Individual Variation in Trophic Egg Production: Evidence for Maternal Manipulation in Response to Resource and Competition Levels

Females of the subsocial shield bug Parastrachia japonensis (Heteroptera: Parastrachiidae) incorporate trophic eggs (nutritive eggs) into their egg mass. Considerable variation occurs among females in trophic egg number and the proportion of an egg mass that is composed of trophic eggs. Because trophic eggs are essential to the development and survival of young, this variation could significantly impact female fitness. We tested the hypothesis that trophic egg abundance is induced by maternal phenotype (weight, body size) and resource exposure. We predicted that resource limitations would cause females to produce fewer fertile eggs and more trophic eggs and that larger and heavier females would produce more of each egg type. Females ovipositing early in the season are exposed to different resource conditions than those that oviposit late. Thus, we compared egg production patterns between these two groups and several other factors related to nesting. No correlation was seen between body size and trophic egg abundance, or, indeed, egg production, overall; however, heavier females produced heavier egg masses. Counter to our prediction, late females, which had greater access to food, produced significantly more total eggs, fewer fertile eggs, and more trophic eggs than early females. A binomial generalized linear model analysis indicated that the factors most correlated with the percentage of an egg mass destined to become trophic eggs were resource abundance, resulting from early or late oviposition, and distance of the nest from the host tree, with closer females producing more trophic eggs. The findings support our hypothesis that resource availability and, to a lesser extent, maternal phenotype affect trophic egg abundance.     

Effects of temperature and season on egg size, hatchling size and adult size in Notiophilus biguttatus

1. Temperature-induced egg size variation and its effects on successive life stages in the carabid beetle Notiophilus biguttatus were examined.
2. In the laboratory, across temperature regimes, egg size and number were inversely related; number of eggs and total egg mass were higher, but egg size was smaller at high temperatures.
3. Food intake rate was shown not to be involved in the temperature effect on egg size.
4. Within the higher temperature regimes, among females, egg size was negatively correlated with number of eggs and with total egg mass.
5. Data on egg mortality and egg development time did not explain why at low temperature eggs were larger than at high temperature.
6. Larvae hatching from eggs produced at a low temperature were heavier than larvae from eggs produced at a high temperature, irrespective of temperature during development.
7. In a prolonged outdoor experiment (January – July), encompassing the main breeding period of N. biguttatus , egg size decreased and both egg production rate and total egg mass increased in the course of the experiment.
8. In the field, an effect of seasonal change in temperature on adult body size was found; teneral beetles that had their juvenile period early in the season were larger than those that had their juvenile period later in the season.
9. The results of the study suggest a mechanistic explanation in which the egg size response to temperature follows from a difference in temperature sensitivity between two processes in oogenesis; adaptiveness of the temperature response was not clarified.     

Susceptibility of Nezara viridula (L.) (Hemiptera: Pentatomidae) Egg Masses of Different Sizes to Parasitism by Trissolcus basalis (Woll.) (Hymenoptera: Platygastridae) in the Field

Egg masses of Nezara viridula (L.) are commonly parasitized by Trissolcus basalis (Woll.), and we investigated the role of size of egg masses on parasitization by T. basalis. Sentinel egg masses were exposed to parasitism in the field for 6–7 days, when they were collected for evaluation of parasitoid emergence. We recorded the number of eggs per egg mass, the number of emerged hosts, and the number of empty and parasitized eggs. We calculated the proportion of attacked host egg masses (DE), the proportion of parasitized eggs per attacked egg mass (PE), and total parasitism (PI). The total number of egg masses exposed to parasitism was 330. The minimum, mean, and maximum egg mass sizes were 25, 75.2, and 111, respectively. DE and PE varied widely between different fields, and they were independent of egg mass size. In 14.2% of all parasitized egg masses, we found simultaneous emergence of T. basalis and N. viridula independently of host egg mass size. PE exhibited low variability compared with PI and DE, which were linearly related. PI and DE values from other field studies are consistent with the linear relationship, suggesting that PI is mostly related to the proportion of the DE. This also suggests that total parasitism is independent of egg mass size, of possible differences in plant species, and T. basalis density and strains.     

