Short-term effects of the heavymetals, aluminium and copper, on polyps
of the common jellyfish, Aurelia aurita
a b s t r a c t
Heavy metals are prominent in the coastal marine environment, especially copper due to its use in anti-fouling
paints and, increasingly, silver due to its use in manufacturing processes and hygiene products. Aurelia aurita is
a common and widespread species of scyphozoan jellyfish found in many coastal habitats, including those
impacted by human activities. While A. aurita is known to be highly tolerant of a wide range of environmental
conditions including large variations in temperature, salinity and dissolved oxygen, nothing is known about its
tolerance to heavy metal pollution. This study examined the independent and interactive effects of copper and
silver on aspects of polyp condition including budding, strobilation, deformities and mortality. The results
showthat 200 μgCu l−1 is above the polyps' tolerance for thismetal and leads to rapidmortality.When this treatment
was excluded, silver had the greatest impact on polyp condition. All metals generally had a greater impact
on polyp condition at higher concentrations. Combination treatments had a lesser effect than single-metal treatments,
suggesting an antagonistic relationship. Copper reduced the detrimental impacts of silverwhen present at
a high enough concentration. Despite reactions to the metals, mortality and deformity responses generally
diminished over time. With budding being proportionally higher than mortality, and increasing over time, it is
suggested that sub-lethal concentrations of metals could actually lead to population growth over timeby the process
of hormesis.
1. Introduction
Increasing levels of industrialisation have led to contaminants
becoming widespread, even reaching ‘untouched’ regions such as
Antarctica (Lenihan and Oliver, 1995). With longevity of many pollutants
being several years (Elmgren et al., 1983; Snyder-Conn et al.,
1990), even minimal but continuous inputs may have ongoing effects
on species and will continue to accumulate to levels above those that
are safe for many species. Heavy metals such as lead, zinc, cadmium,
silver and copper are prominent pollutants in the marine environment
and are derived from several anthropogenic sources such as sewage
discharge, phosphate fertilisers, manufacturing, paint products and
preservatives.
Silver (Ag) has wide-ranging biocidal benefits; particles of silver or
‘nanosilver’ are often used as an antimicrobial agent in clothing, on
product surfaces, in cosmetics and personal hygiene products and in
washing machines, which enters the marine environment by way of
laundrywastewater inputs (Benn andWesterhoff, 2008). Approximately
30% (~300,000 kg) of the silver frommanufacturing and industrial use is
lost to aquatic ecosystems each year (Wijnhoven et al., 2009). In the
ocean, silver is primarily found in the form of AgCl2. It is easily adsorbed
to particles and therefore accumulates in sediments, specifically affecting
benthic organisms, especially filter feeders that naturally accumulate
toxins (Wang, 2001; Wijnhoven et al., 2009). Overall, silver is one of
the most readily bioaccumulated trace metals in invertebrates in the
marine environment (Bianchini et al., 2005; Wang, 2001).
Anthropogenic inputs of copper (Cu) occur primarily from fungicides
(Reichelt-Brushett and Harrison, 2005) and anti-fouling paints
(Alsterberg et al., 2007), with additional inputs from wood preservatives,
sewage sludge (Clark, 2001) and acid mine drainage in regions
where metalliferous ores are mined near to rivers (Braungardt et al.,
2007). For this reason, copper iswidespread in themarine environment,
and is found in especially high concentrations around highly populated
coastlines or in densely packed marinas (Schiff et al., 2007). Natural
oceanic surface-water copper concentrations generally range between
0.03 and 0.23 μg l−1 (see Srinivasan and Swain, 2007),whereas anthropogenic
inputs in estuaries and harbours can exceed the water quality
thresholds of 4 μg l−1 over a 24-hour period (but not exceeding
23 μg l−1 at any one time) (Schiff et al., 2007; US EPA, 2007).
