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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
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
* Author for correspondence (e-mail: a-ishima{at}nagasaki-u.ac.jp)
Accepted 4 September 2007
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Summary |
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Key words: mudskipper, reproduction, burrow, development
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Introduction |
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). Mudskipper terrestrial activity is supported by a capacity
for aerial respiration, to which epithelia in the gills, the buccal-branchial
cavity, and the skin all contribute in varying proportions, depending on
species (Graham, 1997). The
large buccal-branchial cavity of mudskippers is important for holding a
substantial air volume for respiration, as well as for territorial displays
and burrowing (Graham et al.,
2007). For example, the Malaysian mudskipper Periophthalmodon
schlosseri (Pallas) has a buccal-branchial cavity volume that is 16% of
its body volume (Aguilar et al.,
2000), which is much larger than the cavity volume of 2–6%
reported in gobies not specialized for amphibious air breathing
(Gee and Gee, 1991;
Gonzales et al., 2006). The
anatomical and physiological specializations of mudskippers enable them to
maintain metabolic rates in air that are generally equal to or higher than in
water (Graham, 1997;
Kok et al., 1998;
Takeda et al., 1999).
In contrast to activities on the mudflat surface, little is known about
mudskipper behaviour in burrows during high tide. Most mudskippers excavate
burrows and use them as a refuge from predators, for protection from
desiccation and temperature extremes, and for nesting. Although spawning in
burrows affords egg protection, the severe hypoxia of burrow water
(Ishimatsu et al., 2000)
raises the question of what mechanisms are used to ensure adequate
O2 for developing mudskipper eggs
(Gordon, 1995). Mudskipper
burrows often have one or more horizontal or upturned chambers near their
terminus where monolayers of fertilized eggs develop
(Brillet, 1976;
Clayton and Vaughan, 1986;
Kobayashi et al., 1971).
Recent studies document an air-deposition behaviour by burrow-guarding
mudskippers in the field (Ishimatsu et
al., 1998; Ishimatsu et al.,
2000) and in artificial laboratory burrows
(Lee et al., 2005), prompting
the hypothesis that eggs are spawned and develop within a burrow's
air-containing space. We tested this and related aspects of burrow incubation
of eggs by conducting field and laboratory studies of the Japanese mudskipper
Periophthalmus modestus Cantor. In the spawning season (mid-May to
late August in our study area) male P. modestus excavate `J' shaped
burrows (Fig. 1) having two or
three openings on the mudflat surface
(Kobayashi et al., 1971).
Using nuptial colouration and courtship displays the male attracts a female
into its burrow, where spawning occurs, and the fertilized eggs are deposited
in the terminus (Matoba and Dotsu,
1977). Thereafter, the male tends its burrow for about 1 week
until the eggs hatch.
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Burrow respiratory environment
Samples for burrow-water PO2 determinations
were taken in glass tuberculin syringes (1 ml volume), the tips of which were
inserted to a depth of at least 5 cm into the water standing in burrow shafts
at low tide. The filled syringes were immediately stored in ice water and
transported to the Saga Prefectural Ariake Fisheries and Development Center
where, following anaerobic centrifugation to separate the suspended mud
particles, the PO2 of the supernatant in each
was measured using an O2 electrode (E101, Cameron Instrument Co.,
TX, USA) and a meter (OM200, Cameron Instrument Co.). The total gas volume and
its PO2 and PCO2
levels were compared for 20 guarded egg chambers (i.e. eggs present) and 12
pre-spawning egg chambers (i.e. male courting, no eggs in the chamber).
Egg-chamber gas was obtained by forming a shallow depression over the burrow,
lining it with plastic sheeting and placing a thin layer of water therein, and
then compressing the underlying burrow to force air up under the plastic where
it could be withdrawn into a glass syringe for determination of volume and gas
content. Gas PO2 and
PCO2 were measured by chromatography (Shimadzu
GC-14B, Kyoto, Japan). Determinations were also made for both the average
particle size of the mud comprising the layer between the mudflat surface and
the egg chamber (Shimadzu SALD-3100 Laser Diffraction Particle Size Analyzer)
and the redox potentials (ORP electrode, 9678BN and 230Aplus meter,
ThermoOrion, MA, USA) of mud from the egg-chamber surface, the shaft walls,
and at sites remote from the burrow. A combination pH electrode (ThermoOrion
8163BN) was used as a reference electrode to improve stability of the redox
measurements.