Factors affecting variation in the reproductive investment of female treefrogs,Hyla intermedia

In anurans, fecundity (clutch size) is the most important determinant of female reproductive success. We investigated three possible causes responsible for fecundity variation in female Italian treefrogs, Hyla intermedia, during four breeding seasons: (i) variation in morphological (body size and condition) and life-history (age) traits; (ii) variation in the tradeoff between the number and the size of eggs; (iii) seasonal effects and within-season differences in the timing of deposition. At the population level, we found no evidence for a tradeoff between the number and the size of eggs, because they both correlated positively with females’ body size. Conversely, neither age nor post-spawning body condition showed any effect on female reproductive investment. Independent of body size, we found no evidence for variation in reproductive effort among different breeding seasons, but strong evidence for a decrease of clutch size and an increase of egg size with the advancing of a breeding season. To test for the functional significance of the observed temporal variation in allocation strategy, we carried out a rearing experiment in semi-natural conditions on a random sample of ten clutches. The experiment showed a negative effect of clutch size and a positive effect of egg size on both tadpole growth and developmental rates, suggesting that reproductive investment, although constrained by body size, can be adjusted by females to the time of deposition to increase the chances of offspring survival.     

The paradox between the long-term decrease of egg mass size of the calanoid copepod Eurytemora affinis and its long-term constant abundance in a highly turbid estuary (Gironde estuary, France)

Eurytemora affinis egg mass size—a commonly used demographicparameter—was surveyed in the Gironde estuary. Its decreasebetween 1978 and 2003 contrasted with the stability of populationdensity during this long-term period. Different hypotheses weretested to explain this paradox. (i) Upstream shift of the population:Even though the population of E. affinis shifted upstream dueto a greater penetration of marine water, no relationship betweenthe population shift and demographic parameters was observed:the egg mass size exhibited the same evolution upstream. (ii)Water warming: No early egg production and no change of femalesize that could metabolically limit the egg mass size was observed.(iii) Food limitation: The change in food quality observed didnot result in any change in total copepod abundance. (iv) Fasterrenewal of egg masses: The paradox cannot be explained by thisfactor and the number of adults observed nowadays is higherthan the number of eggs produced by females, whereas fecundityrates strongly increased. The paradox is probably explainedby the expulsion of viable subitaneous eggs. This may representa recent behaviour adaptation of the copepod to environmentalchanges.     

Respiration of Aquatic and Terrestrial Amphibian Embryos

Respiratory constraints on the structure of single eggs andegg masses have affected the mode of amphibian reproductionin water and in air. Aquatic eggs generally require less oxygen,develop faster, and hatch earlier, but these characteristicsare related to small ovum size. A comparison of two speciesof aquatic and terrestrial breeding frogs with similarly sizedova shows no differences in hatching stage, maximum rate ofoxygen uptake, oxygen conductance of the egg capsule, or Po₂difference across the capsule. However, the aquatic speciesdevelops about 2.4 times faster and tolerates lower environmentalPo₂, suggesting adaptation for development in ephemeral water.Modelling of diffusive oxygen transport into a single aquaticegg shows that a large amount of jelly (or a boundary layer)around the capsule may not greatly restrict gas exchange, ifthe inner radius of the capsule is large. However, gelatinousegg masses that contain other embryos that compete for oxygenare therefore limited in size, unless the eggs are ventilatedby convection of water among them. Aquatic egg are often suspendedin masses above the substrate, promoting oxygen movement intothe mass from all directions. Terrestrial egg masses are morediffusion limited, because gravity and surface tension collapsethem, preventing convection between the eggs, and restrictingthe source for oxygen diffusion. Terrestrial embryos are oftenlarger than their aquatic counterparts and have higher demandsfor oxygen. Terrestrial conditions have selected for adaptationsthat reduce respiratory competition between embryos, for example,separating of embryos by large volumes of jelly or reducingthe number of eggs in a clutch. The size of foam nests is unlimited,because oxygen for each embryo is supplied directly from thefoam.     

