Ecological differences influence the thermal sensitivity of swimming performance in two co-occurring mysid shrimp species with climate change implications

Temperature strongly affects performance in ectotherms. As ocean warming continues, performance of marine species will be impacted. Many studies have focused on how warming will impact physiology, life history, and behavior, but few studies have investigated how ecological and behavioral traits of organisms will affect their response to changing thermal environments. Here, we assessed the thermal tolerances and thermal sensitivity of swimming performance of two sympatric mysid shrimp species of the Northwest Atlantic. Neomysis americana and Heteromysis formosa overlap in habitat and many aspects of their ecological niche, but only N. americana exhibits vertical migration. In temperate coastal ecosystems, temperature stratification of the water column exposes vertical migrators to a wider range of temperatures on a daily basis. We found that N. americana had a significantly lower critical thermal minimum (CT_min) and critical thermal maximum (CT_max). However, both mysid species had a buffer of at least 4 °C between their CT_max and the 100-year projection for mean summer water temperatures of 28 °C. Swimming performance of the vertically migrating species was more sensitive to temperature variation, and this species exhibited faster burst swimming speeds. The generalist performance curve of H. formosa and specialist curve of N. americana are consistent with predictions based on the exposure of each species to temperature variation such that higher within-generation variability promotes specialization. However, these species violate the assumption of the specialist-generalist tradeoff in that the area under their performance curves is not constant. Our results highlight the importance of incorporating species-specific responses to temperature based on the ecology and behavior of organisms into climate change prediction models.     

Interfemale variation in egg yolk androgen allocation in the European starling: do high-quality females invest more?

Androgenic hormones occur naturally in bird egg yolk and are known to enhance growth in canary and gull chicks. Gil et al. (1999, Science, 286, 126-128) have recently proposed that female allocation of androgens to eggs represents a form of costly maternal investment. This hypothesis predicts that females of high quality or high reproductive potential should invest more yolk androgens in their eggs than females of low quality or low reproductive potential. We tested these predictions by examining interfemale variation in allocation of the androgenic steroids testosterone and androstenedione to eggs in a wild population of European starlings, Sturnus vulgaris. We collected 30 full clutches of eggs and captured 22 of the females that laid these clutches for phenotypic measurements. In agreement with the hypothesis, we found that there was significant interfemale variation in yolk androgen concentrations. Furthermore, older females deposited more androstenedione and testosterone in eggs than 1-year-old females, and females laying early or large clutches deposited more testosterone in eggs than females laying late or small clutches. However, females in good body condition did not deposit more androgens in eggs than females in poor body condition. Large-yolked eggs had a higher total yolk androgen content than small-yolked eggs, but larger eggs did not have higher concentrations of yolk androgens. The results in general support the investment hypothesis of yolk androgen allocation. However, further data are needed regarding the costs of yolk androgen allocation and the effects of yolk androgens on offspring to substantiate the assumptions of the hypothesis. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Thermal dependence of reproductive allocation in a tropical lizard

In ectotherms, environmental temperature is the most prominent abiotic factor that modulates life-history traits. We explored the influence of environmental temperature on reproduction in the Madagascar ground gecko (Paroedura picta) by measuring reproductive traits of females at constant temperatures (24, 27, 30 °C). Females of this species lay clutches of one or two eggs within short intervals. For each female, we measured egg mass for the first five clutches. For one clutch, we also measured the energetic content of eggs via bomb calorimetry. Temperature positively influenced the rate of egg production, but females at 30 °C laid smaller eggs than did females at either 24 or 27 °C. Dry mass of eggs scaled allometrically with wet mass, but this relationship was similar among thermal treatments. Females at all temperatures produced eggs with similar energy densities. Females at 24 °C allocated less energy per time unit (≈8 mW) to reproduction than did females from higher temperatures (≈12 mW). However, females at either 24 or 27 °C allocated significantly more energy per egg than did females at 30 °C. Our results demonstrate that a complex thermal sensitivity of reproductive rate can emerge from distinct thermal sensitivities of egg size, egg composition and clutch frequency.     

