Download Brave New Propagules: Terrestrial Embryos in Anamniotic Eggs

Integrative and Comparative Biology
Integrative and Comparative Biology, volume 53, number 2, pp. 233–247
doi:10.1093/icb/ict018
Society for Integrative and Comparative Biology
SYMPOSIUM
Brave New Propagules: Terrestrial Embryos in Anamniotic Eggs
K. L. Martin1,* and A. L. Carter†,‡
*Department of Biology, Pepperdine University, 24255 Pacific Coast Highway, Malibu, CA 90263, USA; †Charleston
Southern University, South Carolina, USA; ‡Department of Biological Science, California State University, Fullerton,
CA 92831, USA
From the symposium ‘‘Vertebrate Land Invasions – Past, Present, and Future’’ presented at the annual meeting of the
Society for Integrative and Comparative Biology, January 3–7, 2013 at San Francisco, California.
1
E-mail: [email protected]
Synopsis A surprisingly large number of fish and amphibian species reproduce terrestrially despite the absence of the key
evolutionary innovation of the amniotic egg. In contrast with shelled eggs of reptiles and birds, eggs of teleost fish and
amphibians are typically much smaller and enclosed in relatively simple chorionic membranes. Incubation times may be
brief or prolonged, and resultant hatchlings typically require the return to an aquatic habitat. Advantages of terrestrial
incubation include the increased availability of warmer temperatures and avoidance of aquatic hypoxia, whereas disadvantages include desiccation, exposure to novel predators, and the risk of hatching into a hostile habitat. Hatching may
be environmentally cued. Use of energy in the yolk may require trade-offs between growth of the embryo and extended
incubation, as exemplified by a case study of the California Grunion. The physical challenges of terrestrial incubation,
constraints for hatching, effects of egg size, and parental care are explored. Eight different types of early life history
among anamniotic embryos incubating in a terrestrial environment are identified, with examples of these alternate routes
to the invasion of land by vertebrates.
Introduction
Successful nesting and early development out of
water for small, relatively naked eggs of fish and
amphibians provide numerous alternate routes to
vertebrates’ invasion of the land, even if only for a
portion of their life cycles. Species within many lineages of teleost fishes and amphibians place their
eggs terrestrially, despite living aquatically as larvae
or adults and despite lacking the key evolutionary
innovation of the amniotic egg (Thibaudeau and
Altig 1999; Martin et al. 2004). The potential advantages to the embyros, the most vulnerable life stage,
must outweigh the very real threats to the parents
that may temporarily invade a new and difficult habitat to spawn and in some cases provide extended
parental care. This article explores some commonalities and distinctions between different types of terrestrial incubation and early development for teleost
fishes and amphibians.
The anamniotic egg that contains an embryo of a
fish or an amphibian is typically much smaller than the
amniotic egg of a bird or reptile and is more dependent
on environmental conditions than are shelled eggs,
enclosed as they are in relatively simple membranes
of the chorion (Yamagami 1988). Challenges of incubating an anamniotic embryo in a terrestrial environment include desiccation, exposure to novel predators
and pathogens, and the risk of aquatic larvae hatching
into a hostile terrestrial habitat (Middaugh et al. 1983;
Geiser and Seymour 1989). In many cases, embryos
assess and respond to risks during terrestrial incubation, and hatching may be environmentally cued
(Martin et al. 2011a; Warkentin 2011).
Advantages of terrestrial incubation for anamniotic eggs include the potential for more rapid development, with higher temperatures and higher oxygen
levels (Tewksbury and Conover 1987; Martin and
Strathmann 1999; Smyder and Martin 2002).
Diffusion of oxygen is more rapid in air than in
water, thereby avoiding aquatic hypoxia or stagnant
boundary layers (Seymour and Bradford 1995; Marco
and Blaustein 1998; Strathmann and Hess 1999).
Although terrestrial incubation of eggs occurs in
many teleost and amphibian lineages, this does not
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234
indicate shared common ancestry. Instead this lifehistory strategy has repeatedly arisen independently
between and within lineages from different ancestral
states (Martin and Swiderski 2001). It is likely that
different selection pressures are involved in initiating
terrestrial incubation of eggs from anamniotes in different habitats, but all must cope with some of the
same challenges when out of water.
Physical challenges of terrestrial
incubation for anamniotes
The chorion, an extra-embryonic membrane
composed of several proteins, encloses the anamniotic embryo during incubation. After fertilization, the
chorion of anamniotes undergoes a change in the
proteins and a release of the contents of the egg’s
cortical granules that bind to the vitelline envelope,
called hardening (Masuda et al. 1991; Yamagami
et al. 1992). This helps protect the egg against
entry of many foreign substances, including pathogens, and slows water loss. If eggs become too dry,
embryos may become deformed (Mitchell 2002). For
anamniotes that nest terrestrially, parental care often
involves attention to the hydration of the eggs
(Taigen et al. 1984; Caldwell and deOliveira 1999).
Dehydrated eggs may die or hatch early (Touchon
and Warkentin 2010). Salinity changes of the incubation medium can also produce osmotic challenges
that are detrimental to embryonic development
(Matsumoto and Martin 2008).
When incubated out of water, chorions of the
mummichog Fundulus heteroclitus and mangrove killifish Kryptolebias marmoratus have reduced numbers
of aquaporin channels (Tingaud-Sequiera et al. 2009;
Wright 2012) that lessen evaporative water loss. The
annual killifish Austrofundulus limnaeus develops
amyloid fibers in the egg envelope that help it survive dehydration (Podrabsky et al. 2001). The shape
of the egg mass also influences evaporation rates
(Strathmann and Hess 1999; Altig and McDiarmid
2010).
Some of these protections against desiccation also
help shelter against sudden or extreme changes in
temperature. Even when in air, if the eggs are
shaded under a boulder, in a burrow, or buried in
damp sand, the microhabitat retains high humidity
and resists temperature changes while allowing
higher temperatures than in water. A higher temperature on land than in water may extend the spawning season by starting it earlier and possibly increase
the rate of development and the chances of survival
to hatching. On beaches, changing the amount of
shade or the color of the sand can alternatively
K. L. Martin and A. L. Carter
negatively affect this essential habitat, reducing embryos’ survival by increasing temperatures above
lethal levels or altering sex ratios (Matsuzawa et al.
