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First published online October 5, 2006
Journal of Experimental Biology 209, 4024-4032 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02457
Sub-lethal and chronic salinity tolerances of three freshwater insects: Cloeon sp. and Centroptilum sp. (Ephemeroptera: Baetidae) and Chironomus sp. (Diptera: Chironomidae)
Biotechnology and Environmental Biology, School of Applied Sciences, RMIT University, PO Box 71, Bundoora, Victoria, 3083, Australia
* Author for correspondence (e-mail: kathryn.hassell{at}rmit.edu.au)
Accepted 24 July 2006
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Summary |
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Key words: salinity, Ephemeroptera, Chironomidae, stream invertebrate, sub-lethal, toxicity
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). Increased salinity in Australian rivers results from
historical land clearing and over irrigation, which results in rising saline
groundwater making its way to freshwater streams and rivers
(Hart et al., 1991;
Williams, 1987).
It has been suggested that Australian macroinvertebrate fauna would show
adverse effects to increased salinity above 1000 mg l–1
[
1.5 mS cm–1 (Hart et
al., 1991)]. However, the type of exposure and the duration are
factors that complicate this statement. For example, it has been reported that
the abundance of halosensitive species (including mayflies and gastropods) is
reduced at salt concentrations of 1500 mg l–1 (2.2 mS
cm–1) following exposure to either a continuous or pulse
release of saline water (Marshall and
Bailey, 2004). Similarly, changes in macroinvertebrate community
structures, from salt-sensitive taxa to salt tolerant taxa, were observed at
salinities between 0.8–1.0 mS cm–1 in Queensland
streams (Horrigan et al.,
2005). And in a study of the acute salinity tolerances of a range
of macroinvertebrates from the Barwon River in Victoria, a wide range
(5.5–76 mS cm–1) of 72 h lethal concentrations
(LC50) was observed, which are the concentrations capable of
killing 50% of individuals (Kefford et
al., 2003).
These examples demonstrate that there is much variability in reported
salinity tolerances, and that the values depend on the species and responses
that are tested. However, the above examples have all observed short-term
responses, and do not provide any insight into the physiological effects of
long-term (or chronic) exposure to sub-lethal salinity levels, and since the
effects of exposure to environmental contaminants is not only a result of the
amount of substance to which an organism is being exposed, but also the amount
of time that they are exposed to it
(Newcombe and McDonald, 1991),
studies of responses to longer-term sub-lethal doses are needed. In the case
of salinity, environmental increases can be slow and gradual over a long
period of time, thus highlighting the need for long-term investigations.
Sub-lethal stress may be any response that causes a change in the
organism's condition, without mortality. Stress has been defined as a change
in biological condition beyond normal state that challenges homeostasis
(Barton and Iwama, 1991).
Sub-lethal stress responses include changes in growth, development,
reproductive fitness, disease resistance, tissue and organ function and
cellular processes such as osmoregulation
(Barton and Iwama, 1991;
Pickering, 1990;
Schreck et al., 2001).
It has been traditionally assumed that the effects of increased salinity
would display a threshold response, where below a particular level
(threshold), no effects would be observed, and above the threshold fitness
would be decreased (Hart et al.,
1991). In the freshwater cladoceran, Daphnia magna, a
threshold response, as a decrease in survival, growth and reproduction when
salinity levels increased above 6 g l–1 (8.8 mS
cm–1), was observed
(Smolders et al., 2005).
However, in an investigation of sub-lethal salinity tolerance, growth in the
freshwater gastropod Physa acuta was observed to be lower in low
(
0.05 mS cm–1) and high (>1.0 mS
cm–1) salinities than in intermediate salinities
(Kefford and Nugegoda, 2005).
And in a study of mosquitoes, changes in mass and larval stage duration with
increased salinity were reported (Clark et
al., 2004). Two species of mosquitoes were investigated, one being
the euryhaline Ochlerotatus taeniorhynchus, which displayed increases
in pupal mass and larval stage duration as salinity increased, and the other
was the freshwater Aedes aegypti, which displayed a decrease in pupal
mass as salinity increased, and a U-shaped pattern of larval duration (being
most rapid at intermediate salinities).