Variation in Thermal Sensitivity and Thermal Tolerances in an Invasive Species across a Climatic Gradient: Lessons from the Land Snail Cornu aspersum

The ability of organisms to perform at different temperatures could be described by a continuous nonlinear reaction norm (i.e., thermal performance curve, TPC), in which the phenotypic trait value varies as a function of temperature. Almost any shift in the parameters of this performance curve could highlight the direct effect of temperature on organism fitness, providing a powerful framework for testing thermal adaptation hypotheses. Inter-and intraspecific differences in this performance curve are also reflected in thermal tolerances limits (e.g., critical and lethal limits), influencing the biogeographic patterns of species’ distribution. Within this context, here we investigated the intraspecific variation in thermal sensitivities and thermal tolerances in three populations of the invasive snail Cornu aspersum across a geographical gradient, characterized by different climatic conditions. Thus, we examined population differentiation in the TPCs, thermal-coma recovery times, expression of heat-shock proteins and standard metabolic rate (i.e., energetic costs of physiological differentiation). We tested two competing hypotheses regarding thermal adaptation (the “hotter is better” and the generalist-specialist trade-offs). Our results show that the differences in thermal sensitivity among populations of C. aspersum follow a latitudinal pattern, which is likely the result of a combination of thermodynamic constraints (“hotter is better”) and thermal adaptations to their local environments (generalist-specialist trade-offs). This finding is also consistent with some thermal tolerance indices such as the Heat-Shock Protein Response and the recovery time from chill-coma. However, mixed responses in the evaluated traits suggest that thermal adaptation in this species is not complete, as we were not able to detect any differences in neither energetic costs of physiological differentiation among populations, nor in the heat-coma recovery.     

A QUANTITATIVE GENETIC ANALYSIS OF THERMAL SENSITIVITY IN THE LOCOMOTOR PERFORMANCE CURVE OF APHIDIUS ERVI

The thermal sensitivity of locomotor performance in Aphidius ervi, a parasitic hymenopteran, conforms to the “jack-of-all-trades is master of none” model of specialist-generalist trade-offs. Performance breadth and maximal performance at the phenotypic level are negatively correlated in both sexes. A strong, negative genetic correlation was found for males, but not for females. In males, the broad-sense heritability of performance breadth was about 0.16, and that of maximum walking velocity was about 0.29. Neither heritability was significantly different from zero in females. The broad-sense heritability of body mass was about 0.3 in females and 0.6 in males, with a strong negative genetic correlation between size and maximum velocity in males only. These data provide the first quantitative genetic analysis of performance curves in eukaryotic animals, and one of the few demonstrations of the specialist-generalist trade-off that underlies much theory in evolutionary ecology.     

Maternal effects mediated by egg quality in the Yellow-legged Gull Larus michahellis in relation to laying order and embryo sex

Background

Maternal effects mediated by egg size and quality may profoundly affect offspring development and performance, and mothers may adjust egg traits according to environmental or social influences. In avian species, context-dependency of maternal effects may result in variation in egg composition, as well as in differential patterns of covariation among selected egg components, according to, for example, position in the laying sequence or offspring sex. We investigated variation in major classes of egg yolk components (carotenoids, vitamins and steroid hormones) in relation to egg size, position in the laying sequence and embryo sex in clutches of the Yellow-legged Gull (Larus michahellis). We also investigated their covariation, to highlight mutual adjustments, maternal constraints or trade-offs in egg allocation.

Results

Laying sequence-specific patterns of allocation emerged: concentration of carotenoids and vitamin E decreased, while concentrations of androgens increased. Vitamin A, estradiol and corticosterone did not show any change. There was no evidence of sex-specific allocation or covariation of yolk components. Concentrations of carotenoids and vitamins were positively correlated. Egg mass decreased along the laying sequence, and this decrease was negatively correlated with the mean concentrations of carotenoids in clutches, suggesting that nutritionally constrained females lay low quality clutches in terms of carotenoid content. Finally, clutches with smaller decline in antioxidants between first- and last-laid eggs had a larger increase in yolk corticosterone, suggesting that a smaller antioxidant depletion along the laying sequence may entail a cost for laying females in terms of increased stress levels.

