Lizards combine stored energy and recently acquired nutrients flexibly to fuel reproduction

1. Energy allocation strategies for reproduction are viewed typically as a continuum between reliance on 'income' (recently acquired energy) vs. 'capital' (stored reserves) for fuelling reproduction. Because ectothermy facilitates long-term energy storage and often involves low feeding rates, traditional views suggest that many ectotherms rely heavily on stored reserves for egg production. 2. We explored the temporal relationship between energy intake and expenditure in a multi-clutching lizard (Amphibolurus muricatus) by evaluating the effect of maternal nutrition on reproductive output and by contrasting delta(13)C measurements of the maternal diet and endogenous energy stores with that of the eggs produced. 3. Our experiment revealed that females utilize both endogenous energy stores and recently acquired food to fuel reproduction; this pattern did not shift seasonally from first to second clutches produced. Importantly, however, egg lipid was derived primarily from capital, whereas egg protein was derived about equally from both income and capital. 4. Overall, these results suggest that the energy allocation strategy used for reproduction differs among egg components, and that the use of recently acquired energy for reproduction may be more widespread in ectotherms than thought previously.     

Impacts of bleaching on the soft coral Lobophytum compactum. I. Fecundity, fertilization and offspring viability

We document long-term effects of a simulated bleaching event on the reproductive output and offspring viability of the soft coral Lobophytum compactum. Corals were subjected to temperature and solar radiation treatments to produce both moderately (48–60%) and heavily (90–95%) bleached colonies. Although bleached colonies recovered their zooxanthellae within 10 to 18 weeks, impacts on reproductive output were significant for at least two annual spawning seasons. In the first year, both polyp fecundity and mean oocyte diameter were reduced and inversely correlated with the degree of bleaching, with complete failure of fertilization in the group of heavily bleached colonies. For moderately bleached soft corals, survival and growth of sexual offspring did not differ significantly from those of unbleached colonies. Although no further reductions in zooxanthellae densities in experimental soft corals were recorded throughout the subsequent second year, egg size and fecundity of the heavily bleached soft corals were still significantly reduced 20 months later. Severe bleaching clearly has long-term sub-lethal impacts, reducing overall reproductive output for at least two spawning seasons. Accepted: 1 June 2000     

Gametogenesis,brooding and planulation in laboratory populations of a temperate scleractinian coral Balanophyllia elegans maintained under contrasting photoperiod regimes

Summary

Males of Balanophyllia elegans Verrill, 1864 in Monterey Bay, California, spawn in the fall. Fertilization occurs within the females and the internally brooded embryos develop into large benthic planulae that are released mainly in the late winter. Field-collected corals were held in the laboratory under contrasting photoperiod regimes (ambient or in-phase, and 6 months out-of-phase) for 6.5 years. After two years in the laboratory corals planulated at the same time, independent of photoperiod. Corals show a cyclic pattern of later winter and early spring planulation that coincides with declining sea temperatures in Monterey Bay. Gametes appeared in the first laboratory generation at IS months and brooded embryos were found in females at 31 months under both light regimes. Planulae production by laboratory-reared corals peaked at the same time as that of the parents. These findings suggest that the temporal pattern of planulation is regulated by both endogenous and exogenous components that can be modified in some way by disturbance caused to the corals when collected or by the time of collection.     

Main lipid classes in some species of deep-sea corals in the Newfoundland and Labrador region (Northwest Atlantic Ocean)

Corals contain large quantities of lipids in their tissues; these lipids may be either structural or for storage. Little information is available about the lipid content of deep-sea corals, as well as ratios of main lipid classes. In this study, lipid percentages of 81 deep-sea specimens were measured and the presence of six major classes, including sterols (STEROLS), free fatty acids (FFA), triacylglycerols (TG), monoalkyldiacyl glycerol (MADAG), wax (WAX), and sterol esters (SE), was assessed. Deep-sea corals had fewer lipids than their shallow water counterparts. Decision-tree analysis revealed a link between coral groups and total lipid percentages, showing that species within the same group were characterized by similar lipid amounts. Depth did not seem to impact the total lipid percentages, suggesting that deep-sea corals adapt to the differential access to food by changing the proportion of lipid classes while maintaining equivalent lipid levels. In deep-sea species, similar to their shallow water counterparts, energy seems to be stored as neutral lipids (wax esters and triacylglycerols), with the notable difference that a high proportion of MADAG is present. These compounds are less rich in energy than TG. Depth trends were found for FFA, TG and SE with an increase in percentages after 800 m suggesting a potential need for storage due to decreased food availability. A subsequent decrease after 1,100 m was observed for FFA and TG but a more detailed investigation is warranted as the number of specimens acquired from these depths was less than 20. It is nonetheless a surprising result as increased storage is expected when food sources are sparse.     

