertebrates generally are considered as
less efficient predators than fish, they
may also cause substantial reductions of
zooplankton prey species. This has been
shown for backswimmers (Notonecta),
phantom midge larvae (Chaoborus) and
cyclopoid
calanoid and
copepods
(Murdoch et al. 1984; Williamson 1987;
Brett 1992; Arnott & Vanni 1993;
Gliwicz dz Stibor 1993). Many invertebrate predators (e.g. Chaoborus, calanoid
copepods, corixids, water beetles) prefer
smaller prey that are easier to handle and
ingest (Swift & Federenko 1975;
Williamson & Butler 1986; Williamson
1987; Black & Hairston 1988). In
contrast to most invertebrates and like
15
suggested that fish, but not Chaoborus,
increased the availability of phosphorus,
thereby
promoting
phytoplankton
growth.
Numerous studies have shown that a
combination of predation and resource
limitation typically regulates freshwater
plankton populations and drives seasonal
successions (Threlkeld 1987; Hu &
Tessier 1995; III). Data collected in
freshwater ecosystems have generally
shown that resource regulation, with
positive relationships between prey (or
resource availability) and consumer
biomass, is more important at the base of
the food chain (McQueen et al. 1986).
Predation or top down regulation, has its
main support from experimental manipulations. It appears to be most
important at the top of food chains and
has been manifested as negative relationships between planktivore and zooplankton biomass and between largebodied zooplankton (e.g. Daphnia) and
phytoplankton biomass (McQueen et al.
1 9 8 6 ; C a r p e n t e r & Kitchell 1 9 9 2 ;
Mazumder 1994; III).
lowest food threshold may keep the
resource level below the threshold
concentration of other species sufficiently
long time to cause their exclusion. The
food threshold is defined as the food
concentration needed to assure that
assimilation equals respiration (Gliwicz
1990). The competitive outcome can be
reversed if filamentous algae are present,
as larger cladoceran species are more
negatively affected by filaments (Gliwicz
& Lampert 1990). The negative effects
arise due to reductions in ingestion rates
for edible algae and increases in
respiration rates. The opposite view, that
food threshold levels should be lower for
small-bodied species and that smallbodied zooplankton should be competitively superior under low food levels
due to higher foraging efficiency of
smaller species on smaller particles, has
also been shown (Dodson 1974; Neil1
1975; Tessier & Goulden 1987; Koivisto
et al. 1992).
Fish manipulations in lakes have re
peatedly demonstrated the existence of
trophic cascades. Commonly, increased
phytoplankton biomass follows the
addition or increase of planktivorous fish
(see e.g. Carpenter 1988). Proposed
mechanisms are reduced grazing rates,
changes in the zooplankton community
to a dominance of smaller species with
higher nutrient regeneration rates per
weight and recycling of nutrients by the
planktivore (Vanni & Findlay 1990).
There are few experimental studies of
indirect effects of invertebrate predators
on phytoplankton (III). In a mesocosm
study, Vanni and Findlay (1990) found
that fish and the invertebrate predator
Chaoborus caused similar reductions in
zooplankton biomass. However, the
phytoplankton biomass increased only in
the presence of fish. Their result
Predation and competition in rock pool
systems
The effects of predation and zooplankton
competition have also been examined in
rock pools.