This study examined the sub-lethal salinity responses of three species of
freshwater invertebrates, in order to assess if the sub-lethal responses to
salinity are similar across different species that are known to be salt
sensitive in short-term lethal exposures. We chose two baetid mayflies,
Cloeon sp. and Centroptilum sp. (Ephemeroptera: Baetidae)
and Chironomus sp. midges (Diptera: Chironomidae) because both
families have salt-sensitive members with 3-day LC50 ranges of
5.5–6.2 mS cm–1 and 10 mS cm–1,
respectively (Kefford et al.,
2003).
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Materials and methods |
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General methods
All specimens were transported from their collection sites and held in
river water for 24 h prior to the experiments. Growth was measured in terms of
body length (from labrum to end of abdomen) and head width (at the widest
point). In the chironomids, the length of the longest wing of emerged adults
was also measured (distance from the arculus to the tip) as described
(McKie et al., 2004). Tests
were conducted in carbon-filtered Melbourne tapwater (wet lab water) and the
salt source was Ocean Nature salt (Aquasonic, Wauchope, NSW, Australia), which
has the same ionic proportions as seawater and is similar to most Australian
inland saline waters (Bayly and Williams,
1973). Experiments were conducted in 500 ml plastic containers
provided with aeration.
Mayflies
Mayflies were held individually in aerated containers and fed soft,
conditioned leaves from their collection sites. At the beginning of each
experiment mayflies were selected such that none had wing buds. Between six
and eight salinity treatments were used (0.07–15 mS
cm–1), with nine replicates of each. Once per week, water was
changed and all uneaten leaves discarded and replenished with newly collected
leaves. Preliminary results showed high mortalities in all mayflies held at
20–21°C, therefore experiments reported here were conducted at
15±1°C with a 16 h:8 h light:dark photoperiod. Length and width
measurements were taken after 0, 7, 14 and 21 days of exposure. Where
emergence occurred, that individual was excluded for calculation of growth
rates, since many mayflies undergo limited growth in the final instar. Owing
to high mortalities in the wet lab water controls (of the same salinity as
river water) in both mayfly experiments, a second Centroptilum
experiment was carried out with river water as the diluent (instead of wet lab
water).
Chironomids
To ensure all individuals were the same age and species, a single
Chironomus egg mass was collected and held in the laboratory for 24 h
prior to being gently broken apart using forceps and a plastic pipette. The
individuals were then randomly transferred into different salinity treatments
(0.65–25 mS cm–1) with three replicates of each. Each
replicate contained 10–15 individuals and was supplied with a
100x220 mm piece of folded, unbleached toilet paper and a small amount
of crushed trout pellets (Skretting, Australia). Water was changed weekly,
aeration was provided and each container had a mesh covering to allow emerged
adults to leave the water surface and be collected. The experiment was
conducted at 21±1°C with a 16 h:8 h light:dark photoperiod. The
chironomids were observed daily for development of pupae and emergence of
flying adults. Any that emerged were carefully removed and immediately frozen
(–20°C). To minimise handling stress only the emerged adults were
measured.
Statistical analyses
Differences between treatments were evaluated using one-way ANOVA and Tukey
honestly significant difference multiple comparisons tests to detect
significantly different treatment pairs. Log10 transformations were
performed where it improved the assumption of normality and homogeneity of
variance. Standard logistical regression was used to relate the proportion
alive to the salinities tested, and LC50s were calculated from this
regression for five time points: 3 days (72 h), 4 days (96 h), 7 days (168 h),
14 days (336 h) and 21 days (504 h). All statistical analyses were performed
using SPSS for Windows (version 12.0; SPSS Inc., Chicago, IL USA).
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Results |
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5.0 mS cm–1
(Fig. 2B). All individuals in
the 10 mS cm–1 treatment were dead after 8 days, and all
those in the 15 mS cm–1 treatment were dead after 3 days.
Mortality was first observed on day 2. The LC50s for
Centroptilum dropped over the 21 days of the experiment
(Table 1).
