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First published online October 18, 2006
Journal of Experimental Biology 209, 4304-4312 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02521
Influence of ultraviolet radiation on selected physiological responses of earthworms
1 Institute of Zoology, National Taiwan University, No. 1 Roosevelt Road,
Section 4, Taipei 106, Taiwan
2 Department of Life Science, National Taiwan University, No. 1 Roosevelt
Road, Section 4, Taipei 106, Taiwan
* Author for correspondence (e-mail: chenjh{at}ntu.edu.tw)
Accepted 30 August 2006
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Key words: invertebrate, ultraviolet, earthworm, crawling behavior, oxygen consumption
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).
Organisms on Earth are therefore evolutionarily adapted to UV-A, but might not
be adapted to UV-B. Recently, due to atmospheric ozone depletion, a great deal
of attention has been focused on UV-B-induced photodamage to organisms
(Misra et al., 2002). A 10%
decrease in the total stratospheric ozone would increase the amount of UV-B
reaching the Earth's surface by 20% (Misra
et al., 2002). Under normal conditions, many vertebrates and
invertebrates can protect themselves from UV by skin pigments or integuments,
such as feathers, hairs or scales (Charron
et al., 2000). However, the increasing UV-B radiation has
influenced organisms and ecosystems on Earth
(Pool, 1991;
Rozema et al., 2002;
Sommaruga, 2001;
Urbach, 1989). Effects caused
by UV-B, including DNA damage (Davies,
1995), melanogenesis, skin erythema, skin cancer,
immunosuppression and damage to the eyes, have been well studied
(Iyengar, 1994;
Noonal and Lewis, 1995;
Rapp and Ghalyini, 1999;
Urbach, 1989). UV-B also
affects egg hatching and causes deformities in amphibian and fish embryos
(Hunter et al., 1979;
Savage and Danilchik, 1993;
Blaustein et al., 1998;
Epel, 1999;
Steeger et al., 2001).
Although the damaging effect of UV-A on organisms is less than that of
UV-B, the influences of UV-A also need to be considered. In the past, UV-A was
ignored because its intensity reaching the earth does not increase or
decrease. However, there is evidence that it can alter cell membrane
components (Banerjee et al.,
2005), induce DNA-protein crosslinking
(Marrot et al., 2005), and
increase reactive oxygen species (ROS). Thus, it is equally important to know
the effect of UV-A and UV-B on organisms.
Generally, earthworms do not expose themselves to sunlight and only extend
their anterior region outside the soil for feeding or for reproduction at
night. Normally they return to the soil when the sun comes up. However,
sometimes after heavy rain, earthworms do not crawl back into the soil when
the rain stops and can be found dying in puddles
(Darwin, 1881;
Tsai, 1964). Merker and
Brauning [cited by Edwards and Bohlen
(Edwards and Bohlen, 1996)]
suggested that UV radiation is an important factor causing damage to
earthworms when they are on the soil surface. Up to now, only a few reports
have demonstrated that UV is harmful to earthworms
(Albro et al., 1997;
Misra et al., 2005). In the
present study, we tried to test the above hypothesis of Merker and Brauning
(see Edwards and Bohlen, 1996)
and used three species of earthworms, Amynthas gracilis, Metaphire
posthuma and Pontoscolex corethrurus, to investigate whether UV
radiation is a key factor influencing earthworm crawling, mortality and
respiration. A. gracilis usually remains on the soil surface after
heavy rain (Tsai, 1964),
Metaphire posthuma is the species that was found crawling on the soil
after the 1999 `9-21 Chichi earthquake' in central Taiwan
(Liaw and Lee, 2002) and,
according to our long-term observations, P. corethrurus never exposes
its entire body on the soil surface in normal situations.
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), was collected from the main campus of National Taiwan
University, Taipei, northern Taiwan. Metaphire posthuma (Vaillant
1868) (Megascolecidae) was purchased from fishing tackle stores. These
earthworms were kept in a photoperiod controlled room on a 12 h:12 h
light:dark cycle. The room temperature was maintained at 22-25°C, and the
humidity of the culture soil maintained at 70-80%. The earthworms were fed
with green bean sprouts and rice husks. In order to exclude interference due
to body mass, only mature earthworms weighing 0.8-1.0 g were used.
Exposure to UV radiation
The UV light boxes (UV crosslinker, Spectrolinker XL-1000, Spectronics Co.,
Westburg, NY, USA) used in this study had peak of intensities at 312 nm (UV-B)
or 365 nm (UV-A). The UV dose was measured by a sensor in the UV light box.
