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First published online October 31, 2008
Journal of Experimental Biology 211, 3536-3543 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.022277
Reflected polarization guides chironomid females to oviposition sites
1 Department of Atmospheric Sciences, The Hebrew University of Jerusalem,
Jerusalem 91904, Israel
2 Faculty of Science and Science Education, University of Haifa at Oranim, Tivon
36006, Israel
3 Department of Evolution, Systematics and Ecology, The Hebrew University of
Jerusalem, Jerusalem 91904, Israel
4 Department of Life Sciences, Eilat Campus, Ben-Gurion University, Hatmarim
St., Elat 88000, Israel
* Author for correspondence: amit.lerner{at}mail.huji.ac.il
Accepted 23 September 2008
 |
Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: polarization vision, chironomids, oviposition, habitat selection, water turbidity
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). After
mating, the male dies, and the female descends to oviposit on the water
surface. The eggs are laid in the form of egg batches (EB), each containing
thousands of eggs wrapped in a gelatinous layer. Since the adults do not feed
and are short lived, most females lay only once or twice and die soon after.
Females usually oviposit in two stages, at the start of the evening and around
sunrise. After emerging from the egg, the larva descends to the bottom of the
water, where it feeds on the substrate and on suspended matter in the water.
Then, 2—3 weeks later, the larva pupates and once the metamorphosis is
complete, the pupa swims to the water surface, where the adult emerges into
the air and is ready to mate (Pinder,
1986). Mating takes place within a couple of hours.
Chironomids are a nuisance to humans physically, commercially and
healthwise (Armitage et al.,
1995). Recently, the EB of chironomids were identified to host the
Vibrio cholerae bacterium, a human pathogen responsible for the
severe diarreal cholera disease (Broza and
Halpern, 2001; Halpern et al.,
2004). The bacterium shows successive host-pathogen population
dynamics (Halpern et al.,
2006), while exploiting the eggs as a carbon source
(Broza and Halpern, 2001). The
adult midges that emerge from the water surface are suggested to carry the
bacterium between bodies of water (Broza et
al., 2005; Paz and Broza,
2007), assisting the bacterium's dispersion and population
stability.
Schwind (Schwind, 1991) was
the first to suggest that chironomids prefer to oviposit in highly polarized
patches. Meltser et al. (Meltser et al.,
2008) showed that females do not oviposit randomly but prefer
certain water bodies over the others, and that the cue which directs this
preference is not olfactory but visual. Similar to the observations on
blackflies (Diptera: Simullidae) by Golini and Davies
(Golini and Davies, 1975),
Meltser et al. observed that more EB are laid in dark versus bright
reflecting patches. As dark surfaces reflect light with a high percentage of
linear polarization [a correlation known as Umow's law
(Umow, 1905)], Meltser et al.
suggested that the cue that guides the females' choice is the percentage
polarization of the light reflected from the water surface.
Polarization vision (PV) is well known among invertebrates, including
insects, as the microvilli in their photoreceptors are often orthogonally
arranged (for a review, see Horváth
and Varjú, 2004). Insects and other invertebrates use PV
for several tasks, including orientation and navigation [bees
(von Frisch, 1949); ants
(Wehner, 1982); dung beetles
(Dacke et al., 2003); spiders
(Dacke et al., 1999)] and as a
mating signal [butterflies (Sweeney et
al., 2003)]. Flying insects are known to use PV to detect water
bodies [first demonstrated by Schwind
(Schwind, 1991)] and to avoid
flying over the sea [locusts
(Shashar et al., 2005)]. In
laboratory experiments, females of the Australian orchard butterfly
Papilio aegeus showed a clear preference to oviposit on horizontally
polarized patches, regardless of the wavelength of light reflected from the
substrate (Kelber, 1999;
Kelber et al., 2001).
Wildermuth (Wildermuth, 1998)
showed that dragonflies make more attempts to oviposit on high polarization
reflecting substrates, and Kriska et al.
(Kriska et al., 1998) also
reported that species of mayflies (Ephemeroptera) are attracted to and even
occasionally oviposit on horizontally oriented polarization reflecting
substrates. Furthermore, Kriska et al.
(Kriska et al., 2006)
suggested that the large standard deviation from horizontal alignment of the
electric vector (e-vector) of the reflected polarized light is the reason for
the unattractiveness of burnt stubble fields for aquatic insects, emphasizing
the importance of a stable (in their case horizontal) e-vector orientation as
a visual cue.
