Short‐term larval food stress and associated compensatory growth reduce adult immune function in a damselfly

Abstract 1. In animals with a complex life cycle, larval stressors may carry over to the adult stage. Carry‐over effects not mediated through age and size at metamorphosis have rarely been studied. The present study focuses on the poorly documented immune costs of short‐term food stress both in the larval stage and after metamorphosis in the adult stage. 2. The present study quantified immune function [number of haemocytes, activity of prophenoloxidase (proPO) and phenoloxidase (PO)] in an experiment where larvae of the damselfly Lestes viridis were exposed to a transient starvation period. 3. Directly after starvation, immune variables were reduced in starved larvae. Levels of proPO and PO remained low after starvation, even after metamorphosis. In contrast, haemocyte numbers were fully compensated by the end of the larval stage, yet were lower in previously starved animals after metamorphosis. This can be explained as a cost of the observed compensatory growth after starvation. Focusing only on potential costs of larval stressors within the larval stage may therefore be misleading. 4. The here‐identified immunological cost in the adult stage of larval short‐term food stress and associated compensatory growth strongly indicates that physiological costs may explain hidden carry‐over effects bridging metamorphosis. This adds to the increasing awareness that the larval and adult stages in animals with a complex life cycle should be jointly studied, as trade‐offs may span metamorphosis.     

Compensatory growth and oxidative stress in a damselfly

Physiological costs of compensatory growth are poorly understood, yet may be the key components in explaining why growth rates are typically submaximal. Here we tested the hypothesized direct costs of compensatory growth in terms of oxidative stress. We assessed oxidative stress in a study where we generated compensatory growth in body mass by exposing larvae of the damselfly Lestes viridis to a transient starvation period followed by ad libitum food. Compensatory growth in the larval stage was associated with higher oxidative stress (as measured by induction of superoxide dismutase and catalase) in the adult stage. Our results challenge two traditional views of life-history theory. First, they indicate that age and mass at metamorphosis not necessarily completely translate larval stress into adult fitness and that the observed physiological cost may explain hidden carry-over effects. Second, they support the notion that costs of compensatory growth may be associated with free-radical-mediated trade-offs and not necessarily with resource-mediated trade-offs.     

Resource limitation,predation risk and compensatory growth in a damselfly

Periods of poor nutrition during early development may have negative fitness consequences in subsequent periods of ontogeny. In insects, suppression of growth and developmental rate during the larval stage are likely to affect size and timing of maturity, which in turn may lead to reduced reproductive success or survivorship. In light of these costs, individuals may achieve compensatory growth via behavioural or physiological mechanisms following food limitation. In this study, we examined the effects of a temporary period of food restriction on subsequent growth and age and size at maturity in the larval damselfly Ischnura verticalis (Odonata: Coenagrionidae). We also asked whether this temporary period of reduced nutrition affected subsequent foraging behaviour under predation risk. I. verticalis larvae exposed to a temporary food shortage suffered from a reduced growth rate during this period relative to a control group that was fed ad libitum. However, increased growth rates later in development ensured that adult body size measurements (head and pronotum widths) did not differ between the treatments upon emergence. In contrast, adult dry mass did not catch up to that of the controls, indicating that the increased growth rates for size dimensions occur at the cost of similar gains in mass. Predators reduced foraging effort of larvae, but this reduction did not differ between control larvae and those previously exposed to poor nutrition.     

Compensatory growth strategies are affected by the strength of environmental time constraints in anuran larvae

