Timing Of Metamorphosis Research Articles

Effects of ultraviolet‐B radiation on metamorphic traits in the common frog Rana temporaria

AbstractEffects of ultraviolet‐B (UV‐B) radiation on amphibian embryonic and larval development have been investigated in a number of studies, but the effects on later life‐stages (metamorphosis) have received less attention. Hence, the effects of UV‐B radiation treatments (control (no UV‐B), normal and 26% enhanced levels of UV‐B) on the development of the common frog Rana temporaria embryos from fertilization until metamorphosis were investigated. Survival until metamorphosis was significantly higher among individuals exposed to normal, as compared to individuals sheltered from, UV‐B or those exposed to enhanced levels of UV‐B radiation. There were no effects of normal or enhanced levels of UV‐B radiation on the frequency of developmental anomalies. However, UV‐B radiation delayed the timing of metamorphosis in a dose‐dependent fashion, and the individuals from the normal and enhanced UV‐B treatments metamorphosed at smaller size than those raised in the absence of UV‐B radiation. These results suggest that UV‐B radiation experienced through embryonic and larval stages can have negative effects on the growth and development of R. temporaria. Delayed metamorphosis at reduced size is also likely to lower the fitness during later life‐stages.

Larval duration of the tropical eel Anguilla celebesensis from Indonesian and Philippine coasts

A comparative study of the otolith microstructure of glass eels Anguilla celebesensis from the Indonesian and Philippine coasts determined the timing of metamorphosis and age at recruitment to freshwater habitats; 2 samples from Indonesia were analyzed and statistically com- pared with a previously published sample analyzed using the same techniques. Ages at metamor- phosis and at recruitment were, respectively: 98 ± 7.2 d (mean ± SD) and 122 ± 7.2 d for specimens from the Poso River in Indonesia; 90 ± 13.6 and 112 ± 14.2 d for specimens from the Poigar River in Indonesia; and 124 ± 12.0 and 157 ± 13.7 d for specimens from the northern Philippines. The average duration of metamorphosis was very similar (15 to 17 d) in all specimens. A close linear relationship was found between age at metamorphosis and age at recruitment. These findings and the regional geography of the islands and ocean currents suggest that A. celebesensis has several spawning areas and potentially isolated populations in the region, as has been suggested for another, more widely distributed tropical anguillid, A. marmorata.

Temperature, genetic and hydroperiod effects on metamorphosis of brown frogs Rana arvalis and R. temporaria in the field

AbstractTime for metamorphosis and metamorph size of moor frogs Rana arvalis and common frogs R. temporaria were measured in 22 ponds for 1–8 years. Environmental data in these ponds were also measured. Metamorphosis of the frogs took place from the beginning of June to the beginning of August. When both species were found in one pond, the common frogs metamorphosed up to 20 days earlier than the moor frogs. Most variation in time for metamorphosis, among ponds and years, is explained by temperature effects, but a causal relationship was not established. Within a pond, metamorphosis was later in cold summers than in warm summers. Size at metamorphosis was affected by tadpole density; at high densities metamorphs were smaller. Size at metamorphosis was not related to time for metamorphosis. There was an effect of pond drying; if ponds were about to dry up, metamorphosis was accelerated by about 2.4 days. Tadpoles from ponds with a late metamorphosis in the field had tadpoles that metamorphosed early in a common garden experiment, suggesting counter gradient selection.

Predation risk and competition effects on the life-history characteristics of larval Oregon spotted frog and larval red-legged frog.

