Average Incubation Temperature Research Articles

Incubation temperature as a constraint on clutch size evolution

Abstract Elucidating factors that limit the number of offspring produced is fundamental to understanding life‐history evolution. Here, we examine the hypothesis that parental ability to maintain an optimal physical developmental environment for all offspring constrains clutch size via effects on offspring quality. Experimental laboratory studies of birds have shown that a <1°C difference in average incubation temperature has diverse effects on fitness‐related post‐hatching offspring phenotypes. Thus, the inability of parents to maintain optimal incubation temperatures could constrain clutch sizes. A fundamental question that has not been sufficiently addressed is whether larger clutch sizes lead to within nest variation in egg temperature that is large enough to produce offspring with different phenotypes within a brood. This could lead to differential survival among offspring, and could create a trade‐off between offspring number and quality. We manipulated clutch size in nests of free‐living wood ducks and measured incubation temperature among and within clutches using multiple temperature loggers. As clutch size increased, average incubation temperatures were lower and more variable, and eggs took longer to hatch. Notably, the range in average incubation temperature among eggs within nests increased with clutch size and exceeded 1°C in large clutches. Clutch size did not affect hatch success. In conjunction with our companion laboratory studies that used artificial incubation to document the effects of temperature variation on fitness‐related traits in this species, our work suggests that suboptimal incubation temperatures could be a factor that limits clutch size through diminishing returns on post‐hatch offspring quality. A free plain language summary can be found within the Supporting Information of this article.

Incubation Temperature Affects Duckling Body Size and Food Consumption Despite No Effect on Associated Feeding Behaviors.

SynopsisDevelopmental conditions can have consequences for offspring fitness. For example, small changes (<1°C) in average avian incubation temperature have large effects on important post-hatch offspring phenotypes, including growth rate, thermoregulation, and behavior. Furthermore, average incubation temperatures differ among eggs within the same nest, to the extent (i.e., >1°C) that differences in offspring phenotypes within broods should result. A potential consequence of within-nest incubation temperature variation is inequality in behaviors that could cause differences in resource acquisition within broods. To investigate this, we incubated wood duck (Aix sponsa) eggs at one of two ecologically-relevant incubation temperatures (35°C or 36°C), formed mixed-incubation temperature broods after ducklings hatched, and conducted trials to measure duckling behaviors associated with acquisition of heat (one trial) or food (three trials). Contrary to our predictions, we found no effect of incubation temperature on duckling behaviors (e.g., time spent occupying heat source, frequency of feeding bouts). However, we found evidence that ducklings incubated at the higher temperature consumed more food during the 1-h feeding trials, and grew faster in body mass and structural size (culmen and tarsus) throughout the study, than those incubated at the lower temperature. Apparent food consumption during the trials was positively related to culmen length, suggesting that differences in food consumption may be driven by structural size. This could result in positive feedback, which would amplify size differences between offspring incubated at different temperatures. Thus, our study identifies incubation temperature as a mechanism by which fitness-related phenotypic differences can be generated and even amplified within avian broods.

Early developmental responses of three sea urchin species to tralopyril and its two degradation products

Tralopyril (TLP) is a newly emerged antifouling biocide which rapidly degrades in water. The scientific data on its possible adverse effects to biota is very limited, and even more limited is the ecotoxicity data of its degradation products (DPs). In the present study we investigated the toxicity of TLP and its two main DPs on fertilization and embryogenesis of three sea urchin species: Clypeaster japonicus, Pseudocentrotus depressus and Hemicentrotus pulcherrimus. The species sensitivity to chemicals was investigated and compared. Additionally, the stability of TLP in test medium was examined.TLP in test medium degraded into one single degradation product. The degradation was slower at 17 °C (average incubation temperature for winter species H. pulcherrimus) than at 20 °C (incubation temperature for the other two species). Both DPs at 100 μg/L did not appear toxic, however, TLP highly affected larval development of all tested species. Sensitivity was similar for C. japonicus and P. depressus, but higher toxicity was noticed for H. pulcherrimus. The increased TLP toxicity on exposed H. pulcherrimus embryos could be attributed to the higher TLP stability at lower incubation temperature. Results suggest higher vulnerability to TLP for species spawning in colder seasons. Fertilization test appeared to be less sensitive than the embryotoxicity test.