Organisms normally grow at a sub-maximal rate. After experiencing a period of arrested growth, individuals often show compensatory growth responses by modifying their life-history, behaviour and physiology. However, the strength of compensatory responses may vary across broad geographic scales as populations differ in their exposition to varying time constraints. We examined differences in compensatory growth strategies in common frog (Rana temporaria) populations from southern and northern Sweden. Tadpoles from four populations were reared in the laboratory and exposed to low temperature to evaluate the patterns and mechanisms of compensatory growth responses. We determined tadpoles’ growth rate, food intake and growth efficiency during the compensation period. In the absence of arrested growth conditions, tadpoles from all the populations showed similar (size-corrected) growth rates, food intake and growth efficiency. After being exposed to low temperature for 1 week, only larvae from the northern populations increased growth rates by increasing both food intake and growth efficiency. These geographic differences in compensatory growth mechanisms suggest that the strategies for recovering after a period of growth deprivation may depend on the strength of time constraints faced by the populations. Due to the costs of fast growth, only populations exposed to the strong time constraints are prone to develop fast recovering strategies in order to metamorphose before conditions deteriorate. Understanding how organisms balance the cost and benefits of growth strategies may help in forecasting the impact of fluctuating environmental conditions on life-history strategies of populations likely to be exposed to increasing environmental variation in the future.     

Influence of delayed metamorphosis on postsettlement survival and growth in the sipunculan Apionsoma misakianum

Abstract. Certain stresses experienced by marine larvae from many groups can dramatically reduce aspects of juvenile performance. This study reports the effects of delayed metamorphosis and nutritional stress on survival and growth of the deposit-feeding sipunculan Apionsoma (= Golfingia ) misakianum . Approximately 600 larvae collected from the Florida Current plankton were distributed among 3 treatment groups. Ninety larvae (controls) were offered sediment and adult-conditioned seawater 4 d after collection, to induce metamorphosis; larvae of this species could not be induced to metamorphose by increasing the K⁺ concentration of seawater. The remaining 500 larvae were kept swimming for either 2 or 4 weeks, with or without phyto-plankton (clone T-ISO). At the end of the periods of prolonged larval swimming, subsampled larvae (360) were induced to metamorphose as in the controls. Surviving individuals were retrieved 6 weeks after the addition of excess sediment in all treatments, and weighed to document growth. Neither delayed metamorphosis nor starvation influenced juvenile survival. However, starving larvae for 2 weeks significantly reduced mean juvenile growth rates relative to the mean growth rate of control individuals (p<0.0001), while prolonging larval life by 4 weeks significantly reduced mean juvenile growth rates (p<0.05) whether or not larvae were fed. Reduced juvenile growth rates may have been caused by nutritional stress experienced by larvae in both the starved and fed treatments. The rapid response of freshly collected larvae to sediment indicates that competent larvae of this species routinely delay metamorphosis in the field. The extent to which they also experience food limitation is not yet clear. If competent larvae are food limited while delaying metamorphosis in the field, our results suggest that juveniles will grow more slowly and may thus exhibit reduced fitness.     

Effects of induced variation in anuran larval development on postmetamorphic energy reserves and locomotion

Anuran larvae exhibit high levels of phenotypic plasticity in growth and developmental rates in response to variation in temperature and food availability. We tested the hypothesis that alteration of developmental pathways during the aquatic larval stage should affect the postmetamorphic performance of the Iberian painted frog (Discoglossus galganoi). We exposed tadpoles to different temperatures and food types (animal- vs. plant-based diets) to induce variation in the length of the larval period and body size at metamorphosis. In this species, larval period varied with temperature but was unaffected by diet composition. In contrast, size at metamorphosis was shaped by the interaction between food quality and temperature; tadpoles fed on an animal-based diet became bulkier metamorphs than those fed on plant-based food at high (22°C) but not at low (12°C) temperature. Body condition of newly metamorphosed frogs was unrelated to the temperature or food type experienced during the premetamorphic stage. Frogs maintained at high temperature during the larval period showed reduced jumping ability, especially when fed on the plant-based diet. However, when considering size-independent jumping ability, cold-reared individuals exhibited the lowest performance, and herbivores reared at 17°C the highest. Cold-reared (12°C) frogs accumulated larger amounts of energy reserves than individuals raised at 17°C or 22°C. This was still the case after correction for differences in body mass, thus indicating some size-independent effect of developmental temperature. Despite the higher lipid content of the carnivorous diet, the differences in energy reserves between herbivores and carnivores were relatively weak and associated with differences in body size. These results suggest that the consequences of environmental variation in the larval habitat can extend to the terrestrial phase and influence juvenile growth and survival.     

