Adaptive color vision in Pullosquilla litoralis (Stomatopoda, Lysiosquilloidea) associated with spectral and intensity changes in light environment
1 Department of Biological Sciences, University of Maryland, Baltimore
County, Baltimore, MD 21250, USA
2 Department of Integrative Biology, University of California, Berkeley, CA
94720, USA
* Author for correspondence (e-mail: cheroske{at}umbc.edu)
Accepted 17 October 2002
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Summary |
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Key words: mantis shrimp, Pullosquilla litoralis, visual ecology, filter pigments, phenotypic plasticity, color vision
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Introduction |
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Stomatopod crustaceans, including species in the superfamilies
Gonodactyloidea and Lysiosquilloidea, commonly reside in these tropical
waters. Most species are active diurnally when light intensities are highest,
but some become most active at crepuscular periods, perhaps because of
decreased fish predator densities at these times
(Dominguez and Reaka, 1988;
Jutte et al., 1998
).
Additionally, members of both superfamilies have specialized apposition
compound eyes that include a central midband composed of six rows of large
faceted ommatidia (Harling,
2000
; Manning et al.,
1984
; Marshall,
1988
). A total of 10 spectral classes of photoreceptors operating
at wavelengths of >400 nm exists in this midband area
(Cronin and Marshall, 1989b
;
Marshall et al., 1994
), plus
four or more additional ultraviolet classes
(Cronin et al., 1994d
;
Marshall and Oberwinkler,
1999
). Within the ommatidial midband, Rows 1-4 are believed to be
responsible for color vision in both gonodactyloid and lysiosquilloid
stomatopods (Cronin et al.,
1993
,
1994c
;
Marshall et al., 1996
). Below
the level of the 8th retinular cell, these four rows are tiered, with distal
tiers acting as long-pass filters for the proximal tiers below (Cronin and
Marshall,
1989a
,b
;
Marshall et al., 1991
). In
Rows 2 and 3, stomatopods of the family Gonodactyloidea have two sets of
intrarhabdomal filters placed between junctions of the tiers. These filters
serve to narrow the sensitivity of the underlying photoreceptor and aid in
producing the wide range of spectral sensitivities typical for these animals
(Cronin et al., 1994a
). The
narrowly tuned classes of photoreceptors in these rows trade quantity
(reduction in photon catch) for increased spectral coverage (Cronin and
Marshall,
1989a
,b
;
Cronin et al., 1993
,
1994c
). Having a series of
narrowly tuned photoreceptors may also serve to create color constancy in
heterogeneous light environments (Osorio
et al., 1997
).
The visual systems of various mantis shrimp species living in the same
depth range have similar structure and sensitivity and seem well suited to the
variation of light conditions that they encounter (Cronin et al.,
1994b,
1996
,
2000
). While photopigments
remain constant in any given species, intrarhabdomal filters of conspecifics
of some stomatopod species from different depth environments are not only
spectrally different but are also of different lengths and optical densities
(Cronin et al., 2002
;
Cronin and Caldwell, 2002
).
Filter differences vary adaptively with depth and permit individuals occupying
different photic environments to make full use of the ambient spectrum of
light in each habitat. Cronin et al.
(2001
) established that light
treatments in the laboratory that replicated the spectral features of shallow-
or deep-water light environments in nature could cause spectral shifts of
intrarhabdomal filters in a gonodactyloid stomatopod species (Haptosquilla
trispinosa) that occupies a rather large depth range (0-30 m) with
correspondingly diverse photic conditions. Young animals raised in each type
of light environment generated filters that were effectively `tuned' to
utilize the full spectrum of available light. The phenotypic plasticity
evidenced in this species may be representative of many stomatopods that have
large depth ranges (Cronin et al.,
2002
; Cronin and Caldwell,
2002
).
