Download A Suite of Adaptations for Intertidal Spawning1

AMER. ZOOL., 39:313-320 (1999)
A Suite of Adaptations for Intertidal Spawning1
MALCOLM H. TAYLOR
2
Department of Biological Sciences University of Delaware, Newark, Delaware 19716
SYNOPSIS. Salt marshes and similar tide-dominated habitats present an unusual
challenge for reproduction of resident aquatic organisms. Strong currents, siltation
and hypoxia can potentially contribute to reproductive failure through mortality
of the eggs or flushing of the eggs and larvae from the habitat. Fundulus heteroclitus, a small brackish water killifish, is a common resident of tidal marshes along
the east coast of North America from Newfoundland to Florida. The reproductive
strategy of this and related species is based on aerial incubation of eggs in the high
intertidal zone. The eggs are resistant to desiccation and, when fully developed,
hatch on immersion. Copulatory behavior and anatomy of accessory reproductive
structures are adapted to placement of eggs in protected incubation sites. The
gonads of both males and females mature rhythmically with an endogenous circasemilunar period, which is synchronized with the "spring" tides of new and full
moons. Spawning occurs on high tides. Embryos develop in 9—15 days, and usually
hatch on the succeeding spring tide series. Reproductive cyclicity in F. heteroclitus
and related fishes ensures that spawning fish will have access to the high intertidal
zone, thereby permitting aerial incubation of eggs.
High intertidal spawning in fishes involves a complex reproductive strategy requiring adaptations in adults, eggs and larvae. The adults typically display reproductive cyclicity that ensures sexual maturity
at the times of most complete immersion of
the intertidal zone, when spawning sites are
accessible. In addition, eggs of intertidal
spawners are adapted to resist desiccation
and hatch only when immersed in water.
Larval development is completed and the
embryos are ready to hatch before a succeeding spring tide series inundates the
spawning sites. The fry are immediately
free-swimming and able to survive in tidemarsh and shore-zone environments.
Many high intertidal spawners belong to
the order Atheriniformes. The California
grunion, Leuresthes tenuis, (Walker, 1949,
1952) and the related Gulf of California
grunion, L. sardina, (Thomson and
Muench, 1976) spawn in the surf in the
high intertidal zone of sand beaches. The
Atlantic silverside, Menidia menidia, (Middaugh, 1981) deposits eggs in plants and
detritus mats at the high intertidal level in
brackish marshes. At least four species of
killifish of the genus Fundulus spawn in the
high intertidal of salt marshes or sand
beaches (Taylor, 1990). The related annual
killifishes of the tropics inhabit transient
surface pools rather than tidal waters, and
depend on desiccation-resistant eggs for
survival of their populations when surface
pools evaporate between rainy seasons
(Breder and Rosen, 1966). In addition to the
Atheriniformes, several salmonids (McDowall, 1968) and puffers (Uno, 1955)
spawn in the high intertidal zone.
Reproduction in the killifish Fundulus
heteroclitus provides an instructive model
system for description of the egg, larval and
adult adaptations associated with intertidal
spawning. F. heteroclitus, commonly
known as the mummichog, is the most
abundant resident fish in tidal marshes
along the east coast of North America. It
1
From the Symposium Aquatic Organisms, Terres- feeds preferentially on the marsh surface
trial Eggs: Early Development at the Water's Edge (Weisberg et al., 1981) and achieves a biopresented at the annual meeting of the Society for In- mass productivity which is among the hightegrative and Comparative Biology, 3-7 January 1998,
est reported for fish (Meredith and Lotrich,
at Boston, Massachusetts.
2
1979). The first suggestions of its complex
E-mail: [email protected]
313
314
MALCOLM H. TAYLOR
spawning strategy came from observations
on hatching in the laboratory (Oppenheimer, 1937; Milkman, 1954) and egg deposition sites (Able and Castagna, 1975; Taylor et al., 1977).
Tidal marshes present a significant challenge for reproduction of resident fish species: strong currents could flush pelagic
eggs from the marsh; siltation and low dissolved oxygen at night could prevent survival of inundated demersal eggs. Although
complex in terms of the supporting adaptations seen in F. heteroclitus, aerial incubation of eggs is an effective solution to
this challenge.