Maternal investment in reproduction and its consequences in leatherback turtles

Maternal investment in reproduction by oviparous non-avian reptiles is usually limited to pre-ovipositional allocations to the number and size of eggs and clutches, thus making these species good subjects for testing hypotheses of reproductive optimality models. Because leatherback turtles (Dermochelys coriacea) stand out among oviparous amniotes by having the highest clutch frequency and producing the largest mass of eggs per reproductive season, we quantified maternal investment of 146 female leatherbacks over four nesting seasons (2001–2004) and found high inter- and intra-female variation in several reproductive characteristics. Estimated clutch frequency [coefficient of variation (CV) = 31%] and clutch size (CV = 26%) varied more among females than did egg mass (CV = 9%) and hatchling mass (CV = 7%). Moreover, clutch size had an approximately threefold higher effect on clutch mass than did egg mass. These results generally support predictions of reproductive optimality models in which species that lay several, large clutches per reproductive season should exhibit low variation in egg size and instead maximize egg number (clutch frequency and/or size). The number of hatchlings emerging per nest was positively correlated with clutch size, but fraction of eggs in a clutch yielding hatchlings (emergence success) was not correlated with clutch size and varied highly among females. In addition, seasonal fecundity and seasonal hatchling production increased with the frequency and the size of clutches (in order of effect size). Our results demonstrate that female leatherbacks exhibit high phenotypic variation in reproductive traits, possibly in response to environmental variability and/or resulting from genotypic variability within the population. Furthermore, high seasonal and lifetime fecundity of leatherbacks probably reflect compensation for high and unpredictable mortality during early life history stages in this species.     

Life-history variation within a three-spined stickleback population in the Camargue

Among individuals of female three-spined sticklebacks Gasterosteus aculeatus from a population in the Camargue, southern France, studied in 12 successive years, adult L _T ranged from 31–64 mm, clutch size ranged from 33–660 eggs, and mean egg diameter per clutch ranged from 1.15–1.67 mm. Because the population was strictly annual, inter-annual variation corresponded to variation among generations having experienced different environmental conditions. Body mass varied significantly among years, suggesting an effect of varying environmental conditions. Gonad mass and clutch size increased with body mass, but mean egg diameter was not correlated to body mass. Body mass-adjusted gonad mass, interpreted as reproductive effort per clutch, did not vary significantly among years, suggesting that this trait was not influenced by environmental conditions. Body mass-adjusted clutch size and egg size varied significantly among years. Inter-annual variation in body length at breeding, clutch size and egg size was of the same order of magnitude as inter-population variation reported by other authors for this species. During the breeding season, reproductive effort and clutch size tended to increase. Egg size tended to decrease during the breeding season but this seasonal pattern varied among years. Observed life-history variation is discussed both in terms of its evolutionary significance and methodological implications in the study of life-history variation among populations.     

Egg performance on an egg-carrying bug. Experiments in the field

Selection of oviposition sites has direct influence on female fitness. Differences in offspring survival among sites should favour females to select oviposition sites with the highest survival. Golden egg bug females ( Phyllomorpha laciniata; Coreidae, Heteroptera) use conspecifics as oviposition substrates. Most eggs are laid on the back of the bug but they can be found on all body parts. Females never carry their own eggs, and males commonly carry eggs received without copulation with the donor. We examined differences in egg survival relative to paternity to the egg, host sex and body size and attachment of an egg on a host's body in the field. We also studied which bugs received eggs. Egg loss was surprisingly common: 30–80% of recaptured individuals lost eggs during a six-day period. Unexpectedly, host's paternity to the eggs did not affect egg survival. Also, egg loss did not differ among hosts in respect to other parameters studied. Males received more eggs than females, but survival of the eggs was not better on a male's back than on a female's back. Since egg loss is common in the golden egg bug, we suggest that female oviposition strategy to lay eggs on conspecifics is not perfect. This is due to active behaviour of potential hosts (for example, rejected oviposition attempts) or lack of suitable oviposition substrates (conspecifics) in the field. Since eggs do not survive unless carried, females may be acting opportunistically, doing the best job possible by laying eggs on available conspecifics.     

