Reproductive cycles in tropical intertidal gastropods are timed around tidal amplitude cycles

Reproduction in iteroparous marine organisms is often timed with abiotic cycles and may follow lunar, tidal amplitude, or daily cycles. Among intertidal marine invertebrates, decapods are well known to time larval release to coincide with large amplitude nighttime tides, which minimizes the risk of predation. Such bimonthly cycles have been reported for few other intertidal invertebrates. We documented the reproduction of 6 gastropod species from Panama to determine whether they demonstrate reproductive cycles, whether these cycles follow a 2‐week cycle, and whether cycles are timed so that larval release occurs during large amplitude tides. Two of the species (Crepidula cf. marginalis and Nerita scabricosta) showed nonuniform reproduction, but without clear peaks in timing relative to tidal or lunar cycles. The other 4 species show clear peaks in reproduction occurring every 2 weeks. In 3 of these species (Cerithideopsis carlifornica var. valida, Littoraria variegata, and Natica chemnitzi), hatching occurred within 4 days of the maximum amplitude tides. Siphonaria palmata exhibit strong cycles, but reproduction occurred during the neap tides. Strong differences in the intensity of reproduction of Cerithideopsis carlifornica, and in particular, Littoraria variegata, between the larger and smaller spring tides of a lunar month indicate that these species time reproduction with the tidal amplitude cycle rather than the lunar cycle. For those species that reproduce during both the wet and dry seasons, we found that reproductive timing did not differ between seasons despite strong differences in temperature and precipitation. Overall, we found that most (4/6) species have strong reproductive cycles synchronized with the tidal amplitude cycle and that seasonal differences in abiotic factors do not alter these cycles.     

Embryonic development of the false limpet Siphonaria lateralis from Atlantic Patagonia

Siphonariids are pulmonate gastropods inhabiting rocky intertidal habitats, and many studies have focused on these false limpets around the world. In the southern South Atlantic, studies on reproduction and development in species of Siphonaria are scarce. We studied the embryonic development and egg masses of Siphonaria lateralis at its northernmost distribution in Atlantic Patagonia. In S. lateralis, as in most species of Siphonaria, individuals spawn benthic egg masses that strongly attach to intertidal rocky substrata. A single spherical egg that measures ~120 µm develops inside the egg capsule of S. lateralis. Considering the relatively small egg size, and reports from previous studies, the developmental modality of S. lateralis might be expected to include a planktotrophic larval phase. However, we found that hatchlings emerged as 1‐mm crawling juveniles, probably owing to the presence of intracapsular fluid, which may provide the energetic requirements for direct development. The embryonic size changed little from the egg to veliger stages, and then increased rapidly until the hatchling stage. We compared development in S. lateralis with development in the sympatric Siphonaria lessonii, in which egg size was reported to be ~80 µm and hatching occurs as planktotrophic veliger larvae. In these two species, spawn and early intracapsular developmental modes are remarkably different; these differences represent contrasting ways to survive in the harsh and physically stressful intertidal Patagonian coasts.     

Fecundity and Longevity of Green Vegetable Bug,Nezara viridula, Following Parasitism byTrichopoda giacomellii

The effects of parasitism by the ArgentinianTrichopoda giacomellii(Blanchard) on reproduction and longevity of its host,Nezara viridula(L.) are reported. Parasitoid larvae suppress egg maturation, reducing by 70% the fecundity of mature female hosts during the period of larval development. Egg viability was not affected, but mating frequency was reduced by approximately 50%. When parasitized as newly eclosed adults, 84% of females fail to reproduce. In male hosts, fertility and mating frequency were not affected during the period of larval parasitoid development. In male and reproductively immature female hosts, death was coincident with, or occurred shortly after parasitoid emergence (2–4 days); in mature females, death occurred on average 2 weeks after larval parasitoid emergence. Host mortality occurred as a consequence of tissue damage incurred as the parasitoid larvae emerged from the host. Some individuals survived parasitism though no further reproductive activity (mating or oviposition) occurred. The effectiveness ofT. giacomelliias a biological control agent is discussed in relation to its impact on reproduction and survival of its host and contrasted with the action of otherTrichopodaspecies.     

