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AMER. ZOOL., 39:279-288 (1999)
Ready and Waiting: Delayed Hatching and Extended Incubation of
Anamniotic Vertebrate Terrestrial Eggs1
KAREN L. M. MARTIN 2
Department of Biology, Pepperdine University, 24255 Pacific Coast Highway,
Malibu, California 90263-4321
Some anamniotic aquatic vertebrates lay eggs in a terrestrial habitat
that is hostile to the survival of hatchings or larvae. These terrestrial eggs are
ready and able to hatch at a particular developmental time, but do not hatch until
presented with suitable conditions for aquatic larval survival. Beyond this time,
hatching is possible whenever aquatic conditions occur. The duration of extended
terrestrial incubation is dependent on the availability of energy for metabolism
from the yolk. Extended incubation is useful for anamniotic eggs laid in terrestrial
habitats where conditions suitable for larval survival arrive with unpredictable or
variable timing. Examples of anamniotes with delayed hatching and extended terrestrial incubation can be found among teleost fishes, anurans, and caudate amphibians. This paper characterizes the embryonic period, compares this mode with
other forms of developmental plasticity in anamniotes, evaluates the constraints
and advantages of this life history mode, and examines how some fishes and amphibians are able to obtain the benefits of terrestriality for their eggs when the
timing of the return to aquatic conditions is not entirely predictable.
SYNOPSIS.
279
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labels as "embryonic" the cleavage egg,
the egg-encased embryo and the free embryo after hatching but before feeding, and
"larval" after the initiation of exogenous
feeding. However, in anamniotes that delay
hatching by extending incubation, eggs of
the same clutch, with the same fertilization
date, may hatch at very different times.
Thus one individual may be a viable, eggencased embryo, at the same age as another
member of the same clutch is an actively
feeding larva ready to metamorphose, depending on when hatching of each occurs.
For this paper, hatching marks the end of
embryonic development and the initiation
of the larval period.
Delayed hatching and extended incubation should be favored in situations with
relatively high mortality of larvae but relatively safe eggs (Warkentin, 1995). Anamniotic vertebrate eggs may survive and
even thrive terrestrially in moist habitats,
although larvae must be aquatic for feeding
and growth. Terrestriality is advantageous
1
From the Symposium Aquatic Organisms, Terres- to egg incubation in several ways (see
trial Eggs: Early Development at the Water's Edge Strathmann and Hess, 1999; Woods, 1999).
presented at the annual meeting of the Society for Integrative and Comparative Biology, 3-7 January 1998, This paper will examine how some fishes
and amphibians are able to obtain the adat Boston, Massachusetts.
2
vantages of terrestriality for their eggs, even
E-mail [email protected]
INTRODUCTION
Hatching is a life-history switch point
(Sih and Moore, 1993), when an animal
changes from an intracapsular egg to a freeliving larva (Yamagami, 1988). Eggs are
sessile, spherical, and have limited energy,
but larvae are motile, complexly shaped,
and can take in food. Hatching time typically depends on temperature and a genetic
timetable (Yamagami, 1988). However,
some aquatic anamniotes lay eggs terrestrially and can delay hatching by extending
incubation time in response to environmental conditions. Delayed hatching of anamniotic vertebrates is characterized by great
temporal plasticity in the embryonic period
(DiMichele and Taylor, 1980; Bradford and
Seymour, 1985, Darken et al., 1998).
Among anamniote species, hatching occurs at widely different stages of development, thus Balon (1984, p. 37) suggested
that hatching itself is "insignificant in the
life-history model" for fishes. His model
280
K. L. M. MARTIN
when the timing of the return to aquatic
conditions for their larval stage is not entirely predictable.
of delayed hatching with extended terrestrial incubation.
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An environmental trigger for hatching
Anamniotic vertebrates extend incubaDefinition of delayed hatching with
tion by delaying hatching past the time of
extended incubation
developmental readiness. Hatching is initiDelayed hatching with extended incuba- ated by environmental cues corresponding
tion involves straightforward development to the return of aquatic conditions suitable
during an obligatory primary incubation pe- for larval survival and growth. The chorion
riod, when the embryo is ready and able to of anamniotes is very thin, and eggs can
hatch. If aquatic, the embryo hatches at this respond readily to environmental cues
time, but if terrestrial, it remains in the egg (DiMichele and Taylor, 1981; Petranka et
for an extended period without hatching. al, 1982; Sih and Moore, 1993).