The average intensity of UV-A or UV-B in the UV light box was, respectively,
4.5±0.5 or 1.2±0.5 mW cm-2. The dose was calculated
as dose (J m-2)=10xintensity (mW cm-2)xtime
(s). The UV-B dose of 500 J m-2 generated by the UV-B box is
equivalent to the incident UV-B dose over a period of 1 h on a cloudy day in
Taiwan. According to our observations, it takes several hours for an earthworm
crawling on the soil surface after heavy rain to die, so the dose of UV-B was
set to 500-1500 J m-2. Before exposing the earthworms to UV, they
were allowed to settle in the plastic dish for 15 min. They were then placed
in the UV light box and exposed to different doses. To exclude the effect of
heat produced by UV radiation, ice was placed in the UV light box to maintain
the temperature at 25°C.
Abnormal behaviors of earthworms exposed to UV-A or UV-B
On exposure to UV-A or UV-B, two unusual behaviors, S-shaped movement and
jumping behavior, were recorded using a digital camera (JVC, GR-DVM96U,
Yokohama, Japan), and their frequencies counted.
Influence of UV-A or UV-B exposure on crawling activity
Soil (400 g) with a humidity of 70% and pH 7.0 (soil moisture and pH meter;
Soil Tester, Takemura Electric Works, Tokyo, Japan) was packed into a circular
container of radius 10.5 cm and height 5 cm. The final soil density was
approximately 0.72 g cm-3. Crawling time was counted from when the
earthworm first contacted the soil surface to when it was again completely
embedded in the soil. The relative increase in crawling time was defined as
the crawling time after UV exposure/crawling time before UV exposure ratio, a
higher ratio indicating a greater effect on crawling time.
Oxygen consumption
Oxygen consumption was measured using oxygen equipment (YSI5300, YSI5301)
as described previously (Chuang et al.,
2004). Briefly, an earthworm was placed in a water chamber
containing 12 ml of air-saturated water (ASW), the test period was 30 min, and
data were recorded every 5 min. A chamber with no earthworm was used as the
negative control and the oxygen content was found to decrease by 5-7% in 2
h.
ASW at normal atmospheric pressure and a given temperature contains X mg O2 ml-1, which was recorded using a digital oxygen meter (Lutron, Do 5510, Taipei, Taiwan), so Y ml contains XY mg O2. When an earthworm weighing G g causes the oxygen concentration of the water to drop by Z% (percentage in the chamber with a earthworm minus that with no earthworm) in t min, the rate of oxygen consumption is (XYZ%)t/60 mg h-1 and the oxygen consumption rate of a unit weight (g) of earthworm (mg h-1 g-1) is [(XYZ%)t/60]/G.
Because earthworm oxygen consumption has a rhythm
(Chuang et al., 2004), we
tested the effect of UV on oxygen consumption at the same time of day
(13:00-16:00 h). Because the soil temperature in northern Taiwan is around
25°C the experimental temperature was maintained at 25°C.
Mortality of earthworms exposed to UV-A or UV-B
After exposure to UV-A or UV-B, the earthworms were gently transferred to a
90 mm plastic dish containing moist no. 1 filter paper at 25°C. When the
prostomium showed no response to probe contact, the earthworm was recorded as
having died and the time of death recorded.
Tissue damage to earthworms after UV-A or UV-B exposure
After irradiation with 1500 J m-2 UV-A or UV-B for different
time periods, earthworms were anesthetized with 10% ethanol, and then small
tissue blocks were dissected from the body wall, fixed in Bounid's fixative,
dehydrated by an ethanol series, and embedded in paraffin. The tissue samples
were then sliced into 3 µm sections, which were stained with Mayer's
Hematoxylin/Eosin, observed under light microscopy (Leica), and recorded using
a digital camera (Nikon, Coolpix 990).
Statistical analysis
Each experiment was repeated at least 5 times. Differences in jump behavior
were tested using the 
2 distribution. The significance of
differences between the control and treatment groups was examined using ANOVA
or two-way ANOVA. Differences in the means for the different treatment groups
were tested using Duncan's new multiple-range test. A level of significance of
P<0.05 or 0.01 was accepted as significant or highly significant,
respectively.
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2 test, P<0.001).