The combined effect of isolation and Fasciola hepatica infection on the life history traits of Fossaria cubensis.

Life history traits of Fossaria cubensis were compared between isolated and paired snails after infection with three miracidia of Fasciola hepatica. Four experimental groups were tested: isolated-unexposed, paired-unexposed, isolated-infected, and paired-infected. A repeated-measures ANOVA showed statistically significant interactions among isolation, infection, and age effects for shell size, number of egg masses per snail, number of eggs per snail, and number of viable eggs per snail. Isolated-unexposed snails exhibited the higher values of these variables and those of survival and finite and intrinsic rates of natural increase. Infection stimulated shell growth during the prepatent period, but differences were present only in paired snails since isolation causes a similar effect. Reproduction, in terms of the number of egg masses per snail and the number of eggs per mass per snail, decreases in the presence of parasitic infection, whereas isolation stimulates it. These effects were observed from early stages of infection.     

Factors influencing offspring traits in the oviparous multi-clutched lizard,<Emphasis Type="Italic">Calotes versicolor</Emphasis> (Agamidae)

The determinants of offspring size and number in the tropical oviparous multi-clutched lizard,Calotes versicolor, were examined using both univariate and multivariate (path) analyses. InC. versicolor maternal snout-vent length (SVL) and body condition influence clutch mass and clutch size but have no significant influence on offspring size. The positive effect of maternal SVL and body condition on offspring number is counterbalanced by a negative effect of breeding time on egg mass. In fact, breeding time directly influences the offspring body mass and condition through variation in the egg mass. There is a trade-off between offspring mass and condition with offspring number, and breeding time influences both. Offspring hatched from the eggs of early (May–June) or mid (July–August) breeding periods invariably show lower mass and condition than those hatched from the eggs of late breeding season (September–October). Yet, there is no variation in offspring SVL among early, mid and late clutches. Thus, inC. versicolor offspring SVL is optimized while body mass and condition are not optimized.     

Seasonal variation in reproductive measures of tropical Roseate Terns Sterna dougallih previously undescribed breeding patterns in a seabird

Seasonal variation in egg-laying, egg size, hatching success, hatchling mass, fledging success and chick growth of Roseate Terms Sterna dougallii breeding on Aride Island (Seychelles), Indian Ocean, were studied in 1997 and 1998. I investigated to what extent two patterns, common in a range of species, were followed by tropical Roseate Terns: (a) seasonal decrease in clutch size, egg size and breeding success and (b) an increase in breeding success with increasing egg weight. In 1997 (a poor year), the earliest nesting birds laid significantly smaller eggs, and chicks were lighter at hatching than those of peak nesting birds. The mean clutch size, of 1.04 eggs, showed no seasonal variation and no 'b'-eggs hatched. In 1998 (a good year) the earliest nesting birds laid eggs of similar size and their chicks were of similar weight to those of peak nesting birds. Mean clutch size, of 1.25 eggs, increased significantly through the season and about 60% of the 'b'-eggs hatched. In 1997, hatching success was 57% whereas in 1998 it was 80%. In both years, breeding success declined significantly through the season. The fact that the earliest breeding birds laid smaller eggs in a poor year and smaller clutches in a good year is in marked contrast to a range of other species, and to temperate-nesting Roseate Terns. Egg volume explained about half of the variance in hatchling mass in both years, but only 15% of the variation in linear growth rate. Hatching date was the only variable with a significant effect on fledging success. Roseate Terns on Aride seemed to sacrifice egg size and clutch size for earliness of laying. Presumably it is a strategy of older birds to lay as early as possible and may be regarded as a response of tropical Roseate Terns to breeding under relatively poor, and seasonally declining, food conditions.     