Egg-chamber observations
Burrow structure and the instrumentation procedures are detailed in
Fig. 1. For each burrow
selected for instrumentation the first step was to remove standing water in
the shaft to prevent it from accidentally inundating the eggs when the egg
chamber was opened. The mud over the chamber and surrounding the burrow shaft
was then excavated down to the level of the chamber's roof. When the chamber
was opened, the presence of eggs was verified and their state of development
assessed by immersing a small number of eggs in water. If immersed eggs did
not hatch within 5 min, the chamber was considered to contain relatively young
eggs and instrumentation proceeded. The roof of the egg-chamber was fitted
with the upper-half of a plastic bottle into which both an endoscope
(HSCI-S10M, HOGA, Kyoto, Japan) and an O2 electrode (ThermoOrion
083025A) had been mounted. For two burrows a small TeflonTM tube (1 mm
i.d.) was also inserted into the chamber roof so that egg-chamber
O2 levels could be experimentally modulated (see below). Stainless
steel impedance electrodes were inserted in the burrow section below the egg
chamber (Fig. 1). Mud was then
replaced to cover and secure the instruments and the section of burrow shaft
destroyed by digging was reconstructed. Unless egg-chamber excavation and
instrumentation caused the burrow-guarding male to abandon the nest completely
(in such cases the eggs did not hatch), it would re-enter the burrow and
resume its activities. However, the male usually did not use the
hand-constructed opening, but built new connections to the vertical shaft. To
monitor the tidal cycle, a TygonTM tube connected to a pressure
transducer (Keyence AP-81A/AP-12, Osaka, Japan) was deployed on the mud
surface at nearly the same height as the reconstructed burrow opening.
Cables connecting the measuring devices to their monitors (ca. 10 m long) extended to a tent pitched on a nearby pier (ca. 3 m above the mudflat surface). Signals from the O2 electrode were fed to and saved every 5 min in an O2 meter (ThermoOrion 835A). The O2 electrode (a nominal drift of 0.1% per day) was calibrated with humidified N2 gas and air immediately before egg-chamber instrumentation and after termination of the observations. Egg-chamber PO2 data were corrected for hydrostatic pressure using measured water depth and specific gravity of 1.02 for seawater, and drift corrections assumed a linear drift over the observation period. Endoscope video recording was kept minimal to lessen the effects of light on the guarding male's behaviour. Signals from the tide-monitoring pressure transducer were digitized and stored every 5 min in a data acquisition system (Keyence NR-1000).
Preliminary laboratory experiments indicated that the passage of dead P. modestus through a pipe generated impedance signals of more than ±500 mV, and it was expected that this criterion could be used to indicate the number of trips made by the male into the burrow chamber. Burrow impedance signals were amplified with an impedance converter (model 2991, UFI, CA, USA), digitized by another data acquisition system (Keyence NR-2000), and stored in memory cards (32 MB) at a sampling rate of 2 Hz. The digitized data were analysed with software (Wave Shot v.1.05 and Flex Logger v.1.07, Keyence).
The two burrows in which the egg chamber had been fitted with a small TeflonTM tube (Fig. 1) were used to test the effects of a reduction in egg-chamber O2 level on fish passage through the burrow section connecting to the chamber (indicated by impedance spikes) as a possible indicator of air-adding behaviour. For these tests humidified hypoxic-gas mix, in which the PCO2 was adjusted to minimize changes in egg-chamber PCO2, was introduced into the egg chamber to reduce its PO2 to within 0.25 kPa of the levels observed at the beginning of the low tide period. Hypoxic gas injections were made approximately 1 h before the burrow was covered by water of the rising tide and while the burrow-guarding male was on the mudflat surface. After egg incubation and hatching were completed, egg-chamber air was withdrawn through the TeflonTM tube to determine the volume for the computation of air-adding frequency (see Appendix).
Laboratory studies of aerial egg development and hatching
Five intact egg chambers were transported to the laboratory for studies of
egg-hatching success in relation to time and for comparisons of the hatching
success of eggs in air and in water. After clearing mud from around the
chamber, the column of mud surrounding the intact egg chamber (i.e. a
complete, mud-walled, air-filled chamber having a ventral opening into the
burrow shaft) was extracted by sliding a bottomless plastic bottle over it,
placing a plastic plate under the open end of the bottle and lifting it out.
Only egg chambers with relatively young eggs (as defined above) were extracted
and, once in the laboratory, the chambers were incubated in high humidity at
23°C. About 50 eggs were removed from each chamber and used in daily 4 h
tests of hatching competence (done by immersing eggs in freshwater, 50%
seawater and full-strength seawater). Also tested was the viability of eggs
kept submerged in hypoxic water. The total number of eggs in each egg chamber
was estimated from the density of eggs and total surface area of the
chamber.