Mantis shrimp in the superfamily Lysiosquilloidea reside in tropical
coastal environments similar to those of gonodactyloids, but lysiosquilloid
species burrow within coral sediments rather than residing in hard substrata
like most gonodactyloids. Many members of this superfamily also inhabit wide
depth ranges and experience a variety of light environments. Much like
gonodactyloid stomatopod retinas, the retinas of lysiosquilloids contain two
intrarhabdomal filters in Row 2 ommatidia but, unlike gonodactyloids, they
only have one filter in Row 3 photoreceptors (Cronin et al.,
1993,
1994a
).
The research we report here expands upon two different aspects of the
previous work on the adaptable stomatopod color vision system. First, all work
done thus far has been conducted with animals within one superfamily
(Gonodactyloidea). If the flexible color vision system evidenced is generally
adaptable to ambient light conditions, the corresponding changes in
intrarhabdomal filters could occur in all mantis shrimp species with color
vision that inhabit diverse depths, including lysiosquilloids. Second, to
date, stomatopod filter modification has been examined with regard to spectral
changes in light. If the mechanism of filter change involves a response to a
reduction in stimulus to certain photoreceptor classes, as proposed by Cronin
and Caldwell (2002), then an
overall reduction in light intensity across all wavelengths may initiate
similar retinal changes.
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Materials and methods |
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In March 2001, animals were collected as planktonic larvae in a lagoon in Rangiroa in the Tuamotus atolls, French Polynesia and kept in the dark for two days during transport back to the marine aquarium facility at the University of California, Berkeley where they were then maintained in containers with artificial seawater.
Experimental treatments
Upon arrival at the University of California, Berkeley, stomatopods were
placed randomly into one of three light treatments: (1) a broad-spectrum
white-light treatment, (2) a narrow-spectrum blue-light treatment or (3) a
reduced-intensity, broad-spectrum light treatment. Irradiance spectra of these
treatments are provided in Fig.
1. Animals were maintained individually within 250 ml plastic
containers. White lighting was from GE Aqua-Rays tubes (General Electric,
Cleveland, OH, USA) as well as indirect ambient light from a nearby window.
Animals in the reduced-intensity treatment were subjected to the same lighting
conditions as the white-light treatment but were placed in a sealed Styrofoam
container with a 10 cmx17.5 cm window in the lid. The window was covered
with four layers of 50% neutral-density filter material so that light reaching
the animal containers was full spectrum but reduced intensity (<10%
irradiance intensity of the full-spectrum treatment;
Fig. 1). Blue-light-treated
animals were housed in similar 250 ml plastic containers that were placed in a
separate room where lighting was only from GE Aqua-Blue fluorescent tubes
(General Electric, Cleveland, OH, USA) filtered with a blue plastic filter
material that selectively attenuated wavelengths of light of <430 nm and
>480 nm (Fig. 1).
Illumination in all three light treatments was measured using an Ocean Optics
spectrometer (Dunedin, FL, USA). Three times each week, the water in all
experimental containers was changed and animals were fed brine shrimp. In
reduced-intensity-light-treated animals, water changes occurred after sunset
in dimly lit conditions. All animals were maintained on a 12 h: 12 h
light:dark photoperiod.
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After 11 weeks (June 2001), all treated animals (N=5 per
treatment) were shipped to the laboratory at the University of Maryland,
Baltimore County for microspectrophotometry. In brief, our procedures were as
follows (see Cronin and Marshall,
1989a; Cronin et al.,
1994a
). Eyes from freshly sacrificed, sexually mature stomatopods
were sectioned at 14 µm at -30°C in a cryostat. Sections were mounted
in mineral oil between two coverslips and placed on a microscope stage. A
monochromatic, circular beam, 1.5 µm in diameter, was first placed in a
clear region of the slide and varied at 1 nm intervals from 400 nm to 700 nm
for a reference scan. The sample was then moved so that the beam passed
through an intrarhabdomal filter, and an absorbance curve was generated.
Between three and five replicate scans of each filter type, each from a
different filter, were taken per individual, and the absorbance curves were
averaged within filter types over all animals within a treatment.