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Respiration of earthworms after exposed to UV-A or UV-B
As shown in Fig. 5A, under
normal conditions, oxygen consumption of A. gracilis was higher than
that of M. posthuma (P<0.01). After exposure to 1500 J
m-2 of UV-A, A. gracilis oxygen consumption was
significantly decreased (P<0.01), whereas that of M.
posthuma was unaffected. Similar results were obtained after UV-B
exposure (Fig. 5B).
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Mortality of earthworms after exposed to UV-A or UV-B
As shown in Fig. 6A, when
M. posthuma was exposed to 1000 J m-2 of UV-B, the
mortality was about 60% in 48 h, and all tested individuals died within 120 h,
by which time their skin had turned black. All earthworms died within 72 h
after 1500 J m-2 UV-B exposure. This means that the UV-B dosage
exposure and the mortality of M. posthuma showed a positive
correlation (P<0.05). As shown in
Fig. 6B, significant mortality
of A. gracilis was seen in 12 h of exposure to 1500 J m-2
of UV-B (P<0.01), and all earthworms died within 48 h in this
study. Surprisingly, no P. corethrurus died after UV-B exposure.
Strikingly, none of the three species died after UV-A exposure (data not
shown).
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Tissue damage after exposure to UV-A or UV-B
The skin of earthworms exposed to UV-A did not show any obvious differences
(data not shown). However, clear damage was seen on exposure to UV-B. As shown
in Fig. 6, when exposed to 1500
J m-2 of UV-B, the cuticle of A. gracilis swelled, and its
epidermis immediately showed necrosis (Fig.
7A,B). After 2 h of exposure, the cuticle had begun to break down
and the epidermis and circular muscles were seriously necrotic
(Fig. 7C), while, after 18 h of
exposure, the epidermis and circular muscles were completely destroyed and
only the longitudinal muscles remained
(Fig. 7D).
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; Soni and Joshi,
1997; van de Mortel et al.,
1998). In this study, we demonstrate that it also caused damage to
earthworms. Although A. gracilis did not die when exposed to UV-A,
all tested individuals died when exposed to 1000-1500 J m-2 of
UV-B, showing that the lethal effects of UV-B are stronger than those of UV-A.
Because the energy in the same total photon m-2 of UV-A is less
than that of UV-B, the deleterious effects were only slight in UV-A.
Metaphire posthuma also died when exposed to 1000-1500 J
m-2 of UV-B, but their survival times were, on average, longer than
those of A. gracilis. This suggests that the tolerance of A.
gracilis to UV-B is lower than that of M. posthuma. The third
species of earthworm, P. corethrurus, survived well even when exposed
to doses of UV-B as high as 3000 J m-2. Thus, P.
corethrurus presented the highest tolerance to UV-B among these three
species. We suspect that it might have an unknown mechanism for protecting
itself against UV-B exposure. Some chemicals or enzymes, such as
mycosporine-like amino acid, flavonol quercetin or photolyase, are known to
protect organisms against UV (Blaustein et
al., 1994; Banaszak and Trench,
1995a; Banaszak and Trench,
1995b; Carefoot et al.,
1998; van de Mortel et al.,
1998; Inal and Kahraman,
2000), but which mechanism is activated in P. corethrurus
needs further study.
Under normal conditions, earthworm peristalsis is performed by reciprocal
contraction of the circular and longitudinal muscles. If muscle contraction is
not coordinated, crawling activity is affected and the worm exhibits `fictive
locomotion' (Mizutani et al.,
2002). When exposed to UV, A. gracilis showed an S-shape
movement, which is an extraordinary behavior in earthworms in this study. The
behavior is similar to the `fictive locomotion', therefore, we infer that the
actions of their circular and longitudinal muscles were not well coordinated.
Another abnormal behavior, jumping, was seen when A. gracilis was
exposed to UV energies of >1500 J m-2. The behaviors are likely
to reflect chemical irritation that in a higher animal might be considered
`pain'.
Until now, behavioral effects caused by UV exposure have received little
attention. This study reveals striking changes in behavior after UV exposure.
It can be inferred that these abnormal behaviors of the earthworm are mediated
by the nervous system (Howell,
1939; Mulloney,
1970; Vining and Drewes,
1985; Hassoni et al.,
1985). We therefore believe that these earthworms, especially
A. gracilis, might be a new model animal suitable for studying the
related neurophysiology, such as neuromuscular junction regulation and
neurotransmitter release under UV exposure.