2002; Rice 2006).
Terrestrial incubation by teleosts occurs in the tropics, for example, mudskippers Periophthalmus modestus and Periophthalmodon schlosseri (Ishimatsu and
Graham 2011), K. marmoratus (Taylor 2012); temperate zone, for example, grunion Leuresthes tenuis
(Walker 1952), stichaeids, and clingfishes (Coleman
1992, 1999); and the arctic, for example, capelin
Mallotus villosus (Frank and Leggett 1981) and sand
lance Ammodytes hexapterus (Robards et al. 1999).
Among amphibians, terrestrial incubation occurs primarily in the tropics, but temperate examples include
Ambystoma opacum (Petranka et al. 1982), Ambystoma
gracilis (Marco and Blaustein 1998), and Amphiuma
means (Gunzburger 2003), as well as the anuran
Leiopelma archeyi in New Zealand (Thurley and Bell
1994). Climatic change may have more rapid and deleterious effects on teleost species that spawn out of
water than on those that are fully aquatic, because in
water, temperatures change more slowly than in air
(Truchot and Duhamel-Jouve 1980).
Deleterious impacts of ultraviolet radiation on
eggs and developing embryos have been shown for
some aquatic amphibian eggs (Blaustein et al. 1994).
However, this has not been examined for the terrestrial eggs of any species of teleost or amphibian. This
research opportunity should be pursued, although
most terrestrial clutches are shaded to some extent.
Examples of teleosts and amphibians
that incubate terrestrially
Teleosts from many lineages produce eggs that incubate while emergent from water; some examples are
shown in Table 1. All marine teleosts that incubate
their clutches out of water spawn in the intertidal
zone or estuaries (Taylor 1984; DeMartini 1999;
Martin et al. 2004) with the predictable ebb and
flood of the semilunar tidal cycle. Spawning typically
occurs in water during high tides, while emergence
of eggs occurs passively during ebb tides. Tidal
flooding facilitates the entry of larvae into water
after they hatch. Very few freshwater teleosts incubate eggs terrestrially (Breder and Rosen 1966; Abel
et al. 1987; Podrabsky et al. 2010).
Many amphibian species produce eggs that incubate terrestrially (Table 2) by spawning in sheltered
terrestrial locations (Bradford and Seymour 1985),
producing foam nests on land (Taigen et al. 1984;
Callery et al. 2001), nesting in vegetation, or placing
clutches at the water’s edge before a seasonal
235
Terrestrial embryos in anamniotic eggs
Table 1 Some example species of telost fishes that incubate eggs terrestrially
Family
Genus, species
Clutch location
Reference
Ammodytidae
Ammodytes hexapterus
Gravel beaches, spawned at high tide, eggs
exposed to air tidally
Robards et al. (1999)
Atherinopsidae
Leuresthes tenuis
Intertidal beach sand, eggs incubate completely
terrestrially
Walker (1952)
Leuresthes sardina
Intertidal beach sand, eggs incubate completely
terrestrially
Moffatt and Thomson (1978)
Menidia menidia
Seagrass beds, tidal exposure of eggs
Middaugh (1981)
Batrachoididae
Porichthys notatus
Intertidal, eggs attached to lower surface
of boulders
Crane (1981)
Blenniidae
Alticus kirkii
Rocky intertidal, supralittoral zone
Zander et al. (1999)
Cottidae
Clinocottus acuticeps
Under intertidal vegetation, eggs exposed
to air tidally
Marliave (1981)
Fundulidae
Aidinia xenica
Estuarine, eggs exposed tidally to air
Greeley (1984)
Fundulus heteroclitus
Estuarine, in shells or on vegetation
Taylor (1999)
Fundulus grandis
Estuarine
Greeley and MacGregor (1983)
Fundulus similis
Estuarine
Greeley et al. (1986)
Galaxiidae
Galaxias maculatus
River mouth following anadromous run
McDowell and Charteris (2006)
Gasterosteidae
Gasterosteus aculeatus
Rocky intertidal, broadcast but males distribute
over vegetation
MacDonald et al. (1995)
Gobiesocidae
Gobiesox maeandricus
Intertidal, eggs attached to lower surface of
boulders
Coleman (1999)
Gobiidae
Periophthalmus modestus
Mud burrow with air chamber
Ishimatsu and Graham (2011)
Periophthalmodon schlosseri
Mud burrow with air chamber
Ishimatsu and Graham (2011)
Lebiasinidae
Copella arnoldi
Vegetation above streams, males splash the
clutch throughout incubation
Krekorian (1976)
Nothobranchiidae
Nothobranchius (several spp)
Vernal ponds
Podrabsky et al. (2010)
Osmeridae
Hypomesus pretiosus
Gravel beaches, intertidal
Rice (2006)
Mallotus villosus
Gravel beaches, also some subtidal spawning
Frank and Leggett (1981)
Austrofundulus limnaeus
Vernal ponds, embryos survive drought by
diapause
Podrabsky et al. (2010)
Kryptolebias marmoratus
Estuarine, intertidal, populations also in fresh water
Abel et al. (1987) and Taylor (2012)
Anoplarchus purpurescens
Intertidal, parental care in space below boulders
Coleman (1992)
Xiphister atropurpureus
Intertidal, parental care in space below boulders
Marliave and DeMartini (1977)
Takifugu niphobles
Gravel beach intertidal, eggs are broadcast
Yamahira (1996)
Rivulidae
Stichaeidae
Tetraodontidae
This table is intended to show some of the variations in terrestrial nesting and is not a comprehensive list. Taxonomy for species names and
families is according to Froese and Pauly (2013).
drought, so that as the pond dries, the eggs are
exposed to air (Petranka et al. 1982; Marco and
Blaustein 1998; Gunzburger 2003). Table 2 gives
diverse examples from several families but is not
intended to be a comprehensive list.
