Variation in reproductive output of marine turtles

Most marine turtle species are non-annual breeders and show variation in both the number of eggs laid per clutch and the number of clutches laid in a season. Large levels of inter-annual variation in the number of nesting females have been well documented in green turtle nesting populations and may be linked to environmental conditions. Other species of marine turtle exhibit less variation in nesting numbers. This inter-specific difference is thought to be linked to trophic status. To examine whether individual reproductive output is more variable in the herbivorous green turtle (Chelonia mydas Linneaeus 1758) than the carnivorous loggerhead (Caretta caretta Linneaeus 1758), we examined the nesting of both species in Cyprus over nine seasons. Green turtles showed slower annual growth rates (0.11 cm year⁻¹ curved carapace length (CCL) and 0.27 cm year⁻¹ curved carapace width (CCW)) than loggerhead turtles (0.36 cm year⁻¹ CCL, 0.51 cm year⁻¹ CCW). CCL was highly correlated to mean clutch size in both green (R²=0.51) and loggerhead turtles (R²=0.61) and maximal clutch size of green turtles (R²=0.58). Larger females did not lay a greater number of clutches or have a shorter remigration interval than smaller females of either species. On average, the size of green turtle clutches increased and that of loggerhead turtles decreased as the season progressed. Individual green turtles, however, produced more eggs per clutch through the season to a maximum in the third or fourth clutch. In loggerhead turtles, clutches 1-4 were very similar in size but the fifth clutch was 38% smaller than the first. No individuals of either species were recorded laying more than five clutches. Green turtles may not be able to achieve their maximum reproductive output with respect to clutch size throughout the season, whereas only loggerhead turtles laying five clutches (n=5) appear to become resource depleted. Green turtles nesting in years when large numbers of nests were recorded laid a greater number of clutches than females nesting in years with lower levels of nesting.     

Measuring temporal variation in reproductive output reveals optimal resource allocation to reproduction in the northern grass lizard, Takydromus septentrionalis

We measured the reproductive output of Takydromus septentrionalis collected over 5 years between 1997 and 2005 to test the hypothesis that reproductive females should allocate an optimal fraction of accessible resources in a particular clutch and to individual eggs. Females laid 1–7 clutches per breeding season, with large females producing more, as well as larger clutches, than did small females. Clutch size, clutch mass, annual fecundity, and annual reproductive output were all positively related to female size (snout–vent length). Females switched from producing more, but smaller eggs in the first clutch to fewer, but larger eggs in the subsequent clutches. The mass-specific clutch mass was greater in the first clutch than in the subsequent clutches, but it did not differ among the subsequent clutches. Post-oviposition body mass, clutch size, and egg size showed differing degrees of annual variation, but clutch mass of either the first or the second clutch remained unchanged across the sampling years. The regression line describing the size–number trade-off was higher in the subsequent clutch than in the first clutch, but neither the line for first clutch, nor the line for the second clutch varied among years. Reproduction retarded growth more markedly in small females than in large ones. Our data show that: (1) trade-offs between size and number of eggs and between reproduction and growth (and thus, future reproduction) are evident in T. septentrionalis ; (2) females allocate an optimal fraction of accessible resources in current reproduction and to individual eggs; and (3) seasonal shifts in reproductive output and egg size are determined ultimately by natural selection.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 315–324.     

First fossil gravid turtle provides insight into the evolution of reproductive traits in turtles

Here we report on the first discovery of shelled eggs inside the body cavity of a fossil turtle and on an isolated egg clutch, both referable to the Cretaceous turtle Adocus. These discoveries provide a unique opportunity to gain insight into the reproductive traits of an extinct turtle and to understand the evolution of such traits among living turtles. The gravid adult and egg clutch indicate that Adocus laid large clutches of rigid-shelled spherical eggs and established their nests near rivers, traits that are shared by its closest living relatives, the soft-shelled turtles. Adocus eggshell, however, was probably more rigid than that of living turtles, based on its great thickness and structure, features that may represent unique adaptations to intense predation or to arid nest environments. In light of the reproductive traits observed in Adocus, the distribution of reproductive traits among turtles reveals that large clutches of rigid-shelled eggs are primitive for hidden-necked turtles (cryptodirans) and that spherical eggs may have evolved independently within this group.     

