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First published online November 28, 2008
Journal of Experimental Biology 211, 3850-3858 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.024232
Physiological and morphological colour change in Antarctic krill, Euphausia superba: a field study in the Lazarev Sea
1 Marine and Coastal Management, Department of Environmental Affairs and
Tourism, Private Bag X2, Rogge Bay 8012, Cape Town, South Africa
2 Scientific Division Biological Oceanography, Alfred Wegener Institute for
Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven,
Germany
3 Division of Immunology, IIDMM-Institute, University of Cape Town, 7925
Observatory, Cape Town, South Africa
4 School of Applied Sciences, Allergy Research Group, RMIT University,
Melbourne, VIC 3083, Australia
* Author for correspondence (e-mail: lauerswa{at}deat.gov.za)
Accepted 14 October 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: colour change, chromatophore index, UV protection, pigmentation, astaxanthin, erythrophore
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). Such migration
pattern is thought to be a result of environmental factors such as avoidance
of predation and food availability but also to avoid potentially harmful
radiation. Krill is particularly susceptible to ultraviolet radiation (UVR;
280–400 nm) as it results in DNA damage
(Jarman et al., 1999) and
increases mortality (Newman et al.,
1999). Ultraviolet radiation B (UVB; 280–320 nm) is the more
harmful than UVA (320–400 nm) and photosynthetically active radiation
(PAR; 400–700 nm) in this regard. Recent research provided evidence that
E. superba responds to solar radiation by moving away from the light
source (Newman et al., 2003),
ensuring a safe distance from UVR.
Owing to the high attenuation of UVR by the seawater column
(Jerlov, 1976), the vertical
migration pattern is a very effective avoidance of damaging radiation. The
migration is not completely regular, however, and large surface swarms of
krill have been observed occasionally during day light (e.g.
Marr, 1962;
Ozawa et al., 1968;
Kubotka, 1981). It is during
such periods, and during ascent and/or descent, when krill is exposed to a
significant portion of UVR, which can penetrate clear Antarctic waters to at
least 20 m (Jerlov, 1976;
Karentz and Lutze, 1990;
Ban et al., 2007). Owing to the
loss of stratospheric ozone, the amount of UVR reaching the surface of the
oceans, especially UVB, has increased in the recent decades
(Solomon, 1990;
Smith et al., 1992) and so
should have exposure of krill to harmful UVR.
In addition to behavioural changes, crustaceans can respond to varying
light conditions with two types of colour change: (1) physiological colour
change (chromomotor change) and (2) morphological colour change (chromogenic
change). Physiological colour change is a relatively fast movement (seconds to
minutes) of pigments in specialised cells. These chromatophores of vertebrates
and invertebrates enable fast pigment movement within their limits. Many
crustaceans contain clusters of differently coloured chromatophores
(erythrophores, leucophores, melanophores and xanthophores, which are red,
white, black and yellow, respectively). These clusters are called
chromatosomes, which facilitate, together with diffuse pigmentation around
them, adaptation to a wide range of background colours for camouflage
(Noël and Chassard-Bouchard,
2004). The enclosure of pigments, such as astaxanthin, in
chromatophores guarantees their fast movement over a defined area of the
animal's surface and enables adaptation to background colours and protection
from solar radiation. Pigment granules can be transported towards the centre,
so concentrating them and producing `blanching' or can be spread out into
extensions (chromorhizae) of the cell, dispersing them and producing
colouration. The granules move along microtubules of the cytoskeleton with the
help of kinesin and myosin protein motors
(Boyle and McNamara, 2005).
Pigment movement inside crustacean chromatophores is under endocrine control.
Upon reception of an environmental trigger (e.g. light), this is facilitated
by the release of antagonistic chromatophorotrophic hormones from the sinus
gland in the eyestalk: the octapeptide RPCH (red pigment-concentrating
hormone) triggers pigment aggregation whereas the octadecapeptide(s) PDH
(pigment-dispersing hormone) leads to the dispersion of pigments in the
chromatophores (see Rao, 2001;
Kwok et al., 2006).
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). Physiological and morphological colour changes are
interlinked: When the pigment remains dispersed or concentrated for an
extended period (days, months) due to prolonged stable light or background
conditions, the concentration of pigment and/or the number of chromatophores
increases or decreases. This relationship was postulated by Babak
(Babak, 1913) and has therefore
become known as Babak's law.
Colouration of krill has been used in the fishing industry as an indicator
for quality (Kawaguchi and Nicol,
2007): `Red' krill (as compared with `white' and `pink' krill) is
caught during summer and from close to the surface and is red because of its
overall pigmentation. It is considered lower quality than white krill caught
in great depth and white `winter krill'. The `reddishness' is obvious when
looking at pictures of surface-swarming krill as well of freshly caught krill
[e.g. fig. 4b in Kawaguchi and
Nicol (Kawaguchi and Nicol,
2007)]. The red colour is caused by the carotenoid astaxanthin,
the dominant pigment in E. superba
(Grynbaum et al., 2005) and
E. pacifica (Funk and Hobson,
1991), and its esters. Astaxanthin is thought to be responsible
for photo-protection in crustaceans
(Green, 1966;
Gilchrist and Lee, 1972;
Hairston, 1979).