Invertebrate
predators
dominate in rock pools and fish is
normally absent. Introduction of fish in
natural rock pools eliminated Daphnia
magna, followed by an increase in the
number of small-bodied species (Ranta et
al. 1987). The number of phytoplankton
cells increased in two out of three
manipulations. In a study in experimental
rock pools, we found that three spinedstickleback (Gasterosteus aculeafus) eliminated the D. magna population, followed by an increase in phytoplankton
16
biomass (At-n& & Koivisto personal observations). In a laboratory study, Ranta
and Espo (1989) found that rock pool
corixids and water beetles preyed on both
chironomid larvae and D. magna. The
water insects preferred chironomids and
only small size classes of Daphnia wefe
captured. It has also been demonstrated
that corixids are able to decimate
chironomids in natural rock pools
(Pajunen & Salmi 1991), but it is less
likely that the usually small water insect
populations am able to regulate the
dominating Daphnia populations in rock
pools (Ranta & Espo 1989). Gammarus
duebeni is omnivorous, capable to reduce
D. magna populations under laboratory
conditions, and is also able to feed on
macroscopic green algae (Enteromotpha
sp.) (personal observations). Among the
herbivorous species in freshwater rock
pools, the cladocerans of the genus
Daphnia and Chydorus sphaericus snre
generalistic filter feeders. In contrast to
the size-efficiency hypothesis, it has been
shown that growth and reproduction of
Chydorus sphaericus at-e less affected by
low food levels than is D . m a g n a
(Koivisto et al. 1992). Within the genus
Daphnia in rock pools, the smallest
species (D. Zongispina) is competitively
superior to the largest species (D. magna)
(Hanski & Ranta 1983). The trophic
position of the cyclopoid copepods is
unclear. It has in the present studies been
assumed that Cyclops sp. change from
herbivory (nauplia) to carnivory (adults)
during their ontogeny (Morgan 1980;
Sprules 1988; Soto 1991; Adrian 1991).
Cyclopoid copepodites may furthermore
enter the brood pouch of daphnids and
prey on eggs (Gliwicz & Stibor 1993;
Gliwicz & Lampert 1994).
Consumer regulation of lower trophic
levels by Notonecta and Daphnia in
experimental rock pools
The regulation of phytoplankton and
zooplankton by the backswimmer
Notonecta and D. magna was studied in
experimental rock pools with two and
three trophic levels (III). The backswimmer was added after an initial stabilisation period of six weeks, and the
experiment was terminated eight weeks
later, due to high Notonecta mortality. In
the two trophic level treatments, we
predicted lower phytoplankton biomass in
the presence of Daphnia, as compared to
the treatment with small-bodied zooplankton. We also expected Notonecta to
reduce Daphnia, followed by an increase
in phytoplankton biomass. The result of
the manipulations showed that consumer
regulation was a dominant force in
determining the biomass of phytoplankton and Daphnia in a planktonic
rock pool community. While Daphnia
reduced phytoplankton production and
biomass,
small-bodied
zooplankton
(Cyclops and Chydorus) increased with
increasing phytoplankton biomass. This
suggest that they were food limited and a
negative correlation
with Daphnia
biomass hence indicates interspecific
competition for limited resources. The
presence of the invertebrate predator
Notonecta produced a top-down effect
which was similar to that reported for
planktivorous fish, i. e. a reduction of
Daphnia followed by an increase of
small-bodied zooplankton species and
phytoplankton biomass. Notonecta selectively preyed on Daphntit and the intense
predation reduced the Daphnia population
which was extinct within four weeks.
The backswimmer seemed unable to use
Chydorus or Cyclops sis food resource and
starved to death after the extinction of the
Duphniu population. Ultimately, however, resource availability determined the
biomass at each trophic level. The food
limitation of zooplankton was indicated
by low egg ratios of Duphnia and a
positive response of small-bodied zooplankton to increased phytoplankton biomass. The production of resource-limited
Duphnia could not support Notonectu
which starved to death after the extinction
of Duphniu.
eliminated the population within four
weeks. Daphnids subjected to Notonectu
predation disappeared simultaneously
from control and cadmium treatments,
and the cadmium x Notonectu interaction
was insignificant.
Conclusions
Rock pool organisms are well adapted to
large fluctuations in abiotic factors. This
is exemplified in this thesis by a higher
physiological tolerance to
salinity
changes in rock pool Gummarus duebeni
as compared to littoral G. oceunicus. The
rock pool gammarid was less affected by
additions of diesel-oil and cadmium.