During extended incubation, the embryo is
Hatching is initiated by a low partial
active metabolically and is able to hatch at pressure of oxygen in the water around the
any time. Extended incubation is faculta- eggs of the salamander Ambystoma opacum
tive, not obligatory. If the eggs are aquatic, (Petranka et al, 1982), the frog Pseudothey will hatch as soon as they are devel- phryne bibroni (Bradford and Seymour,
opmentally ready, with no delay (David, 1985; Geiser and Seymour, 1989), and the
1939; DiMichele and Taylor, 1981; Brad- salt marsh fish Fundulus heteroclitus
ford and Seymour, 1985). When terrestrial (DiMichele and Taylor, 1981; DiMichele
eggs are placed in water, they hatch readily, and Powers, 1984a). Low oxygen tensions
within minutes or hours (Fig. 1), and com- are unlikely in air because of rapid diffumence larval development.
sion and a small boundary layer effect
Delayed hatching with extended incuba- (Bradford, 1984; Strathmann and Hess,
tion is found in variable habitats, such as 1999).
vernal freshwater pools or the marine interDelaying hatching and extending incutidal zone, including salt marsh and sandy bation in response to environmental cues is
beaches. Hatching occurs on the return of particularly beneficial when suitable enviaquatic conditions, in the form of high tides ronmental conditions do not arrive at a set
(Walker, 1952; DiMichele and Taylor, 1980; time, as with variable heights of highest
Taylor, 1990) or rainfall (Petranka and Pe- tides (Moffat and Thomson, 1978), or untranka, 1981; Bradford and Seymour, predictable rains (Petranka and Petranka,
1981; Bradford and Seymour, 1985). The
1985).
duration
of extended incubation following
Eggs are constantly metabolically active
throughout terrestrial incubation, with no readiness to hatch may be a few days or
diapause or metabolic arrest (DiMichele several months (Fig. 2), depending on yolk
and Powers, 1981a; Seymour et al, 1991, reserves and the developmental program.
Darken et al., 1998). Metabolism is enabled Amphibians that delay hatch until rainfall
and limited by the amount of yolk and the arrives appear to have a greater length of
temperature (Moffatt and Thomson, 1978; maximal delay than fish hatching in response to the more predictable return of
Bradford, 1990). Development continues tides; anamniotes that respond to tides can
within the egg during extended incubation, generally delay hatching for only one or
but at a much slower rate than for individ- two tidal cycles, or less. In some cases the
uals of the same age that have already delay can extend the time of the incubation
hatched (Bradford and Seymour, 1988). period four to six fold (Fig. 2).
Yolk reserves decline substantially during
extended incubation, and if eggs remain terEXAMPLES OF ANAMNIOTES WITH
restrial, the embryos die without hatching
DELAYED HATCHING
when reserves are exhausted (Bradford and Teleosts
Seymour, 1988; Darken et al, 1998). The
Among teleosts, the best-studied example
anamniote taxa in Table 1 have this mode of delayed hatching with extended incuba-
281
DELAYED HATCHING OF TERRESTRIAL EGGS
AQUATIC CONDITIONS
TERRESTRIAL CONDITIONS
EGG
EGG
I
I
EMBRYO
development to hatching readiness
EMBRYO
development to hatching readiness
(EITHER)
^ \
aquatic conditions arrive
(OR)
I
HATCHING at primary time
LARVAL STAGE BEGINS
terrestrial conditions delay hatching
embryonic incubation is extended
(OR)
luration
HATCHING after exten
I
LARVAL STAGE BEGINS
if terrestrial conditions persist,
EMBRYO DIES without hatching
FIG. 1. Sequence of events in eggs of anamniotic vertebrates that can delay hatching with extended incubation,
exposed to aquatic and terrestrial conditions.
tion is the mummichog Fundulus heteroclitus (Cyprinodontidae). This fish spawns
aquatically in salt marshes at highest tides.
