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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 Downloaded from http://az.oxfordjournals.org/ by guest on November 19, 2016 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. Downloaded from http://az.oxfordjournals.org/ by guest on November 19, 2016 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 (EITHER) aquatic conditions arrive (OR) 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. Downloaded from http://az.oxfordjournals.org/ by guest on November 19, 2016 luration HATCHING after exten 282 K. L. M. MARTIN Species A. gracile A. cingulatum ] 150 % [Ml | 500 % [mim A. opacum 730 % P. bibroni "| 400 % G. maculatus mini | 430 % Ad. xen/ca flM F. confluentes [Mil F. heteroclitus mm LU Primary D Extended | 170 % 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). Downloaded from http://az.oxfordjournals.org/ by guest on November 19, 2016 0 | 570 % 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). Downloaded from http://az.oxfordjournals.org/ by guest on November 19, 2016 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- Downloaded from http://az.oxfordjournals.org/ by guest on November 19, 2016 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. Downloaded from http://az.oxfordjournals.org/ by guest on November 19, 2016 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. Downloaded from http://az.oxfordjournals.org/ by guest on November 19, 2016 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. ACKNOWLEDGMENTS REFERENCES Anderson, J. D. and G. K. Williamson. 1976. Terrestrial mode of reproduction in Ambystoma cingulatum. Herpetologica 32:214-221. Balon, E. K. 1984. Patterns in the evolution of reproductive styles in fishes. In G. W. Potts and R. J. Wootton (eds.) Fish reproduction: Strategies and Tactics, pp. 35-53. Academic Press, London. Bradford, D. F. 1984. 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