We conducted an artificial pond experiment to test hypotheses about the effects of competition and non-lethal predator cues on metamorphic characteristics of sympatric Oregon spotted frogs (Rana pretiosa) and red-legged frogs (Rana aurora) in southwestern British Columbia. Tadpoles were exposed to the presence or absence of one another, two density levels and to the presence or absence of predacious odonate larvae (Aeshna palmata) isolated in enclosures. In the artificial pond study, R. aurora were significantly larger at metamorphosis (12%) and exhibited only slightly longer larval periods when exposed to Aeshna. In the presence of R. pretiosa, they significantly decreased time to metamorphosis, and were significantly larger at metamorphosis (12%) than those reared alone. Rana pretiosa in treatments with R. aurora were somewhat larger at metamorphosis when a non-lethal predator was present, and in treatments where R. pretiosa were alone with a predator tadpole mass at metamorphosis was smaller than those in the absence of Aeshna, but these results were not statistically significant. Both species reduced activity and moved away from the predator in the presence of an enclosed dragonfly larva in the laboratory. Most tadpole mesocosm experiments have found that the trade-off between size and timing of metamorphosis is extremely important to amphibians, but we suggest that the trade-off discussed in traditional amphibian models may not apply to species like R. pretiosa that are exposed to the same gape-limited predators upon reaching metamorphosis.

INDUCED MORPHOLOGICAL DEFENSES IN THE WILD: PREDATOR EFFECTS ON A MAYFLY, DRUNELLA COLORADENSIS

Phenotypic plasticity may enable organisms to optimize their phenotypes in environments that are heterogeneous over time or space. For example, inducible defenses are favored for prey populations faced with variable predation risk. We studied the impact of brook trout (Salvelinus fontinalis) on the development of defensive morphological characters in larvae of the mayfly, Drunella coloradensis, both in natural streams and in a series of experiments carried out in streamside, circular, flow-through chambers. Drunella larvae in natural streams with trout had longer caudal filaments per unit body size and relatively heavier exoskeletons than Drunella in fishless streams. Female larvae that developed in fish streams were also significantly smaller and less fecund at metamorphosis than those living in fishless streams, suggesting a possible fitness cost associated with development of morphological defenses. However, timing of metamorphosis of Drunella larvae to the adult stage did not differ between fish and fishless streams. Larvae originating from fish and fishless streams were reared and exposed to water with fish cues or fishless control water for three weeks (1998) or until they developed black wing pads, i.e., just before emergence (1999). In both experiments waterborne fish cues induced the development of relatively longer caudal filaments, but only in Drunella originating from sites without fish. Waterborne fish cues had no effect on Drunella growth rates, behavior, or size at emergence. Drunella originating from fish streams had significantly lower mortality when exposed to predation by trout than Drunella originating from fishless streams. Caudal filament length appears to enhance survival, as Drunella with intact caudal filaments had lower predation rates than Drunella with their tails artificially shortened. This study provides evidence of chemically induced morphological plasticity that could reduce predation rates of these mayflies in natural stream environments.

High density effects on the growth, development and survival of Litoria aurea tadpoles

Increased production of frogs is expected as markets increase and wild stocks dwindle. With conventional rearing techniques, high tadpole densities lower metamorphosis weight, and increase metamorphosis time (MT) and variation. These problems result from low water quality and competition for feed. In this study, tadpoles of Litoria aurea, a species with a similar ecology and physiology to commercial frog species, were reared at high to very-high densities (40, 80, 120, 160 and 330 l −1). Adequate dissolved oxygen was achieved with shallow water (1.2 cm), water was changed every 12 h, and the tadpoles feed to satiation. Individual weight and survival were calculated at 14-day intervals until first metamorphosis at 45 days. With increasing density, tadpole weight declined from 4.23±0.10 to 1.68±0.18 (g). Survival was greater than 85% for all densities except for 330 l −1 (64%). At metamorphosis, mean survival, metamorphosis time, and weight were calculated for densities of 40–180 l −1. The weight of juveniles (1.90–2.10 g) from the 40–80 l −1 densities compared favorably with that of wild juveniles (1.8 g). Metamorphosis time was 52–62 days, which compares favorably with the ≈100 days achieved by conventional techniques with commercial species at much lower densities (≈2 l −1). This study shows the use of high density rearing techniques with tadpoles; (1) produce consistently high quality metamorphs, (2) shorten rearing time and metamorphosis period, (3) potentially use water, feed and space more efficiently.

Acceleration of Ambystoma tigrinum metamorphosis by corticotropin-releasing hormone.