Conclusions

Since some of the analyzed yolk components (e.g. testosterone and lutein) are known to exert sex-specific phenotypic effects on the progeny in this species, the lack of sex-specific egg allocation by mothers may either result from trade-offs between contrasting effects of different egg components on male and female offspring, or indicate that sex-specific traits are controlled primarily by mechanisms of sexual differentiation, including endogenous hormone production or metabolism of exogenous antioxidants, during embryonic development.     

Family planning inDaphnia: resistance to starvation in offspring born to mothers grown at different food levels

Summary We observed a shift in maternal investment per offspring in clonal cultures of twoDaphnia species. Mothers grown at high food levels produced large clutches of smaller eggs but their offspring could not survive long under starvation conditions. Genetically identical mothers grown at low food levels produced small cultches of larger eggs, and their offspring, albeit low in numbers, were able to survive long periods of starvation. Our data show thatDaphnia mothers are capable of assessing food level and use this information in adjusting their fractional peroffspring allocation of reproductive resources.     

Detrimental influence on performance of high temperature incubation in a tropical reptile: is cooler better in the tropics?

Global temperatures have risen over the last century, and are forecast to continue rising. Ectotherms may be particularly sensitive to changes in thermal regimes, and tropical ectotherms are more likely than temperate species to be influenced by changes in environmental temperature, because they may have evolved narrow thermal tolerances. Keelback snakes (Tropidonophis mairii) are tropical, oviparous reptiles. To quantify the effects of temperature on the morphology and physiology of hatchling keelbacks, clutches laid by wild-caught females were split and incubated at three temperatures, reflecting the average minimum, overall average and average maximum temperatures recorded at our study site. Upon hatching, the performance of neonates was examined at all three incubation temperatures in a randomized order over consecutive days. Hatchlings from the ‘hot’ treatment had slower burst swim speeds and swam fewer laps than hatchlings from the cooler incubation temperatures in all three test temperatures, indicating a low thermal optimum for incubation of this tropical species. There were no significant interactions between test temperature and incubation temperature across performance variables, suggesting phenotypic differences caused by incubation temperature did not acclimate this species to post-hatching conditions. Thus, keelback embryos appear evolutionarily adapted to development at cooler temperatures (relative to what is available in their habitat). The considerable reduction in hatchling viability and performance associated with a 3.5 °C increase in incubation temperature, suggests climate change may have significant population-level effects on this species. However, the offspring of three mothers exposed to the hottest incubation temperature were apparently resilient to high temperature, suggesting that this species may respond to selection imposed by thermal regime.     

Geographic mosaics of phenology,host preference,adult size and microhabitat choice predict butterfly resilience to climate warming

The climate‐sensitive butterfly Euphydryas editha exhibited interpopulation variation in both phenology and egg placement, exposing individuals to diverse thermal environments. We measured ‘eggspace’ temperatures adjacent to natural egg clutches in populations distributed across a range of latitudes (36°8′–44°6′) and altitudes (213–3171 m). Eggs laid > 50 cm above the ground averaged 3.1°C cooler than ambient air at 1 m height, while eggs at < 1 cm height averaged 15.5°C hotter than ambient, ranging up to 47°C. Because of differences in egg height, eggs at 3171 m elevation and 20.6°C ambient air experienced mean eggspace temperatures 7°C hotter than those at 213 m elevation and ambient 33.3°C. Experimental eggs survived for one hour at 45°C but were killed by 48°C. Eggs laid low, by positively geotactic butterflies, risked thermal stress. However, at populations where eggs were laid lowest, higher oviposition would have incurred incidental predation from grazers. Interpopulation variation in phenology influenced thermal environment and buffered exposure to thermal stress. At sites with hotter July temperatures, the single annual flight/oviposition period was advanced such that eggs were laid on earlier dates, with cooler ambient temperatures. The insects possessed two mechanisms for advancing egg phenology; they could advance timing of larval diapause‐breaking and/or shorten the life cycle by becoming smaller adults. Mean weight of newly‐eclosed females varied among populations from 92 to 285 mg, suggesting that variable adult size did influence phenology. Possible options for in situ mitigation of thermal stress include further advancing phenology and raising egg height. We argue that these options exist, as evidenced by current variation in these traits and by failure of E. editha to conform to restrictive biogeographic constraints, such as the expectation that populations at equatorial and poleward range limits be confined to higher and lower elevations, respectively. This optimistic example shows how complex local adaptation can generate resilience to climate warming.     