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;
Ishimatsu et al., 2000), there
was a significant inverse relationship between
PO2 and PCO2
(PCO2=2.65–0.11PO2,
r=–0.577, N=20, P=0.008,
Fig. 2). The egg-chamber
volumes of `still courting' (i.e. no eggs present) and `egg-guarding' males
did not differ (47±19 vs 43±15 ml, N=12) and,
while the
PO2–PCO2
regression slopes of the two were also not different (ANCOVA,
P=0.141), the mean PO2 of the `no-egg'
chambers was significantly less (6.15±4.66 kPa vs
13.8±3.0 kPa, P=0.04, t-test, d.f.=30).
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Maintenance of egg-chamber O2 by male's air-adding behaviour
Of 44 attempts to instrument burrows, only 6 records were obtained in which
egg-chamber PO2, endoscope video recordings,
and impedance data spanned 4 days or longer.
The PO2 records documented tidal-cycle related changes; O2 increased during low tide but dropped during high tide (Fig. 3A). The corresponding endoscope records verified that the eggs remained in air, that the male occasionally entered the egg chamber and that it was not adversely affected by the presence of air therein. The quality of the simultaneous burrow impedance records did not enable full quantification of male movement pattern. However, a semi-quantitative pattern of fish movement was discernible and, in the majority of cases, this showed that the male's passage through the burrow section under the egg chamber (and entry into the egg chamber) occurred mainly during low tide (Fig. 3A). The increase in egg-chamber PO2 during low tide was a common finding for all of the instrumented burrows. The average egg-chamber PO2 was 12.8±0.99 kPa (N=4) at the beginning of low tide exposure (i.e. burrow opening exposed to air) and was 16.8±0.32 kPa at the end of the low tide. The correspondence between the increase in PO2 and the impedance records suggests that during low tide the male adds gulps of air to the egg chamber and this raises PO2.
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Egg-chamber PO2 as a possible modulator of air-adding behaviour
To examine possible role of egg-chamber hypoxia as a modulator of
air-adding behaviour, a volume of hypoxic gas was injected into the egg
chamber to reduce PO2 to within 0.25 kPa of the
level observed at the beginning of the low tide period.
Fig. 4A,C show the gradual rise
in egg-chamber PO2 that occurred in two burrows
from the beginning of the low-tide period through about 7 h and up to the time
of hypoxic-gas introduction (arrowheads). Although hypoxic gas injection
reduced egg-chamber PO2 to near the level
observed at the beginning of each low tide, the male fish was able to rapidly
restore the PO2 within 1 h. For both of these
burrows ANCOVA comparisons show a significantly greater rate of
PO2 increase for the 60 min after hypoxia
injection than for the first 60 min of low-tide exposure, which implies that
air-adding behaviour was not solely modulated by egg-chamber air
PO2. This possibility is further supported by
the fact that the air-adding frequency (fa) following
hypoxic gas injection lies far above the calculated
fa–PO2 relationships
(Fig. 4B,D).
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Laboratory studies of mudskipper eggs
Eggs from the incubated chambers developed normally in air and had embryos
ready for hatching (indicated by frequent turning) within 6–7 days of
their estimated fertilization time
(Kobayashi et al., 1972). This
contrasts to eggs from these same burrows which, when placed in hypoxic water
(PO2
2 kPa, simulating typical burrow-water
conditions), succumbed within 2 days.
Although the laboratory-incubated eggs developed in air, they did not hatch and eventually died. It was found that water immersion (either in freshwater or seawater) was necessary to trigger egg hatching. Hatching competence tests on developing eggs over a 12-day period showed a 5–6 day window within which immersion must take place to ensure a mean successful hatch rate of 80% (Fig. 5). Eggs remaining in air beyond this time had a reduced hatching competence. Although hatching occurred in water of different salinities (i.e. freshwater, 50% seawater and full-strength seawater), larvae induced to hatch in freshwater did not survive unless transferred to higher salinities.
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Hatch induction caused by air removal and egg-chamber flooding
Endoscope video records (see Movie 1 in supplementary material) documented
the male's role in hatch induction (Fig.
6, Table 1).
Approximately 80 min after the burrow openings were inundated by the rising
tide, the egg-guarding male triggered egg hatching by expelling air from the
egg chamber, which immersed the eggs. Air removal was done by transporting air
gulps into the burrow shaft leading to the openings
(Fig. 1) and releasing them. As
this was occurring bubbles were observed exiting from the burrow openings.