Eggs adhere on seagrasses and are emerged
into air at low tides (Taylor et al., 1977,
1979). During emergence, high partial pressures of oxygen inhibit hatching (DiMichele and Powers, 1984a). Eggs are able
to hatch within nine to twelve days following fertilization, but they can extend incubation to thirty-seven days after fertilization
(DiMichele and Taylor, 1980; Fig. 2).
Hatching occurs at any time in the extended
incubation period, within fifteen to twenty
minutes after eggs are immersed in water
(Taylor et al., 1977).
The ability to delay hatching and extend
incubation is not present uniformly
throughout populations of F. heteroclitus.
Eggs may develop and hatch at different
rates following same spawning run. The homozygous genotype LDH-BbBb is present at
higher than expected frequencies in
emerged eggs after a high tide (DiMichele
TABLE 1. Anamniotic vertebrates known to extend incubation by delaying hatching during terrestrial development. *
Taxa
Osteichthyes:
Cyprinodontiformes
Atheriniformes
Salmoniformes
Lissamphibia:
Anura
Caudata
Genus and species
Reference*
Fundulus heteroclitus
F. confluentes
Aidinia xenica
Leuresthes tenuis
Galaxias maculatus
DiMichele and Tayler, 1980
Tayler, 1990
Hastings and Yerger, 1971
Moffatt and Thomson, 1978
McDowall, 1968
Pseudophryne bibroni
Ambvstoma opacum
A. cingulatum
A. gracile
Bradford and Seymour, 1985
Petranka and Petranka, 1981
Anderson and Williamson, 1976
Marco and Blaustein, 1999
* For additional references, please see the text.
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(EITHER)
aquatic conditions arrive
282
K. L. M. MARTIN
Species
A. gracile
A. cingulatum
] 150 %
[Ml
| 500 %
[mim
A. opacum
730 %
P. bibroni
"| 400 %
G. maculatus mini
| 430 %
flM
F. confluentes
[Mil
F. heteroclitus
mm
LU Primary
D Extended
| 170 %
0
| 570 %
20
| 310 %
40
60
80
100 120 140 160
Days to hatching
FIG. 2. Normal time in days to hatching readiness or primary hatching, compared to maximal duration of
extended incubation, for eight species of anamniotes. Percentage increase in incubation time is indicated. Primary
and extended incubation times were taken from the following references: F heteroclitus (DiMichele and Taylor,
1980), F. confluentes (Taylor, 1990), Ad. xenica (Hastings and Yerger, 1971), L. tenuis (Darken et al., 1998), G.
maculatus (McDowell, 1968); P. bibroni (Bradford and Seymour, 1985); A. opacum (Petranka and Petranka,
1981), A. gracile (Marco and Blaustein, 1999) and A. cingulatum (Anderson and Williamson, 1976). Most of
these values are approximations, estimated from field studies without controlled temperatures. See Table 1 for
taxonomic information.
et al, 1986). This genotype is slower to
hatch than eggs of heterozygous LDH-BaBb
that are slower than LDH-BaBa. Some genotypes of F. heteroclitus may spawn higher in the intertidal zone than others (DiMichele and Powers, 1984c).
Aidinia xenica (Cyprinodontidae), the diamond killifish, also spawns in tidal marshes semilunarly at the highest tides. Its eggs
normally require ten to fourteen days to
reach hatching readiness, but may extend
incubation for ten additional days if terrestrial (Hastings and Yerger, 1971). Eggs of
Fundulus confluentes (Cyprinodontidae)
also hatch in ten to fourteen days (Harrington, 1959), but can delay to eighty days if
the eggs are emerged on littoral plants.
When placed in water, the eggs hatch in
thirty minutes.
California grunion, Leuresthes tenuis
(Atherinidae) eggs can delay hatching and
extend incubation (David, 1989; Moffatt
and Thomson, 1978; Darken et al, 1998).
Grunion emerge from the ocean to spawn
terrestrially on nights following the highest
semilunar tides (Walker, 1952). Eggs de-
velop above the water line buried in moist
sand (David, 1939), and are ready to hatch
in nine days (Walker, 1952). If the eggs are
washed out to sea during the next high
tides, they hatch rapidly (Walker, 1952).
However, if the waves do not reach the
eggs, as happens frequently along the California coast, the eggs can extend incubation to thirty-five days (Moffatt and Thomson, 1978; Darken et al, 1998; Fig. 2). This
period encompasses the next two highest
semilunar tides.