Delimitation of the embryonic thermosensitive period for sex determination using an embryo growth model reveals a potential bias for sex ratio prediction in turtles

The sexual phenotype of the gonad is dependent on incubation temperature in many turtles, all crocodilians, and some lepidosaurians. At hatching, identification of sexual phenotype is impossible without sacrificing the neonates. For this reason, a general method to infer sexual phenotype from incubation temperatures is needed. Temperature influences sex determination during a specific period of the embryonic development, starting when the gonad begins to form. At constant incubation temperatures, this thermosensitive period for sex determination (TSP) is located at the middle third of incubation duration (MTID). When temperature fluctuates, the position of the thermosensitive period for sex determination can be shifted from the MTID because embryo growth is affected by temperature. A method is proposed to locate the thermosensitive period for sex determination based on modelling the embryo growth, allowing its precise identification from a natural regime of temperatures. Results from natural nests and simulations show that the approximation of the thermosensitive period for sex determination to the middle third of incubation duration may create a quasi-systematic bias to lower temperatures when computing the average incubation temperature during this period and thus a male-bias for sex ratio estimate.

Long-term consequences of high incubation temperature in a wild bird population.

Because incubation by birds is energetically costly, parents frequently trade off investment in incubation against self-maintenance. This can be manifested by a reduction in incubation temperature, which comes at high somatic costs for nestlings. The extent to which these costs constrain fitness is poorly understood. We incubated wild blue tit clutches at three biologically relevant temperatures and subsequently recorded winter survival and survival to the breeding season. Fledglings from the coldest treatment (35.0°C) survived less well than other fledglings, but the proportion of winter and breeding survivors did not differ significantly between treatments. However, survival probability in both seasons increased with body mass at fledging in birds from low and mid incubation temperatures, but decreased with fledging body mass in the high-temperature treatment. Mid-temperature nestlings were heavier as adults, weighing 7% more than low- and high-temperature survivors. Thus, high incubation temperature can be beneficial in the short term, but costs of accelerated embryonic development may equal those of protracted development in the long term. Such hidden consequences of faster development could maintain natural selection for average incubation temperature.

Local variation in weather conditions influences incubation behavior and temperature in a passerine bird

Incubation is an important component of avian parental care and slight changes in incubation temperature can affect offspring phenotype. Although many extrinsic and intrinsic factors may generate variation in incubation temperature, they remain underexplored under natural conditions. Using a robust data set encompassing 55 nests, 22 816 behavioral observations, and &gt; 1 million paired ambient and egg temperatures, we describe the relationships among abiotic factors, female incubation behavior, incubation temperature, and incubation period for tree swallows Tachycineta bicolor. We report a large amount of individual variation in incubation behaviors and average incubation temperatures for our study population. The average on‐bout incubation temperature was 34.1°C, with daily egg temperatures ranging from 18.0–39.2°C. Females modulated the number of times they left the nest and the amount of time they stayed off the nest according to interactions between precipitation and temperature patterns. Models generated from our observations predicted that the number of female off‐bouts was the lowest under warm and dry conditions while more off‐bouts were taken under cold and dry or warm and wet conditions. During cold and dry conditions, females stayed off their nest ∼4 times longer than under warm and dry conditions. However, this pattern was reversed under periods of rainfall; females tended to take shorter off‐bouts when it was rainy and cold compared to longer off‐bouts during warmer rain events. Furthermore, variation in female behavior was associated with differences in overall incubation temperature such that females that maintained greater incubation constancy produced higher incubation temperatures at a given ambient temperature than those that displayed lower incubation constancy. Our results provide perspective on the timing of breeding, as some of the advantages of breeding early may be countered by cooler, early season temperatures and precipitation that cause reproducing females to favor self‐maintenance at a potential cost to optimal incubation temperatures for offspring development.

Temperature experienced during incubation affects antioxidant capacity but not oxidative damage in hatchling red-eared slider turtles (Trachemys scripta elegans).

Our understanding of how oxidative stress resistance phenotypes are affected by the developmental environment is limited. One component of the developmental environment, which is likely central to early life oxidative stress among ectothermic and oviparous species, is that of temperature. We investigated how incubation temperature manipulations affect oxidative damage and total antioxidant capacity (TAC) in red-eared slider turtle (Trachemys scripta elegans) hatchlings. First, to determine whether temperature fluctuations elicit oxidative stress, eggs from clutches were randomly assigned to either a constant (29.5 °C) or daily fluctuating temperature incubation (28.7 ± 3 °C) treatment. Second, to assess the effect of temperature fluctuation frequency on oxidative stress, eggs were incubated in one of three fluctuating incubation regimes: 28.7 ± 3 °C fluctuations every 12 h (hyper), 24 h (normal) or 48 h (hypo). Third, we tested the influence of average incubation temperature by incubating eggs in a daily fluctuating incubation temperature regime with a mean temperature of 26.5 °C (low), 27.1 °C (medium) or 27.7 °C (high). Although the accumulation of oxidative damage in hatchlings was unaffected by any thermal manipulation, TAC was affected by both temperature fluctuation frequency and average incubation temperature. Individuals incubated with a low frequency of temperature fluctuations had reduced TAC, while incubation at a lower average temperature was associated with enhanced TAC. These results indicate that although sufficient to prevent oxidative damage, TAC is influenced by developmental thermal environments, potentially because of temperature-mediated changes in metabolic rate. The observed differences in TAC may have important future consequences for hatchling fitness and overwinter survival.