Video records showed that flooding the chamber required the removal of an
average of 103±42 air gulps, which gave an almost exact volume of total
egg-chamber air (47 ml) based on the buccal-branchial capacity of P.
modestus (0.46 ml in a 2.6 g fish,
Table 1). Hatching occurred
during evening or nocturnal rising tides
(Fig. 7) but was not correlated
with the lunar cycle.
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;
Helfman et al., 1997;
Martin et al., 2004).
Mudskippers differ from these fishes that spawn at the water's edge since a
lack of cover and the extreme conditions on the mudflat preclude placement of
eggs on the open surface and make it impossible for an adult mudskipper to
remain with the eggs and care for them. Sequestration in burrows protects
mudskipper eggs from predation and tidal extremes in current flow, temperature
and salinity. However, the burrow water is extremely hypoxic
(Gordon, 1995;
Gonzales et al., 2006) (data
in the present study), so this requires a solution for the O2
supply problem which, as demonstrated here for P. modestus, is done
by egg development in air and refinements in parental care.
This study documents the critical importance of the male mudskipper in excavating a burrow, complete with an air chamber, at a position in the intertidal zone where it will have access to atmospheric air during low tide. Even though direct evidence for the presence of air in egg chambers could not be obtained, the differences in mud colour and the positive redox potential of chamber mud, the successful aerial egg development in the laboratory, and the burrow-guarding male's air-adding behaviour all attest to air deposition in egg chambers of intact P. modestus burrows. It should be noted that for another mudskipper, Periopthalmodon schlosseri, which is much larger than P. modestus, it has been possible to confirm the presence of air in egg chambers of intact burrows by directly inserting an endoscope through a much larger vertical shaft (A. Ishimatsu, T. Takeda, Y. Tsuhako and K. H. Khoo, manuscript in preparation).
Just as air access at low tide is required for egg-chamber O2
replenishment during incubation (Fig.
3), submersion of the burrow opening by a rising tide is necessary
for the male to induce hatching and larval escape by flooding the egg chamber
(Fig. 6). In addition to being
in synchrony with the tidal cycle, the male's egg-chamber management behaviour
is also modulated by its PO2
(Fig. 4). The aerial-egg
development and water-induced hatching demonstrated for P. modestus
in this study agrees with observations of Brillet
(Brillet, 1976) who, while not
detailing methodology, reported that the eggs of P. sobrinus [=P.
argentilineatus Valenciennes (Murdy,
1989)] required both air incubation and subsequent submersion for
hatching and did not survive if incubated in water or kept in air but not
immersed after development.
Air-adding behaviour
On the basis of the presence of air in the egg chambers of males engaged in
courtship (i.e. no eggs present), we speculate that both spawning and
fertilization occur in air, although this has not been observed. Details about
fish aerial spawning behaviour were recently described for the rockhopper
blenny Andamia tetradactyla (Bleeker)
(Shimizu et al., 2006). The
female deposits a monolayer of eggs in rock crevices along the splash zone,
which the male fertilizes by rubbing its genital papillae over them.
Periophthalmus modestus and other mudskippers may have a similar
spawning behaviour and, while this is not documented, egg-chamber videos
(Movie 1 in supplementary material) show that males can emerge into the air
phase and both turn and crawl on the mud and egg surfaces.
The comparable volumes of the `no-egg' and `egg-containing' chambers imply that the egg chamber is maximally filled with air at construction and that air additions during egg incubation displace excess air into the burrow shaft from where it ultimately exits the burrow. The pre-spawning deposition of air inside an egg chamber may be beneficial for maintaining egg-chamber PO2 during the incubation period because it would oxidize the highly reducing surrounding mud and thus lessen the total O2 need once eggs are added.