Reproduction and larval rearing of amphibians

Reproduction technologies for amphibians are increasingly used for the in vitro treatment of ovulation, spermiation, oocytes, eggs, sperm, and larvae. Recent advances in these reproduction technologies have been driven by (1) difficulties with achieving reliable reproduction of threatened species in captive breeding programs, (2) the need for the efficient reproduction of laboratory model species, and (3) the cost of maintaining increasing numbers of amphibian gene lines for both research and conservation. Many amphibians are particularly well suited to the use of reproduction technologies due to external fertilization and development. However, due to limitations in our knowledge of reproductive mechanisms, it is still necessary to reproduce many species in captivity by the simulation of natural reproductive cues. Recent advances in reproduction technologies for amphibians include improved hormonal induction of oocytes and sperm, storage of sperm and oocytes, artificial fertilization, and high-density rearing of larvae to metamorphosis. The storage of sperm in particular can both increase the security and reduce the cost of maintaining genetic diversity. It is possible to cryopreserve sperm for millennia, or store it unfrozen for weeks in refrigerators. The storage of sperm can enable multiple parentages of individual females' clutches of eggs and reduce the need to transport animals. Cryopreserved sperm can maintain the gene pool indefinitely, reduce the optimum number of males in captive breeding programs, and usher in new generations of Xenopus spp. germ lines for research. Improved in vitro fertilization using genetic diversity from stored sperm means that investigators need the oocytes from only a few females to produce genetically diverse progeny. In both research and captive breeding programs, it is necessary to provide suitable conditions for the rearing of large numbers of a diverse range of species. Compared with traditional systems, the raising of larvae at high densities has the potential to produce these large numbers of larvae in smaller spaces and to reduce costs.     

Reproduction and the origin of polyploids in hybrid salamanders of the genus Ambystoma

Eggs and larvae produced by diploid, triploid, and tetraploid females collected from breeding ponds on Pelee Island in Lake Erie were studied to examine the reproductive mechanism. No instance of parthenogenesis was found as all examined females required sperm to produce viable progeny. Diploid females produced diploid and triploid larvae, triploid females produced triploid and tetraploid larvae, and tetraploid females produced triploid and tetraploid larvae. The majority of the eggs produced by hybrid females do not develop or do not complete embryogenesis. Electrophoretic examination of females and their offspring demonstrate that the male genome is being incorporated in reduced as well as unreduced eggs produced by all three ploidy classes of females. The elevation of ploidy among Pelee Island Ambystoma is attributed to sperm incorporation in unreduced eggs. Triploid as well as tetraploid individuals are constantly being produced. A critical examination of the literature on parthenogenetic or gynogenetic modes of reproduction in North America Ambystoma hybrids shows no conclusive evidence supporting these modes and it is suggested that the reproductive mechanism found among Pelee Island female hybrids may be more generally applied to other hybrid Ambystoma populations.     

Experimental fragmentation reduces sexual reproductive output by the reef-building coral Pocillopora damicornis

Natural and anthropogenic disturbances may fragment stony reef corals, but few quantitative data exist on the impacts of skeletal fragmentation on sexual reproduction in corals. We experimentally fragmented colonies of the branching coral Pocillopora damicornis and determined the number and size of planula larvae released during one lunar reproductive cycle. Partially fragmented colonies significantly delayed both the onset and peak period of planula release compared with intact control colonies. Most fragments removed from the corals died within 11–18 days, and released few planulae. The total number of planulae released per coral colony varied exponentially with remaining tissue volume, and was significantly lower in damaged versus undamaged colonies. However, the number of planulae produced per unit tissue volume, and planula size, did not vary with damage treatment. We conclude that even partial fragmentation of P. damicornis colonies (<25% of tissue removed) decreases their larval output by reducing reproductive tissue volume. Repeated breakage of corals, such as caused by intensive diving tourism or frequent storms, may lead to substantially reduced sexual reproduction. Therefore, reef management should limit human activities that fracture stony corals and lead to decreases in colony size and reproductive output. Accepted: 2 February 2000     

