The ecology of lizard reproductive output

Aim We provide a new quantitative analysis of lizard reproductive ecology. Comparative studies of lizard reproduction to date have usually considered life‐history components separately. Instead, we examine the rate of production (productivity hereafter) calculated as the total mass of offspring produced in a year. We test whether productivity is influenced by proxies of adult mortality rates such as insularity and fossorial habits, by measures of temperature such as environmental and body temperatures, mode of reproduction and activity times, and by environmental productivity and diet. We further examine whether low productivity is linked to high extinction risk. Location World‐wide. Methods We assembled a database containing 551 lizard species, their phylogenetic relationships and multiple life history and ecological variables from the literature. We use phylogenetically informed statistical models to estimate the factors related to lizard productivity. Results Some, but not all, predictions of metabolic and life‐history theories are supported. When analysed separately, clutch size, relative clutch mass and brood frequency are poorly correlated with body mass, but their product – productivity – is well correlated with mass. The allometry of productivity scales similarly to metabolic rate, suggesting that a constant fraction of assimilated energy is allocated to production irrespective of body size. Island species were less productive than continental species. Mass‐specific productivity was positively correlated with environmental temperature, but not with body temperature. Viviparous lizards were less productive than egg‐laying species. Diet and primary productivity were not associated with productivity in any model. Other effects, including lower productivity of fossorial, nocturnal and active foraging species were confounded with phylogeny. Productivity was not lower in species at risk of extinction. Main conclusions Our analyses show the value of focusing on the rate of annual biomass production (productivity), and generally supported associations between productivity and environmental temperature, factors that affect mortality and the number of broods a lizard can produce in a year, but not with measures of body temperature, environmental productivity or diet.     

Offspring growth, survival and reproductive success in the bank vole: a litter size manipulation experiment

To estimate the optimality of brood size, it is essential to study the effects of brood size manipulation on offspring survival and reproductive success. Moreover, testing the generality of the hypothesis of reproductive costs requires experimental data from a diversity of organisms. Here I present data on the growth, survival and reproductive success of bank vole Clethrionomys glareolus individuals from manipulated litters. Furthermore, the survival of mothers whose litter size was manipulated was studied. At weaning, the mean weight of pups from enlarged litters was lower and from reduced litters higher compared to control litters. After winter, at the start of the breeding season, individuals from enlarged litters, especially males, were still lighter than individuals from the other two treatments. Litter enlargements did not increase the number of reproducing female offspring per mother, nor did the litter sizes of female offspring differ between treatments. There were no differences between treatments in winter survival of offspring after weaning, but among female offspring, weaning weight explained the survival probabilities over winter. A higher weight of females at winter determined the probability of starting to reproduce in spring. The survival of mothers did not seem to be influenced by litter manipulation performed the previous year. According to the results, mothers nursing enlarged or reduced litters do not gain any fitness benefits in terms of number of offspring surviving to breeding. The results are consistent with the majority of experiments conducted in birds, which have found costs of enlarged brood appearing as offspring trade-offs rather than parent trade-offs. Received: 14 December 1997 / Accepted: 1 March 1998     

On net reproductive rate and the timing of reproductive output

Abstract: Understanding the relationship between life-history patterns and population growth is central to demographic studies. Here we derive a new method for calculating the timing of reproductive output, from which the generation time and its variance can also be calculated. The method is based on the explicit computation of the net reproductive rate (R0) using a new graphical approach. Using nodding thistle, desert tortoise, creeping aven, and cat's ear as examples, we show how R0 and the timing of reproduction is calculated and interpreted, even in cases with complex life cycles. We show that the explicit R0 formula allows us to explore the effect of all reproductive pathways in the life cycle, something that cannot be done with traditional analysis of the population growth rate (lambda). Additionally, we compare a recently published method for determining population persistence conditions with the condition R0 > 1 and show how the latter is simpler and more easily interpreted biologically. Using our calculation of the timing of reproductive output, we illustrate how this demographic measure can be used to understand the effects of life-history traits on population growth and control.     

Offspring size at weaning affects survival to recruitment and reproductive performance of primiparous gray seals

Offspring size affects survival and subsequent reproduction in many organisms. However, studies of offspring size in large mammals are often limited to effects on juveniles because of the difficulty of following individuals to maturity. We used data from a long‐term study of individually marked gray seals (Halichoerus grypus; Fabricius, 1791) to test the hypothesis that larger offspring have higher survival to recruitment and are larger and more successful primiparous mothers than smaller offspring. Between 1998 and 2002, 1182 newly weaned female pups were branded with unique permanent marks on Sable Island, Canada. Each year through 2012, all branded females returning to the breeding colony were identified in weekly censuses and a subset were captured and measured. Females that survived were significantly longer offspring than those not sighted, indicating size‐selective mortality between weaning and recruitment. The probability of female survival to recruitment varied among cohorts and increased nonlinearly with body mass at weaning. Beyond 51.5 kg (mean population weaning mass) weaning mass did not influence the probability of survival. The probability of female survival to recruitment increased monotonically with body length at weaning. Body length at primiparity was positively related to her body length and mass at weaning. Three‐day postpartum mass (proxy for birth mass) of firstborn pups was also positively related to body length of females when they were weaned. However, females that were longer or heavier when they were weaned did not wean heavier firstborn offspring.     