The correlation between male activity (impedance data) near the egg chamber
and its increase in PO2
(Fig. 3) most likely reflects
transport of mouthfuls of fresh air into the chamber. Because burrow shafts
are water-filled during low tide, it is not possible that air in the burrow
was trapped during low tide as suggested for P. sobrinus
(Brillet, 1976). Also, the
small particle size of the overlying dense mud, its low redox potential, and
the egg-chamber's position 20 cm under the mud surface
(Fig. 1), exclude the
possibility that the high egg-chamber PO2
results from the diffusion of atmospheric air. That the decline in egg-chamber
PO2 during high tide reflects egg-mass
respiration is suggested by the product of the measured rate of O2
consumption of a developing mudskipper egg [76.5± 12.0 nl
h–1/hatch-competent egg
(Etou et al., 2007)] and our
estimate of the number of eggs in the chamber (5200). Assuming an egg-chamber
air volume of 47 ml and a temperature of 24°C, the respiring egg mass
would consume 1.1–2.0 ml of O2 during a daytime high-tide
period on the day of hatching (duration ranging 170–310 min,
N=4; note that hatching occurred at the nocturnal high tide of the
same day), and this accounts for 75–100% of the observed egg chamber
aerial O2 depletion of the high-tide periods (1.2–2.3 ml
O2) calculated from the slope of egg-chamber air
PO2 over time (–0.013 to –0.018 kPa
min–1).
The lowest egg-chamber PO2 levels recorded
at the end of high tide ranged from 8.2 to 14.5 kPa (N=8). These are
above the critical PO2 (i.e. the O2
partial pressure below which aerobic metabolism declines) of a P.
modestus egg [4.3 kPa (Etou et al.,
2007)]. Although the high-tide decline in
PO2 did not reach the eggs' critical
PO2, this level would have eventually been
reached if the male had not added air during the subsequent low tide. Also,
variables such as chamber volume, egg mass, the burrow's position in the
intertidal zone, tidal amplitude, and whether or not the male also requires
egg-chamber O2 for respiration could all combine to cause greater
reductions in egg-chamber O2 during high tide.
Most nest-guarding fishes respond to hypoxia with fanning or other
ventilation behaviours to augment O2 delivery to the eggs
(Jones and Reynolds, 1999;
Takegaki and Nakazono, 1999).
For species guarding eggs in the intertidal zone, fanning may be needed during
low tide when pools are isolated and convective O2 delivery is
reduced. In this respect the air-adding behaviour of P. modestus
parallels fanning in being hypoxia-induced and linked to the tidal cycle. A
principal difference between the two is that, while requirements for fanning
can vary depending on variations in the physical and biotic factors around an
underwater nest, the small, mud-enclosed burrow egg chamber will always
require the addition of air, which can only be done during low tide. The male
must therefore ensure that there is sufficient O2 to meet the
requirement of the eggs during the subsequent high tide.
The mechanism enabling P. modestus to monitor O2 levels
in its egg chamber may not differ from the O2 sensing mechanisms of
other fish species. Most fishes have O2-sensitive chemoreceptors
that monitor the external environment and these are often positioned in the
buccal-branchial cavity, associated with the gills or other structures
(Milsom and Burleson, 2007).
These external receptors have an important role in rapid responses to hypoxia,
which appears important for air-breathing fishes
(Graham, 1997). For Pn.
schlosseri aerial hypoxia is a more important driver of air ventilation
than aquatic hypoxia (Aguilar et al.,
2000). While the air-adding behaviour of P. modestus is
likely a ventilatory response driven by external O2 receptors, it
requires a more sophisticated behavioural combination of air gulping at the
water surface, transporting mouthfuls of air down through the burrow shaft,
releasing these into the egg chamber and repeating this action until
egg-chamber PO2 reaches a level sufficient to
sustain the O2 consumption of the eggs during the following
high-tide period. The injection of hypoxic gas into the egg chamber late in
the low-tide period increased the male's air-adding frequency and egg-chamber
O2 was restored to its pre-hypoxia injection level within 1 h
(Fig. 4). The far higher rate
of air addition triggered by this treatment implies that the male somehow
modulates this behaviour by integrating information on egg-chamber
PO2 that must be attained by the end of low
tide and the time available before the next submersion. This could be tested
through hypoxic gas injections at different times during low tide.
A male P. modestus can readily add air during low tide, but
numerous obstacles prevent this at high tide. When the burrow is submerged (by
as much as 2 m at high tide in our study site), the male would need to swim to
the surface, gulp air, and return it to the burrow. Direct observations of
male activity during high tide are difficult because the water covering the
mudflat at high tide is extremely turbid. Nevertheless, mudskippers were never
observed surfacing to gulp air during high tide. If the male's primary duty is
to guard the nest, it may spend high tide near the burrow openings where,
while intercepting potential predators, it could respire aquatically
(Tamura et al., 1976). Both
endoscope and impedance data suggest that the male does not spend much time in
the egg chamber during high tide. However, this conclusion is tentative
because endoscope recording times were kept minimal to lessen disturbance from
its light and the lower number of impedance spikes at high tide does not
indicate that the fish is not in the egg-chamber.