Chironomids are sensitive to light at 370—400 nm (ultraviolet for
humans) and at 490—510 nm (green for humans) with no apparent overlap
between the two ranges (Kokkinn and
Williams, 1989). Chironomids were also found to be attracted to
horizontal polarization over vertical polarization
(Danthanarayana and Dashper,
1986). Meltser et al. (Meltser
et al., 2008) caught more chironomid females in polarized light
traps than in unpolarized traps (transmitting equal intensity), whereas male
numbers in both traps were the same. This supports the suspicion that the
ability of the females to sense polarization is used for a rather feminine
activity, such as oviposition. Here, we examine the hypothesis that chironomid
females select the water body to oviposit by the percentage polarization of
the light reflected from a water surface and not by the light intensity.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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).
Experiments were conducted along the banks of the northeastern pond, where the
highest number of EB was recorded.
Experiment 1: oviposition preference under controlled illumination
To check whether the females choose a site for oviposition by the reflected
intensity or by polarization, their preference for egg traps reflecting linear
polarized light vs depolarized light was examined at two intensity
levels. For this purpose, four traps were placed in a tent (185 cmx305
cmx310 cm). Each trap was constructed of a wooden box (30 cmx30
cmx30 cm) with a 10 W incandescent light bulb placed in the middle of
the base (Fig. 1). A 10
cmx10 cm open hatch was placed above the bulb, where a filter including
diffusers (commercial wax paper) and a linear plane polarizer (Polaroid HN38S)
was placed. The combination of diffusers and polarizers in the four filters
was, respectively (Fig. 2):
three diffusers + one polarizer (ordered from the light bulb to the viewer),
transmitting high intensity polarized light (PHIH); one polarizer + three
diffusers, transmitting high intensity unpolarized light (PLIH); 15 diffusers
+ one polarizer, transmitting low intensity polarized light (PHIL); and one
polarizer + 15 diffusers, transmitting low intensity unpolarized light (PLIL).
On top of the filter, a glass aquarium of 15 cmx15 cmx10 cm was
placed, filled with tap water 2 cm high (450 cm3). In addition,
four fluorescent bulbs were placed inside the tent to attract the chironomids.
The experimental procedure included turning on the fluorescent light from 30
min before sunset until 30 min after, then shutting down the fluorescent light
and turning on the light bulbs in the boxes overnight. The EB laid in the
aquarium of each box were counted on the following morning.
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Experiment 2: oviposition preference under natural illumination
To investigate the females' preference under natural illumination, sets of
four black plastic tubs of 40 cmx50 cmx20 cm (40 l) were placed
around the pond's banks. Each tub was filled with 20 L of tap water (clear, no
organic matter) or pond water (turbid; total organic carbon (TOC)
concentration, 23.1 mg l—1). The tap and pond water
turbidities were measured using a HACH portable turbidimeter 2100P at
0.9±0.2 and 46.0±11.1 NTU, respectively (N=20). During
a preliminary check, we observed that tubs that were white above water level
were not attractive to the females, as no EB were laid in them although they
were filled with pond water and reflected high polarization. Therefore, two of
the tubs in each set were painted white up to water level (WT/WP for white
painted tubs filled with tap/pond water), and the other two tubs were not
painted and were left black (BT/BP for black tap/pond water tubs). The
distance between the tubs was 1 m to allow the females to choose between
several available oviposition habitats located nearby. The reflected
intensity, spectra, percentage polarization, and e-vector orientation were
measured at sunset within an hour before complete darkness, when the sun was
obscured by the Carmel Mountains. EB laid in the tubs were counted in the
following morning.
Light measurements
Intensity, spectra, percentage linear polarization, and e-vector
orientation were measured using a custom made polarimeter as described by
Cronin and Shashar (Cronin and Shashar,
2001; Sabbah and Shashar,
2007). Briefly, an optic fiber (Ocean Optics, Dunedin, Florida,
USA; UV/VIS 600 µm) was attached to one side of the tub to a
spectrophotometer calibrated for intensity and spectral measurements (Ocean
Optics ADC-1000-USB), recording readings at 1 nm practical resolution (0.33 nm
nominal resolution) in the range 300—800 nm. The other end of the optic
fiber was connected to a 5 deg. acceptance angle restrictor, to which a
rotatable plane polarizer (Polaroid HN38S) was attached. Each measurement
included a set of three readings with the polarizer set at orientations of 0
deg., 45 deg. and 90 deg. with respect to the horizon (I0,
I45, I90). Since the polarizer we used
absorbs UV radiation (below 400 nm), the three light components, intensity,
percentage polarization, and e-vector orientation were calculated from the
three readings for each nanometer in the range 490—510 nm in which
chironomids are known to be sensitive
(Kokkinn and Williams, 1989).
