The influence of maternal thermal environments on reproductive traits and hatchling traits in a Lacertid lizard,Takydromus septentrionalis

The thermal environment can induce substantial variation in important life-history traits. Experimental manipulation of the thermal environment can help researchers determine the contribution of this factor to phenotypic variation in life-history traits. During the reproductive season, we kept female northern grass lizards, Takydromus septentrionalis (Lacertidae), in three temperature-controlled rooms (25, 28 and 32 °C) to measure the effect of the maternal thermal environment on reproductive traits. Maternal thermal environment remarkably affected reproductive frequency and thereby seasonal reproductive output, but had little effect on reproductive traits per clutch or hatchling traits. Females kept at 32 °C produced more clutches and thus had shorter clutch intervals than females from 28 to 25 °C. Clutch size, clutch mass, relative clutch mass, egg size and hatchling traits did not vary among the three treatments. The eggs produced by the females were incubated at 27 °C and the traits of hatchlings were measured. The result that egg (offspring) size was independent of maternal thermal environments is consistent with the prediction of the optimal egg size (offspring) theory. The eggs produced by low temperature females (28 and 25 °C) took longer time to complete their post-oviposition development than did eggs produced by high temperature females (32 °C). This suggests that the eggs from low temperatures might have been laid when the embryos were at relatively early stages. Therefore, maternal thermal environment prior to oviposition could affect post-oviposition development in T. septentrionalis.     

Parental food conditions affect sex-specific embryo mortality in the yellow-legged gull (Larus michahellis)

Different mortality of males and females during early post-hatching development in sexually size-dimorphic bird species is usually attributed to different nutritional requirements of the sexes, because mortality is mostly biassed toward the larger sex. We investigated whether sex-specific embryo mortality in the yellow-legged gull (Larus michahellis), a size-dimorphic seabird, depends on parental condition. To test this, we experimentally modified parental nutritional conditions by supplementary feeding of yellow-legged gulls during egg formation, to evaluate sex-biassed environmental sensitivity of gull embryos. We found that eggs were larger in supplemented clutches, but egg size did not affect embryo survival. Survival of male gull embryos was more related to parental food conditions than was survival of female embryos. Survival of male embryos in supplemented clutches was greater than in unsupplemented clutches whereas survival of female embryos was similar in both groups. Because size at hatching was similar in both sexes our results suggest that male phenotype disadvantage is not exclusively linked to the energy demands of size-dimorphic development at the embryo stage.     

Development and the influence of nurse egg allotment on hatching size in Searlesia dira (Reeve, 1846) (Prosobranchia : Buccinidae)

The reproductive biology of the intertidal prosobranch Searlesia dira (Reeve, 1846) was examined with special attention given to variability in the nurse egg to embryo ratio among capsules, among clutches and among geographically isolated populations. Embryos and nurse eggs were distributed among the capsules in a manner consistent with the hypothesis that nurse eggs were genetically predetermined, that each female had a genetically defined nurse egg to embryo ratio, and that each capsule represented a random sample of that ratio. The binomial distribution of embryos and nurse eggs among the capsules resulted in some capsules receiving many more embryos per nurse egg than others. The number of nurse eggs an embryo succeeded in eating was proportional to the number of capsule-mates sharing a capsule. Embryos eating more nurse eggs hatched out at a larger size. Differences in the nurse egg to embryo ratios among capsules in the same clutch were much larger than that of the mean ratios among clutches. Among-site differences in the mean nurse egg to embryo ratios suggest that selection pressure for different mean hatching sizes may have acted on the mean nurse egg to embryo ratios.In contrast to the predictions of optimal hatching size theory, hatching size varied widely within clutches as a consequence of differences in nurse egg to embryo ratios among capsules. This variance may be adaptive for species that lay their eggs months before juveniles emerge into an unpredictable environment, or simply be a consequence of an imperfect mechanism for increasing hatching size.     