Induction of hatching by air removal
Inundation is the most common hatch mechanism for the aerially spawned eggs
of fishes (Yamagami, 1988) and
amphibians (Warkentin, 2002).
Egg submergence may be by rain-caused flooding or by cyclic change in water
height (spring tides). In cases where immersion occurrence is less
predictable, extra yolk supply within the egg extends hatch competency
(Moffatt and Thomson, 1978).
Egg hatching for P. modestus differs from these general examples in
that, once development is complete, the guarding male triggers hatching by
inundating the egg chamber. This behaviour, which usually occurs during a
nocturnal rising tide (Fig. 7),
may be initiated through the male's capacity to sense that egg development is
complete (e.g. increased vibrations from turning larva) or through an
endogenous factor (e.g. a tidal rhythm) regulating its behaviour. However,
because P. modestus eggs only have a 5–6 day window for
hatching competence, the male's initial selection of burrow position within
the intertidal zone and the timing of spawning in its burrow relative to the
tidal cycle are important factors in hatching success.
It is not known how hatched larvae make their way from the egg chamber to
the open water where they will live in the plankton for about 50 days
(Kobayashi et al., 1972).
Preliminary field experiments suggest that relatively few of the hatched
larvae are able to find their way out of the burrow. However, rapid escape is
important as survival of newly hatched larvae kept in hypoxic water
(PO2=2.0 kPa) quickly decreased with time (35%
in 3 h and <10% in 8 h) (Etou et al.,
2007). Whether or not the guarding male is involved in
transporting larvae out of the burrow remains to be determined.
The origin of subterranean aerial brooding in mudflat gobies
Fishes in the family Gobiidae are typically substrate brooders and attach
adhesive eggs to rocks, in depressions, or to the inside of enclosed spaces
including burrows (Breder and Rosen,
1966; Thresher,
1984). In addition to egg guarding, male gobies carry out other
parental-care behaviours such as preening and fanning that have been described
for other species (Blumer,
1982; Breder and Rosen,
1966). As common among gobies, these traits appear to have
developed before mudskipper's invasion of the land and have set a stage for
the development of their novel reproductive strategy. Acquisition of
air-breathing capability is a vital prerequisite for brooding eggs in a burrow
filled with hypoxic water, which demands the storage of air within the burrow
and aerial egg development. Several of the other species classified with
mudskippers in the subfamily Oxudercinae also live in burrows and have the
capacity to gulp air at low tide, suggesting that they are also air breathers
(Graham et al., 2007). Another
mudflat dweller, the eel goby Odontamblyopus lacepedii, which is
sympatric with P. modestus, has recently been shown to be a
facultative air breather (Gonzales et al.,
2006). Odontamblyopus, however, is not amphibious and is
restricted to its extensive mudflat burrow where, during low tide, it breathes
air to sustain metabolism. The eel goby's reproductive behaviour is not known,
however, fish that spawned in captivity attached their eggs along the upper,
inner side of the submerged clay pipes in their holding tank
(Dotsu and Takita, 1967),
implying that burrow spawning may occur. If O. lacepedii and some of
the other oxudercines are burrow-brooders then, because of severely hypoxic
burrow water (Gonzales et al.,
2006; Ishimatsu et al.,
2000), both air storage and air-adding behaviour during low tide
are likely requirements for reproductive success. Investigations into the
reproductive strategies of other gobies of Oxudercinae and related subfamilies
would shed light onto the evolution of subterranean aerial brooding of
mudskippers.
Conclusion
In summary, mudskippers maximize their potential for reproductive success
in the mudflat habitat with eggs that are capable of developing within the air
placed in the burrow egg chambers by the male. In addition to guarding the
nest, the male carries out elaborate egg-care behaviours that include gulping
air and transporting it to the egg chamber at low tide to ensure adequate
oxygen supply for the subsequent high tide (when air cannot be obtained), the
orchestration of submergence hatch induction by removing air and thus flooding
the egg chamber during a rising tide, and possibly the facilitation of burrow
escape by the newly hatched larvae.
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References |
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Aguilar, N. M., Ishimatsu, A., Ogawa, K. and Khoo, K. H. (2000). Aerial ventilatory responses of the mudskipper, Periophthalmodon schlosseri, to altered aerial and aquatic respiratory gas concentrations. Comp. Biochem. Physiol. 127A,285 -292.
Blumer, L. S. (1982). A bibliography and categorization of bony fishes exhibiting parental care. Zool. J. Linn. Soc. 76,1 -22.
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