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), most of them decapods. Data are scarce for Antarctic krill
and other eupausids. The present field study was therefore aimed at providing
initial information on aspects of colour change in Antarctic krill. They were
accumulated during observations and experiments onboard a summer and a winter
cruise in the Lazarev Sea and are discussed in the context of exposure of
krill to environmental conditions. |
MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Physiological colour change
Experiments were generally executed at a water temperature of
0–1°C with no light except the experimental illumination and a dim
microscope light present. The same group of lateral chromatophores on the 5th
abdominal segment of each individual krill was observed in all
experiments.
Experimental illumination
Light quality and quantity was determined using a Li-250 light meter (for
PAR; LiCor Biosciences, Lincoln, NE, USA) and a UVA/B radiometer PMA 2100 V
1.19 (Solar Light Company, Glenside, PA, USA). Experimental illumination was
provided by 8 W fluorescent tubes. At a distance of 20 cm, the PAR lamp (Snode
CW) emitted 0.11 mW cm–2 of visible light, 0.005 mW
cm–2 of UVA radiation and no UVB radiation. The UVA tube
(Silvania BL350) produced 0.01 mW cm–2 PAR, 0.1 mW
cm–2 UVA and 0.003 mW cm–2 UVB. The UVB tube
(Vilber Lourmat VL-8 M) produced 0.001 mW cm–2 PAR, 0.005 mW
cm–2 UVA and 0.211 mW cm–2 UVB.
GrafixTM cellulose acetate film (Grafix, Cleveland, OH, USA) was used to
filter out UV radiation of wavelengths lower than 293 nm when the UVA and UVB
tubes were used. The comparison of physiological colour change in winter and
summer was conducted at 0.05 mW cm–2 PAR, 0.001 mW
cm–2 UVA and no UVB. Similar size adults [carapax length
(CL), summer: 13.4±1.0 mm; winter: 13.6±1.9 mm] were used.
Staging of chromatophores
For the investigation of a possible physiological colour change, a standard
for krill was established against which dispersal or concentration of pigment
inside the chromatophores was estimated
(Fig. 2A). The resulting
chromatophore index (CI) is based on that suggested previously
(Fig. 2B) by Hogben and Slome
(Hogben and Slome, 1931) for a
frog. The index uses stage 1 (pigment fully concentrated in centre of cell) to
stage 5 (pigment fully dispersed into chromorhizae) with three stages spaced
in-between. For better resolution, half stages were used during observations
(not depicted).
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For photographs of physiological colour change, individual krill was placed
in a dissecting dish (water temperature 
1°C) and held in position by
insect pins without harming the animals. Pictures were taken using a Stemi DV
4A DR microscope (Carl Zeiss) equipped with a Canon PowerShot G5 digital
camera. Single chromatophores were photographed using an Axiovert 135
microscope equipped with an Axiocam MRc 5 digital camera (Carl Zeiss).
Morphological colour change
Chromatophore count
Chromatophores on the fourth, fifth and sixth abdominal segment of
similar-size male adults (CL: 13.9±1.2 mm winter; 14.1±1.5 mm
summer) and sub-adults (CL: 10.3±1.2 mm winter; 10.6±1.2 mm
summer) were counted under a dissecting microscope (Zeiss Stemi DV 4A DR)
after the animals had been exposed to light (to improve visibility of
chromatophores).
Astaxanthin content
Standardisation of astaxanthin quantification was necessary: its
concentration in krill is gender and age specific
(Jackowska et al., 1980;
Funk and Hobson, 1991).
Moreover, eyestalks contain large amounts of astaxanthin
(Maoka et al., 1985;
Funk and Hobson, 1991). In
addition, the stomach of (feeding) summer krill most probably contains more
ingested pigments than that of non-feeding winter krill. To keep the influence
of such variations low, only abdomens of male sub-adults of similar size (see
above) were chosen and analysed separately. They were ground to a fine powder
under liquid N2 and astaxanthin was subsequently extracted twice in
100% methanol. The supernatants were combined and analysed by HPLC according
to the method of Auerswald and Gäde
(Auerswald and Gäde, 2005)
using synthetic astaxanthin (Sigma, St Louis, MO, USA) as standard.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Krill was sometimes bright red (i.e. pigment dispersed) when taken from darkness. As this was unexpected, the first experiments were conducted to exclude factors other than light that could influence pigment movement. Two such factors taken into consideration are, a potential natural circadian variation and stress or disturbance.
Circadian rhythm
Circadian variation of pigment dispersal has been reported for some
crustacean species (see Noël and
Chassard-Bouchard, 2004) and this was hence tested in krill.
