Temperature-dependent rate of clutch production in a tropical lizard (Paroedura picta: Gekkonidae): Intraspecific test of the metabolic theory of ecology

Recently, a general model based on scaling of metabolic rate and reaction kinetics that predicts dependence of various biological rates on temperature and body size has been proposed as a core of the “Metabolic Theory of Ecology” (MTE). However, its thermal component has been rarely explicitly tested and its usefulness for prediction of thermal effect on key life-history traits such as reproductive rate and hence fitness is still questionable. Here, we tested its applicability to temperature-dependent rate of clutch production in a tropical gecko. The thermal effects on reproductive rates in reptiles are only poorly known and difficult to estimate, because most species lay clutches largely infrequently. Females of the Madagascar ground gecko (Paroedura picta) lay clutches in unusually short intervals, which allowed us to use this species as a model for estimation of dependence of rate of clutch production on temperature. We kept adult females at three constant temperatures (24, 27, 30 °C) and recorded their reproductive characteristics. Increasing temperature positively influences rate of clutch production, but in a manner not predicted by a simple model of reaction kinetics. The results in P. picta suggest that predictions of fitness consequences of shifts in thermal environment can be more complicated than expected under the general relationship of the MTE.     

Maternal thermoregulation influences offspring viability in a viviparous lizard

Gravid females of the viviparous scincid lizard Eulamprus heatwolei were maintained in the laboratory, with some females allowed to bask for 8 h/day and others for only 2 h/day. Maternal basking regimes influenced the gestation period, and significantly affected the body shapes, activity levels and running speeds of the offspring born to these females. Neonates from females with lesser basking opportunities were relatively short and fat, were very active, and were relatively fast runners. Effects of the embryos' thermal regime on the young lizards' morphology and running speed were still detectable two months after birth. Thus, much of the morphological and behavioral variation among neonatal reptiles may arise from phenotypically plastic responses to the thermal environments experienced during embryonic development, rather than from heritable genetic differences among individuals. Hence, selection on maternal thermoregulatory behavior may be an important avenue for adaptive modifications to neonatal phenotypes in reptiles.     

Environmental effects on variation and covariation in reproductive traits of Western Bluebirds

Summary Environmental conditions can influence the expression and correlations of phenotypic traits. I studied phenotypic plasticity in reproductive traits of Western Bluebirds breeding in northern Arizona. Data collected over 4 years on two contrasting habitats identified significant spatial and temporal variation in bluebird reproduction. Clutch size was similar over different environmental conditions whereas timing of clutch initiation, percent fledging success, and frequency of second nest attempts were flexible. Correlations between traits varied widely—often changing sign—among samples from different years or habitats. Correlations of traits with reproductive success were also dependent on environmental conditions. Variation in traits reflected behavioral responses by nesting adults to differences in time for breeding and feeding conditions. Density of trees differed between habitats and had opposing effects on these environmental variables; breeding seasons were generally longer, but feeding rates to nestlings were lower on the more open habitat. Late Spring snows delayed reproduction and increased the importance of limited time for breeding; feeding conditions were more influential following a dry Spring. This and other studies illustrate that data on phenotypic plasticity are important when evaluating the ecological and evolutionary forces underlying life histories.     

Effects of temperature on reproductive output, egg provisioning, juvenile hormone and vitellogenin titres in the butterfly Bicyclus anynana

Environmentally induced phenotypic plasticity is common in nature. Hormones, affecting multiple traits and signaling to a variety of distant target tissues, provide a mechanistic link between environments, genes and trait expression, and may therefore well be involved in the regulation phenotypic plasticity. Here, we investigate whether in the tropical butterfly Bicyclus anynana temperature-mediated plasticity in egg size and number, with fewer but larger eggs produced at lower temperatures and vice versa, is under control of juvenile hormone, and whether different temperatures cause differences in egg composition. Female B. anynana butterflies showed the expected response to temperature, however, we found no evidence for an involvement of juvenile hormone. Neither haemolymph JH II and JH III titres nor vitellogenin levels differed across temperatures. The smaller eggs produced at the higher temperature contained relatively higher amounts of water, free carbohydrates and proteins, but relatively lower amounts of lipids. While these smaller eggs had a lower absolute energy content, total reproductive investment was higher at the higher temperature (due to a higher fecundity). Overall, our study indicates that temperature-mediated plasticity in reproduction in B. anynana is mechanistically related to a biophysical model, with oocyte production (differentiation) and oocyte growth (vitellogenesis) having differential temperature sensitivities.     