The detrimental effects of heavy metals on marine invertebrates
include reduced survival, impaired fertilisation success and increased
respiration (Brown et al., 2004; Reichelt-Brushett and Harrison, 2005), although
sub-lethal levels may actually stimulate reproductive growth—a
stress response phenomenon termed hormesis (Stebbing, 1981,
2002). Benthic fauna are an especially useful indicator of ecosystem
health and local environmental conditions as they reflect not only recent
environmental conditions but also previous conditions (Reish,
1986), especially sessile organisms that are unable to actively relocate.
The common jellyfish, Aurelia aurita, has a metagenic life cycle typical
of scyphozoans, involving a pelagic sexually-reproducing medusa and
a benthic asexually-reproducing polyp. It has a widespread distribution
throughout the coastal seas, estuaries and bays of northern Europe
(Lucas, 2001). Polyps of Aurelia are found on many artificial substrates
(Duarte et al., 2013) such as concrete, plastics and wood (Holst and
Jarms, 2007; Hoover and Purcell, 2009), and many of which are found
in marinas, where heavy metals may also accumulate due to proximity
to input sources, reduced circulation and lower flushing rates.
The genus as awhole is able to tolerate awide range of temperatures
and salinities (Lucas, 2001) as well as anthropogenic disturbance such
as eutrophication and accompanying hypoxia (Ishii et al., 2008; Thein
et al., 2012). Polyp survival is an important factor governing medusa
population size from year to year. Polyps are able to survive months of
starvation and with a limited food supply, energy is preserved by
inhibiting strobilation (Di Camillo et al., 2010). When environmental
conditions are unfavourable, for example, lack of food or increased
temperature (Thein et al., 2012), polyps may turn into podocysts—a
protective dormant life stage encapsulated in a chitin cuticle. Podocysts
can remain dormant for at least 3 years, until such time as conditions
become favourable again (Arai, 2009; Thein et al., 2012). While the
effects of factors such as temperature, salinity, food availability and dissolved
oxygen on polyp survival and asexual reproductive activity have
been tested experimentally before (see Lucas et al., 2012), the effects of
pollutants have not. The focus of this study is to investigate the impact
of heavy metals, specifically copper and silver, on the survival, development
and asexual reproduction of A. aurita polyps. As individual heavy
metals are rarely found in isolation in the marine environment, and
may work synergistically or antagonistically, we investigated the
impacts of these metals individually and in combination for accurate
environmental representation (Norwood et al., 2003).
During both the pre-conditioning and experimental periods polyps
were fed once a week with excess newly-hatched Artemia (reared in
artificial seawater, salinity 29–31) to ensure optimumnutritional condition.
Polyps were allowed to feed for 24 h, after which all undigested
Artemia were removed and 66% (500 ml) of the water was changed to
maintain water quality (Willcox et al., 2007) and prevent the build-up
of ammonia. A full water change was carried prior to the start of the
experiment to ensure accuracy of trace metal additions and elimination
of contaminants. Artificial seawater was maintained at 12 °C before
introduction to tanks, ensuring that as little temperature change as
possible was encountered by the polyps upon introduction of the new
water.
A total of 15 experimental tanks were set up: 1 control (artificial seawater
only) and 4 metal concentrations (low silver 1 μg l−1; high silver
10 μg l−1; lowcopper 20 μg l−1; and high copper 200 μg l−1), each condition
was repeated in triplicate. Metal concentrations were based on
reported polluted environmental conditions (Bryan and Gibbs, 1983;
Howe andDobson, 2002) and previously observed sensitivities inmarine
benthic invertebrates (Reichelt-Brushett and Harrison, 2005). Within
each container, the plate of polyps was positioned with the most highly
populated surface facing upside-down, as polyps in the natural environment
tend to prefer this position (Holst and Jarms, 2007). The number
and condition of polyps were noted at the start of the experiment.During
the course of the experiment, any detached polyps were removed to prevent
a build-up of decaying organic matter which may lead to increased
water toxicity. The experiment ran for 21 days.