Environmental radiometry
Downwelling irradiance was measured from 410 nm to 694 nm using a MER-1015
scanning spectroradiometer (Biospherical Instruments, San Diego, CA, USA) with
an attached cosine collector. Data were taken in typical Pullosquilla
habitat at Cook's Bay near the University of California's Gump Marine Station,
Moorea, French Polynesia at approximately noon on a clear, sunny day during
August 1991. Spectral data were collected at 1 m depth intervals from 1 m to
22 m by a SCUBA diver positioning the spectroradiometer in midwater
(Cronin et al., 1994c).
Spectral sensitivity model
Within the specialized ommatidial midband in P. litoralis,
ommatidial Rows 1-4 contain two tiered photoreceptors, each with a spectrally
different photopigment, for a total of eight classes below the level of the
8th retinular cells (Jutte et al.,
1998). Using previously published photopigment absorption data for
P. litoralis (at peak densities of 0.008 per µm), together with
known rhabdom lengths and diameters (see
Jutte et al., 1998
), we
generated sensitivity curves for all eight receptor classes (see
Cronin et al., 1994d
, 2002b
for further details on sensitivity modeling) in both white- and blue- or
gray-treated animals. These models also assume absorbances of overlying optics
and R8 rhabdomeric cells to be exclusively in the ultraviolet (<400 nm;
Cronin et al., 1994d
). Because
stomatopod photopigments in individual receptor classes do not appear to vary
within a species (Cronin et al.,
2000
), and Row 2 filters also do not change, sensitivities in
receptors of Rows 1, 2 and 4 are computed to be the same in all animals.
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Results |
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Spectral sensitivity models
Row 3 sensitivities change between white- and blue- or gray-light-treated
animals due to the spectral shift in the distal Row 3 filter
(Fig. 3). The adaptable Row 3
filters change the sensitivity functions of both underlying Row 3
photoreceptors, moving the sensitivity maxima of receptors in
reduced-light-treated animals to wavelengths 20 nm shorter compared with
homologous receptor classes of white-light-treated animals. In the proximal
tier, the sensitivity maximum of the photoreceptor changes from 635 nm to 615
nm, while in distal receptors, the sensitivity maximum shifts from 630 nm to
610 nm in full-intensity white-light-treated and reduced-light-treated
animals, respectively.
|
We measured downwelling irradiance spectra at 1 m intervals (from the water surface to 22 m) throughout the depth range of habitats occupied by P. litoralis. Knowing these, and using our modeled spectral sensitivity functions for the Row 3 photoreceptors (Fig. 3), we estimate that in a stomatopod living in a shallow water environment (depth=1 m), approximately 0.4% of the photons arriving at the receptor tip are absorbed in the distal photoreceptor of Row 3 and 1.0% are absorbed in the proximal tier (Table 1). Correspondingly, an animal residing in deeper habitats (depth=20 m) but utilizing adapted Row 3 filters could absorb 1.5% of the photons entering the ommatidium in the distal photoreceptor and 2.9% in the proximal tier. Photon capture proportions for `deep' animals are higher in the Row 3 photoreceptors despite the overall decrease in irradiant spectral bandwidth at the depth used in the calculations, due to the increased overlap between Row 3 spectral functions and the ambient irradiance spectra in deeper water environments (Fig. 4). While the short-wavelength shift in Row 3 filters of `deep' animals does confer a relatively greater photon capture rate to Row 3 photoreceptors, the reduced light intensity and spectral range found at 20 m depth (for example) still reduce overall capture rates of these photoreceptors in `deep' animals to <17% of Row 3 receptors in shallow animals living in the bright light conditions occurring at 1 m depth (ratio of deep:shallow photon capture rates are 16% and 9% in adapted distal and proximal Row 3 receptors, respectively).
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Discussion |
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The lysiosquilloid Pullosquilla litoralis was previously reported
to inhabit only tropical waters less than 2 m deep
(Jutte, 1997) but, more
recently, we have observed P. litoralis in habitats from 1 m to 30 m.
