Irreversibility of a bad start: early exposure to osmotic stress limits growth and adaptive developmental plasticity (original) (raw)
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Full compensation of growth in salt‐tolerant tadpoles after release from salinity stress
Journal of Zoology, 2017
The benefit of compensatory growth is to minimize the negative effects of stress experienced by organisms early in development once the conditions improve. Tadpoles of crab-eating frog Fejervarya cancrivora are euryhaline, have the highest salt tolerance among reported anuran species and may exhibit a different pattern of compensatory growth after stress release. We examined how F. cancrivora tadpoles responded and possibly recovered from salinity stresses. Specifically, we tested whether tadpoles expressed compensatory growth, what degree of compensation they expressed after release from salinity stress and whether the stage at and duration during which they experienced salt stress influenced the size at and time to metamorphosis of tadpoles. We found that the effects of salinity stress on the growth and development of tadpoles are quite different between early and late exposure to high salinity (LHH vs. LLH). Exposure to high salinity late in development (LLH) reduced growth but not the rate of development, resulting in smaller metamorphs but a similar time to metamorphosis when compared to the control treatment (LLL). By contrast, exposure to high salinity early in development (LHH) retarded rates of growth and development of tadpoles, but the resulting prolonged larval period enabled tadpoles to catch up and reach similar metamorphic sizes to LLL treatment metamorphs. Most importantly, tadpoles released from salinity stress (LHL) exhibited similar time to and size at metamorphosis when compared to the LLL tadpoles, suggesting that they can exhibit full compensation of growth. Compensatory growth may be a useful mechanism for F. cancrivora tadpoles inhabiting brackish habitats, allowing them to overcome the effects of dramatically increased salt levels by expressing catch-up growth when the salt stress ceases.
Compensatory growth in tadpoles after transient salinity stress
Marine and Freshwater Research, 2010
Many freshwater habitats worldwide are being degraded by an anthropogenic increase in salinity. Although salt concentrations are known to fluctuate with variable freshwater inflows, we know little about what effects this may have on freshwater organisms. Using a species of frog, Litoria ewingii, we measured tadpole growth both during and after salt stress to determine their capacity to compensate or recover from this stress. During exposure to ecologically relevant concentrations of salt (5%, 10% and 15% seawater), tadpoles grew slower and were significantly smaller than those in our freshwater control (0.4% seawater). Upon return to fresh water, previously salt-exposed tadpoles grew faster than those in the control group, and by the eighth day of the 'recovery' period, no longer differed significantly in size. The results of our study demonstrate a capacity for tadpoles to compensate for a period of environmental stress by temporarily increasing growth rate when the stress abates.
Zoological Science, 2009
We studied salinity tolerance and the effects of salinity on growth, development, and metamorphosis in Fejervarya limnocharis tadpoles living in brackish water. Specifically, we examined whether tadpoles exhibit adaptive plasticity in development when exposed to different salinities. Tadpoles collected on Green and Orchid Islands off Southeastern Taiwan were assigned to salinities of 0, 3, 5, 7, 9, 11, and 13 parts per thousand (ppt). The daily survival, weekly growth, and development of tadpoles were recorded until metamorphosis. More than 50% of tadpoles survived in 9 ppt for over a month, and a few individuals survived in 11 ppt for 20 days, suggesting that F. limnocharis tadpoles tolerate salinity better than the tadpoles of most species studied to date. Tadpoles at 9 ppt had lower survivorship, and retarded growth and development (from Gosner stage 26 to 35) compared to the other treatments. Tadpoles metamorphosed early at a smaller size as salinity increased, suggesting the existence of adaptive developmental plasticity in F. limnocharis in response to osmotic stress. Phenotypic plasticity in the age and size at metamorphosis in response to salinity may provide a means for tadpoles to adapt to the unpredictable salinity variation in coastal rock pools.