Ecological context
Few teleost species inhabiting freshwater habitats
have eggs that incubate out of water. The tropical
Copella arnoldi (Lebiasinidae) spawns with a
tandem leap from water to an overhanging leaf,
with both partners providing gametes during an athletic mating event (Breder and Rosen 1966). In captivity, both parents leap up to attach a clutch to an
aquarium glass wall above the water line. Its
common name, the Splash Tetra, comes from the
male’s parental care; he splashes the exposed clutch
with a tail-flip every few minutes throughout its
3-day incubation period, thereby preventing desiccation (Krekorian 1976). Another freshwater teleost,
Brycon petrosus, has been observed out of water in
Panama moving between aquatic habitats, ripe and
full of gametes, but no actual terrestrial clutches have
236
K. L. Martin and A. L. Carter
Table 2 Some example species of Amphibia that incubate eggs terrestrially
Family
Genus, species
Clutch location
Reference
Alytidae
Alytes obstetricans
Eggs incubate in strings wrapped around parent’s legs,
larvae may hibernate
Summers et al. (2006a)
Dendrobatidae
Colostethus mertensi
Terrestrial foam nests near streams, males transport
hatchlings to water
Junca et al. (1994)
Oophaga pumilio
Terrestrial eggs, male hydrates with urine, female
carries tadpoles to water
Caldwell and deOliveira (1999)
Limnonectes arathooni
Eggs laid and hatch on land, male parental care,
tadpoles tumble into pools
Brown and Iskander (2000)
Few large terrestrial eggs, direct development
Callery et al. (2001)
Anurans
Dicroglossidae
Eleutherodactylidae Eleutherodactylus coqui
Hemiphractidae
Cryptobatrachus boulengeri Terrestrial, direct development, female carries on back
Summers et al. (2006a)
Stefania evansi
Direct development on mother’s back
Wassersug and Duellman (2005)
Fritziana goeldi
Marsupial frogs, pouch
Hemisotidae
Hemisus marmoratus
Terrestrial in burrows, covered with infertile eggs,
direct development
Kaminsky et al. (1999)
Hylidae
Agalychnis callidryas
Eggs laid on tree leaves above pools
Warkentin (2011)
Dendropsophus ebraccatus
On vegetation, tree leaves
Touchon and Warkentin (2010)
Gastrotheca guentheri
Terrestrial, eggs carried on female back
Wassersug and Duellman (2005)
Leiopelmatidae
Leiopelma archeyi
Terrestrial in moist areas under logs, direct development
Thurley and Bell (1994)
Limnodynastidae
Philoria sphagnicolus
Terrestrial, direct development
Seymour et al. (1995)
Microhylidae
Oreophryne oviprotector
Terrestrial breeding, male guards eggs
Gunther et al. (2012)
Hylophorbus rufescens
Terrestrial
Bickford (2004)
Arenophryne rotunda
Moist sand, direct development
Roberts (1984)
Crinia nimbus
Moss, moist vegetation
Mitchell and Seymour (2000)
Geocrinia Victoriana
Terrestrial eggs laid on grass or leaf litter, hatch
when area floods
Martin and Cooper (1972)
Geocrinia vitellina
Terrestrial, direct development
Mitchell (2001)
Kyarranus loveridgei
Terrestrial, direct development
Seymour et al. (1995)
Pseudophryne australis
Terrestrial eggs, constitutive hatch, rainfall releases
eggs into pools
Thumm and Mahoney (2002)
Pseudophryne bibroni
Pond edges, environmentally cued hatch
Bradford and Seymour (1985)
Rhacophorus malabaricus
Foam nests in trees by ponds, tadpoles drop into water
Kadadevaru and Kanamadi (2000)
Chiromantis xerampelina
Arboreal foam nests
Seymour and Loveridge (1994)
Ambystoma opacum
Pond edges that may dry
Petranka and Petranka (1981)
Ambystoma cingulatum
Mats of vegetation, bare soil
Anderson and Williamson (1976)
Ambystoma gracile
Pond edges that may dry
Marco and Blaustein (1998)
Myobatrachidae
Rhacophoridae
Urodeles
Ambystomatidae
Ambystoma maculatum
Pond edges that may dry
Petranka et al. (1982)
Amphiumidae
Amphiuma means
Pond edges, development may bypass larval stage
Gunzburger (2003)
Plethodontidae
Bolitoglossa rostrata
Terrestrial in burrows or cavities, direct development
Houck (1977)
Plethodon cinereus
Terrestrial in leaf litter, rotting logs, or cavities
Tornik (2010)
This table is intended to show some of the variations in terrestrial nesting and is not a comprehensive list. Amphibiaweb.org was used for
species names and families.
yet been identified (Kramer 1978). Clutches of K.
marmoratus have been observed developing out of
water (Abel et al. 1987). This waterfall-climbing
fish can live in estuarine or freshwater conditions
and is known to make terrestrial excursions when
moving from one pond to another. Adult K. marmoratus can survive out of water for weeks (Wright
2012). The annual killifishes of South America and
Terrestrial embryos in anamniotic eggs
Africa (genera Austrofundulus, Aphyosemion, and
Nothobranchius) also produce clutches in ponds
that evaporate, placing them out of water for part
of their development (Podrabsky et al. 2010).
Undoubtedly other examples await discovery.
Estuarine teleosts that spawn aquatically at high
tide and oviposit in sites that strand the eggs
during development include the mummichog,
Fundulus heteroclitus, that spawns on vegetation or
in empty mollusk shells (Taylor et al. 1977). The
Atlantic Silverside Menidia menidia spawns in water
over surfgrass beds, and the eggs are exposed to air
during daily low tides (Middaugh 1981). This may
be the case for estuarine populations of K. marmoratus, although spawning has not yet been observed in
the wild (Taylor 2012).
Some species of teleost live subtidally and migrate
to the intertidal zone solely to spawn during high
tides (DeMartini 1999). Most do not emerge from
water, or emerge only briefly while spawning, and an
ability to breath air is not necessary (Martin et al.