Influence of incubation recess patterns on incubation period and hatchling traits in wood ducks Aix sponsa

Parental effects are influential sources of phenotypic variation in offspring. Incubation temperature in birds, which is largely driven by parental behavior and physiology, affects a suite of phenotypic traits in offspring including growth, immune function, stress endocrinology, and sex ratios. The importance of average incubation temperature on offspring phenotype has recently been described in birds, but parental incubation behaviors like the duration and frequency of recesses from the nest can be variable. There are few studies describing how or if thermal variation as a result of variable incubation affects offspring phenotype. We incubated wood duck Aix sponsa eggs under three different incubation regimes, based on patterns that occur in nature, which varied in off‐bout duration and/or temperature. We measured incubation period, morphometrics at hatching, and monitored growth and body condition for nine days post hatch. When average incubation temperature was allowed to drop from 35.9°C to 35.5°C as a result of doubled off‐bout duration, we found a significant 2 d extension in incubation period, but no effects on duckling hatch mass, or growth and body condition up to nine days post hatch. However, when average incubation temperatures were equivalent (35.9°C), doubling the duration of the simulated off‐bouts did not influence incubation period or any post hatch parameters. Our results suggest that if incubating parents can maintain favorable thermal environments in the nest via altered behavior (e.g. manipulating nest insulation) and/or physiology (e.g. heat production), parents may be able to avoid the costs of longer incubation periods resulting from increased off‐bout duration.

Nesting Ecology and Conservation of the Loggerhead Sea Turtle (Caretta caretta) in Rio de Janeiro, Brazil

Loggerhead turtle (Caretta caretta) nesting in the Southwest Atlantic has been monitored for decades, but information from northern Rio de Janeiro State (Brazil) has been lacking until now. In this study, we documented 11,086 nests laid between the 1992/1993 and 2010/2011 nesting seasons (∼1000 nests per season) and found significant variations in incubation period and hatching success among in situ and relocated nests. Because loggerhead nests in Rio de Janeiro are presumed to produce a large proportion of male hatchlings because of lower average incubation temperatures, this area is an important component of loggerhead population biology and conservation in Brazil and the southwest Atlantic region.

Seasonal variations in larval biomass and biochemical composition of brown shrimp, Crangon crangon (Decapoda, Caridea), at hatching

The “brown shrimp”, Crangon crangon (Linnaeus 1758), is a benthic key species in the North Sea ecosystem, supporting an intense commercial fishery. Its reproductive pattern is characterized by a continuous spawning season from mid-winter to early autumn. During this extended period, C. crangon shows significant seasonal variations in egg size and embryonic biomass, which may influence larval quality at hatching. In the present study, we quantified seasonal changes in dry weight (W) and chemical composition (CHN, protein and lipid) of newly hatched larvae of C. crangon. Our data revealed significant variations, with maximum biomass values at the beginning of the hatching season (February–March), a decrease throughout spring (April–May) and a minimum in summer (June–September). While all absolute values of biomass and biochemical constituents per larva showed highly significant differences between months (P < 0.001), CHN, protein and lipid concentrations (expressed as percentage values of dry weight) showed only marginally significant differences (P < 0.05). According to generalized additive models (GAM), key variables of embryonic development exerted significant effects on larval condition at hatching: The larval carbon content (C) was positively correlated with embryonic carbon content shortly after egg-laying (r 2 = 0.60; P < 0.001) and negatively with the average incubation temperature during the period of embryonic development (r 2 = 0.35; P < 0.001). Additionally, water temperature (r 2 = 0.57; P < 0.001) and food availability (phytoplankton C; r 2 = 0.39; P < 0.001) at the time of hatching were negatively correlated with larval C content at hatching. In conclusion, “winter larvae” hatching from larger “winter eggs” showed higher initial values of biomass compared to “summer larvae” originating from smaller “summer eggs”. This indicates carry-over effects persisting from the embryonic to the larval phase. Since “winter larvae” are more likely exposed to poor nutritional conditions, intraspecific variability in larval biomass at hatching is interpreted as part of an adaptive reproductive strategy compensating for strong seasonality in plankton production and transitory periods of larval food limitation.