Incubation capacity limits maximum clutch size in black-tailed gulls Larus crassirostris

Factors determining clutch size of birds have long been the central issue in studies in life histories. It is assumed that the configuration of brood patches could limit the maximum clutch size. To test this hypothesis we manipulated clutch sizes and measured egg temperature as well as reproductive consequences in black-tailed gulls Larus crassirostris , which usually lay two egg clutches and have three brood patches. Mean egg temperature in 4-egg clutches (32.6±1.0°C) was significantly lower than in 2-egg (34.6±0.4°C) and 3-egg clutches (34.1±0.4°C), because egg temperature of the coolest egg within a 4-egg clutch was often substantially lower than the other three eggs. The proportion of eggs hatching from 4-egg clutches (11.6%) was lower than those of 2-egg (49.1%) and 3-egg clutches (52.0%). Four-egg clutches had longer incubation periods (29.6±1.3 day) than 2-egg (28.1±1.7 day) and 3-egg clutches (28.0 ±1.3 day). The results indicate that incubation capacity, which may be determined by the configuration of brood patches, limits the maximum clutch size in black tailed gulls, but not the actual clutch size typically laid.     

Maternal behavior and clutch manipulation in the ring-legged earwig (Dermaptera: Carcinophoridae)

The expression and maintenance of maternal behavior in the earwig,Euborellia annulipes, was examined through manipulation of clutch size, age, and species and through observations of interactions between brooding females. Females underwent discrete gonadotrophic cycles culminating in oviposition of first clutches that were highly variable in size. Neither the head capsule width nor the age of the mother was correlated with clutch size. Maternal care extended through embryogenesis and for the week following hatching. Clutch removal significantly shortened the interclutch interval, indicating that the presence of brood inhibited the onset of the second gonadotrophic cycle. Brooding females readily accepted replacement clutches of the same age. Thus, mothers did not appear to distinguish their own eggs from those of other females. Experimental doubling of clutch size did not significantly reduce the proportion hatching or fledging. In contrast, reducing clutch size diminished the percentage successfully fledging. Manipulation of clutch age resulted in reduced hatching/fledging success. Placing two females, each with newly laid clutches, in the same cage usually resulted in egg transfer from the nest of one female to that of the other within 12 h. Nests of females with larger forceps were significantly more likely to contain both clutches. When mothers with first clutches were paired with mothers with third clutches, eggs were more likely to be transferred to the nest of the older female.E. annulipes females with newly laid clutches appeared to accept as replacement clutches eggs of the earwigDoru taeniatum. Alien clutches were maintained for the typical duration of embryogenesis; however, noD. taeniatum hatchlings were observed.     

Does the cost of incubation set limits to clutch size in common eiders Somateria mollissima?

We examined the effect of natural clutch size on the cost of incubation in a population of common eiders Somateria mollissima nesting in Tromsø, northern Norway. The body condition of females at day 5 in the incubation period was not related to clutch size (3–6 eggs), but females incubating large clutches lost more mass and had a lower body condition at day 20 in the incubation period than females incubating small clutches. Females incubating large clutches had a slightly shorter incubation period and a lower egg predation rate. The results do not support the hypothesis that the female's ability to produce eggs is the only ultimate control of clutch size in eider. Instead the results suggest that there may be an interaction between the allocation of body reserves to eggs and incubation, and that females producing large clutches allocate more of their body reserves to incubation than females producing small clutches, in order to shorten the incubation period and to minimise the risk of predation on eggs.     