This range coincides well with the spectral range of light reflected from the
pond before sunset, the starting time of chironomid activity
(Fig. 3). The sets of three
readings were analyzed using the equations developed by Wolff and Andreou
(Wolff and Andreou, 1995),
modified by Shashar et al. (Shashar et
al., 2004), and described in detail by Sabbah and Shashar
(Sabbah and Shashar, 2007). In
experiment 1, the distance between the fiber and water surface was 5 cm,
oriented to the nadir, and in experiment 2, the fiber was mounted on a tripod,
40 cm above water level, 30 deg. from the nadir, at varying azimuthal angles.
In the measurements from the `natural' chironomid pond, the sensor was placed
on the bank edge, 40 cm above water level, 45 deg. from the nadir, and 230
deg. from the north. All light measurements from the tubs in the second
experiment and from the pond were performed under clear sky, after the sun was
obscured by the Carmel Mountains before sunset. Therefore only diffuse
skylight was available as a light source.
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Polarization as a predictor to the amount of food in the water
To examine the correlation of polarization with the amount of food in the
water, the intensity, percentage polarization, and e-vector orientation of
radiation reflected from different pond water concentrations were measured in
the waste stabilization station on January 1, 2008; between 7.00 h and 10.00 h
local time (UTC+2 h). Reflected light was measured from a 70 l white barrel
filled with 60 l (water depth, 45 cm) of pond water diluted with tap water.
The amount of food in the water was estimated as the total organic carbon
(TOC) concentration, measured for a concentration of 100% of pond water using
a Tekmar Dohrmann Apollo 9000 TOC Combustion Analyzer and calculated for each
dilution according to the partial volume of the pond water (TOC was assumed to
be zero in tap water and to be homogenously distributed in the pond water).
The sensor was mounted on a tripod at 40 cm above water level, oriented 30
deg. from the nadir and 230 deg. from the north. The measurements were
conducted in a location shaded from direct sunlight.
Statistical analyses
EB counts were analyzed using repeated measures analysis of variance
[RM-ANOVA (Sokal and Rohlf,
1995)]. The RM-ANOVA treats the EB values of the four patches
within each sampling day as a repeat. In experiment 1, we examined whether
intensity and polarization affected the EB number laid, and therefore we
applied RM-ANOVA with two within-subject factors: intensity (low/high) and
polarization (low/high). We used planned comparisons in experiment 1 to test
whether specific pairs of egg traps differ statistically. In experiment 2, we
examined whether tub type affected the EB number laid, and therefore we
applied RM-ANOVA with a single within-subject factor, consisting of four
levels. Pair-wise comparisons of the four artificial patches in experiment 2
were examined using Bonferroni post-hoc tests. The mean and standard
deviation of the e-vector orientations reflected from the tubs in experiment 2
were calculated using the equations for circular statistics
(Batschelet, 1981). The
statistical analyses of the first experiment were conducted using
STATISTICA® 8 (StatSoft,
2007) and those of the second experiment using SPSS® 13.0
(SPSS, 2004).
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) for Drosophila. Whole heads were embedded in an
Araldite resin and sectioned using a Leica UltraCut UCT ultramicrotome. The
sections were stained with uranyl acetate and lead citrate, and viewed and
photographed with a JEOL JEM-1230 transmission electron microscope (TEM)
operated at 120 kV. |
RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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0.001),
except for the pair BT and BP, which did not differ significantly from one
another (P
1). The mean ± s.d. of the mean reflected
intensity measured from the tubs at each nanometer over the spectral range of
490—510 nm was 2.06±0.07x10—3,
1.86±0.06x10—4,
1.53±0.06x10—4 and
1.37±0.04x10—4 (µEcm—2
s—1 nm—1), for the tub treatments WT, WP, BT
and BP, respectively. Pair-wise comparisons following Kruskal—Wallis
non-parametric ANOVA (Siegel and
Castellan, 1988) applied for wavelengths 400, 450, 490, 500, 510,
550, 600, 650 and 700 nm revealed that in wavelengths <600 nm (the range
relevant to chironomid vision), only WT intensity differed significantly from
each of the other three patches (P<0.05). None of the e-vector
orientations reflected from the tubs differed significantly from 0 deg.
(horizontal).
