‘Optimal thermal range’ in ectotherms: Defining criteria for tests of the temperature-size-rule

Thermal performance curves for population growth rate r (a measure of fitness) were estimated over a wide range of temperature for three species: Coleps hirtus (Protista), Lecane inermis (Rotifera) and Aeolosoma hemprichi (Oligochaeta). We measured individual body size and examined if predictions for the temperature-size rule (TSR) were valid for different temperatures. All three organisms investigated follow the TSR, but only over a specific range between minimal and optimal temperatures, while maintenance at temperatures beyond this range showed the opposite pattern in these taxa. We consider minimal and optimal temperatures to be species-specific, and moreover delineate a physiological range outside of which an ectotherm is constrained against displaying size plasticity in response to temperature. This thermal range concept has important implications for general size-temperature studies. Furthermore, the concept of 'operating thermal conditions' may provide a new approach to (i) defining criteria required for investigating and interpreting temperature effects, and (ii) providing a novel interpretation for many cases in which species do not conform to the TSR.     

The relative importance of temperature and diet to larval development and adult size of the winter stonefly, Soyedina carolinensis (Piecoptera: Nemouridae)

SUMMARY. 1. Soyedina carolinensis Claassen, a leaf shredding stonefly, was reared in a series of three laboratory experiments from early instar to adult on different species of deciduous leaves and at various constant and fluctuating temperature regimes.
2. Experiment 1, which involved rearing larvae on fourteen different leaf diets at ambient stream temperatures, showed that diet significantly affected larval growth and adult size but did not affect overall developmental time.
3. Experiment 2, which involved rearing larvae on five different leaf diets at each of three fluctuating temperature regimes (viz ambient White Clay Creek (WCC), ambient WCC+3°C, and ambient WCC+6°C), showed that: (i) adding 6°C to the normal temperature regime of WCC was lethal to 99% of the larvae regardless of diet; and (ii) warming WCC by 3°C did not affect developmental time but did significantly reduce adult size relative to adults reared at WCC temperatures on certain diets.
4. Experiment 3, which involved rearing larvae on five different leaf diets at each of five constant temperatures (viz 5, 10, 15, 20, 25°C), showed that: (i) temperature significantly affected the mortality, growth, and development time of larvae whereas diet only affected larval growth and mortality; (ii) temperatures at or near 10°C yielded maximum larval growth and survival for most diets; (iii) at 5°C, larval mortality was high and growth was low resulting in a few small adults for most diets; (iv) larval mortality was at or near 100% at 15°C regardless of diet; and (v) no larvae survived at 20 and 25°C.     

Climate warming is associated with smaller body size and shorter lifespans in moose near their southern range limit

Despite the importance of body size for individual fitness, population dynamics and community dynamics, the influence of climate change on growth and body size is inadequately understood, particularly for long‐lived vertebrates. Although temporal trends in body size have been documented, it remains unclear whether these changes represent the adverse impact of climate change (environmental stress constraining phenotypes) or its mitigation (via phenotypic plasticity or evolution). Concerns have also been raised about whether climate change is indeed the causal agent of these phenotypic shifts, given the length of time‐series analysed and that studies often do not evaluate – and thereby sufficiently rule out – other potential causes. Here, we evaluate evidence for climate‐related changes in adult body size (indexed by skull size) over a 4–decade period for a population of moose (Alces alces) near the southern limit of their range whilst also considering changes in density, predation, and human activities. In particular, we document: (i) a trend of increasing winter temperatures and concurrent decline in skull size (decline of 19% for males and 13% for females) and (ii) evidence of a negative relationship between skull size and winter temperatures during the first year of life. These patterns could be plausibly interpreted as an adaptive phenotypic response to climate warming given that latitudinal/temperature clines are often accepted as evidence of adaptation to local climate. However, we also observed: (iii) that moose with smaller skulls had shorter lifespans, (iv) a reduction in lifespan over the 4‐decade study period, and (v) a negative relationship between lifespan and winter temperatures during the first year of life. Those observations indicate that this phenotypic change is not an adaptive response to climate change. However, this decline in lifespan was not accompanied by an obvious change in population dynamics, suggesting that climate change may affect population dynamics and life‐histories differently.     