Salinity is one of the variables that
restricts the distribution of species in
rock pools and high salinity negatively
affected the physiological status of D.
magna, leading to negative effects on
growth and reproduction. The physiological index (0:N ratio) and life history
variables led to comparable conclusions,
supporting the relevance of the
physiological index. It has also been
shown that D. magna is more tolerant to
e.g. copper than are other cladocerans
(Koivisto et al. 1992), thus indicating
that species tolerant to high degrees of
natural abiotic stress are also more
tolerant to pollution stress (Fisher 1977;
Leblanc 1985).
The relevance of a particular experimental system can be discussed on
two levels: Firstly, does the model
system mimic the natural system it is
supposed to represent? To evaluate our
experimental units it can be concluded
that the seasonal development resembled
natural rock pools with permanent
Duphniu magna presence. The patterns of
lower phytoplankton biomass in asso-
Efsects of cadmium addition on trophic
interactions in rock pool food webs
The effects of cadmium addition were
studied parallel to the above described
trophic manipulations (IV). We used a
control (no cadmium added) and a
nominal cadmium concentration of 20
ppb. Cadmium was added at the same
time as Notonectu. Cladocerans (Duphniu
and Chydorus) were assumed to be the
most susceptible species (Hurlbert et al.
1972; Hodson et al. 1979; Hamilton et
a 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 indirect
phytoplankton,
positive effect on
comparable to that of Notonectu addition
was expected. A significant cadmium x
Notonectu interaction was also expected,
i. e. a stronger reduction of Daphnia
when simultaneously exposed to both
mortality factors. C a d m i u m h a d a
negative effect on all trophic levels, but
the results did not support the
hypothesis. The added cadmium strongly
inhibited the phytoplankton production,
which did not respond positively to
Duphniu
biomass.
Consequently, cadmium addition and
predation by Notonectu did not cause
similar effects in rock pool food webs.
The backswimmer was a more efficient.
predator on Duphniu than expected, and
18
ciation with Daphnia presence was found
in both natural and experimental rock
pools and is well-known from lake
studies. Most variables, with the
exception of phytoplankton biomass,
were in the range found in natural pools
but tended to be less variable. The lower
phytoplankton biomass and the lower
degree of fluctuations were probably
partly an effect of the absence of water
inflow. However, this was an inevitable
consequence of the experimental set-up.
Secondly, is the “original” system
ecologically representative for other
ecosystems, i.e. can we extrapolate from
the particular to the general? Freshwater
rock pools differ in several ways from
lakes: The fluctuations in physicochemical variables are larger in rock
pools and probably influence the outcome
of biotic interactions and the organisation
of communities to a higher degree than in
lakes. The food webs are simple, and
planktivores are mainly represented by
generalistic invertebrates unlikely to
regulate the dominant daphnids. Thus, the
“pelagic” part of rock pools are not similar to that of most lakes. However, rock
pools may fairly well approximate other
fishless habitats like ponds and bog lakes
or a lake situation with low planktivore
biomass due to high piscivore abundance.
As shown by this thesis, tolerance to
abiotic variables may also imply
increased tolerance to pollutants and the
use of rock pool systems may thus
underestimate the impact of toxic compounds. On the other hand, if direct or
indirect effects arise in this type of
systems, they will probably also arise
elsewhere.
In my opinion, experimental ecosystems can be used to disclose potential
direct and indirect impacts of e.g.
addition/removal of species or environ-
mental stress. The results from the
experimental rock pools showed that the
size-selective
invertebrate
predator
Notonecta in low densities has the
potential to produce indirect positive
effects on phytoplankton and small
zooplankton. This can be of importance
in other fishless habitats. The addition of
cadmium negatively affected all trophic
levels, b u t t h e s e n s i t i v i t y differed
between organisms (the studied cladocerans were more affected than Cyclops).
If a corresponding change, from cladoceran to copepod dominance, occurs in
natural freshwater systems, it will have
major impact on phytoplankton biomass
and the diet of planktivores. I suggest
that the experimental rock pools systems
am m o s t appropriate for studying
interactions between phytoplankton and
zooplankton or interactions within
zooplankton. Manipulations of levels and
qualities of food supply as well as of
abiotic variables and toxicants could be
possible.
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