Individual sub-adult krill were set up in 50 ml containers in the dark and,
starting after an adaptation period of 12 h, the chromatophore index (CI) of
six individuals was observed at intervals of 2–3 h. Individuals were
taken out one by one and great care was taken to avoid disturbance of other
krill set up for later observation. Although there was some variation in the
CI between a minimum of 1.1±0.2 and a maximum of 1.5±0.4, there
was no indication of a circadian rhythm during the experimental period of 28.5
h (Fig. 6). The lowest
individual CI recorded was 1 whereas the highest was 2.
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Stress
To determine the effect of stress, two groups of individually kept krill
were adapted to the dark. The possible influence of stress (caused by
disturbance) was investigated by agitating individuals of one group in the
dark by consistent gentle stirring (with a glass rod) for 10 min after which
the CI was recorded. The CI of the undisturbed dark-adapted control group was
recorded for comparison. The CI of stressed krill (3.1±0.6) was
significantly higher than in undisturbed animals (1.3±0.4), confirming
that stress causes pigment dispersal (Fig.
7). It is noteworthy in this regard that dying krill has a CI of 5
and that eyestalk ablation leads to irreversible dispersal to stage 5.
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Wavelength
Chromatophores react to the UVA and UVB component of PAR. After recording
the initial CI, krill were exposed to similar doses of PAR (33 mJ
cm–2), UVA (30 mJ cm–2) and UVB (63 mJ
cm–2) and, after 5 min, the CI was recorded again
(Fig. 9). PAR and UVA caused
similar changes in the CI, of 2.2±0.3 and 2.3±0.5, respectively,
whereas the change in the CI was less (1.4±0.4) after exposure to UVB.
All changes were higher than in a dark-adapted control group (0.4±0.6).
Within all experimental groups, except control, CI changes were significant
(P<0.02, paired t-test).
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Comparison of summer vs winter responses
Physiological colour change in adult male krill was significantly faster in
summer than in winter: the time to reach maximum dispersion (ETMAX)
was approximately three times longer in winter than in summer, and
ET50 was more than double (Fig.
12). ET50 in summer of 2:35±0:21 min was
significantly different from the ET50 in winter of 5:37±0:55
min (Student's t-test, P<0.05).
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Chromatophore count
The number of chromatophores is generally higher in krill caught in the
summer than in winter. This was quantified in a clearly definable part of the
body: the fourth to sixth abdominal segments. There were significantly more
chromatophores on all these segments of adult and sub-adult krill; however,
this difference was most pronounced in the sixth segment, with 250% and 483%
more chromatophores in sub-adult and adult summer krill, respectively
(Table 1). The difference was
most obvious in the sixth abdominal segment: it is almost free of
chromatophores in winter (sub-adults depicted in
Fig. 13).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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), (2)
efficient DNA repair mechanisms (Malloy et
al., 1997) and (3) pigmentation (present study). The last method
adapts to variations in short-term light conditions by physiological colour
change, whereas long-term (seasonal) changes in the light regime result in a
morphological colour change. Both are facilitated by chromatophores. Here, we
describe quantitatively, for the first time, colour change for a euphausid
crustacean.
Short-term colour change
The main purpose of physiological colour change in krill seems to be
protection from potentially harmful solar radiation (from above) without
compromising camouflage from predators in open water against surface light
(i.e. from below). To balance between the two required states, opposing and
rapidly convertible appearances are required: coverage of large areas of the
body by pigments for UV protection versus a high degree of
transparency for camouflage. Complete dispersal of the pigment, as in the
chromatophore index 5 (CI 5) ensures UV protection, whereas complete
aggregation (CI 1) meets the requirements for camouflage. In nature,
transition between the two situations is necessary during ascent and descent
of the diel vertical migration. There is no scientific information available
confirming a rhythmic pigmentation pattern that matches this movement. Fishery
reports indicate, however, that white krill is caught close to the sea floor,
whereas red krill is caught closer to the surface
(Kawaguchi and Nicol, 2007).
We did not find any rhythmicity of the chromatophore index in winter krill.
Such a rhythm may still exist in other seasons, when periodicity of daylight
is more pronounced. These periods, however, were not covered in the present
study.
Fishery reports also mention that neighbouring krill aggregations often
have completely different degrees of redness whereas the colouration is
uniform within a single aggregation
(Kawaguchi and Nicol, 2007).
Assuming aggregations mentioned in those reports were exposed to similar light
conditions, these observations would be supportive of our experimental
findings that stress is a trigger of pigment dispersal independent of light.
In nature, such stressors could be, for example, the presence of predators or
fishing operations. The uniformity of colouration would imply some sort of
communication of the signal within the aggregation.