Altitudinal variation in egg retention and rates of embryonic development in oviparous Zootoca vivipara fits predictions from the cold-climate model on the evolution of viviparity

The evolution of reptilian viviparity is favoured, according to the cold‐climate hypothesis, at high latitudes or altitudes, where egg retention would entail thermal benefits for embryogenesis because of maternal thermoregulation. According to this hypothesis, and considering that viviparity would have evolved through a gradual increase in the extent of intrauterine egg retention, highland oviparous populations are expected to exhibit more advanced embryo development at oviposition than lowland populations. We tested for possible differences in the level of egg retention, embryo development time and thermal biology of oviparous Zootoca vivipara near the extreme altitudinal limits of the species distribution in the north of Spain (mean altitude for lowland populations, 235 m asl.; for highland populations, 1895 m asl.). Altitude influenced neither temperature of active lizards in the field nor temperature selected by lizards in a laboratory thermal gradient, and pregnant females selected lower temperatures in the thermal gradient than did males and nonpregnant females across altitudinal levels. Eggs from highland populations contained embryos more developed at the time of oviposition (Dufaure and Hubert's stages 33–35) than eggs of highland populations (stages 30–34) and partly because of this difference incubation time was shorter for highland embryos. When analysed for clutches from both altitudinal extremes at the same embryonic stage at oviposition (stage 33), again incubation time was shorter for highland populations, indicating genuine countergradient variation in developmental rate. Our results indicate that temperature is an environmental factor affecting the geographical distribution of different levels of egg retention in Z. vivipara, as predicted by the cold‐climate hypothesis on the evolution of viviparity.     

Plasticity and limitations of extended egg retention in oviparous Zootoca vivipara (Reptilia: Lacertidae)

The transition between oviparity and viviparity in reptiles is generally accepted to be a gradual process, the result of selection for increasingly prolonged egg retention within the oviduct. We examined egg retention plasticity in an oviparous strain of the lacertid lizard Zootoca vivipara, a species having both oviparous and viviparous populations. We forced a group of female Z. vivipara to retain their clutch in utero by keeping them in dry substrata, and assessed the effect on embryonic development and hatching success, along with offspring phenotype and locomotor performance. Forced egg retention for one additional week affected the developmental stage of embryos at oviposition, as well as hatchling robustness and locomotor performance. However, embryos from forced clutch retention treatment reached one stage unit more than control embryos at oviposition time. Embryos from control eggs were more developed than embryos from experimental eggs after approximately the same period of external incubation, showing that embryonic development is retarded during the period of extended egg retention, despite the high temperature inside the mother's body. Significant differences in external incubation time were only found in one of the two years of study. Hatching success was much lower in the experimental group with forced egg retention (21.1%) than in the control group (95.4%). Therefore, we conclude that there are limitations that hinder the advance of intrauterine embryonic development beyond the normal time of oviposition, and that extended egg retention does not represent clear advantages in this population of Z. vivipara. Nevertheless, the fact that some eggs are successful after forced egg retention could be advantageous for the females that are able to retain their clutch under unfavourable climatic conditions. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 75–82.     

Photosynthetic responses of Zostera marina L. (Eelgrass) to in situ manipulations of light intensity

Summary Photosynthetic responses of the temperate seagrass, Zostera marina L., were examined by manipulations of photon flux density in an eelgrass bed in Great Harbor, Woods Hole, MA during August 1981. Sun reflectors and light shading screens were placed at shallow (1.3 m) and deep (5.5 m) stations in the eelgrass bed to increase (+35% to +40%) and decrease (-55%) ambient photon flux densities. The portion of the day that light intensities exceeding the light compensation point for Z. marina (H _comp) and the light saturation point (H _sat) were determined to assess the impact of the reflectors and shades. The H _comp and H _sat periods at the deep station shading screen were most strongly affected; H _comp was reduced by 11% and H _sat was reduced by 52%. Light-saturated photosynthetic rates, dark respiration rates, leaf chlorophyll content, chlorophyll a/b, PSU_{O 2} size, PSU density, leaf area, specific leaf area, leaf turnover times and leaf production rates were determined at the end of three sets of 1- to 2-week experiments. None of the measured parameters were affected by the photon flux density manipulations at the shallow station; however, at the deep station leaf production rates were significantly reduced under the shading screen and chlorophyll a/b ratios were higher at the reflector. These results indicate that adjustment to short-term changes in light regime in Z. marina is largely by leaf production rates. Further, the most dramatic changes in the periods of compensating or saturating photon flux densities had the greatest impact on the measured photosynthetic responses.     