Throughout its range, F. heteroclitus deposits its eggs at the high water mark on
the exceptionally high spring tides associated with new and full moons. In southern
and mid-Atlantic marshes, eggs are deposited on, or near, the marsh surface along
creeks and man-made mosquito ditches
(Able and Castagna, 1975; Taylor et al.,
1977, 1979; Kneib and Stiven, 1978). Preferred spawning sites include the leaves at
the bases of the tall form of Spartina alterniflora and empty shells of the Atlantic
ribbed mussel {Geukensia demissa). The
eggs are approximately 2.0 mm in diameter
and are laid in multiple clutches which may
total several hundred or more in G. demissa
shells and usually less than 50 in S. alterniflora plants. The eggs are injected into the
narrow gapes of the shells and leaves
through an ovipositor which runs along the
anterior edge of the female's anal fin. The
males lack a similar specialization.
Northern populations (New England),
and populations in low salinity waters near
the fall-line (tidal-nontidal boundary) of estuaries use less protected spawning sites.
Their eggs are typically laid in algal mats
or buried in sand near the high water mark.
They are characterized by a dense covering
of long chorionic fibrils that attach the eggs
to the substrate or to each other (Brummett,
1966; Morin and Able, 1983). It is assumed
that these fibrils reduce desiccation, but this
has not been tested experimentally. Eggs
from the southern and mid-Atlantic populations have shorter fibrils (Morin and Able,
1983) that are less visible and less effective
in holding clutches together.
IN*
1.45
El
.5
125
52 i.O5 H
Ui
0.65
12
13
DAY OF DEVELOPMENT
FIG. 1. Experimental placement of groups of fertilized F. heteroclitus eggs in relation to tidal inundation in a Delaware salt marsh. Tide height is relative
to mean low water at Roosevelt Inlet (0.5 km from
study site). Hatching success of Groups 1-6 is described in the text. (Adapted from Taylor and DiMichele, 1983.)
The survival value of intertidal spawning
for F. heteroclitus was demonstrated by
placing fertilized eggs from the Delaware
Bay population in mussel shells positioned
at various heights on the wall of a tide
marsh ditch (Taylor and DiMichele, 1983).
Six groups of 40-50 eggs in mesh bags
were placed in shells at levels shown in
Figure 1. Groups 1 (continuous immersion)
and 2 (immersion by each flood tide) failed
to develop completely and eventually died.
Eggs placed near the high tide line (Groups
3-5) developed normally and hatched in 9
to 14 days as the high tide reached them.
Group 6, which was intended to be a negative control, hatched late on day 14 when
flooded by rain. In the natural habitat, such
larvae might not survive long enough to
find their way to open water. The height at
which successful hatching occurred
(Groups 3—5) corresponds to a band several
meters wide on the marsh surface. Spartina
alterniflora plants and empty mussel shells
were typically abundant in this area and the
eggs were above the level where hypoxic
water might reach them at low tide.
Placement of eggs in the high intertidal
zone depends on synchronization of spawning with high spring tides at new or full
moon. Male and female F. heteroclitus
have a semilunar gonadal cycle (Fig. 2)
which is in phase with the spring tide cycle
INTERTIDAL SPAWNING IN F.
5/29 6/12
6/27 7/11
7/27
DATE (1976)
8/9
8/25
FIG. 2. Spawning cycle of F. heteroclitus in a Delaware salt marsh. Each data point is the mean of 5—10
fish sampled on the night high tide. Gonadosomatic
index is gonad weight expressed as a percent of body
weight (bars are ± 1 S.E.M.). Percent "ripe" in each
sample was assessed by "stripping" fish with light
pressure. Filled circles represent "new" moon and
open circles "full" moon. (From Taylor et al., 1979).
(Taylor et al., 1979). Mature gametes are
produced primarily in the 5 days prior to a
spring tide. In females, a group of follicles
completes vitellogenesis, hydrates, and
ovulates in each cycle (Taylor and DiMichele, 1980; Hsiao et al, 1996). Spawning occurs primarily on the night high tides,
over several days centered on the highest
spring tide.
The spawning cycle is endogenous, continuing in the laboratory in the absence of
daily, tidal and lunar cues (Taylor, 1984).