Eupausid eyes are very sensitive to light and can detect light fields of
two magnitudes below that experienced in 250 m depth during daylight
(Onsrud and Kaartvedt, 1998;
Zhou and Dorland, 2004). But,
although this should ensure avoidance, at least of PAR, krill swarms
occasionally occur, for unknown reasons, at the surface during daylight
(Marr, 1962;
Ozawa et al., 1968;
Kubotka, 1981). Furthermore,
krill remains closer to the surface during the day in early summer to take
advantage of phytoplankton (Taki et al.,
2005). Exposure occurs close to the sea surface but can also occur
at greater depths. In the Antarctic summer, significant portions of UVR reach
depths of 20–50 m (Ban et al.,
2007) and are still biologically harmful at 30 m depth
(Karentz and Lutze, 1990).
Krill is well equipped to respond physiologically to such exposure. Very
low doses of PAR are sufficient to trigger a response of the erythrophores in
E. superba: the lowest tested dose of 0.6 mJ cm–2 (5
min exposure at an irradiance level of 0.02 mW cm–1), caused
significant dispersal. Estimated from readings of the surface irradiance at
Palmer Station at noon in early Antarctic summer
(Helbing et al., 1996) and
attenuation tables (Jerlov,
1976), such a dose represents 0.1–0.3% of surface
irradiation. Physiological colour change may therefore be starting as deep as
approximately 50 m, depending on the amount of matter influencing attenuation
of PAR (Jerlov, 1976).
Furthermore, krill is susceptible to doses of PAR and UVR that occur in their
natural environment (Newman et al.,
1999) and krill DNA, because of its high content of T–A base
pairs [and, therefore, high amounts of (T)n arrays], was shown to
be particularly prone to damage by UVB radiation
(Jarman et al., 1999). This is
countered by a very efficient photoenzymatic DNA repair mechanism
(Malloy et al., 1997). In
captivity, krill also responds to PAR and UVA with an avoidance strategy
– which was assumed to be a mechanism to stay clear of the more harmful
UVB radiation (Newman et al.,
2003).
When behavioural response (avoidance) is not possible, UV protection by
pigmentation, as demonstrated in our study, is yet another physiological
mechanism to avoid damage and increase survival. Size and distribution of
pigmentation support this interpretation: the majority of chromatophores are
located dorsally so that natural radiation can be blocked. With diameters
reaching 450 µm on the dorsal parts of the abdomen and thorax, krill
chromatophores are large, compared with those of other crustaceans
(Noël and Chassard-Bouchard,
2004) and when in CI 5, they cover large portions of light-exposed
areas with a screen of astaxanthin granules (see Figs
5 and
11). Astaxanthin proved to be
efficient in protecting copepod crustaceans from the harmful effects of UVR
(Hairston, 1976;
Hairston, 1978;
Davenport et al., 2004). The
highly transparent nature of krill probably necessitates additional protection
of deep-lying critical structures, such as the ventral double strand of the
nervous system, by `profound' chromatophores.
For camouflage against surface light, all pigmentation requires to be
controlled and, hence, has to be within chromatophores. The absence of visible
diffuse pigmentation in E. superba is advantageous in this regard. In
crustacean species that camouflage against a background, diffuse pigmentation
is common around chromatophores or chromatosomes (see
Noël and Chassard-Bouchard,
2004). Full aggregation of red pigment in the erythrophores causes
blanching of the animal to an extent that it is almost completely transparent
against surface light. This camouflage effect is enhanced, and the remaining
silhouette further blurred, by counter-illumination by the krill's
photophores, which are arranged to emit all their light downwards. To maximise
efficiency of this system, the axes of both eyes and photophores are
synchronously aligned towards a single-point light source [i.e. the sun
(Grinnell et al., 1988)].
Many crustacean species possess a variety of differently coloured
chromatophores and diffuse pigmentation for efficient camouflage
(McNamara, 1981;
Noël and Chassard-Bouchard,
2004). Antarctic krill, by contrast, in which UV protection is the
top priority during diel vertical migration, has only one monochromatic type
of chromatophores – erythrophores – and lacks diffuse
pigmentation. Erythrophores are generally characterised by intense pigment
movement that is facilitated by a high abundance of microtubules
(Noël and Chassard-Bouchard,
2004). They are therefore most suited for the rapid colour change
required in krill.
Seasonal differences in colour change
In addition to short-term changes in pigmentation, we found evidence that
there are also seasonal differences in (1) the speed of physiological colour
change between summer and winter and (2) the number of chromatophores and
concentration of astaxanthin (i.e. morphological colour change).
Physiological colour change was much slower in animals that were
investigated in winter, when days are short and the sun is low. Since
physiological colour change is energy dependent, this may be the result of the
metabolic depression that postlarval krill undergoes in winter and which is
characterized by low feeding and respiration rates as well as reduced activity
of metabolic and digestive enzymes
(Atkinson et al., 2002;
Meyer et al., 2002).
Recently, it was demonstrated for the first time that the reduced metabolic
activity of krill, which is already in place at the onset of winter, is
triggered by the Antarctic light regime
(Teschke et al., 2007). The
slow colour change we found in winter might also be a result of this general
slow down of metabolism.