Recruitment patterns of scleractinian corals in an isolated sub-tropical reef system

The density of recruits of scleractinian corals on settlement plates at Lord Howe Island, a small isolated sub-tropical island 630 km off the Australian coastline, was within the range of values reported for comparable studies on the Great Barrier Reef. However, there was a difference in the relative abundance of taxonomic groups, with recruitment at Lord Howe Island during the summer of 1990/91 dominated by corals from the Family Pocilloporidae, Family Poritidae, and sub-genus Acropora (Isopora) (in order of abundance). By contrast, on the Great Barrier Reef, recruits are generally predominantly species from the Family Acroporidae (other than the Acropora (Isopora) group). Both the recruits and the established coral communities at Lord Howe Island are dominanted by corals which release brooded planulae, as opposed to the pattern of mass-spawning with external fertilisation more typical of Great Barrier Reef corals. I hypothesise that the release of brooded planulae would be advantageous in an isolated reef community because (a) brooded larvae can travel large distances and survive the journey to the isolated reef and/or (b) brooded larvae have a shorter period before they are competent to settle and are therefore more likely to be retained on the parental reef once a population has been established.     

Allocation policy of female freshwater pearl mussels

Living exclusively in trout streams which are very poor in nutrients, freshwater pearl mussels are physiologically adapted to the low food supply by a reduced metabolism. Longevity of these mussels spans decades and life-time fecundity of females is very high (up to 2*10⁸ larvae). Their resource allocation policy favours survival over current reproduction. Reproductive effort (per reproductive period) falls within the lowest range of values reported for molluscs (0.8–5.3% of the total organic substance). The soft parts (without larvae) of reproducing females are heavier compared to pausing ones, indicating that only those females reproduce which exceed a threshold value of body weight. The more they exceed this value the more larvae they produce. Surplus energy (the amount above the threshold) is not completely devoted to reproduction but is in part invested in somatic functions. At the population level this allocation system results in largely size independent fecundity values, varying considerably between individuals and in a variable percentage (5–54%) of females taking part in reproduction every year. The evolution of this system must be attributed to the reduced metabolism and growth. This provides the basis for a very long life accompanied with many spawning periods. Accordingly fitness can be improved by extending longevity. Received: 27 April 1998 / Accepted: 13 July 1998     

Changes in gametogenesis and fecundity of acroporid corals that were exposed to elevated nitrogen and phosphorus during the ENCORE experiment

Colonies of two scleractinian reef coral species, Acropora longicyathus and Acropora aspera were transplanted into patch reefs at One Tree Reef, Great Barrier Reef, Australia as part of the ENCORE experiment. These corals and colonies of A. aspera which were naturally present in the patch reefs were exposed to four treatments over two years: controls with normal seawater, elevated levels of nitrogen only, phosphorus only, or nitrogen plus phosphorus. These corals were sampled and used to determine whether gametogenic cycles and fecundity were affected by nutrient enrichment. Acropora longicyathus had a single annual gametogenic cycle. Corals exposed to elevated nitrogen produced significantly smaller and fewer eggs and contained less testes material than those which were not exposed to nitrogen. Exposure to elevated phosphorus only resulted in corals producing more but smaller eggs, and more testes material. Egg numbers of colonies from other treatments decreased as the gametogenic cycles continued, but those of the phosphorus colonies showed almost no reduction in egg numbers between the early and late stages of the gametogenic cycles. These results have important management implications for coral reefs as they demonstrate that small increases in concentrations of nitrogen and phosphorus can have severe effects on reproductive activity in these species of scleractinian corals.     