Grunion embryos increase metabolism
during the primary incubation period until
ready to hatch, then they consume energy
at a constant rate during extended incubation (Darken et al, 1998). At any time after
hatching readiness, if the eggs are immersed, hatching will occur. However,
hatching success decreases over time
(Darken et al, 1998), indicating a cost to
survivorship during the extended incubation period. If hatching does not occur within six weeks post-fertilization, the yolk reserves are exhausted and the embryos die
(Darken et al, 1998).
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Ad. xen/ca
DELAYED HATCHING OF TERRESTRIAL EGGS
Anura
The terrestrially breeding frog Pseudophryne bibroni (Myobatrachidae) lays eggs
terrestrially beneath vegetation (Bradford
and Seymour, 1988). Embryos develop to
Gosner stages 24-26 approximately thirtythree days after fertilization, whether in water or in air. Then if aquatic, they hatch
(Bradford and Seymour, 1985). Both aquatic and terrestrial groups continue to grow
identically to stage 27 at thirty-six days,
then the terrestrial embryos delay hatching,
extend incubation, and dramatically slow
development (Seymour et ah, 1991). Eggs
in extended incubation have a fairly constant metabolic rate that is lower than actively swimming larvae of the same age,
and deplete yolk more slowly than larvae
(Bradford and Seymour, 1985), even though
the larvae are feeding. Eggs can hatch at
any time if immersed in water. In the field,
incubation may be extended three months
past the time of readiness to hatch, for a
total incubation of four months (Fig. 2).
With terrestrial development, P. bibroni
tadpoles hatch at a larger, more advanced
stage than similar amphibians that lay eggs
after the pools refill. If left in air, the eggs
usually do not hatch spontaneously, remaining in the egg capsule until death (Geiser
and Seymour, 1989).
Caudata
The marbled salamander Ambystoma
opacum (Ambystomatidae) lays eggs in the
fall in depressions at the edges of ephemeral pools. Embryos develop to hatching
readiness in nine to fifteen days, but may
remain within eggs for three to four months
(Petranka and Petranka, 1981). Eggs are
guarded by the female parent and embryonic survival increases with duration of parental care (Jackson et al., 1989), but females frequently desert nests after several
weeks (Petranka, 1990). Eggs hatch in minutes to hours after they are inundated with
rainwater (Petranka et al., 1982). The size
of the hatchling increases to some extent
with increased incubation time, and yolk reserves decrease (Petranka, 1998).
Another Ambystoma species courts terrestrially, A. cingulatum, the flatwoods salamander (Petranka, 1998). It breeds in pine
flatwoods, marshes, and roadside ditches
(Anderson and Williamson, 1976), depositing eggs under mats of vegetation or occasionally on bare soil (Anderson and Williamson, 1976; Means et al., 1996). Ready
to hatch in two weeks, eggs do not hatch
until inundated, so incubation may be extended as much as two to three months in
the field (Anderson and Williamson, 1976).
Hatching occurs within a few hours after
rainfall (Anderson and Williamson, 1976).
Ambystoma gracile (Ambystomatidae)
lays its eggs aquatically attached to submerged branches in pools, but over time
with evaporation, some of the eggs may be
emerged into air (Marco and Blaustein,
1999). The emerged eggs do not hatch with
the aquatic eggs at twenty days, but can extend incubation by at least eleven more
days, delaying hatching until submerged
(Marco and Blaustein, 1999).
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The California grunion's congener, the
Gulf grunion, L. sardina (Atherinidae), also
spawns out of water at high tides (Thomson
and Muench, 1976). However, L. sardina
eggs do not apparently delay hatching or
extend incubation (Moffatt and Thomson,
1978). The highest tides in the Gulf of California are much more consistent in height
than those on the coast of California, and
this environment difference may have led
to the evolution of delayed hatching and extended incubation in L. tenuis but not L.
sardina (Moffatt and Thomson, 1978).
A freshwater salmoniform fish, Galaxias
maculatus (Galaxiidae), migrates catadromously downstream to tidal estuaries in Australia (Pollard, 1971) where it spawns
aquatically on flooded grass flats following
the highest spring tide (McDowall, 1968).