Long-term exposure to a particular light regime or background – and
therefore maintaining the chromatophores with a CI 1 or CI 5 – results
in a slow change in the number of chromatophores and/or the amount of pigment,
i.e. a morphological colour change, according to Babak's Law
(Babak, 1913). Our results give
a clear-cut indication that such a morphological colour change takes place in
Antarctic krill. Both, the concentration of the major pigment astaxanthin and
the number of chromatophores in krill, are substantially higher in summer
– when exposure to light is maximal – than in the darkness of
winter. We have confirmed quantitatively for the first time, what fisheries
reports have indicated: red krill is typical for summer and white krill occurs
in winter (Kawaguchi and Nicol,
2007). Our two-season sampling only provided a snapshots of the
extreme `endpoints' of a possible morphological colour change, and data are
still missing for the transitional periods of spring and autumn as well as
laboratory experiments that mimic a full seasonal transition.
In addition to the amount of light available, the quantity of food consumed
may influence seasonal astaxanthin concentration. Astaxanthin cannot be
synthesized de novo by crustaceans and its precursors have to be
acquired via food intake
(Goodwin, 1984;
Britton, 1995). Algae form the
bulk of their food and the biggest source of astaxanthin precursors for
non-larval krill in summer. As an effect of light regime and sea ice coverage,
phytoplankton is very much limited in the Antarctic winter: chlorophyll
a concentrations drop by at least two orders of magnitude from
>10µg l–1 seawater in summer to <0.1µg
l–1 in winter (Atkinson et
al., 2002). More importantly, the light regime sets in motion an
internal cascade of events (Teschke et
al., 2007) that leads to non-feeding in winter and metabolic
depression (Quentin and Ross, 1991;
Atkinson et al., 2002). So,
even if phytoplanktic (or zooplanktic) food became available, krill would not
be able to make use of it. However, experimental evidence to verify if and to
what extent the lack of precursors causes a reduction in astaxanthin
concentration in winter, is still unavailable.
Mechanisms of colour change in Antarctic krill
Quantity and quality of light are important environmental factors in
triggering colour change. Detailed data on the response of pigment movement in
crustacean chromatophores to different doses of radiation is very scarce, in
contrast to dose dependence for their respective chromatophorotropins (see
Rao, 2001). In addition,
existing results are hardly comparable because of the different experimental
setup, different wavelengths used and the use of chromatophores from different
ontogenetic stages (i.e. eggs, larvae or adults). A recent study has
investigated the relationship of pigment dispersal and UVA dose in an adult
eyestalk-less decapod crustacean, and found an ED50 of
approximately 500 mJ cm–2
(Gouveia et al., 2004). This
is much higher than the ED50 of 5.13 mJ cm–2 for
E. superba in the present study in response to PAR. In summer,
sensitivity may be even higher than in winter. We did not establish a
dose–response curve for UVA in the present study. From the change in the
CI after irradiation with a dose of UVA similar to that of PAR, however, it
can be assumed that such a curve would be in the same order of magnitude as
that for PAR. The CI of aggregated erythrophores of an intact shrimp species
in the above-mentioned study only increased by approximately 1.5 at a dose of
2500 J cm–2 UVA (Gouveia
et al., 2004). The eyes are the main organ for photoreception in
crustaceans and the higher sensitivity in E. superba may be due to
the fact that the eyes in our experimental animals were fully intact.
Clearly, PAR and UVA cause pigment dispersal in krill erythrophores.
Interestingly, UVB radiation triggered moderate pigment dispersal too,
although krill does not avoid UVB under laboratory conditions
(Newman et al., 2003). The
latter observation suggested that it cannot be detected. The result of our
study may be an artefact resulting from pollution of UVB with other
wavelengths and a higher dose of UVB (relative to the UVA and PAR used to
irradiate the other experimental groups) or a possible direct reception of UVB
by krill chromatophores. Such direct reception of radiation by chromatophores
is known from experiments with decapod crustaceans
(Coohill et al., 1970;
Gouveia et al., 2004).
Pigment dispersal in response to light exposure in krill is very swift.
This is facilitated by the exclusive presence of erythrophores (see above) and
provides rapid UV protection when necessary. Dense bundles of microtubules, a
trademark of erythrophores, are visible in krill erythrophores
(Fig. 4); similar to those in
the glass shrimp Palaemonetes vulgaris
(Robison and Charlton, 1973).
Although exact details of pigment movement inside chromatophores are yet to be
established, there is evidence that pigment granules move along the
cytoskeleton (particularly the microtubules) in association with kinesin and
myosin protein motors (Boyle and McNamara,
2005). In summer krill, a period of only 5–7 min is
necessary to change from complete transparency to full colouration. Based on a
diameter of a large abdominal erythrophore of about 450 µm (see above),
this is a speed (in summer) of approximately 40 µm
min–1.