Not All Offspring Are Created Equal: Variation in Larval Characteristics in a Serially Spawning Damselfish

The way organisms allocate their resources to growth and reproduction are key attributes differentiating life histories. Many organisms spawn multiple times in a breeding season, but few studies have investigated the impact of serial spawning on reproductive allocation. This study investigated whether resource allocation was influenced by parental characteristics and prior spawning history in a serial spawning tropical damselfish (Pomacentrus amboinensis). The offspring attributes of isolated parents of known characteristics were monitored over a 6-week breeding period in the field. Smaller females produced larvae of longer length and larger energy reserves at hatching. This finding is contrary to several other studies that found larger females produce offspring of greater quality. We found that resource allocation in the form of reproductive output was not influenced by the number of spawning events within the breeding season, with larger females producing the greatest number of offspring. Larval characteristics changed as spawning progressed. There was a general decline in length of larvae produced, with an increase in the size of the larval yolk-sac, for all females regardless of size as spawning progressed. This trend was accentuated by the smallest females. This change in larval characteristics may reflect a parental ability to forecast unfavourable conditions as the season progresses or a mechanism to ensure that some will survive no matter what conditions they encounter. This study highlights the importance of accounting for temporal changes in reproductive allocation in studies of reproductive trade-offs and investigations into the importance of parental effects.     

Gregariousness and protandry promote reproductive insurance in the invasive gastropod Crepidula fornicata: evidence from assignment of larval paternity

According to the size-advantage hypothesis, protandric sequential hermaphroditism is expected when the increase in reproductive success with age or size is small for males but large for females. Interestingly, some protandrous molluscs have developed gregarious strategies that might enhance male reproductive success but at the cost of intraspecific competition. The gastropod Crepidula fornicata, a European invading species, is ideal for investigating mating patterns in a sequential hermaphrodite in relation to grouping behaviour because individuals of different size (age) live in perennial stacks, fertilization is internal and embryos are brooded. Paternity analyses were undertaken in stacks sampled in three close and recently invaded sites in Brittany, France. Paternity assignment of 239 larvae, sampled from a set of 18 brooding females and carried out using five microsatellite loci, revealed that 92% of the crosses occurred between individuals located in the same stack. These stacks thus function as independent mating groups in which individuals may reproduce consecutively as male and female over a short time period, a pattern explained by sperm storage capacity. Gregariousness and sex reversal are promoting reproductive insurance in this species. In addition, females are usually fertilized by several males (78% of the broods were multiply sired) occupying any position within the stack, a result reinforcing the hypothesis of sperm competition. Our study pointed out that mating behaviours and patterns of gender allocation varied in concert across sites suggesting that multiple paternities might enhance sex reversal depending on sperm competition intensity.     

The effects of size, age and a cost of early breeding on reproduction in female mountain hares

Both age and size may influence female reproductive performance in mammals, and successful early reproduction may lead to reduced success at later attempts. The effects of age, size and early reproduction on distribution of reproductive effort throughout a single breeding season was examined in female mountains hares Lepus timidus L. Hind foot length was used as an index of body size, because, unlike body weight, it did not fluctuate with reproductive status. Fifty-six female carcasses were collected from March to October 1984, and their litters were assigned to one of three chronologically equal'litter periods'(1–3) of equal length. Whereas number of ova shed was always independent of age, large females shed more ova than did smaller females in litter periods 1 and 2. Prenatal mortality of ova and embryos was highest during litter period 1, when it was independent of age and size. Although prenatal mortality remained high in first year females in litter period 2, there was an overall decline through to the final litter period when it was negligible. Total number of young produced through the season increased with skeletal size in old females (age > 1), but not significantly in first year females. It is concluded that large size, rather than age, favours early reproduction in mountain hares. Every additional offspring produced in litter periods 1 and 2 reduced that female's production in period 3. After correcting for this cost of early reproduction the number of young produced in the final litter period also increased with maternal size.     