Accordingly, the wide depth range that these animals inhabit has a similarly
broad range of light conditions. As these animals have planktonic larval
stages, the quality of light that any individual may occupy after
metamorphosis may not be predictable. Also, if P. litoralis is mobile
as an adult, it may encounter variable light environments throughout its life.
Therefore, in P. litoralis, the possession of tuneable color vision
enables effective sensory function in the different photic conditions of its
range of habitats.
Previous to this work, only stomatopods within the superfamily
Gonodactyloidea have evidenced these tuneable Row 3 filters
(Cronin and Caldwell, 2002;
Cronin et al., 2001
). Cronin
and Caldwell (2002
) showed that
spectral and structural changes in intrarhabdomal filters of three
gonodactyloid species could alleviate the effects of the reduced spectral
range of light available in deeper habitats. Typically, narrowspectrum,
deep-water animals developed blue-shifted filters that were also anatomically
shorter than those collected in shallow water. We have shown that direct
adaptation to surrounding photic conditions also occurs in the lysiosquilloid
species P. litoralis. We used our measured spectral changes in Row 3
filters to construct photoreceptor sensitivity spectra for deep- and
shallow-adapted animals (Fig.
3), which were then used to estimate photon capture rates in the
environmental lighting conditions at variable depths. When comparing photon
capture rates of Row 3 receptors at 1 m depth with the red-shifted (shallow)
filters to capture rates of receptors with blue-shifted (deep) distal filters
at various depths and light environments, it is clear that the deep-adapted
Row 3 photoreceptors have a greater level of stimulation in natural light down
to at least 5-7 m depth (Fig.
5). At greater depths, the reduction in ambient light intensity
and spectral range overwhelms the benefit of the increased photon capture rate
associated with the tuneable filter. Because of the absorptive properties of
water, even at shallow depths there are relatively few photons available at
the long wavelengths at which the Row 3 photoreceptors operate. The situation
becomes much worse at greater depth; in this case, the spectral properties of
the adaptable distal filters are insufficient to offset the effects of the
greatly decreased light levels. It is possible that at intermediate depths
within the range of P. litoralis (e.g. 5-15 m), a reduction in filter
length can increase photon capture efficiency to ameliorate the decreased
illumination to some extent. At this time, our model is conservative in its
predictions on depth variation in the function of the adaptable color vision
system of P. litoralis.
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The type of filter that was formed in the distal, Row 3 position varied
among our light treatments. Within the white-light-treated animals, two
longer-wavelength classes of filters were present. While the longest class
(50% absorbance at 590 nm) is typical for shallow P. litoralis
(Jutte et al., 1998), the
other class (50% absorbance at 580 nm) was slightly blue-shifted. This type
may be an intermediate or mixed type that is still adapting to the light
environment after 11 weeks. If this is the case, adaptation to bright
environments may require a longer period of time. The reduced spectral range
(blue) and reduced intensity (gray) treatments produced animals with
homogeneous short-wavelength shifted Row 3 filters with 50% absorbance at 570
nm. From these results, it is apparent that the mechanism controlling the
spectral shift occurring in stomatopod Row 3 intrarhabdomal filters is not
wavelength dependent (implying some interaction among photoreceptors) but
arises simply from a reduced intensity of light stimulus in single
photoreceptors.
The mechanism of filter change remains unknown. Hypothesized to be
constructed of fused carotenoprotein vesicles, intrarhabdomal filters are
created by the surrounding retinular cells of the photoreceptor
(Cronin et al., 1994a;
Marshall, 1988
;
Marshall et al., 1991
). The
data from the present work seem to support the hypothesis put forth by Cronin
and Caldwell (2002
) that
spectral changes in intrarhabdomal filters may arise from feedback between the
photoreceptive and synthetic machinery of the Row 3 photoreceptors. Variation
in intracellular calcium levels associated with light and dark adaptation may
control or initiate the filter changes observed in both gonodactyloid and
lysiosquilloid stomatopod retinas. If this is the case, one would predict that
individual ommatidia may respond differentially, depending on each one's
levels of light or dark adaptation.
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Acknowledgments |
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