Larvae provide first evidence of successful reproduction by pallid sturgeon, Scaphirhynchus albus, in the Mississippi River

The pallid sturgeon (Scaphirhynchus albus) was not described until 1905, when it was commonly caught by commercial fishers. This species began to decline in the early 1900s presumably because of overharvest and habitat degradation. The U.S. Fish and Wildlife Service listed S. albus as an endangered species in 1990. Because S. albus live in deep, turbid rivers that are difficult to sample, very little is known about its reproductive timing and spawning habitat. The act of spawning has never been observed in nature. Captures of wild young S. albus verifying natural reproduction are rare, the last being a 4‐year‐old fish taken in 1978. In this paper, we describe the first collection of a larval S. albus from the wild and subsequent larval collections in the Mississippi River from 1998 to 2000 using a modified slingshot balloon trawl (the Missouri Trawl) designed to capture small fishes in deep, turbulent rivers. We captured larval Scaphirhynchus spp., including verified S. albus, in association with island habitats often in heavy detritus, especially at downstream tips. We postulate that Scaphirhynchus spp. spawned at the heads of islands upstream from where we collected larvae, but we cannot be certain. The capture of larval S. albus verifies reproduction possibly from the lower Missouri River to the upper and lower Mississippi River. However, we found no evidence of recruitment of S. albus from 1998 to 2000 as we were unable to capture juveniles after 374 trawl hauls that captured over 21 735 fish.     

Sexual and asexual reproduction of the holothurian Stichopus chloronotus (Echinodermata): a comparison between La Réunion (Indian Ocean) and east Australia (Pacific Ocean)

Summary

Stichopus chloronotus (Brandt, 1835) is one among nine aspidochirotide holothurian species known to reproduce both sexually by broadcast spawning and asexually by transverse fission. New data on the sexual cycle of this species in La Réunion are presented here and information available on sexual and asexual reproduction in this species is summarised. Sexual reproduction on La Réunion shows a distinct seasonality with a main spawning period in the warm season (November-February). The spawning period the Great Barrier Reef appears to be at the same time. Some intriguing deviations from unity in sex-ratio, usually biased towards more male individuals, have been observed in both geographic regions (sex ratio at La Reunion 31:1). New data on the asexual reproduction of this species in La Réunion confirm the high rates of fission. The peak of asexual reproduction in both the Indian and Pacific Ocean was observed in winter (June-July). Thus, asexual reproduction in this species occurs outside the season for sexual reproduction. The rate of asexual reproduction appears to vary between sample locations. However, results of population genetic studies on S. chloronotus (Uthicke et al., 1999; Uthicke et al., 2001) indicated that in most populations investigated a maximum of about 60% of all individuals may be derived from sexual recruitment. Cluster analyses on genetic distances between populations grouped populations within Oceans together, with the exception of one sample from a nearshore reef of the GBR. Although genetic differences between the two regions exist, these are relatively small regarding the large geographic distance. We conclude that asexual reproduction in S. chloronotus is important to maintain local population sizes, but that larval exchange between populations mediated by sexual reproduction is important for colonisation of new areas and to provide connectivity between populations. Here, we present the first synthesis of these phenomena for a holothurian species.     

Reproduction and larval development of the gastropodAlaba vladivostokensis in Vostok Bay, the Sea of Japan

The reproduction and development of the prosobranch gastropodAlaba vladivostokensis Bartsch were studied. In Vostok Bay,A. vladivostokensis reproduces in the warmest season at water temperatures of 19–23°C. The females lay egg masses in the shape of flat, coiled bands on eelgrass leaves and on sargosso thalluses. The total period of development from egg laying to larval settling takes 25–27 days. The reproduction and development patterns and larval morphology ofA. vladivostokensis are similar to that ofAustralaba picta (A. Adams), which inhabits the coast of Japan. It is suggested that the population ofA. vladivostokensis in Peter the Great Bay should considered as part of the wide geographical range ofA. picta.     