2004). Mallotus villosus visit gravel beaches to spawn
in Canada, Iceland, and Alaska (Frank and Leggett
1981). Fugu puffers, Takifugu niphobles, spawn high
in the intertidal zone on gravel beaches in Japan,
occasionally accidentally emerging onto shore
during a flurry of activity (Yamahira 1996). These
species broadcast their eggs without burial, but
their eggs may adhere to rocks and tumble into crevices that shade them and reduce rates of desiccation.
A population of white stickleback, Gasterosteus aculeatus, spawns on rocky beaches in Canada in a
manner that apparently began only recently
(MacDonald et al. 1995). Although these eggs are
not guarded by a parent, the male distributes them
among vegetation. Many embryos do not survive in
this harsh environment (Frank and Leggett 1981;
Yamahira 1996), but some do.
An exception to this type of exposure of eggs to
air by low tides is seen among the tropical mudskippers (Gobiidae, Oxudercinae). These amphibious
species, highly active out of water on mudflats that
are exposed to air during low tides, spawn within
water-filled burrows (Ishimatsu et al. 2009). The
eggs are attached to the ceiling of a chamber that
is then filled with air by a parent. The parent
swims to the burrow opening, takes a gulp of air
into the buccal chamber that is created by sealing
the operculae, then returns to the burrow to expel
its air into the chamber. This is repeated until the
clutch is completely surrounded by air (Ishimatsu
et al. 2007). Although the water within and surrounding the mud burrow may be quite hypoxic,
the partial pressure of oxygen (pO2) in the air
237
surrounding the eggs is much greater and may be
refreshed by guarding parents during the few days
of incubation.
For amphibians, incubation time is typically weeks
or months, much longer than the few days that most
teleosts need (Pauly and Pullin 1988), and seasonal
drought can expose aquatic eggs to terrestrial conditions. Eggs in clutches from amphibians often are
surrounded by gel layers that are not found around
teleost clutches. Larval life may await the return of
rainfall (Bradford and Seymour 1985), but one
advantage of terrestrial development may be that
some of the most terrestrial amphibians can incubate
eggs on land and bypass the larval stage completely
by hatching directly as froglets, that is, ‘‘direct development,’’ although Leptodactylus labyrinthicus and
other species may also nest aquatically, and larvae
may vary the time they spend in the nest (Shepard
and Caldwell 2005). Development may progress
slowly if incubation is extended in the absence of
the cue to hatch for terrestrial embryos of
Pseudophryne bibronii (Bradford and Seymour 1985;
Bradford 1990) and Amphiuma means (Gunzburger
2003).
Parental care and invasion of the land
Choice of oviposition site is one form of parental
care that may minimize exposure to the disadvantages of terrestrial incubation for anamniotic eggs.
However, placing the developing embryos of fish or
amphibians out of water may make other forms of
parental care both more difficult and more necessary
(Shine 1978; Thibaudeau and Altig 1999; Summers
et al. 2006a). Many teleosts that spawn on beaches
protect their clutches from desiccation by ovipositing
in sheltered locations, including under boulders
such as the midshipman Porichthys notatus,
clingfish Gobiesox maeandricus, and some stichaeids
(Coleman 1999), or in shells or vegetation, like M.
menidia (Middaugh 1981) or F. heteroclitus (Taylor
1999). Species of grunion, L. tenuis and Leuresthes
sardina, dig into the sand to bury clutches in this
moist, well-drained substrate (Walker 1952; Moffatt
and Thomson 1978). Osmerids including the surf
smelt Hypomesus pretiosus and M. villosus may
scratch a shallow nest in gravel that probably provides at least a little protection of the clutch from
desiccation (Frank and Leggett 1981).
The ‘‘safe harbor’’ hypothesis suggests that if the
egg stage has high survivorship, this may be enhanced by parental care during incubation, leading
to selection for longer duration of incubation, and
additional development, with less time in later stages
238
that might have lower survivorship (Shine 1978).
Parental care reduces the risk of predation to the
embryos (Tornik 2010) and provides some protection against desiccation and changes in temperature
(Taigen et al. 1984; Sargent et al. 1987; Summers
et al. 2006a). Care may be continuous, by guarding
the eggs, or as for C. arnoldi, by splashing them
throughout incubation (Krekorian and Dunham
1972). For amphibians, parental care is rarely seen
in species with aquatic nests but frequently seen in
species with terrestrial nests (Bickford 2004;
Summers et al. 2006a).
Most species of teleosts that guard nests in the
intertidal zone are intertidal residents that remain
even as tides ebb (Coleman 1999), whether or not
eggs are present. Many temperate fishes that are residents of tidepools, including stichaeids, sculpins,
and clingfishes, are quite tolerant of amphibious
emersion during low tides (Graham 1997; Martin
and Bridges 1999; Martin 2013), but they typically
are relatively inactive out of water. Because these
adults are in the same habitat, whether or not they
are guarding, it is unlikely that the parents suffer an
increased risk of predation, although this has not
been tested.
Two subtidal teleost species remain in the intertidal zone to guard clutches. The sharpnose sculpin,
Clinocottus acuticeps (Cottidae), guards submerged
eggs during high tides, but the parent usually
swims into subtidal water during low tides
(Marliave 1981). The usually subtidal P. notatus
(Batrachoididae) moves into the intertidal zone in
summer to spawn under rocks, and males remain
with the embryos even after they hatch (Crane
1981). Sheltered in a chamber beneath a boulder
that contains a shallow pool of water, male P. notatus
can exchange oxygen and carbon dioxide in air for
extended periods of time (Martin 1993), but do not
emerge from water or breathe air at any other time
in their life cycle.
Some eggs are broadcast onto gravel or cobble
beaches without further parental attention or
burial, as in T. niphobles (Yamahira 1996) and
M. villosus (Frank and Leggett 1981). These species
spawn in temperate habitats where rainy, cloudy,
cool conditions prevail and may slow embryos’ metabolism and reduce the need for resistance to desiccation. In addition, these adherent eggs frequently
may be tidally submerged during incubation, thereby
replenishing stores of water previously lost during
periods of exposure to air.