Alternative reproductive tactics in snail shell‐brooding cichlids diverge in energy reserve allocation

Life history theory predicts that the amount of resources allocated to reproduction should maximize an individual's lifetime reproductive success. So far, resource allocation in reproduction has been studied mainly in females. Intraspecific variation of endogenous energy storage and utilization patterns of males has received little attention, although these patterns may vary greatly between individuals pursuing alternative reproductive tactics (ARTs). ARTs are characterized by systematic variation of behavioral, physiological, and often morphological traits among same‐sex conspecifics. Some individuals may rely on previously accumulated reserves, because of limited foraging opportunities during reproduction. Others may be able to continue foraging during reproduction, thus relying on reserves to a lesser extent. We therefore predicted that, if male tactics involve such divergent limitations and trade‐offs within a species, ARTs should correspondingly differ in energy reserve allocation and utilization. To test this prediction, we studied short‐term and long‐term reserve storage patterns of males in the shell‐brooding cichlid Lamprologus callipterus. In this species, bourgeois males investing in territory defense, courtship, and guarding of broods coexist with two distinct parasitic male tactics: (1) opportunistic sneaker males attempting to fertilize eggs by releasing sperm into the shell opening when a female is spawning; and (2) specialized dwarf males attempting to enter the shell past the spawning female to fertilize eggs from inside the shell. Sneaker males differed from other male types by showing the highest amount of accumulated short‐term and long‐term fat stores, apparently anticipating their upcoming adoption of the nest male status. In contrast, nest males depleted previously accumulated energy reserves with increasing nest holding period, as they invest heavily into costly reproductive behaviors while not taking up any food. This conforms to a capital breeder strategy. Dwarf males did not accumulate long‐term fat stores at all, which they can afford due to their small behavioral effort during reproduction and their continued feeding activity, conforming to an income breeder strategy. Our data confirm that the resource storage patterns of males pursuing ARTs can diverge substantially, which adds to our understanding of the coexistence and maintenance of alternative reproductive patterns within species.     

Long sperm fertilize more eggs in a bird

Sperm competition, in which the ejaculates of multiple males compete to fertilize a female''s ova, results in strong selection on sperm traits. Although sperm size and swimming velocity are known to independently affect fertilization success in certain species, exploring the relationship between sperm length, swimming velocity and fertilization success still remains a challenge. Here, we use the zebra finch (Taeniopygia guttata), where sperm size influences sperm swimming velocity, to determine the effect of sperm total length on fertilization success. Sperm competition experiments, in which pairs of males whose sperm differed only in length and swimming speed, revealed that males producing long sperm were more successful in terms of (i) the number of sperm reaching the ova and (ii) fertilizing those ova. Our results reveal that although sperm length is the main factor determining the outcome of sperm competition, complex interactions between male and female reproductive traits may also be important. The mechanisms underlying these interactions are poorly understood, but we suggest that differences in sperm storage and utilization by females may contribute to the outcome of sperm competition.     

Male reproductive allocation in fireflies (Photinus spp.)

Abstract. Resource allocation between somatic and reproductive structures has important fitness consequences for individuals, and optimal trade-offs are expected to depend not only on mating system differences among species but also on levels of resource stress within species. We tested the prediction that polyandry (associated with increased sperm competition) will increase male reproductive allocation in bioluminescent fireflies in Photinus spp. by comparing the relative mass of testes, seminal vesicles, and reproductive accessory glands among a monandrous and several polyandrous species. In addition, we examined a single population of a polyandrous species, Photinus greeni , to see how reproductive allocation might shift between years in response to different levels of larval resource stress. As predicted, males of P. collustrans , a monandrous species, showed a fivefold lower allocation to sperm production and a 100-fold lower allocation to reproductive accessory glands compared with males from polyandrous species. We also found evidence within P. greeni of a trade-off between allocation either to reproduction or to somatic tissue; following larval resource stress, males eclosed at significantly shorter body lengths, yet showed a 35% increase in their reproductive allocation. These results demonstrate that mating systems strongly influence male allocation to reproductive accessory glands as well as to sperm production. Furthermore, these results suggest that under larval resource stress males of Photinus spp. increase their allocation to reproduction at the expense of somatic tissue, thus maximizing their ability to produce nuptial gifts required for reproductive success.     