Effect of different diets on the growth and development of Harmonia axyridis (Pallas)

Harmonia axyridis (Pallas) is an important natural enemy of crop pests. Feeding H. axyridis through artificial diets (ADs) is an important means to achieve large-scale production. In this study, the effects of different diets on the growth, development and reproduction of H. axyridis were comprehensively evaluated, and the reasons for the reduced reproductive capacity of H. axyridis fed ADs were preliminarily explored. Artificial diets were prepared using pig liver and pork as the main ingredients. Larval duration, larval survival rate, egg production and other traits were comprehensively evaluated. Harmonia axyridis fed ADs during both the larval and adult periods completed growth and development from larva to adult but had a prolonged development duration (6.13-day extension) and reduced survival rate (15.3% reduction) in the larval stage. In addition, adults could not lay eggs. Next, individuals of H. axyridis were fed Megoura japonica (Matsumura) in the larval stage and an AD, adequate aphids (AA) or an artificial diet plus 5 (AD5), 10 (AD10) or 25 (AD25) aphids in the adult stage. The adults in the AD group produced a small number of eggs (103.3 eggs). When aphids were added to the diet, egg production gradually increased with the number of aphids added. The AD25 group exhibited no significant difference in egg production compared with that in the AA group (983.8 eggs and 1,158.3 eggs, respectively). Anatomical observations of the H. axyridis adults in these five groups revealed that ovary development was slowest in the AD group. In addition, we found that the levels of vitellogenin and juvenile hormone were significantly lower in the AD group than in the AA group. These results provide a foundation for formulating ADs for H. axyridis and improving the large-scale reproduction of this species.     

Acceptance and suitability of novel trees for <Emphasis Type="Italic">Orthotomicus erosus</Emphasis>, an exotic bark beetle in North America

To predict whether an herbivorous pest insect will establish in a new area, the potential host plants must be known. For invading bark beetles, adults must recognize and accept trees suitable for larval development. The preference-performance hypothesis predicts that adults will select host species that maximize the fitness of their offspring. We tested five species of North American conifers and one angiosperm for adult acceptance and suitability for reproduction of the Mediterranean pine engraver, Orthotomicus erosus (Wollaston). Red pine, Pinus resinosa Aiton, and white spruce, Picea glauca (Moench) Voss, were accepted by adult beetles and suitable for reproduction to the extent of adult replacement. Others, such as balsam fir, Abies balsamea (L.) Mill., eastern hemlock, Tsuga canagensis (L.) Carrière, and tamarack, Larix laricina (Du Roi) Koch, were acceptable but unsuitable. The presence of tree species that are acceptable to adults but unsuitable for reproduction may affect the ability of O. erosus to establish across North America.     

Pollen feeding,resource allocation and the evolution of chemical defence in passion vine butterflies

Evolution of pollen feeding in Heliconius has allowed exploitation of rich amino acid sources and dramatically reorganized life‐history traits. In Heliconius, eggs are produced mainly from adult‐acquired resources, leaving somatic development and maintenance to larva effort. This innovation may also have spurred evolution of chemical defence via amino acid‐derived cyanogenic glycosides. In contrast, nonpollen‐feeding heliconiines must rely almost exclusively on larval‐acquired resources for both reproduction and defence. We tested whether adult amino acid intake has an immediate influence on cyanogenesis in Heliconius. Because Heliconius are more distasteful to bird predators than close relatives that do not utilize pollen, we also compared cyanogenesis due to larval input across Heliconius species and nonpollen‐feeding relatives. Except for one species, we found that varying the amino acid diet of an adult Heliconius has negligible effect on its cyanide concentration. Adults denied amino acids showed no decrease in cyanide and no adults showed cyanide increase when fed amino acids. Yet, pollen‐feeding butterflies were capable of producing more defence than nonpollen‐feeding relatives and differences were detectable in freshly emerged adults, before input of adult resources. Our data points to a larger role of larval input in adult chemical defence. This coupled with the compartmentalization of adult nutrition to reproduction and longevity suggests that one evolutionary consequence of pollen feeding, shifting the burden of reproduction to adults, is to allow the evolution of greater allocation of host plant amino acids to defensive compounds by larvae.     