Intrauterine and post-ovipositional embryonic development of Amerotyphlops brongersmianus (Vanzolini, 1976) (Serpentes: Typhlopidae) from northeastern Argentina

The reproductive biology and embryonic development of Typhlopidae have rarely been explored. This family of snakes includes mostly oviparous species with uterine egg retention, but the morphology and development of embryos remain unknown. This work aimed to describe the embryonic development of Amerotyphlops brongersmianus from the northeast of Argentina. For this purpose, embryos from intrauterine eggs of gravid females and eight post-ovipositional eggs incubated in the laboratory were analyzed. Embryonic stages, corresponding to the early, mid and advanced development, and a hatchling were described. The main organs and systems form during the period of intrauterine embryonic retention. Comparing to other snakes, differences in the development of cranial structures such as encephalic vesicles and mandibular and maxillary processes were identified. After oviposition the development and differentiation of the tissues and organs completes, the body scales develop, the characteristic pattern of pigmentation establishes and the embryo grows and consumes the yolk. On average, the incubation period lasts 55 days. Differences in the stage of development at oviposition among females of different populations were observed. Embryonic retention could extend up to advanced stages of development.     

Access to multiple mates increases fecundity but does not affect per‐offspring maternal investment in a marine gastropod

Females of many organisms mate more than once and with more than one male, suggesting that polyandry confers some advantage to the female or her offspring. However, variation in maternal investment in response to mate choice and mate number can confound efforts to determine if there are benefits of polyandry. Access to multiple mates could increase maternal investment in offspring via a number of different mechanisms. Few studies have determined if investment is influenced by mate choice and number, and data are particularly lacking for marine invertebrates. This study was designed to determine if maternal investment and offspring size increase with access to increasing numbers of mates in the protandrous intertidal slipper snail Crepidula cf. marginalis. Virgin female slipper limpets were exposed to one, three, or five potential mates and their fecundity, egg size, and hatchling size were measured for multiple clutches. Treatment had a significant effect on fecundity, with fecundity increasing with the number of potential mates. Treatment did not have an effect on the size of eggs or hatchlings, on the variation in egg size or hatchling size within broods, or on the frequency of oviposition. Treatment did alter the variation in average offspring size among females, but not in the way predicted by theory. The main result, that access to multiple mates does not have an effect on per offspring maternal investment, makes C. cf. marginalis an ideal candidate to study the effects of polyandry on offspring fitness without having to take into account confounding effects of variation in maternal investment.     

Position of egg within a clutch is linked to size at hatching in a demersal tropical fish

Size variation among propagules is ubiquitous and small initial differences in size can be critical to survival, particularly in taxa where initial survival is variable and strongly size-dependent. Despite this, the sources of size variation among fish at hatching are rarely investigated. This study examined spatial position within egg clutches as a source of size variation at hatching of the benthic spawning fish Amphiprion melanopus. We quantified within-clutch size variation at hatching and found that newly hatched larvae from the periphery (5 mm from edge) of 2-dimensional clutches were smaller in standard length, cranial depth, eye diameter and body area (7%, 8%, 4% and 11%, respectively) than larvae from the interior positions within clutches. To investigate the source of this variation, sizes of embryos at different locations with clutches were measured within 2 h of fertilisation (8 d before hatching). Newly laid embryos from the clutch periphery were smaller in length and volume than embryos from the clutch interior (> 2% and 4-6%, respectively). These eggs from the periphery also had a 33% lower rate of oxygen consumption than did embryos from the clutch interior, throughout development. The relationships between position within a clutch and egg size, oxygen consumption and larval size imply that size variation in larval fish at hatching is partly generated during early embryogenesis, either from maternal endowment or maternal nest design, and was amplified throughout development.     