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However, since survival of both mayfly species was low in all treatments, we concluded that something other than salinity may have been hindering their survival, such as the water used to make up the test solutions. To test this prospect, a second experiment with Centroptilum was conducted, using river water as the diluent (instead of wet lab water). Survivorship was generally improved, with around 80–100% survival in treatments up to 0.5 mS cm–1 then a steady drop at 1.0 and 2.5 mS cm–1. At the highest concentration tested (5.0 mS cm–1), only 11% survived (Fig. 2C). Mortality was first observed on day 6. As before, the LC50s reduced over the course of the experiment (Table 1).
Although we tried to select small mayflies to allow the greatest scope for growth, some Cloeon (10%) and Centroptilum (25%) did emerge (Fig. 2, Tables 2, 3, 4, respectively). No emergence was observed in the second Centroptilum experiment in salinities above 2.5 mS cm–1, however, the number of survivors at 5.0 mS cm–1 was low and thus may explain why there was no emergence observed at this salinity (Tables 3, 4).
Emergence of flying adult chironomids was significantly affected by salinity and followed an inverted U shape (Fig. 3). No pupation or emergence occurred at 20 or 25 mS cm–1. Time to emergence was also significantly affected by salinity but displayed a different pattern to that of emergence (Fig. 4). Time to emergence increased with increased salinity above 2.5 mS cm–1. However, between 0.15–2.5 mS cm–1, time to emergence was similar. A 15% increase in the time to emergence occurred at 5.0 and 10 mS cm–1 relative to 0.15–2.5 mS cm–1, and at 15 mS cm–1 a substantial increase of 88% in the time to emergence was observed.
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A small number of deformities (abnormal wings or non-hardened exoskeletons) were observed in emerged adult chironomids in the 2.5, 5.0 and 15 mS cm–1 treatments, however there didn't appear to be any pattern between treatments (Table 5). The overall male: female ratio of emerged chironomids was 51:49 with no evidence of any difference between salinity treatments (Table 5).
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Chironomids of the same treatment were grouped together for weight determination and no apparent differences were observed in dry mass or wet mass across treatments (Table 5).
Growth
Mayflies
Growth rates in Cloeon and Centroptilum grown in wet lab
water were highly variable, and not significantly different between treatments
in terms of body length or head width (Tables
2,
3,
4). In the second
Centroptilum experiment, the highest mean growth rates (0.071 mm
day–1) were observed at 2.5 mS cm–1 and
below this salinity, body length growth rates ranged from 0.037–0.054 mm
day–1 (Fig.
5). At 5.0 mS cm–1 the mean growth rate was zero
or negative. No statistical differences were found between any of the
treatments. However, the sample size, especially at 5.0 mS
cm–1 was low (three individuals) due to high mortality and it
is thus unwise to rule out the possibility of a type II error
(Fig. 2C).
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Chironomids
The growth rates of Chironomus were determined by the relationship
between size at emergence and the number of days to emergence. There were no
differences between any treatments for the size at emergence (body length,
head width or wing length), however there were significant differences in body
length growth rates from different salinity treatments. Growth rates were
slightly reduced in the 5 and 10 mS cm–1 treatments relative
to the 0.15–2.5 mS cm–1 treatments, and greatly reduced
in the 15 mS cm–1 treatment
(Fig. 6). Wing length and head
width measurements displayed similar trends
(Table 5).
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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10 mS cm–1 for Cloeon and 5.0 mS
cm–1 for Centroptilum). The growth rates of mayflies
did not display any statistically significant differences across treatments,
however in the highest salinity treatment, where there were survivors at 21
days, the growth rate was lower than the other treatments for which there were
survivors at 21 days. Growth is an energy-dependent function, and the
reduction in growth observed in mayflies as salinity increased may be evidence
of a shift in energy partitioning towards maintaining osmoregulatory
functions.