Reversibility of predator‐induced plasticity and its effect at a life‐history switch point

In natural systems, organisms are frequently exposed to spatial and temporal variation in predation risk. Prey organisms are known to develop a wide array of plastic defences to avoid being eaten. If inducible plastic defences are costly, prey living under fluctuating predation risk should be strongly selected to develop reversible plastic traits and adjust their defences to the current predation risk. Here, we studied the induction and reversibility of antipredator defences in common frog Rana temporaria tadpoles when confronted with a temporal switch in predation risk by dragonfly larvae. We examined the behaviour and morphology of tadpoles in experimental treatments where predators were added or withdrawn at mid larval development, and compared these to treatments with constant absence or presence of predators. As previous studies have overlooked the effects that developing reversible anti‐predator responses could have later in life (e.g. at life history switch points), we also estimated the impact that changes in antipredator responses had on the timing of and size at metamorphosis. In the presence of predators, tadpoles reduced their activity and developed wider bodies, and shorter and wider tails. When predators were removed tadpoles switched their behaviour within one hour to match that found in the constant environments. The morphology matched that in the constant environments in one week after treatment reversal. All these responses were highly symmetrical. Short time lags and symmetrical responses for the induction/reversal of defences suggest that a strategy with fast switches between phenotypes could be favoured in order to maximise growth opportunities even at the potential cost of phenotypic mismatches. We found no costs of developing reversible responses to predators in terms of life‐history traits, but a general cost of the induction of the defences for all the individuals experiencing predation risk during some part of the larval development (delayed metamorphosis). More studies examining the reversibility of plastic defences, including other type of costs (e.g. physiological), are needed to better understand the adaptive value of these flexible strategies.     

Effects of starvation on larval growth, survival, and metamorphosis of Manila clam Ruditapes philippinarum

The effects of starvation on larval growth, survival, and metamorphosis of Manila clam Ruditapes philippinarum at the temperature of 19.6–21.6 °C, the salinity of 34‰ and pH of 8.0 were investigated from May 18 to July 18, 2006. In this study, the early, middle and late umbo-veliger larvae with the shell lengths of 100, 140, and 190 μm were subject to temporary food deprivation for up to 4.5, 20, and 25d at 0.5, 4, 5d intervals, followed by refeeding for the remaining of a 24, 20, 25d period, respectively. The results suggested that the larvae should have shown considerable tolerance to starvation due to their endogenous and exterior nutrition material, for larvae and time to the point-of-no-return (PNR: the threshold point during starvation after which larvae could no longer metamorphose even if food is provided) were calculated to be 4.25, 17.54, and 22.17d. As the starvation period prolonged, the mean shell length of larvae starved got close to constants at 1.5, 4, and 15d after starvation, which were different for larvae at different stages when starvation began, survival of larvae decreased, and was lower in treatments starved earlier in development than those starved later, for the early, middle and late umbo-veliger larvae, after 4.5, 20 and 25d of starvation period, few larvaes were alive. After starvation period, the alive larvaes were able to metamorphose and had a capability of compensatory growth when refeeding was given. Starvation not only affected metamorphosis rate, but also caused the delay in the time to metamorphosis and the decrease in the metamorphosed sizes. For example, for the continuously-fed larvae, duration to metamorphosis was 20.7d, for larvae with a size of 100-μm starved for up to 4d, larvae with a size of 140-μm starved for up to 16d, larvae with a size of 190-μm starved for up to 20d, duration to metamorphosis were 29.7, 31.7, and 37.7d, the delay in duration to metamorphosis were 9, 11, and 17d, respectively. Furthermore, importance of nutrition material for maintaining larval survival during starvation and the compensatory growth on larvae at the same feeding time were discussed.     