An experimental study of the effects of weed invasion on lizard phenotypes

We examined how a weed affected the basking and activity of a diurnal lizard, and the potential cascading effects of these shifts for life history strategies and expression of morphology. Hatchlings of the diurnal lizard Lampropholis delicata were raised to maturity in outdoor enclosures that mimicked high, moderate and low invasion by a sprawling plant (blue periwinkle, Vinca major). Skinks depend on sunlight for growth and maintenance. Periwinkle differs from displaced grassland by being structurally complex and blocking sunlight. Lizards restricted to the enclosure floor achieved preferred body temperatures only when exposure to periwinkle was moderate or low. However, lizards in high invasion enclosures could reach preferred body temperatures by climbing plants and basking on exposed canopy. This shift in basking strategy resulted in lizards growing longer hind limbs compared with animals that rarely (moderate invasion) and never (low invasion) climbed plants. Consequently, lizards reared in high invasion enclosures sprinted faster than conspecifics reared in lower invasion environments. Throughout the study there was no significant variation among treatments in the tendency of animals to be moving when they were not hidden. However, lizards in high invasion treatments hid more often during the day, were lighter in body mass, and females had lighter clutch masses and offspring than did those from moderate and low invasion enclosures. Thus, microhabitat degradation can drive a cascade of changes to an animal’s ecology.     

Effects of temperature and salinity on the life history of the sailfin molly (Pisces: Poeciliidae): lipid storage and reproductive allocation

While the life history traits of animals usually exhibit substantial phenotypic plasticity, such plasticity might reflect either a simple alteration in the level of energy accrual and use or a genuine shift in energy allocation tactics between environmental conditions. The latter would represent genuine plasticity in the life history itself, and thus it is important to distinguish which of these two processes underlies the observed plasticity of life history traits. We investigated this issue by examining the effects of temperature and salinity variation during ontogeny on the allocation of biomass and lipid storage in male sailfin mollies, Poecilia latipinna. We raised males from four natural populations from birth to maturity in controlled laboratory conditions. Neither distinct temperatures (23 or 29°C) nor different salinity regimes (2, 12, or 20 parts per thousand) affected body mass, although males from different populations differed substantially in body mass. However, males raised at the higher temperature had a greater allocation of biomass to testis and a lower allocation to viscera mass. The amount of stored lipid was altered by temperature variation but the direction and magnitude of the effect varied substantially among males from the different populations. Salinity variation affected neither biomass allocation nor the level of lipid storage. These results indicate that male mollies possess a flexible developmental program with respect to temperature that canalizes body size and alters the allocation of biomass among competing demands for reproductive readiness and capacity for energy storage. Received: 25 November 1996 / Accepted: 1 December 1997     

Life-history traits of the lizard Sceloporus undulatus from two populations raised in a common laboratory environment

Hatchling Sceloporus undulatus elongatus from Washington Co., Utah and S. u. garmani from Woods Co., Oklahoma were raised to maturity and reproduction under identical laboratory conditions with ad libitum food availability. Growth, allometry, age and size of maturity, clutch size and egg mass were compared among lab-raised cohorts from the two populations, among lab-raised and field-caught animals (including their field-caught mothers) and, for growth, with values obtained by previously published field studies on the same or nearby populations. For all traits population differences observed in previous field studies and current field samples resulted from both a plastic response to proximate environmental conditions and intrinsic (possibly genetic) difference. The most plastic traits were growth and age of maturity. Cohorts from both populations expressed the ability to mature in less than 6 months in the laboratory but only the S.u. garmani express early maturity in the field. Allometric differences generated during growth in the lab were not observed in field samples but may reflect an adaptive physiological difference. The least plastic trait was egg mass. The only trait for which the rank order of the difference in the field was reversed in the lab was growth rate. S.u. elongatus grew significantly faster than S.u. garmani in the lab but much slower in the field. The tendency of S.u. garmani females to breed at minimum size of maturity may be greater than that of S.u. elongatus.     

Thermal and reproductive biology of high and low elevation populations of the lizard Sceloporus scalaris: implications for the evolution of viviparity