The eggs wash down clumps of grass as the
tide ebbs, protecting them from desiccation.
They develop out of water high in the intertidal zone, and are ready to hatch in two
weeks, upon immersion during the next
highest tide. However, if the water does not
reach the eggs, hatching can be delayed and
incubation extended as much as two months
or more (McDowall, 1968; Fig. 2).
283
284
K. L. M. MARTIN
the delay by initiating hatching as in the
terrestrially developing species.
Embryonic aestivation
Aestivation in annual fishes is not delayed hatching with extended incubation in
the sense used in this paper. Austrofundulus
myersi and Cynolebias (Cyprinodontidae)
develop under different schedules when environmental conditions vary (Wourms,
1972). In one mode, eggs are laid in temporary pools with terrestrial development to
the point of readiness to hatch, then enter
diapause with very low metabolism for several months. The eggs hatch when the pools
are filled with water after rain (Taylor,
1990). These are obligatory arrests of development during diapause, unlike the facultative and variable delay before hatching
of the cyprinodont Fundulus heterocUtus or
others listed in Table 1, that maintain metabolism during incubation (Taylor, 1990).
The embryonic metabolic arrest of annual
fishes, called diapause III by Wourms
(1972), may be an intensification of delayed
hatching (Taylor, 1990), but it is not clear
which mode is ancestral, or indeed if each
developmental mode evolved separately.
Predator-induced accelerated hatching
The tree frog Agalychnis callidryas (Hylidae) lays eggs out of water attached to tree
leaves. The tadpoles hatch and fall into
pools below within eight days (Warkentin,
1995). If the eggs are preyed upon terrestrially by a snake, they can hatch sooner, as
early as five days. The larvae from accelerated hatches are smaller and less developed, and more vulnerable to aquatic predators, than larvae that remain in eggs longer
(Warkentin, 1995).
Predator-induced delayed hatching
A different mode of developmental plasticity is shown by the aquatic eggs of the
salamanders Ambystoma texanum and A.
barbouri (Ambystomatidae; Sih and
Moore, 1993). The embryos sense potential
predators via chemical cues, and delay
hatching to reduce predation risk until a later, larger stage of development. This delayed hatching differs in three important
ways from that of Ambystoma opacum (Petranka and Petranka, 1981) and the other
anamniotes listed in Table 1. First, A. texanum and A. barbouri eggs are aquatic at
all times. Second, A. texanum and A. barbouri larvae hatch at a more advanced stage
after a set delay, according to an alternative
developmental timetable, while eggs that
extend incubation indeterminately have larvae that hatch at nearly the same stage as
those of the primary incubation time (Fig.
1). Third, environmental cues initiate the
delay of hatching, rather than terminating
Terrestrial incubation of amphibians
Terrestrial oviposition and development
occur in most species of the Australian frog
family Myobatrachidae in the genera Pseudophryne, Geocrinia, and Helioporus
(Bradford, 1990). Any of these may have
the ability to extend incubation and delay
hatching, although study is needed.
Amphibians that breed terrestrially have
protracted development in general (Bradford, 1990), even though only a few species
actually delay hatching. The large terrestrial
eggs of the plethodontid salamander Bolitoglossa produce young that emerge at an
advanced stage (Hanken, 1979), with the
longest known amphibian incubation.
Air emergence of intertidal fish eggs
Many species of intertidal fishes (and invertebrates) spawn in the intertidal zone
(Taylor, 1990; DeMartini, 1999), including
several other species that spawn on the
highest semilunar tides, for example Fundulus majalis, F. similis, F. grandis (Taylor,
1990) and the puffer fish Takifugu niphobles (Yamahira, 1996). It is likely that these
eggs are exposed to air for varying periods
of time during incubation, and T. niphobles
eggs do not hatch if emerged, but the ability
to delay hatching and extend incubation has
not been studied in these fishes, and may
not be present (or necessary).
DISCUSSION
Delayed hatching with extended incubation is strikingly similar in widely disparate
lineages (Table 1). Clearly this mode of re-
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DEVELOPMENTAL PLASTICITY IN OTHER
ANAMNIOTIC VERTEBRATES
DELAYED HATCHING OF TERRESTRIAL EGGS
production is beneficial under certain specialized circumstances, but may be too costly in terms of egg provisioning to be a
widespread in any clade. Consider the potential constraints and advantages of this reproductive mode.
anamniotic eggs of many species may benefit from some incubation in air.