Effects of early resource limitation and compensatory growth on lifetime fitness in the ladybird beetle (Harmonia axyridis)

Acceleration of growth following a period of diet restriction may result in either complete or partial catch-up in size. The existence of such compensatory growth indicates that organisms commonly grow at rates below their physiological maxima and this implies a cost for accelerated growth. We examined patterns of accelerated growth in response to temporary resource limitation, and assayed both short and long-term costs of this growth in the ladybird beetle Harmonia axyridis. Subsequent to the period of food restriction, accelerated growth resulted in complete compensation for body sizes, although we observed greater larval mortality during the period of compensation. There were no effects on female fecundity or survivorship within 3 months of maturation. Females did not discriminate against males that had undergone compensatory growth, nor did we observe effects on male mating behaviour. However, individuals that underwent compensatory growth died significantly sooner when deprived of food late in adult life, suggesting that longer-term costs of compensatory growth may be quite mild and detectable only under stressful conditions.     

Growth and survival rate of the larvae ofHynobius nebulosus Tokyoensis Tago (Amphibia,Hynobiidae)

Growth and population density of the larvae, Hynobius nebulosus tokyoensisTago , were estimated in a small pond within the study site settled in Habu village of Hinodemachi, a suburb of Tokyo City, during the period from 1975 to 1980. The mortality factors which influenced the survival rate of larvae were also evaluated from the ecological point of view. Laboratory experiments on the growth of larvae and predation by newts were conducted in pararell with the field survey. The results showed that growth rate of larvae under the natural condition was very slow, as compared with that under the laboratory condition with sufficient food supply, and mean body size at metamorphosis was negatively correlated with the density at that time. This suggested that food resources were in short supply in the pond, and there occurred a severe intraspecific competition for food among larvae. The mortality rate of larvae was so high, 80–99% in each year, and the density of larvae survived until metamorphosis varied so greatly from year to year that the larval stage was the most important stage throughout the life cycle to the maintenance of a population for this salamander. The most important factors which contributed to this high mortality were the predation by the newt, Triturus pyrrhogaster pyrrhogasterBoie , and cannibalism. From the laboratory experiment, it was found that predators could attack only small larvae successfully, and successful attack rate decreased sharply as larvae grew larger. This relationship resulted in the characteristic L-shaped pattern of survivorship curve of larvae; that is, heavy mortality just after hatching period.     

Reconstructing larval growth and habitat use in an amphidromous goby using otolith increments and microchemistry

High‐resolution analysis of growth increments, trace element chemistry and oxygen isotope ratios (δ¹⁸O) in otoliths were combined to assess larval and post‐larval habitat use and growth of Awaous stamineus, an amphidromous goby native to Hawai‘i. Otolith increment widths indicate that all individuals experience a brief period of rapid growth during early life as larvae and that the duration of this growth anomaly is negatively correlated with larval duration. A protracted high‐growth period early in larval life is associated with a lower ratio of Sr:Ca, which may reflect low salinity conditions in nearshore habitats. A distinct shift in δ¹⁸O (range: 4–5‰) is closely associated with the metamorphic mark in otoliths, indicating that larval metamorphosis occurs promptly upon return to fresh water. Strontium and other trace elements are not as tightly coupled to the metamorphosis mark, but confirm the marine‐to‐freshwater transition. Integration of microstructural and microchemical approaches reveals that larvae vary substantially in growth rate, possibly in association with habitat differences. Although time and financial costs make it difficult to achieve large sample sizes, present results show that examining even a small number of individuals can lead to novel inferences about early life history in diadromous fishes and illustrates the value of integrating analyses.     

