First published online November 2, 2007
Journal of Experimental Biology 210, 3946-3954 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.010686
Mudskippers brood their eggs in air but submerge them for hatching
Atsushi Ishimatsu1,*,
Yu Yoshida1,
Naoko Itoki1,
Tatsusuke Takeda2,
Heather J. Lee3 and
Jeffrey B. Graham3
1 Institute for East China Sea Research, Nagasaki University, Tairamachi,
Nagasaki 851-2213, Japan
2 Department of Animal and Marine Bioresource Science, Faculty of
Agriculture, Kyushu University, Hakozaki, Fukuoka 812-8581, Japan
3 Center for Marine Biotechnology and Biomedicine and Marine Biology
Research Division, Scripps Institution of Oceanography, University of
California, San Diego, La Jolla, CA 92093-0204, USA
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Fig. 1. Three-dimensional drawing of a Periophthalmus modestus burrow
showing monitoring device positions: O2 electrode (O), endoscope
camera (E), tube for gas injection (G), stainless-steel electrodes (S) for
impedance measurement (I), and pressure transducer tube connection (T). Thick
dotted line above egg chamber shows the level of burrow excavation required
for instrumentation. Thin broken line under the egg chamber shows approximate
position of the air–water interface.
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Fig. 2. Relationship between PO2 and
PCO2 of Periophthalmus modestus
egg-chamber air determined for burrows with egg-guarding males (solid circles)
and courting males (open circles). Regression equations are
PCO2=2.62–0.11PO2
(r=–0.577, N=20, P=0.008) for burrows with
guarding males, and
PCO2=1.53–0.05PO2
(r=–0.678, N=12, P=0.015) for burrows with
courting males. Slopes are not significantly different from each other
(ANCOVA, P=0.141).
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Fig. 3. Continuous records of Periophthalmus modestus egg-chamber air
PO2 (black line) and the timing of the male's
egg-chamber visits (indicated by impedance signals, grey spikes) in relation
to the tidal cycle. Data acquisition began with the day of instrumentation and
continued until egg hatching, initiated by the male on a rising tide (blue
triangle). The beginning of day zero is set to the time when a burrow was
covered by an incoming tide, following which egg hatching occurred. The
initial high PO2 reflects the opening of the
egg chamber to air during instrumentation. (A) Record for a burrow regularly
covered (blue bars) and uncovered by the tidal oscillation (red lines show the
highest tide). (Note: No impedance data for day –3 due to a technical
problem.) (B) Record for a burrow located sufficiently high on the mudflat to
be continually exposed to air until day zero when the rising tide covered the
burrow (blue bar) and hatching occurred (blue triangle).
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Fig. 4. Effect of hypoxic gas injection on egg-chamber
PO2 (A,C) and estimated air-adding frequency
(B,D) of two male Periophthalmus modestus. (A,B) Burrow instrumented
on June 30, 2004. (A) Real-time records of the low-tide increase in
egg-chamber PO2 contrasted with the
significantly higher (3.2x, P<0.0001, ANCOVA)
PO2 increase rate observed over 60 min
following hypoxia injection (arrowhead) than at the beginning of the low-tide
period with nearly identical initial PO2. (B)
An inverse relationship between egg-chamber PO2
and air-adding frequency (fa) as determined for five
complete low-tide periods preceding hypoxic-gas injection (solid symbols) and
fa after injection (open symbol). Egg-chamber
PO2 at the beginning of each 60 min segment is
plotted against fa (see Appendix). Regression line
equation;
fa=1.39PO2–0.872
(P=0.006, r=0.449, the post-hypoxia value is not included in
the regression). (C,D) Burrow instrumented on July 29, 2004. (C) Real-time
records of egg-chamber PO2. Hypoxia injection
(arrowhead) caused 3.2-fold higher PO2 increase
than at the beginning of the low-tide period (P<0.0001, ANCOVA).
(D) An inverse relationship determined for four low-tide periods and higher
fa immediately following hypoxia injection, as in A.
Regression line equation;
fa=19.68PO2–1.729
(P<0.0001, r=0.881). Solid and open symbols represent
data points obtained before and after hypoxic-gas injection, respectively, as
in B.
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Fig. 5. Daily determinations of the hatching percentage of Periophthalmus
modestus eggs taken from five intact, air-filled egg chambers (separate
lines) that were incubated in the laboratory. Hatching was induced by
submerging about 50 eggs removed from the chambers in 50% seawater.
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Fig. 6. Interior view of Periophthalmus modestus egg chamber. (1) Eggs on
the mud wall of a laboratory-incubated chamber (scale bar 1 mm). (2–7)
Endoscope video frames documenting hatch-induction behaviour (June 19, 2002).
Vertical view is down, through the egg chamber (note glistening monolayer of
eggs on the mud wall), to the burrow-water surface. The male appears at the
surface with its mouth open, and becomes progressively larger as it moves
closer to the camera. Removing mouthfuls of air (3,4,6,7) raises the water
level, which immerses the eggs, causing them to hatch. (8) Hatched larvae
[average total length 2.84 mm (Kobayashi
et al., 1972 )] swimming in the flooded egg chamber 48 min after
frame 7 (see also Movie 1 in supplementary material).
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Fig. 7. Relationships between tidal height and the timing of hatch induction of
Periophthalmus modestus. The horizontal grey bar represents heights
of mudflat surface in which openings of P. modestus burrows were
located. Different curves show changes in tidal height during the last tidal
cycles of egg incubation periods determined for 11 burrows. Curves are
adjusted to the peaks of flood tide (time zero). The rectangle encloses the
curves for an approximate range in which hatch induction occurred.
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© The Company of Biologists Ltd 2007