Previous work of others and ours has shown that corticotropin-releasing hormone (CRH) is a positive stimulus for thyroid and interrenal hormone secretion in amphibian larvae and that activation of CRH neurons may mediate environmental effects on the timing of metamorphosis. These studies have investigated CRH actions in anurans (frogs and toads), whereas there is currently no information regarding the actions of CRH on metamorphosis of urodeles (salamanders and newts). We tested the hypothesis that CRH can accelerate metamorphosis of tiger salamander (Ambystoma tigrinum) larvae. We injected tiger salamander larvae with ovine CRH (oCRH; 1 microg/day; i.p.) and monitored effects on metamorphosis by measuring the rate of gill resorption. oCRH-injected larvae completed metamorphosis earlier than saline-injected larvae. There was no significant difference between uninjected and saline-injected larvae. Mean time to reach 50% reduction in initial gill length was 6.9 days for oCRH-injected animals, 11.9 days for saline-injected animals, and 14.1 days for uninjected controls. At the conclusion of the experiment (day 15), all oCRH-injected animals had completed metamorphosis, whereas by day 15, only 50% of saline-injected animals and 33% of uninjected animals had metamorphosed. Our results show that exogenous oCRH can accelerate metamorphosis in urodele larvae as it does in anurans. These findings suggest that the neuroendocrine mechanisms controlling metamorphosis are evolutionarily conserved across amphibian taxa.

Fitness consequences of the timing of metamorphosis in a freshwater crustacean

Metamorphosis is a common life‐cycle transition in organisms as diverse as amphibians, insects, fishes and crustaceans, and the timing of this transition often affects an individual's fitness. Here, we measured age and size at metamorphosis in laboratory‐reared individuals of the freshwater copepod, Diaptomus leptopus, and then followed individuals over their entire life cycle to assess the fitness consequences of variation in age and size at metamorphosis. In 3 separate experiments, individuals were raised in different food conditions: low food (0.2 μg C/ml) switched to high food (0.7 μg C/ml), or high food switched to low food, at several different larval and juvenile stages. Control individuals were reared on high or low food concentrations over their entire life cycles. For each individual, we measured age and size at metamorphosis and age and size at maturity; for females, we also measured total lifetime egg production, longevity, and calculated a composite fitness measure, λ. Statistical analyses showed no significant effects of age or size at metamorphosis on these same traits measured at maturity, or on the fitness components we estimated. The first individuals to mature had the highest total egg production and individual fitness; differences in body size at maturation explained none of the variation observed in fitness components. Our results show that metamorphosis was uncoupled from maturity and from fitness components by growth and development achieved during the juvenile phase of the life cycle, and support the conclusion that fitness consequences of metamorphosis depend fundamentally on the organization of an organism's life cycle. They also suggest that body size plays a different life‐history role in these organisms than is recognized in most poikilotherms, and suggest the hypothesis, based on laboratory experiments, that selection may act primarily on juvenile developmental rates in field populations.

Growth history and inshore migration of the tropical eel, Anguilla marmorata , in the Pacific

A comparative study of the otolith microstructure and microchemistry of Anguilla marmorata glass eels in the western North Pacific (Japan, Taiwan, the Philippines, Indonesia) determined the timing of metamorphosis and age at recruitment to freshwater habitats with a view to learning about the early life history and recruitment of this species of tropical anguillid eel, which has a wide range throughout much of the western Pacific and parts of the Indian Ocean. Three new samples (from Japan, Taiwan, Indonesia) were analyzed and statistically compared along with two other previously published samples that were analyzed using the same techniques. Ages at metamorphosis and recruitment, respectively, were 123±13.4 days (mean±SD) and 154±17.0 days in specimens from Japan, 116±14.6 days and 145±15.6 days in those from Taiwan, 120±13.0 days and 154±13.5 days in the Philippines stock and 132±9.7 days and 159±11.7 days, and 120±15.6 days and 152±15.2 days in the Indonesian stock. The average duration of the period of metamorphosis estimated from otolith microstructure was very similar (15–17 days) in the specimens from all locations. A close linear relationship was found between the ages at metamorphosis and recruitment at all locations, suggesting that individuals that metamorphosed earlier were recruited to freshwater habitats at a younger age. Back-calculated hatching dates ranged over about 6 months of the year, suggesting that this species may spawn throughout much of the year. It is hypothesized that specimens from all four sites are from the same spawning population originating in a spawning area in the North Equatorial Current of the western North Pacific.