Patterns of natural selection on size at metamorphosis in water frogs

Strategies for optimal metamorphosis are key adaptations in organisms with complex life cycles, and the components of the larval growth environment causing variation in this trait are well studied empirically and theoretically. However, when relating these findings to a broader evolutionary or ecological context, usually the following assumptions are made: (1) size at metamorphosis positively relates to future fitness, and (2) the larval growth environment affects fitness mainly through its effect on timing of and size at metamorphosis. These assumptions remain poorly tested, because data on postmetamorphic fitness components are still rare. We created variation in timing of and size at metamorphosis by manipulating larval competition, nonlethal presence of predators, pond drying, and onset of larval development, and measured the consequences for subsequent terrestrial survival and growth in 1564 individually marked water frogs (Rana lessonae and R. esculenta), raised in enclosures in their natural environment. Individuals metamorphosing at a large size had an increased chance of survival during the following terrestrial stage (mean linear selection gradient: 0.09), grew faster and were larger at maturity than individuals metamorphosing at smaller sizes. Late metamorphosing individuals had a lower survival rate (mean linear selection gradient: -0.03) and grew more slowly than early metamorphosing ones. We found these patterns to be consistent over the three years of the study and the two species, and the results did not depend on the nature of the larval growth manipulation. Furthermore, individuals did not compensate for a small size at metamorphosis by enhancing their postmetamorphic growth. Thus, we found simple relationships between larval growth and postmetamorphic fitness components, and support for this frequently made assumption. Our results suggest postmetamorphic selection for fast larval growth and provide a quantitative estimate for the water frog example.     

Development, growth, and egg production of Ageneotettix deorum (Orthoptera: Acrididae) in response to spider predation risk and elevated resource quality

Abstract.  1. Predation risk to insects is often size- or stage-selective and usually decreases as prey grow. Any factor, such as food quality, that accelerates developmental and growth rates is likely to reduce the period over which prey are susceptible to size-dependent predation.
2. Using field experiments, several hypotheses that assess growth, development, and egg production rates of the rangeland grasshopper Ageneotettix deorum (Scudder) were tested in response to combinations of food quality and predation risk from wolf spiders to investigate performance variation manifested through a behaviourally mediated path affecting food ingestion rates.
3. Grasshoppers with nutritionally superior food completed development ≈ 8–18% faster and grew 15–45% larger in the absence of spiders, in comparison with those subjected to low quality food exposed to spider predators. Growth and development did not differ for grasshoppers feeding on high quality food when predators were present in comparison with lower quality food unimpeded by predators. Responses indicated a compensatory relationship between resource quality and predation risk.
4. Surviving grasshoppers produced fewer eggs compared with individuals not exposed to spiders. Because no differences were found in daily egg production rate regardless of predation treatment, lower egg production was attributed to delayed age of first reproduction. Results compare favourably with responses observed in natural populations.
5. Risk of predation from spiders greatly reduced growth, development, and ultimately egg production. Increased food quality counteracts the impact of predation risk on grasshoppers through compensatory responses, suggesting that bottom-up factors mediate effects of spiders.     

The relationship among egg size,density and food level on larval development in the wood frog (Rana sylvatica)

Summary Although inter- and intraspecific variation in egg size among amphibians has been well documented, the relationship between egg size and fitness remains unclear. Recent attempts to correlate egg size intraspecifically with larval developmental patterns have been equivocal. In this study the development of larvae derived from large eggs and small eggs, from a single population in Maryland were compared under a range of food levels and larval population densities. Both food level and density had significant effects on the length of the larval period and size at metamorphosis. However, the response among larvae derived from different egg sizes was not additive. At low densities and high food levels, larvae from small eggs had longer larval periods and a larger size at metamorphosis than larvae derived from large eggs. In contrast, at high densities larvae from small eggs had longer developmental periods but were smaller at metamorphosis than larvae from large eggs. In addition, larvae from small eggs were more sensitive to density irrespective of food level. These results suggest that optimal egg size is correlated with environmental factors, which may explain the maintenance of both geographic and within population variation in egg size commonly observed in amphibians.     