Among amphibians, parents may provide hydration for terrestrial nests (Taigen et al. 1984; Caldwell
and deOliveira 1999), guard the progeny (Gunther
K. L. Martin and A. L. Carter
et al. 2012), incubate the eggs on the parent’s back
or legs (Wassersug and Duellman 2005; Summers
et al. 2006a), and/or transport tadpoles from terrestrial nests to water (Crump 1996; Caldwell and
deOliveira 1999). Guarding parents adjust hydration
of the eggs to the weather conditions (Delia et al.
2013).
Initiation of hatching after terrestrial
incubation
Although many species of teleosts and amphibians
spawn in places where eggs are exposed to air,
their larvae may require an aquatic habitat upon
hatching. In some cases, eggs are deposited on vegetation overhanging water, and tadpoles drop into
the water upon hatching, for example, the tree frog
Agalychnis callidryas (Warkentin 2011) and the gliding frog Rhacophorus malabaricus (Kadadevaru and
Kanamadi 2000).
To prevent emergence of delicate aquatic larvae
into the harsh, unsuitable terrestrial environment,
many anamniotic species that breed terrestrially
have environmentally cued hatching (ECH) (Martin
et al. 2011a; Warkentin 2011). In combination with
temperature, the duration of development may determine the date when hatching competence is
attained (Smyder and Martin 2002), but not actual
date of hatching.
Environmental cues allow synchronization of the
hatch. Hatching for terrestrial anamniotes typically
requires the appropriate level of development, submergence in water, and an additional environmental
cue (Martin et al. 2011a; Warkentin 2011). This cue
may be decreased oxygen levels, formed by boundary
layers as the eggs are submerged, as in F. heteroclitus
(DiMichele and Taylor 1981) and A. opacum
(Petranka et al. 1982). In mudskippers P. modestus
and Pn. schlosseri, hatching is triggered by the parent
removing air from the brooding chamber by mouthfuls, submerging the eggs in hypoxic water by reversing the earlier process (Ishimatsu et al. 2007), and
allowing the hatchlings to swim freely out into open
water.
Other ECH triggers include mechanical agitation
of seawater caused by surf waves, for example, in
L. tenuis (Griem and Martin 2000), and disturbance
by snakes or wasps for A. callidryas (Warkentin
2011). Predators have been shown to trigger early
hatching in many amphibians incubating either in
air or in water (Warkentin 2011). Early hatching
has not been shown in any teleosts with terrestrial
eggs to date, although in water, fathead minnows
hatch early in the presence of crayfish (Kusch and
Terrestrial embryos in anamniotic eggs
Chivers 2004) and whitefish eggs in water hatch early
in the presence of disease (Wedekind 2002).
Some eggs, for example, M. villosus, show constitutive hatching, requiring neither submergence nor
an environmental cue to hatch (Frank and Leggett
1981). The tiny fragile embryos hatch in the interstices of gravel beaches when they are competent to
hatch and may find small pockets of water or be
stranded out of water completely. They suffer high
mortality until are released to the ocean by wind
waves, which are not as predictably timed as tides
(Frank and Leggett 1981). Terrestrial hatching occasionally occurs during extended incubation for the
frog Pseudophryne bibroni; those larvae survive briefly
but succumb to desiccation if rainfall does not occur
soon enough (Geiser and Seymour 1989).
Egg size and terrestrial incubation
Larger eggs may allow embryos to incubate longer
and progress to a later stage of development before
hatching (Shine 1978; Balon 1984; Pauly and Pullin
1988). Terrestrial eggs of teleosts are generally large
and demersal, as is typical among (e.g.) atherinids,
cottids, and killifish (Parenti 1981). Provisioning of
yolk is the major influence on the size of eggs, but
many environmental variables also play a role (Shine
1989; Chambers 1997; Johnston and Leggett 2002;
Summers et al. 2006b). Egg size is positively correlated with offspring size (Smith and Fretwell 1974),
duration of developmental time to hatching (Pauly
and Pullin 1988), maternal size (Einum and Fleming
2002), habitat quality (Reznick and Yang 1993),
availability of oxygen (Einum et al. 2002), seasonal
duration of spawning (Bagenal 1971), geographic location (Marteinsdottir and Able 1988; Chambers
1997; Martin et al. 2009), and parental care (Shine
1978; Sargent et al. 1987; Summers et al. 2006a).
Amphibian eggs in general are much larger than
teleost eggs. Within Amphibia, parental care correlates with larger eggs (Shine 1978, 1989; Nussbaum
and Schultz 1989; Crump 1996), and among amphibians, parental care and larger eggs are almost
always associated with nesting on land or in places
where eggs may emerge into air during development
(Summers et al. 2006a). However, not all amphibians
that incubate eggs terrestrially provide parental care.
Although many different environmental variables
were tested for correlation with egg size in amphibians, Summers et al. (2006b) did not find any significant association between egg size and temporary
habitats or environmental dryness. Bradford (1990)
found that, for all studied amphibians, duration of
incubation and rate of development both scale to
239
ovum volume, but protraction of development by
delayed hatching, as in P. bibronii, was not significantly related to ovum volume or to temperature.
However, endotrophy, the ability to metamorphose
without feeding, requires a minimum size even in
water (Doughty 2002), suggesting that larger egg
size provides opportunities for developmental plasticity (Bernardo 1996). The largest amphibian eggs
are those that incubate fully in air and bypass larval
life completely (Doughty 2002), even though the
froglets they produce may be quite small.
Maternal provisioning of eggs plays a major role
in survival of embryos and subsequent size of hatchlings (Sinervo 1990; Bernardo 1996), duration of incubation (Pauly and Pullin 1988), or both. In many
species of fish, egg size varies considerably among
individuals (Iguchi and Yamaguchi 1994). Increased
egg size should increase the potential for survival,
independent of the size of adults (Duarte and
Alcaraz 1989; Hendry and Day 2003).