However, a tidal or semilunar period entraining stimulus is apparently necessary,
since fish maintained in the laboratory
eventually lose their synchronization with
the natural spring tide cycle (Taylor, 1991).
HETEROCLITUS
315
The nature of this stimulus has not been
determined.
Success of intertidal spawning in fish depends on synchronization of hatching with
high tides. In F. heteroclitus, two mechanisms prevent hatching of eggs in air
(DiMichele and Taylor, 1980): 1) dissolved
oxygen levels above 6.0 ml/L inhibit hatching, and 2) reduced turgor pressure (cell
volume) prevents hatching regardless of oxygen availability.
The hatching mechanism is typical of teleosts, depending on release of an enzyme,
chorionase, from hatching gland cells. In F.
heteroclitus, these cells are located in the
buccal cavity and opercular epithelium.
They are fully developed at 10 days of age
in embryos maintained at 20°C. Release of
chorionase appears to be largely a mechanical process resulting from the buccal
movements initiated by reduction in available oxygen when the eggs are transferred
from air to water (DiMichele and Taylor,
1981). Although eggs with competent
hatching glands may be immersed on high
tides, hatching is not initiated until the embryos' oxygen consumption exceeds the
rate of uptake from the surrounding water
(DiMichele and Powers, 1984). Thus,
hatching is a "respiratory-stress" response,
and appears to be initiated by neural signals
from the "respiratory center" in the hindbrain (DiMichele and Taylor, 1981). Circulation of water past the egg can increase
oxygen availability and postpone hatching.
This apparently is a factor in aerated aquaria, but probably not in the natural habitat.
The eggs of Fundulus heteroclitus and
other semilunar spawners typically complete development over a single spring tide
cycle and are ready to hatch when rising
tides reach their incubation sites. Eggs of
the Delaware population incubated in their
natural habitat at ambient temperatures with
a day-night range of 25.5-18°C developed
in 9-12 days (Taylor and DiMichele, 1983).
DiMichele and Westerman (1997) summarized field observations on populations in
Massachusetts, Delaware and Georgia, indicating median hatching times of 10.5—
12.5 days for the two northern populations
and 14-15 days for the Georgia fish. Although the eggs of the Georgia fish were
316
MALCOLM H. TAYLOR
TABLE 1. Influence of incubation temperature on
hatching time of embryos from three populations of
Fundulus heteroclitus.
could contribute to differences in hatching
times exists in a number of physiological
parameters including metabolic rate (PaynMean hatching time* — (days)
Population
ter et al., 1991) enzyme activity (DiMichele
and Powers, 1991) and hemoglobin func15°C
tion (Powers et al, 1979).
Mass.
15.0 ± 1.3
Delaware
20.3 ± 2.2
It has been suggested (DiMichele and
Florida
died
Westerman, 1997) that the latitudinal vari20°C
ation in development times of F. heterocliMass.
10.5 ± 1.0
tus populations is attributable to genotypic
Delaware
15.7 ± 2.5
variation in enzymes which influence de20.2 ± 6.0
Florida
velopment rate. Mitton and Koehn (1975)
25°C
found 12 of 25 proteins isolated from F.
9.1 ± 1.0
Mass.
heteroclitus to be polymorphic. The majorDelaware
NA
ity of these are liver enzymes involved in
Florida
16.3 ± 3.0
energy metabolism, and several have been
30°C
found to vary latitudinally in allele freMass.
died
quency (Powers et al, 1991). Particular geDelaware
8.8 ± 1.0
notypes of lactate dehydrogenase-B, malate
Florida
13.0 ± 2.7
dehydrogenase-A and glucose phosphate* Mean ± SEM, NA = No data available. From
isomerase-B are correlated with differences
DiMichele and Westerman, 1997.
in development rate and temperature tolerance (DiMichele and Powers, 1991). Various combinations of alleles for these eninundated by high tides through day 17, it zymes could produce a latitudinal gradawas estimated that 7% of the embryos re- tion.
DiMichele and Westerman (1997) have
mained unhatched, and presumably viable.
These could conceivably have hatched on documented a genetic component to the latitudinal variation in development time. Rethe succeeding spring tide series.