Size compensation in moth larvae: attention to larval instars

Environmental perturbations such as starvation and poor diet often prevent animals from attaining their optimal sizes. When the perturbation has a transient character, compensatory responses are expected in terms of faster growth or a prolonged developmental period. In the case of insect larvae, details of such responses are insufficiently known at the proximate level. Attention to responses at the level of particular larval instars should promote an understanding of insect developmental plasticity also in a more general context. To provide an instar‐specific analysis of compensatory growth, larvae of the moth Orgyia antiqua (L.) are reared on inferior diet during one larval instar. Responses in growth parameters are recorded in the course of the manipulated instars, as well as at the level of the entire larval period. The negative relationship between development time and size in response to the inferior food quality, typical of the entire larval periods, is also observed within the manipulated instars taken separately. The manipulated larvae remain smaller than the larvae of the control group (significant in males only), even by the end of the subsequent instar during which all individuals are provided with superior host. In males, close to full size compensation by the time of pupation is achieved only by means of adding an extra larval instar. The inability of larvae to fully compensate during one and even two instars is considered as an indication of the presence of constraints on the within‐instar growth pattern. An alternative, adaptational explanation for the incomplete compensation could be based on the cost of prolonged development period. Given the ecological context of the species' life history, such an explanation appears less likely.     

Physiological effects of compensatory growth during the larval stage of the ladybird,Cryptolaemus montrouzieri

The growth rate of insects may vary in response to shifty environments. They may achieve compensatory growth after a period of food restriction followed by ad libitum food, which may further affect the reproductive performance and lifespan of the resulting phenotypes. However, little is known about the physiological mechanisms associated with such growth acceleration in insects. The present study examined the metabolic rate, the antioxidant enzyme activity and the gene expression of adult Cryptolaemus montrouzieri (Coleoptera: Coccinellidae) after experiencing compensatory growth during its larval stages. Starved C. montrouzieri individuals achieved a similar developmental time and adult body mass as those supplied with ad libitum food during their entire larval stage, indicating that compensatory growth occurred as a result of the switch in larval food regime. Further, the compensatory growth was found to exert effects on the physiological functions of C. montrouzieri, in terms of its metabolic rates and enzyme activities. The adults undergoing compensatory growth were characterized by a higher metabolic rate, a lower activity of the antioxidant enzymes glutathione reductase, catalase, and superoxide dismutase and a lower gene expression of P450 and trehalase. Taken together, the results indicate that although compensatory growth following food restriction in early larval life prevents developmental delay and body mass loss, the resulting adults may encounter physiological challenges affecting their fitness.     

Food availability controls the onset of metamorphosis in the dung beetle Onthophagus taurus (Coleoptera: Scarabaeidae)

In nature, larvae of the dung beetle Onthophagus taurus (Schreber 1759) are confronted with significant variation in the availability of food without the option of locating new resources. Here we explore how variation in feeding conditions during the final larval instar affects larval growth and the timing of pupation. We found that larvae respond to food deprivation with a reduction in the length of the instar and premature pupation, leading to the early eclosion of a small adult. To achieve pupation, larvae required access to food for at least the first 5 days of the final instar (= 30% of mean third‐instar duration in control individuals), and had to exceed a weight of 0.08 g (= 58% of mean peak weight in control individuals). Larvae that were allowed to feed longer exhibited higher pupation success, but increased larval weight at the time of food deprivation did not result in increased pupation success except for larvae weighing > 0.14 g. Larvae responded to food deprivation by initiating and undergoing the same sequence of developmental events, requiring the same amount of time, as ad libitum‐fed larvae once those had reached their natural peak weight. Our results reveal a striking degree of flexibility in the dynamics and timing of larval development in O. taurus. They also suggest that premature exhaustion of a larva's food supply can serve as a cue for the initiation of metamorphosis. Premature metamorphosis in response to food deprivation has been documented in amphibians, but this is, to the best of our knowledge, the first time such a behaviour has been documented for a holometabolous insect. We discuss our findings in the context of the natural history and behavioural ecology of onthophagine beetles.     