As previously noted, we did not find an endogenous circadian rhythm of
pigmentation in winter krill. Antarctic krill performs more or less regular
vertical migrations that are most pronounced in summer
(Taki et al., 2005). Although
summer krill migrates from close to the surface at night to deeper water,
swarms, or parts thereof, remain in light-exposed depths above 50 m during
daytime (Godlewska and Klusek,
1987; Godlewska,
1993; Taki et al.,
2005). This is sufficient to trigger colour change (see above),
creating the possibility of some degree of rhythmicity in light exposure. The
result could well be a pigmentation rhythm in summer. Circadian variation in
pigmentation in crustaceans is mediated by their antagonistic
chromatophorotropins: rhythmic synthesis and release of PDH was suggested to
be behind pigment dispersal in crab melanophores
(Granato et al., 2004) whereas
rhythmic expression of the RPCH gene was found in a crayfish
(Martinez-Perez et al., 2005).
Adversely, eyestalk-ablated fiddler crabs maintained their pigmentation rhythm
in another study (Webb et al.,
1954). An attempt to use eyestalk-ablated krill in the present
study failed, because animals that were eyestalk-ablated at CI 1 subsequently
displayed maximal and irreversible pigment dispersal. Future research should
therefore cover summer and should also tackle the involvement of
chromatophorotrophic hormones in E. superba. This will reveal how
colour change is triggered and this signal is mediated.
Adaptation of pigmentation to either UV protection (of animals living close
to the surface) OR camouflage (of animals from deeper water) within one
species has been shown, for two morphs of a copepod species
(Luecke and O'Brien, 1981).
This is a more permanent adaptation (i.e. morphological colour change) that is
not suitable for a species such as krill that encounters both situations in a
short period of time, with different requirements for each of them.
During morphological colour change, destruction of chromatophores can be
fast and the various types of chromatophores are destroyed and produced at
different rates. In Palaemonetes vulgaris, for example, red and black
chromatophores disappeared at the highest rate
(Brown, 1934). In the Hawaiian
ghost crab, Ocypode ceratophtalma, the rate of black chromatophore
destruction was actually measured and happens at a rate of 0.76 chromatophores
mm–2 day–1 during 7 days after transfer from
a black to a white background (Green,
1964). In krill, the change is not as drastic as in the
Ocypode experiment though. Moreover, crabs from a black background
had 12 times more black chromatophores than those from a white background
whereas the difference in erythrophore count in krill from different seasons
was only a factor of less than two as estimated from the surface area (30
mm–2) of the fifth abdominal segment (lateral and dorsal) and
the difference in chromatophore count (80; see
Table 1), the rate of
destruction in adult krill is much lower at approximately 0.01 erythrophores
mm–2 day–1 during a period of 240 days.
Future research will have to reveal the fate of astaxanthin and erythrophores
on the transition from summer to winter.
Our present study has revealed some basic information on physiological and morphological colour change in Antarctic krill. More systematic field research and laboratory studies – in vivo and in vitro – are necessary in the future to verify results presented here and to provide a comprehensive model of colour change in Antarctic krill.
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Acknowledgments |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Atkinson, A., Meyer, B., Bathmann, U., Stübing, D., Hagen, W. and Schmidt, K. (2002). Feeding and energy budget of Antarctic krill Euphausia superba at the onset of winter. II: Juveniles and adults. Limnol. Oceanogr. 47,953 -966.
Auerswald, L. and Gäde, G. (2005). The West Coast rock lobster, Jasus lalandii, as a valuable source for chitin and astaxanthin. Afr. J. Mar. Sci. 27,257 -264.
Babak, E. (1913). Über den Einfluss des Lichtes auf die Vermehrung der Hautchromatophoren. Arch. Ges. Physiol. 149,462 -470.[CrossRef]
Ban, S., Ohi, N., Leong, S. C. Y., Takahashi, K. T., Riser, C. W. and Taguchi, S. (2007). Effect of ultraviolet radiation on survival of krill larvae and copepods in Antarctic Ocean. Polar Biol. 30,1295 -1302.[CrossRef]
Boyle, R. T. and McNamara, J. C. (2005). Association of kinesin and myosin with pigment granules in crustacean chromatophores. Pigment Cell Res. 19, 68-75.[CrossRef]
Britton, G. (1995). Structure and properties of carotenoids in relation to function. FASEB J. 9,1551 -1558.[Abstract]
Brown, F. A. (1934). The chemical nature of the
pigments and the transformations responsible for color changes in
Palaemonetes. Biol. Bull.
67,365
-380.
Coohill, T. P., Bartell, C. K. and Fingerman, M. (1970). Relative effectiveness of ultraviolet and visible light in eliciting pigment dispersion in melanophores of the fiddler crab, Uca pugilator. Physiol. Zool. 43,232 -239.