Clutch size for Mediterranean loggerhead turtles (Caretta caretta)

We investigated the number of eggs laid and the total clutch volume for loggerhead turtles ( Caretta caretta L.) nesting on the Greek island of Cephalonia (38° 09' N, 20° 33' E) during 1990. Both the number of eggs laid and clutch volume were positively related to female body size, and the mean explained variation for these relationships (36·6% and 37·7%, respectively) were not significantly different. Clutch volume decreased as the season progressed because individuals laid successively smaller clutches. The inter-nesting interval (range 15–19 days) did not significantly influence the number of eggs laid or clutch volume. For individuals seen laying more than once, female size in combination with the number of a clutch in relation to all the clutches observed for that individual, together explained 65·5% of the variation in clutch volume.     

Can natural phenotypic variances be estimated reliably under homogeneous laboratory conditions?

The phenotypic variance is assumed to be greater in a more heterogeneous environment. The validity of this assumption is important for microevolutionists to extrapolate results from the laboratory to field environments. We subjected clutches of eggs from common snapping turtles (Chelydra serpentina) to a split-family design to evaluate the variability in incubation time and four size traits of neonates from eggs incubated in the laboratory and those left in situ. Mean size measurements were similar between the laboratory and the field, but incubation time was systematically longer in the field. We found no tendency among clutches for hatchlings resulting from eggs incubated in laboratory or field environments to demonstrate greater variability. Also contrary to expectation, clutches that experienced greater thermal variation in the field did not exhibit greater variation in phenotypic traits. Consequently, extrapolating results from the laboratory to the field may not always be problematic for microevolutionary analyses.     

Observation of reproductive cycle of female yellow-margined box turtle (Cuora flavomarginata) using radiography and ultrasonography

This study presents a combination of radiography and ultrasonography to observe the reproductive cycle of 24 captive female yellow-margined box turtles in Taiwan. Radiography was mainly used to monitor clutch size, whereas ultrasonography was applied to detect changes in the follicles throughout the year. The observation of the 24 female turtles was performed from April 2007 to June 2008. Their average carapace length was 16.62 ± 1.66 cm and their average body weight was 812 ± 164.98 g. The mean clutch size was three (87 eggs/29 clutches) and the reproductive frequency was 95.83% (23/24). Double clutches were detected in 79.2%, and 20.8% had single clutches. Ovulation occurred from March through August, and the average follicular diameter was 2.16 ± 0.18 cm. Follicles entered the latent period in October (at 1.54 ± 0.26 cm), and vitellogenesis of the next reproductive cycle began in November. Using radiography, the eggshell could be detected on the ninth day after ovulation. The average period of the single clutch group was 6.9 weeks (range 5.1-8.5 weeks). In the double clutch group, the average period of the first clutch was 5.5 weeks (range 4-7.8 weeks) and that of the second clutch was 5.2 weeks (range 4-7.8 weeks). This study has advanced the understanding of reproductive physiology of yellow-margined box turtle and established a valuable and practical model for comparative study of the reproductive physiology of other chelonians.     

Multiple paternity in egg clutches of hawksbill turtles (Eretmochelys imbricata)

We present the first data collected on the genetic mating system of the hawksbill turtle Eretmochelys imbricata, the only marine turtle not studied to date. We examined paternity within 12 egg clutches from ten female hawksbill turtles from Sabah Turtle Islands, Malaysia. A total of 375 hatchlings were analysed using five microsatellite markers. Results demonstrated that clutches from two out of ten females were sired by multiple males (maximum of two). Although at a low frequency, observation of multiple paternity indicates that hawksbill turtles exhibit the same genetic mating system (polyandry) as observed for other species of marine turtles. Consistent paternity across multiple clutches laid by individual females in one breeding season supports the hypothesis that sperm are stored from mating prior to nesting and are then used to fertilize all subsequent clutches of eggs that season.     