Relationships between larval nutritional experience, larval growth rates, juvenile growth rates, and juvenile feeding rates in the prosobranch gastropod Crepidula fornicata

Planktonic larvae experiencing short periods of starvation or reduced food supply often grow and develop more slowly, have poor survival, fail to metamorphose, metamorphose at smaller sizes, or grow slowly as juveniles. In this study, we examined the impact of short periods of food limitation at various stages of larval development on larval and juvenile growth in Crepidula fornicata. In addition, we considered whether juveniles that were stressed as larvae grew poorly because of reduced rates of food collection due to impaired gill function. For 5 experiments, larvae were either starved for several days beginning within 12 h of hatching or were starved for the same number of days following 1 or more days of feeding at full ration (cells of the naked flagellate Isochrysis galbana, clone T-ISO, at 18×10⁴ cells ml⁻¹). In one experiment, larvae were transferred for 2 or 4 days to seawater with extremely low phytoplankton concentration (1×10⁴ cells ml⁻¹). In all experiments, larvae were returned to full ration following treatment. Control larvae were fed full ration from hatching to metamorphosis. When larvae reached shell lengths of about 900 μm they were induced to metamorphose and then reared individually at full ration in glass bowls, with phytoplankton suspension replenished daily. Larval and juvenile growth rates were determined by measuring changes in shell length (longest dimension) over time. Juvenile feeding rates were determined by monitoring changes in phytoplankton concentration over 2–3 h at the end of the growth rate determinations. In general, larval growth rates for the first 2 days after the resumption of feeding were inversely proportional to the length of time that larvae were starved. However, larval growth rates ultimately recovered to control levels in most treatments. Starving the larvae caused a significant reduction in initial juvenile growth rates (first 3–4 days post-metamorphosis) in most experiments even when larval growth rates had recovered to control levels prior to metamorphosis. Juvenile growth rates were not significantly reduced when larvae were subjected to reduced food availability (1×10⁴ cells ml⁻¹), even for treatments in which larval growth rates were compromised. Mean weight-specific filtration rates for juveniles were significantly reduced (p<0.05) following larval feeding experience in only one or possibly 2 of the 4 experiments conducted. Our data suggest that although larvae of C. fornicata may fully recover from early nutritional stress, the resulting juveniles may exhibit poor initial growth due to impaired gill function, reduced digestive capability, or reduced assimilation efficiency.     

Models of metamorphic timing: an experimental evaluation with the pond-dwelling salamander Hemidactylium scutatum (Caudata: Plethodontidae)

Amphibian larvae vary tremendously in size at metamorphosis and length of larval period. We raised pond-dwelling four-toed salamander (Hemidactylium scutatum) larvae to test two models that predict a larva’s age and size at metamorphosis. The Wilbur-Collins model proposes that the developmental rate of a larva responds to changes in growth rate in an adaptive manner throughout the larval period, and that metamorphosis can be initiated after a minimum size has been reached. The Leips-Travis or fixed-rate model states that developmental rate is set early in the larval period, perhaps by early growth rate or food availability and their positive correlation with developmental rate, and that changes in growth rate during the larval period affect size at metamorphosis, but have no effect on the age of an individual at metamorphosis. A modified version of the Wilbur-Collins model suggests that a larva’s developmental rate becomes fixed about two-thirds of the way through the larval period, with changes in growth rate after that point only affecting size at metamorphosis. Larvae were raised on eight different feeding regimes which created two constant and six variable growth histories. Growth history did significantly affect size at metamorphosis. However, an a posteriori statistical test revealed a group of seven and an overlapping group of six treatments with indistinguishable lengths of larval period, indicating a general picture of a fixed developmental rate regardless of growth history. This result is unique among similar studies on invertebrates, fish, and frogs. There was no association between early growth or food level and development rates. Neither the Wilbur-Collins nor the Leips-Travis fixed-rate models were supported. The invariable developmental rate of Hemidactylium and recent osteological evidence from the literature suggest that larvae begin the process of metamorphosis as soon as they hatch, probably a trait selected for by strong predation pressure in the aquatic environment. A variety of different approaches (ecological, developmental, phylogenetic) are necessary to fully evaluate the adaptive nature of the timing of transitions between life cycle stages. Received: 3 June 1999 / Accepted: 18 March 2000