Short-term effects of the heavymetals, aluminium and copper, on polypsof the common jellyfish, Aurelia auritaa b s t r a c tHeavy metals are prominent in the coastal marine environment, especially copper due to its use in anti-foulingpaints and, increasingly, silver due to its use in manufacturing processes and hygiene products. Aurelia aurita isa common and widespread species of scyphozoan jellyfish found in many coastal habitats, including thoseimpacted by human activities. While A. aurita is known to be highly tolerant of a wide range of environmentalconditions including large variations in temperature, salinity and dissolved oxygen, nothing is known about itstolerance to heavy metal pollution. This study examined the independent and interactive effects of copper andsilver on aspects of polyp condition including budding, strobilation, deformities and mortality. The resultsshowthat 200 μgCu l−1 is above the polyps' tolerance for thismetal and leads to rapidmortality.When this treatmentwas excluded, silver had the greatest impact on polyp condition. All metals generally had a greater impacton polyp condition at higher concentrations. Combination treatments had a lesser effect than single-metal treatments,suggesting an antagonistic relationship. Copper reduced the detrimental impacts of silverwhen present ata high enough concentration. Despite reactions to the metals, mortality and deformity responses generallydiminished over time. With budding being proportionally higher than mortality, and increasing over time, it issuggested that sub-lethal concentrations of metals could actually lead to population growth over timeby the processof hormesis.1. IntroductionIncreasing levels of industrialisation have led to contaminantsbecoming widespread, even reaching ‘untouched’ regions such asAntarctica (Lenihan and Oliver, 1995). With longevity of many pollutantsbeing several years (Elmgren et al., 1983; Snyder-Conn et al.,1990), even minimal but continuous inputs may have ongoing effectson species and will continue to accumulate to levels above those thatare safe for many species. Heavy metals such as lead, zinc, cadmium,silver and copper are prominent pollutants in the marine environmentand are derived from several anthropogenic sources such as sewagedischarge, phosphate fertilisers, manufacturing, paint products andpreservatives.Silver (Ag) has wide-ranging biocidal benefits; particles of silver or‘nanosilver’ are often used as an antimicrobial agent in clothing, onproduct surfaces, in cosmetics and personal hygiene products and inwashing machines, which enters the marine environment by way oflaundrywastewater inputs (Benn andWesterhoff, 2008). Approximately30% (~300,000 kg) of the silver frommanufacturing and industrial use islost to aquatic ecosystems each year (Wijnhoven et al., 2009). In theocean, silver is primarily found in the form of AgCl2. It is easily adsorbedto particles and therefore accumulates in sediments, specifically affectingbenthic organisms, especially filter feeders that naturally accumulatetoxins (Wang, 2001; Wijnhoven et al., 2009). Overall, silver is one ofthe most readily bioaccumulated trace metals in invertebrates in themarine environment (Bianchini et al., 2005; Wang, 2001).Anthropogenic inputs of copper (Cu) occur primarily from fungicides(Reichelt-Brushett and Harrison, 2005) and anti-fouling paints(Alsterberg et al., 2007), with additional inputs from wood preservatives,sewage sludge (Clark, 2001) and acid mine drainage in regionswhere metalliferous ores are mined near to rivers (Braungardt et al.,2007). For this reason, copper iswidespread in themarine environment,and is found in especially high concentrations around highly populatedcoastlines or in densely packed marinas (Schiff et al., 2007). Naturaloceanic surface-water copper concentrations generally range between0.03 and 0.23 μg l−1 (see Srinivasan and Swain, 2007),whereas anthropogenicinputs in estuaries and harbours can exceed the water qualitythresholds of 4 μg l−1 over a 24-hour period (but not exceeding23 μg l−1 at any one time) (Schiff et al., 2007; US EPA, 2007).The detrimental effects of heavy metals on marine invertebratesinclude reduced survival, impaired fertilisation success and increasedrespiration (Brown et al., 2004; Reichelt-Brushett