Viviparity in squamate reptiles is presumed to evolve in cold climates by selection for increasingly longer periods of egg retention. Longer periods of egg retention may require modifications to other reproductive features associated with the evolution of viviparity, including a reduction in eggshell thickness and clutch size. Field studies on the thermal and reproductive biology of high (HE) and low (LE) elevation populations of the oviparous lizard, Sceloporus scalaris, support these expectations. Both day and night-time temperatures at the HE site were considerably cooler than at the LE site, and the activity period was 2 h shorter at the HE than at the LE site. The median body temperature of active HE females was 2°C lower than that of LE females. HE females initiated reproduction earlier in the spring than LE females, apparently in order to compensate for relatively low temperatures during gestation. HE females retained eggs for about 20 days longer than LE females, which was reflected by differences in the degree of embryonic development at the time of oviposition (stages 35.5–37.0 versus stages 31.0–33.5, respectively). These results support the hypotheses that evolution of viviparity is a gradual process, and is favored in cold climates. Females in the HE population exhibited other traits consistent with presumed intermediate stages in the evolution of viviparity; mean eggshell thickness of HE eggs (19.3 m) was significantly thinner than that of LE eggs (26.6 m) and the size-adjusted clutch sizes of HE females (9.4) were smaller than those of LE females (11.2).     

Maternal effects on phenotypic plasticity in larvae of the salamander <Emphasis Type="Italic">Hynobius retardatus</Emphasis>

Maternal effects are widespread and influence a variety of traits, for example, life history strategies, mate choice, and capacity to avoid predation. Therefore, maternal effects may also influence phenotypic plasticity of offspring, but few studies have addressed the relationship between maternal effects and phenotypic plasticity of offspring. We examined the relationship between a maternally influenced trait (egg size) and the phenotypic plasticity of the induction rate of the broad-headed morph in the salamander Hynobius retardatus. The relationship between egg size and the induction of the broad-headed morph was tested across experimental crowding conditions (densities of low conspecifics, high conspecifics, and high heterospecific anuran), using eggs and larvae from eight natural populations with different larval densities of conspecifics and heterospecifics. The broad-headed morph has a large mouth that enables it to consume either conspecifics or heterospecifics, and this ability gives survival advantages over the normal morph. We have determined that there is phenotypic plasticity in development, as shown by an increase in the frequency of broad-headed morph in response to an increase in the density of conspecifics and heterospecifics. This reaction norm differed between populations. We also determined that the frequency of the broad-headed morph is affected by egg size in which larger egg size resulted in expression of the broad-headed morph. Furthermore, we determined that selection acting on the propensity to develop the broad-headed morph has produced a change in egg size. Lastly, we found that an increase in egg size alters the reaction norm to favor development of the broad-headed morph. For example, an equal change in experimental density produces a greater change in the frequency of the broad-headed morph in larvae developing from large eggs than it does in larvae developing from small eggs. Population differences in plasticity might be the results of differences in egg size between populations, which is caused by the adaptive integration of the plasticity and egg size. Phenotypic plasticity can not evolve independently of maternal effects.     

Energetics of embryonic development: effects of temperature on egg and hatchling composition in a butterfly

Phenotypic plasticity may allow an organism to adjust its phenotype to environmental needs. However, little is known about environmental effects on offspring biochemical composition and turnover rates, including energy budgets and developmental costs. Using the tropical butterfly Bicyclus anynana and employing a full-factorial design with two oviposition and two developmental temperatures, we explore the consequences of temperature variation on egg and hatchling composition, and the associated use and turnover of energy and egg compounds. At the lower temperature, larger but fewer eggs were produced. Larger egg sizes were achieved by provisioning these eggs with larger quantities of all compounds investigated (and thus more energy), whilst relative egg composition was rather similar to that of smaller eggs laid at the higher temperature. Turnover rates during embryonic development differed across developmental temperatures, suggesting an emphasis on hatchling quality (i.e. protein content) at the more stressful lower temperature, but on storage reserves (i.e. lipids) at the higher temperature. These differences may represent adaptive maternal effects. Embryonic development was much more efficient at the lower temperature, providing a possible mechanism underlying the temperature-size rule.     

Plasticity of grasshopper vitellogenin production in response to diet is primarily a result of changes in fat body mass

Life history plasticity is the developmental production of different phenotypes by similar genotypes in response to different environments. Plasticity is common in early post-embryonic or adult development. Later in the developmental stage, the transition from developmentally plastic to canalized (i.e., inflexible) phases is often associated with the attainment of a threshold level of storage. Thresholds are often described simply as total body mass or cumulative consumption of food. The physiological characteristics of thresholds, such as the contributions of the growth of particular organs or the production rate of proteins, are largely unstudied. To address the physiology underlying a threshold-induced developmental transition, total vitellogenin production in response to diet quality in the lubber grasshopper was studied. For individuals that differed in age or dietary protein, somatic mass, ovarian mass, fat body mass, mass-specific vitellogenin production, vitellogenin titer, and storage protein titer were measured. Age and diet strongly affected these parameters, with ovarian mass and fat body mass contributing most to the differences. During mid vitellogenesis, females were highly plastic in response to changing food quality. Only during late vitellogenesis were females unresponsive to changes in food quality. Fat body mass was a more important component of plasticity than was mass-specific vitellogenin production. Because these two variables together make up total vitellogenin production, the greater contribution of fat body mass than mass-specific vitellogenin production suggests that growth factors may be more important than tissue stimulators in producing developmental changes in total vitellogenin production. To our knowledge, this is the first study to demonstrate that mass gain of an organ is more important to developmental plasticity than is the output of that same organ.     