Ontogeny of Crustacean Respiratory Proteins

The respiratory proteins hemoglobin and hemocyanin share the function of oxygen transport, but the proteins belong to separate gene families, and their active sites and the metal ions that bind the oxygen differ. Either hemoglobin or hemocyanin, but not both, is expressed in the hemolymph of many arthropod crustaceans. Hemoglobin is present in Branchiopoda, Ostracoda, Copepoda, rhizocephalan Cirripedia and one suborder of amphipodan Malacostraca, while hemocyanin has been described in Malacostraca. Recent work by several laboratories have provided new information on the gene structure, exon-intron patterns, site of synthesis and expression of hemoglobins in the branchiopods Artemia and Daphnia. These studies suggest the branchiopods are excellent model organisms for studies of oxygen sensors and hypoxia inducible transcription factors during developmental and adult stages. The focus in our laboratory on the ontogeny of hemocyanin in the Dungeness crab, Cancer magister, has demonstrated that both structure and function of hemocyanin change from megalopa to adult crab. The hemocyanin of an oceanic megalopa contains four subunits. Another subunit appears about the time of metamorphosis to first juvenile instar, and expression of a sixth subunit begins four or five molts later. The timing of onset of adult hemocyanin can be altered experimentally by food levels and temperature. Gene expression and functional properties of both red and blue oxygen transport proteins of crustaceans change during ontogeny to insure oxygen delivery appropriate for each developmental stage.

The role of low levels of juvenile hormone esterase in the metamorphosis of Manduca sexta

The activity of juvenile hormone esterase (JHE) in feeding fifth instar larvae of Manduca sexta increases gradually with larval weight and rises to a peak after larvae pass the critical weight when juvenile hormone secretion ceases. Starvation of larvae of Manduca sexta (L.) that had exceeded the critical weight inhibited peak levels of JHE, but did not delay entry into the wandering stage when larvae leave the plant in search of a pupation site. This suggests that peak levels of JHE may not be essential for the normal timing of metamorphosis. Starved larvae pupated normally, indicating the peak of JHE was not necessary for a morphologically normal pupation. Treatments of larvae with the selective JHE inhibitor O-ethyl-S-phenyl phosphoramidothiolate (EPPAT) that began immediately after larvae achieved the critical weight (6.0 to 6.5 grams for our strain of Manduca) delayed entry into the wandering stage. By contrast, EPPAT treatment of larvae at weights above 8.0 g had no effect on the subsequent timing of the onset of wandering. Therefore, although the normal timing of the onset of wandering does not require peak levels of JHE, it requires low to moderate levels of JHE to be present until larvae reach a weight of about 8.0 g.

Timing of metamorphosis and the onset of the negative feedback loop between the thyroid gland and the pituitary is controlled by type II iodothyronine deiodinase in Xenopus laevis.

Two important features of amphibian metamorphosis are the sequential response of tissues to different concentrations of thyroid hormone (TH) and the development of the negative feedback loop between the pituitary and the thyroid gland that regulates TH synthesis by the thyroid gland. At the climax of metamorphosis in Xenopus laevis (when the TH level is highest), the ratio of the circulating precursor thyroxine (T4) to the active form 3,5,3'-triiodothyronine (T3) in the blood is many times higher than it is in tissues. This difference is because of the conversion of T4 to T3 in target cells of the tadpole catalyzed by the enzyme type II iodothyronine deiodinase (D2) and the local effect (cell autonomy) of this activity. Limb buds and tails express D2 early and late in metamorphosis, respectively, correlating with the time that these organs undergo TH-induced change. T(3) is required to complete metamorphosis because the peak concentration of T4 that is reached at metamorphic climax cannot induce the final morphological changes. At the climax of metamorphosis, D2 expression is activated specifically in the anterior pituitary cells that express the genes for thyroid-stimulating hormone but not in the cells that express proopiomelanocortin. Physiological concentrations of T3 but not T4 can suppress thyrotropin subunit beta gene expression. The timing and the remarkable specificity of D2 expression in the thyrotrophs of the anterior pituitary coupled with the requirement for locally synthesized T3 strongly support a role for D2 in the onset of the negative feedback loop at the climax of metamorphosis.