Case study: egg size in Leuresthes tenuis
In the intertidal zone, the intermittent ebb and flow
of water has led to synchronization of both spawning
and hatching to semilunar high tides for many species. One of the most extreme examples of intertidal
spawning with ECH is the California Grunion,
L. tenuis (Walker 1952). This species lives subtidally
but surfs onshore in waves at the time of semilunar
tides, dropping out of the waves onto sandy beaches
to spawn (Walker 1952; Moffatt and Thomson
1978). The females dig tail-first into the soft, fluid
sand and bury the eggs while the males provide milt.
Adults are out of water only a few minutes during
spawning, but the buried embryos incubate completely out of water in damp sand (Darken et al. 1998;
Martin et al. 2009). Nearly 2 weeks later, wave action
during the rising semilunar tides frees the eggs from
the sand and triggers hatching (Griem and Martin
2000).
Provisioning these terrestrial eggs with yolk
prepares them for potential delay of the hatch in
the absence of environmental cues (Martin et al.
2011b). Leuresthes tenuis provision eggs with lipids
and protein for embryonic growth and development
to the point of hatching competence. The eggs also
provide energy for extended incubation that may
continue for many days after that time. Embryos
are competent to hatch within 10 days post-fertilization (dpf) at 208C but, unless triggered to hatch,
these embryos can survive enclosed in the egg
through as much as two additional high tides
(Smyder and Martin 2002), more than three times
240
as long as necessary to reach hatching competence
(Darken et al. 1998; Moravek and Martin 2011).
If not triggered to hatch, embryos of L. tenuis stop
growing but remain metabolically active and alert
(Darken et al. 1998). The length of the embryo, pectoral fin length, and diameter of the eye do not
change between achievement of hatching competence
and hatching, even if these are separated by weeks
(Moravek and Martin 2011). Most development is
arrested except that the otoliths continue to accrue,
melanophores become increasingly pigmented, and
marginal teeth develop (Moravek and Martin
2011). Continuously using up yolk with no decrease
in oxygen consumption, they are able to hatch
within seconds of receiving the cue to do so
(Speer-Blank and Martin 2004; Martin et al.
2011a). Upon hatching, the larvae feed immediately
and grow rapidly (May 1971), at the same rate
whether hatched early or late (Martin et al. 2011b).
One could hypothesize larger eggs for those species that can delay hatching, than for closely related
species that do not delay hatching. The congener of
L. tenuis, the Gulf Grunion L. sardina, lives in the
Gulf of California and spawns in a similar manner
on shore. Leuresthes sardina has significantly smaller
eggs, 1.25 mm (Moffatt and Thomson 1978) yet a
larger adult body size than L. tenuis. Moffatt and
Thomson (1978) hypothesized that the reason
L. tenuis has larger eggs than L. sardina is because
L. tenuis is more likely to need to extend the duration of incubation, because tidal height is more variable between semilunar tides of new and full moons
on the outer coast of California than within the Gulf
of California where L. sardina lives. Still the ability of
L. sardina to extend incubation and delay hatching
has not been tested.
To examine the relationship of egg size to potential duration of extended incubation within L. tenuis,
eggs were collected in Malibu, California, during two
different spawning runs. In May 2011, 12 partial
clutches were collected from beach sand following a
spawning run. In June 2011, 10 adult female fish
were captured by hand during the spawning run
and stripped of their gametes for in vitro fertilization
by multiple males. These females were measured for
total length and mass and then released. For each,
clutch size was measured by volume in milliliter.
Embryos from both the May and June runs
(N ¼ 22 clutches) were cultured in the laboratory according to the method of Smyder and Martin (2002).
From each clutch, 10 eggs were measured for diameter and lipid sphere 4 dpf, when the oil droplets
coalesce (David 1939). Embryos of L. tenuis are competent to hatch in 10 dpf at 208C but do not hatch
K. L. Martin and A. L. Carter
until immersed in seawater and agitated (Griem and
Martin 2000). If they are not triggered to hatch, then
L. tenuis arrest development but remain metabolically active and alert (Moravek and Martin 2011).
Continuously using up yolk with no decrease in
oxygen consumption, they are able to hatch within
seconds of receiving the cue to do so (Speer-Blank
and Martin 2004).
Following the attainment of hatching competence
at 10 dpf, each day 10 embryos from each clutch
were triggered to hatch by agitation in seawater
(Griem and Martin 2000). Hatching success was calculated, and the hatchlings’ total lengths were measured by ocular micrometer under a dissecting
microscope and converted to millimeter.
Adult length and mass are linearly related (Johnson
et al. 2009) and in this study correlated (Spearman
Rank Correlation, ¼ 0.67, P ¼ 0.04). The mean diameter of eggs was correlated with the diameter of the
drop of lipid at four dpf (Spearman Rank
Correlation, ¼ 0.72, P ¼ 0.0018).However, maternal
length of June fish did not predict egg diameter
(Spearman Rank Correlation, ¼ 0.61, P ¼ 0.07) or
clutch volume ( ¼ 0.42, P ¼ 0.21). Nor did maternal
mass correlate either with clutch volume (Spearman
Rank Correlation, ¼ 0.239, P ¼ 0.47) or egg diameter (Spearman Rank Correlation, ¼ 0.297,
P ¼ 0.37). Between clutches, mean egg diameter differed significantly, and the egg diameters from the
May runs, 1.826 0.005 were significantly larger than
those from the June runs, 1.698 0.022, by Student’s
t-test (t ¼ 6.25, df ¼ 20, P50.0001).
Between clutches, for both May and June, mean
egg diameter had a significant effect on mean length
of hatchlings (analysis of variance, F1,20 ¼ 9.032,
P ¼ 0.01). Within clutches, the total length of hatchlings did not differ whether they were triggered to
hatch early at 15 dpf or after extended incubation at
25 dpf (paired t-test, df ¼ 21, t ¼ 0.34, P ¼ 0.73).
Mean egg diameter was strongly correlated with duration of extended incubation, the final day that 50%
or more hatched (Spearman Rank Correlation,
¼ 0.7, P ¼ 0.001), suggesting there is a trade-off
for energy use between additional growth or development of the embryo, and the duration of extended
incubation for this species.