Male size determines reproductive output in a paternal mouthbrooding fish

Size can have strong effects on reproductive success in both males and females, and in many species large individuals are preferred as mates. To estimate the potential benefits from mate choice for size in both sexes, I studied the effects of the size of each sex on the reproductive output of pairs of Banggai cardinalfish, Pterapogon kauderni, a sexually monomorphic obligate paternal mouthbrooder. When pairs were allowed to form freely, a size-assortative mating pattern was observed and larger pairs had a higher reproductive output as determined by total clutch weight and egg size. To separate the potential benefits from mate choice for size for each sex, I subsequently used these pairs to form reversed size-assortative pairs, that is, the largest male paired to the smallest female and vice versa. I found a positive correlation between male size and clutch size: relatively heavier clutches were found in pairs where females were given a larger male. This suggests that the size of the male influences clutch weight. For egg size, however, the size of both sexes seemed important. The study reveals the benefits of mutual mate choice on size in this species: larger females provide larger eggs and larger males can brood heavier clutches. Furthermore, these results suggest that females differentially allocate resources into the eggs according to the size of the mate.Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved .     

Maternal nutrition affects reproductive output and sex allocation in a lizard with environmental sex determination

Life-history traits such as offspring size, number and sex ratio are affected by maternal feeding rates in many kinds of animals, but the consequences of variation in maternal diet quality (rather than quantity) are poorly understood. We manipulated dietary quality of reproducing female lizards (Amphibolurus muricatus; Agamidae), a species with temperature-dependent sex determination, to examine strategies of reproductive allocation. Females maintained on a poor-quality diet produced fewer clutches but massively (twofold) larger eggs with lower concentrations of yolk testosterone than did conspecific females given a high-quality diet. Although all eggs were incubated at the same temperature, and yolk steroid hormone levels were not correlated with offspring sex, the nutrient-deprived females produced highly male-biased sex ratios among their offspring. These responses to maternal nutrition generate a link between sex and offspring size, in a direction likely to enhance maternal fitness if large body size enhances reproductive success more in sons than in daughters (as seems plausible, given the mating system of this species). Overall, our results show that sex determination in these animals is more complex, and responsive to a wider range of environmental cues, than that suggested by the classification of 'environmental sex determination'.     

Weapon performance, not size, determines mating success and potential reproductive output in the collared lizard (Crotaphytus collaris)

In territorial polygynous taxa, reproductive success reflects phenotypic variation. Using Crotaphytus collaris, a sexually dimorphic lizard in which males use the head (i.e., jaws and associated musculature) as a weapon when territorial interactions escalate to fights, we tested the hypothesis that weapon performance (i.e., bite force) is a better predictor of fitness than body or weapon size. Bite-force performance predicted the number of female home ranges overlapped, estimated mating success, and potential reproductive output. However, no body or weapon size measure correlated with these estimates of fitness, and only one weapon dimension (head width) correlated with bite force. These results indicate that weapon performance has far stronger effects on fitness than body or weapon size, likely because it directly influences fight outcomes. As such, it is desirable that the use of morphology as a proxy for performance and its presumed extensions to fitness be based on empirical morphology-performance relationships.     

Effects of season and population size on pollination and reproductive output in a Mediterranean shrub

• Pollinator guilds may change throughout extended flowering periods, affecting plant reproductive output, especially in seasonal climates. We hypothesised a seasonal shift in pollinator guild and an autumn reduction in pollinator abundance, especially in small and sparse populations.
• We recorded pollinator identity, abundance and behaviour in relation to flower density from plant to population throughout the extended flowering of Ononis tridentata. We evaluated female reproductive output by recording pollination success and pre‐dispersal seed predation in eight populations of contrasting size and density. Offspring quality was also characterised through seed weight and germination.
• A diverse guild of insects visited O. tridentata in spring, while only Apis mellifera was observed in autumn. Visitation frequency did not vary seasonally, but the number of flowers per foraging bout was lower, and seeds were heavier and had a higher germination rate in autumn. Plant and neighbourhood flowering display were not related to pollinator visitation frequency or behaviour. However, the rate of fertilised ovules, seed set and autumn flowering display size were positively related to population density.
• The maintenance of pollination in autumn enhances the reproductive performance of O. tridentata due to higher quality of autumn seed, and to a large reduction in seed predator pressure. We also suggest that observed changes in pollinator behaviour could be one of the processes behind seasonal variation in seed performance, since geitonogamous crosses were less likely to occur in autumn.