Long-term assessment of settlement and growth of juvenile winter flounder ( Pseudopleuronectes americanus) in New Jersey estuaries

We examined patterns of metamorphosis, settlement, and growth for young-of-the-year winter flounder over a ten year period (1990–1999) in four estuaries spanning the coast of New Jersey, USA, with the objective to determine the spatial and temporal coherence in these processes. We hypothesised that these processes could be influenced by large-scale climatic factors such as temperature and small-scale, local factors such as predator and prey abundances and differences associated with the localised population structure of winter flounder. Newly settled juveniles were collected in late May/early June each year. Increment counts on sagittal otoliths were used to determine the date of metamorphosis, and increment widths were used to estimate growth rates at two times, just after settlement and just prior to capture. A high level of consistency in spatial patterns among four individual estuaries was evident, and was largely driven by the northernmost site, Sandy Hook, which had higher fish densities and later metamorphosis than the three other sites, and faster growth rates than the two mid-coast sites (Barnegat Bay and Great Bay). In contrast to spatial patterns, consistent temporal patterns were evident only in the timing of metamorphosis, which was delayed in colder years at all sites. Weekly plankton sampling over the same ten year period at one site (Great Bay) yielded winter flounder larvae during a relatively narrow period in spring, with a later peak of abundance in colder years, in agreement with back-calculated dates of metamorphosis for settled juveniles. These patterns suggest that the timing of settlement is driven by large-scale climatic factors that influence the timing of spawning and/or larval development. Interannual variability in densities and growth rates, however, appeared to be independent at each site, indicating control by local environmental factors or genetic differences among local populations. The spatial consistency of growth rates suggests that appropriate nursery areas can be readily identified for juvenile winter flounder. However, subsequent recruitment needs to be verified at the level of local populations to identify contributing source habitats.

VARIATION IN MAYFLY SIZE AT METAMORPHOSIS AS A DEVELOPMENTAL RESPONSE TO RISK OF PREDATION

Animals with complex life cycles often show large variation in the size and timing of metamorphosis in response to environmental variability. If fecundity increases with body size and large individuals are more vulnerable to predation, then organisms may not be able to optimize simultaneously size and timing of metamorphosis. The goals of this study were to measure and explain large-scale spatial and temporal patterns of phe- notypic variation in size at metamorphosis of the mayfly, Baetis bicaudatus (Baetidae), from habitats with variable levels of predation risk. Within a single high-elevation watershed in western Colorado, USA, from 1994 to 1996 we measured dry masses of mature larvae of the overwintering and summer generations of Baetis at 28 site-years in streams with and without predatory fish (trout). We also estimated larval growth rates and development times at 16 site-years. Patterns of spatial variation in mayfly size could not be explained by resource (algae) standing stock, competitor densities, or physical-chemical variables. However, size at metamorphosis of males and females of summer generation Baetis was smaller in fish streams than in fishless streams and decreased as densities of predatory stoneflies increased. Furthermore, overwintering individuals matured at larger sizes than summer generation Baetis, and the size of emerging Baetis declined over the summer, but predominantly in trout streams. Theoretical consideration of the effect of predation risk on size and timing of metamorphosis accurately predicted the observed temporal variation in size and timing of mayflies at emergence in fish and fishless streams. Baetis populations had similar growth rates but followed different developmental trajectories in high and low risk environments. In risky environments larval development was accelerated, resulting in metamorphosis of younger and smaller individuals, minimizing exposure of larvae to risk of mortality from trout predation, but at the cost of future reproduction. In safe environ- ments, larvae extended their development, resulting in larger, more fecund adults. Thus, we propose that large-scale patterns of variation in size and timing of metamorphosis represent adaptive phenotypic plasticity, whereby mayflies respond to variation in risk of predation, thereby maximizing their fitness in variable environments.