The egg diameter reported for L. tenuis varies
widely between studies and populations, suggesting
that the sizes and numbers of eggs may depend on
available food resources for this iteroparous fish.
Between populations, differences can be much
greater than within populations. A population of
L. tenuis within San Francisco Bay had significantly
smaller adults than did L. tenuis from Malibu, a
241
Terrestrial embryos in anamniotic eggs
mean length of 119.2 2.24 mm rather than
166.3 2.07 mm (Johnson et al. 2009). Eggs were
also significantly smaller, 1.52 0.01 mm in diameter
(Martin et al. 2009). Clutch volumes in populations
of L. tenuis from southern California typically are
between 1000 and 3000 eggs (Walker 1952). In
2007, 23 clutches from L. tenuis in San Francisco
Bay had a mean of 804 108 eggs, compared with
15 clutches from L. tenuis in southern California
with a mean of 2936 319 eggs, a significant difference (Student’s t-test, df ¼ 36, t ¼ 7.377;
P50.0001). Comparing these larger differences between populations, maternal body size significantly
affects clutch size. The population from San
Francisco Bay was not tested for survival during
extended incubation but one would predict a shorter
duration than found in this study.
Adult L. tenuis do not grow during the spawning
season, and each individual may spawn every 2 weeks
between March and August (Walker 1952). Spawning
runs vary in numbers and intensity over the habitat
range and the course of the season (Martin et al.
2006). This large reproductive output coupled with
adjustments in number and size of eggs may improve
reproductive success in the unpredictable terrestrial
environment.
Types of terrestrial incubation
Comparing the many different examples of terrestrial
incubation of anamniotic eggs by teleost fishes
(Table 1) and amphibians (Table 2), some patterns
may help show the similarities and differences. For
comparison, eight different terrestrial incubation
types have been identified in Table 3, and these are
briefly described below. Terrestrial incubation may
be brief or of extended duration, hatching may be
constitutive or environmentally cued, and development may occur continuously or incorporate some
pauses (Martin 1999; Podrabsky et al. 2010;
Warkentin 2011).
Type 1: conservative constitutive
This type is most similar to incubation in water.
Eggs incubate in air either continuously or
intermittently, and when they are mature enough,
they hatch, whether or not they are immersed. A
combination of temperature and a genetic developmental program determine the time of hatch without
additional environmental cues. One example of
this is the capelin M. villosus (Frank and Leggett
1981).
Table 3 Types of terrestrial development seen in anamniotic fishes and amphibians, with some examples
Early development in terrestrial habitat
Example species
Reference
Conservative constitutive: Continuous development to
maturation, hatch even if emerged
Capelin Mallotus villosus
Frank and Leggett (1981)
ECH early alert: Continuous development to maturation, hatch
even if emerged, potential to hatch early if disturbed by
predators or other threats
Red-eyed tree frog Agalychnis callidryas
Warkentin (2011)
Cautious constitutive: Continuous development to maturation,
hatch only upon tidal immersion
Fugu puffer Takifugu niphobles
Yamahira (1996)
ECH with parental involvement: Continuous development to
hatching competence, hatch upon immersion caused by
parental behavior
Mudskipper Periophthalmus modestus
Ishimatsu and Graham (2011)
ECH ready and waiting: Continuous development to hatching
competence, environmentally cued hatching, potential for
extended incubation with active metabolism but
developmental stasis
California grunion Leuresthes tenuis
Moravek and Martin (2011)
ECH ready and progressing: Continuous development to hatching
competence, environmentally cued hatching, potential for
extended incubation while slowly continuing developmental
progress
Australian toadlet Pseudophryne bibroni
Bradford and Seymour (1985)
Precocious: Continuous development beyond usual hatching
stage, prolonged incubation while continuing developmental
progress, hatch as juvenile completely bypassing aquatic
larval stage
Foam nesting frog Leptodactylus fuscus
deCarvalho et al. (2012)
Diapause: Discontinuous development with obligatory periods of
metabolic and maturational stasis, environmentally cued
hatching
Annual killifish Austrofundulus limnaeus
Podrabsky et al. (2010)
242
Type 2: ECH early alert
This type involves eggs that can hatch early in
response to a predator, disease, or other perceived
threat (Warkentin 2011). Eggs that are in air will
hatch in air; if development is completed without
an environmental cue for early hatching, then the
genetically programmed constitutive hatch will
occur, even if emerged. An example is the red-eyed
tree frog A. callidryas (Warkentin 2011).
Type 3: cautious constitutive
This type has terrestrial eggs that are constitutively
ready to hatch but will hatch only when submerged.
After hatching competence, this may involve a delay
of hours waiting for a higher tide, not days. An
example is the Fugu puffer T. niphobles (Yamahira
1996).
Type 4: ECH by parental involvement
This type exhibits ECH and is best exemplified by
the active role that mudskippers P. modestus and Pn.
schlosseri play by both providing an air chamber for
the incubation of their eggs and then removing the
air and allowing the eggs to hatch in water at the
appropriate time (Ishimatsu and Graham 2011).
Type 5: ECH ready and waiting
These animals develop to hatching competence but
require an environmental cue to hatch. If that cue
does not arrive, the embryos remain alert and active
but cease growth and development, so that stage at
hatching is relatively static, but time of hatching is
variable. An example is the California Grunion
L. tenuis (Moravek and Martin 2011).
Type 6: ECH ready and progressing
In this type, an animal spawns in ephemeral ponds
that dry up while the clutch is incubating; the embryos do not hatch until the rains return and submerge them. If hatching is delayed while waiting for
the environmental cue, embryos continue to pass
through developmental stages, and therefore, both
the time and the stage at hatching are variable, depending on the rainfall. Slow larval development
after hatching competence occurs in the frogs
Pseudophryne bibroni (Bradford and Seymour 1985)
and Arenophryne rotunda (Roberts 1984).
Both Types 5 and 6 can result in siblings from the
same clutch hatching at different times; these examples of heterokairy (Spicer and Burggren 2003) have
different phenotypes at the same age or dpf. This
trend to continue larval development within the
K. L. Martin and A. L. Carter
egg culminates in the seventh type of terrestrial
development.