Observations on the female reproductive cycles of captive Asian yellow pond turtles (Mauremys mutica) with radiography and ultrasonography

The annual reproductive cycle of 27 female Mauremys mutica was observed by radiography and ultrasonography from April 2006 to August 2007. Radiography was used to monitor clutch size and ultrasonography was used to monitor changes in the ovarian follicles. The follicles started to enlarge in September and became preovulatory in January. The mean maximum follicle diameter of ovulation was 18.30±1.44 mm, and ovulation occurred from March through August. Eggs were laid between April and August. Turtles entered latent period in early August and the maximum follicular size was at a low of 13.22±2.36 mm in late September. The vitellogenesis of the next reproductive cycle began in October. The 24 adult females laid 56 clutches containing a total of 227 eggs. Average clutch size was 4.05 eggs (range 1–8) and there were 2.33 clutches (range 1–4) per female. Egg shell images were first observed on the sixth or seventh day after ovulation. The oviductal period averaged 6.9 weeks (range 2–16 weeks) on the first clutch, 3.4 weeks (range 2–8 weeks) on the second, and 2.75 weeks (range 2–6 weeks) for the third. Radiography and ultrasonography are non‐invasive and convenient methods to evaluate the reproductive cycle of female M. mutica. They should be applicable to other turtles and should greatly enhance knowledge of reproductive physiology. Zoo Biol 29:50–58, 2010. © 2009 Wiley‐Liss, Inc.     

The effect of extreme northerly climatic conditions on the life history of the minnow, Phoxinus phoxinus (L.)

Over its exceptionally wide geographical range the minnow displays a remarkable variability in its life history. In southern England many fish mature after one year and few fish survive to their third birthday. Very few fish spawned for more than one season but a 65-mm female is estimated to spawn up to 3172 eggs over the extended spawning season. In the River Utsjoki in Finnish Lapland maturity was strongly size-dependent and delayed until the fish reached 5, 6 or even 7 years of age, with a maximum age of 13 years at a length of only 75 mm. Unlike some other small-sized species in unproductive environments, individual females continued to spawn successive clutches of eggs though over a much shorter spawning season. The maximum estimated egg production was 824 for a 65-mm fish. Temperature had a strong direct or indirect effect on growth, with significantly lower growth increments in cold summers. At a second Arctic site in eastern Lapland growth rates were higher and maturity earlier, yet clutch size was greatly reduced with a seasonal fecundity estimate of only 314. There were only small differences in size of eggs or larvae between the populations. Evidence from other species indicates that most of the observed changes over the range of the minnow are phenotypic responses to the contrasting environments. However, the different strategies displayed at the two Arctic sites could represent the results of selection for differences in pre- and post-reproductive survival.     

Costs of large communal clutches for male and female Greater Rheas Rhea americana

The breeding system of the Greater Rhea Rhea americana is almost unique among birds as it combines harem polygyny and sequential polyandry, with communal egg-laying and uniparental male care. In this species, large communal clutches (more than 30 eggs) are rare and have a lower hatching success than smaller clutches. Here we analyse the proximate causes of hatching failures and the costs of large communal clutches (and therefore the costs of extensive polygyny) for males and females. We evaluated if length of the nesting period, egg viability, egg losses during incubation and male parental activity at the nest were affected by clutch size. We also evaluated if chicks hatched from large clutches have a lower survival during the first 2 months after hatching. Large clutches had longer nesting period and lower hatching success, mainly as a result of bacterial contamination of the eggs and increased hatching asynchrony. In addition, large clutches tended to lose more eggs as a result of accidental breakage or predation. Male activity at the nest and chick survival were not related to clutch size. Low hatching success, nest predation risk and energetic costs associated with large clutches penalize females that join large harems and males that accept additional eggs into the nest.     