Two eggs,two different constraints: a potential explanation for the puzzling intraclutch egg size dimorphism in Eudyptes penguins

Phenotypic plasticity and phenotypic stability are major components of the adaptive evolution of organisms to environmental variation. The invariant two-egg clutch size of Eudyptes penguins has recently been proposed to be a unique example of a maladaptive phenotypic stability, while their egg mass is a plastic trait. We tested whether this phenotypic plasticity during reproduction might result from constraints imposed by migration (migratory carry-over effect) and breeding (due to the depletion of female body reserves). For the first time, we examined whether these constraints differ between eggs within clutches and between egg components (yolk and albumen). The interval between colony return and clutch initiation positively influenced the yolk mass, the albumen mass, and the subsequent total egg mass of first-laid eggs. This time interval had only a slight negative influence on the yolk mass of second-laid eggs and no influence on their albumen and subsequent total masses. For both eggs, female body mass at laying positively influenced albumen and total egg masses. Female investment into the entire clutch was not related to the time in the colony before laying but increased with female body mass. These novel results suggest that the unique intraclutch egg size dimorphism exhibited in Eudyptes penguins, with first-laid eggs being consistently smaller than second-laid eggs, might be due to a combination of constraints: a migratory carry-over effect on the first-laid egg and a body reserve depletion effect on the second-laid egg. Both these constraints might explain why the timing of reproduction, especially egg formation, is narrow in migratory capital breeders.     

Experimental evidence for physical cues involved in oviposition site selection of lotic hydrobiosid caddis flies

Cues involved in determining the distribution of invertebrate propagules within a stream landscape contribute greatly to our knowledge of the supply and arrangement of new recruits and thus an improved understanding of factors that might ultimately affect population parameters. Previous observations indicated that both current velocity and rock size were important determinants of the egg mass distribution of certain hydrobiosid caddis flies that lay their eggs in single masses beneath emergent rocks. These observations were tested experimentally in a temperate, upland Australian stream. Manipulations of current speed confirmed that females of Ulmerochorema sp. and the Taschorema complex deposited more eggs on rocks in elevated current speeds (>0.40 ms(-1)) whereas Apsilochorema sp. deposited more eggs on rocks in slow currents (<0.30 ms(-1)). This latter result did not coincide with previous observational data. The anomaly between observational and experimental data, however, was reconciled by the outcome of a further experiment that tested the influence of the emergent or 'landing pad' size of rocks as the abundance of Apsilochorema egg masses increased with landing pad size independent of the prevailing flow conditions. Landing pad size did not influence the abundance of egg masses of Taschorema or Ulmerochorema. Patterns of female visits to rocks indicated that taxa might distinguish between favoured egg-laying sites prior to landing on rocks. Large aggregations of adult male and female Ulmerochorema collected from rocks favoured for oviposition provide indirect evidence for mating induced swarming behaviour associated with oviposition site selection. This study provides a framework for more sophisticated questions relating to the influence of oviposition site selection on structuring populations of lotic macroinvertebrates.     

Age‐related changes in the development of oocytes and testicular follicles after emergence in Stavsolus japonicus (Plecoptera)

Abstract Female stoneflies oviposit several times during the adult stage of their life cycle. The number of eggs within the deposited egg masses decreases at successive ovipositions. To clarify the reason for this decrease and to determine the conditions of testicular follicles, the patterns of development of oocytes and testicular follicles on different days after emergence are investigated in the systellognathan species Stavsolus japonicus (Okamoto) (Perlodidae). The size of the mature oocytes in the ovariole peaks a few weeks after emergence but decreases to the lowest level by 35 days after emergence. Several maturing oocytes can be observed in the ovarioles of individuals a few weeks after emergence but only one mature oocyte is observed at 35 days after emergence. The decreased number of eggs laid per mass by older individuals may therefore be due to the lower maturation of all the ovarioles.     