Variation in Mayfly Size at Metamorphosis as a Developmental Response to Risk of Predation

Animals with complex life cycles often show large variation in the size and timing of metamorphosis in response to environmental variability. If fecundity increases with body size and large individuals are more vulnerable to predation, then organisms may not be able to optimize simultaneously size and timing of metamorphosis. The goals of this study were to measure and explain large-scale spatial and temporal patterns of phenotypic variation in size at metamorphosis of the mayfly, Baetis bicaudatus (Baetidae), from habitats with variable levels of predation risk. Within a single high-elevation watershed in western Colorado, USA, from 1994 to 1996 we measured dry masses of mature larvae of the overwintering and summer generations of Baetis at 28 site-years in streams with and without predatory fish (trout). We also estimated larval growth rates and development times at 16 site-years. Patterns of spatial variation in mayfly size could not be explained by resource (algae) standing stock, competitor densities, or physical–chemical variables. However, size at metamorphosis of males and females of summer generation Baetis was smaller in fish streams than in fishless streams and decreased as densities of predatory stoneflies increased. Furthermore, overwintering individuals matured at larger sizes than summer generation Baetis, and the size of emerging Baetis declined over the summer, but predominantly in trout streams. Theoretical consideration of the effect of predation risk on size and timing of metamorphosis accurately predicted the observed temporal variation in size and timing of mayflies at emergence in fish and fishless streams. Baetis populations had similar growth rates but followed different developmental trajectories in high and low risk environments. In risky environments larval development was accelerated, resulting in metamorphosis of younger and smaller individuals, minimizing exposure of larvae to risk of mortality from trout predation, but at the cost of future reproduction. In safe environments, larvae extended their development, resulting in larger, more fecund adults. Thus, we propose that large-scale patterns of variation in size and timing of metamorphosis represent adaptive phenotypic plasticity, whereby mayflies respond to variation in risk of predation, thereby maximizing their fitness in variable environments.

The effect of food on growth and metamorphosis of paedomorphs in Triturus alpestris apuanus

The effect of food level on growth and metamorphosis of paedomorphs was examined in an experimental replicated design in Triturus alpestris apuanus. Paedomorphosis concerns the retention of larval characteristics in adult individuals. Newts that forgo metamorphosis and then retain gill and gill slits in the adult stage maintain an aquatic life but keep potential for undergoing metamorphosis. Paedomorphs metamorphosed later in treatments with food as a non-limiting factor than in stressful treatments where food was limited. Timing of metamorphosis did not differ between males and females. Food level greatly affected growth rates. These results confirm and extend optimality models that predict paedomorphosis under advantageous aquatic conditions (paedomorph advantage hypothesis) and metamorphosis in stressful aquatic habitats.

Dispersal pattern of glass eel stage of Anguilla australis revealed by otolith growth increments

Glass eels of the Australasian shortfin eel Anguilla australis (Richardson 1841) were col- lected from 6 Australian and 2 New Zealand estuaries. Their ages were estimated by counting daily growth increments in the otoliths. According to mean size and age at capture, the glass eels were classified into a northern Australia group or a southern Australia and New Zealand group. The mean length of glass eels increased from 47.6 ± 2.11 mm in northern estuaries to 59.2 ± 3.61 mm in the south. The mean age of glass eels at capture was significantly lower in the north (214 ± 14.6 to 223 ± 17.7 d) than in the south (243 ± 19.7 to 261 ± 22.4 d) (p < 0.05). In contrast, the otolith growth rate was greater in the north than in the south. The dramatic increase in increment width and the decline of the Sr:Ca ratios in otoliths were used to determine the timing of metamorphosis from lep- tocephalus to glass eel stage. The mean ages of leptocephali at metamorphosis were significantly lower in the north (160 ± 14.2 to 161 ± 12.6 d) than in the south (168 ± 14.5 to 189 ± 16.9 d), indicating that faster-growing and earlier-metamorphosed leptocephali recruited to northern Australia and slow-growing and late-metamorphosed leptocephali recruited to southern Australia and New Zealand. In addition, based on current direction and the similarity in age of leptocephali at metamor- phosis, age at capture and the period between metamorphosis and estuarine arrival, New Zealand glass eels are unlikely to be transported across Tasman Sea from southern Australia by the East Aus- tralian Current, and must reach their destination via a different route(s).