Food availability affects the maternal transfer of androgens and antibodies into eggs of a colonial seabird

Mothers can improve the quality of their offspring by increasing the level of certain components in their eggs. To examine whether or not mothers increase deposition of such components in eggs as a function of food availability, we food-supplemented black-legged kittiwake females (Rissa tridactyla) before and during egg laying and compared deposition of androgens and antibodies into eggs of first and experimentally induced replacement clutches. Food-supplemented females transferred lower amounts of androgens and antibodies into eggs of induced replacement clutches than did non-food-supplemented mothers, whereas first clutches presented no differences between treatments. Our results suggest that when females are in lower condition, they transfer more androgens and antibodies into eggs to facilitate chick development despite potential long-term costs for juveniles. Females in prime condition may avoid these potential long-term costs because they can provide their chicks with more and higher quality resources.     

Plasticity in incubation behavior and shading by king rails Rallus elegans in response to temperature

King rails experience a wide range of temperatures during the course of the breeding season throughout their rapidly contracting geographic range. Incubating parent birds are adapted to keep their eggs within a temperature range appropriate for embryo development, but king rail clutches are at risk of exceeding lethal temperatures in the latter half of the nesting season. We investigated whether behavioral plasticity during incubation enables parents to maintain clutch temperature within tolerable limits for embryo development. Video revealed that king rail parents interrupted incubation to stand above and shade their eggs. We tested the hypothesis that the onset of shading was a direct response to ambient temperature (adaptive plasticity). We monitored clutch temperature directly by experimentally adding into clutches a model egg embedded with a programmable iButton. We measured ambient temperature at the nest site simultaneously. Parents spent proportionately more time shading and less time incubating their eggs at higher ambient temperatures. Shading may primarily function in cooling the parent. The frequency and duration of shading bouts were significantly greater at higher ambient temperatures. Parents also took more frequent but shorter recesses in hotter conditions. Diurnal recesses exposed eggs to direct sunlight, and the highest clutch temperatures were recorded under these conditions. Complete hatching failure in at least one nest was attributable to high clutch temperature for an extended period. Because mean ambient temperature increases throughout the breeding season, we investigated seasonal patterns in onset of incubation and its effect on hatching rate. Later in the season, parents tended to initiate incubation earlier, and hatching asynchrony increased significantly. Together these results suggest that breeding king rails may be constrained in their ability to cope with sustained high temperatures should seasonal averages continue to rise as predicted.     

Differential impact of hotter drought on seedling performance of five ecologically distinct pine species

Increasing temperature and drought intensity is inducing the phenomenon of the so-called “hotter drought”, which is expected to increase in frequency over the coming decades across many areas of the globe, and is expected to have major implications for forest systems. Consequences of hotter drought could be especially relevant for closely related species overlapping their distributions, since differences in response can translate into range shifts. We assessed the effect of future climatic conditions on the performance of five ecologically distinct pine species common in Europe: Pinus halepensis, P. pinaster, P. nigra, P. sylvestris and P. uncinata. We hypothesised that Mediterranean species inhabiting dry, low-elevation sites will be less affected by the expected warming and drought increase than species inhabiting cold-wet sites. We performed a controlled conditions experiment simulating current and projected temperature and precipitation, and analysed seedling responses in terms of survival, growth, biomass allocation, maximum photochemical efficiency (F _v/F _m) and plant water potential (Ψ). Either an increase in temperature or a reduction in water input alone reduced seedling performance, but the highest impact occurred when these two factors acted in combination. Warming and water limitation reduced Ψ, whereas warming alone reduced biomass allocation to roots and F _v/F _m. However, species responded differentially to warmer and drier conditions, with lowland Mediterranean pines (P. halepensis and P. pinaster) showing higher survival and performance than mountain species. Interspecific differences in response to warmer, drier conditions could contribute to changes in the relative dominance of these pine species in Mediterranean regions where they co-occur and a hotter, drier climate is anticipated.     

Carcinophyly of fish of the genus Careproctus (Scorpaeniformes: Liparidae) in waters of southeastern Sakhalin (Sea of Okhotsk)

In waters of southeastern Sakhalin (Sea of Okhotsk), clutches of snailfishes of the genus Careproctus containing eggs at different stages of development or prolarvae were found on gills of the largest individuals (mainly in males) of three species of crabs (Lithodidae)-Paralomis verrilli (clutches were found in 1.4% of individuals), P. multispina (0.8%), and Lithodes covesi (11.6%). With an increase in the carapace width of lithodid crabs, the amount of eggs of snailfishes deposited in them and their diameter increase. More frequently, clutches are located from the left side of the carapace of crabs. Two-side clutches occur in larger individuals of crabs. No direct relationship between the presence of clutches of snailfishes on gills of lithodid crabs with necrosis or reduction of gills was revealed. The form of relations between lithodid crabs and Careproctus snailfishes was defined as “lodging” with different degree of impact on the host.     