Davenport, J., Healy, A., Casey, N. and Heffron, J. J. A. (2004). Diet-dependent UVAR and UVBR resistance in the high shore harpacticoid copepod Tigriopus brevicornis. Mar. Ecol. Prog. Ser. 276,299 -303.[CrossRef]
Funk, V. A. and Hobson, L. A. (1991). Temporal variations in the carotenoid composition and content of Euphausia pacifica Hansen in Saanich Inlet, British Columbia. J. Exp. Mar. Biol. Ecol. 148,93 -104.[CrossRef]
Gilchrist, B. M. and Lee, W. L. (1972). Carotenoid pigments and their possible role in reproduction in the sand crab, Emerita analoga (Stimpson, 1857). Comp. Biochem. Physiol. 42B,263 -294.[CrossRef][Medline]
Godlewska, M. (1993). Acoustic observations of krill (Euphausia superba) at the ice edge (between Elephant I. and South Orkney I., Dec. 1988/Jan. 1989). Polar Biol. 13,507 -514.
Godlewska, M. and Klusek, Z. (1987). Vertical distribution and diurnal migrations of krill Euphausia superba Dana: from hydroacoustical observations, SIBEX, December 1983/January 1984. Polar Biol. 8,17 -22.[CrossRef]
Goodwin, T. W. (1984). The Biochemistry of Carotenoids, Vol. 2, Animals. New York: Chapman and Hall.
Gouveia, G. R., Lopes, T. M., Neves, C. A., Nery, L. E. M. and Trindade, G. S. (2004). Ultraviolet radiation induces dose-dependent pigment dispersion in crustacean chromatophores. Pigment Cell Res. 17,545 -548.[CrossRef][Medline]
Granato, F. C., Tironi, T. S., Maciel, F. E., Rosa, C. E., Vargas, M. V. and Nery, L. E. M. (2004). Circadian rhythm of pigment migration induced by chromatophorotrophins in melanophores of the crab Chasmagnatus granulata. Comp. Biochem. Physiol. 138A,313 -319.[CrossRef][Medline]
Green, J. P. (1964). Morphological color change
in the fiddler crab, Uca pugnax (S.I. Smith). Biol.
Bull. 127,239
-255.
Green, J. P. (1966). Variation in the pigmentation of Simocephalus vetulus (Crustacea: Cladocera). J. Zool. (Lond.) 149,174 -187.
Grinnell, A. D., Narins, P. M., Awbrey, F. T., Hamner, W. M. and
Hammner, P. P. (1988). Eye/photophore coordination and
light-following in krill, Euphausia superba. J. Exp.
Biol. 134,61
-77.
Grynbaum, M. D., Hentschel, P., Putzbach, K., Rehbein, J., Krucker, M., Nicholson, G. and Albert, K. (2005). Unambiguous detection of astaxanthin and astaxanthin fatty acid esters in krill (Euphausia superba Dana). J. Sep. Sci. 28,1685 -1693.[CrossRef][Medline]
Hairston, N. G. (1976). Photoprotection by
carotenoid pigment in the copepod Diaptomus nevadensis. Proc. Natl.
Acad. Sci. USA 73,971
-974.
Hairston, N. G. (1978). Carotenoid photoprotection in Diaptomus kenai. Verh. Int. Ver. Theor. Angew. Limnol. 20,2541 -2545.
Hairston, N. G. (1979). The adaptive significance of colour polymorphism in two species of Diaptomus (Copepoda). Limnol. Oceanogr. 24, 15-32.
Helbing, E. W., Chalker, B. E., Dunlap, W. C., Holm-Hansen, O. and Villafafie, V. E. (1996). Photoacclimation of antarctic marine diatoms to solar ultraviolet radiation. J. Exp. Mar. Biol. Ecol. 204,85 -101.[CrossRef]
Hogben, L. and Slome, D. (1931). The pigmentary effector system. IV: the dual character of endocrine co-ordination in amphibian color change. Proc. R. Soc. Lond., B, Biol. Sci. 108,10 -53.
Jackowska, H., Czerpak, R. and Mical, A. (1980). Carotenoids of Antarctic krill (Euphausia superba Dana, Euphausia chrystallorophias Holt et Tattershall) in dependence on age, structure and sex. Pol. Arch. Hydrobiol. 27,291 -303.
Jarman, S., Elliott, N., Nicol, S., McMinn, A. and Newman, S. (1999). The base composition of krill genome and its potential susceptebility to damage by UV-B. Antarct. Sci. 11,23 -26.
Jerlov, N. H. (1976). Marine Optics. Amsterdam: Elsevier.
Karentz, D. and Lutze, L. H. (1990). Evaluation of biologically harmful ultraviolet radiation in Antarctica with a biological dosimeter designed for aquatic environments. Limnol. Oceanogr. 35,549 -561.
Kawaguchi, S. and Nicol, S. (2007). Learning about Antarctic krill from the fishery. Antarct. Sci. 19,219 -230.[CrossRef]
Kubotka, K. (1981). Relation between solar light intensity and vertical distribution of krill swarms. Antarct. Rec. 73,88 -96.
Kwok, R., Chan, S. M., Martinez-Perez, F., Zinker, S. and Tobe, S. S. (2006). Crustacean chromatophorotrophins and hyperglycaemic hormone peptide families. In Handbook Of Biologically Active Peptides (ed. A. J. Kastin), pp.229 -234. London: Elsevier.