The latitudinal difference in development ciprocal crosses of fish from the Massachutimes of F. heteroclitus populations com- setts and Florida populations were mainpensates for temperature differences over tained at 20°C. These fish developed at rates
the geographic range of the species. Di- which, while not significantly different
Michele and Westerman (1997) recorded from each other, were intermediate relative
hatching times for eggs from Massachu- to the Massachusetts and Florida populasetts, Delaware and Florida populations at tions, and statistically overlapping the Deltemperatures ranging from 15 to 30°C (Ta- aware population.
Although this reciprocal-cross experible 1). Eggs from the Massachusetts population reached the hatching stage more rap- ment indicates that there are genetic differidly at each temperature than did fish col- ences in F. heteroclitus populations at diflected in Delaware or Florida. Eggs from ferent latitudes, phenotypic variation within
fish collected in Massachusetts failed to sur- a single genotype could also be a contribvive at 30°C, and those from the Florida uting factor. This phenomenon, often repopulation died at 15°C. Although water ferred to as phenotypic plasticity (Via,
temperatures are variable within the habi- 1987), involves environmentally dependent
tats of these populations, temperatures are variability in the expression of one or more
approximately 8°C cooler during the genes in an organism. In the case of develspawning season in the northern habitats opment rate, which is presumably influenced by many enzymes as well as memthan in Florida.
Thus, each of the three populations ap- brane permeability and other processes, it is
pears to be adapted to the thermal regime easy to imagine temperature effects on exof its habitat such that hatching occurs in pression of individual genes leading to a
10-15 days. Latitudinal variation which graded change in development rate along a
INTERTIDAL SPAWNING IN F. HETEROCUTUS
latitudinal temperature gradient. Measurement of phenotypic plasticity requires comparison of the variation in a character, such
as development rate, in genetically identical
organisms exposed to a range of values for
the environmental parameter, in this case
temperature. In order to carry out such an
experiment with F. heteroclitus, it will be
necessary to use cloned individuals.
The population-specific relationship between development rate and temperature in
F. heteroclitus is presumably maintained by
natural selection. Eggs which reach the
hatching stage either before or after they are
inundated by high tides are vulnerable to
triggering of hatching by rainfall. Larvae
hatching under these conditions would, in
many cases, die as a result of predation or
desiccation before they were able to reach
tidal waters. Selection of hatching times is
complicated by variability in spawning relative to the day of spring tide. Thus, synchronization of hatching readiness with
spring tides would require a longer incubation time in eggs laid before the preceding spring tides than in eggs laid after the
spring tides.
Williamson and DiMichele (1997) used a
computer simulation to identify variables
that might influence hatching success, and
thereby select for optimal development
times. The tested variables included predation, false hatching cues {i.e., rainfall),
spawning time, and development rate.
Hatching was considered successful if,
based on tide height predictions, the eggs
were immersed when they completed development.
Results obtained by running this model
for 57 generations indicated that if spawning occurred on all days when the fish had
access to the area where eggs are normally
found, optimal hatching success was seen
in embryos which were ready to hatch after
10 days incubation. For the purposes of the
model, Williamson and DiMichele (1997)
defined "spring tide" as the period when
tides reached the level of the eggs in Group
3 of Figure 1, generally five days. Spawning throughout or in the latter half of the
spring tide series was more successful than
spawning in the first half of the series. Not
surprisingly, if spawning was limited to the
317
first half of the spring tide cycle, longer development times yielded greater survival.
Overall, 12-20% of embryos in the model
were not immersed on the succeeding
spring tide series, but these could have
hatched on a later series. Fully developed
embryos of F. heteroclitus (DiMichele and
Taylor, 1980) and F. confluentus (Harrington, 1959) have been shown to survive
more than 30 days of aerial incubation.
In conclusion, Fundulus heteroclitus exhibits a "suite" of adaptations which permit
survival in a tide-dominated environment.
Intertidal spawning is the focus of these adaptations which involve adults and developing embryos. The adults exhibit a semilunar gonadal cycle and egg deposition behavior, which are necessary to place the
eggs in protected sites in the high intertidal
zone. The eggs tolerate aerial incubation,
and the embryos develop at a rate which
brings them to the hatching stage as the
marsh is again flooded by spring high tides.