Growth and uptake of mineral by embryos of the direct-developing frog Eleutherodactylus coqui

Embryos of the direct-developing frog Eleutherodactylus coqui take up small quantities of yolk and yolk mineral early in incubation but increase their uptake of yolk reserves at later stages of development. Growth and accumulation of calcium and magnesium by embryos also occur slowly at first and at a higher rate later. Accumulation of calcium and magnesium by embryos is largely a function of variation in size of embryos, but uptake of phosphorus is unrelated to size. Althrough patterns of growth and uptake of mineral by embryonic coquis resemble those for embryos of oviparous amniotes, embryonic coquis do not deplete the yolk of its nutrients to the same degree. Thus, residual yolk of coqui hatchlings contains a high percentage of the nutrient reserves originally present in the egg. This difference between embryonic coquis and embryos of oviparous amniotes may indicate that transfer of nutrients from yolk to embryo becomes limiting during the grwoth phase. Alternatively, some aspects of the neurologic system are so poorly developed at hatching that coqui may not be able to find prey effectively. A large nutrient reserve could sustain hatchling while the neurologic system continues to mature.     

Factors influencing the embryonic development and hatchling size of the oceanic squid Illex coindetii following in vitro fertilization

Egg masses of oceanic squid accidently collected in the wild have been observed only from a few spawning events in aquaria, and as a consequence, the study of their embryos and hatchlings is very limited. Here, we used in vitro fertilization techniques to understand the abiotic factors that influenced egg development and hatchling performance of the ommastrephid squid Illex coindetii from the Mediterranean Sea. Egg and hatchling sizes of these ommastrephids are close to the minimum for cephalopod species, and therefore, short embryonic developmental periods were expected under a Mediterranean temperature regime. Low incubation densities and the use of antibiotics in the incubation medium resulted in relatively high survival rates to hatchling. Hatching time was inversely proportional to incubation temperature and ranged from 5 to 11 days at 21 °C and 13 °C, respectively. The addition of oviducal jelly to the eggs immediately after fertilization, followed by another addition at the beginning of organogenesis, resulted in better chorionic expansion, with an increase in egg diameter, delayed hatching and higher hatchling weight, which suggests a better use of yolk reserves. Larger hatchlings in length and weight also tended to be produced at low temperature, probably also due to better yolk absorption. As this species spawns all year round, size differences between summer and winter hatchlings may be suspected. In vitro fertilization techniques used in the laboratory proved to be useful in shedding some light on the early life of this oceanic squid. Further research is needed to elaborate on tests to predict gamete quality and to develop methods to avoid premature hatching.     

Hypoxia and temperature: Does hypoxia affect caiman embryo differentiation rate or rate of growth only?

In crocodilians, the rate of embryonic development and consequently many posthatch attributes are affected by temperature. Since temperature exhibits strong influences on fitness (embryo survivorship and phenotype) by shaping development, we manipulated oxygen concentration in order to uncouple the effects of developmental rate from the direct effects of temperature. Here we consider whether oxygen constrains either differentiation rate (progression from one stage to the next) or embryonic growth (size). Thus, we incubated Caiman latirostris eggs at various oxygen concentrations, and at two temperatures (31 °C, 100% female-producing temperature, and 33 °C, 100% male-producing temperature). We monitored the developmental stages of these embryos within the thermosensitive period (stages 20–24), and assessed several physiological and morphological hatchling traits. While embryonic size was strongly influenced by oxygen, differentiation rate did not seem to be affected. Very low oxygen concentrations and high temperatures inhibited embryo survival. In addition, oxygen availability affected incubation period and hatchling size, whereas temperature did not cause a significant variation in hatchling size. By investing energy in differentiation hypoxic embryos decreased their size.     

Embryos of non-native anoles are robust to urban thermal environments

The transformation of natural habitats into urban landscapes dramatically alters thermal environments, which in turn, can impact local biota. Ectothermic organisms that are oviparous are particularly sensitive to these altered environments because their embryos cannot behaviorally thermoregulate and the surrounding environment determines the temperature experienced during development. We studied the effects of urban and forested thermal environments on embryo development and hatchling phenotypes in two non-native lizards (Anolis sagrei and A. cristatellus) in metropolitan Miami, Florida. To determine if embryos from urban and forested sites are adapted to their respective thermal environments, we incubated eggs from each site using temperatures that simulate likely nest conditions in both urban and forested environments. For both species, urban thermal environments accelerated embryonic development, but had no impact on egg survival or any of the phenotypic traits that were measured (e.g., body size, running performance, and locomotor behavior). Our results provide no evidence that embryos from urban and forested sites are adapted to their respective thermal environments. Instead, the lack of any major effects suggest that embryos of both species are physiologically robust with respect to novel environments, which could have facilitated their success in establishing in non-native ranges and in human-modified landscapes.     