Type 7: precocious or direct development
This type is exemplified by eggs of many species of
anurans, and some caudates, that are spawned into
fully terrestrial bubble nests to develop directly
(Shepard and Caldwell 2005). These species spend
the entire larval period within the egg, hatching as
miniatures of the adults.
Type 8: true diapauses
This type involves periods of obligatory, extreme
metabolic depression, and developmental stasis,
as seen in the eggs of the annual killifish,
Austrofundulus (Podrabsky et al. 2010). Reducing
the metabolic rate of these embryos almost to a
standstill allows survival of burial in anoxic mud
and avoids the need for large eggs to survive delays
of months or even years before resumption of
growth and development to hatching. Even in this
case, there are occasional examples of ‘‘escape’’ eggs
that proceed directly through development without
diapause (Podrabsky et al. 2010).
This list is not exhaustive, and there are certainly
other permutations of early development for anamniotic vertebrates incubating on land. Kryptolebias
marmoratus enters what has been called a ‘‘diapause’’
that has not been fully described (Wright 2012),
apparently halting development when its eggs
remain out of water after reaching hatching competence. The details and metabolic consequences or
correlates of this have not yet been described, but
may be more similar to the case of L. tenuis with
Type 5 (Table 3) than to the true diapause, Type 8,
of annual killifishes.
Although rare, there are some viviparous amphibians, including caecilians and salamanders (Duellman
and Trueb 1986). Whether this is part of a continuum toward, or an alternative to, terrestrial incubation (Zug et al. 2001) is not clear. However,
viviparity has arisen in many lineages of fishes.
Although viviparity may permit a greater transition
to land in some situations, it also provides higher
survival of embryos or other advantages unrelated
to terrestriality in others.
Summary: terrestrial incubation of
anamniotic eggs is widespread and
diverse
Why do fishes and amphibians continue to invade
land at the earliest stages of life? Selection pressures
for spawning on shore include avoidance of aquatic
243
Terrestrial embryos in anamniotic eggs
predators (Walker 1952; Touchon and Warkentin
2009). However, both adults and eggs are targeted
by aggregations of predators from both water and
land during the spawning runs (Middaugh 1981;
Gregory 2001) and while incubating (Olson 1950;
Middaugh et al. 1983; Touchon and Warkentin
2009; Warkentin 2011; DeCarvalho et al. 2012).
Recreational anglers stand on shore and use their
hands to scoop up vulnerable M. villosus and
L. tenuis during spawning runs (Frank and Leggett
1981; Gregory 2001). Predation today is likely quite
different from predation at the time of the initial
transition to land by vertebrates, and predation on
spawning runs that are predictable in occurrence is
likely to be higher than predation on smaller aggregations or pairs (Thurley and Bell 1994).
Conversely, avoiding aquatic hypoxia definitely is
a selection advantage of terrestrial incubation
(Middaugh et al. 1983; Tewksbury and Conover
1987). These energetically demanding, rapidly growing embryos must get enough oxygen to metabolize;
some eggs, especially if buried, die if immersed without hatching. If aquatic nests of amphibians sink
below the water’s surface, the deeper they sink, the
more likely it is that embryos drown, unable to sustain sufficient exchange of oxygen (Seymour and
Bradford 1995). Placing clutches on the ceiling of
brood chambers in intertidal boulders or in burrows
allows aerial exposure during low tides or during
times of stagnant water when aquatic hypoxia
would otherwise be a problem (Strathmann and
Hess 1999; Richards 2011).
Selection pressures for tidally terrestrial eggs and
embryos may be different, and emergences of shorter
duration, than pressures that lead to emergence of
nests from temporary pools or stagnant fresh water.
Even when terrestrial, eggs of fishes and amphibians
are usually in a humid environment or hydrated by a
parent. The shape and structure of eggs and nests
can vary tremendously (Altig and McDiarmid
2010), and these variations affect both diffusion of
oxygen and resistance to desiccation (Strathmann
and Hess 1999).
Eggs are self-contained, and embryos are unable to
obtain additional food until they hatch. A large, wellprovisioned egg allows plasticity of development
(Bernardo 1996). Thus, amphibian embryos adapted
to direct development require large eggs (Duellman
and Trueb 1986). The regulatory genes involved in
developmental stasis or progression for anamniotes
with ECH are not known and may have profound
implications for understanding energetics and cell
differentiation during early life.
The progress of development differs among embryos that remain at a given stage during extended
incubation, compared with others that develop
beyond that stage. Embryos that continue development during extended incubation may metamorphose at a smaller size than do those that hatch at
the time of hatching competence and can feed
during the larval period (Bradford and Seymour
1985), whereas those that simply remain static in
development start the larval period later, but at the
same size as embryos hatching without extended
incubation (Moravek and Martin 2011).
Clearly, behavioral plasticity and awareness of surroundings are necessary for both adults and the
embryos of these atypical fishes and amphibians, particularly for adults with terrestrial spawning and embryos with ECH. More comparisons between species
with different incubation habitats are needed. The
wide variety of species that spawn terrestrially,
shown in examples in Tables 1 and 2, and the diversity of types of development in Table 3 suggest that
terrestrial development is beneficial for many anamniotic species in multiple habitat types, and this
has evolved independently as the source of many
different present, past, and future transitions of
aquatic vertebrates to land.
Acknowledgments
We thank J. A. Powell, M. Holmes, C. Moravek, and
the Grunion Greeters for assistance, and R. Seymour,
R. Strathmann and A. Gibb for helpful discussions.
Support for participation in this symposium was
provided by the Society for Integrative and
Comparative Biology and its Divisions of Animal
Behavior, Comparative Biomechanics, Comparative
Biology and Phylogenetics, Comparative Physiology
and Biochemistry, Ecology and Evolution,
Evolutionary Developmental Biology, Neurobiology,
and Vertebrate Morphology; and the US National
Science Foundation (IOS 1237547).
Funding
Supported by National Science Foundation (DBI1062721) and Pepperdine University.
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