and Harrison, 2005), althoughsub-lethal levels may actually stimulate reproductive growth—astress response phenomenon termed hormesis (Stebbing, 1981,2002). Benthic fauna are an especially useful indicator of ecosystemhealth and local environmental conditions as they reflect not only recentenvironmental conditions but also previous conditions (Reish,1986), especially sessile organisms that are unable to actively relocate.The common jellyfish, Aurelia aurita, has a metagenic life cycle typicalof scyphozoans, involving a pelagic sexually-reproducing medusa anda benthic asexually-reproducing polyp. It has a widespread distributionthroughout the coastal seas, estuaries and bays of northern Europe(Lucas, 2001). Polyps of Aurelia are found on many artificial substrates(Duarte et al., 2013) such as concrete, plastics and wood (Holst andJarms, 2007; Hoover and Purcell, 2009), and many of which are foundin marinas, where heavy metals may also accumulate due to proximityto input sources, reduced circulation and lower flushing rates.The genus as awhole is able to tolerate awide range of temperaturesand salinities (Lucas, 2001) as well as anthropogenic disturbance suchas eutrophication and accompanying hypoxia (Ishii et al., 2008; Theinet al., 2012). Polyp survival is an important factor governing medusapopulation size from year to year. Polyps are able to survive months ofstarvation and with a limited food supply, energy is preserved byinhibiting strobilation (Di Camillo et al., 2010). When environmentalconditions are unfavourable, for example, lack of food or increasedtemperature (Thein et al., 2012), polyps may turn into podocysts—aprotective dormant life stage encapsulated in a chitin cuticle. Podocystscan remain dormant for at least 3 years, until such time as conditionsbecome favourable again (Arai, 2009; Thein et al., 2012). While theeffects of factors such as temperature, salinity, food availability and dissolvedoxygen on polyp survival and asexual reproductive activity havebeen tested experimentally before (see Lucas et al., 2012), the effects ofpollutants have not. The focus of this study is to investigate the impactof heavy metals, specifically copper and silver, on the survival, developmentand asexual reproduction of A. aurita polyps. As individual heavymetals are rarely found in isolation in the marine environment, andmay work synergistically or antagonistically, we investigated theimpacts of these metals individually and in combination for accurateenvironmental representation (Norwood et al., 2003).During both the pre-conditioning and experimental periods polypswere fed once a week with excess newly-hatched Artemia (reared inartificial seawater, salinity 29–31) to ensure optimumnutritional condition.Polyps were allowed to feed for 24 h, after which all undigestedArtemia were removed and 66% (500 ml) of the water was changed to
maintain water quality (Willcox et al., 2007) and prevent the build-up
of ammonia. A full water change was carried prior to the start of the
experiment to ensure accuracy of trace metal additions and elimination
of contaminants. Artificial seawater was maintained at 12 °C before
introduction to tanks, ensuring that as little temperature change as
possible was encountered by the polyps upon introduction of the new
water.
A total of 15 experimental tanks were set up: 1 control (artificial seawater
only) and 4 metal concentrations (low silver 1 μg l−1; high silver
10 μg l−1; lowcopper 20 μg l−1; and high copper 200 μg l−1), each condition
was repeated in triplicate. Metal concentrations were based on
reported polluted environmental conditions (Bryan and Gibbs, 1983;
Howe andDobson, 2002) and previously observed sensitivities inmarine
benthic invertebrates (Reichelt-Brushett and Harrison, 2005). Within
each container, the plate of polyps was positioned with the most highly
populated surface facing upside-down, as polyps in the natural environment
tend to prefer this position (Holst and Jarms, 2007). The number
and condition of polyps were noted at the start of the experiment.During
the course of the experiment, any detached polyps were removed to prevent
a build-up of decaying organic matter which may lead to increased
water toxicity. The experiment ran for 21 days.
การแปล กรุณารอสักครู่..