Intraspecific Variation of Reproductive Traits in a Mediterranean Lizard: Clutch, Population, and Lineage Effects

Widely distributed terrestrial ectotherms from the southern European peninsulas show patterns of subdivision (related to isolation in temperate refugia) that allow us to test the relative importance of phylogeographic lineage, population of origin and familial effects as sources of variation for life-history traits. We collected gravid females from 15 geographically separated populations of the lacertid lizard Psammodromus algirus, a widely distributed species with well differentiated eastern and western lineages. We incubated eggs under two treatments of constant (28°C) and fluctuating (28 ± 4°C) temperature, and we examined clutch, population, and lineage effects on several traits of females, eggs, and hatchlings. Incubation time was mainly explained by differences between lineages, but it was also influenced by population and female effects. Within each lineage, incubation was shorter at cooler and wetter sites, and for a given climate it was shorter for eastern than for western populations, suggesting that countergradient variation has evolved independently in the two lineages. Female size, clutch size, and relative fecundity were primarily influenced by inter-population differences, a pattern that seemed attributable to environmental differences in productivity, because mean female size was positively correlated with a gradient of increasing precipitation and decreasing temperature. Clutch size was mainly, but not entirely, dependent on female SVL, suggesting both a proximate effect of local conditions and intrinsic differences among populations. Females from drier and warmer sites produced larger hatchlings. Mean egg mass was mainly determined by familial effects. Eggs incubated at a constant temperature hatched earlier than did their siblings incubated at fluctuating temperatures, a fact that could be explained by considering that in Mediterranean environments developmental rate might increase at a lower speed above average incubation temperature than it does decrease below it.

Notes on ex-situ incubation and hatchlings of Eutropis carinata (Schneider, 1801) (Reptilia: Scincidae) from Sri Lanka

Eutropis carinata is widely distributed skink in Sri Lanka. This observation describes ex-situ incubation and hatching of this species at Colombo district in Sri Lanka. In total, 25 eggs with two adults of E. carinata were located from a termite mound while some villagers where trying to kill a cobra ( Naja naja ) living in the mound. Of these skink eggs, 20 were successfully incubated. The incubation period was 30 days from the date eggs were collected. The average incubation temperature varied from 26–28°C. Mean egg length was 15.6 mm and mean egg width 10.4 mm. Mean hatchling SVL was 28.5 mm and mean TL is 41.3 mm. The mean weight of hatchlings was ~3 g and the mean total length is 69.8 mm. After about five days, hatchlings were released at the original place of the clutch. Key Words: Eutropis carinata ; ex-situ incubation; egg hatching; conservation; Sri Lanka DOI: 10.4038/tapro.v1i1.2780 TAPROBANICA, April, 2009. Vol. 01, No. 01: pp. 63-65

Reproduction of the shorthorn sculpin Myoxocephalus scorpius in northern Norway

The reproduction and life history events of the shorthorn sculpin Myoxocephalus scorpius were studied in an unexploited high latitude population in Tromsø, northern Norway. Shorthorn sculpins were sampled from November 1998 to March 1999 to determine sex ratio, spawning period, oogenesis, fecundity, embryogenesis and hatching. Spawning occurred between January and March. The catches of males were maximal in January and February, while catches of predominantly immature females increased towards the end of the spawning period. This may be related to different migration patterns in males and females. It is possible that after spawning, females migrate to other areas, whereas males stay behind and guard the eggs. The spawned eggs were smaller than reported from other study areas. Larvae hatched after 7 weeks at an average egg incubation temperature of 3.3 °C. Fecundity in females ranged from 1200 to 29 000 eggs, with a length exponent of 3.0. The relatively large size (7.6–8.8 mm in length), advanced performance and developmental status at hatch of shorthorn sculpin larvae suggest that the reproductive strategy of the shorthorn sculpin is an intermediate between strategies that have many small larvae and those that have fewer, larger and more developed larvae.