     

Effects of reproductive timing and colony size on the survival, offspring colony size and drone production in the honey bee (Apis mellifera)

ABSTRACT. 1. The effects of colony size and time of reproduction on the survival and size of offspring colonies and on drone production were examined for honey bees, Apis mellifera L. Drone and worker production and survival of parental and offspring colonies were monitored following swarming. Also, the temporal patterns of drone emergence and availability of unmated queens were examined.
2. Colony size at swarming was positively correlated with the number of workers invested in offspring colonies and the number of queens produced. However, colony size at swarming was not correlated with the number of offspring colonies produced.
3. Swarm size was positively correlated with drone and worker production after swarms were hived. Worker production of hived swarms was positively correlated with colony survival. Offspring queens which inherited a parental nest survived longer than queens in either primary swarms or afterswarms, presumably due to the advantage of inheriting a nest.
4. Drone emergence peaked just prior to swarming, the time when unmated queens were available. High drone production by colonies initiated by swarms probably reflected an attempt to reproduce prior to winter. The probabilities of a second swarming cycle within the same year and of surviving the winter were low for colonies initiated from swarms.     

Consequences of adult size for survival and reproductive performance in a herbivorous ladybird beetle

Abstract.

• 1 A univoltine herbivorous ladybird beetle Epilachna niponica (Coleoptera: Coccinellidae) shows a large variation in adult size within a population.
• 2 Large adults had higher survival from emergence to the reproductive season, and the size-dependent adult survival was most apparent during hibernation. On the other hand, adult survival during pre-hibernation contributed little to size-dependent overall survival.
• 3 Neither reproductive lifespan nor lifetime fecundity were a function of adult size, though large females produced larger size of egg batches.
• 4 Size of adult beetles was significantly reduced by leaf damage to plants on which they grew up on larval stage. Since leaf herbivory increases through the season, late emerged adults that were subjected to food deterioration during the larval period were smaller than early-emerged individuals.

     

Corticosterone stimulates hatching of late-term tree lizard embryos

The regulation of hatching in oviparous animals is important for successful reproduction and survival, but is poorly understood. We unexpectedly found that RU-486, a progesterone and glucocorticoid antagonist, interferes with hatching of viable tree lizard (Urosaurus ornatus) embryos in a dose-dependent manner and hypothesized that embryonic glucocorticoids regulate hatching. To test this hypothesis, we treated eggs with corticosterone (CORT) or vehicle on Day 30 (85%) of incubation, left other eggs untreated, and observed relative hatch order and hatch time. In one study, the CORT egg hatched first in 9 of 11 clutches. In a second study, the CORT egg hatched first in 9 of 12 clutches, before vehicle-treated eggs in 10 of 12 clutches, and before untreated eggs in 7 of 9 clutches. On average, CORT eggs hatched 18.2 h before vehicle-treated eggs and 11.6 h before untreated eggs. Thus, CORT accelerates hatching of near-term embryos and RU-486 appears to block this effect. CORT may mobilize energy substrates that fuel hatching and/or accelerate lung development, and may provide a mechanism by which stressed embryos escape environmental stressors.     

Relationships between egg size, chick size at hatching, and chick survival in the Whimbrel Numenius phaeopus

The relationships between egg size, chick size at hatching and chick survival in Whimbrels Numenius phaeopus were studied over a three-year period in the Shetland Isles. Three measurements of chick size at hatching were all positively correlated with egg volume, though the relationship was strongest with hatchling body-weight. In two of the three years the proportion of chicks from a brood which survived to fledging increased significantly with the mean hatching weight of chicks in the brood. Within broods, a significant effect of hatching weight on survival was detectable only up to 7 days after hatching. Between years the egg volumes and hatchling weights of individual female Whimbrels showed relatively little variability, indicating that these attributes could be controlled to a large extent by inheritance.     

Thermal dependence of reproductive allocation in a tropical lizard

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

Fitness of juvenile lizards depends on seasonal timing of hatching,not offspring body size

To understand how selection shapes life-history traits, we need information on the manner in which offspring phenotypes influence fitness. Life-history allocation models typically assume that “bigger offspring are better”, but field data paint a more complex picture: larger offspring size sometimes enhances fitness, and sometimes not. Additionally, higher survival and faster growth of larger offspring might be due to indirect maternal effects (e.g., mothers allocate hormones or nutrients differently to different-sized eggs), and not to offspring size per se. Alternative factors, such as seasonal timing of hatching, may be more important. We examined these issues using 419 eggs from captive jacky dragon lizards (Amphibolurus muricatus). The mothers were maintained under standardized conditions to minimize variance in thermal and nutritional history, and the eggs were incubated under controlled conditions to minimize variance in offspring phenotypes due to incubation temperature and moisture. We reduced the size of half the eggs (and, thus, the size of the resultant hatchlings) from each clutch by yolk extraction. The hatchlings were marked and released at a field site over a 3-month period, with regular recapture surveys to measure growth and survival under natural conditions. Growth rates and survival were strongly enhanced by early-season hatching, but were not affected by hatchling body size.     

Daily timing of hatching of a rotifer,Keratella cochlearis

Groups of Keratella cochlearis f. tecta were collected over a complete diel period from a shallow pool. Observed in the laboratory, the hatchings of the field-produced eggs were not significantly periodic.