The influence of clutch size on survival and reproductive potential of Hessian fly

The clutch size laid by Hessian flies (Mayetiola destructor Say) (Diptera: Cecidomyiidae) was manipulated over a range of 1 to 30 eggs on single wheat plants (Triticum aestivum, L.). Pupae developing from egg clutches were removed from plants, counted and reared through to adult eclosion. Wing lengths of adult males and females were recorded and used as an indicator of body size. Survival to pupal and adult stages, as well as mean wing length of resulting males and females, decreased as clutch size increased. Wing length of females from clutches showed a positive linear relationship with potential fecundity. The benefits of small clutches for a female Hessian fly's offspring are discussed in the context of the foraging behaviour of the ovipositing female. We predict that under high probabilities of survival and availability of host plants, females will lay smaller-sized clutches per plant. However when the probability of survival is low and host plants scare, the female will respond by laying larger-sized clutches.     

Parental quality and egg size affect chick survival in a precocial bird, the lapwing Vanellus vanellus

Effects of egg size and parental quality on lapwing Vanellus vanellus chick survival were studied in southwestern Sweden over 6 years. Chicks from large eggs were heavier at hatching and survived significantly better than those from small eggs. To control for the confounding effect of parental quality on egg size and chick survival, we performed a cross-fostering experiment during 2 years, exchanging clutches between nests with large and small eggs. In control clutches, chicks from large eggs survived better than those from small eggs, but we found no significant difference in chick survival between exchanged clutches. Thus, egg size did not affect chick survival independently of parental quality. Fledging success increased with parental age and/or experience, and with female body mass. Hence, both egg size and parental quality affect chick survival in the lapwing. Received: 22 February 1996 / Accepted: 30 September 1996     

Laying characteristics of one- and two-year old pheasants (Phasianus colchicus, L.)

The aim ofthe study was to assess laying traits, the weight of eggs and characters ofthe laying rhythm of pheasants in the first and second years of reproduction. Pheasants (10 cockerels and 50 hens) were kept in aviaries. Daily, individual control of laying was performed beginning with the day of the first laying and ending with the last egg. The following parameters were evaluated: age at first laying, length of the laying period, number of laid eggs and the average weight of the egg in the 8th week of laying. The laying rhythm was also assessed and comprised: the number of egg clutches, the number of eggs in a clutch, the number of eggs in the longest clutch, the number of intervals, the length of intervals and the longest interval between clutches. During the first period of reproduction, in comparison with the second, pheasants laid slightly more eggs of similar average weight. The first laying period was longer than the second and was characterised by a greater number of egg clutches and greater number of intervals between clutches. The greatest number of eggs was laid in 10-egg and longer clutches, although the l-egg clutches were the most numerous. A positive correlation was found between the number of eggs and the number of clutches, the greatest number of eggs in a clutch and the number of intervals between clutches. The similar values of the reproductive characters of one- and two-year old pheasants point to the possibility of longer utilization of these birds than only for one laying period. On the other hand, the considerable variability between the experimental hens with regard to the number and the length of egg clutches, as well as the intervals between them, indicate the possibility to carry out selection taking into account traits characterising the laying rhythm.     

Clutch size, development and wing morph differentiation of Melittobia digitata

Melittobia digitata Dahms (Hymenoptera, Eulophidae) is a wing polymorphic, gregarious ectoparasitoid of bees and wasps. In nature, females of this wasp start to produce their progeny after feeding on the host. The first adults to develop will emerge as short wing morphs (SWM). Mother and daughters will lay eggs in the same hosts, and the following females to develop will emerge as long wing morphs (LWM). We evaluated the effects of the clutch size on the development, egg load, and wing morph differentiation of M. digitata. Developmental time was shorter when insects developed in small clutches, and immature survivorship was reduced in the largest clutch (400 eggs/host). Morph differentiation was also affected by the clutch size. SWMs developed in small clutches (5 and 25 eggs/host) while LWMs in large clutches (200 and 400 eggs/host). However, both morphs developed in intermediate clutches (50 and 100 eggs/clutch), with a decreasing number of SWMs developing with the increase in the clutch. The size and egg load of each morph was affected with the increase in the clutch size, although the forewing length/hind-tibia length ratio was kept constant for each morph developing from different clutch sizes. Egg load of LWMs was also reduced when compared to the SWMs that developed from the same clutch, although LWMs females were larger (longer tibia length). We discuss the possible mechanisms inducing the morph differentiation in M. digitata, as well as the physiological, behavioral, and ecological changes facing each morph.     