For example when the beetle Tenebrio molitor was exposed to
different levels of oxygen, changes in growth rates, moulting frequency and
survival were observed (Greenberg and Ar,
1996). In hypoxic environments (10% oxygen) low growth rates,
increased moulting and increased mortality occurred. These authors concluded
that the lower growth rates in hypoxic environments could have been due to
water loss associated with frequent opening of the spiracles and increased
moulting, using energy that would have otherwise been invested in growth
(Greenberg and Ar, 1996). It is
therefore possible to conclude that mayflies similarly partition energy away
from growth when exposed to environmental stressors.
The 21 day LC50 for Centroptilum in river water (2.7 mS
cm–1) was approximately half that of the 3 days
LC50 (5.5–6.2 mS cm–1) previously reported
(Kefford et al., 2003). A
similar finding has been reported for the acute and chronic salinity
tolerances in the salt tolerant damselfly Ishnura heterosticta
(Kefford et al., 2006). They
found that the chronic salinity concentration over a 21 day period was between
20–30 mS cm–1, whereas the acute, 3 day LC50
was around 50 mS cm–1. It is curious that two taxa with very
different salt tolerances have similar ratios of acute to chronic tolerances
(ACR 2). This may give some indication of the level of safety required
when predicting chronic salinity tolerances from acute salinity tolerance
data. Further studies of this nature on other species are required to confirm
this ratio.
This study did not follow all mayflies right through to eclosion, which may
have provided evidence of smaller adults emerging at increased salinity levels
due to lowered growth rates in the nymphs prior to the initiation of
metamorphosis. When Ephemerella mayflies were collected from water of
different temperatures, those with low larval masses tended to metamorphose at
a similar time to those with high larval masses, resulting in smaller adults.
It was hypothesised that once the process of metamorphosis had been started
(via hormonal regulation), no postponement was able to allow for much
additional larval tissue growth, hence those that received the signal to
initiate metamorphosis at a smaller size tended to emerge as smaller adults
(Sweeney and Vannote, 1981).
From the low growth rates yet similar level of emergence across salinities in
the second Centroptilum experiment we can speculate that a similar
phenomenon has occurred in our study. However, without further experimentation
this cannot be confirmed.
It would also seem that the tested baetid mayflies are from very sensitive
taxa that do not perform particularly well in laboratory experiments, since
the survival rates were low in all salinities and in the controls. This is not
usually the case with other species that we have tested
(Kefford and Nugegoda, 2005;
Kefford et al., 2006). The
improved performance of Centroptilum mayflies in the second
experiment where river water was used to make up the saline solutions suggests
that the wet lab water could be one cause of the lower survival rates, and
this factor should be considered in future experiments where mayflies and
other similarly sensitive species are studied.
Emergence in chironomids was greatest in intermediate salinities, and
decreased above or below that, producing an inverted U-shaped survival
response. Chironomids held in high salinities (>2.5 mS
cm–1) had lowered growth rates and extended larval periods,
yet the size of emerged adults was not significantly different between
salinity treatments. Likewise, although there were differences in growth
rates, time to emergence and survival in the damselfly I.
heterosticta, the size of final instar and emerged adults were similar
across all treatments (Kefford et al.,
2006). These studies indicate that the process of development is
protracted with increased salinity, which is in contrast to the current
results on mayflies where development time was not affected by increased
salinity.
Mayflies have very short adult life spans that generally last for only a
few days (Carey, 2002). Adult
mayflies do not feed and the process of oviposition results in the female's
abdomen bursting, subsequently resulting in death
(Carey, 2002). Owing to their
short adult existence, mayflies have developed life histories that are
synchronous, ensuring emergence is timed with other individuals to allow for
successful reproduction (Newbold et al.,
1994). Perhaps a delay in pupation and subsequent emergence of
chironomids or damselflies is a less important factor than for mayflies, since
they have longer adult life spans (Ruppert
and Barnes, 1994) and the requirement for synchronous emergence to
ensure successful reproduction is less critical.