Intensity and polarization reflections from the chironomids' native pond during twilight
The intensity and polarization reflected from the chironomids' `natural'
pond surface were recorded from an hour before sunset until darkness to
document the visual cues available for the chironomid females in their natural
habitat (Fig. 5). While the
intensity decreased by 96% during this period, the percentage polarization
remained high and stable at around 60%. The e-vector orientation was also
stable around the horizontal (0±4 deg.; mean ± s.d.).
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Egg number laid under natural illumination in experiment 2
The mean ± s.d. of EB percentages laid in the tubs were
0.6±1.2% in WT, 6.1±5.0% in WP, 38.3±12.7% in BT and
55.1±10.6% in BP, respectively (Fig.
8; see Table 2 for
the actual number of eggs found). The percentage of EB laid in WT did not
differ significantly from 0% [95% confidence interval
(CI95)=—0.1% to 1.2%]. The RM-ANOVA with a single
within-subject factor revealed a significant difference between the number of
EB laid in the four tubs (F3,13=6.5, P=0.006).
Post-hoc Bonferroni pair-wise comparisons of EB numbers showed a
significant difference between all treatments (P<0.05).
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Intensity and polarization correlation with organic carbon concentrations in the water
The correlation of the reflected intensity and polarization with the TOC
concentrations in the water is shown in
Fig. 9. Although the intensity
decreased with increasing TOC concentration, the percentage polarization
increased, reaching a maximum of 13%. The e-vector orientation did not change
with increasing TOC concentration and was nearly horizontal at
—6°±17°.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Kriska et al., 1998;
Kelber, 1999;
Kelber et al., 2001). Here we
quantitatively show that the choice of chironomid females as to where to
oviposit is guided by the percentage polarization, independent of the
intensity reflected from water bodies, and that the preference to oviposit
(the number of EB laid) increases as the percentage polarization of the light
reflected from the water surface increases.
In experiment 1, chironomid females held within the tent had to oviposit in
one of the treatments presented to them. The EB numbers revealed the animals'
preference for both high light intensity and high percentage polarization,
independently (Fig. 7). In
experiment 2, conducted under open, natural conditions, the females could
oviposit in the experimental patches as well as in the nearby pond. The
results of this experiment demonstrate that percentage polarization is the
signal attracting females to water bodies, as the number of EB laid in the
unpolarized patches was not significantly different from zero
(Fig. 8), whereas it was
positively related to the percentage polarization in polarized patches. This
finding agrees with the observations in previous studies that flying insects
tend to oviposit on high polarization reflecting substrates
(Schwind, 1991;
Kriska et al., 1998;
Kelber, 1999;
Kelber et al., 2001;
Bernath et al., 2002).
One concern in examining the response to polarization in insects is that specific orientations of polarization may be perceived by the animals as exceptionally bright (Kentaro Arikawa, personal communication), and if the insects are attracted to bright areas, they might show pseudo-polarotaxis. However, in our tent experiment, the light passed through a linearly polarizing filter, and the animals' flight and orientation of approach was not restricted; on average the filter could have been seen from any direction and could have presented a range of polarization orientations. Furthermore, the position of the polarizing filters was shuffled randomly between the days of the experiments. Therefore, such a polarization-based intensity gain is unlikely in our setting.
Another concern in most behavioral choice studies is that other unexpected visual cues may guide the studied behavior, producing false positive results. In our case, we tried to avoid, or at least critically examined, such undesired cues in both experiments. In the tent experiment (experiment 1), we used the very same filters in differing order to maintain the spectra of reflected radiation and intensity (when relevant) of the targets. In the outdoor experiment (experiment 2), at wavelengths <600 nm, all treatments had nearly the same spectra, and with the exception of the white painted tubs, all treatments had similar intensities (Fig. 4A). The low numbers of EB laid in the white painted tubs in experiment 2, despite the attraction to high intensity reflection exhibited in experiment 1, strengthen our reasoning that the polarization of reflection is the most important cue directing oviposition by chironomids in the wild. Having said that, one should note that in experiment 2, pond water was always favored over tap water (Fig. 4). Although there is no question that chironomid females readily lay eggs in tap water, and that polarization has a greater impact than the origin/quality of the water, it may possibly be that pond water carries an additional, yet undetermined, quality adding to its attractiveness.