Antigua revisited: the impact of climate change on sand and nest temperatures at a hawksbill turtle (Eretmochelys imbricata) nesting beach

Whether a turtle embryo develops into a male or a female depends, as with many other reptiles, on the temperature during incubation of the eggs. With sea turtles, warm temperatures produce 100% females. Therefore, global warming has the potential to drastically alter their sex ratios. Air temperatures on Antigua have increased by 0.7°C over the last 35 years. Measurements in both the sand and the clutches laid by hawksbill turtles (Eretmochelys imbricata) at Pasture Bay, Antigua, show that for important parts of the nesting season temperatures are already above the level producing 50% of each sex (pivotal level). Comparisons are made to sand temperature measurements taken on this beach in 1989 and 1990. It is estimated that fewer males were produced in 2003 than in the previous years. Recommendations are made for close monitoring of the fertility of eggs and for research on any turtles nesting at cooler times of year.     

Analysis of the laying rhythm and reproductive traits of geese

The aim of the performed investigations was to analyse the laying rhythm and reproductive traits of Ko?uda white geese from the W11 reproduction strain and to determine the heritability of these traits as well as correlations between the laying rhythm traits and reproductive traits. The total number of geese participating in the experiment included 383 one-year old layers from the control flock (the first year of reproductive utilisation). The following traits characterizing the laying rhythm were assessed individually for each layer: the number of 2 and 3-egg clutches or more, length (in days) of 2- or more egg clutches as well as the length of intervals between the laid eggs during the entire laying period. The following reproductive traits were also assessed individually for each bird: age at sexual maturity, initial number of eggs (eggs laid during the period from January, 1st to April, 30th), number of eggs during the whole laying period, laying intensity (the total number of eggs x 100/length of the laying period in days) as well as the length of the reproductive period. It was found that Ko?uda white geese laid most of their eggs (on average 70.2%) singly and not in clutches. With regard to egg clutches, it was found that 2-egg clutches constituted 85.3% of eggs laid in clutches. Moderate or high variability of traits associated with the laying rhythm and reproduction were demonstrated. The observed moderate heritability of the laying rhythm traits indicate that they may be utilised in the selection programs for geese. On the other hand, the reported high, positive genetic correlation coefficients between the number of egg clutches and the initial and total egg number as well as laying intensity confirm the existence of interactions between these traits. This fact may be helpful in breeding programs for determining the optimal selection systems for geese.     

Allocation of offspring size and sex by female black ratsnakes

How females allocate resources to each offspring and how they allocate the sex of their offspring are two powerful potential avenues by which mothers can affect offspring fitness. Previous research has focussed extensively on mean offspring size, with much less attention given to variance in offspring size. Here we focussed on variation in offspring size in black ratsnakes, Elaphe obsoleta . We collected and hatched 105 clutches (1283 eggs) over 9 years. We predicted that females should lay larger eggs, or more variable eggs, when the environment is less predictable. We also predicted that females laying early or laying larger eggs should produce mostly sons because adult males are larger than adult female ratsnakes. The largest hatchling was more than twice the length and almost four times the mass of the smallest hatchling. Variation in offspring size was itself highly variable, with CVs in offspring mass among clutches ranging from 1% to 25%. With one exception, the variables we expected should influence variation in offspring size had little effect. We found that clutch size increased with maternal size and that egg size decreased with clutch size, but we found no evidence that variance in egg size among clutches increased as the season progressed or that females increased the mean size of their offspring the later in the season they laid their eggs. Females in better condition after they finish laying their eggs did produce larger eggs. There was no relationship between within-clutch variation in egg size and laying date or mean egg size. Finally, sex ratio did not vary with mean egg size or hatching date. Given evidence that offspring size in snakes affects survival, selection should reduce variation in offspring size unless that variance enhances maternal fitness and yet we found little support for hypothesized advantages of varying offspring size.     