DEVELOPMENTAL CONSEQUENCES OF AN EVOLUTIONARY CHANGE IN EGG SIZE: AN EXPERIMENTAL TEST

Larvae of two species of sea urchins (Strongylocentrotus droebachiensis and S. purpuratus) differ in initial form and in the rate of development. To determine whether these differences are attributable to the large interspecific difference in egg size, we experimentally reduced egg size by isolating blastomeres from embryos. The rate of development of feeding larvae derived from isolated blastomeres was quantified using a novel morphometric method. If the differences early in the life histories of these two species are due strictly to differences in egg size, then experimental reduction of the size of S. droebachiensis eggs should yield an initial larval form and rate of development similar to that of S. purpuratus. Our experimental manipulations of egg size produced three clear results: 1) smaller eggs yielded larvae that were smaller and had simpler body forms, 2) smaller eggs resulted in slower development through the early feeding larval stages, and 3) effects of egg size were restricted to early larval stages. Larvae from experimentally reduced eggs of the larger species had rates of development similar to those of the smaller species. Thus, cytoplasmic volumes of the eggs, not genetic differences expressed during development, account for differences in larval form and the rate of form change. This is the first definitive demonstration of the causal relationship between egg size (parental investment per offspring) and life-history characteristics in marine benthic invertebrates. Because larval form influences feeding capability, the epigenetic effects of egg size on larval form are likely to have important functional consequences. Adaptive evolution of egg size may be constrained by the developmental relationships between egg size and larval form: evolutionary changes in egg size alone can result in concerted changes in larval form and function; likewise evolutionary changes in larval form and function can be achieved through changes in egg size. These findings may have broader implications for other taxa in which larval morphology and, consequently, performance may be influenced by changes in egg size.     

Breeding sites and species association of the main Bluetongue and Schmallenberg virus vectors,the Culicoides species (Diptera: Ceratopogonidae), in northern Europe

Several species of Culicoides (Diptera: Ceratopogonidae) biting midges are biological vectors of bluetongue virus (BTV) and, as recently discovered, Schmallenberg virus (SBV) in northern Europe. Since their recent emergence in this part of the continent, these diseases that affect domestic and wild ruminants have caused considerable economic losses to the sheep and cattle industries. The substrates that are suitable for larval development of the main vector species are still relatively unknown. This study assessed all the substrates present in the immediate surroundings of a Belgian cattle farm and aimed to highlight the main breeding sites of these midge species. A total of 1639 immature Culicoides and 1320 adult specimens belonging to 13 species were found in 15 out of the 43 substrates studied: maize silage residues for C. obsoletus/C. scoticus, old overwintered cattle dung in the meadow for C. chiopterus and C. dewulfi, ground of a flooded meadow, green filamentous algae and underlying substrate, silt from a pond, and ground of hollows caused by the crossing of machines on a dirt track for C. festivipennis, silt from a pond for C. nubeculosus, and ground of a flooded meadow for C. lupicaris. Identification of these micro-habitats and the associations among the species they contain could allow their localization and the development of new strategies of vector control, while preventing the creation of new Culicoides larval micro-habitats. Finally, measures designed to reduce larval populations could improve efficacy of vaccination campaigns against BTV in Europe.     

Reproductive strategies of epialgal bryozoans

Summary

Bryozoans are common encrusting organisms in many shallow-water marine environments. Although reproducing sexually, their success as space occupiers resides largely in their capacity for colonial growth by zooidal budding (regarded by some as a form of asexual reproduction). This paper examines the reproductive strategies of several bryozoan species commonly associated with the fronds of coastal macroalgae. These range from ephemeral species that grow rapidly, reproduce and die (Electra pilosa, Celleporella hyalina, Membranipora membranacea) to more or less annual species with well-developed reproductive and growth cycles (Flustrellidra hispida, Alcyonidium spp.). Whilst many of these bryozoans brood relatively few short-lived lecithotrophic larvae, others produce large numbers of longer-lived planktotrophic larvae. The seasonal and daily patterns of larval release are described for selected species. Resource allocation to sexual and colonial functions is considered in the context of environment-genotype interactions. Reproductive strategy is especially important in determining dispersal and colonising ability, and these in turn are major determinants of ecological pattern in epialgal bryozoan communities.     