One should note that the microvilli arrangement found in an ommatidium from the ventral part of a female eye (Fig. 10) support the behavioral findings. The microvilli in each rhabdom are seen to be parallel to one another and are generally aligned along three axes within the ommatidium, providing a potential anatomical basis for polarization sensitivity. Further detailed examination of the microvilli in different regions of the eye and a comparison with males, as well as a neurological study of the response of chironomids to polarized light, are needed to fully understand the properties of their polarization sensitivity.
Advantages of using polarization over intensity as an environmental cue during sunset
Short-lived animals, such as chironomids, need to have rapid and stable
environmental cues in their search for ovipositing sites. As mentioned
earlier, Meltser et al. (Meltser et al.,
2008) showed that, unlike mosquitoes, the preference of chironomid
females for an oviposition site is not guided by odor. Our light measurements
confirmed that whereas intensity decreases rapidly during sunset, percentage
polarization and e-vector orientation, which are determined by scattering and
absorption of light by suspended matter in the water, remain high and stable
throughout this period (Fig.
5). Furthermore, by using polarization as a cue,
polarization-sensitive animals can prolong their time of activity into the
twilight period [e.g. by using polarized moonlight, as do dung-beetles
(Dacke et al., 2003)].
Polarization as a predictor of the amount of food in water
In Fig. 9, it is
demonstrated that polarization reflected from the water surface is positively
correlated with the total organic carbon (TOC) concentration in the water. We
therefore believe that polarization can serve as a visual proxy for the amount
of food in the water available to the larvae of chironomid females. It is
important to note, however, that water depth and the darkness of the pond
floor, as well as non-organic light absorbing particles, which reflect low
intensity and high percentage polarization even in clear water, can easily
deceive ovipositing chironomid females, as exemplified in the results from the
black tub filled with tap water (BT) in experiment 2.
Wavelength sensitivity to polarization by chironomids
Schwind (Schwind, 1995)
showed that different species of aquatic insects respond differently to
surfaces reflecting polarization at different wavelengths. He divided species
into short wavelength users (UV; 
<400 nm) and long wavelength users
(green-yellow; =500—550nm). Chironomids are known to be
sensitive to light in both spectral regions
(Kokkinn and Williams, 1989).
In this study, UV radiance could not be correlated with oviposition response
due to system (polarizer) limitations. Since the radiance of green light could
be correlated with oviposition response, we can say that it is likely that at
least the `green' photoreceptors are polarization sensitive. The use of
spectral polarization by chironomids warrants further examination.
Percentage polarization or e-vector orientation — which is the guiding cue?
Over the years, most studies investigating the use of light polarization by
polarization-sensitive animals surmised that the cue actually used by the
animals is the e-vector orientation rather than the percentage polarization.
This is the case for navigating insects such as bees, ants, crickets and for
flying insects that use polarization to detect water bodies. Our results
indicate that at least in the case of chironomids, the cue is the percentage
polarization (Fig. 8). In our
experiments, the orientation of polarization was close to horizontal in all
cases because of strong attenuation (scattering and absorption) by suspended
matter in the water. As mentioned earlier, percentage polarization, which is
determined by the concentration of the suspended matter, can serve as a proxy
for the amount of particles containing organic carbon.
It is possible, however, that the low oviposition rates that we found at low percentage polarizations (<10%) are the result of high noise in the visual system of the animals that makes them insensitive to this low polarization signal. Such high neurological noise could also lower the response to polarizations of less than 20% (Figs 4 and 8). Further neurological measurements are required to assess and characterize the signal within the chironomid's brain.
Chironomid populations and cholera control
Chironomids are the carriers of the Vibrio cholerae bacterium, a
human pathogen responsible for the fatal cholera disease. The bacterium, which
feeds on the eggs, can be dispersed between water bodies by the adults
(Broza and Halpern, 2001;
Halpern et al., 2004;
Broza et al., 2005;
Halpern et al., 2006;
Paz and Broza, 2007). This
study suggests two ways to control chironomid abundance and dispersal and
consequently to limit the persistence and spread of cholera: (1) decrease the
number of preferred habitats for oviposition, and (2) direct the females to
alternative, more attractive artificial habitats and then collect or destroy
the eggs. The first strategy can be achieved by decreasing the percentage
polarization of light reflected from a water body by increasing the
reflectivity of the water. The second strategy can be achieved by creating
artificial trapping ponds near natural ponds that will be more attractive to
the females because of their high polarization reflection. This may be
expanded to polarized light traps placed alongside specific water bodies
(Kentaro Arikawa, personal communication). It is worth mentioning again our
preliminary observation that tubs with white edges above water level are
completely unattractive to chironomid females.
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Acknowledgments |
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