Effect of treatment with formaldehyde and formic acid on immunoglobulin content of stored bovine colostrum

Colostrum was collected from the first postpartum milking of German Black Pied cows. Four independent pools of colostrum were made and the following preservation methods replicated in each pool, viz. formaldehyde treatment, 0.1% (F1) and 0.05% (F2); formic acid treatment, 0.5% (FA1) and 0.1% (FA2) and an untreated control (NF). All the colostrum batches were stored at an average incubation temperature of 28°C in 200-ml plastic bottles. Samples were collected from every batch on Day 0 (before incubation) and subsequently after every week for 4 weeks. All the samples collected were analysed for immunoglobulin (IgG1, IgG2, IgA and IgM) content of the whey fraction using the single radial immunodiffusion (SRID) method. pH was measured using a glass electrode pH meter.Formaldehyde treatment of colostrum maintained almost constant immunoglobulin levels under the conditions of this experiment. There were significant drops in the mean IgG1 (P < 0.0001) and IgM (P < 0.005) contents in the control (NF) and the formic acid treated (FA1 and FA2) colostrum. The levels of IgA and IgG2 remained fairly constant for all treatments and there was no observable trend with storage duration. The pH of formaldehyde treated colostrum remained above 4.8 for the 4 weeks of storage whereas that of the untreated control colostrum dropped to below pH 4.8 in the first 3 days and remained stable to the 4th week. This work has shown that inclusion of formaldehyde at levels as low as 0.05% (wt/vol.) preserves immunoglobulins of colostrum stored at high ambient temperature. The use of formic acid was not beneficial for preservation of colostral immunoglobulins. Thus colostrum preserved with formaldehyde may be of good feeding value for newborn calves whereas that preserved with formic acid may be useful only for older calves.

Temperature is a powerful promoter of interleukin 2 transcription

Elevated temperature has profound effects on the immune system, particularly by increasing T-cell proliferation rates, interleukin 1 (IL-1)-driven secretion of IL-2, and primary antibody responses to T-dependent antigens. Therefore, this study shows, in detail, the effects of incubation temperature (29°C to 41°C) on proliferation, IL-2 secretion, and IL-2 mRNA expression in both a murine thymoma cell line (EL4-6.1) and in nontransformed murine splenocytes. Temperature was found to be a positive regulator of IL-2 secretion whether or not IL-1 was part of the activation signal. Parallel effects were observed at the level of IL-2 gene expression. Messenger RNA was quantitated with a novel system, using solution hybridization followed by detection of RNA-DNA complexes by enzyme immunoassay. The time to onset of IL-2 mRNA expression was inversely related to temperature, and mRNA levels increased 20- to 50-fold with increases in average incubation temperature from 29°C to 39°C. This effect was observed whether cells were incubated at constant temperature or exposed intermittently to elevated temperature. Over the same intervals of time and temperature, mRNA levels for τ-actin and β-tubulin remained relatively constant. Taken together, these findings suggest that temperature-mediated augmentation of IL-2 secretion does not require the presence of IL-1, and that the effect occurs at a pretranslational level.

Prediction of Egg Development and Mortality Rates in Capelin (Mallotus viliosus) from Meteorological, Hydrographic, and Biological Factors

We studied the factors governing in situ egg development and mortality rates in beach spawning capelin (Mallotus villosus). Time to hatching was strongly influenced by the average incubation temperature which varied between years and between cohorts in a single year, and between positions on the beach (high, mid, low tide zone). Average incubation temperatures were determined by a complex of variables which included water temperature, maximum and minimum air temperature, and hours of sunlight. Mortality rates were both spatially and temporally variable. Over 70% of the temporal and spatial variance in egg mortality was attributed to the interacting effects of egg density, water temperature, maximum and minimum air temperature, hours of sunlight, rainfall, and tidal amplitude. Multivariate equations for predicting egg mortality as a function of these variables are given. The principal climatic and hydrographic variables influencing egg mortality vary only slightly over a 7° range of latitude encompassing the main spawning sites of the eastern Newfoundland and southern Labrador coasts. The potential thus exists for synchronous year to year changes in egg mortality over this spawning range as a result of annual variations in climate and hydrographic conditions. Such synchronous changes may contribute to the substantial year to year fluctuations in capelin year-class strength.Key words: capelin, Mallotus viliosus; development, mortality, meteorology, hydrology, temperature, intertidal zone, year-class, egg, beach spawning

The Wild Turkey in Louisiana

couple junction was in the air-cell compartment of the egg when the embryo pipped through the shell. The experiments were conducted with a flock of semiwild birds, the body temperatures of which, it is believed, should be similar to those in the wild. From this study it has been found that the average incubation temperature of the embryo is 101.30F., the average shell temperature 100.40F., the average breast temperature of the incubating goose 101.10F., the average maximum temperature reached in the nest 101.50F., and the usual incubation period 26 days. The fact that the incubation period was 5 days longer for eggs in a machine than for eggs under a goose, indicates that the incubator top temperature of 99.50F., is subnormal and should be raised at least 1.5 to 2 degrees. The temperature rises with the development of the embryo. There is a slight variation in temperature among various birds. The construction of the nest is a vital factor in the variation between top and bottom temperatures of eggs because of the amount of heat that is dissipated into the ground or nesting material on the underside of the egg.