Influence of egg size differences within egg clutches on larval parameters in nine libellulid species (Odonata)

Abstract.  1. In libellulids, egg size differs between species and populations. There are also size differences within egg clutches of individual females.
2. Past experiments suggest that there are two different types of egg clutches in libellulids. Egg size decreases significantly during oviposition in species that perform non-contact guarding during oviposition. In contrast, in species ovipositing in tandem, egg size is randomly distributed.
3. This study deals with the possible consequences of egg size variation within the different egg clutch types. The study examined whether there is a correlation between egg development time, offspring sex or larval size and egg size.
4. The current experiments were conducted in Namibia and Germany. Five non-contact guarding and four tandem guarding libellulid species were used.
5. In some species larger eggs needed more time to develop, in some species no correlation between egg size and egg development time could be found, whereas in other species larger eggs developed faster.
6. The sex ratio was biased towards females in Leucorrhinia dubia and in Sympetrum striolatum and egg size was not associated with gender.
7. In both egg clutch types larger eggs resulted in larger larvae. In this study, evidence was found that the effects of egg size diminished with progressing larval development under good conditions. However, it is possible that the effects may have a greater influence under harsh circumstances.     

The seasonal timing of oviposition in sand lizards (Lacerta agilis): why early clutches are better

We studied a population of sand lizards (Lacerta agilis) near the northern edge of the species' range in coastal Sweden. We captured, marked, released and recaptured 98 adult female lizards over 5 years. Hatchlings from 146 laboratory-incubated clutches (1279 eggs) from field-caught gravid females were measured, weighed, marked and released at the study site. Female sand lizards usually laid only a single clutch of 4 to 15 eggs each year, but varied considerably in the time of year at which they laid their eggs. Oviposition dates shifted between years depending on weather (basking opportunities), but the relative timing of oviposition was consistent within a given female from year-to-year. The first females to oviposit each year were large animals in good physical condition, that had grown rapidly in previous years. “Early” clutches were larger than “later” clutches, had higher hatching success, and tended to have higher post-hatching survival rates. Offspring from early clutches were larger than “later” hatchlings, and differed in body proportions (probably because seasonal changes in maternal temperatures directly modified offspring phenotypes). Overall, our study documents several strong correlates of the timing of oviposition, and suggests that variation in this trait among females has strong fitness consequences, perhaps related to maternal “quality”. The correlations we observed between oviposition date and other traits that have been invoked as determinants of hatchling survival in reptiles (e.g., hatchling size, body shape, opportunities for multiple mating by the mother) suggest that hypotheses advocating simple causal connections between these traits and hatchling success should be viewed with caution.     

Seasonal acclimation in metabolism reduces light requirements of eelgrass (Zostera marina)

We investigated the ability of eelgrass (Zostera marina) to adjust light requirements to seasonal changes in temperature, light and nutrient conditions through changes in metabolism, pigment and nutrient content. In agreement with expectations we found that rates of respiration and light saturated photosynthesis of summer acclimated plants peaked at higher temperatures (5 °C and 2 °C higher, respectively), and were lower than of winter acclimated plants, both at sub- and supra-optimal temperatures. Moreover respiration rates were generally more sensitive to increasing temperatures than photosynthetic rates, especially so for cold acclimated plants in February (36% higher Q₁₀-values). These changes were accompanied by a reduction in chlorophyll a and nitrogen concentrations in leaves by 35% and 60% respectively from February to August. The critical light requirement (E_C) of Z. marina to maintain a positive carbon balance increased exponentially with increasing temperature but less so for summer-acclimated than for winter-acclimated plants. However, combining E_C vs temperature models for whole-plants with data on daily light availability showed that seasonal acclimation in metabolism increased the annual period, when light requirements were meet at the 2-5 m depth interval, by 32-66 days. Hence, acclimation is an important mechanism allowing eelgrass to grow faster and penetrate to deeper waters. Critical depth limits estimated for different combinations of summer temperatures and water clarity in a future climate scenario, suggested that expected increases in temperature and nutrient run-off have synergistic negative effects, especially in clear waters, stressing the importance of continued efforts to improve water clarity of coastal waters.     