Increased developmental plasticity
through extended incubation may increase
egg survival if the habitat is not favorable
for larvae at the "expected" or primary
hatching time. Therefore, embryos are not
compelled to hatch at a particular time into
an unfavorable, terrestrial habitat to face
death, but instead can delay hatching until
favorable, aquatic conditions occur. Amphibian larvae with extended incubation
may be somewhat larger or more advanced
in development than those that hatch at the
primary time (Petranka, 1990; Sih and
Moore, 1993; Warkentin, 1995), and this
may give them an advantage in competition
with other species.
Hatching in response to an environmental
cue may allow synchronization. Hatch synchronization could increase larval survival
by decreasing likelihood of predation or by
initiating larval development simultaneously so that all individuals can be deployed
into an ephemeral habitat rapidly. Synchronization may compensate for different developmental rates in a clutch or within a
population (DiMichele and Powers, 1984c).
Conversely, hatching with an environmental trigger may permit several hatch dates
for a single population with different nest
sites (Petranka and Petranka, 1981; DiMichele et al., 1986), resulting in less competition for food and space.
Constraints of delayed hatching with
extended incubation
The constraints of delayed hatching with
extended incubation include increased egg
size, vulnerability of anamniotic eggs to terrestrial conditions, and costs in mortality or
condition of the eggs and larvae.
Eggs that delay hatching must have large
yolks to provide energy during extended incubation (Moffett and Thomson, 1978;
Bradford and Seymour, 1985). Although
both grunion fish are similar in adult size,
the mean egg volume of the California
grunion L. tenuis is 310% greater than in
the gulf grunion, L. sardina, with yolk accounting for 85% of the total (Moffatt and
Thomson, 1978). The eggs of L. tenuis delay hatching and eggs of L. sardina do not.
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Advantages of delayed hatching with
extended incubation
Three major advantages of delayed
hatching with extended incubation for anamniotes include the use of novel habitats
for reproduction, the benefits of terrestriality for eggs, and increased developmental
plasticity.
With delayed hatching and extended incubation, anamniotes can reproduce in
ephemeral aquatic habitats. Challenging terrestrial periods are endured in the more resistant, encapsulated egg form rather than
as freely swimming larvae. Delayed hatching permits reproduction in habitats that are
unsuitable for larvae or adults, allowing
multiple habitats or niche shifts over the life
cycle (Petranka and Petranka, 1981), or
multiple spawning sites with different microhabitat characteristics for the population
(Taylor and DiMichele, 1983). Alternatively, other anamniotes breeding in ephemeral
aquatic habitats may rely on rapid development, for example the desert toad Scaphiopus spends only twelve hours as an egg
(Zweifel, 1968), and the waterproof frog
Chiromantis proceeds from egg to tadpole
in three days (Seymour and Loveridge,
1994). Delayed hatching allows extended
incubation, extended use of unpredictable
habitats, and temporal separation between
adult and larval stages. In addition, larvae
from eggs that were laid in a previous season and hatch as soon as it rains will
emerge sooner than larvae from other species that just begin to breed following the
rains (Petranka, 1990).
Air exposure may be beneficial for anamniotic eggs. Air temperatures are generally warmer and oxygen availability greater
than in water (Seymour and Bradford,
1995; Seymour, 1999), possibly encouraging rapid development. Resistance to diffusion is less in air than water (Bradford,
1990; Woods, 1999). So long as desiccation
is avoided (Strathmann and Hess, 1999),
285
286
K. L. M. MARTIN
Darken et al, 1998). Oviposition site affects survival of Ambystoma opacum eggs
in epehmeral pond habitats; if too high they
freeze, and if too low they die if they hatch
and the pool dries up afterwards (Petranka
and Petranka, 1981). During a drought year,
only 20% of A. opacum nests survived
(Jackson et al, 1989).