Control theory predictions of reproductive allocation in female dusky salamanders

A model of the reproductive ecology of female dusky salamanders was used to investigate the allocation scheme that a female might use to maximize her reproductive success. Analysis of the model with techniques of optimal control theory suggests that fecundity is maximized either by allocating food resources to reproduction for the entire time period prior to egg laying, or by growing first, then switching to reproduction later in the year. The analysis also indicates that egg mortality will be minimized if the female provides maternal care at the maximum level throughout egg brooding. These results are not specific to dusky salamanders, but can be extended to other organisms with similar reproductive characteristics.     

The effects of water availability on the life history of the desert snail,Trochoidea seetzeni

Summary In the Negev desert of Israel, the pulmonate land snailTrochoidea seetzeni is active, grows and reproduces in the month following the torrential winter rains. Thereafter, these snails estivate until the following year's rains. By experimental supplementation of water in the field, we examined the ability of these snails to alter their life histories. Specifically, we measured changes in feeding activity, overall activity levels, movement patterns and reproductive output. We found that snails on artificially-watered plots stopped feeding on higher plants and fed on soil-surface algae growing as a result of increased water availability. Most snails moved onto the watered plots, and reduced the total amount of movement once there, in response to increased food availability. Snails on the watered plots grew more and remained active for a longer period into the summer months than did snails on control plots. However, we found little evidence for the ability of these snails to alter their reproductive outputs in response to increased water (and hence food) availability. There was also no carry-over effect of high water availability in one season enhancing reproduction in the following season. We postulate that the low level of phenotypic plasticity recorded here is a consequence of an adaptive conservative strategy to maintain a high reproductive output under extremely unpredictable desert conditions.     

Offspring number in a livebearing fish (<Emphasis Type="Italic">Poecilia mexicana</Emphasis>, Poeciliidae): reduced fecundity and reduced plasticity in a population of cave mollies

Life history traits within species often vary among different habitats. We measured female fecundity in mollies (Poecilia mexicana) from a H₂S-rich cave and from a neighbouring surface habitat, as well as in laboratory-reared individuals of both populations raised in either light or continuous darkness. Compared to conspecifics from surface habitats, cave-dwelling P. mexicana had reduced fecundity (adjusted for size) in the field. In the laboratory, the fecundity of surface mollies was higher in light than in darkness, whereas fecundity in the cave mollies was almost unaffected by the ambient light conditions. Our results suggest a heritable component to the reduction in fecundity in female cave mollies. Moreover, the reduced plasticity in fecundity of cave mollies in response to light conditions might be an example of genetic assimilation or channelling of a life history trait in a population invading a new environment.     

Thermal biology,population fluctuations and implications of temperature extremes for the management of two globally significant insect pests

The link between environmental temperature, physiological processes and population fluctuations is a significant aspect of insect pest management. Here, we explore how thermal biology affects the population abundance of two globally significant pest fruit fly species, Ceratitis capitata (medfly) and C. rosa (Natal fruit fly), including irradiated individuals and those expressing a temperature sensitive lethal (tsl) mutation that are used in the sterile insect technique. Results show that upper and lower lethal temperatures are seldom encountered at the field sites, while critical minimum temperatures for activity and lower developmental thresholds are crossed more frequently. Estimates of abundance revealed that C. capitata are active year-round, but abundance declines markedly during winter. Temporal autocorrelation of average fortnightly trap captures and of development time, estimated from an integrated model to calculate available degree days, show similar seasonal lags suggesting that population increases in early spring occur after sufficient degree-days have accumulated. By contrast, population collapses coincide tightly with increasing frequency of low temperature events that fall below critical minimum temperatures for activity. Individuals of C. capitata expressing the tsl mutation show greater critical thermal maxima and greater longevity under field conditions than reference individuals. Taken together, this evidence suggests that low temperatures limit populations in the Western Cape, South Africa and likely do so elsewhere. Increasing temperature extremes and warming climates generally may extend the season over which these species are active, and could increase abundance. The sterile insect technique may prove profitable as climates change given that laboratory-reared tsl flies have an advantage under warmer conditions.     