Directionality theory and the evolution of body size

Directionality theory, a dynamic theory of evolution that integrates population genetics with demography, is based on the concept of evolutionary entropy, a measure of the variability in the age of reproducing individuals in a population. The main tenets of the theory are three principles relating the response to the ecological constraints a population experiences, with trends in entropy as the population evolves under mutation and natural selection. (i) Stationary size or fluctuations around a stationary size (bounded growth): a unidirectional increase in entropy; (ii) prolonged episodes of exponential growth (unbounded growth), large population size: a unidirectional decrease in entropy; and (iii) prolonged episodes of exponential growth (unbounded growth), small population size: random, non-directional change in entropy. We invoke these principles, together with an allometric relationship between entropy, and the morphometric variable body size, to provide evolutionary explanations of three empirical patterns pertaining to trends in body size, namely (i) Cope's rule, the tendency towards size increase within phyletic lineages; (ii) the island rule, which pertains to changes in body size that occur as species migrate from mainland populations to colonize island habitats; and (iii) Bergmann's rule, the tendency towards size increase with increasing latitude. The observation that these ecotypic patterns can be explained in terms of the directionality principles for entropy underscores the significance of evolutionary entropy as a unifying concept in forging a link between micro-evolution, the dynamics of gene frequency change, and macro-evolution, dynamic changes in morphometric variables.     

Optimum body size: effects of food quality and temperature,when reproductive growth rate is restricted,with examples from aphids

Most models of optimum energy partitioning predict variability in adult size, although not always explicitly. Increase in size is usually attributed to an increase in the growth rate or decline in mortality. The model presented shows that this may not always be the case. Even when mortality is kept constant in organisms with overlapping generations, a constraint on the maximum reproductive growth rate may lead, when the rate of overall growth increases, to either an increase or a decline in the optimum adult body size. It is shown that adult size could be a consequence of the differential responses of life history traits to changes in temperature and food quality. This is clearly advantageous for short lived organisms, like aphids, each generation of which only experience a very small part of the great seasonal range in conditions. This hypothesis complements Iwasa's (1991) explanation of the phenotypic plasticity observed in long lived organisms. The predictions are illustrated with empirical data from aphids. The model presented, which has been verified against a very large data set, indicates that for aphids the adult weight observed at a particular combination of temperature and food quality is that at which the population growth rate, r_m, is maximized. We conclude that predictions about adult size from models based on the partitioning of energy are more likely to apply to organisms that scramble for resources, i.e., “r” selected species. The size of organisms that contest for resources is more likely to be determined by competitive status and avoidance of natural enemies.     

Optimal allocation of energy to growth and reproduction

The optimal allocation of energy to growth and reproduction is considered for three different cases, i.e., a single reproduction (semelparity), reproduction through repeated discrete clutches, and continuous reproduction. The problem reduces to optimizing age and size at maturity. The best strategy is to continue growth until the change of production rate with respect to increasing body size, multiplied by life expectancy for those attaining adulthood and reproducing successfully, is greater than one. The time at which semelparous species reproduce may also be optimized; for the other modes of reproduction only physiological factors or seasonality can limit the maximum age. A brief growing season or high mortality rate are factors leading to early maturity and small adult body size.     

Warming temperatures and smaller body sizes: synchronous changes in growth of North Sea fishes

Decreasing body size has been proposed as a universal response to increasing temperatures. The physiology behind the response is well established for ectotherms inhabiting aquatic environments: as higher temperatures decrease the aerobic capacity, individuals with smaller body sizes have a reduced risk of oxygen deprivation. However, empirical evidence of this response at the scale of communities and ecosystems is lacking for marine fish species. Here, we show that over a 40‐year period six of eight commercial fish species in the North Sea examined underwent concomitant reductions in asymptotic body size with the synchronous component of the total variability coinciding with a 1–2 °C increase in water temperature. Smaller body sizes decreased the yield‐per‐recruit of these stocks by an average of 23%. Although it is not possible to ascribe these phenotypic changes unequivocally to temperature, four aspects support this interpretation: (i) the synchronous trend was detected across species varying in their life history and life style; (ii) the decrease coincided with the period of increasing temperature; (iii) the direction of the phenotypic change is consistent with physiological knowledge; and (iv) no cross‐species synchrony was detected in other species‐specific factors potentially impacting growth. Our findings support a recent model‐derived prediction that fish size will shrink in response to climate‐induced changes in temperature and oxygen. The smaller body sizes being projected for the future are already detectable in the North Sea.     