Preference and performance of the sawfly Diprion pini on host and non-host plants of the genus Pinus

The sawfly, Diprion pini L., is a pest of Pinus in Europe and is mainly found on P. sylvestris L. and P. nigra laricio Poiret. The relative importance of female oviposition capacity and behaviour, egg development, and larval survival on a new host plant was measured on 11 pine species. Five were natural host plants and six non-host plants, five of which are not indigenous to Europe. Oviposition choice tests showed that females discriminated between the pine species. Egg and larval development also differed between pine species. However, the female choice was not linked with hatching rate and larval development. Results of biological tests clearly indicated that there were different response patterns of D. pini life stages in relation to pine species, and these patterns were the same with insects of four different origins. We discuss the importance of each potential barrier to colonisation of a new host.     

Heterochrony in Growth and Development in Anurans from the Chaco of South America

Heterochrony refers to those permutations in timing of differentiation events, and those changes in rates of growth and development through which morphological changes and novelties originate during phyletic evolution. This research analyzes morphological variation during the ontogeny of 18 different anuran species that inhabit semi-arid environments of the Chaco in South America. I use field data, collection samples, and anatomical methods to compare larval growth, and sequences of ontogenetic events. Most species present a similar pattern of larval development, with a size at metamorphosis related to the duration of larval period, and disappearance and transformations of larval features that occur in a short period between forelimb emergence and tail loss. Among these 18 species, Pseudis paradoxa has giant tadpole and long larval development that are the results of deviations of rates of growth. In this species events of differentiation that usually occur at postmetamorphic stages have an offset when tail is still present. Tadpoles of Lepidobatrachus spp. reach large sizes at metamorphosis by accelerate developmental rates and exhibit an early onset of metamorphic features. The uniqueness of the ontogeny of Lepidobatrachus indicates that evolution of anuran larval development may occasionally involve mid-metamorphic morphologies conserving a free feeding tadpole and reduction of the morphological-ecological differences between tadpoles and adults.     

The slow‐growth high‐mortality hypothesis: direct experimental support in a leafmining fly

1. Based on the slow‐growth high‐mortality (SGHM) hypothesis, which predicts that prolonged larval development increases mortality from their natural enemies, studies have often assumed that low quality of plants that slows larval development would function as a defence against insect herbivores. However, empirical support for the SGHM hypothesis has been limited, especially in natural and ecologically relevant contexts. 2. In a leafminer Amauromyza flavifrons Meigen (Agromyzidae, Diptera), the SGHM hypothesis was tested along with four other hypotheses (e.g. prey size, mine appearance, density‐dependent parasitism, and plant quality hypotheses) to control for spurious associations between development time and parasitism that are primarily driven by other larval traits. Two host plant species, Saponaria officinalis and Silene latifolia, were grown under varying nitrogen levels, and leafminers developing on these plants were exposed to, or protected from, a natural assembly of parasitoids across the entire course of larval development. 3. On both host plant species, leafminers that survived to an adult stage in the presence of parasitoids had a shorter development time than those in the absence of parasitoids, indicating that parasitoids disproportionately kill leafminers with longer larval development. The results provided concrete evidence for the SGHM hypothesis within the natural ecological context for these interacting species. Moreover, reduced plant quality was associated with higher larval mortality on Sa. officinalis only in the presence of parasitoids, suggesting that low quality could function as indirect plant resistance via SGHM under some tri‐trophic interactions.     