Predator-induced delayed maturity in bluegill sunfish (Lepomis macrochirus): variation among populations

Previous studies suggested that differences in age at maturity among populations of bluegill sunfish (Lepomis macrochirus) were not genetically based, but rather were a phenotypic response to the presence of predators. I conducted two experiments to determine if the presence of largemouth bass affected age at maturity in bluegill sunfish. Bluegills from three populations were tested to see if the response to the threat of predation varied among source populations. Juvenile bluegills were maintained in the presence of predators or in controls with no contact with predators. Refuge use and growth were monitored during the experiments and reproductive activity was evaluated when bluegills reached age 1. Bluegills from one population exhibited delayed maturity in the presence of predators. Individuals from the other two populations showed no significant differences between predator and control treatments. The population that responded to the presence of predators had a history of high predation levels over the past 30–40 years. The other populations had a history of low levels of predation. This study suggests that presence of predators can induce phenotypic shifts in age at maturity of bluegills, but that the magnitude of response varies among populations in a manner consistent with historical patterns of coexistence. Received: 7 August 1996 / Accepted: 8 August 1997     

Evolution of thermal physiology and growth rate between populations of the western fence lizard (Sceloporus occidentalis)

Summary Hatchling Sceloporus occidentalis from northern populations (central Oregon) grow more slowly than hatchlings from southern populations (southern California) in nature. In this study, I determine whether this difference in growth rate results from differences in thermal environment and/or in thermoregulatory behavior. To determine the degree to which the thermal environment affects growth rate among populations, I reared hatchings from the northern and southern populations in a cycling thermal regime in one of three experimental treatments differing in access to radiant heat (6, 9, or 12 h radiant heat; remainder of 24 h at 15°C). I also measured the body temperature that each individual voluntarily selected over the course of the daily activity cycle. Growth rate varied positively with duration of access to radiant heat. Within the three treatments, individual growth rate was positively correlated with body temperature. Moreover, the difference in growth rate between the northern and southern populations was due in part to differences in behavior — individuals from northern populations selected lower body temperatures. I found that significant variation in body temperature was associated with family membership, suggesting that thermal physiology has a genetic basis. Moreover, growth rate was correlated with body temperature among families in each population suggesting a genetic correlation underlies the phenotypic correlations. Thus, genetically based variation in thermal physiology contributes to differences in growth rate among individuals within a population as well as to differences among populations.     

Developmental plasticity of HPA and fear responses in rats: a critical review of the maternal mediation hypothesis

Developmental plasticity of HPA and fear responses in rats has been proposed to be mediated by environment-dependent variation in active maternal care. Here, we review this maternal mediation hypothesis based on the postnatal manipulation literature and on our own recent research in rats. We show that developmental plasticity of HPA and fear responses in rats cannot be explained by a linear single-factor model based on environment-dependent variation in active maternal care. However, by adding environmental stress as a second factor to the model, we were able to explain the variation in HPA and fear responses induced by postnatal manipulations. In this two-factor model, active maternal care and environmental stress (as induced, e.g., by long maternal separations or maternal food restriction) exert independent, yet opposing, effects on HPA reactivity and fearfulness in the offspring. This accounts well for the finding that completely safe and stable, as well as, highly stressful maternal environments result in high HPA reactivity and fearfulness compared to moderately challenging maternal environments. Furthermore, it suggests that the downregulation of the HPA system in response to stressful maternal environments could reflect adaptive developmental plasticity based on the increasing costs of high stress reactivity with increasingly stressful conditions. By contrast, high levels of environmental stress induced by environmental adversity might constrain such adaptive plasticity, resulting in non-adaptive or even pathological outcomes. Alternatively, however, developmental plasticity of HPA and fear responses in rats might be a function of maternal HPA activation (e.g., levels of circulating maternal glucocorticoid hormones). Thus, implying a U-shaped relationship between maternal HPA activation and HPA reactivity and fearfulness in the offspring, increasing maternal HPA activation with increasing environmental adversity would explain the effects of postnatal manipulations equally well. This raises the possibility that variation in active maternal care is an epiphenomenon, rather than a causal factor in developmental plasticity of HPA and fear responses in rats. Developmental plasticity of HPA and fear responses in rats and other animals has important implications for the design of animal experiments and for the well-being of experimental animals, both of which depend on the exact underlying mechanism(s). Importantly, however, more naturalistic approaches are needed to elucidate the adaptive significance of environment-dependent variation of HPA reactivity and fearfulness in view of discriminating between effects reflecting adaptive plasticity, phenotypic mismatch and pathological outcomes, respectively.