Seasonality of reproduction by liverbearing fishes in tropical rainforest streams

Reproductive ecology, population structure, and diets of three common livebearing poeciliid fishes (Alfaro cultratus, Phallichthys amates, Poecilia gilli) from rainforest streams in Costa Rica were investigated over ten continuous months. The region experiences little annual temperature variation, and although monthly rainfall is continuous each year, two brief dry seasons typically occur. Monthly changes in indices of ovarian condition, percentages of females with developing embryos, and population size structure revealed that reproductive output by females of all three species varied seasonally. Based on testicular condition, males were reproductively active year-round, however the mean gonadal index for males of two algivorous species showed low levels of seasonal cycling that largely coincided with female variation in reproductive effort. All three species had seasonal differences in the female size-brood size relationship, whereby larger females tended to carry more embryos during the wet season. Several important adult and neonate food resources are more available in the flooded forest during the wet season, which is also the period when conspecifics and predators are at their lowest per-area densities. Three hypotheses are discussed: (1) brood size in relation to conspecific density-mating frequency, (2) reproductive allocation in response to variation in adult food resources, and (3) selection for greater reproductive effort during conditions optimal for juvenile growth and survival. Data for Alfaro were consistent with the latter two hypotheses. In Phallichthys and Poecilia, diets were poorer during wet seasons, indicating that reproductive effort does not coincide with availability of adult food resources, and that selection probably favors greater reproductive effort during periods optimal for juvenile growth and survival.     

Adaptive divergence in body size overrides the effects of plasticity across natural habitats in the brown trout

The evolution of life-history traits is characterized by trade-offs between different selection pressures, as well as plasticity across environmental conditions. Yet, studies on local adaptation are often performed under artificial conditions, leaving two issues unexplored: (i) how consistent are laboratory inferred local adaptations under natural conditions and (ii) how much phenotypic variation is attributed to phenotypic plasticity and to adaptive evolution, respectively, across environmental conditions? We reared fish from six locally adapted (domesticated and wild) populations of anadromous brown trout (Salmo trutta) in one semi-natural and three natural streams and recorded a key life-history trait (body size at the end of first growth season). We found that population-specific reaction norms were close to parallel across different streams and Q_ST was similar – and larger than F_ST – within all streams, indicating a consistency of local adaptation in body size across natural environments. The amount of variation explained by population origin exceeded the variation across stream environments, indicating that genetic effects derived from adaptive processes have a stronger effect on phenotypic variation than plasticity induced by environmental conditions. These results suggest that plasticity does not “swamp” the phenotypic variation, and that selection may thus be efficient in generating genetic change.     

Rapid population divergence in thermal reaction norms for an invading species: breaking the temperature-size rule

The temperature-size rule is a common pattern of phenotypic plasticity in which higher temperature during development results in a smaller adult body size (i.e. a thermal reaction norm with negative slope). Examples and exceptions to the rule are known in multiple groups of organisms, but rapid population differentiation in the temperature-size rule has not been explored. Here we examine the genetic and parental contributions to population differentiation in thermal reaction norms for size, development time and survival in the Cabbage White Butterfly Pieris rapae, for two geographical populations that have likely diverged within the past 150 years. We used split-sibship experiments with two temperature treatments (warm and cool) for P. rapae from Chapel Hill, NC, and from Seattle, WA. Mixed-effect model analyses demonstrate significant genetic differences between NC and WA populations for adult size and for thermal reaction norms for size. Mean adult mass was 12-24% greater in NC than in WA populations for both temperature treatments; mean size was unaffected or decreased with temperature (the temperature-size rule) for the WA population, but size increased with temperature for the NC population. Our study shows that the temperature-size rule and related thermal reaction norms can evolve rapidly within species in natural field conditions. Rapid evolutionary divergence argues against the existence of a simple, general mechanistic constraint as the underlying cause of the temperature-size rule.     