Luecke, C. and O'Brien, W. J. (1981). Phototoxicity and fish predation: selective factors in color morphs in Heterocope. Limnol. Oceanogr. 26,454 -460.
Malloy, K. D., Holman, M. A., Mitchell, D. and Detrich, H.
W. (1997). Solar UVB-induced DNA damage and photoenzymatic
DNA repair in antarctic zooplancton. Proc. Natl. Acad. Sci.
USA 94,1258
-1263.
Maoka, T., Katsuyama, M., Kaneko, N. and Matsuna, T. (1985). Stereochemical investigation of carotenoids in the Antarctic krill Euphausia superba. Bull. Jap. Soc. Sci. Fish. 5,1671 -1673.
Marr, F. W. S. (1962). The natural history and geography of the Antarctic krill (Euphausia superba Dana). Discovery Reports 32,33 -64.
Martínez-Pérez, F., Zinker, S., Aguilar, G., Valdés, J. and Aréchiga, H. (2005). Circadian oscillations of RPCH gene expression in the eyestalk of the crayfish Cherax quadricarinatus. Peptides 26,2434 -2444.[CrossRef][Medline]
McNamara, J. C. (1981). Morphological
organization of crustacean pigmentary effectors. Biol.
Bull. 161,270
-280.
Meyer, B., Saborowski, R., Atkinson, A., Buchholz, F. and Bathmann, U. (2002). Seasonal differences in citrate synthase and digestive enzyme activity in larval and postlarval Antarctic krill, Euphausia superba. Mar. Biol. 141,855 -862.[CrossRef]
Newman, S. J., Nicol, S., Ritz, D. and Marchant, H. (1999). Susceptibility of Antarctic krill (Euphausia superba Dana) to ultraviolet radiation. Polar Biol. 22,50 -55.[CrossRef]
Newman, S. J., Ritz, D. and Nicol, S. (2003). Behavioural reactions of Antarctic krill (Euphausia superba Dana) to ultraviolet and photosynthetically active radiation. J. Exp. Mar. Biol. Ecol. 297,203 -217.[CrossRef]
Nicol, S. (2006). Krill, currents and sea ice: Euphausia superba and its changing environment. BioScience 56,111 -119.[CrossRef]
Noël, P. Y. and Chassard-Bouchaud, C. (2004). Chromatophores and pigmentation. In The Crustacea I (ed. J. Forest and J. C. von Vaupel Klein), pp.145 -160. Leiden: Brill NV.
Onsrud, M. S. R. and Kaartvedt, S. (1998). Diel vertical migration of the krill Meganyctiphanes norvegica in relation to physical environment, food and predators. Mar. Ecol. Progr. Ser. 171,209 -219.
Ozawa, K., Yamada, T. K., Kira, M. and Shimizu, T. (1968). Observation of patches of Euphausia superba.J. Tokyo Univ. Fish. 9,101 -109.
Quetin, L. B. and Ross, R. M. (1991). Behavioural and physiological characteristics of the Antarctic krill, Euphausia superba. Am. Zool. 31, 49-36.
Rao, K. R. (2001). Crustacean pigmentary-effector hormones: chemistry and functions of RPCH, PDH, and related peptides. Am. Zool. 41,364 -379.[CrossRef]
Robison, W. G. and Charlton, J. S. (1973). Microtubules, microfilaments, and pigment movement in the chromatophores of Palaemontes vulgaris (Crustacea). J. Exp. Biol. 186,279 -304.
Smith, R. C., Prezelin, B. B., Baker, K. S., Bidigare, R. R.,
Boucher, N. P., Coley, T., Karentz, D., MacIntyre, S., Matlick, H. A.,
Menzies, D. et al. (1992). Ozone depletion: ultraviolet
radiation and and phytoplankton biology in Antarctic waters.
Science 255,952
-959.
Solomon, S. (1990). Progress towards a quantitative understanding of Antarctic ozone depletion. Nature 347,347 -354.
Taki, K., Hayashi, T. and Naganobu, M. (2005). Characteristics of seasonal variation in diurnal vertical migration and aggregation of Antarctic krill (Euphausia superba) in the Scotia Sea, using Japanese fishery data. CCAMLR Science 12,163 -172.
Teschke, M., Kawaguchi, S. and Meyer, B. (2007). Simulated light regimes affect feeding and metabolism of Antarctic krill Euphausia superba. Limnol. Oceanogr. 52,1046 -1054.
Webb, H. M., Bennett, M. F. and Brown, F. A.
(1954). A persistant diurnal rhythm of chromatophoric response in
eyestalkless Uca pugilator. Biol. Bull.
106,371
-377.
Zhou, M. and Dorland, R. D. (2004). Aggregation and vertical behavior of Euphausia superba. Deep Sea Res. Part II Top. Stud. Oceanogr. 51,2119 -2137.[CrossRef]
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