An asymptotic relationship was observed between temperature and pupal
duration in a study of some Australian chironomids, and at higher temperatures
development time was faster, yet wing length was reduced
(McKie et al., 2004). In our
study, larval development time was prolonged with increased salinity and the
number of individuals emerging decreased, but their size and weight was
similar between salinity treatments. So, whereas temperature initiated an
increase in the rate of development and a decrease in the growth rate, we have
observed salinity to cause a delay in development time but not growth. If we
assume that the size of the emerged adults is a major factor influencing
successful reproduction, then increased salinity may have little overall
effect on reproduction, as it may just affect the frequency of reproductive
events rather than the success of those events.
Although we generally presume that a reduction in growth is undesirable, in
some situations it may actually benefit an organism. For example, it may be
beneficial for a chironomid to delay pupation if adverse salinity conditions
exist, since salinity tolerance in chironomids is much lower in pupae than
larvae, because the pupae have no means of osmotic regulation
(Berezina, 2003). Yet this
delay would only be a temporary solution because the stress would need to be
alleviated to still allow for successful emergence.
Similar to that hypothesised for lowered growth in mayflies, the increased times to emergence in chironomids may be due to increased energy requirements for osmoregulation as the salinity increased. Likewise in low-salinity environments ionic stress would be apparent and require energy to hold on to ions (rather than having them lost to the environment), which helps explain the U-shaped survival curve that was observed.
Inverted U-shaped growth patterns in response to salinity have been
observed in freshwater snails (Jacobsen
and Forbes, 1997; Kefford and
Nugegoda, 2005) and mosquitoes
(Clark et al., 2004;
McGinnis and Brust, 1983).
However, in the salt tolerant damselfly I. heterosticta, growth
followed a step (or step then ramp) function, with low salinities having no
effect on growth, intermediate salinities resulting in maximum growth, and at
very high salinities reduced growth and eventually mortality
(Kefford et al., 2006). For
the present study we calculated growth rates in chironomids based on size at
emergence and time to emergence, and observed a non-linear decrease in
response to increased salinity. Again this illustrates that not all growth
patterns in response to increased salinity are the same, therefore further
studies of a variety of species is still needed.
This study focussed on the individual-level traits of growth and survival,
but it has been suggested that environmental assessment should focus on
changes at the population level (Admiraal
et al., 2000; Forbes and Calow,
1999). For studies of salinity tolerance this could be a desirable
way of assessing impacts, since there is much variation in salinity tolerances
in different freshwater species (Hart et
al., 1991; Kefford et al.,
2003; Metzeling et al.,
1995), making it very difficult to assign threshold levels of
impact.
No consistency was found in which chosen traits (i.e. growth, survival,
fecundity) were most sensitive to toxicant stress
(Forbes and Calow, 1999), and
hence these authors concluded that in order to get a proper indication of
impact, organisms should be studied at the population level, in particular the
population growth rate. Since the change in population growth rate
incorporates all life stages and all life history traits, it may provide a
better measure of effect. Similarly, it has been suggested that shifts in
population life cycles and growth dynamics provide better indications of heavy
metal stress in chironomids than simply observing one generation, and this
also allows for determination of induced tolerance across generations
(Postma and Davids, 1995).
However, measuring effects at the population level can be much harder to
demonstrate scientifically because it relies on continual monitoring data,
which is often not available (Admiraal et
al., 2000). In addition it is only possible to study populations
when species are common, and common species may not reflect responses of all
species.
This study has demonstrated that intensive investigation of different
species is important when assessing the effects on freshwater biodiversity
from increasing salinity, because subtle differences exist in species'
physiological responses to salinity stress, and understanding the physiology
of an organism's response to stress helps in the implementation of
environmental management procedures to reduce the impact
(Schreck et al., 2001). Safety
factors applied to salinisation of freshwaters should be recalculated as
results of more such studies become available.
We conclude that increased salinity appears to interfere with normal growth processes in mayflies, resulting in smaller and presumably less fecund adults, whereas in chironomids developmental processes are prolonged, resulting in a longer life cycle that has potential to alter life cycle dynamics and the frequency of reproductive events. This illustrates the need for further investigation of sub-lethal responses to salinity stress for a wide range of freshwater invertebrates to establish likely outcomes of increased salinity in Australian waterways.
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Acknowledgments |
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