Effect of maternal foraging habitat on offspring quality in the loggerhead sea turtle (Caretta caretta)

Exploring a trade‐off between quantity and quality of offspring allows differences in the fitness between alternative life histories to be accurately evaluated. We addressed the mechanism that maintains alternative life histories (small oceanic planktivores vs. large neritic benthivores) observed in a loggerhead sea turtle (Caretta caretta) population, which has been suggested to be environmental, based on the lack of genetic structure and a large difference in reproductive output. We examined whether maternal foraging habitat affects offspring quality, by measuring the morphology, emergence success, and righting response of hatchlings following incubation in a common open sand area over the whole nesting season at Yakushima Island, Japan, and by recording early growth and survival of offspring that were reared in a common environment at a Japanese aquarium. Furthermore, we tested whether sea turtles adjust egg size in response to temporal shifts of the incubation environment. There were no significant differences in any hatchling traits between oceanic and neritic foragers (which were classified by stable isotope ratios), except for clutches laid during the warmest period of the nesting season. There were also no significant differences in the growth and survival of offspring originating from the two foragers. The size of eggs from both foragers significantly increased as the season progressed, even though the rookery had heavy rainfall, negating the need to counteract heat‐related reduction in hatchling morphology. In comparison, the sizes of adult body and clutches from both foragers did not vary significantly. The results further support our previous suggestions that the size‐related foraging dichotomy exhibited by adult sea turtles does not have a genetic basis, but derives from phenotypic plasticity. Adjustment in reproductive investment may be associated with: (1) predation avoidance, (2) founder effect, and/or (3) annual variation in egg size.     

Reproduction of the Australian freshwater turtle Emydura krefftii (Chelonia: Chelidae)

A study of the reproduction of Krefft's river tortoise, Emydura krefftii , was conducted in the perched dune lakes of Fraser Island, Queensland. Mature male specimens exhibit a postnuptial pattern of spermatogenesis typical of temperate-zone turtles elsewhere, with a peak in spermatogenic activity in autumn and a cessation of activity during the breeding season in spring and early summer. The spermatogenic cycle is paralleled by seasonal variation in testicular weight (standardized for body size) and in the diameter of the seminiferous tubules. Sperm are abundant in the epididymal canals throughout the year. Mating was observed in autumn, late winter and spring.
Females have a cyclic reproductive pattern, with distinct phases of follicular enlargement, ovulation and oviducal period, and quiescence. Yolk begins to accumulate in the ovaries in late summer, and the accumulation continues unabated through the winter, presumably by the transfer of material from fat stores to the ovaries. Ovulations occur from late winter to mid-summer. Atresia of follicles that fail to ovulate was demonstrated histologically.
Emydura krefftii lay up to three clutches of hard-shelled ellipsoid eggs per season. Each clutch contains between four and 10 eggs; the number is strongly correlated with maternal body size. Reproductive potential ranges from 12 eggs per annum for a female that has recently matured (carapace length c. 150 mm), to 30 eggs per annum for a full-sized female (length c. 250 mm). Selected life-history traits of Emydura krefftii are discussed in the context of findings for other populations of the species and for other species of freshwater turtle.     

Pre-laying nutrition mediates maternal effects on offspring immune capacity and growth in the pied flycatcher

We have aimed at detecting prelaying maternal effects on nestling antibody defences and growth through experimental food supplementation of female pied flycatchers Ficedula hypoleuca and subsequent exchange of whole clutches with control nests. The levels of immunoglobulins and the mass and size of chicks at 12 days of age were ascertained. This is the first study controlling for maternal incubation effects by exchanging eggs rather than nestlings. Our prediction is that the females' availability of pre-laying nutritional resources affects offspring immune capacity and growth through maternal effects in the eggs when conditions during incubation and rearing are controlled for. Nestling immunoglobulin Y (IgY) levels and tarsus length were indeed positively associated with maternal food supplementation at laying. The only rearing environmental effect detected was that of mite infestation which affected both IgY levels and growth of nestlings. Nestlings that recruited to the population in the subsequent 2 years had higher IgY levels than those that did not. Maternal adaptations for allocating resources to eggs play an important role in moulding offspring phenotypes and may affect their survival prospects.