Oviposition in an eruptive moth species, Yponomeuta evonymellus, is insensitive to the population density experienced during the larval period

We studied if the population density experienced during larval development affects the reproductive schedule of Yponomeuta evonymellus L. (Lepidoptera, Yponomeutidae), a moth species characterized by outbreak population dynamics. More specifically, we predicted that reproduction would be delayed to facilitate emigration from sites with suboptimally high densities of conspecifics. We manipulated larval densities in the laboratory, as well as in those pupae collected from the extremes of natural densities. As the response, we also recorded the timing and sizes of egg clutches laid. The results did not support our initial predictions: the timing of oviposition was not dependent on larval growth conditions. This apparent lack of adaptation might be related to the loss of ‘memory’ during metamorphosis in holometabolous insects. However, oviposition schedules were also only minimally sensitive to elevated adult density. An inability to respond to high larval densities may contribute to the outbreak dynamics in this species.     

Patterns of resource distribution among conspecific larvae in two fruit fly species: Anastrepha fraterculus and Ceratitis capitata (Diptera: Tephritidae)

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A window of opportunity: Subdominant predators can use suboptimal prey

Introduced species have been linked to declines of native species through mechanisms including intraguild predation and exploitative competition. However, coexistence among species may be promoted by niche partitioning if native species can use resources that the invasive species cannot. Previous research has shown that some strains of the aphid Aphis craccivora are toxic to a competitively dominant invasive lady beetle, Harmonia axyridis. Our objective was to investigate whether these aphids might be an exploitable resource for other, subdominant, lady beetle species. We compared larval development rate, survival, and adult weight of five lady beetle species in no‐choice experiments with two different strains of A. craccivora, one of which is toxic to H. axyridis and one that is nontoxic. Two lady beetle species, Cycloneda munda and Coleomegilla maculata, were able to complete larval development when feeding on the aphid strain that is toxic to H. axyridis, experiencing only slight developmental delays relative to beetles feeding on the other aphid strain. One species, Coccinella septempunctata, also was able to complete larval development, but experienced a slight reduction in adult weight. The other two lady beetle species, Hippodamia convergens and Anatis labiculata, demonstrated generally low survivorship when consuming A. craccivora, regardless of aphid strain. All five species showed increased survival and/or development relative to H. axyridis on the “toxic” aphid strain. Our results suggest that this toxic trait may act as a narrow‐spectrum defense for the aphids, providing protection against only some lady beetle enemies. For other less‐susceptible lady beetles, these aphids have the potential to provide competitive release from the otherwise dominant H. axyridis.     

Benthic ctenophore (Order Platyctenida) reproduction,recruitment, and seasonality in south Florida

Reproductive structures, modes, and seasonal patterns of size–class abundances are examined in two benthic platyctene (Family Coeloplanidae) ctenophore species present in dissimilar shallow marine environments in subtropical southeast Florida. Coeloplana waltoni, a minute (1–3 mm body length) epizoic associate of octocorals, occurs in exposed environments often under turbulent conditions, and Vallicula multiformis (2–10 mm) commonly occurs epiphytically on macroalgae in protected, calm‐water environments. Reproductive activity in C. waltoni is most active during the warm‐water summer season (June–October); gonadal development in V. multiformis occurs year‐round, and is most pronounced during sea‐warming periods in late spring (May) and late summer to early autumn (August–October), with release of cydippid larvae. Both species are hermaphroditic brooders, exhibiting paedogenesis (early gonadal development) at body lengths approximately one‐third (Coeloplana) to one‐sixth (Vallicula) of maximum adult size. Juvenile individuals (<0.6 mm) increased in abundance in C. waltoni during the summer reproductive period, and large (≥1 mm) pink‐colored individuals comprised 50% or more of samples from July through September. Seasonal abundance of gravid individuals and the timing of cydippid larval release in V. multiformis did not correspond closely with juvenile or adult population densities. Asexual fragmentation occurred in both ctenophore species, but was observed more frequently in individuals of V. multiformis. This asexual mode of reproduction probably accounted in part for the discordance between ctenophore abundances and larval recruitment events by sexual means. Morphological structures and behaviors associated with reproduction are described in this study. Uncommon images of reproductive products (gametes, embryos, larvae), spawning events, brooding, and asexual fragmentation are included, some for the first time in the published literature.