Adult insect personality in the wild—Calopteryx splendens as a model for field studies

Animal personality has received increasing interest and acknowledgment within ecological research over the past two decades. However, some areas are still poorly studied and need to be developed. For instance, field studies focused on invertebrates are currently highly underrepresented in the literature. More studies including a wider variety of traits measured and species tested are needed to improve our understanding of trait‐correlation patterns and generalities. We studied nine behavioral traits, in the damselfly Calopteryx splendens, from an array of three experiments: (i) courtship, (ii) aggressiveness, and (iii) boldness, and calculated their repeatability. The behaviors were measured twice in two different contexts: (i) undisturbed territory and (ii) partially deteriorated territory. Traits related to courtship and boldness were all repeatable across the two contexts. Among aggressive behaviors, only one trait (number of hits) was repeatable. This work demonstrates, for the first time, the presence of within‐population personality differences in an adult damselfly in the wild. We further propose C. splendens as a promising model species for testing personality in the wild under highly controlled environmental conditions.     

The role of environment and core‐margin effects on range‐wide phenotypic variation in a montane grasshopper

The integration of genetic information with ecological and phenotypic data constitutes an effective approach to gain insight into the mechanisms determining interpopulation variability and the evolutionary processes underlying local adaptation and incipient speciation. Here, we use the Pyrenean Morales grasshopper (Chorthippus saulcyi moralesi) as study system to (i) analyse the relative role of genetic drift and selection in range‐wide patterns of phenotypic differentiation and (ii) identify the potential selective agents (environment, elevation) responsible for variation. We also test the hypothesis that (iii) the development of dispersal‐related traits is associated with different parameters related to population persistence/turnover, including habitat suitability stability over the last 120 000 years, distance to the species distribution core and population genetic variability. Our results indicate that selection shaped phenotypic differentiation across all the studied morphological traits (body size, forewing length and shape). Subsequent analyses revealed that among‐population differentiation in forewing length was significantly explained by a temperature gradient, suggesting an adaptive response to thermoregulation or flight performance under contrasting temperature regimes. We found support for our hypothesis predicting a positive association between the distance to the species distribution core and the development of dispersal‐related morphology, which suggests an increased dispersal capability in populations located at range edges that, in turn, exhibit lower levels of genetic variability. Overall, our results indicate that range‐wide patterns of phenotypic variation are partially explained by adaptation in response to local environmental conditions and differences in habitat persistence between core and peripheral populations.     

Sensitive males: inbreeding depression in an endangered bird

Attempts to conserve threatened species by establishing new populations via reintroduction are controversial. Theory predicts that genetic bottlenecks result in increased mating between relatives and inbreeding depression. However, few studies of wild sourced reintroductions have carefully examined these genetic consequences. Our study assesses inbreeding and inbreeding depression in a free-living reintroduced population of an endangered New Zealand bird, the hihi (Notiomystis cincta). Using molecular sexing and marker-based inbreeding coefficients estimated from 19 autosomal microsatellite loci, we show that (i) inbreeding depresses offspring survival, (ii) male embryos are more inbred on average than female embryos, (iii) the effect of inbreeding depression is male-biased and (iv) this population has a substantial genetic load. Male susceptibility to inbreeding during embryo and nestling development may be due to size dimorphism, resulting in faster growth rates and more stressful development for male embryos and nestlings compared with females. This work highlights the effects of inbreeding at early life-history stages and the repercussions for the long-term population viability of threatened species.     

Conservation of Dehaasia pugerensis (Lauraceae), a tree endemic to East Java (Indonesia) and last collected in 1940

Dehaasia pugerensis Koord. & Valeton is a threatened Indonesian Lauraceae species. It is an endemic tree known only from Jember Regency in East Java. To enhance the conservation of D. pugerensis, we conducted a population survey in several locations in Jember where the species were previously collected. The objectives were to: i) assess the current population status of D. pugerensis, ii) collect plant materials (seed, seedling, or cutting) to serve as ex situ collections, and iii) update the conservation status of the species according to IUCN Red List Category and Criteria. We only found D. pugerensis in 6 out of 16 locations in Wuluhan and Ambulu District during the survey. We successfully located 560 individuals of the species, of which 194 individuals (34.6%) were in the mature stage. Based on the diameter and height classes, the population of D. pugerensis formed a reverse J-shaped size distribution. We successfully collected 23 seeds and 15 seedlings of the species for ex situ collections. Our findings showed that the current status of D. pugerensis is Critically Endangered (CR) based on criteria B1ab(i,ii,iii,iv,v)and C2a(ii). Under these categories, the species faces an extremely high risk of extinction in the wild. Therefore, prompt comprehensive conservation actions are needed to ensure the survival of the species.     