Salinity tolerance in Pelobates fuscus (Laurenti, 1768) tadpoles (Amphibia: Pelobatidae)
We investigated the effect of salinity on larval development and survival rate to metamorphosis in the common spadefoot toad Pelobates fuscus (Laurenti, 1768). Our hypothesis was that higher salinity would decrease tadpole survival rate and body size at metamorphosis, and delay metamorphosis. The response of the tadpoles was evaluated through an experimental design with three salinity treatments of 2, 4, and 8‰ compared to a control (deionized water). Survival varied across the treatments: neither of the tadpoles in 8‰ salinity treatment survived the experiment, nor achieved metamorphosis. Salinity levels of 2 and 4‰ had no significant influence on the mean time to metamorphosis, body mass and SVL at metamorphosis. Our results suggest that P. fuscus tadpoles have a tolerance threshold for brackish water up to 4‰, above which survival is impaired.
Journal of experimental zoology. Part A, Ecological genetics and physiology, 2014
Salinity in affected freshwater ecosystems fluctuates with seasonal rainfall, tidal flux, rates of evaporation, chemical runoff and the influence of secondary salinization. Environmental stressors such as salinity can have lasting effects on anuran development, yet little is known about the effects of fluctuating salinity on tadpole ontogeny or the effects of differing magnitudes of salinity exposure, as would occur in natural wetland systems. We examined how salinity fluctuations affected survival, growth and development of Litoria ewingii by exposing tadpoles to a range of salinity concentrations (5.6-10.85 ppt) at three different stages of development (hind limb-bud formation; toe differentiation and forearm development). We also investigated the plasticity of tadpole growth rates in response to non-lethal, transient salinity influxes, specifically examining the capacity for compensatory growth and its relationship to the timing, magnitude or frequency of salinity exposure. Our r...
Developmental and Evolutionary History Affect Survival in Stressful Environments
PLoS ONE, 2014
The world is increasingly impacted by a variety of stressors that have the potential to differentially influence life history stages of organisms. Organisms have evolved to cope with some stressors, while with others they have little capacity. It is thus important to understand the effects of both developmental and evolutionary history on survival in stressful environments. We present evidence of the effects of both developmental and evolutionary history on survival of a freshwater vertebrate, the rough-skinned newt (Taricha granulosa) in an osmotically stressful environment. We compared the survival of larvae in either NaCl or MgCl 2 that were exposed to salinity either as larvae only or as embryos as well. Embryonic exposure to salinity led to greater mortality of newt larvae than larval exposure alone, and this reduced survival probability was strongly linked to the carry-over effect of stunted embryonic growth in salts. Larval survival was also dependent on the type of salt (NaCl or MgCl 2) the larvae were exposed to, and was lowest in MgCl 2 , a widely-used chemical deicer that, unlike NaCl, amphibian larvae do not have an evolutionary history of regulating at high levels. Both developmental and evolutionary history are critical factors in determining survival in this stressful environment, a pattern that may have widespread implications for the survival of animals increasingly impacted by substances with which they have little evolutionary history.
Environmental deterioration increases tadpole vulnerability to predation
Biology Letters, 2008
Human-induced environmental change is occurring at an unprecedented rate and scale. Many freshwater habitats, in particular, have been degraded as a result of increased salinity. Little is known about the effects of anthropogenic salinization on freshwater organisms, especially at sublethal concentrations, where subtle behavioural changes can have potentially drastic fitness consequences. Using a species of Australian frog (Litoria ewingii ), we experimentally examined the effects of salinization on tadpole behaviour and their vulnerability to a predatory dragonfly nymph (Hemianax papuensis). We found that tadpoles exposed to an ecologically relevant concentration of salt (15% seawater, SW) were less active than those in our freshwater control (0.4% SW). Tadpoles in elevated salinity also experienced a higher risk of predation, even though the strike rate of the predator did not differ between salt and freshwater treatments. In a separate experiment testing the burstspeed performance of tadpoles, we found that tadpoles in saltwater were slower than those in freshwater. Thus, it would appear that salt compromised the anti-predator response of tadpoles and made them more susceptible to being captured. Our results demonstrate that environmentally relevant concentrations of aquatic contaminants can, even at sublethal levels, severely undermine the fitness of exposed organisms.