An environmental cue for hatching is advantageous for terrestrially breeding anamniotes, however errors in initiating hatching
are potentially fatal. Anamniotic larvae
must be aquatic to feed and grow. Terrestrial tadpole larvae of the frog P. bibroni
are occasionally observed in the field (Geiser and Seymour, 1989), and may survive for
a few days under humid conditions, but
they die quickly if desiccated. Larvae from
terrestrial eggs of the tidally spawning fish
Mallotus villosus (Atherinidae) hatch out of
water in the absence of an environmental
trigger, upon reaching developmental readiness (Frank and Leggett, 1981). M. villosus
larvae stay within the pebble substrate for
several days until washed by waves out to
sea, but larval condition deteriorates with
time spent terrestrially (Frank and Leggett,
1981). These fish have less viability and resistance to the elements as larvae than they
had as eggs.
Future study
There are undoubtedly additional advantages to delayed hatching with extended incubation. Delayed hatching may stagger life
history stages across a season, or prolong
the life span by elongating the embryonic
period before entering the larval or juvenile
stages. It would be instructive to compare
larval growth and progression of development after different incubation durations in
anamniotes that delay hatching, and to examine the life history characteristics of their
natural populations.
Plasticity of embryonic development is
necessary for delayed hatching with extended incubation (Fig. 1). Comparisons with
other forms of embryonic plasticity, such as
predator-induced delayed hatching (Sih and
Moore, 1993) or predator-induced accelerated hatching (Warkentin, 1995), could be
useful in determining pathways or mechanisms for developmental heterochrony.
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In eggs of Galaxias maculatus, the yolk is
so large that larvae hatched out during the
primary incubation period do not need to
feed for two additional weeks (McDowall,
1968). Moreover, larger yolks may result in
smaller clutch sizes, although appropriate
comparisons have not been made.
More yolk means larger eggs. Larger
eggs have a reduced surface area in relation
to volume (Seymour and Bradford, 1995),
yet the egg surface must supply oxygen by
diffusion to the embryo. Larger egg size
has been correlated with terrestrial development in amphibian eggs (Bradford,
1990), perhaps enabled by the increased
diffusion rate of oxygen in air.
Terrestrial eggs are vulnerable to terrestrial conditions, including predators such as
invertebrates and birds that they would not
face in water (Walker, 1952; Tewksbury
and Conover, 1987; Jackson et al, 1989;
Warkentin, 1995). Vulnerability to predators is prolonged when incubation is extended, and fungal or other infections have
a longer time to infect and grow on eggs.
Parental care can reduce this vulnerability,
but at some cost to the guarding parent
(Jackson et al, 1989; Petranka, 1990). On
the other hand, aquatic predation clearly is
reduced while eggs remain terrestrial
(Walker, 1952; Warkentin, 1995).
Anamniotic eggs will die if desiccated,
however the consequences of less extreme
hydric conditions are not known. The risk
can be minimized by microhabitat selection
(Petranka and Petranka, 1981; Taylor and
DiMichele, 1983; Middaugh et al, 1983).
There seems to be little apparent effect of
water potential of the terrestrial substrate on
embryonic growth in frog eggs (Bradford
and Seymour, 1988), but in turtles, increased water potential results in larger
hatchlings (Packard, 1999). The jelly capsule around amphibian eggs may help
emerged eggs resist desiccation (Seymour,
1999, Marco and Blaustein, 1999).
Extending incubation too long increases
mortality. Egg survival declines over time
in grunion eggs, and there is decreased
hatching success (Darken et al, 1998).
Eggs usually do not hatch spontaneously,
and they do not survive after yolk reserves
are exhausted (Geiser and Seymour, 1989;
DELAYED HATCHING OF TERRESTRIAL EGGS
Certain anamniote taxa, for example the
Cyprinodontidae, Ambystomatidae, and
Myobatrachidae, contain multiple species
with the ability to delay hatching and extend incubation (Table 1). Phylogenetic analyses of each of these groups, mapping on
physiological, developmental, behavioral,
and life history traits, could begin to elucidate the evolutionary history of this intriguingly adaptable reproductive mode.
I am grateful to Dave Bradford, Rachel
Darken, Jim Petranka, Roger Seymour, Richard Strathmann, Malcolm Taylor, Paul
Verrell, and Boyd Walker for insightful discussions on the ideas in this manuscript.
Thanks to Gregory Martin for the art in
Figure 1. Financial support was provided
by the National Science Foundation, IBN
9727979 and DBI 9605062.
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