Geographic variation in hatchling size in an oviparous skink: effects of maternal investment and incubation thermal environment

Geographic variation in offspring size can be viewed as an adaptive response to local environmental conditions, but the causes of such variation remain unclear. Here, we compared the size and composition of eggs laid by female Chinese skinks (Plestiodon chinensis) from six geographically distinct populations in southeastern China to evaluate geographic variation in hatchling size. We also incubated eggs from these six populations at three constant temperatures (24, 28 and 32 °C) to evaluate the combined effects of incubation temperature and population source on hatchling size. Egg mass and composition varied among populations, and interpopulation differences in yolk dry mass and energy content were still evident after accounting for egg mass. Population mean egg mass and thus hatchling mass were greater in the colder localities. Females from three northern populations increased offspring size by laying larger eggs relative to their own size. Females from an inland population in Rongjiang could increase offspring size by investing relatively more dry materials and thus more energy into individual eggs without enlarging the size of their eggs. The degree of embryonic development at oviposition was almost the same across the six populations, so was the rate of embryonic development and thus incubation length at any given temperature. Both incubation temperature and population source affected hatchling traits examined, but the relative importance of these two factors varied between traits. Our data show that in P. chinensis hatchling traits reflecting overall body size (body mass, snout‐vent length and tail length) are more profoundly affected by population source. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 283–296.     

Count Your Eggs Before They Invade: Identifying and Quantifying Egg Clutches of Two Invasive Apple Snail Species (Pomacea)

Winning the war against invasive species requires early detection of invasions. Compared to terrestrial invaders, aquatic species often thrive undetected under water and do not garner notice until too late for early action. However, fortunately for managers, apple snails (Family Ampullariidae, Genus Pomacea) provide their own conspicuous sign of invasion in the form of vibrantly colored egg clutches. Managers can potentially use egg clutches laid in the riparian zone as a means of early detection and species identification. To facilitate such efforts, we quantified differences in characteristics (length, width, depth, mass, egg number) of field-laid clutches for the two most common invasive species of apple snail, P. canaliculata and P. maculata, in native and non-native populations. Pomacea canaliculata native and non-native populations differed noticeably only in width. Native P. maculata clutches possessed significantly greater width, mass and eggs numbers compared with native P. canaliculata. Non-native P. maculata clutches significantly exceeded all other populations in all measured characteristics. Consequently, these traits may successfully distinguish between species. Fecundity data also allowed us to develop models that accurately estimated the number of eggs per clutch for each species based on clutch dimensions. We tested one, two and three dimensional models of clutches, including rendering a clutch as either a complete ellipsoid or an ellipsoid intersected by a cylinder to represent the oviposition site. Model comparisons found the product of length and depth, with a different function for each population, best predicted egg number for both species. Comparisons of egg number to clutch volume and mass implied non-native P. canaliculata may be food limited, while non-native P. maculata appeared to produce such enormous clutches by having access to greater nutrients than the native population. With these new tools, researchers and managers can quickly identify, quantify and begin eradication of new non-native apple snail populations.     

Effects of light on seagrass photosynthesis,growth and depth distribution

The relationships between light regime, photosynthesis, growth and depth distribution of a temperate seagrass, Zostera marina L. (eelgrass), were investigated in a subtidal eelgrass meadow near Woods Hole, MA. The seasonal light patterns in which the quantum irradiance exceeded the light compensation point (H_comp) and light saturation point (H_sat) for eelgrass photosynthesis were determined. Along with photosynthesis and respiration rates, these patterns were used to predict carbon balances monthly throughout the year. Gross photosynthesis peaked in late-summer, but net photosynthesis peaked in spring (May), due to high respiration rates at summer temperatures. Predictions of net photosynthesis correlated with in situ growth rates at the study site and with reports from other locations.The maximum depth limit for eelgrass was related to the depth distribution of H_comp, and a minimum annual average H_comp (12.3 h) for survival was determined. Maximum depth limits for eelgrass were predicted for various light extinction coefficients and a relationship between Secchi disc depth and the maximum depth limit for survival was established. The Secchi disc depth averaged over the year approximates the light compensation depth for eelgrass. This relationship may be applicable to other sites and other seagrass species.