Ectotherms, Temperature, and Trade-offs: Size and Number of Eggs in a Carabid Beetle

We studied the allocation of total egg mass to size and number in the carabid beetle Notiophilus biguttatus F. at several temperature and day length regimes. Eggs increase in number and decrease in size with increasing (constant) temperature. Day length interacts with temperature: at short day the effect of temperature on size and number of eggs is weaker than at long day. In diurnally fluctuating temperature regimes, egg size is affected disproportionately by the high temperature period. All treatments, however, are similar in affecting number and size of eggs in an opposite direction. Consequently, egg size is explained to a high degree by egg production rate. The relationship between size and number of eggs among treatments is furthermore characterized by a decrease in egg size with an increase in total egg mass production. Within treatments, rate of egg production and egg size are negatively correlated among females in the low-temperature groups but not in the high-temperature groups; the correlations among females are also characterized by a decrease in egg size, with an increase in total egg mass production. Hence, possible trade-offs between size and number of eggs are masked by phenotypic variation in reproductive effort. The observations enable us to propose a simple conceptual model that explains the within-treatment correlation by the same causal factor as the negative relationship among treatment means.     

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.     

The influence of temperature and spatial distribution on the susceptibility of southern leopard frog eggs to disease

Since host defenses to infectious disease are often costly, one would expect hosts to use their defenses only when the threat of infection is high. Southern leopard frogs (Rana sphenocephala) at Ellenton Bay in South Carolina (USA) have an extended breeding season and their eggs are exposed to a wide range of temperatures depending on the time of year when they are laid. Adults aggregate their egg masses in cold temperatures, but separate them in warm temperatures. The spatial aggregation of egg masses may insulate eggs from cold temperatures, but may also affect the transmission of pathogens between the eggs. I examined the effects of temperature, pathogens, and spatial distribution on the survival of R. sphenocephala in the egg stage. Field observations found that temperature had little effect on the number of infected eggs within egg masses, but that egg masses in colder water were more likely to be aggregated together. In a controlled laboratory experiment, the presence of aquatic oomycetes led to higher mortality in cold temperatures than they did at warmer temperatures. Infectious disease may be a selective force that favors R. sphenocephala adults that aggregate their offspring when the threat of disease is high. Host aggregation can reduce the risk of infection when pathogens have a slow generation time that hinders them from responding to an abundance of hosts.     

Population quality,dispersal and numerical change in the gypsy moth,Lymantria dispar (L.)

Summary First instars from small and large gypsy moth eggs differ significantly in their head capsule width, weight, hatching time and the length of thoracic setae. Pupal weight and the developmental period of immature stages of the gypsy moth originating from small or large eggs do not differ significantly. The mean number of eggs per mass produced by females originating from small eggs is greater than that of females from large eggs although not statistically significant. Highly significant differences in mean egg size of egg masses of each type of female were also observed. The relationship between egg size and dispersal strategies are discussed.Paper No. 2229 Massachusetts Agricultural Experiment Station. University of Massachusetts at Amherst. This research supported (in part) from Experiment Station Project No. 355     

Influence of Diaphania hyalinata (L.) (Lepidoptera: Crambidae) egg density on the parasitization capacity of Trichogramma exiguum Pinto & Platner and Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae)

The effects of the egg density of Diaphania hyalinata (L.) on several biological parameters of Trichogramma exiguum Pinto & Platner and T. pretiosum Riley were investigated. For that, 24h-old egg masses were isolated in glass tubes (15 replicates; 1 egg mass = 1 replicate), and offered to parasitization by a newly-emerged female of T. pretiosum or T. exiguum 24h at the proportion of one female to 5, 10, 15, 20, 25, 30, 35 and 40 eggs of D. hyalinata. The following parameters were evaluated: number of parasitized eggs, number of individuals per egg, viability and sex ratio. Trichogramma exiguum parasitized more eggs than T. pretiosum when more than 25 eggs were available per female. The percentage of emergence was satisfactory to T. pretiosum in densities up to 15 eggs/female and up to 20 eggs/female for T. exiguum. The number of individuals per egg was not statistically different in both species except in the density of 25 eggs/female. It can be concluded that T. exiguum performed better than T. pretiosum at larger clutch sizes, as T. exiguum parasitization capacity increased as a result of the size of the host clutch size.