Environmental stress and the costs of whole-organism phenotypic plasticity in tadpoles
Journal of Evolutionary Biology, 2007
Costs of phenotypic plasticity are important for the evolution of plasticity because they prevent organisms from shaping themselves at will to match heterogeneous environments. These costs occur when plastic genotypes have relatively low fitness regardless of the trait value expressed. We report two experiments in which we measured selection on predator-induced plasticity in the behaviour and external morphology of frog tadpoles (Rana temporaria). We assessed costs under stressful and benign conditions, measured fitness as larval growth rate or competitive ability and focused analysis on aggregate measures of whole-organism plasticity. There was little convincing evidence for a cost of phenotypic plasticity in our experiments, and costs of canalization were nearly as frequent as costs of plasticity. Neither the magnitude of the cost nor the variation around the estimate (detectability) was sensitive to environmental stress.
Pond drying cues and their effects on growth and metamorphosis in a fast developing amphibian
The hydroperiod of breeding habitats imposes a strong selection on amphibians and pond-breeding species usually exhibit a high degree of plasticity in the duration of larval period. However, the potential for phenotypic plasticity in fast developing species was investigated only in a small number of anurans, and the specific response to environmental cues such as low water versus decreasing water level, as well as the effects of such cues on particular developmental stages, are even less understood. In this context, we investigated the plastic response to pond desiccation in a neotropical species (Ceratophrys stolzmanni) by raising tadpoles in three water level treatments: constant high, constant low, and decreasing. The growth rates were the highest reported for amphibian tadpoles (up to 0.3 g day À1) and the time to metamorphosis was short in all treatments, with the fastest developing tadpole metamorphosing in only 16 days after egg deposition. Individuals from the constant high water level treatment had a higher growth rate than those in the other two treatments, whereas decreasing and constant low water levels had similar effects on development, speeding up metamorphosis. In turn, this involved a cost as these tadpoles had a lower body size and mass at metamorphosis than the ones raised in constant high water levels. The final stages of metamorphosis, when tadpoles are the most vulnerable, were shorter in tadpoles exposed to a decreasing water level, allowing them to leave water quickly. Our experiment demonstrates that phenotypic plasticity is maintained even in environments devoid of permanent aquatic habitats. Ceratophryd tadpoles are able to shorten their developmental time when they perceive a risk of desiccation and react similarly to cues coming from the two unfavorable water conditions showing their adaptation to ephemeral and unpredictable breeding habitats.
Aquaculture Reports, 2019
This experiment was conducted to know the effects of salinity stress on the early life stages of zebrafish (Danio rerio). The objectives were evaluated by varying all combinations of developmental stages of zebrafish embryos exposing to a salinity gradient. The results demonstrated that zebrafish embryos (2 to 4-cell stage) could survive to hatching at 2 ppt (hatching rate 54.5%) but lowered at 4 ppt (hatching rate 23.5%). Acute exposure to 2 to 4cell stage embryos for 60 and 120 min to different salinities (i.e., 0, 6, 8, 10, and 12 ppt) and then returned to freshwater (0 ppt) could hatch up to 8 ppt only at 60 min but not at 120 min exposures to embryos. The hatching rate was 14.5% and it took 20 h more times to hatch compared to control (0 ppt). While blastula stage exposed to 8 and 10 ppt salinities for 60 min, the hatching success was 59% and 36%, respectively. Although gastrula stage embryos were able to develop at 12 ppt salinity kept for 60 min the hatching success was markedly reduced (20.5%). Tolerance to salinity increased from advancing stages of development, i.e. the gastrulae were more tolerant of salinity change than the blastulae and the blastulae were more tolerant than the cleaving embryos. It is concluded that with the increasing salinities, the chances of embryogenesis and the survival of eggs decreased. In addition, tolerance to salinity increased from advanced stages of development.