Hatching does not occur in air, but is triggered immediately upon immersion. Genetic variation has been shown to exist in development rates of F. heteroclitus embryos
(DiMichele and Powers, 1991; DiMichele
and Westerman, 1997) and may contribute
to selection for the other traits which are
important for success of intertidal spawning.
Although the gonadal cycle, larval development and hatching mechanism of F.
heteroclitus have been described, two questions stand out as topics for future research.
First, in spite of some experimental work
(Taylor, 1991), the entraining stimuli for the
semilunar reproductive cycle have not been
firmly established. Moonlight, tidal water
pressure or turbulence and the combination
of diurnal and tidal stimuli are potential
candidates. Identification of an entraining
agent by classical biological rhythm methodology is difficult because the number of
spawning cycles in a season is not sufficient
to document a phase shift caused by an entraining stimulus.
A second area for future work is the desiccation resistance of the eggs. Although
the eggs of F. heteroclitus and other high
intertidal spawners normally survive aerial
incubation without obvious desiccation,
318
MALCOLM H. TAYLOR
their resistance to dehydration has not been
compared experimentally to species whose
eggs incubate in water. It is assumed that
the structure of the chorion, including the
presence of fibrils, contributes to this adaptation, but the question has not been explored experimentally, and there are no
studies directly comparing the thickness
and structural detail of the egg membranes
of species exhibiting aerial and aquatic incubation.
The adaptations for high intertidal
spawning in species other than F. heteroclitus have received relatively little attention. In many cases, our knowledge is limited to descriptive observations of the timing and location of spawning. Some of this
information has been previously reviewed
(Taylor, 1984, 1990).
Available data on atherinid species are
consistent with the F. heteroclitus model.
Eggs of the California grunion, L. tenuis,
(Clark, 1925; Martin, 1999) and Atlantic
silverside, M. menidia (Middaugh, 1981)
incubate in air and hatch when immersed.
Development rates in the grunion are similar to those seen in F. heteroclitus, and the
eggs are capable of surviving in air for at
least two spring tide cycles (Darken et al.,
1998). The mechanism by which immersion
initiates hatching in the atherinidae has not
been investigated, but the hypoxia trigger
seen in F. heteroclitus could function in
these species as well.
The California grunion (Clark, 1925) and
the Atlantic silverside (Middaugh et al.,
1984) display peaks in production of mature oocytes consistent with a semilunar gonadal cycle. It is likely that other atherinids
which spawn on spring tides have semilunar gonadal cycles similar to that seen in F.
heteroclitus but a clear demonstration of
this point will require observations of gonadal maturity over several spawning cycles.
The ovarian cycle in Fundulus heteroclitus is endogenous, and limits production
of mature oocytes to a time period which
in the natural habitat coincides with the
spring tides. The grunion reproductive cycle has not been examined under controlled environmental conditions, but experiments on M. beryllina (Sherrill and
Middaugh, 1993) indicate that the semilunar spawning cycle in this species does
persist under non-tidal conditions in the
laboratory. Conover and Kynard (1984) reported nearly continuous spawning in
groups of M. menidia in the laboratory.
They concluded that the spawning periodicity in this species results from direct
responses to tide and light cycles, not entrainment of an endogenous gonadal cycle.
However, their laboratory observations
were based on groups of fish which did, in
fact, show an apparent semilunar periodicity in egg production, and single females,
with males, which in only one case of four
survived and spawned long enough to collect meaningful data. Endogenicity of the
atherinid semilunar spawning cycle is an
important question which could conceivably lead to significant generalizations
about the entrainment of such cycles.
Comparison of the known features of intertidal spawning in the atherinidae to the
adaptations which have been described for
F. heteroclitus supports commonality of
evolution of this system in the atheriniform
fishes. Data for other piscine groups which
include intertidal spawners are primarily
descriptive (see reviews by Taylor 1984,
1990). Several salmonids, osmerids and tetraodontids spawn on spring tides leaving
eggs to incubate in air. Development typically takes about 10 days and would permit
hatching on the following spring tide series.
The reproductive strategies of these fishes
are a potentially fruitful area of research
which could significantly expand our understanding of high intertidal spawning as
an adaption to tide marsh and shore-zone
habitats.
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Corresponding Editor: Paul Verrell