Different Temperature and Cooling Patterns at the Blunt and Sharp Egg Poles Reflect the Arrangement of Eggs in an Avian Clutch

Incubation is an energetically demanding process during which birds apply heat to their eggs to ensure embryonic development. Parent behaviours such as egg turning and exchanging the outer and central eggs in the nest cup affect the amount of heat lost to the environment from individual eggs. Little is known, however, about whether and how egg surface temperature and cooling rates vary among the different areas of an egg and how the arrangement of eggs within the clutch influences heat loss. We performed laboratory (using Japanese quail eggs) and field (with northern lapwing eggs) experiments using infrared imaging to assess the temperature and cooling patterns of heated eggs and clutches. We found that (i) the sharp poles of individual quail eggs warmed to a higher egg surface temperature than did the blunt poles, resulting in faster cooling at the sharp poles compared to the blunt poles; (ii) both quail and lapwing clutches with the sharp poles oriented towards the clutch centre (arranged clutches) maintained higher temperatures over the central part of the clutch than occurred in those clutches where most of the sharp egg poles were oriented towards the exterior (scattered clutches); and (iii) the arranged clutches of both quail and lapwing showed slower cooling rates at both the inner and outer clutch positions than did the respective parts of scattered clutches. Our results demonstrate that egg surface temperature and cooling rates differ between the sharp and blunt poles of the egg and that the orientation of individual eggs within the nest cup can significantly affect cooling of the clutch as a whole. We suggest that birds can arrange their eggs within the nest cup to optimise thermoregulation of the clutch.     

Identification of parasitized nests by using egg morphology in the Common Goldeneye: an alternative to blood sampling

We used data from three Common Goldeneye Bucephala clangula populations in Finland to study if the variation between females in egg morphology, as measured using a method developed by Eadie (1989), can be used to identify parasitized clutches. Eadie's method is based on z-score standardized measures of length, width, and weight of eggs. Using these measures, Euclidean distance for each pair of eggs within a clutch was calculated. Euclidean distance between the two most dissimilar eggs (maximum Euclidean distance, MED) was used as the criterion to identify parasitized clutches. Test clutches of 3 eggs that included one egg from each of three different females had a higher MED (2.80) than 3-egg clutches that included eggs from one female only (2.05), proving that there is statistically significant variation in egg morphology between females. Test clutches that included three eggs from each of three different females (9 eggs in all) had a mean MED of 4.51. The mean MED of naturally parasitized clutches (4.83) was higher than that of nonparasitized clutches (2.12). Further analyses suggested that MED>3.0 can be used as a conservative and reliable criterion to identify parasitized clutches. Our results confirm that Eadie's method is reliable enough to identify parasitized clutches in Common Goldeneyes.     

Age and season impact resource allocation to eggs and nesting behavior in the painted turtle

Theory predicts that in long-lived organisms females should invest less energy in reproduction and more in growth and self-maintenance early in life, with this balance shifting as females age and the relative value of each reproductive event increases. We investigated this potential trade-off by characterizing within-population variation in resource allocation to eggs by female painted turtles (Chrysemys picta) and relating this variation to their nesting ecology and life history. We examined lipid and protein allocation to yolks, accounting for both relative female age and seasonal effects (first vs. second clutches within a female). Older females appear to increase their investment in reproduction by producing larger eggs, but these eggs are not disproportionately more lipid or protein rich than the smaller eggs from younger females. Within the nesting season, first clutches have more lipid and protein than second clutches. We also found that younger females nest closer to the water than older females. Our results indicate that trade-offs involving resource allocation and nesting behavior do occur both seasonally and with age, suggesting ontogenetic variation in life-history strategies in this long-lived organism.