Simultaneous versus sequential optimal experiment design for the identification of multi-parameter microbial growth kinetics as a function of temperature

Optimal experiment design for parameter estimation (OED/PE) has become a popular tool for efficient and accurate estimation of kinetic model parameters. When the kinetic model under study encloses multiple parameters, different optimization strategies can be constructed. The most straightforward approach is to estimate all parameters simultaneously from one optimal experiment (single OED/PE strategy). However, due to the complexity of the optimization problem or the stringent limitations on the system's dynamics, the experimental information can be limited and parameter estimation convergence problems can arise. As an alternative, we propose to reduce the optimization problem to a series of two-parameter estimation problems, i.e., an optimal experiment is designed for a combination of two parameters while presuming the other parameters known. Two different approaches can be followed: (i) all two-parameter optimal experiments are designed based on identical initial parameter estimates and parameters are estimated simultaneously from all resulting experimental data (global OED/PE strategy), and (ii) optimal experiments are calculated and implemented sequentially whereby the parameter values are updated intermediately (sequential OED/PE strategy).This work exploits OED/PE for the identification of the Cardinal Temperature Model with Inflection (CTMI) (Rosso et al., 1993). This kinetic model describes the effect of temperature on the microbial growth rate and encloses four parameters. The three OED/PE strategies are considered and the impact of the OED/PE design strategy on the accuracy of the CTMI parameter estimation is evaluated. Based on a simulation study, it is observed that the parameter values derived from the sequential approach deviate more from the true parameters than the single and global strategy estimates. The single and global OED/PE strategies are further compared based on experimental data obtained from design implementation in a bioreactor. Comparable estimates are obtained, but global OED/PE estimates are, in general, more accurate and reliable.     

Can transgenerational plasticity contribute to the invasion success of annual plant species?

Adaptive transgenerational plasticity (TGP), i.e., significantly higher fitness when maternal and offspring conditions match, might contribute to the population growth of non-native species in highly variable environments. However, comparative studies that directly test this hypothesis are lacking. Therefore, we performed a reciprocal split-brood experiment to compare TGP in response to N and water availability in single populations of two invasive (Amaranthus retroflexus, Galinsoga parviflora) and two congeneric non-invasive introduced species (Amaranthus albus, Galinsoga ciliata). We hypothesized that the transgenerational effect is adaptive: (1) in invasive species compared with non-invasive adventives, and (2) in stressful conditions compared with resource-rich environments. The phenotypic variation among offspring was generated, in large part, by our experimental treatments in the maternal generation; therefore, we demonstrated a direct TGP effect on the offspring’s adult fitness. We found evidence, for the first time, that invasive and non-invasive adventive species differ regarding the expression of TGP in the adult stage, as adaptive responses were found exclusively in the invasive species. The manifestation of TGP was more explicit under resource-rich conditions; therefore, it might contribute to the population dynamics of non-native species in resource-rich sites rather than to their ecological tolerance spectra.     

Effects of salinity and temperature on long-term survival of the eel pathogen Vibrio vulnificus biotype 2 (serovar E)

Vibrio vulnificus biotype 2 (serovar E) is a primary eel pathogen. In this study, we performed long-term survival experiments to investigate whether the aquatic ecosystem can be a reservoir for this bacterium. We have used microcosms containing water of different salinities (ranging from 0.3 to 3.8%) maintained at three temperatures (12, 25, and 30 degrees C). Temperature and salinity significantly affected long-term survival: (i) the optimal salinity for survival was 1.5%; (ii) lower salinities reduced survival, although they were nonlethal; and (ii) the optimal temperature for survival was dependent on the salinity (25 degrees C for microcosms at 0.3 and 0.5% and 12 degrees C for microcosms at 1.5 to 3.8%). In the absence of salts, culturability dropped to zero in a few days, without evidence of cellular lysis. Under optimal conditions of salinity and temperature, the bacterium was able to survive in the free-living form for at least 3 years. The presence of a capsule on the bacterial cell seemed to confer an advantage, since the long-term survival rate of opaque variants was significantly higher than that of translucent ones. Long-term-starved cells maintained their infectivity for eels (as determined by both intraperitoneal and immersion challenges) and mice. Examination under the microscope showed that (i) the capsule was maintained, (ii) the cell size decreased, (iii) the rod shape changed to coccuslike along the time of starvation, and (iv) membrane vesicles and extracellular material were occasionally produced. In conclusion, V. vulnificus biotype 2 follows a survival strategy similar to that of biotype 1 of this species in response to starvation conditions in water. Moreover, the aquatic ecosystem is one of its reservoirs.     