As regards earthworm respiration, oxygen is dissolved in the mucus on the
epidermis, diffuses through the capillaries, and is transported throughout the
body. Blood flow in earthworm vessels occurs through pumping by muscle
contraction (Edwards and Bohlen,
1996). When muscle contractions are interrupted, the blood cannot
be transported, causing anoxia, anaerobic respiration, and decreased oxygen
consumption. Our results demonstrated that the oxygen consumption of A.
gracilis significantly decreased after UV-B exposure. It is therefore
reasonable to infer that the UV-induced abnormal crawling behavior and muscle
contraction affected the respiration of the earthworms. In addition, when an
earthworm's skin is damaged by UV, oxygen diffusion from the epithelia to the
capillaries is reduced. With a low oxygen supply, it may be difficult for the
muscles to contract, and crawling activity would decrease. Such a vicious
cycle between behavioral activity and respiration will finally kill the
UV-exposed A. gracilis. A similar phenomenon has been reported in
tadpoles of Bufo bufo (Formicki
et al., 2003). In addition, the oxygen consumption of the fish,
Cichlasoma nigrofasciatum, is reduced when its gills are damaged by
UV exposure (Winckler and Fidhiany,
1996).
The intensity of UV-B used in this study was 9 times higher than that used
by Misra et al. (Misra et al.,
2005), but the total UV-B dosage to which their earthworms were
exposed was between 14 400-43 200 J m-2, which is far higher than
the 1500 J m-2 dosage used in this study. However, the pathological
effect on the M. posthuma skin exposed to the two different energies
of UV-B was similar. Several reports have demonstrated that UV induces
production of reactive oxygen species (ROS) and photo-oxidation
(Misra et al., 2005;
Girotti, 2001;
Kulms and Schwarz, 2002;
Picardo, 2003;
Rijnkels et al., 2003).
Lumbricus terrestris secretes a photoreactive sterol and produces
1O2 during UV-A irradiation
(Albro et al., 1997). Some
reports have shown that UV induces cell apoptosis and other effects
(Morita and Krutmann, 2000;
Norbury and Hickson, 2001;
Denning et al., 2002;
Zhou and Steller, 2003). We
have therefore started to study whether skin damage in UV-exposed earthworms
is related to ROS generation.
In the present study, we have demonstrated that UV can threaten an
earthworm's existence by two different mechanisms. Firstly, an acute response
immediately evoked abnormal moving behaviors and slowed the crawling activity
of UV-exposed earthworms. Photoreceptors have been found in earthworms
(Mulloney, 1970;
Myhrberg, 1979), so we suspect
that these quick responses might be mediated by a novel type of UV-sensitive
photoreceptor in earthworms. Secondly, chronic responses, including skin
necrosis and decreased respiration, caused the UV-exposed earthworms to die
within a couple of days.
In most UV-damage studies, researchers have used cells to study the
damaging effects of UV (Ichihashi et al.,
2003), but little is known about its effects on animal behavior or
physiology. In recent times, the generally accepted animal model for UV
studies has been the hairless mouse (Van
Weelden and Van der Leub, 1985), but these animals are expensive
to purchase and handle, and the relevant effects occur very slowly
(Lee et al., 2000). Normally,
terrestrial animals have higher tolerance to UV-B than aquatic animals
(Gies et al., 1995), as many
protect themselves from UV-B by pigments or integuments, such as feathers,
hair, a shell or scales. Earthworms have no such protective structures.
Although earthworms live in the soil, UV radiation is a serious menace when
they crawl out of the soil. Accordingly, the doses of UV to which the
earthworms were exposed in this study were lower than those used in studies on
other animals, such as the mouse, fish or frog
(Blaustein et al., 1997;
Steegar et al., 2001; Dissemond et al.,
2003), but the effects were still obvious. A. gracilis
was shown to be the most sensitive of the three species used in this study,
while P. corethrurus showed no marked response to UV. Hairless mice
exposed to 3000 J m-2 UV-B show skin erythema, but do not die
(Lee et al., 2000), while
Tubefix dies when the UV-B energy is 5 times greater
(Soni and Joshi, 1997) than
that which kills A. gracilis. A. gracilis thus has a higher
sensitivity than these organisms. In addition, earthworms are cheaper than
other model animals. We therefore suggest that earthworms, especially A.
gracilis, could be a new animal model for studying UV-induced damage,
such as erythema, free radical formation and lipid peroxidation
(Taira et al., 1992;
Gilchrest et al., 1996;
Johar et al., 2003), while
P. corethrurus could be used to study protection from UV.
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