Mating frequency and resource allocation to male and female function in the simultaneous hermaphrodite land snail Arianta arbustorum

Sex allocation theory predicts that mating frequency and long‐term sperm storage affect the relative allocation to male and female function in simultaneous hermaphrodites. We examined the effect of mating frequency on male and female reproductive output (number of sperm delivered and eggs deposited) and on the resources allocated to the male and female function (dry mass, nitrogen and carbon contents of spermatophores and eggs) in individuals of the simultaneous hermaphrodite land snail Arianta arbustorum. Similar numbers of sperm were delivered in successive copulations. Consequently, the total number of sperm transferred increased with increasing number of copulations. In contrast, the total number of eggs produced was not influenced by the number of copulations. Energy allocation to gamete production expressed as dry mass, nitrogen or carbon content was highly female‐biased (>95% in all estimates). With increasing number of copulations the relative nitrogen allocation to the male function increased from 1.7% (one copulation) to 4.7% (three copulations), but the overall reproductive allocation remained highly female‐biased. At the individual level, we did not find any trade‐off between male and female reproductive function. In contrast, there was a significant positive correlation between the resources allocated to the male and female function. Snails that delivered many sperm also produced a large number of eggs. This finding contradicts current theory of sex allocation in simultaneous hermaphrodites.     

Mixed asexual and sexual reproduction in the Indo‐Pacific reef coral Pocillopora damicornis

Pocillopora damicornis is one of the best studied reef‐building corals, yet it's somewhat unique reproductive strategy remains poorly understood. Genetic studies indicate that P. damicornis larvae are produced almost exclusively parthenogenetically, and yet population genetic surveys suggest frequent sexual reproduction. Using microsatellite data from over 580 larvae from 13 colonies, we demonstrate that P. damicornis displays a mixed reproductive strategy where sexual and asexual larvae are produced simultaneously within the same colony. The majority of larvae were parthenogenetic (94%), but most colonies (10 of the 13) produced a subset of their larvae sexually. Logistic regression indicates that the proportion of sexual larvae varied significantly with colony size, cycle day, and calendar day. In particular, the decrease in sexual larvae with colony size suggests that the mixed reproductive strategy changes across the life of the coral. This unique shift in reproductive strategy leads to increasingly asexual replications of successful genotypes, which (in contrast to exclusive parthenogens) have already contributed to the recombinant gene pool.     

Production and supply of larvae as determinants of zonation in a brooding tropical coral

Production and settlement of planktonic larvae of the coral Favia fragum (Esper) were studied. The species is restricted to shallow back- and fore-reef habitats throughout the Caribbean Sea. Adults are in their greatest abundance on the reef-crest and shallow reef slope (<3 m) at Tague Bay, St. Croix, in the US Virgin Islands. Because F. fragum broods larvae that are capable of immediate settlement, this distribution pattern may be due to variation in fecundity among depths. Corals were collected from shallow (1.0 m) and deep depths (10-13 m) and cultured in individual containers exposed to shaded ambient light. Corals from shallow depths had greater fecundity (polyp⁻¹ lunar cycle⁻¹) and were larger than deep corals. To test the hypothesis that fecundity was related to successful fertilization, corals were kept in different densities in an area with sea-grass, where there were no natural adults. Production of larvae 6 months later was not affected by density of adults, possibly due to self-fertilization. Larval choice of habitat was also examined. In the laboratory, twice as many larvae settled on coral rubble fragments collected from depths where adults were common (1.5 and 3 m) than on those from depths where adults were rare (10 m). Larval supply may establish the vertical distribution of adults on St. Croix.     

Changes in body composition and morphology of young-of-the-year gulf menhaden, Brevoortia patronus Goode, in Fourleague Bay, Louisiana

Body composition (lipid, water, protein, energy content) and metamorphosis of young-of-the-year gulf menhaden, Brevoortia patronus Goode, were examined over a yearly cycle in Fourleague Bay, Louisiana. Metamorphosis from larvae to juveniles, as indicated by the body depth to length ratio, was completed by 30 mm S.L. Analysis of the length/weight relationship indicated separate equations for larvae/postlarvae (< 30 mm S.L.) and juvenile/subadults (30–100 mm S.L.). Major body composition changes from larvae to subadult included an increase in lipid content, a corresponding increase in energy content, and a decrease in nitrogen content. Young-of-the-year gulf menhaden did not exhibit the seasonal pattern of condition factors typical of adult clupeids. There may be a shift in energy allocation away from protein growth to lipid storage associated with attainment of a larger size. Initiation of emigration may be related to lipid storage and temperature change, with higher lipid content fish migrating first. End-of-year variations in fish size and lipid storage may be related to environmental conditions, such as water temperature and salinity.