Effect of three isolates of Pandora neoaphidis from a single population of Sitobion avenae on mortality,speed of kill and fecundity of S. avenae and Rhopalosiphum padi at different temperatures

We studied the effect of three Pandora neoaphidis isolates from one Sitobion avenae population, three temperatures, and two aphid species namely S. avenae and Rhopalosiphum padi on (i) aphid mortality, (ii) time needed to kill aphids, and (iii) aphid average daily and lifetime fecundity. A total of 38% of S. avenae and 7% of R. padi died and supported fungus sporulation. S. avenae was killed 30% faster than R. padi. Average daily fecundity was negatively affected only in S. avenae inoculated with, but not killed by, P. neoaphidis. Nevertheless, lifetime fecundity of both aphid species inoculated and sporulating with P. neoaphidis was halved compared to lifetime fecundity of surviving aphids in the control. Increased temperature resulted in higher mortality rates but did not consistently affect lethal time or fecundity. Results suggest that (i) temperature effects on virulence differ between isolates, even when obtained within the same host population, and (ii) even though an isolate does not kill a host it may reduce its fecundity. Our findings are important for the understanding of P. neoaphidis epizootiology and for use in pest-natural enemy modelling.     

Diatoms can be an important exception to temperature–size rules at species and community levels of organization

Climate warming has been linked to an apparent general decrease in body sizes of ectotherms, both across and within taxa, especially in aquatic systems. Smaller body size in warmer geographical regions has also been widely observed. Since body size is a fundamental determinant of many biological attributes, climate‐warming‐related changes in size could ripple across multiple levels of ecological organization. Some recent studies have questioned the ubiquity of temperature–size rules, however, and certain widespread and abundant taxa, such as diatoms, may be important exceptions. We tested the hypothesis that diatoms are smaller at warmer temperatures using a system of geothermally heated streams. There was no consistent relationship between size and temperature at either the population or community level. These field data provide important counterexamples to both James’ and Bergmann's temperature–size rules, respectively, undermining the widely held assumption that warming favours the small. This study provides compelling new evidence that diatoms are an important exception to temperature–size rules for three reasons: (i) we use many more species than prior work; (ii) we examine both community and species levels of organization simultaneously; (iii) we work in a natural system with a wide temperature gradient but minimal variation in other factors, to achieve robust tests of hypotheses without relying on laboratory setups, which have limited realism. In addition, we show that interspecific effects were a bigger contributor to whole‐community size differences, and are probably more ecologically important than more commonly studied intraspecific effects. These findings highlight the need for multispecies approaches in future studies of climate warming and body size.     

Plasticity to wind is modular and genetically variable in Arabidopsis thaliana

Thigmomorphogenesis, the characteristic phenotypic changes by which plants react to mechanical stress, is a widespread and probably adaptive type of phenotypic plasticity. However, little is known about its genetic basis and population variation. Here, we examine genetic variation for thigmomorphogenesis within and among natural populations of the model system Arabidopsis thaliana. Offspring from 17 field-collected European populations was subjected to three levels of mechanical stress exerted by wind. Overall, plants were remarkably tolerant to mechanical stress. Even high wind speed did not significantly alter the correlation structure among phenotypic traits. However, wind significantly affected plant growth and phenology, and there was genetic variation for some aspects of plasticity to wind among A. thaliana populations. Our most interesting finding was that phenotypic traits were organized into three distinct and to a large degree statistically independent covariance modules associated with plant size, phenology, and growth form, respectively. These phenotypic modules differed in their responsiveness to wind, in the degree of genetic variability for plasticity, and in the extent to which plasticity affected fitness. It is likely, therefore, that thigmomorphogenesis in this species evolves quasi-independently in different phenotypic modules.