METAMORPHOSIS OF BARNACLE NAUPLII: EFFECTS OF FOOD VARIABILITY AND A COMPARISON WITH AMPHIBIAN MODELS

Like many animals, barnacles have a complex life cycle with shifts in both diet and habitat. The life cycle of most barnacles has three distinct phases: (1) a planktotrophic nauplius, (2) a non-feeding, planktonic cyprid that subsists on energy reserves, and (3) a benthic juvenile and adult. We conducted a series of experiments to measure the effects of variable food concentration during the naupliar phase on the age, size, and lipid reserves of Balanus glandula cyprids. When food shifted during only the first ∼25% of the naupliar phase (the first three instars), the initial food level did not affect the timing of metamorphosis to the cyprid. Shifts in food that were restricted to the final ∼40% of the naupliar phase (the sixth instar) also did not affect age at metamorphosis. During the intermediate portion of the naupliar phase, enhanced food decreased the age at metamorphosis, while reduced food lengthened the naupliar phase. Cyprid size generally correlated positively with changes in food, but a maximal size appeared to result when food increased during the intermediate portion of the naupliar phase (when the timing of metamorphosis was plastic). Amphibian models adequately describe the effects of variable food on the size and age at metamorphosis to the cyprid, provided that the model specifies an upper limit to size at metamorphosis when food is enhanced prior to fixation of development rate. In contrast to effects on size and age at metamorphosis, cyprids' lipid concentration (lipid per unit body size) only responded to shifts in food that occurred during the sixth instar. This resulted because shifts in food during the sixth instar affected both cyprids' size and lipid content (lipid per cyprid). Earlier shifts in food greatly affected a cyprid's size, but had little effect on lipid content or lipid concentration. Because the size, age, and lipid reserves of cyprids all have fitness implications, the net effects of food variability are complicated and depend on exactly when the variability occurs. Short-term changes in food encountered after the third instar and before the sixth will alter the length of the naupliar period and the size of cyprids. Variability restricted to the sixth instar will not alter the age at metamorphosis, but will affect the cyprid's size, lipid content, and lipid concentration.

Adaptive evolution of larvae and life cycles

The larval patterns of marine invertebrates pose intriguing questions for both evolutionary and developmental biologists. However, combined investigations have been rare. Quantitative models analyze the selective factors that drive evolutionary change in larval nutrition and timing of metamorphosis. Developmental studies describe the morphogenesis characterizing ancestral and derived larval patterns. Rigorous evolutionary analysis of the transition to derived modes of development is lacking and detailed developmental and ecological data are needed to test and refine theoretical models. A major challenge facing studies of life cycle evolution is the elucidation of the genetic structure and covariance of important developmental and larval traits.

Response of Treefrog Larvae to Drying Ponds: Comparing Temporary and Permanent Pond Breeders

Most amphibian species with an aquatic larval stage use one of two types of breeding habitats: ephemeral or permanent water bodies. A common assumption is that, once a minimum developmental threshold has passed, tadpoles of species that use temporary ponds can respond adaptively to a drying larval habitat by hastening development to metamorphose before the pond dries. We investigated how different pond drying regimes affected the timing of metamorphosis and body size at metamorphosis of two closely related species of hylid treefrogs, one of which commonly breeds in temporary ponds (Hyla gratiosa) and the other in permanent ponds (Hyla cinerea). We experimentally manipulated the water level in cattle-tank communities, exposing tadpoles of each species to a slow drying treatment, a fast drying treatment, and a constant water level treatment. There was no direct effect of pond drying on the larval period or body size at metamorphosis of either species. The drying treatments indirectly affected these traits by increasing larval densities, which extended the larval period and produced smaller sizes at metamorphosis. The timing of metamorphosis and body size at metamorphosis of H. gratiosa were more plastic than the corresponding traits in H. cinerea, but this greater plasticity cannot be interpreted as adaptive. Our results emphasize the utility of the comparative approach in interpreting the potential adaptive responses of species to environmental variation.